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BIONOMICS, PARASITISM AND IMPACT OF PESTICIDES ON
T E T RAS T ICHUS ASPARAGI CRAWFORD (HYMENOPTERA: EULOPHIDAE):
AN EGG-LARVAL PARASITOID OF THE COMMON ASPARAGUS BEETLE

CRIOCERIS ASPARAGI L. (COLEOPTERA: CHRYSOMELIDAE)

by

PALASUBERNIAM KALIANNAN

A THESIS

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

MASTER OF SCIENCE

Department of Entomology

1998

ABSTRACT

BIONOMICS, PARASITISM AND IMPACT OF PESTICIDES ON
TETRASTICHUS ASPARA GI CROWFORD (HYMENOPTERA: EULOPHIDAE):
AN EGG-LARVAL PARASITOID OF THE COMMON ASPARAGUS BEETLE
CRIOCERISASPARAGI L. (COLEOPTERA: CHRYSOMELIDAE)

By

Palasuberniam Kaliannan

T etrastichus asparagi Crawford (Hymenoptera: Eulophidae) is the primary
parasitoid of the common asparagus beetle, Crioceris asparagi L. (Coleoptera:
Chrysomelidae). Failure to control the common asparagus beetle effectively will
affect the yield and growth of the plant. This study assessed the bionomics,
parasitism and the impact of pesticides on T. asparagi and the common asparagus
beetle. In the field, standard commercial practices for control of the beetle were
compared to an integrated pest management approach. Parasitism by T. asparagi
was very low in all the treatments. Eggs collected from a carbaryl and chlorpyrifos
treated field, had zero parasitism. The insecticides free asparagus fields had 14.2-
50.9°/o parasitism depending on the methods of asparagus crop management. In the
laboratory, all the insecticides tested caused 100% mortality to T. asparagi. The
fungicide chlorothalonil also caused 10-60°/o mortality of T. asparagi in the bioassay.
Asparagus beetle eggs and honey water as food increased both longevity and
fecundity of T. asparagi in laboratory studies. Volunteer asparagus ferns and nectar
producing plants in the field and field margins can enhance T. asparagi survival

and longevity.

to mani, neetha, theeba,and preetha and my parents,
without your encouragement and love, this journey of mine could not
have been accompolished

iii

ACKNOWLEDGMENTS

I am greatly indebted to my advisor, Dr. Edward Grafius, for his guidance, advice.
support and encouragement throughout my program at Michigan State University. I also
highly appreciate his insightful editorial suggestions whilst I was writing this thesis. His
suggestions have greatly improved the quality of this work. Without his financial support
especially towards the end of my program, I could not have been able to complete my
studies. I acknowledge the financial assistance provided by Michigan Asparagus Growers
Council. My sincere thanks go to my committee members Dr. George Ayers, Dr. Doug
Landis and Dr. Mary Hausbeck for their guidance throughout my program and their
advice and comments on this research project.

I am grateful to all the members of the “Grafius Working Group” (1997—1998)
who helped and accompanied me to the field. My special thanks to Dr. Walter Boylan
Pett, Beth Bishop, Paul Kolarik. Adam Byrne, Terry Davis Mike Haas, Norm Meyers.
Brian Cortright. Bill Quakenbush and Taylor for their help and sense of humor all along
the way.

I would like to take this opportunity to thank the staff of the Entomology
Department for their help and kindness. Ong Hong Peng provided invaluable advice on
statistics.

Last but not least, I wish to thank the Government of Malaysia. Public Service

Department. for funding and providing me an opportunity to pursue my studies at MSU.

 

 

 

 

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TABLE OF CONTENTS

LIST OF TABLES ............................................................................................... vii
LIST OF FIGURES ........................................................................................... .ix
KEY TO SYMBOLS AND ABBREVIATIONS ..................................... xi

GENERAL INTRODUCTION]

CHAPTER 1

An Integrated Crop Management System to Reduce Pesticide Use in
Asparagus Production for Control of the Common Asparagus Beetle
Crioceris Asparagi L. (Coleoptera: Chrysomelidae) and Conservation
of its Biological Control Agent Tetrastichus asparagi Crawford
(Hymenoptera: Eulophidae)

Introduction ........................................................................... 9

Materials and Methods ............................................................................... 13

Results and Discussion ............................................................................... 20

Conclusion.................... ......................................................................... 37
CHAPTER 2

Impact of Pesticides on the Common Asparagus Beetle Crioceris
Asparagi (L) (Coleoptera: Chrysomelidae) and the Effect on its
Biological Agent, Tetrastichus asparagi Crawford (Hymenoptera:

Eulophidae)

Introduction ........................................................................ 41
Materials and Method ................................................................................ 45
Results and Discussion ............................................................................. 49
Conclusion ............................................................................ 74

CHAPTER 3

Effect of Nutrients on the Longevity and F ecundity of
Tetrastichus asparagi Crawford (Hymenoptera: Eulophidae).
An Egg-larval Parasitoid of the Common Asparagus Beetle (Coleoptera:

C hrysomelidae)

Introduction .......................................................................... 79
Materials and Method ................................................................................ .86
Results and Discussion ................................................................................. 89
Conclusion.............. ................................................................................ 97

Overall conclusion 99
Appendix 1104
List of References .................................................................................... 107

vi

CHAPTER 1

Table 1

Table 2

Table 3

Table 4

Table 5

Table 6

Table 7

Table 8

CHAPTER 2

Table 1

Table 2

Table 3

Table 4

LIST OF TABLES

Schedules and rates of pesticides applied in the field at Oceana
County ......................................................................... 16

Damage assessment of spears according to category
of damage ......................................................................... 21

Distribution of adults and eggs of the common. asparagus beetles
per spear between treatments ................................................. 22

Damage assessment of spears according to category of damage
at different dates ................................................................. 24

Distribution of beetles, larvae, and eggs of the common asparagus
beetles per plant in various treatments at fern stage ......................... 25

Percentage parasitism by T. asparagi of common asparagus
beetle larvae from Oceana County at fern stage
(1997) ............................................................................. 31

Percentage parasitism by T. asparagi of larvae of asparagus
beetles from MSU Collins Road Entomology Research Farm
in East Lansing 1997 ........................................................... 32

Percentage parasitism by T. asparagi of asparagus beetle larvae
from Oceana County, and MSU Farms in Michigan during fern
stage in July and August 1998 ................................................ 32

Pesticides used in the field studies at the MSU Collin Road
Botany Research Farm, East Lansing ....................................... 46

Distribution of adults and eggs of C. asparagi per spear
between treatments ............................................................ 50

Mean of spear damage category between treatments ....................... 51

Distribution of adults and eggs of C asparagi per spear
between dates ................................................................... 52

vii

Table 5

Table 6

Table 7

Table 8

Table 9

Table 10

Table 11

Table 12

Table 13

Table 14

Mean of spear damage category between dates ..........................

Statistics for T. asparagi introduced onto treated filter paper
1.0 mg (AI)/ml concentrations ............................................

Statistics for T. asparagi introduced onto treated filter paper at

0.1 mg (Al)/ml concentrations ..............................................

Statistics for T. asparagi introduced onto fern l h after it was

sprayed in the field at 1.0 mg (AI)/ml concentrations.......... . . . . . . . . . ..

Statistics for T. asparagi introduced onto fern 24 h after it was

sprayed in the field at 1.0 mg (AD/ml concentrations ........................

Statistics for the common asparagus beetle introduced onto

treated filter paper at1.0 mg (AI)/ml concentrations . . .

Statistics for the common asparagus beetle introduced onto

treated filter paper at 0.1 mg (AD/ml concentrations. . . . . . . . . . .

Statistics for the common asparagus beetle introduced onto

fern 1 h after it was sprayed in the field at 1.0 mg (AI). ml
concentrations...
Statistics for the common asparagus beetle introduced onto

fern 24 h after it was sprayed in the field at 1.0 mg (AI) ml
concentrations. ..

Statistics for the common asparagus beetle larvae introduced
onto fern 24 h after it was sprayed in the field at 1.0 mg (AI).ml

concentrations

viii

.53

58

62

.64

..64

67

.69

.. 69

...71

73

LIST OF FIGURES

CHAPTER 1
Figure l The experimental field layout plan at Oceana County ................... 15
Figure 2 Mean (1' SE) number of adults, eggs, and larvae per plant at

seven days interval for the three treatments ............................. 28
CHAPTER 2
Figure 1 Percent egg parasitized (i SE) in various insecticides

treatment (A). Percent asparagus beetle adult emergence (B) from
various insecticides treatment in the field. Bars with the same
letters are not significantly different 54

Figure 2 Percent mortality (i SE ) of T. asparagi adults 0.5, l, 2. 4
and 4 h after being exposed to filter paper treated with
1.0 mg(AI)/ml (Graph A) and 0.1 mg(AI)/ml (Graph B)
pesticide solutions .......................................................................... 59

Figure 3 Percent mortality of T. asparagi 30 min (A) and 24 h (B)
after being exposed to filter paper treated at
1.0 mg (AI)/ml pesticide solution. Bars with the same letters
are not significantly different [ P>0.05, F=11.6 (A); (B) F=153.7,
df=23]... ............................................................................................ .60

Figure 4 Percent mortality of T. asparagi 30 min (A) and 24 h (B)
after being exposed to treated filter paper at 0.1 mg (AI)/ml
pesticide solution. Bars with the same letters are not
significantly different (P>0.05, F=146.1, df=23 (B).
Data in (A) were all 0% except in malathion (5%) and therefore
could not be analyzed using standard ANOVA ................................ .61

Figure 5 Percent mortality of T. asparagi adults at 0.5, 1, 2, 4, 24 h being
exposed to l h after the fem was treated (A) or 24 h after the
fern was treated (B) with 10 mg (AD/ml pesticides
solutions ............................................................................................. 63

Figure 6 Percent mortality (i SE) of the common asparagus beetle
adults at 4, 8, 16 24 48 and 72 h after being exposed to

1.0 mg (AD/ml (A) and 1.0 mg(AI)/ml (B) with pesticide
solutions” . . . . .. 68

Figure 7 Percent mortality (2': SE) of the common asparagus beetle
adults at 4, 8, 16, 24, 48 and 72 h being exposed to 1 h after
the fern was treated (A) or 24 h after the fern was treated (B)
with 1.0 mg (AI)/ml pesticide solutions ................................... 70

Figure 8 Percent mortality (1: SE) of the common asparagus beetle
larvae at 4, 8, 16, 24, 48 and 72 h being exposed to 24 h after
the fern was treated with 1.0 mg (AI)/ml pesticide

solutions ........................................................................ 73
CHAPTER 3
Figure l Longevity of T. asparagi when fed with various nutrients

food source in the laboratory ............................................. 90
Figure 2 Number of eggs eaten, number of eggs parasitized and number

of adult beetle emerged with various nutrients sources in

laboratory .................................................................... 94

Figure 3 Reproductive output per T. asparagi (i SE) at 48 h in the
laboratory. Eggs eaten and fecundity per female (A), adult
emergence per female (B), and ratio of eggs feeding versus
oviposition ................................................................... 95

KEY TO SYMBOLS AND ABBREVIATIONS

mm

cm

ha

ml

min

df

ANOVA

millimeter

centimeter

meter

hectares

milliliters

minutes

hour

day

treatment sample size
degree of freedom

analysis of variance

xi

General Introduction

Asparagus, Asparagus officinalis L., is a vegetable crop that is grown primarily in
Michigan, California. and Washington and to a lesser extent in other states. The growers
in the United States harvested 102 million kg of fresh asparagus in 1993 with a total
value of $166 million (United States Department of Agriculture 1995-1996). About 57%
of the production are destined for fresh market use and the rest for canning or freezing.

Asparagus (family: Liliaceae) is a dioecious perennial plant grown commercially
in a variety of environments and soil types. It takes about three years for asparagus to
develop from seeds to mature plants. The plant can be divided into three parts: crown.
spear, and fern. The crown is an underground rhizome on which the buds are borne and
elongate to form spears. The ferns have whorls of needle-like leaves called cladophylls.
The cladophylls are the main region of photosynthesis. Carbohydrates produced during
photosynthesis are stored in the roots and are important for spear production for the next
harvest. The plant is fairly drought tolerant. with roots that can reach a depth of 5-7 m in
sandy soils (Pierce 1987).

Generally. asparagus spears in established plantings emerge from subterranean
crowns early in the spring as soil temperature approaches 11°C. Harvest usually begins in
late April to mid May and ends in Michigan, early or late June. The spears are harvested
daily or every second or third day depending on the temperature. Once spear harvest
ceases. the plants are allowed to grow into fern during the rest of the growing season
(Pierce 1987).

Prior to spear emergence in the spring, the previous season's vegetation (weeds

and ferns) are destroyed by mowing and pre emergence herbicides are applied. During

harvest. insecticides are applied to control the common asparagus beetle Crioceris
asparagi L. (C hrysomelidae: Coleoptera) and various cutworms (Noctuidae) (Foster and
Flood 1995). The period of time following the last harvest and prior to the growth of fern
is referred to as layby. Pesticides are applied during the fern stage to control insects.
diseases. and weeds that interfere with optimal growth.

The common asparagus beetle is the most serious pest during harvest (spear
stage) and fern stage. Both adults and larvae feed on the foliage throughout their
development. During harvest. eggs are laid on spears and adult feeding may make spears
unmarketable. Defoliation can be especially damaging to seedlings. the roots of which
become weakened when their tops are devoured (Johnston 1915). The larvae, as well as
adult attack the most tender portions of the plants, but the beetle also chews the epidermis
of the stems. New fern produced immediately after harvest is believed to be especially
important to restore plant resources for future year's crop. However, the quantitative
relationship between defoliation due to beetle damage and yield reduction is unknown.

Defoliation due to fungus diseases has shown to reduce the yield (Menzies 1983).
He reported that purple spot disease. Stemphyllum vesicarium, could cause yield
reductions up to 52%. Presently. no till system practiced by farmers have contributed to
an increase in purple spot disease that affect stems, branches, and cladophylls and results
in premature defoliation (Hausbeck 1993).

The common asparagus beetle was introduced into North America from Europe. It
was first reported on Astonia, Long Island. New York in 1859 and soon spread to other
parts of the United States (Riley and Walsh 1869). Now. the common asparagus beetle is

the most important pest wherever asparagus is grown commercially in United States

[J

(Eskelson et al. 1997). Adults overwinter in the soil and emerge in the spring. The time
taken from laying of the egg to the emergence of the adult is about 25 -35 (:1, depending
on the weather, i.e. shorter during the hotter part of the season and longer in the cooler
days in May and June (Chittenden 1917). During hot weather, eggs hatch within 3 (1
(Taylor 1975). The larval stage lasts for 10 to 12 d. The adults emerge after 10 t015 d
depending on the surrounding temperature. The adult beetle also responds to disturbance
by dodging evasively and feigning death and falling to the ground. (Capinera 1976). This
dodge-feign defense strategy may provide greater protection from avian predators.

The spotted asparagus beetle, Crioceris duodecimpzmctata L. is a minor pest of
asparagus. It emerges from overwintering later than the common asparagus beetle. It
causes minor feeding damage on spears and lays eggs on the fern. Larvae feed within the
asparagus fruit "berry" and cause no injury to the fern.

Insecticides are often required to control the common asparagus beetle both
during harvest to prevent egg laying. and during the fern stage to reduce defoliation.
There is little or no tolerance level for asparagus beetle eggs on the spears due to the
strict quality control requirements of the processors and consumers. Asparagus spears are
harvested every 1-2 (1 during the early growing season and beetle control is necessary to
reduce egg laying and feeding on the spears. However. insecticides that have a pre-
harvest interval of 1 d or less and which are safe for natural enemies at the same time are
not available making it difficult to control this pest. The producers are also experiencing
increasing restrictions on pesticide use. due to the safety, health, and environmental
concerns and stringent regulations imposed by the United States Environmental

Protection Agency.

9.)

Field and lab studies have shown that biological control of the common asparagus
beetle can reduce beetle populations below economic levels in some situations. Capinera
& Lilly (1975) and Johnson (1915) reported that asparagus beetle eggs were frequently
preyed upon by coccinellids and eulopid wasps in the field. The most important
parasitoid is Tetrasriclms asparagi Crawford (Hymenoptera: Eulophidae) and it is also
found to prey on asparagus beetle eggs (Johnston 1915). Watts (1938) found that
Paralispe infernalis (Townsend) (Tachinidae: Diptera) parasitizes the common asparagus
beetle in the southern United States while T. asparagi is predominant in northern regions
(Stone et al. 1965). In Massachusetts. Capinera & Lilly (1974) found that T. asparagi
was the only important parasitoid of the common asparagus beetle encountered in the
field. Hendrickson et al. (1991) reported that in the larvae of the common asparagus
beetle and the spotted asparagus beetle collected from the fields in France, researchers
discovered five primary parasites: Diaparis truncatus (Gravebhorst) (Hymenoptera:
lchneumonidae), Lemophagus crioceritor Aubert (Hymenoptera: lchneumonidae),
Meigenia mutabilis (Fallen) (Diptera: Tachinidae). T. asparagi and T errastichus
crioceridis Graham. Of these. two species were new to science: L. crioceritor described
by Aubert (1986) and T. crioccridi.s' described by Graham (1983). The hyperparasitie.
Mcsochorus testaceus Gravenhorst (Hymenoptera: lchneumonidae), was recovered from
32.1% of the host insects parasitized by L. crioceriror.

Coccinellids are also an important mortality factor preying on both eggs and
larvae of the common asparagus beetle (Capinera & Lilly 1975). Common species are:
Hippodamia convergcns L. Colcomcgilla maculata Lengi Timberlike, and A dulia

bipunctata L. High mortality by lady beetles can reduce the potential population that will

develop in the following growing season (Eskelson et al. 1997).

