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This is to certify that the

thesis entitled

Increasing biological control of onion maggot,
Delia antiqua (meigen), with integrative
management control methods and approaches

presented by

Brian P. McCornack

has been accepted towards fulﬁllment
of the requirements for

M. S . degree in Entomology

 

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To AVOID FINES return on or before date due.
MAY BE RECALLED with earlier due date if requested.

 

DATE DUE

DATE DUE

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6/01 c:/ClFlC/DateDue.p65-p.15

—‘

INCREASING BIOLOGICAL CONTROL OF ONION MAGGOT,
DELIA ANTIQUA (MEIGEN), WITH INTEGRATIVE MANAGEMENT
CONTROL METHODS AND APPROACHES
By

Brian P. McComack

A THESIS

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

MASTER OF SCIENCE
Department of Entomology

2002

ABSTRACT

INCREASING BIOLOGICAL CONTROL OF ONION MAGGOT
(DELIA ANTIQUA (MEIGEN)) WITH INTEGRATIVE MANAGEMENT
CONTROL METHODS AND APPROACHES

By

Brian P. McComack

Onion maggot, Delia antiqua (Meigen), is the most economically important pest in
Michigan onions, Allium cepa L. In years of severe outbreak it can cause a 40-80%
reduction in yield. Management options for this pest includes a heavy reliance on a broad
spectrum insecticide, chlorpyn'fos, for effective control. The goal of this research is to
determine the potential for integrating the insect growth regulator cyromazine with modiﬁed
cultural practices to conserve biological control agents and enhance the Integrated Crop

Management program for onions in Michigan. My objectives were to: I) examine carabid
beetle predation of onions maggot larvae and pupae using greenhouse and laboratory studies,
2) determine the effects of refuge habitats on carabid communities in Michigan onions, and
3) evaluate the combination of cyromazine and refuge strips in onions as a new tool for
management of onion maggot. In greenhouse and laboratory studies, several carabid beetle
species consumed onion maggot pupae and larvae in no-choice bioassays. Signiﬁcant
differences in the number of pupae recovered depending on pupae depth and the predator
species tested was observed. Larvae consumption/disappearance ranged ﬁom 47-5 7% in the
greenhouse study, however, there were no signiﬁcant differences observed. The presence of a
refuge strip signiﬁcantly increased the number of beetles captured in the adjacent onion crop
habitat. Differences at the species level was also observed. Integrating multiple aspects of
onion maggot control (i.e. biological, cultural, and chemical) will provide a more efﬁcient

and sustainable approach to managing onion maggot populations in Michigan onions.

“To forget how to dig the earth and
tend soil is to forget ourselves.”

-Gandhi

iii

ACKNOWLEDGMENTS

I would like to thank Ed Graﬁus, Maria Davis, Doug Landis, and Richard Harwood
for their support, encouragement, ideas, and entomological wisdom during my studies at
Michigan State University. Their inspiration and attention to detail has taught me a great
deal about the scientiﬁc process and the criteria needed for quality research. Their belief in
my skills, creativity, desires, and passion has been a tremedous gift in my entomological
adventure. This research could not have been done without the help of the vegetable
entomology lab and its members: Beth Bishop, Walter Pett B.D.E. (Best Dressed
Entomologist), Adam Byme, Mike Najara, Nick Bramble, and its various student workers.
The person who was literally at my side during my entire research program was Emmalyn
Partlow. She was a trememdous asset to this project and I will be forever thankful!

I would like to extend a thank you to Ron Gnagey, the Michigan State University
Muck Soils Research Farm manager, for all his hard work, his willingness to help, and his
ﬁeld experience. Many thanks to Stan VanSingel and Bruce and Wayne Kielen.

I wouldn’t be here today if it wasn’t for my families. The love and support of my
parents, brothers and sisters, their conﬁdence in the choices I’ve made as a person, and the
values they possess make them truly incredible human beings. I want to thank the person
who has given me the most support in this venture, my wife, Heather. She deﬁnes beauty,
compassion, and love. I am forever greatful!

I came to Michigan to become an entomologist, and I left with so much more. Life is
an incredible journey, an amazing dance, and a beautiful chance to rediscover. The support

and community I discovered in Nia will be with me always. Thank you Ms. Winalee.

iv

TABLE OF CONTENTS -

LIST OF TABLES ................................................................................................................. vii
LIST OF FIGURES ................................................................................................................. ix
CHAPTER 1: INTRODUCTION ........................................................................................... 1
Onion Production ......................................................................................................... 1

Onion Pests ................................................................................................................... 2

Onion Maggot .............................................................................................................. 3
Distribution ...................................................................................................... 3

Life History ...................................................................................................... 3

Mating .............................................................................................................. 6

Host plants ....................................................................................................... 8
Host selection and host quality ......................................................................... 9

Control Strategies ....................................................................................................... 13
Chemical Control Methods ............................................................................ l4

Biological Control ......................................................................................... 15

Carabids ..................................................................................................................... 16
Conservation Biological Control ............................................................................... 18