T. aspuragi is a gregarious. and monophagous egg-larval parasitoid of the
common asparagus beetle. The time taken from laying of eggs to emergence of adult
takes about 25-30 days depending on the weather. The larval stage lasts for 12-17 days
and from pupal stage to adult it takes 12-15 days.

T. aspuragi does not accept the eggs or larvae of the spotted asparagus for
oviposition (Van Alphen 1980). Van Alphen also found that the T. asparagi is able to
discriminate between unparasitized and parasitized hosts. and reject parasitized hosts
after antennation or probing with the ovipositor. '1‘. asparugi fed upon 73 % and 50% of
the host eggs (Johnson 1915. Capinera & Lily 1975. respectively) and parasitism was
25%. Hendrickson et al. (1991) reported that the parasitism was only 0.5 % in Newark.
Delaware. during 1986-1989. He also reported that, during the same period. 10.3% of the
hosts were parasitized by T. asparagi in France. At L' Assompton, Quebec. the average
maximum parasitism by T. asparagi was 39.1% in the first generation and 49.2% in the
second generation for 1980-1987. Hendrickson et al. (1991) explained that the difference
between parasitism in these areas was mainly due to the climatic preferences of the T.
aspuragi. C apinera & Lily (1975) suggested that any chemical control programs aimed at
C. asparagi should be designed to minimize interference with this predator/parasitoid.

The common asparagus beetles overwinter as adults in crop residues and debris.
Insecticides such as carbaryl (both dust and liquid formulations) are often applied as a
blanket application at the beginning of the cropping season with the intent of reducing the
newly emerging beetle population. During the harvesting period, the economic threshold

level recommended for insecticides treatment is 5-10% of plants with asparagus beetle

adults or 2% of spears with eggs (Grafius & Hutchison 1995). Generally. Michigan
growers apply carbaryl dust at the beginning ofthe season and spray with other
insecticides during fern stage to protect from defoliation by the larvae and to promote
vigor. It is hypothesized that an 1PM approach. with minimum tillage. promoting natural
enemies and judicious use of pesticides. will reduce the damage caused by the common
asparagus beetle to an acceptable level. My goal is to develop an integrated crop

management system that favors T. usparugi survival and longevity in asparagus fields.

The objectives of this study were:

i) to evaluate an integrated pest management approach in reducing the common

asparagus beetle

ii) to examine the impact of pesticides normally used in asparagus fields for the

common asparagus beetle control and also their effects on T. asparagi.

iii) to examine the influence of various nutrient sources on longevity and fecundity of

adults of T. asparagi.

Chapter 1:

An Integrated Crop Management System to Reduce Pesticide Use in Asparagus
Production for Control of the Common Asparagus Beetle Crioceris asparagi L.
(Coleoptera: Chrysomelidae) and Conservation of its Biological Control Agent

T etrastichus asparagi Crawford (Hymenoptera: Eulophidae).

Abstract: A field experiment was conducted in asparagus (Asparagus officianalis L) to

evaluate the efficacy of integrated crop management (1PM) versus standard commercial
practice on the control of the common asparagus beetle ((i'rioceris asparagi L). The
conventional practice of a pre-season blanket application ofcarbaryl dust did not provide
effective control of the common asparagus beetle during the harvesting period. However.
it may have an impact on the initial emergence and survival of the parasitoid,
Tetrastichus asparagi Crawford (Hymenoptera: Eulophidae). T. asparagi feeds on eggs
of the common asparagus beetle and parasitizes eggs. Parasitism by T. asparagi was
1.1% in commercial farmers' fields in Oceana County and 50.9% at the Michigan State
University Collins Road Entomology Research Farm. East Lansing in 1997. In 1998.
parasitism was 1.1% in commercial farmers' field. while 18.7% in an organic farmer's
field in Oceana County. and 15.2% in Michigan State University Collins Road
Entomology Research and Horticulture Research Farm. East Lansing. The frequent
application of insecticides in commercial fields could have contributed to the low
parasitism. An integrated approach to control the common asparagus beetle can be
enhanced by eliminating the preseason blanket application of insecticides thus
encouraging the T. asparagi. Area wide scouting or cluster sampling may be required for
establishing threshold levels and initiating control action.

Key Words: Insecta. (L'rioccris asparagi. Tetra.s'tichus asparagi, pesticides. parasitism.

biological control. integrated pest management.

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Introduction

The therapeutic approach of killing agricultural pest organisms with toxic
pesticides has been the most common pest control strategy since World War 11. Synthetic
pesticides were actively marketed throughout the world beginning at that time and their
use has since played an integral role in the technological advances that have reduced
agricultural labor and increased productivity (USDA 1992). Pesticide use. however has
led to safety, health and environmental concerns. and ecological disruptions (Benbrook
1996. Mott 1991. Harper & Zilberman 1989. Hallberg 1987). Lewis et al. (1997)
proposed a fundamental shift to a total systems approach for crop protection. required to
solve escalating economic and envirmimental consequences ofcombating agricultural
pests.

A survey conducted by Eskelson et al. (1997) on the problems faced by
asparagus growers reported that pesticide use was a major issue among growers. Due to
the high quality standards required on asparagus. growers use pest control tactics that are
highly efficacious and fast acting. Michigan growers use from six to eight sprays per year
for major insect pest control on both spears and fern hoping to reduce the potential beetle
population (Norm Meyers. personal communication).

In Michigan. there are approximately 475 farmers. planting 7,500 hectares of
asparagus. 13.8 million kg of asparagus were produced in 1996. About 88% ofthe
Michigan crop is sold to processors and the remaining 12% to the fresh market (Michigan
Department of Agriculture 1996—97). Generally, asparagus spears emerge from the
subterranean crown early in the spring as soil temperature approaches 1 1”C (Taylor &

Harcourt 1978). Most damage is done at this stage by common asparagus beetle adults of

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the overwintered generation that feed and lay eggs on the spears potentially making the
spears unmarketable (Eskelsen et al. 1997). In Washington. Michigan. and Illinois. the
annual loss to beetle damage. resultant market culling. and the cost ofchemicals used to
control the beetles is between $1.4 and $1.6 million per year (Hendrickson et al. 1991).

Spears are mostly hand harvested by snapping them at the soil surface. This
method of harvesting may further reduce the quality by damaging the shoot epidermis
and squashing the eggs and beetles leaving black molasses like fluid on the shoots. Since
spears are harvested every 1 to 2 d in Michigan. the hand harvesting method by snapping
them at above soil surface while sitting on the moving tractor. has greatly affected the
quality of asparagus spears (Eskelsen et al. 1997).

Since the size of the industry is small, only a few pesticides are registered to be
used on asparagus. Uncertainty surrounding federal regulation of pesticides has resulted
in a high level ofconcern among growers' organizations regarding the future availability
of pesticides (Eskelson et a1. 1997). Inability to control this pest effectively or reduce the
population can result in large losses and affect the income of the growers. Therefore
reliance on non-chemical control methods should be examined to sustain the industry.

Integrated Pest Management (IPM)) or Integrated Crop Management (ICM) has
received the most attention as a comprehensive approach pest management. The term
IPM has been defined in many ways. Barlett (1956) first used the term as "integrated
control" and Van den Bosch (1962) broadened the term to include the use of biological
control, cultural. and artificial practices. The Office of Technology Assessment (OTA-
USDA, 1979) defines IPM as ” the optimization of pest control in an economically and

ecologically sound manner. accomplished by the coordinated use of multiple tactics to

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assure stable crop production and to maintain pest damage below the economic injury
level while minimizing hazards to humans. plants and the environment." According to the
Council on Environmental Quality 1980. IPM relies on "a systems approach to reduce
pest damage to tolerable levels through a variety of techniques including predators and
parasites. genetically resistant hosts. natural environmental modifications. and when
necessary and appropriate. chemical pesticides."

IPM techniques are also designed to meet health and environmental concerns and
to address the problem of pest resistance to pesticides (Cornejo et al. 1992). In practice.
IPM has been primarily a monitoring program in which thresholds are established and
chemical pesticides are used only on a need basis.

Comparative studies of the economic returns of IPM programs versus
conventional chemical pesticide programs are few (Trumble et al. 1997). There are many
examples of development of IPM programs (Teng (1994). Zehnder (1994). Chau (1995).
and van Lenteren (1997). There are many reports on how to encourage growers to
implement IPM strategies (Ramirax & Mumford 1995, Hutchins 1995). However. there
are only a few studies with field implementation of IPM programs that document an
increase in net profits compared to conventional pesticide programs (McNamara et a1.
1991).

In the Netherlands. farms that implemented an integrated approach for pest
management reduced pesticide use by over 90% (van Lenteren 1997). They found that
judicious use ofchemical pest control based on careful population sampling and decision
thresholds, use of organic manure and effective use ofcrop residues reduced pesticide use

and encouraged further implementation of an integrated farming approach.

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Walgenbach & Estes (1992) documented the net profits associated with the use of various
control strategies in staked tomato systems in North Carolina. Here, the best profits were
obtained by using broad-spectrum pesticides. Whereas. Trumble & Morse (1993) and
Trumble et a1. (1994) reported that in California. the reduction in input costs associated
with reduced pesticide use more than offset any potential losses in income from
occasional smaller yields.

In Malaysia and Indonesia. through IPM. the cost of rice production was reduced
to about 30-40% (unpublished data). This was mainly due to regular scouting and
monitoring that led to reduction in pesticide use. Yields were also lower on these farms
but were compensated for by cost reduction through lower pesticide and inorganic inputs.

Surveys conducted by C zapar et al. (1995) found that 76% of the field crop
farmers in Illinois carried out weekly or biweekly scouting to monitor the pest situation in
their fields. Nearly 100% of potato growers in Michigan implement some type of IPM
approach including scouting and crop rotation to reduce damage caused by the Colorado
potato beetle. Leplinotarsa dcccmlineala (Say) (Grafius 1997). In studies comparing the
standard commercial and IPM practices for celery production. Trumble et al. 1997 found
that the net profits with IPM were higher and fewer pesticides were used.

Many factors influence the adoption of IPM among farmers. A survey conducted
in 3 states on farmers growing vegetable crops (Michigan, Florida and Texas) by USDA
(Cornejo et a1. 1992) showed that IPM is adapted by significantly higher numbers of
asparagus growers than growers of other vegetables. In that survey. Michigan farmers
had the highest IPM adoption rate of all crops in the three states. Farmers who adopt IPM

tend to be less risk averse and use more managerial time on farm activities than non-

 

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adopters. Adopters are also more likely to operate large. irrigated farms and use more
family labor. The survey also indicated that a large percentage of non-users of IPM
preferred to spray pesticides on an insurance and calendar basis.

The objective of this study was to evaluate the effectiveness of an integrated pest
management approach in controlling the most serious insect pest of asparagus. the
common asparagus beetle. by reducing the quantity and frequency of application of

insecticides and strictly following economic threshold levels.

Materials and Methods
Field Sites.

The experiment was carried out in Oceana County. Michigan. The asparagus
plants were of variety ‘Mary Washington‘. 15 years old. planted at 0.3 m apart within the
my 1' and 1.2-1.5 m between rows. The treatment plots were selected along the border ofa
commercial asparagus field with a buffer zone of9 m (3 rows of unsprayed asparagus
rows to the east and west, 25 m on the north and 8 m on the south (Figure 1). Each
treatment plot was 15 in x 7 rows (including 2 border rows) replicated 4 times. Buffer
zones consisted of asparagus plants ofthe same variety and age. Large plantings of
asparagus. corn. and carrots and a woodlot occur within 0.5 km of the experimental plots.
A large piece ofvacant land covered with weeds is found within 15 in south of the

experimental plot.

General Plot Maintenance.
Plot maintenance. pesticide applications. and harvesting were done by West

Michigan Crop Consultants (John Baker). Before the harvesting season began. herbicides

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and carbaryl dust were applied both on the experimental plot and the neighboring
asparagus areas. All the treatment plots utilized a no-tillage system for weed management
and were sprayed with a mixture ofpre-emergent and post-emergent herbicides early in
the spring and again when the weeds were tall during mid-summer. By the time harvest
was complete. the experimental plots were fairly weedy. with Sctaria lures'ccns (L)
(yellow foxtail ). .11 maramlms retro/laws (L.') (redroot pigweed). and Asccpias svriaca
(L.) (milkweed). Herbicides were sprayed again in all the experimental plots.

We did not consider the crop yield because many factors contribute to the yield
and especially the previous years' crop management. Since asparagus is a perennial crop.

asparagus fields have to be managed for long-term productivity.

Treatments.

Treatments were: A) untreated. B) standard commercial. and C) Integrated Pest
Management (IPM). The untreated plot was used as the control while the standard
commercial plot was sprayed with pesticides as practiced by growers (Table l). The IPM
plot was sprayed when 10% of the fern dcfoliated by asparagus beetle larvae. or 50-75%
of the plants were infested with larvae (Grafius & Hutchison 1995). The pesticides used
represent the most commonly recommended in Michigan for the control of insects.
diseases. and weeds of asparagus crop (Michigan State University Extension Bulletin
312). From May 25, 97 until July 22. 97 no pesticides were sprayed due to very frequent
harvesting.

For all the treatments. spraying was carried out in the evening when the wind was

calm, using a motorized boom sprayer with a flat fan nozzle at 13.6 kg pressure per

Asparagus

Figure 1: The experimental field layout plan at Oceana County

 

 

 

 

 

 

 

 

 

 

 

 

 

FL 1 FL 2 FL 3
Other fields
0.5 km N
Buffer Zone T
(25 m)

 

B A C

 

Buffer Zone A B C Buffer Zone
(3 m) (3 m)

B C A

 

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C A B

Buffer Zone
( 8 m)

 

 

 

 

 

 

 

 

Vacant lot covered with weeds

A- Untreated Plot B- Standard Commercial Plot C- IPM Plot

Location of fields where sampling of larvae was done for parasitization
studies in the year 1997.

FL 1 - Field Number One
FL 2 - Field Number Two
FL 3 - Field Number Three

 

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square cm and 220 l of water/ha. For application ofcarbaryl dust. a motorized duster was
used.

Asparagus spears were picked until late June in the experimental field. Then the
spears were allowed to grow into fern. In the second week of July. all the guard rows
were labeled to indicate the boundaries between treatments and replicates. Daily
maximum and minimum temperatures. precipitation. and relative humidity were collected

from a nearby weather station.

Sampling:

Spear Damage. Harvesting of spears was done every 2 (1 beginning on May 27.
1997 but spears were assessed in the field every 4 d interval beginning June 1 1th 97 and
ending on June 27, 1997. 20 spears, 10-12 cm height per plot at each date.

The spear damage was assessed on a scale of 1-4. Generally the processors prefer
asparagus of good quality (no damage and without beetle eggs) while the fresh market
accepts asparagus spear with low damage rating (1-2 small feeding scars). Moderate and
severe damage categories are generally discarded at the time of harvesting. If 1 to 2 eggs
present per spear. it was considered low damage category unless the eggs are laid in
clusters of more than 5. then it is considered moderate damage category. The damage
ratings were:

1) No damage (no symptoms of damage)

2) 1-2 feeding scars/spear (low damage)

3) 3-4 feeding scars/spear, (moderate damage) and

4) more than 4 feeding scars/spear (severe damage)

The data collected in the damage assessment were transformed using arcsinc
square root before analyzing by standard analysis of variance (SAS Institute 1989) and
the means were compared using Fisher's Protected LSD test.

F ern stage. Numbers of adults. larvae and eggs were recorded weekly from 20
plants from each replicate during fem stage from July 30 through August 30. 1997.
Sampling was done in the late morning when the beetles and larvae were actively feeding
on plants. Only third and fourth instars were counted to avoid recounting of the same
individuals the following week. All shriveled eggs that had been either hatched or been
fed upon by predators. were not included for the egg count. To reduce the edge effect.
only the center row of each plot was sampled and no plants were selected within 2 m of
the end of the plot. Total counts over the four replicates by treatment and for five dates
were analyzed by standard analysis of variance (SAS Institute 1989) and the means were

compared using Fisher's Protected LSD test.

Parasitism Studies.
In 1997. mature common asparagus beetle larvae were collected at the fern stage
from 2 different geographical locations:
1. Oceana County (3 locations within experimental plots. 3 commercial fields ca. 0.5 km
north of the experimental plots.
2. MSU Collins Road Entomology Research Farm in East Lansing.
The larvae were collected weekly for 5 weeks from July until the end of August.
The larvae collected were brought back to the laboratory and 5 larvae were placed in each
petri dish (22.5 x 1.2 etn diam). The larvae were supplied with fresh asparagus fern as

needed and kept in a growth chamber at 23 _2 ° C. 16:8 (light: dark) 11 photoperiod and

approximately 55-60% relative humidity. The emergence of adult T. asparagi or adult
beetles was recorded. Dead common asparagus beetle larvae were dissected and
examined for the presence of parasitoid larvae.

Sampling Within the Experimental Plot. A total of40 larvae were collected
randomly from each treatment plots. No more than one mature larva was collected from
each plant on any sampling date and the total number was kept low to minimize any
effect that the removal might have 011 the population dynamics in the experimental plots.

Commercial Fields. A total of 50 mature larvae were collected randomly on
each sampling date from three commercial fields located within 0.5 km of the
experimental plot. The fields received similar pesticides as the standard commercial
treatment in my experiment.

MSU Collins Road Entomology Research Farm, East Lansing. The common
asparagus beetle larvae were collected randomly on each sampling date (ranging from 10
- 50 depending on the availability in the field). No insecticides or fungicides were applied
during the season: one application of herbicide (glyphosate at a rate of l lit/ha) was made
in early summer. No other crops were planted within 50 m, apples were grown and
frequently sprayed with methyl parathion (insecticide) and chlorothalonil (fungicide)
about 70 m to the east.

In 1998, mature larvae were collected from four locations on three different dates.
Two locations were in from Oceana County and 2 were from MSU Research Farms. Two
growers were selected from Oceana County (a commercial grower and an organic
farmer). The commercial grower frequently applied pesticides as described before. The

organic grower did not use any pesticides, not even herbicides. The two locations at MSU

were: Collin Road Entomology Research Farm. and Horticulture Research Farm in East
Lansing. Both these farms only used herbicides (glyphosate at a rate of 1 lit/ha) at the

beginning of the growing season. Larvae were collected on July 17, August 14 and 21,
1998 from Oceana County. and July 3. 16: August 5 and 12. 1998 from MSU Research

Farms. The larvae were reared as above to determine the parasitism rate.

Results and Discussions

During the spear stage the common asparagus beetle was the only insect pest
found feeding on the spear. As the spears began to develop into fern other insects and
predators began to inhabit the field. The lady beetle (Hippodamia comer-gens Guerin.
Coleoptera: Coccinellidae) was found feeding on asparagus beetle eggs and young larvae.
As common asparagus beetle larval populations increased. predacious pentatomids,
Podisus maculivent‘ris Say. chrysopids, Chrysopcrla ru/ilabris Burmister. Neuroptera:
Chrysopidae and starlings, .S'turnus vulgaris L., were frequently found feeding on the
larvae. Spotted asparagus beetles. (.‘rioccris duodecimpzmctata L. and Japanese beetles
(Papillajapanica Newman. Coleoptera: Scarabaeidae) were also found feeding on the
fern. Asparagus aphids ( Bl‘achycorj’nclla [= Brachycolus ] asparagi Mordvilko.
Homoptera: Aphidae). are one of the key pests of asparagus but were present at very low

levels and did not cause any significant damage during the observation period.

Spear Damage
Assessment by Treatment. All plots received the same treatment during the
spear stage and there were generally no significant differences in most of the damage

categories between the treatments (IPM. standard. and control), as expected (Table 2).

This could be due to variation between the plots that occurred during the observation.
The beetles continued to emerge and feed on the spears. The number of beetles and eggs

per spear were not significantly different between the treatments (Table 3).

Table 2: Damage assessment ofspears according to category of damage with different

 

 

 

treatment

Spears (% :t SE)
Treatment N no damage low damage moderate damage severe damage
IPM 400 68.3 i 2.5a 14.6 i 2.7b 7.9 i 1.4a 7.4 25 1.3a
Standard 400 67.2 _ 2.2a 21.1 i 2.7a 7.1 i 1.5a 4.5 25 1.7a
Untreated 400 66.8 i 2.4a 16.5 i 2.1ab 9.0 i 1.5a 7.8 i 1.7a

 

Values with the same letter in the column are not significantly different (Fisher's
Protected LSD Test. P>0.05)

In observations in the field. the distribution of beetles was highly variable. larvae
and eggs were often clumped on only a few plants. The adults tend to cluster together
either for mating or perhaps are attracted to a favorable microclimate. This distribution is
called over-dispersion or clumped (Taylor 1975). He explained that if an insect
distributes over a number of units at random. the distribution of numbers per unit will
approximate a Poisson series, the variance of the population (32) being equal to its mean
(>7). When the variance is larger than the mean. the distribution is called 'over-
dispersion,’ and often can be approximated by the 'negative binomial distribution'. It is
the most useful distribution so far pr0posed for over-dispersed insect count (Taylor

1975).

Table 3. Distribution of adults and eggs of the common asparagus beetle per

spear between treatments

 

 

 

Treatment

IPM Standard Untreated
Adult (n=400)
meani SE 0.1 i 0.02a 0.1 i 0.02a 0.1 i 0.02a
Coefficient ofVariation 4 4 4
k 0.16 0.16 0.16
52 0.16 o. 16 0.16
Egg (n=400)
MeaniSE 1.2:0.23a 1.5i0.21a 1.2i0.17a
Coefficient ofVariation. 3.8 2.8 2.8
k 0.07 0.14 0.14
s2 21.2 17.6 11.56

 

Values with the same letter in the same row are not significantly different (Fisher's

Protected LSD Test P>0.05)

2 7

k = >2 /s“->'Z

Coefficient of Variation = s/ >‘<

adopted from (Anscombe. 1949)

ix.)
is.)

adopted from (Southwood. 1978)

The measure of dispersion can be described by 2 parameters. i.e.. exponent k. and
Coefficient of Variation (CV). k measures the index of aggregation in the population
while the CV. measures the level of dispersion from randomness or Poisson distribution.
The result (Table 3) shows that the variance is greater than the mean. The smaller the
index (k). the greater is the over-dispersion i.e. clumping or aggregation (Southwood
1978). The smaller the index (k). the larger will be C.V.

If aggregation occurs. there are more zeroes and high values than expected. and as
a result the variance exceeds the mean. This departure from randomness is termed "over-
dispersion." The results (Table 3) well fit into the description indicating that
overdispersion occurred in the field.

Waters (1959) pointed out that the degree of aggregation of a population which
the index (k) expresses could well affect the influence of predator and parasites. He
explained that the segregation recognized by the negative binomial might be due either to
active aggregation by the insects or to some heterogeneity of the environment
(microclimate. soil. plant. or natural enemies). In this case. the frequent disturbance due
to harvesting of spears could have affected the dispersal and aggregation of the common
asparagus beetles. The beetles always dodge and feign to the ground when they are
disturbed during harvesting and will climb tip to feed on the nearby spears later.

In studies on the distributional pattern of the C. asparagi in Canada. Taylor &
Harcourt (1972) found that all life stages were over-dispersed and did not conform to the
Poisson distribution, due to preponderance of uninfested and highly infested plants.
Migration or emigration would not have seriously affected the population dynamics since

the common asparagus beetle only feeds on asparagus (Chittenden 1917). The harvesting

I‘d
Lu

of spears was done almost simultaneously with the rest of the growers and there would
not be any preference on the site for aggregation of this beetle to the experimental plots.
Though the beetles may have moved within a short range for feeding or oviposition
purposes.

Spear damage with date. The percentage of spears in the no damage category
was significantly lower on .Iune 1 l and 15. 1997 than on later dates (P<0.05; F=5.01;
df=14. 45) (Table 4). The percentage in the no damage category increased significantly as
harvesting progressed (P<0.05; F =4.91: df= 4. 45). At the same time the percentage of
spears in the low damage category was higher compared to later dates (P<0.05; F=3.83;

df= 4, 45). The initial low number of spears may have influenced the severity of damage

Table 4: Damage assessment of spears according to category of damage at different dates

 

Spears (% 3: SE)

 

 

Date N no damage low damage moderate damage severe damage
.lune 11. 1997 240 54.9 i 2.8a 28.9 i 3.5c 10.7 i 2.4b 4.6 i 0.9a
.lune 15. 1997 240 61.8 i 2.2c 19.6 i 2.4b 10.7 i 1.9b 7.9 i 1.3a
.lune 19, 1997 240 69.8 i 1.3b 4.7 i 2.8b 7.2 i 1.7ab 7.5 i 1.6a
June 23.1997 240 70.7 i- 2.1ab 6.3 i 1.4a 4.7 i 1.2a 7.2 i 2.4a
June 27. 1997 240 77.6 i 1.8a 7.3 i 1.4a 5.7 i 1.2a 7.2 : 1.4a

 

 

Values with the same letter in the same column are not significantly different (Fisher's
Protected LSD Test P>0.05).

at early stages of spear production. As the quantity of spear production increased with
time, the percent damage dropped. thus increasing the marketable quality (i.e.. no damage
category) (Table 4). There was no difference in the severe damage categories between
dates.

The blanket application ofcarbaryl dust in mid-April did not effectively control
the emerging beetles resulting in a high percentage of spears being destroyed at the
beginning of harvesting (May 27). The grower may have to delay the application of
carbaryl or increase the frequency of insecticide application to reduce the damage. Even
though carbaryl can provide effective control against asparagus beetle. the timing of
application is very critical in reducing or suppressing the beetle population while

preserving the natural enemies.

F ern Stage

Adults. There were significantly fewer adults in the standard commercial plots
compared to other treatments (Table 5) (P<0.05; F=24.76; df=2. 1 197) and no difference
between the untreated and IPM plots. The weekly application of carbaryl and pemtethrin
(Table 1) resulted in a lower number of adult beetles in the standard commercial plot.
Although the IPM plot was sprayed once in late summer (July 23, 1997) with carbaryl
and permethrin, the adult numbers were not significantly reduced compared to the
numbers in untreated plots.

Eggs. There were significantly fewer eggs in the standard commercial

plots compared to the IPM and untreated plots (P<0.05: F=23.14; df=2. 1 197) reflecting

the reduced adult numbers.

Table 5. Distribution of beetles. larvae. and eggs of the common asparagus beetle per
plant in various treatments at fern stage.

 

 

 

 

 

Treatment

IPM Standard Untreated
Adult (n=400)
mean iSE 0.8 i 0.3la 0.2 i 0.04b 0.9 i 0.36a
C.V 7.1 3.8 7.9
k 0.02 0.01 0.02
s3 38.4 0.64 51.84
Egg (n=400)
meani SE 11.2 i 1.51a 4.5 i 0.96b 9.5 i 1.02a
C.V 2.7 4.3 2.2
k 0.1 0.1 0.2
s?- 912.1 368.6 416.2
Larvae (n=400)
meani SE 0.7 i 0.15a 0.01 i 0.01b 1.8 i 0.21c
C.V 3 0.2 4 7
k 0.1 3.3x10‘3 0.21
32 0 0.04 17.6

 

Values with the same letter in the same row are not significantly different
(Fisher's Protected LSD Test P>0.05)

Larvae. The mean number of larvae in the standard commercial treatment plot
was significantly lower than in the IPM and untreated plots (P<0.05; F =74.41; df =2.

1 197). The application ofcarbaryl and permethrin in IPM plots on July 23. 1997 may
have killed some of the young larvae, reducing larval numbers.

The results (Table 5) indicate that beetles, eggs. and larvae were over dispersed
similar to distributions on the spear stage. The aggregation index (k) was small and the
variance (82) was much higher than the mean indicating that the beetle, egg and larval
population were over dispersed. At fern stage. the branches and leaves (cladophylls) are
much denser than during the spear stage. The aggregation of beetles and larvae at this
stage could be due to 1) abiotic factors such as light, temperature or moisture; 2) mating

response and 3) nutritional response.

Dates.

Adults. There was significantly fewer adults on July 30, 1997 compared to
August 8 and 15, 1997 (Figure 2) (P<0.05; F=15.53; df=4. 1195). Carbaryl and
permethrin application on July 23, 1997 significantly reduced the number of adults on
July 30, 1997. We expected to see more adults on August 30. 1997. due to an increase in
the mean numbers of larva on August15. 1997 or may not emerge due to diapause.

Eggs. There were significantly lower number of eggs on June 30. 1997.
corresponding to the lower numbers of adults during this period (Figure 2) (P<0.05;
F=40.47; df=4.1 195). There were significantly more eggs on August 8 and 15. 1997 than
on July 30, 1997 and this may be due to an increase in the number of adults on the

August 8,1997.

 

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Figure 2: Mean (i SE) number of adults, eggs. and larvae per
plant at seven days interval for the three treatments.

Larvae. The larval number significantly increased on August 22 and 30. 1997 in
accordance with the number of eggs which had increased on August 8 and 15 (Figure 2)
(P<0.05. F=32.64. df=4. l 195). The length oftime needed for the eggs to hatch is about
5-8 d. and higher larval numbers were anticipated during the fourth and fifth weeks. The
average number of eggs per plant in the IPM and untreated plot continued to increase
(Figure 2) as fern foliage and height increased.

The common asparagus beetle is a sporadic pest. The scouting methods used to
determine the threshold level to initiate spraying might not always represent the true
characteristics of the field population due to the over-dispersion of this beetle.

The economic threshold used to initiate spraying is > 2% of spears having eggs.
or > 5% of spears infested with beetles. or >10% defoliation of at fern stage. The
scouting methods used for monitoring thresholds and determining action threshold levels
may not be accurate due to over-dispersal as mentioned by Taylor & Harcourt (1972).
Random sampling method used to determine the threshold level might not effectively
represent the true nature of the situation. This could have affected the results of the three
treatments used in this experiment. The scouting method used in the monitoring system to
determine the threshold will influence the action. I would propose that sampling for
asparagus beetle would have to be an area based survey or cluster sampling rather than
focusing on individual plants. Cluster sampling will include a naturally occurring
population within a cluster of spears or ferns.

There were greater numbers of uninfested and lesser number of highly infested
spears or fern in the field. It can be concluded that percent of spears damaged will be

equal to the crop loss.

Parasitism Studies

There was zero parasitism by T asparagi during harvest in Oceana County.
Percentage of parasitism by T. asparagi was 1.1 1% in Oceana County and 50.9% at the
MSU Collins Road Entomology Research Farm during fern stage in 1997 (Table 6 and
7). Out of 1350 asparagus beetle larvae collected during the fern stage from the
experimental plots and the surrounding locations from Oceana County. only 15 larvae
were parasitized by T. asparagi (Table 6); seven larvae produced live T. asparagi adults
and eight parasitized larvae died and had immature parasitoid larvae present within them.
During the larval development period in the laboratory. 493 asparagus beetle larvae and
57 pupae died of unknown causes other than parasitism. Out of the 1 10 larvae collected
from MSU Collins Road Entomology Farm. 53 were parasitized and emerged into adult
parasitoids while three dead larvae had immature parasitoid larvae. Five beetle pupae
died from unknown causes, which were not due to parasitism.

In 1998. parasitism was again low (1.1%,) in commercial farms but the rate of
parasitism was much higher in the organic farm in Oceana County (18.7%) (Table 8).
The parasitism rate was 14.2% at the MSU Collins Road Entomology Research Farm and
16.2% at the MSU Horticultural Research Farm. This parasitism level was somewhat
similar to the level on the organic grower's farm in Oceana County. The farms where
pesticides were not used had higher parasitism rate compared to commercial farms in
Oceana County.

Though parasitism differed at the MSU Collins Road Entomology Research Farm
between 1997 and 1998, this was mainly due in part to the sampling frequency and total

number collected at each date. In 1997. the larvae collection was staggered over five

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Table 7: Percentage parasitism by T. aspuragi of larvae of the common asparagus beetles
from MSU Collins Road Entomology Research Farm in East Lansing (1997)

 

 

Date 7 July 14 July 21 July 31 July 8 August
No. Collected 50 20 20 10 10
No. Parasitized 14 13 12 8 9
% Parasitism 28 65 60 80 90

 

Table 8: Percentage parasitism by T. asparagi on asparagus beetle larvae from Oceana
County. and MSU Collin Road Research Farms in East Lansing during fern stage on July
and August 1998.

 

Location No. Collected No parasitized % Parasitism

 

Oceana County

Commercial Farm 760 9 1.1

Organic Farm 858 161 18.7
MSU, East Lansing

Entomolgy Farm 550 78 14.2

Horticulture Farm 600 97 16.2

 

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date and very few larvae were present at later dates (Table 7). But in 1998, higher
numbers of larvae were present and the number collected at each date ranged between 50
and 150.

An average of5. 15 (range = 5-8) and 5.75 (range = 3-13) parasitoids were reared
from each host larva from Oceana County and MSU Collins Road Entomology Farm.
respectively. An average of 4.75 was reported by C apinera & Lilly (1975) and 6.50 per
host was reported by Johnston (1915). Parasitoids from lightly parasitized hosts emerged
later than heavily parasitized hosts. The parasitoids emerging from lightly parasitized
hosts were often larger (visual appearance) than parasitoids from heavily parasitized
hosts. No statistical test was carried out to confirm this observation. A similar trend was
reported by Capinera & Lilly (1975').

According to Capinera & Lilly (1975), the mortality of the common asparagus
beetle due to T. asparagi increased with an increase in the number of available hosts in a
density dependent manner in a non-insecticide sprayed farm. But this was not so in the
case of samples collected from commercial farm in Oceana County where high numbers
of larvae did not show high parasitism. The higher rate of parasitism in the organic
grower’s field and MSU research farms indicate that there was likely some pesticide
impact on parasitoid survival in the commercial fields.

T. asparagi undergoes three generations in a year on Long Island and in
Massachusetts (Johnston 1915. Capinera & Lilly 1975). The trend was similar in MSU
Collins Road Entomology Research Farm. In 1997 and 1998. adults were very abundant
in early June, July and late August, indicating that the population continued to survive

even though the beetle egg population had decreased drastically towards the end of

 

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August. There are other biotic and abiotic factors influencing the T. asparagi population
survival in the field.

During the studies, only T. asparagi females were observed among the adults
collected from the field and among those reared in the laboratory and as confirmed by
Dr. David Prokrym and Deb Nelson from USDA. APHIS, Niles. Michigan. Reproduction
in the laboratory has been entirely parthenogenetic as affirmed by (Johnston 1915). The
parthenogenetic development is an advantage for parasitoid reproduction because it does
not require males for mating but eliminates genetic recombination to adapt to new
environmental conditions.

Overall Discussion

Parasitoid feeding on beetle eggs and parasitizing eggs and larvae did not
sufficiently reduce the emerging beetle population in our experiments in commercial
farms in Oceana County. Percentage of parasitism was very low (1 .1%) at fern stage both
in 1997 and 1998. This was probably due to at least partly to the impact of pesticides
used. Tipping & Burbutis (1983) showed that carbaryl (Sevin 50 WP) residues at 1.4
kg/ha inhibited emergence of T richagramma nubilae Ertle & Davis (Hyemenoptera:
Trichogrammatidae) an egg parasitoid of the European corn borer. ()strim‘a nubilis
(Hiibner). in both a greenhouse study and field test. The timing of application of carbaryl
dust may be critical. Even though a blanket application of carbaryl dust was done very
early in the season in Oceana County. it may have affected parasitoids: we were able to
collect only four adult parasitoids during the spear stage in 1997.