CHAPTER 2: CARABIDAE PREDATION ON ONION MAGGOT,
DELIA ANYYQUA (DIPTERA: ANTHOMYIIDAE), LARVAE

AND PUPAE IN THE GREENHOUSE AND LABORATORY .......................................... 26
Abstract ...................................................................................................................... 26
Introduction ................................................................................................................ 27
Materials and Methods ............................................................................................... 29

No-choice predator bioassays ........................................................................ 29
Greenhouse and laboratory experiments ........................................................ 30
Results and Discussion ............................................................................................... 32
No-choice predator bioassays ........................................................................ 32
Greenhouse and laboratory experiments ....................................................... 33

CHAPTER 3: GRASSY REFUGE STRIPS AND A NARROW
SPECTRUM INSECTICIDE (CYROMAZINE) CONSERVE
GROUND BEETLE (COLEOPTERA: CARABIDAE) POPULATIONS

IN MICHIGAN ONIONS ...................................................................................................... 42
Abstract ...................................................................................................................... 42
Introduction ................................................................................................................ 43
Materials and Methods ............................................................................................... 45

1999 ﬁeld study ............................................................................................. 45
Established grassy refuges within an onion ﬁeld .......................................... 46
Results and Discussion .............................................................................................. 49

1999 ﬁeld study ............................................................................................. 49

Established grassy refuges within an onion ﬁeld ........................................... 50
CONCLUSIONS .................................................................................................................. 109
LITERATURE CITED ........................................................................................................ l 1 1
APPENDIX 1 ...................................................................................................................... 123

LIST OF TABLES

Table 1. Mean number of onion maggot larvae consumed per day ! S.E. by various carabid
species captured in commercial onion ﬁelds.

Table 2. Mean number of onion maggot pupae consumed per day ! S.E. by various carabid
species captured in commercial onion ﬁelds.

Table 3. Analysis of variance for activity-densities of common carabid species captured in
enclosure plots at the Michigan State University Muck Soils Research Farm, Clinton County
MI in 1999. Tests for enclosure effects on carabid activity-densities are shown.

Table 4. Carabid species captured during the 2000 (30 May-18 September) and 2001 (6
J une- l 7 September) trapping periods at the Michigan State University Muck Soils Research
Farm, Clinton County MI. {

Table 5. Analysis of variance for traps catches within the entire plot at the MSU Muck Soils
Research Farm, Clinton Co MI in 2000.

Table 6. Analysis of variance for trap catches within the crop areas adjacent to refuge or
control strips at the MSU Muck Soils Research Farm, Clinton Co MI in 2000.

Table 7. Analysis of variance for traps within reﬁrge or control strips at the MSU Muck
Soils Research Farm, Clinton Co MI in 2000.

Table 8. Per trap analysis of variance for activity-densities of common carabid species
captured in 2000. Tests for refuge effects on carabid activity—densities within refuge or
control strips, within the adjacent crop area, or the entire system is shown.

Table 9. Analysis of variance for traps catches within the entire plot at the MSU Muck Soils
Research Farm, Clinton Co MI in 2001.

Table 10. Analysis of variance for trap catches within the crop areas adjacent to refuge or
control strips at the MSU Muck Soils Research F arm, Clinton Co MI in 2001.

Table 11. Analysis of variance for traps within refuge or control strips at the MSU Muck
Soils Research Farm, Clinton Co MI in 2001.

Table 12. Analysis of variance for activity-densities of common carabid species captured in
refuge and insecticide treated plots in 2001. Tests for reﬁJge, insecticide, and
reﬁrgeﬁnsecticide effects on carabid activity-densities within refuge or control strips, within
the adjacent crop area, or the entire system are shown.

Table 13.Effects of refuge treatment and insecticide on seasonal mean carabids/trap in 2001.

vii

Table 14 . Mean number of species captured per plot within the refuge or control strip,
within the adjacent crop area, or within the entire system ! SE. in 2001. Means for refuge,
insecticide, and interaction between re fuge“insecticide are shown.

Table 15 . Shannon Weaver indices (H’) for diversity of species captured per plot within the
refuge or control strip, within the adjacent crop area, or within the entire system ! SE. in

2001. Means for refuge, insecticide, and interaction between refuge*insecticide are shown.

Table 16. Analysis of variance of onion harvest weights and number of onions 3 in 2001.
Tests for refuge, insecticide, and reﬁrge*insecticide effects are shown.

viii

LIST OF FIGURES

Figure l. Arena design for pupal predation by carabids, Pterostichus melanarius and
Poecilus Iucublandis. One 1 liter plastic cup (1 1.5 cm diameter, 14 cm height) was inverted
on top of another 1 liter plastic cup. The top cup had 2 sections (8 x 8 cm) removed and
replaced with screen mesh (mesh size = 1 x 1 mm).

Figure 2. Correlation between mean number of onion maggot pupae consumed by A)
Poecilus lucublandis and B) Pterostichus melanarius at varying depths (0 cm,
1 cm, 4 cm, or 8 cm).