The effects of pesticides can be reduced by either changing the pesticide in ways

that reduce the damage it causes or by using natural enemies resistant to the pesticides

 

1110)“ l

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(Hoy 1982, Hoy et al. 1990). Gage and Haynes (1975) successfully used temperature
driven models of insect development to time pesticide applications against adult cereal
leaf beetle ()u/ema n-zclanupus (L.) (Coleoptera: Chrysomelidae). Pesticides were applied
only after the beetle had emerged but prior to emergence of the parasitoid, T clraslichus
_/'u/is (Walker) (Hymenoptera: Eulophidae) to increase the parasitism level. They also
stressed that the weather played a major role in factors such as adult parasite
overwintering survival and emergence from overwintering sites.

Noncrop habitat bordering agricultural fields has favorable effects on a number of
beneficial arthropods Booij & Noorlander (1992) and Dennis & Fry (1992). Although a
large piece of vacant land covered with grasses. flowering weeds and woodlot existed
within 15 m and 50 m of the experimental plot, the parasitoid population was very low
both at spear and fern stage. Probably the grasses and weeds in the vacant lot did not
provide the required nectar sources and ecological niches needed by the parasitoid. The
frequent application of pesticides by the farmers surrounding the treatment plots may
have affected the survival and reproductive potential of the parasitoid.

In my observation at the MSU Collin Road Entomology Research F arm. Botany
Research Farm in early May 1998, the volunteer ferns in the inter-rows between the
asparagus plants were continuously inhabited by T asparagi when spears were being
regularly harvested. The beetle eggs present in the volunteer ferns became hosts for T.
asparagi not only for oviposition but also as food source. van den Bosch & Telford
(1964) and Stehr (1975) emphasized the needs of natural enemies, including adequate
availability of hosts. and alternate hosts when the primary one is scarce. additional

sources of food. shelter. overwintering sites. mates. and an attractive host habitat for long

DJ
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term conservation.

Capinera & Lilly 1975. Johnston 1915) found that adult T. asparagi kill a
significant proportion ofthe host through host feeding. Host feeding is an additional
source of mortality to parasitism (destructive host feeders typically use another host
individuals for oviposition and feeding). and some parasitoid species may at times kill
more hosts by feeding than by parasitism (Kidd & Jervis 1989). This is true in this case
where the adult T. asparagi consumes the egg content until the egg shriveled or
collapsed. Johnston (1915) in his study of the biology of T. asparagi. stated that the host-
feeding habit ofthe adult was evidently as useful in checking its host as was its
parasitism.

The continuous removal of spears and destruction of volunteer fern drastically
reduce the T. asparagi population in the field. Reeve (1988 & 1990) and Wissinger
(1997) stressed that herbivores and natural enemies would require refuges during periods
ofcrop habitat destruction. with requisite movement and recolonization between the crop
and alternate habitat. The maintenance of unsprayed refuges within fields has been
suggested as a mechanism for conserving natural enemies and managing for pesticide
resistance (Robert et al. 1996). Site specific management can slow the development of
pesticide resistance and conserve natural enemies in potato fields (Midgarden et al. 1997.
Weisz et al. 1995a. b: Weisz et al. 1996). At the moment there is rapid emergence of
'precision agriculture.’ or site specific management in many parts of agriculture in the
United States (Robert et al. 1996). From my personal observation and past records in

other crops. IPM with site specific management has the potential in asparagus to conserve

 

T. as;

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T. asparagi and help control the common asparagus beetle C. asparagi with much
reduced insecticide application.
Conclusion

The reliance on existing T. asparagi and the use of economic thresholds in the
IPM plot did not lower the beetle populations compared to pesticide treated plots at fern
stage. The beetles, eggs and larvae were aggregated within a few plants. This may have
influenced poor or under estimation of economic threshold of 10% defoliation in the IPM
plot. There was a poor correlation between the level of damage and beetle population
during the harvesting period. The application of insecticide (carbaryl dust) before crop
emergence may have a negative impact on the natural enemies and could have
contributed to the low level ofe ’g-larval parasitism in Oceana County. The high
percentage parasitism in MSU Collins Road Entomology Research Farm in (1997) and
the organic farm from Oceana County su 'gest that the insecticide free cropping and
complex habitat can enhance the abundance of parasitoids. The average maximum
parasitism obtained in farmers' field in Quebec. Canada was 49.2%. This shows that there
is potential in conserving the parasitoid in the asparagus crop management system.

During the early growing season I would recommend that no insecticide should be
applied and volunteer ferns in the inter rows should be allowed to establish. This is
because the volunteer ferns will provide the substrate for the newly emerging beetles to
feed and lay eggs. The newly emerging T. asparagi will be able to feed on the eggs and

continue to oviposit.

Frequent harvesting of spears will create instability in the habitat thus

encouraging the beetles to lay eggs on the fern. This will improve the quality of spears

and in.

and adj
the pre

determi

 

and increase the productivity of the farm.

Incorporating site specific habitat management. using ofless toxic insecticides.
and adjusting the timing of pesticide applications will give considerable improvement to
the present approach of asparagus IPM which mainly focuses on scouting and

determining threshold level for beetle management.

38

 

Cha

II

Chapter 2

Impact of Pesticides on the Common Asparagus Beetle Crioceris asparagi (L.)
(Coleoptera: Chrysomelidae) and Effects on its Biological Control Agent,

T etrastichus asparagi Crawford (Hymenoptera: Eulophidae)

Abstract: Studies were done both in the field and laboratory on the impact of pesticides
on adult Tetrastichus asparagi Crawford and it’s host, the common asparagus beetle
Crioceris asparagi (L.). Carbaryl, chlorpyrifos, and permethrin were used in the field
studies. The number of beetles and eggs were significantly lower in carbaryl and
chlorpyrifos treated plots compared to the untreated ones. Parasitism by T. asparagi was
significantly higher in the untreated plots. Parasitism was 6.2% and 1.4% in the untreated
and permethrin treated plots, respectively and zero in carbaryl and chlorpyrifos treated
plots. Residual bioassays using pesticide treated asparagus ferns and filter papers were
carried out on T. asparagi. asparagus beetles and larvae. Carbaryl, chlorpyrifos and
malathion at 1.0 mg active ingredients (AI)/ml concentration, caused 100% mortality to
both T. asparagi and asparagus beetles when exposed for 1 h to field sprayed asparagus
fern within 4 and 16 h of treatment. Permethrin was least toxic but still caused
significant mortality in the bioassays. Chlorothalonil, a fungicide, was also toxic to T
asparagi and caused 20-60% mortality. The eggs laid by the beetles on the volunteer fern
were the main source of nutrients to T. asparagi. Volunteer fem can enhance the survival
and parasitism of T. asparagi within the asparagus fields. The presence of volunteer fern
may also increase the rate of parasitism by T. asparagi.

Key Words: lnsecta, C. asparagi, T. asparagi. pesticides. parasitism, toxicity.

40

Introduction

Production of commercial asparagus is currently reliant on pesticides inputs. A
combination of low prices and high quality standards puts pressure on growers to produce
large quantities of acceptable quality. Such a situation results in a high degree of risk to
the grower, resulting in heavy use of pesticides to control the pests. Most commercial
asparagus growers use insecticides to control the common asparagus beetle Crioceris
assparagi L. (Coleoptera: Chrysomelidae) which is the most serious pest of asparagus.

A survey conducted between 1991-1994 by Eskelson et al. (1997) found that
nationally. carbaryl was applied to 18.592 hectares per year during and after harvest to
control the common asparagus beetles. If carbaryl was not available, permethrin would be
applied on 84% of the area, and methomyl and malathion on 8% of the area. In Michigan,
carbaryl was applied to 7,001 hectares per year specifically for control of the common
asparagus beetles. Carbaryl is often applied 2 or 3 times in the same area to control the
common asparagus beetle. Other insecticides such as chlorpyrifos. malathion, permethrin
and methomyl would be used if carbaryl was not available to control the asparagus
beetles. The estimated cost for treatment with carbaryl was $354,973 per year in
Michigan. For the control of rust and purple spot diseases, mancozeb was applied to
7,001 hectares per year. Without disease control, asparagus yield would decrease by as
much as 0-20% in the first year and by as much as 50% if not treated continuously for
two years (Johnson and Lunden 1992).

The use of a wide range of pesticides kills both predators and parasites along
with the pests (Morse et al. 1987, Croft 1990). In many instances, natural enemies are

more susceptible than pests to commonly used pesticides (Idris and Grafius 1993a,b). In

41

addition to suffering mortality. natural enemies may become less effective following
pesticide use (Waage 1989). Carbaryl is toxic to most natural enemies at field rates
(Barletts 1963 and 1964). Tipping and Burbutis (1983) showed that carbaryl (Sevin 50
WP) residues at 1.4 kg active ingredient per ha. inhibited the emergence of
Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). an egg
parasitoid of the European corn borer. ()slrinia nubilis (Hiibner). in both a greenhouse
study and a field test. Free and Hagley (1985) found that a 0.2 % solution of technical
grade carbaryl killed 100% of both chrysopid larvae and adults. Chrysopa oculata Say.
when sprayed from a potter tower. In addition to direct effects on parasitoid adults.
insecticides may indirectly affect parasitoid larvae within their host. For instance.
Apantheles melanoscelus Ratzeburg (Hymenoptera: Braconidae) larvae within its host
larvae gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae) are indirectly killed
by carbaryl and Bacillus Ihuringiensis Berliner (Ahmad & Forgash 1976. Ahmad et al.
1978. Thorpe et al. 1990).

Synthetic pyrethroids show variable toxicity to parasitic hymenoptera, from 100%
mortality of the braconid, A panic/es ornigis Weed. (Hymenoptera: Braconidae). a parasite
of the apple leafminers (Lepidoptera: Gracillariidae). to low mortality of Macrocentrus
ancylivarus (Rohwer). a braconid parasite of the oriental fruit moth Grapholitha molcsta
(Busck) in field treatments (Croft & Whalon 1982). The most extreme case of unfavorable
selectivity was reported for the eulophid. Tetrastichus_/'ulis (Walker), permethrin,
fenvalerate and cypermethrin was 1000x. 850x, and 150x more toxic to T julis adults than
to the host adult, Oulema malanapus (L.) (Coats et al. 1979). Niemczik et al. (1981) also

found that permethrin was toxic to the green lacewing. Chrysopcrla carnea (Steph).

 

A field trial in India showed that decamethrin and phoxim are least toxic to the

parasitoid Tetrastichus sp.. an important parasite of the mango hopper, Idioscopus
clypealis Leth (Verghese et al. 1990). When sprayed with cypermethrin. Tetrasticlms sp.
population was 0.90/ panicle versus 0.07/panicle when sprayed with methamidophos.
Verghese et al. (1990) also discovered that even permethrin adversely affected the

T errastichus sp. in mango flowers. in agreement with Coats et al. (1979). They suggested
that deltametrin may be included in future integrated pest control programs in mango.

Mogal et al. (1982) reported dichlorvos (0.05 per cent) as the only compound which
allowed the survival of the parasite T etrastichus sp., a parasite of Contarnia sorghicola
Cogounder on jowar plant in lab conditions. Jalaluddin and Mohanasundram (1989)
indicated that among the chemicals tested against Tetrastichus israeli (Mani & Kuran),
fish oil rosin soap was found to be the least toxic and the order of relative toxicity was
methyl parathion > dimethoate > methomyl > fish oil rosin soap.

Pesticides also affect the rate of parasitism of biological control agents. Parasitism
was very low in commercial asparagus fields and much higher in untreated fields (Chapter
1). Dreigstadt et al. (1994) found that the elm leaf beetle Xanthogaleruca liteola (Muller)
was parasitized by Tetrastichus gallerucae (Fonscolombe), an egg parasitoid and
Tetrastichus brevistigma (Gahan), a larval parasitoid. They further suggested that avoiding
foliar application of broad-spectrum insecticides or using less toxic insecticides such as
Bacillus thuringiensis Berliner could conserve these parasitoids. Conversely, there are
cases where pesticides do not seriously affect the parasitism rate. Sastrosiswojo &
Sastrodiharjo (1986) reported that Diadegma eucerophaga (Horstmann) was not adversely

affected by insecticides in two of the three insecticide-treated fields. In cotton, Microprilis

demolitor (Wilkinson) and M. croccipe.s' Cresson both parasitize Heliothis zea (Boddie)
larvae and are not affected by the insecticides and fungicides applied to control their host
(Powell et al. 1986, Culin & Dubose 1987). These two parasitoids sometimes have higher
parasitism rates in fields treated with pyrethroids rather than in fields treated with
organophosphate insecticides.

Fungicides for control of plant pathogens may also affect entomophagous fungi.
Mancozeb and chlorothalonil are widely used for controlling diseases in the asparagus
field. The entomophagous fungus, Ir'erticillium lecani (Zimm), that often affect aphids in
potatoes, alfalfa and other cereal crops, is highly sensitive to fungicides like mancozeb
and captafol but not to copper or chlorothalonil (Grossman 1990). Chlorothalonil is
reported not to kill the entomophthoracea fungi. Erym'a bluckii (Lakon) and Zoophthora
radio-ans (Brefed) that attack diamondback moth larvae and pupae (Tomiya & Aoki
1982).

Most insecticides have detrimental impacts on biological control agents.
However, some of the insecticides used in cotton production possess either differential or
selective toxicity to certain beneficial insects (Lingren & Ridway 1967, Cate et al. 1972.
Powell et al. 1986). In the asparagus agro-system. frequent application of insecticides
drastically reduced parasitism in commercial fields (Chapter 1). Pesticides can have a
major effect on biological control programs. Parasitoids and many predators cannot
survive very strong selection pressure from frequent insecticide applications. The greater
susceptibility of parasitoids and predators compared to the hosts is most likely due to a
difference in the ability of parasitoids and their hosts to detoxify insecticides. Parasitoid

are ecological specialists. having only to attack their hosts. while the latter have to

44

detoxify numerous toxic components of plants on which they feed (Croft and Whalon
1990).

The objective of this study was to evaluate the control of the common asparagus
beetle by pesticides normally used in asparagus fields and their effects on its biological

control agent, T asparagi.

Materials and Methods

Field Evaluation

Sites. An asparagus field on the Michigan State University Collin Road Botany
Research Farm, East Lansing was chosen to carry out this study. This farm was selected
based on the landscape architecture. suitability of soil, and young asparagus planting. The
asparagus field covered about 0.75 hectare and is surrounded by a wide variety of
vegetation. On the northern side, there is 0.5 ha of apple orchard with heavy flowering
during the time of the experiment, a large area of pasture grass on the east, and mixed
grasses on the west. There was no record of pesticide applications in the surrounding
areas during the observation period. This asparagus field consists of 5 varieties of Syn
456, Jersey Knight, Mary Washington, Jersey Giant, and Apollo, planted between 1995-
1996. Variety Syn 456 was chosen for the purpose of this experiment. Rows were 1.6 m
apart and plants were 0.5 m apart in the row. Volunteer ferns 12-150m tall. 10-20/n12.
were found growing between the asparagus rows.

The plots were 1 row x 10 m long. separated by an untreated row and there were
untreated border rows on each side of the entire area. Treatments were arranged in a

completely randomized manner. four replications per treatment.

45

Treatments. The plots were treated with carbaryl. chlorpyrifos or permethrin or
left untreated. Treatments were applied on May 7, 15, and 21, 1998, using a hand held
carbon dioxide sprayer with one nozzle over the row at 4.5 kg per cm3 pressure.
Pesticides used were of commercial formulations (Table 1).

Table 1: Pesticides used in the field studies at the Michigan State University Collin
Road Botany Research Farm at East Lansing.

 

Common Name Trade Name Rate
(active ingredient)

 

carbaryl Sevin XLR Plus 1.1 1 kg /ha
(Rhone Poulenc
Raleigh. NC)

chlorpyrifos Lorsban 4E 1.1 l kg/ha
(Dow Elanco
Indianapolis, IN)

permethrin Pounce 3.2 EC 0.1 1 kg/ha
(FMC.
Omaha, NE)

 

Sampling. 24 11 after each application of pesticides. 20 were randomly assessed
from each replicate for the presence of asparagus beetles, eggs, and feeding damage
incurred. The damage categories used were the same as in the previous experiment. At
the same time 20 fresh eggs were collected from each replicate (80 eggs/treatment) and
reared in the laboratory to determine parasitism. The data was analyzed using standard
analysis of variance (ANOVA) and the means were compared using Fisher's protected
LSD test (SAS Institute 1989). Percentage spears in each category was arcsin

transformed before analysis.

46

Laboratory Evaluation (Residual Bioassay)

Parasitoid rearing. A large numbers of third and fourth instars ofthe common
asparagus beetle were collected from Michigan State University Collins Road
Entomology Research and the Horticultural Research Farm. East Lansing during August
1998. The insecticides spraying records maintained by the Entomology and Horticultural
Research Farm indicated that no insecticides were sprayed in the field in 1998. The
larvae collected were then placed in 30 X 20 X 1.5 cm deep plastic trays for rearing in the
laboratory. They were fed with fresh asparagus ferns every 2 d. The parasitized larvae at
pre-pupal stage (I could observe the parasitoid larvae through the host integument after
they completely consumed the fatty tissue of the host) were then transferred into petri
dishes (22.5 cm x 1.2 cm) and kept in a growth chamber at 23 i 2°C and 16:8 (LzD)
photoperiod and 55-60% relative humidity. As adult parasitoids emerged, they were
transferred into another petri dish (22.5 cm x 1.2cm). A small vial filled with honey water
(10% dilution) and plugged with a sponge was placed inside the petri dish to feed the
adult parasitoids. A few drops of honey water were added to the sponge every 2 d.
Parasitoids from first and second generation laboratory reared culture was used in the
bioassays.

Asparagus adult beetles and larvae. Adult beetles and third and fourth instars
larvae were collected from the Michigan State University Collin Road Horticultural
Research Farm. a day before the bioassays were carried out. The adult beetles and the
larvae were provided with fresh asparagus ferns and water until they were used in the

bioassays.

47

Pesticides used. Pesticides used were commercial formulations of carbaryl
(Sevin XLR Plus, Rhone Poulenc, Raleigh, NC). permethrin (Pounce 3.2 EC, FMC.
Omaha Ne), chlorpyrifos (Lorsban 4E Dow Elanco, Indianapolis, IN), malathion
(Malathion 57 EC, Uniroyal Chemical Company, Madison. WI and chlorothalonil (Bravo
Weather Stik, ISK Bioscience Corporation, Mentor, OH). They represent the most
commonly used pesticides in Michigan for control of pests and diseases of asparagus.
Pesticide solutions were prepared at two rates; 1.0 mg active ingredients (AI)/ml and 0.1
mg AI/ml (field concentrations for 1.1 kg/ha is 3.9 mg AI/ml).

A bioassay was conducted to compare the response of T. asparagi adults, and
C. asparagi adults and larvae where both species might be walking on surfaces
containing pesticides residues in the field.

Treated filter paper assay. 1.0 mg Al/ml and 0.1-mg AI/ml concentrations were
prepared from the above listed pesticides. A 20-cm filter paper (Whatman No.1) was then
placed inside a 22.5-cm diameter petri dish and 1 ml of the pesticide solutions were
titrated onto the filter paper and air dried for 2 h. For control, the filter paper was treated
similarly with tap water. The parasitoids. and the asparagus beetles were assigned
randomly to treatments and petri dishes kept at 23 i 2°C and 16:8 (L: D) photoperiod.
The treatments were replicated four times (4 petri dishes for each insecticide for
parasitoids, beetles or larvae) with 5 insects per replicate. Parasitoid mortality was
recorded at 0.5. l, 2. 4 and 24 h. Beetle mortality was recorded at 4, 8, 16, 24, 48 and 72
h. The larval mortality was recorded at 8. 16. 24. 48. and 72 h. Parasitoids were

considered dead if they were observed to be an incapacitated i.e.. erect wings. curled

antennae and failure to move in response to tapping the side of the petri dish. Beetles and

48

larvae were considered dead if they could not walk one body length when gently probed.
Beetles and larvae surviving more than 24 h were provided with fresh asparagus fern.
The data was analyzed using analysis of variance and the means were compared using
Fisher's protected LSD test (SAS Institute 1989).

Field sprayed asparagus fern assay. The pesticides were sprayed with 1.0 mg
AI/ml concentration on the asparagus ferns in the field covering an area of (1 m x 1 m).
For control. the ferns were treated similarly with tap water. The ferns were collected 1 h
and 24 h after application of pesticides in the field. Two small branches of the fern were
plucked and inserted into a vial containing water, the vial was plugged with a sponge and
placed inside a petri dish (21.5 x 1.2 cm). The parasitoids and beetles were assigned to
treatments and mortality was assessed.

Only 24 11 treated fern bioassay was done on the beetle larvae due to insufficient
number of third and fourth instar stages obtained from the field. There were difficulties
in separating them between the parasitized and non-parasitized beetle larvae at third or
fourth instar stage, therefore the larvae exposed to various treatments were randomly
chosen. 1 observed that all the treatments had parasitized larvae but in varying numbers.
No statistical analysis was done on the emergence of adult T. asparagi because of the

varying number of parasitized larvae present at the beginning of the bioassay.

Results and Discussion
Field Evlluation
Spear damage. The mean number of beetles and eggs per spear were

significantly lower in carbaryl and chlorpyrifos treated plots compared to pertnethrin

49

treated and control plots (P<0.05; F=12.37; df =1 1, 948) (Table 2). These treatments also
had less damage compared to permethrin and untreated plots (Table 3). Severe damage
category was significantly higher in the untreated plot compared to other treatments (P<
0.05; F=32.76; df= 11. 948.).

Table 2: Distribution of adults and eggs of the common asparagus beetle per spear
between treatments

 

 

 

 

Treatment

Carbaryl Chlorpyrifos Permethrin Control
Adult (n=240)
meant SE 0.1 i 0.03a 0.1 i 0.02a 0.2 i 0.04b 0.3 i 0.05b
C.V 4.67 3 3.11 6.70
k 0.83 0.01 0.22 0.02
s2 0.22 0.10 0.38 4.04
Egg (n=240)
meani SE 0.3 _+_ 0.13a 0.3 i 0.08b 0.5 i 0.20b 0.8 i 0.17b
C.V 6.70 4.30 6.18 3.60
k 0.02 0.07 0.33 0.11
s2 4.04 1.53 9.59 6.93

 

Values with the same letter in the row are not significantly different (P> 0.05,
Fisher's PLSD).

50

Table 3: Spear damage categories between treatments

spears (% i SE)

Treatments N No damage Low damage Moderate damage Severe damage

 

Carbaryl 240 47.7 i 5.6a 27.3 i 0.03a 11.8 i 2.8a 21.5 i 3.8a
Chlorpyrifos 240 50.8 i 7.0a 21.4 i 6.1a 8.4 i 3.3a 21.9 i 4.4b
Permethrin 240 39.7 i 7.4b 23.9 i 2.63 15.5 i 3.6a 25.7 i 6.1b

240 37.9 i 7.1b 22.5 i 2.4b 4.8 i 3.6a 37.8 i 6.5c

Untreated

 

Values with the same letter in the column are not significantly different (P> 0.05. Fisher's LSD)
The percentage was transformed to arcsinc before analysis to determine the significance

The distributions of the beetles and eggs were similar to that mentioned in
(Chapter 1) i.e.. overdispersed. The results (Table 2 and 4) show that the variances were
greater than the means and the coefficients of variation were greater than 2. indicating the
aggregating behavior in this beetle.

Spear damage at different date. Percentage of spears in the no damage category
was significantly lower on May 7 and 15. 1998 compared to May 21. 1998 ( P<0.05;
F =42.42; df=] 1, 948). The severe damage category was significantly lower on 21St May
compared to May 7, 1998 (P<0.05; F=32.76: df=l l, 948). as shown in Table 5. This may
be due to the damage caused by newly emerged adult beetles at the beginning of the
spring season, thus reducing the marketable quality of spears. The percentage of spears in

low and moderate damage categories was not significantly different at different dates. No

further harvesting was done after May 21. 1998.

51

Table 4: Distribution of adults and eggs of C. asparagi per spear between dates

 

 

 

 

Dates
7‘h May 1998 15‘h May 1998 21"t May 1998

Adult (n=320)

meani SE 0.1 :t 0.02a 0.4 i 0.06b 0.1 fl: 0.02a
C.V 3.60 2.68 3.58

k 0.33 0.21 0.33

52 0.13 1.15 0.13

Egg (n=320)

meani SE 0.3 i 0.08a 0.8 i 0.1% 0.3 i 0.11c
C.V 4.76 4.23 6.56
k 0.13 0.33 0.03

2 2.04 11.54 3.87

S

Values with the same letter in the row are not significantly different (P> 0.05.

Fisher's PLSD).

Table 5: Mean of spear damage category between dates

spears (% :t SE)

 

No damage Low damage Moderate damage Severe damage

 

Treatments N

May 7. 1998 320 39.9i2.1b 31.2i2.1a 14.0i2.8a 26.7i1.8b

May 15, 1998 320 22.9 i 4.3c 26.4 i 2.0a 17.3 i 3.3a 42.6 i 3.8b
6.6 i 2.7b 6.3 i 1.9c

May 21. 1998 320 69.4 i 2.9a 13.7 i 2.3b

Values with the same letter in the column are not significantly different (P> 0.05. Fisher's LSD)

 

The percentage was transformed to arcsinc before analysis to determine the significance

Rate of Parasitism (eggs collected from the treated plots)

Many beetle eggs were found to have collapsed and withered indicating host
feeding had occurred. On some asparagus stalks. the only viable eggs appeared to be
those recently deposited. The feeding of the parasitoid was so extensive that only a few
fresh eggs were able to be collected from spears within the treated plots for rearing.
Johnson (1915). Capinera & Lily (1975) reported that 71.29% and 50% of the eggs were
destroyed through host feeding respectively. There was no parasitism at all from eggs
collected from carbaryl and chlorpyrifos treated plots. Parasitism by T. asparagi in

untreated plots was 6.25% and in plots treated with permethrin was 1.43% (Figure 1A).

Percentage parasitism was significantly higher in the untreated than in the treated plots.
Significantly fewer adult beetles that emerged from the eggs collected from carbaryl.
chlopyrifos and permethrin treated plots than that from the untreated plot (Fisher PLSD;
P<0.05; F=2.83; df=3. 44) (Figure 18). This indicates that the insecticides could have
directly or indirectly killed the parasitoid embryo. This is similar to the results of Culin &

Dubose ( l 987) where chlordimeform. methyl parathion and esfenvalerate had

53

 

 

 

 

 

8
a

a (A)
6A 6 ~ ~~~~~
31:51
NCD 4 L, ,, , ,
5+1
3: o | | b b

untreated permethrin chlorpyrifos carbaryl

 

Adult emergence
(% i SE)

untreated permethrin chlorpyrifos carbaryl

Treatments

Figure 1: Percent of eggs parasitized (1- SE) in various insecticide
treatments (A). Percent asparagus beetle adult emergence (B) from
various insecticide treatments in the field. Bars with the same letters are
not significantly different (P>0.05).

54

 

significantly reduced the percent of Microplitis demolitor (Wilkinson) parasitized larvae
surviving to parasitoid pupation Heliothis zea (Boddie).
Capinera & Lily (1975) estimated the percentage parasitism in their study was
about 25%. In my studies it varied from 1.1% to 50.9% depending on the stage of crop
and type of crop management practices implemented (Chapter 1).

Due to the over-dispersal of beetles and eggs, parasitism may not be consistent
throughout the fields. T. asparagi may also be more abundant in certain parts of the field
for various reasons. They are either attracted to food resources or host cues. Parasitoids
may orient towards volatile chemicals produced from their hosts that attract the

parasitoids (Vet and Dickle 1992).

During harvesting. because of the removal of asparagus spears at 2-3 (1 intervals,
the beetles often laid eggs on the volunteer ferns growing between rows and on newly
developing spears. The number of eggs found in the volunteer ferns ranged from 3 to
18/fem. These volunteer ferns became the host plant as well as food source and shelter

for the parasitoids. T. asparagi continued to feed on the eggs. Numerous beetle eggs were
found to have collapsed and shriveled within the volunteer ferns, indicating parasitoid
feeding. The adults of T. asparagi were abundant and at times as many as five or six
adults were present on a single volunteer fern. The structure formed by the cluster of fern
may modify the microclimate making it more favorable for the parasitoid (Tahvanairen &
Root 1972). The "resource concentration hypothesis" suggests that specialists insect
herbivores should be more abundant where their foods are concentrated (Root 1973).
According to Sheehan (1986), specialist parasitoids may be more likely to find and less

likely to leave, concentrated patches of their prey's food.

55

 

Tamaki and Halfliill (1968) indicated that providing some structural diversity
such as having bands on peach trees encourage a number of predatory insects. This small
cluster of volunteer ferns may somewhat simulate the situations of a small asparagus field

that serve as refuges for the parasitoids. Townes (1972) and F elland (1990) described that

many natural enemies are habitat specialists in addition to or rather that being host
specialists.

Food sources or microclimate are the most likely influences on the distribution of
adult T. asparagi within the volunteer fern. It is unlikely that T. asparagi is attracted to
the host odor rather than encountering the resources i.e. egg as foods. T. asparagi may
seek the cooler, more humid microclimate of the volunteer fern. Hall & Ehler (1979)
found no difference in establishment rates of predators and parasites between unstable
and intermediate environments but a significantly higher establishment rate in stable
environments. In addition to parasitism, host feeding is a source of mortality. Some
parasitoid species kill more hosts by feeding than by parasitism (Kidd & Jervis 1989,
Heimpel & Collier 1996). Many insect parasitoids use hosts for oviposition and also as
food sources including Tetrasrichusflavigaster Brothers & Moran (Marchal 1905),

T etrastichus gallerucae F onscolombe (Howard 1910), T etrastichus chrysopae Crawford

(Clancy 1943), T etrastichus coccinellae Kurdjumov (Moran et. al.1969). Tetrastichus

incertus Ratzeburg (Dowell 1978).
I dris & Grafius (1993 a, b) found that there was lower parasitism when larvae of

Plutella xylostella (L.) (diamondback moth) were exposed to Diadegma insulare

(Cresson) in cages treated with permethrin than in untreated cages (i.e.. 7.8% and 79.4%

respectively). Powell et al. (1986) reported that there was an unusually high rate of

56

 

parasitism of cotton bollworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) larvae
by Microplitis croceipes (Cresson) in fields treated with pyrethroids compared to
parasitism in fields treated with organophosphates. Landis and Haas (1992) found that

parasitism 0f Ostrinia nubilalis (Hubner) by Eriborus Iercbrans (Gravenhorst) is not

correlated with host abundance.

Parasitism in all plots was very low, perhaps because eggs collected were often

 

freshly laid, with little exposure to T. asparagi oviposition. Plots were small and T.
asparagi adults could move freely between plots. It is not known whether it is residues of

carbaryl and chlorpyrifos that killed T. asparagi adults very rapidly and prevented

ovi position or carbaryl and chlorpyrifos residues that had affected the T. asparagi adult
behavior. Alternatively, eggs in all plots may have been parasitized equally but larval
parasitoid survival may have been affected by the carbaryl or chlorpyrifos treatment.
Other reasons could be that the adult parasitoid preferred to feed and oviposit on eggs

present in the volunteer ferns (more stable habitat) than on spears that were being

harvested frequently (unstable habitat).

The preferred stage of egg for oviposition by T. asparagi is 2-3 (1 old when the
embryo begins to develop (van Alphen 1980). The eggs will hatch after 3 d. T asparagi
has a very narrow window or period for oviposition to occur. In this experiment, eggs
were collected 24 h after insecticides have been applied, so it has to oviposit prior to
insecticide application or 1 d earlier. If the applications of insecticides coincided with the

time of oviposition, then the mortality of T. asparagi would be higher. The holes made by
T asparagi to oviposit onto the beetle eggs may also have allowed the diffusion of

insecticides solution within the eggs, thus poisoning the developing embryo.

57

Host feeding might also have reduced the availability of 1-2 day old eggs required

for oviposition.

Laboratory Evaluation (Residual Bioassav)

Treated filter paper assay (Adult T. asparagi)

1.0 mg AI/ml concentrations. Mortality of T. asparagi adults in the treated filter
paper assay was significantly higher with chlorpyrifos. malathion, carbaryl than with
permethrin and chlorothalonil (at 0.5 h; P<0.05; F=1 1.61; df=5. 23) (Figure 2A) (Table
6). In fact chlorpyrifos and malathion caused 100% mortality within 2 h of exposure
(Figure 2A). The mortality of T. asparagi at 30 min and 24 h exposure with all pesticides

solutions tested is shown (Figure 3A).

Table 6: Statistics for T. asparagi introduced onto treated filter paper at 1.0 mg
(AI)/ml concentrations

 

 

Exposure (hours) P F df
0.5 0.0001 11.6 4, 18
1 0.0001 10.9 4, 18
2 0.0001 60.6 4, 18
4 0.0001 70.4 .
24 0.0001 153.8 4, 18

 

0.1 mg AI/ml concentrations. Mortality of T. asparagi adults in the treated filter
paper assay was significantly higher with carbaryl than with chlorpyrifos, malathion
permethrin or chlorothalonil (at 2 h; P<0.05; F=13.l; df=5. 23) (Figure 2B) (Table 7).
Carbaryl, chlorpyrifos. and malathion caused 100% mortality at 24 11 exposure at 0.1 mg

AI/ml. Although permethrin showed less mortality. it still caused significant mortality to

58

 

__ .. <>- chlorpyrifos
t+carbaryl

- A- malathion

*- -X- permethrin

— +chlorothalanil
*—e—water

 

 

Mortality i SE (%)

 

 

g 100-
(‘2 8°“
+1 50.
E 40
N

E 20*
E o.

 

 

 

Figure 2: Percent mortality (i SE) of T asparagi adults 0.5, 1, 2, 4, 24 h
after being exposed to filter paper treated with 1.0 mg (AI)/ml (Graph A)
and 0.1 mg (AI)/ml (Graph B) pesticide solutions.

59

8O

 

60 a a (A)

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

A
2°
V
b b b
3 120
z (B)
so
60. b
40
20 c d
o I l
s. e if; a a 2
e w - E 5
'- 0 cu ,_ o
2 E o I-
.c a. O
o E
0

Figure 3: Mortality of T. asparagi 30 min (A) and 24 h (B) after being
exposed to filter papers treated with 1.0 mg (AI)/ml pesticide solutions.
Bars with the same letter are not significantly different [(A) P>0.05,
F=11.6: (B) F=153.7: df=23].

60

 

(A)

8888

 

 

 

 

”'6‘

\

i, 10

E o D-
CB

fl

1—

§ 120

100

 

 

 

oases

carbaryl
malathion
permethrin
water

in
.2
':
>4
0.
h
.2
.c
o

chlorothalonil

Figure 4: Mortality of T. asparagi 30 min (A) and 24 h (B) after being
exposed to filter papers treated with 0.1 mg (AI)/ml pesticide solutions.
Bars with the same letter are not significantly different (B) p> 0.05,

F =146.6 and df=23. Data in (A) were all 0% except in malathion (5%) and
therefore could not be analysed using standard ANOVA.

6|

T asparagi. The mortality of T asparagi at 30 min and 24 11 exposure with all pesticides

solutions tested is shown (Figure 4).

Table 7: Statistics for T. asparagi introduced onto treated filter paper at 0.1 mg (Al)/ml
concentrations

 

 

Exposure (hours) P F df
0.5 0.45 1.0 4. 18
1 0.56 0.9 4, l8
2 0.0001 13.1 4.18
4 0.0001 31.5 4, 18
24 0.0001 146.6 4. 18

 

Field sprayed asparagus fern assay (Adult T. asparagi)

1.0 mg AI/ml concentrations. For T. asparagi introduced onto fern 1 h after it
was sprayed in the field, mortality after 0.5 h exposure was significantly higher with
carbaryl, chlorpyrifos, than with malathion, permethrin or chlorothalonil (P<0.05;
F=4.62; df=5. 23) (Figure 5A) (Table 8). After 4 h exposure mortality was significantly
higher with carbaryl. chlorpyrifos, and malathion than with permethrin or chlorothalonil
(P<0.05; F=23.9; df=5. 23) (Figure 5A). After 24 h exposure all insecticides including
permethrin were highly toxic to T. asparagi, causing 100% mortality (Figure 5A). Even

chlorothalonil was found to be toxic and caused 60% mortality at 24 h of exposure.

 

+chlomyfifos
- —B—carbaryl

- -A- malathion

‘ - -X- permethrin
‘- -X- chlorothalonil

 

 

Mortality i SE (%)

 

 

100
80 -
60
40
20

 

 

Mortality i SE (%)

 

Time (hours)

Figure 5: Percent mortality (i SE) of T. asparagi adults at 0.5, 1, 2, 4. and 24 h
being exposed to 1 h after the fern was treated (A) or 24 h after the fern was
treated (B) with 1.0 mg (AI)/ml pesticide solutions.

63

Table 8: Statistics for T. asparagi introduced onto fern 1 h after it was sprayed in the
field at 1.0 mg (AI)/ml concentrations

 

 

Exposure (hours) P F df
0.5 0.0001 4.6 4, 18
1 0.0001 30.9 4, 18
2 0.0001 21.5 4, 18
4 0.0001 23.9 4. 18
24 0.0001 53.5 4, 18

 

For T asparagi introduced onto fern 24 h after it was sprayed in the field.
mortality after 0.5 h exposure was significantly higher with carbaryl, than with
chlorpyrifos. malathion. permethrin or chlorothalonil. (P<0.05; F=18.1; df=5. 23) (Figure
SB) (Table 9). After 4 h exposure mortality was significantly higher with carbaryl,
chlorpyrifos, than with malathion, permethrin or chlorothalonil (P<0.05; F=158.6; df=5.
23) (Figure 5B). After 24 h exposure all insecticides including permethrin were highly
toxic to T. asparagi, causing 100% mortality (Figure 5B).

Table 9: Statistics for T. asparagi introduced onto fern 24 h after it was sprayed in the
field at 1.0 mg (AI)/ml concentrations

 

 

Exposure (hours) P F df
0.5 0.0001 18.1 4. 18
1 0.0001 29.2 4, 18
2 0.0001 88.6 4, 18
4 0.0001 158.6 4, 18
24 0.0001 237.7 4, 18

 

64

Little is known about the impact of pesticide residues on T. asparagi. In the field,
the adult parasitoids are exposed to pesticides during application and immature stages are
exposed within the asparagus beetle eggs and larvae.

The evaluation of these pesticides both in field and laboratory, indicated that
carbaryl (carbamate). chlorpyrifos and malathion (organophosphate) were extremely
toxic to T asparagi. But these three compounds are widely used by the commercial
asparagus growers in Michigan and in other states (Eskelson et al. 1996). The insecticide
residues on the field treated fern (foliar residue) and on the filter paper were equally toxic
to adult T. asparagi.

Carbaryl is very toxic to many natural enemies (Barlett 1963, 1964); Moffitt et al.
(1972), Grafton Cardwell & Hoy (1986), Travis et al. (1978), Wilkinson et al. 1975,
Tipping & Berbutis 1983; Pree & Hagley 1985; Prokrym 1988; Thorpe et al. 1995).
Chlorpyrifos and Malathion (organophosphates) are also toxic to many parasites and
predators (Plapp & Vinson 1977. Plapp & Bull 1978, Idris & Grafius 1993 a,b).

Coats et al. (1979) reported that permethrin was 1000x more toxic to T. julis than
the adult host 0. melanopus. Among the pyrethroids they tested, cypermethrin was least
toxic to T. julis but still toxic to the host. Pyrethroids showed variable toxicity to parasites
ranging from 100% to a low of 3% (Croft and Whalon, 1982). In laboratory experiments
(Idris and Grafius 1993a, b) pyrethroid insecticides (permethrin, cypermethrin, and
esfenvalerate) were more toxic to D. eucerophaga than P. xylostella. Verghese et al.
(1990) stressed that deltamethrin (Decis) was the least toxic to Tetrastichus sp. which is
an important parasite of mango hoppers. Permethrin was the least toxic of all the

insecticides tested in my studies (partly due to short persistency) (Powell et al. 1986).

65

Although literature both supported and refuted the toxicity of synthetic
pyrethroids, research does show that pyrethroids can be used with lower risk compared to
the other insecticides like carbomate and organophosphate, which are used widely by
commercial asparagus growers.

Chlorothalonil was not expected to kill T. asparagi, but when used heavily in
controlling the purple leaf spot disease at fern stage, it might have an effect on T.
asparagi. The results indicated that it caused 60% mortality within 24 h when T
asparagi was exposed to residues in the field treated fern for 1 h at 1.0 mg (AI)/ml
concentration. This might be the case when T. asparagi is exposed to ferns immediately
after spraying in the field. In other bioassays. mortality due to chlorothalonil was 0-20 %.

In Michigan, other than chlorothalonil, mancozeb is the most commonly used
fungicides to control purple leaf spot diseases in asparagus (Johnson and Lunden 1992).
Mancozeb is no longer used in asparagus crop and the change to chlorothalanil likely will
decrease the impact on T. asparagi. F elton & Dahlam (1984) reported that fungicide
maneb, was more toxic to M. croccipc.s' than its host Heliothis virescens (Fabricius)
(Lepidoptera: Noctuidae) even at low concentrations. Prokrym (1988) showed that
excessive use of maneb fungicide killed the entomophthoracean fungi that used to
regulate aphid populations in asparagus fields. Chlorothalonil is also reported not to kill
the entomphthoracean fungi Erynia blucki (Lakon) and Zoophthora radicans (Brefeld)
that often infected diamond back moth larvae and pupae (Tomiyama & Aoki 1982. and

Wilding 1986).

66

 

W ---... mm.- -~--~~——----w---~ 4»-

Treated filter paper assay (Asparagus Beetle)

1.0 mg AI/ml concentrations. Mortality of adult beetles was significantly
higher with carbaryl than with chlorpyrifos. malathion, permethrin or chlorothalonil after
4 exposure (P<0.05; F=25.5; df=5. 23) (Figure 6A) (Table 10). After 48 h exposure
mortality was also significantly higher with carbaryl and Chlorpyrifos than with
malathion, permethrin or chlorothalonil (P<0.05; F=30.6; df=5. 23) (Figure 6A).
Carbaryl, chlorpyrifos and Malathion caused 100% mortality after 72 h exposure.

Table 10: Statistics for the common asparagus beetle introduced onto treated filter paper
at 1.0 mg (AI)/ml concentrations

 

 

Exposure (hours) P F df
4 0.0001 25.5 4, 18
8 0.0001 114.5 4, 18
16 0.0001 67.5 4, 18
24 0.0001 25.4 4, 18
48 0.0001 30.6 4, 18
72 0.0001 62.5 4. 18

 

0.1 mg AI/ml concentrations. All insecticides showed delayed poisoning at the
beginning when exposed to 0.1mg(AI)/ml concentration compared to the 1.0 mg (AI)/ml
concentration (Figure 6B) (Table 11). After 48 h exposure carbaryl and chloripyrifos
caused significantly higher mortality than other pesticides used in this bioassay (P<0.05;

F=4.1; df=5. 23).

67

 

1

   

ceases

 

 

 

 

100 _. L _ _,._ L2- ELLA. fl _.

8MB ‘ H .i'ili

 

 

 

Figure 6: Percent mortality (i SE) of the common asparagus beetle adults
at 4. 8, 16. 24, 48 and 72 h after being exposed to treated filter paper with
1.0 mg (AI)/ml (A) and 0.1 mg (AI)/ml (B) with pesticide solutions.

68

Table 11: Statistics for the common asparagus beetle introduced onto treated filter paper
at 0.1 mg (AI)/ml concentrations

 

 

Exposure (hours) P F df
4 * 4. l8
8 * 4. 18
16 0.0684 2.5 4. 18
24 0.0037 5.3 4. 18
48 0.0124 4.1 4, 18
72 0.0005 7.7 4, l8

 

* - Zero mortality

Field Sprayed F ern (Adult Beetle)

1.0 mg AI/ml concentrations. For adult beetles introduced onto fern 1 h after it
was sprayed in the field. mortality after 4 h exposure was significantly higher with
carbaryl than with chlorpyrifos. malathion. permethrin or chlorothalonil (P<0.05; F =50.2:
df=5. 23) (Figure 7A) (Table 12). All insecticides caused 100% mortality after 16 h of
exposure. Chlorothalonil although a fungicide but still caused 80% mortality. It may have
some insecticidal impact on the adult beetle.

Table 12: Statistics for the common asparagus beetle introduced onto fern 1 h after it was
sprayed in the field at 1.0 mg (A1)/ml concentrations

 

 

Exposure (hours) P F df
4 0.0001 50.2 4. l8
8 0.0001 73.8 4, 18
16 0.0001 75.8 4. 18
24 0.0001 362.8 4, 18
48 0.0001 114.5 4. 18
72 0.0001 104.5 4. 18

 

()9

 

 

 

 

100 - o—g-aTl—rx x x x--4
, L t ., , i- 0: clildrpyrifos

—B—carbaryl

- ~A- malathion

- -x- permethrin

- -X- chlorothalonil

‘ .—°,T,‘”§t?" - ,

 

 

 

Mortality i SE (%)

 

Time (hours)

 

100 -
80 -
60
40
20

 

 

Mortality i SE (%)

 

Time (hours)

Figure 7: Percent mortality (3: SE) of the common asparagus beetle adults
at 4. 8. 16. 24. 48. and 72 h after being exposed to 1 h after the fern was

treated (A) or 24 after the fern was treated (B) with 1.0 mg (AI)/ml
pesticide solutions.

70

1.0 mg AI/ml concentrations. For T. asparagi introduced onto fern 24 h after it
was sprayed in the field, mortality after 4 h exposure was significantly higher with
carbaryl, than with chlorpyrifos. malathion. permethrin or chlorothalonil (P<0.05;
F=57.5; df=5. 23). (Figure 78) (Table 13). Chlorpyrifos caused 100% mortality after 48 h
of exposure.

Table 13: Statistics for the common asparagus beetle introduced onto fern 24 h after it
was sprayed in the field at 1.0 mg (AI)/m1 concentrations

 

 

Exposure (hours) P F (if
4 0.0001 57.5 4, 18
8 0.0001 355.1 4. 18
16 0.0001 69.6 4, 18
24 0.0001 146.6 4, 18
48 0.0001 106.9 4, 18
72 0.0001 36.9 4, 18

 

Little is known about the impact of pesticide residues on the common asparagus
beetle. In the field, adult beetles. larvae and eggs are often exposed to insecticides. The
effect of insecticides on mobile insects has substantial impact on the dispersal and
population dynamics of insects (Tabashnik et a1. 1988). Since the adult beetles aggregate
on preferred spears and ferns, the frequent application of insecticides may cause
significant mortality. But the dodge and feign behavior exhibited by this beetle when
disturbed (Capinera and Lilly 1976) will prevent direct contact with insecticides. So the
effect of insecticides can only be through ingestion or contact with residues. The adult

beetles did feed when exposed to ferns treated with insecticides in captivity during the

71

bioassay studies, though the feeding rate was slow. Although both contact and residual
toxicity can cause beetle mortality in the field. the mortality of this beetle would largely

be due to the latter.

Field sprayed fern assay (Asparagus Beetle Larvae)

1.0 mg Al/ml concentrations. After 8 h exposure, mortality of asparagus beetle
larvae was significantly higher with carbaryl or malathion than with chlorpyrifos.
permethrin or chlorothalonil (P<0.05; F=19.2; df=5. 23) (Figure 8) (Table 14). However,
after 16 to 72 h exposures. mortality was higher with carbaryl, chlorothalonil, malathion
than with permethrin. Malathion and carbaryl were very toxic to beetle larvae and were
the most effective insecticides that could be used at larval stage. The rate of mortality was
much faster when compared to other insecticides used in this experiment.

Table 14: Statistics for the asparagus beetle larvae introduced onto fern 24 h after it was
sprayed in the field at 1.0 mg (Al)/ml concentration

 

 

Exposure (hours) P F df
8 0.0001 19.2 4. 18
16 0.0001 50.7 4. 18
24 0.0001 999.9 4, 18
48 0.0001 315.3 4. 18
72 0.0001 290.8 4. 18

 

The mortality caused by permethrin was significantly lower than other
insecticides even after being exposed to 72 h at 1.0 mg (AI)/ml concentrations. The

larvae were found to continue to feed continuously on fern that was treated with Figure 8

i SE (%)

Mortali

100

 

 

 

 

 

Time (hours)

- -<>- Tclilorpyrifos
—0—carbaryl

- A- malathion

’- -x- permethrin
—X— chlorothalonil

Figure 8: Percent mortality (3: SE) of the common asparagus beetle larvae
at 8. 16. 24. 48. and 72 h being exposed to 24 h after the fern was treated

with 1.0 mg (AI)/ml pesticide solutions.

permethrin and cholorothalanil. The parasitized larvae produced live adults of T
asparagi in both pemiethrin and chlorothalonil treatments.

Even though permethrin is highly toxic to the adult T. asparagi, the parasitized
larvae at advanced stage seem to be less sensitive to permethrin. The time taken for the
parasitoid larvae to emerge into adult on permethrin treated fern was longer (mean= 21.5
days) than on normal water treated fern (mean = 15.5 days). The parasitized larvae may
have undergone physiological stress due to the exposure to permethrin residues that
delayed development.

Conclusion
It is clear that T. asparagi alone is incapable of controlling and regulating the
asparagus beetle populations under normal commercial production conditions. Insecticides
were still required to reduce the damage caused by the beetle both at spear and fern stage.
The use of insecticides to control the common asparagus beetle likely reduced both the
rate of parasitism and the adult beetle emergence. Both field and lab tests indicated that
carbaryl, chlopyrifos, malathion an permethrin were highly toxic to T. asparagi adults.

The most critical in asparagus beetle management is the timing of insecticide

application. The blanket application of carbaryl dust practiced by the commercial growers
probably is not the right formulation and method because the parasitoids overwinters in
and emerge from the soil. The carbaryl dust may form a thin layer on top of the soil. the
residue may potentially kill some of the young susceptible emerging adult parasitoids.
Also, dust formulations are known to be much more toxic to honey bees than other
formulations (Michigan State University Extension Bulletin E 312. 1998).

The relatively safer insecticides such as synthetic pyrethroids. can be used to

74

reduce the beetle population. Even though it did cause mortality to T. asparagi, the rate of
poisoning by permethrin was slower than the other insecticides. In the field, the toxicity of
permethrin may be further reduced due to the chemical breakdown by sunlight. The
interactions with pesticides breakdown in the field are not known. The permethrin activity
reduced the most by 24 h post spray interval. The laboratory bioassay chiefly tested the
physiological and metabolic resistance that may inhibit behavioral responses of T
asparagi toward pesticides when applied in the field.

In order to reduce the impact of pesticide residues to the newly emerged
parasitoid, the selected pesticides should have short or moderate persistency and the
application should be carried out evening. T asparagi adults have peak searching activity
from 10.00 AM to 2.00 PM and relatively less in the late afternoon (personal observation).
According to (Grafius & Hutchison 1995), the adult beetles are most active feeding and
egg laying during mid-day. Pesticides could be applied on alternate rows rather than as a
blanket spray (Casagrande & Haynes 1986). This would allow adult parasitoids and
parasitized larvae in the unsprayed rows to survive and multiply.

T asparragi is host specific and is known only to feed on the common asparagus
beetles' eggs. It is unlikely that the surrounding crops: apple trees, mixed grasses, and
pastures could have contributed to the significant impact on the dynamics of T. asparagi
within the trial plot. However refuges, nectar and diurnal changes may have influenced the
movement, migration and rate of parasitism. Strong winds may have carried the adult
parasitoid to the neighboring plots subsequently affecting the parasitism. In addition to the
environmental factors. T asparagi is highly mobile and may distribute themselves

throughout the field without being affected by individual plot treatment. Good

75

understanding about the parasitoid behavior, the habitat requirement for parasitoid
sustainability, and the selectivity or toxicity of insecticides to both the beetle and

parasitoid could ensure the successful implementation of the IPM system.

76

Chapter 3

Effect of Nutrients on the Longevity and Fecundity of T etrastichus asparagi
Crawford (Hymenoptera: Eulophidae), an Egg-Larval Parasitoid of the Common

Asparagus Beetle (Coleoptera: Chrysomelidae)

77

Abstract: Studies were done in the laboratory on the effect of various food nutrients on
the longevity and fecundity of Tetrastichus asparagi Crawford, an egg parasitoid of the
common asparagus beetle Crinccris asparagi (L). Longevity of T. asparagi was 16.9 (:1
when fed with host egg + honey water and only 3.8 d only when asparagus flowers were
provided. Host feeding was not significantly different among the various nutrient sources
eggs, eggs+honey water. eggs + asparagus flowers. and eggs + asparagus shoots. The
number of eggs parasitized was 0.7 per T asparagi when host egg + honey water was
provided and only 0.2 eggs were parasitized when host eggs + asparagus flowers were
provided. The number of adult T. asparagi that emerged from the eggs + honey water
treatment was significantly higher than from egg + asparagus flowers treatment (2.37 and
0.73) per female respectively. The longevity and fecundity of T. asparagi was not
affected at all when asparagus cut flowers were used. It is likely that asparagus cut
flowers might not have had produced enough nectar or pollen or had some repellant
effect. Host feeding was the main mortality caused by T. asparagi and 4.3 eggs per T.
asparagi were eaten on the first 48 h of egg provision. Host feeding was gradually
reduced as the T asparagi aged. This study indicated the T. asparagi longevity and

fecundity may be enhanced in the field by providing habitats that provide nectar sources.

Key Words: lnsecta, T etrastichus asparagi. Crioceris asparagi, common asparagus

beetle, host feeding. parasitism. longevity. and fecundity

78

 

 

 

Introduction

Tetraslichus spp. (Hymenoptera: Eulophidae) can be major mortality factors of
many insects. They often host feed on eggs and oviposit in one or more of the stages
(egg, larvae, or pupae) of the host. Some examples of host feeding species are:
Tetrastichusflavigaster Brothers & Moran (Marchal 1905). Tetrastichus gallerucac
Fonscolombe (Howard 1910). Telraslichus asparagi Crawford (Johnston 1915),
Tetrastichus chrysopae Crawford (Clancy 1943), T ctraslichus coccinellae Kurdjumov
(Moran et. al.1969) and T ctrastichus inccrtus Ratzeburg (Dowell 1978). Species not
known to host feed include: T etrastichus giflardianus Silvestri (Clausen et al. 1965),
Tctrastichusjulis (Stehr 1974), Tetrastichus brevistigma (Fonscolombe) (Clausen 1978)
and Tcl‘rastichus sesamiae Risbec (Okeyo-Owuor 1991).

T asparagi is a monophagus gregarious egg-larval parasitoid that feeds on the
eggs of the common asparagus beetle. Crioceris asparagi (L. ) (Coleoptera:
Chrysomelidae). T. asparagi feeds and oviposits on the egg (Johnston 1915, Capinera &
Lilly 1975). Based on the characteristics of host feeding parasitoids as explained by
Jervis & Kidd (1986). T asparagi is 'synovegenic' because females emerge with only a
fraction of their egg compliment and for production of new eggs, depends upon the
female's ability to utilize host materials and or other nutrient sources (Flanders 1950).

T. asparagi is thelyothokus; all adults are females (i.e.. parthenogenetic
development where, unmated females produce only females (Johnston 1915).

Food consumption by the adult females of many parasitoids affect their

reproduction, survival. and host searching efficiency (Jervis et al. 1996). The parasitoids

use hosts not only for oviposition but also as food source (Jervis and Kidd 1986; Heimpel

79

& Collier 1996). Even host-feeding parasitoids (those that feed on host blood, tissue, or
eggs) also consume non-host foods. Host materials are used primarily for egg production
and non-host materials for maintenance (Engelman 1970 and Jervis et al. 1993).
According to Jervis and Kidd (1986), the host feeding behavior of T. asparagi is non-
concurrent (different individual hosts are used for feeding and oviposition) and
destructive (the host dies as the result of feeding).

Host feeding parasitoids also differ in their lifetime patterns of host feeding and
oviposition. A large number of species are able to lay eggs without host feeding (known
as autogenous). T asparagi could be described as an autogenous host feeder based on the
description of the feeding behavior by van Alphen (1980). He found that newly emerged
adult females, immediately started to oviposit when exposed to freshly laid beetle eggs.
He reiterated that host feeding is not a pre-requisite for oviposition in this species as was
previously believed. However he did not indicate whether host feeding increased the
longevity in this species.

Some species like Scam/711s bualeane Hartig (Hymenoptera: Ichneumonidae)
(Leuis, 1961a) and Exerristes comstockii (Cresson) (Hymenoptera: Ichneumonidae)
(Bracken 1965). are anautogcnous, whereby females oviposit only if they have previously

host fed (often called 'obligate' host feeders) (Jervis and Kidd 1986).

Influence of adult diet on longevity and fecundity. Both longevity and
fecundity are likely to be influenced by the types of host food (egg, larvae, pupa or adult)
and non-host food (nectar, pollen and honey dew) consumed by a parasitoid (Leuis 1961
a, b; Avidov et al. 1970; Shahjahan 1974; Idoine & Ferrow 1988; Idris & Grafius 1995;

Jervis et a1. 1996). Generally the egg contents of insects are rich in proteins. essential

80

vitamins and salts (Bracken 1965 & 1966). They also found that absence of amino acids.
inorganic salts and vitamins proved detrimental to the parasitoid but the absence of RNA
and cholesterol from such diets had no effect on fecundity. Absence of certain B vitamins
also decreased parasitoid egg hatch (Bracken 1966). Parasitoids that host feed on insect
eggs primarily consumes vitellogenins which are composed mainly of protein. but may
also contain some carbohydrates and lipids (Woodring 1985).

Jervis et al. (1996) summarized the rank order in term of proteinaceous food
quality, i.e.. fecundity value of non-host foods: pollen > honeydew > nectar and the
quality in terms of energy and survival value: honeydew > nectar > pollen.

Although most species show an increase in longevity with host feeding in the
presence of honey. there are exceptions. Heimpel & Collier (1996) showed for female
parasitoids given host meals without sugar. host feeding prolonged life in 12 parasitoid
species but not in seven others. Host feeding with sugar enhanced longevity of 1 1 species
but in two species. longevity was not affected. For ichneumonoids and chrysopids host
feeding prolonged life in all species whereas for chalcidoids, host feeding prolonged life
in some but not all species. This may reflect differences in the metabolism of nutrients or
energy obtained from host feeding (Collier 1995a).

In a study of T. giflardianus, a larval parasitoid of tephritid fruit flies, the
longevity of ovipositing females was 60% less than longevity of females deprived of
hosts (Purcell et al. 1996). For T. gallarucae. an egg parasitoid of the elm leaf beetle.
Xanthogaleruca luteala (Muller) (Coleoptera: Chrysomelidae), females lived for 59 (I

when fed with host eggs and honey water (Hamerski & Hall 1988).

81

Bai & Smith (1993) found that longevity in Trichogramma minutum (Riley)
(Hymenoptera: Trichogrammatidae) was increased by the presence of hosts when
supplemental honey was present. A separate experiment done by (Bai & Smith 1993)
found no such effect. Sahragard, Jervis & Kidd (1991) showed that the female
Dicondylus indianus OLMI (Hymenoptera: Dryinidae) fed on honey, lived only 6-7 d
while those fed on hosts (but not honey) lived at least 1 1 d. Trichogramma plateneri
(Nagarkati) (Hymenoptera: Trichogrammatidae) females when given hosts and honey did
not live longer than females fed honey only (Hohmann et al. 1988) and differences in the
number of hosts that Trichogramma embryophagum Riley (Hymenoptera:
Trichogrammatidae) fed upon did not affect longevity (Klomp & Teerink 1967).

For aphelinid, Aphytis melinus (Debach) (Hymenoptera: Aphelinidae), host
feeding prolonged life in the presence of honey but did not do so in its absence. One
explanation is that adult parasitoids may require sugars that are not present in
haemolymph. Another potential explanation involves the rate of oosorption and or
catabolism (Collier 1995a). A. melinus resorb eggs at a rate of l/d or less (Heimpel &
Rosenheim 1995).

Female S. buolianae. provided with larvae of Galleria mellonclla (L.), (greater
wax moth) + pollen + sucrose lived significantly longer than those fed on other diets in
the same experiment. When the females were supplied with body fluids of the host, their
lifes were shorter than when carbohydrates were supplied. Females supplied with water

or honeydew alone died sooner than females fed on any other diet in the experiment

(Leuis 1961. b).

82

Syme (1975) reported that the fecundity of Hyssapus 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. He also
confirmed that some flower types were ignored when nectar was not accessible because
of physical limiting factors.

The avoidance of some flower types is likely to be attributable to accessability or
the nutritional value, repellency or toxicity of different nectars (Jervis et al. 1993). Idris
and Grafius (1995) showed that D. insulare fecundity and longevity when fed on several
flowers including Brassica kaber (D. C) Wheeler, Barbarea vulgaris R. Br. and Dacus
carota L.,honey-water was equal to when honey water was supplied as food. When the
females Encarsiaformosa (Gahan) (Hymenoptera: Aphelinidae) were allowed to feed on
small hosts as well as honeydew, they did not live longer than females fed on honeydew
alone. Females that were given honeydew and large hosts to feed on or oviposit lived

longer than honeydew-fed females (van Lenteren et al. 1987).

Host feeding and fecundity. Host feeding may have profound effects on host
parasitoid population dynamics Jervis and Kidd (1986). Hosts are also a valuable source
of nutrients for egg production and maintenance (Jervis et al. 1996). The likely question
to be asked was whether the adults prefer to feed or oviposit to maximize their
reproductive success.

Hamerski & Hall (1988) observed that T. gallerucae destroyed 65% of the host
eggs by host feeding and the rate of parasitism was highly variable. Debach (1943)

attributed 71 % of the mortality of black scale Saissetia oleac Bernard (Homoptera:

Coccidae) to Melaphycus bclvolus (Compere ) (Hymenoptera: Encyrtidae). 55% were

83

killed by host feeding and 16% by parasitism.

The number of eggs produced varies with the type of food given (Debach &
White 1960; Barlett 1964; Leuis 1961a). Female Bracon hebetor Say (Hymenoptera:
Braconidae). Nasom'a vilripennis (Walker) (Hymenoptera: Pteromalidae) and Aphytis
lingnanensis Compere (Hymenoptera: Pteromalidae) also produced eggs but in smaller
numbers, when starved or given only water (Benson 1973. Debach & White 1960.
Edwards 1954b, Lum 1977). In all species. the fecundity was greatest in females
provided with haemolymph. and was further improved by including other foods in the
diet (Leuis 1961 a). Only the inclusion of honeydew and a certain type of pollen in the
diet, resulted in a decrease in fecundity. Bracon serinopae Cherian (=Habrobracan
seronopae) (Hymenoptera: Braconidae). a wasp that is parasitic on the Anagast'a
(=Ephestia) ruheniella (Zeller) (Mediterranean flour moth). The A. ruheniella fed females
were fertile while honey fed females were sterile.

Some synovegenic parasitoids, including majority of the host feeding species. are
able to resorb eggs when hosts are absent or scarce. This is considered to be a last resort
survival tactic on the part of the female. The nutrients from the eggs can be used to
maintain the female until she can resume oviposition (Jervis & Kidd 1986, 1992a).
Edwards (1945a) stated that egg maturation and resorption could occur simultaneously in
N. vitripennis. Oosorption may prolong the life of adult female parasitoids, presumably
by supplying energy and or nutrients to the metabolic processes (Debach & Rosen 1973.
Bell & Bohn 1975, Collier 1995a).

Diurnal patterns also affect host feeding and oviposition. Two best studied

patterns were Gonotopus sepsoides Westwood and Microterysflavus Howard

84

(Hymenoptera: Erytridae). G. sepsoides usually feed on the first host individually
encountered during the day and subsequent hosts are used for ovipostion (Collin. Ward &
Nixon 1981). In M. flavus the host feeding is not essential for oviposition at the
beginning ofthe day. The females mainly oviposit during the first half ofthe day and
host feed during the second half (Barlett 1964).

T. asparagi adult eats an average of 2.5 beetle eggs per day (Russell & Johnston

1912). Johnston (1915) indicated that up to 71 per cent of the beetle eggs' mortality was
attributed to host feeding by T. asparagi. In his opinion, T. asparagi appeared to be of
greater value as an egg destroyer than as a parasitoid. In his laboratory trials, 19 females
with an average life of about 7.5 days. fed upon 518 host eggs but parasitized only 279.
The host feeding mortality of 65% was close to mortality he observed in the field.
According to Capinera & Lilly (1975) the mortality rate due to host feeding by T.
asparagi was 50% and mortality from parasitism was about 25%. Hendrickson et al.
(1991) reported that the parasitism rate varied from 0.5% to 49.3% depending on the
location and climate. In my studies. parasitism ranged from 1.1 1% to 50.9% (Chapter 1)
depending on the methods of asparagus crop management.

Johnston (1915), Capinera & Lilly (1975) and van Alphen (1980) worked on a
range of topics including life cycle. host feeding behavior and ovipositional behavior but
included no information on the nutrients requirement for longevity and fecundity of T
asparagi.

The asparagus plant also produces large number of flowers and are good sources
of pollen and nectar (Pellet 1976, Howes 1979). The asparagus inflorescence is dioecious

and flowers having nectaries at the base of the corolla. The individual flower is

85

pendulous, bell shaped, and about 6 mm long.

Honeybees were found to utilize the asparagus flower during mid-day either for
both nectar and pollen. I assume that the T asparagi adult might acquire protein from the
common asparagus beetle eggs through host feeding and nectar sources from asparagus
flowers.

An understanding of the relative importance of asparagus flowers' as nectar
sources and plant exudes to the adult T. asparagi may be important to enhance its role
and effectiveness in asparagus beetle management in the field.

The objective of this study was to examine the availability and influence of
various sources of nutrients (beetle eggs. honey, nectar source from asparagus flower) on

the longevity and fecundity of T asparagi in laboratory conditions.

Materials and methods

Food Sources

Asparagus beetle egg. Adult common asparagus beetles were collected from
Michigan State University Collin Road Entomology Research Farm and Horticulture
Research Farm and released into rearing cages (30cm X 30 cm X 30 cm). Fresh
asparagus ferns were collected from the fields cut into smaller branches 12-15 cm in
height and inserted into vials containing distilled water. The vials with ferns were then
placed vertically in the rearing cages. After 24 hours. the ferns were removed from the
cage and the asparagus beetle eggs were counted. In my preliminary observations. the
number ofegg fed ranged between 3 - 7 per 2 d. The branches with 210 eggs were then

transferred into another small vial containing distilled water and plugged with sponge.

Eggs >10 were removed. These vials with fern & eggs were used for the T. asparagi

86

longevity and fecundity experiments.

Sources of insects. 1-3 d old T asparagi from the first generation of laboratory
reared was used in the study. Parasitoid rearing methods were similar to the experiment
in Chapter 2.

Asparagus flowers. Asparagus flower stalks were collected from the asparagus
field. About 10 cm length of the stalks with 3-4 newly opened flowers and 3-4 unopened
flower buds were cut and inserted into a vial containing distilled water and plugged with
a sponge. Fresh flower stalks were replaced at every 2 d.

Asparagus shoot. Young terminal shoots were collected from the field and cut
into 8 cm lengths. The small stalks were then inserted into a vial containing distilled
water and plug with a sponge. These terminal shoots were used in the experiment. Fresh
young terminal shoots were replaced every 2 d.

Honey water. Honey was diluted with distilled water (10% honey, vol : vol) and
used in this experiment. The honey solution was poured into small vials by using syringe
and plugged with a sponge.

Water. Tap water was used as a control in the longevity studies.

Longevity

Treatments. The following treatments were used: 1) fresh beetle eggs (10). 2)
honey water, 3) asparagus flowers, 4) tap water, 5) no food, 6) fresh beetle eggs (10) +
honey water honey. 7) fresh beetle eggs + asparagus flowers and 8) fresh beetle eggs +
asparagus shoots.

The vials containing the food sources were placed horizontally in a petri dish

( 1 50 x 15 mm) and cotton rolls were placed on both sides of the vials to avoid

87

movements of the vials within the petri dish that could accidentally injure or kill the adult
parasitoids. The adult T asparagi were introduced into each of the petri dishes (1 per
dish, 5 dishes /treatment) using the same method applied in Chapter Two. They were then
held at growth chamber at 24 i 2°C. 50-70% relative humidity, and 16:8 (LzD)
photoperiod. Fresh food nutrients were replaced every 2 d. Two drops of honey water
were added to the vial containing honey water every 2 d.

The eggs were replaced at 2 d interval because earlier experiments showed that
T asparagi do not feed on old eggs and the eggs start to hatch by the third day. T
asparagi tend to prefer old eggs (2-3 days) for oviposition (van Alphen 1980). The
survival of T asparagi was recorded daily to measure longevity.

Data was analysed using l-way analysis of variance and the means were separated

using Fisher's protected LSD test (SAS Institute 1989).

F ecundity

Treatments. The following treatments were used: 1) fresh beetle eggs (10). 2)
eggs (10)+ honey water. 3) eggs (10) + asparagus flower, and 4) eggs (10) + asparagus
shoots. The adult T asparagi were introduced into each of the petri dishes containing
various nutrients using similar methods as in the earlier experiments (l/dish. 5
dishes/treatment). They were held at 24 i 2°C. 50-70% relative humidity. and 16:8 (L: D)
photoperiod.

To measure the host feeding, I counted the eggs that were fed at 2 d intervals. For
fecundity evaluations. I took the eggs that were not eaten and transferred them into
another petri dish and allowed them to hatch. The newly emerged larvae were reared in

the laboratory by feeding them with fresh ferns until pre-pupal stage. At this stage. the

88

developing T asparagi larvae within the host larvae could be seen. For adult T. aspuragi
emergence. the pre-pupal cells containing the parasitoid larvae were allowed to continue
to develop. I also dissected the dead host larvae to determine the parasitism and
fecundity. The fecundity was calculated as the sum of all eggs that had been parasitized
during her life (10 eggs offered at 2 d interval). The number of eggs eaten were recorded
on alternate days until the adult T asparagi survived.

The data was analyzed using analysis of variance (SAS Institute 1989) and the

means were compared with Fisher's protected LSD.

Results and discussion

Longevity.

The mean longevity of adults provided with egg + honey water was significantly
higher compared to longevity of adults provided with egg + asparagus flower or egg +
asparagus shoot (P< 0.05: F=8.08; df=3. 32) (Figure 1). Mean longevity of adult T
asparagi was higher in the treatment with asparagus beetle eggs + honey water (16.9
i189 d) compared to other food nutrients having beetle eggs or honey water alone (i.e.
ranged between 12.4 i 2.4 to 13.0 i 2.34 (1).

Adults provided with eggs + honey water lived 4 times as long as those fed with
asparagus flower or water. Asparagus flowers were not significantly better than water or
no food at all and the longevity was between (3.8 i 0.96 to 4.6 i 0.68 d). It is likely that
T. asparagi was not feeding on the nectar or pollen present in the asparagus flower. The
adults may not feed on the nectar or pollen although occasionally they walked over the

asparagus flowers.

89

 

ab

16
12

   
   

 

Longevity ((1 :5 SE)
on

eggs + honey water
honey water 1 .

Figure l: Longevity of T asparagi when fed on various food sources in

ab b
a ab

    
 

1161.11.11.11 l‘

   

   

IH-llllll 1.111111.

am... 11 '

    
 
   

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1111111.:

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a
O
O

.C
(0
U)
C
3
0
>5

4.
m
U)
U)
0

asparagus beetle eggs
eggs + asparagus flower

Food Sources

no food or water

asparagus flowers

the laboratory. Bars with same letters are not significantly different

(P>0.05, F=8.08, df=3. 32).

90

 

The nectar and pollen of asparagus flowers might have been inaccessible or
contain some repellent or toxic properties. Jervis et al. (1993) found that some parasitoids
ignored certain flower types whose nectar they cannot exploit due to the physically
l imiting factors, and some avoided due to the nutritional value, repellency. or the toxicity

of different nectars. Syme (1975) found that the parasitoids when given a choice of
‘flower species in the laboratory, has been found not to visit some nectar producing
species while readily visiting others. Avidor, Bashin, & Garson (1970) found that certain
aphid honeydews depressed longevity, possibly because of the harmful effects of some
Oligosaccharides.

Mouth part structure and body sizes are likely to be important factors limiting the
range of food sources (Jervis et al. 1993). T. asparagi does not have long elongated
mouth parts, unlike ichneumonids or braconids which have elongated mouth parts that
are used to exploit flowers with deep corollae and sugar rich nectars. In a study on the
longevity and fecundity of female D. insulare (Idris and Graflus 1995) correlated the
diameter of the corolla opening of various wild flowers with longevity and fecundity:
WidCl‘ flowers were more nutritive. They also found that the longevity and fecundity
varied with wildflower species.

Nutritional factors have been shown to be important in the longevity of T.
asparagi. The result also indicated that even without eggs, honey water alone provided
the necessary nutrients required for longevity. In this case, honey water was comparable

to the host food in providing the required nutrients for survival and longevity.

Purcell et al. (1996), Okeyo-owuor (1991), Hamerski & Hall (1988), van Lenteren

et al. (1987) indicated that host feeding and sugar solution extended the longevity of

9|

many parasitoids; host meals alone were not sufficient. This perhaps is the case with

T. asparagi, fed with eggs + honey water which increased longevity at least by 3 d
compared to eggs or honey water alone, although differences were not statistically
significant.

T. asparagi adults varied in size, in agreement with Capinera and Lilly (1975).

The larger adults lived longer than smaller ones. There was a possibility that later
emerged adults may live longer than the earlier emerging adults. This variation would
have been distributed across the treatments because the adults were randomly assigned to

all treatments.

Fecundity.

Probing by the adult T asparagi started within a few minutes of the first
introduction of eggs. The parasitoids walked around the asparagus fern while drumming
with the antennae. After the adult had selected an egg, it climbed on it and inserted her
ovipositor. The ovipositor moved up and down with a pumping motion. The pumping
motion lasted up to 31 min in the laboratory (personal observation). The detailed
sequences of ovipositional behavioral components have been described by Russel and
Johntson 1912 and van Alphen 1980).

Although T. asparagus used in this experiment were 1-3 (1 old, they had no prior
experience, but still started to probe the eggs immediately. Sometimes it was difficult to
ascertain whether the ovipositor insertion was merely to create holes for feeding or for
oviposition. T. asparagi deposits eggs inside the host eggs and monitoring actual egg
deposition was difficult. Some parasitoids leave ovipositional scar on the hosts. but that

left by T asparagi is hard to discern. Dissection of asparagus beetle eggs always

damaged the T. asparagi eggs and it was hard to determine the number of eggs deposited
by T asparagi on each asparagus beetle eggs. Egg feeding was the most frequently
observed event compared to oviposition. Generally host feeding or sucking continued
until the shell collapsed.

The number of eggs eaten was not significantly different between food sources. It
ranged from 2.5 to 2.7/48 h (Figure 2A). Eggs + honey water treatment had significantly
higher percentage of egg parasitism, compared to the other food sources (P< 0.05;
F=6.42: df=3. 176) (Figure ZB). The number of eggs parasitized was 0.7, 0.5. 0.2 and 0.2
in the eggs + honey water. eggs only, eggs + asparagus flowers and eggs + asparagus
shoots, respectively.

Numbers of adult T asparagi emergence was significantly higher in the egg +
honey water treatment compared to eggs + asparagus flowers and eggs + asparagus
shoots (P< 0.05; F=5.99; df=3, 176) (Figure 2C). There was no difference between egg +
honey water and eggs only. The analysis indicated that there was no interaction between
food sources and date, so I used one-way analysis to evaluate the reproductive rate with
time.

Egg feeding was the main impact of T asparagi on the common asparagus beetle.
4.3 eggs were eaten within 48 h of egg provision and the number eaten gradually
decreased as T asparagi aged (Figure 3A). Even though many eggs were presented
(n=10 per 48 h), rarely was more than one egg was used by the parasitoids during the first
48 h period to oviposit. The initial egg load within this synovegenic parasitoid, could
have resulted in higher fecundity that led to a higher number of adult parasitoid

emergence at the beginning (Figure 3B).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Figure 2: Number of eggs eaten (A), number of eggs parasitized (B) number of
adult T asparagi emerged per T asparagi with various nutrient sources in
laboratory. Bars with same letter are not significantly different (P> 0.05).

94

 

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Figure 3: Reproductive output per T. asparagi (i SE) at 48 h in the laboratory.
eggs eaten and fecundity per female (A), Adult emergence per female (B), and
ratio of eggs feeding versus oviposition per female (C).

95

 

The pattern of daily fecundity in T asparagi was similar to that found in most
insects: an initial high fecundity followed by a general decline with age (Figure 3A). On
average 2.9 adults emerged from an individual parasitized egg at the beginning and
gradually were reduced to 0.85 on the 6‘h day and later increased to 1.35 on the 8th day.
Individual parasitoids may attain high fecundity through high rates of host feeding at the
beginning and gradually drOp later. Van Lanteren et al. (1987) reported similar
observations on Encarsiaformosa (Gahan) (Hymenoptera: Aphelinidae). They also found
that the size or long life increased the fecundity. Being synovegenic, the adult needs to
continue to feed on the eggs for further oogenesis and egg development.

The daily ratio of host feeding versus oviposition was plotted (Figure 3 C).
Initially the adult consumed approximately 4 eggs per oviposition. As it become older.
they required more than 9 eggs per oviposition. Age is also an important factor in
determining fecundity. Even though the host feeding was very much reduced towards the
end, the honey water probably would have provided the extra nutrients required for
maintenance rather than reproduction.

Oviposition started immediately on the first day of egg provision. The pattern was
similar to that found by van Alphen (1980), where the newly emerged adult of T
asparagi immediately begin to oviposit, but at the same time it consumes 4.3 eggs/2 d.
Regression analysis showed, significantly no relationship between the amount of host
feeding and fecundity (r2 =0.09, F: 18.7, P=0.0001). Other studies have shown a
significant positive correlation between the amount of host feeding and fecundity

(Sugimoto & Ishii 1979, and Sahregard, Jervis & Kidd 1991).

96

The fecundity of T asparagi drastically dropped after 6 (1. According to (Leuis
1961a, 1967), fecundity was also critically dependent upon the age at which the female
was supplied with egg or haemolymph. Fecundity may be significantly reduced when
eggs of poor quality were supplied too late in life and for too brief a period.

Female fecundity seems to be closely related to body size and fitness (Murdoch et al.
1992). Adult sizes were not controlled in my study and could have affected the results of
individual female fecundity.

Egg resorption could be one of the reasons for poor fecundity among the adult
T asparagi. Jervis & Kidd (1986; and 1992a) explained that some synovegenic
parasitoids, especially host feeding species, are able to resorb eggs when hosts for

feeding are absent or scarce or of poor quality.

Conclusion

Nutrient availability and quality strongly influenced the longevity and fecundity
of T asparagi. Egg feeding in the presence of honey water extended the longevity and
increased the fecundity. The asparagus cut flower used in the study might not have
produced enough nectar or pollen that may had affected the T asparagi longevity. Egg
feeding was the main mortality factor compared to oviposition.

When considering the potential of T asparagi for biological control, there are
both advantages and disadvantages. The gregarious habit of this wasp and female biased
sex are positive features and these may contribute to the increased establishment rates
and shorter generation time. The potential disadvantage is that there is a relatively low

parasitism rate and short lifespan compared to other egg parasitoid (e.g. T gallerucae

97

 

female lived an average of 59 d when fed a 1:] water and honey mixture) Hamerski &

Hall (1988).

T asparagi longevity and fecundity can be improved in the asparagus agrosytem
by providing habitats that can provide nectar sources and a moderate microclimate for

effective management of the common asparagus beetle.

98

OVERALL CONCLUSION

Integrated pest management (1PM) or integrated crop management (ICM)
programs involves both crop management processes and ecological processes. Crop
management processes involve human intervention while ecological processes involve
interaction between pests, natural enemies and other components in the ecosystem. At
present human intervention in IPM systems. focuses on pest scouting to determine action
thresholds for pesticide application. The ecological processes, like resource sites, food,
shelter, favorable microclimate and favorable habitat for natural enemies have not been ...-
considered in the IPM programs, especially within the asparagus production system.

Commercial asparagus production is a relatively an intensive production system.
Prior to spear emergence, the vegetation from the previous season has to be destroyed by
mowing or applying pre-post emergence herbicides. The harvesting of spears is done at
1-2 d interval and lasts for about 40 d. Asparagus spears have to be protected from
feeding and laying eggs by the common asparagus beetle. The frequent disturbance by
the harvesting of spears makes the implementation of the ecological processes a real
challenge in this crop. A survey done by USDA (C onejo et al. 1992) indicated that
asparagus growers in Michigan adopted IPM practices for controlling pests in asparagus
field. The routine scouting and determining the economic threshold before initiating
insecticidal spraying is the only activity being carried out. If the pest population is below
economic threshold, then it is generally assumed that the natural enemies are effectively
controlling them.

The results of my study showed that IPM approach is a workable option with

some modification. The standard practice of blanket application of carbaryl dust at

99

beginning of the spring season did not provide effective control of the common asparagus
beetle at the spear stage. About 30-3 5% of the spears were damaged through feeding by
the adult asparagus beetles in all plots. The reliance on existing T asparagi and the use of
economic action threshold to control the beetles did not differ from the untreated plots.
The beetles were overdispersed thus the action threshold would not have been an accurate
estimate and poor control of beetle might have occurred in the IPM plots.

Consequently, the application of carbaryl dust could have an impact on the initial
emergence and continued survival of T asparagi. The adult T asparagi overwinters in
the soil debris as an adult. The dust formulation would have an impact on the parasitoid
because the dust forms a thin layer on the surface of soil and may be toxic to the newly
emerging adults.

Both field and laboratory studies indicated that the commonly used insecticides
(carbaryl, chlorpyrifos and malathion) caused 100% mortality to T asparagi, the
common asparagus beetle and larvae. Even though permethrin showed slow poisoning, it
caused 100% mortality to T asparagi after 24 h exposure to foliar residues.
Chlorothalonil was also found to be toxic to T asparagi and caused 20-60% mortality.
(Idris & Grafius 1993 a, b) indicated that chlorothalonil was not toxic to D. insulare. a
larval parasitoid of diamondback moth. In this case, T asparagi may be more sensitive to
fungicides residues. Of all the insecticides tested, malathion was most toxic to the larvae
of the common asparagus beetle although all insecticides caused 100% mortality after 24
h exposure. The parasitized larvae produced life adults of T asparagi when exposed to

foliar residues of both permethrin and chlorothalonil.

100

 

Parasitism by T asparagi was highly variable depending on the type of crop
management practices carried out by the growers. In 1997, parasitism was 1.1% in
commercial farmers' field and 1.2% in the experimental plots in Oceana county . The
average parasitism was 50.9% in MSU Collin Road, Entomology Research Farm where
no insecticides were used. In 1998, parasitism in the commercial farmer's field was 1.1%
and 18.7% in the organic farmer's field in Oceana County. In MSU Research Farms. the
average parasitism was 15.2%. The eggs collected from insecticides (carbaryl and
chlorpyrifos) treated plots showed no parasitism at all while permethrin and untreated
plots had 1.4% and 6.3% respectively.

The difference in parasitism between the commercial farms and organic farms
may be due to the impact of pesticides on T asparagi. The zero parasitism in the eggs
collected from the insecticides treated plots indicates that T asparagi was very
susceptible to pesticide treatments or that the insecticide residues would have killed the
developing embryos.

The phenology from egg laying by the common asparagus beetle to oviposition by
T asparagi, is considered a crucial period. T asparagi has a very narrow window for
oviposition to occur. The preferred stage of eggs for host feeding is 1 d old or less and for
oviposition is 2-3 (1 old. After 3 d, the eggs will hatch. T. asparagi has a narrow window
of between 24 to 48 hours to oviposit. The opportunity cost here is to feed or oviposit.
According to Johnston (1915), T asparagi preferred to host feed than oviposit. Thus, we
can anticipate a lower recoupment rate for next generation. If pesticides were applied at
this critical period, it will further reduce the existing parasitoid populations and delay the

development in the next generation. In such a critical situation, insecticide application is

101

totally incompatible in conserving the existing T asparagi population.

The field studies also indicated that the presence of volunteer ferns in the inter-
rows of the asparagus plant became the host for the beetle and T asparagi. As harvesting
progressed, apparently the constant removal of spears created habitat instability thus
encouraging more and more beetles to lay eggs in the fern. The number of eggs found in
the volunteer fern ranges from 3 to 18. This food resource attracted the adult T asparagi
and it continued to feed on them. This is in accordance with the 'resource concentration
hypothesis' where the specialist insect herbivores are abundant when food resources are
concentrated (Root 1973). Sheehan (1986) also emphasized that specialist parasitoids
may be more likely to find, or less likely to leave, concentrated patches of their prey's
food. Numerous beetle eggs were found to have collapsed within the volunteer ferns.
indicating T asparagi feeding. One can determine the difference between the host
feeding and larval emergence from the eggs. Host feeding will cause the eggs to be
completely shriveled while larval emergence will have exit holes and the eggs will still be
in oval shape. T asparagi were abundant and at times as many as 5—6 adults were present
in a single volunteer fern. The volunteer ferns were about 10-12 cm in height and
sporadic would cause a minimal impact to the production of asparagus spears or soil
fertility. But the stable habitat provided by the volunteer ferns will greatly benefit the T
asparagi survival and conservation of this parasitoid.

Studies in the laboratory indicated that T asparagi requires nectar sources
for increasing the longevity and fecundity. The longevity was increased four fold when
T asparagi was fed with host eggs and honey water compared to asparagus flower alone.

The longevity was increased by 3 d when T asparagi was provided with host eggs and

102

honey water compared to host eggs alone. The fecundity of T asparagi was also
increased when honey water was provided. Maybe, the asparagus cut flowers did not
have had produced enough nectar or pollen for the parasitoid to feed on and survive.

In an IPM system, we can incorporate other steps to reduce the impact of
pesticides on the parasitoids. The blanket application of carbaryl dust is more harmful
than beneficial. Relatively safer insecticides such as pyrethroids (i.e., deltamethrin) can
be used to control the common asparagus beetles. To reduce the impact of pesticides, the
application should be carried out late in the evening. T asparagi adults were more
abundant from 10.00 AM to 2.00 PM. Volunteer ferns should be allowed to grow as early
in the season as possible and maintained until main crop fern establishment. This will
provide a substitute host for the beetle and T. asparagi. During the fern stage, pesticides
could be applied on alternate rows rather than as a blanket spray. Nectar producing
plants or weeds could be encouraged within the hedge of the asparagus fields.

Further studies on the T asparagi behavior in the field should be investigated.
The use of volunteer ferns as a hedge plant may be useful in the conservation of this
parasitoid. The influence of diurnal factors affecting the behavior should also be
investigated in detail. The analysis of chemical composition of asparagus plants will help
to understand the behavior of T. asparagi.

To start with, our concept of asparagus growing systems should be expanded to
include the volunteer ferns within the cropping system so as to improve the present IPM

system.

 

APPENDIX

1 ()4

APPENDIX 1

Record of Deposition of Voucher Specimen*

The specimens listed on the following sheet(s) have been deposited in the named
museum (3) 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.

Title of thesis or dissertation (or other research projects);

Bionomics, parasitism and impact of pesticides on Tetrastichus asparagi Crawford
(Hymenoptera: Eulophidae): an egg parasitoid of the common asparagus beetle Crioceris
asparagi L. (Coleoptera: Chrysomelidae)

Museum (3) where deposited and abbreviations for table on following sheets:

Entomology Museum. Michigan State University (MSU)

Other Museums:

lnvestigator's Name (5) (typed)

Palasubemiam Kaliannan

 

 

 

Date 21 December 1998

 

*Reference: Yoshimoto, C. M. 1978. Voucher Specimens for Entomology in North
America. Bull. Entomol. Soc. Amer. 242141-42.

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 (3) files.

Research project files.

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

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Voucher Specimen Data

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106

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