Figure 3. Carabid beetle activity-density for the species Poecilus chalcites, Poecilus
lucublandis, and Pterostichus melanarius at the Michigan State University Muck Soils
Research Farm, Clinton County MI in 2000.

Figure 4. Plot layout for evaluating the effects of a grassy ﬁeld edge on carabid beetle
populations in 1999 at the MSU Muck Soils Research Farm in Clinton County, MI. A) Full-
enclosure plot, B) partial-enclosure plot, and C) a grassy ﬁeld edge.

Figure 5. Plot layout for evaluating the effects of newly established refuge strips on carabid
beetle populations at the MSU Muck Soils Research Farm in Clinton County, MI in 2000.

Figure 6. Generalized plot layout of one block for evaluating the effects of established
refuge strips, insecticide treatments (A-untreated, B-cyromazine, and C-chlorpyrifos) and
interaction between refuge and insecticide on carabid beetle populations at the MSU Muck
Soils Research Farm, Clinton County MI in 2001. Pitfall traps were used to monitor beetle
activity-densities.

Figure 7. Grassy ﬁeld border effects on all carabids captured within an onion ﬁeld in 1999.
Mean number of carabids captured during the trapping period are shown. Means with a
different letter are signiﬁcantly different: Fisher’s protected LSD test, (P<0.05).

Figure 8. Grassy ﬁeld border effects on trap catch of common carabid species within an
onion ﬁeld in 1999. Mean number of carabids captured during the trapping period are
shown. Means within a species followed by a different letter are signiﬁcantly different:
Fisher’s protected LSD test, (P<0.05).

Figure 9. Seasonal activity-density for all carabid beetles captured per trap during the 2000
ﬁeld season. * Means within a pitfall trap location are statistically signiﬁcant: Fisher’s
protected LSD test, (P<0.05).

Figure 10. Grassy refuge effects on carabid activity-densities of common carabid species
captured within an onion ﬁeld in 2000. Mean number of carabids captured within a location
are shown: A) within the crop area, B) within the refuge strip or onion control strip, and C)

within the entire plot. *Means within a species are statistically signiﬁcant: Fisher’s protected
LSD test, (P<0.05).

Figure 11. Grassy refuge effects on activity-densities of carabids captured throughout the
2000 trapping period (30 May- 18 September) within an onion ﬁeld. Mean number of
carabids captured per plot ! SE: A) Within adjacent crop area, B) Within the 3.6 m wide
grassy refuge strip or onion control strip, and C) Within the entire system. *Means within a
trapping period are statistically signiﬁcant: F isher’s protected LSD test, (P<0.05).

Figure 12. Seasonal mean carabid beetles per trap captured during 2001. A) Effect of
refuge strip habitats (*means within a location are statistically signiﬁcant: Fisher’s protected
LSD test, P<0.05), and B) insecticide treatments on carabid beetles captured in the total plot,
within the crop areas, and within the refuge strips (different letters denote signiﬁcant differ-
ences within a location, Fisher’s LSD tests, P<0.05). ns=no signiﬁcant differences.

Figure 13. Grassy refuge effects on activity-densities of common carabid species captured
within an onion ﬁeld in 2001. Mean number of carabids captured per location are shown:
A) within adjacent crop area, B) within refuge or onion control strips, and C) within the
entire plot. *Means within a species are statistically signiﬁcant: Fisher’s protected LSD test,
(P<0.05).

Figure 14. Grassy refuge effects on activity—densities of all carabids captured throughout the
2001 trapping period (6 June - 17 September). Mean number of carabids captured per trap
date: A) within adjacent crop area, B) within the refuge or onion control strips, and C)
within the entire plot. *Means within a trapping period are statistically signiﬁcant: Fisher’s
protected LSD test, (P<0.05).

Figure 15. Insecticide effects on activity-densities of common carabid species captured
within an onion ﬁeld in 2001. Mean number of carabids captured per location are shown:
A) within adjacent crop area, B) within reﬁrge or onion control strips, and C) within the
entire plot. Different letters within a species denote signiﬁcant differences using Fisher’s
protected LSD tests, P<0.05. ns = no signiﬁcant differences.

Figure 16. Insecticide effects on on activity-densities of all carabids captured throughout the
2001 trapping period (6 June - 17 September). Mean number of carabids captured per trap
date: A) within adjacent crop area, B) within the refuge or onion control strips, and C)
within the entire plot. *Means within a trapping period are statistically signiﬁcant: Fisher’s
protected LSD test, (P<0.05).

Figure 17. Mean number of Bembidion quadrimaculatum L. captured within the refuge
strip or onion control strip during the 2001 ﬁeld season. *Means within a trap date are
statistically signiﬁcant: Fisher’s protected LSD test, (P<0.05).

Figure 18. Mean number of Pterostichus melanarius (111.) captured within the entire plot
affected by the presence of refuge or onion control strip during the 2001 ﬁeld season.
*Means within a trap date are statistically signiﬁcant: Fisher’s protected LSD test, (P<0.05).

Figure 19. Grassy refuge or control strip effects on onion yield in 2001. A) Number of
onions and B) harvest weight. *Mean onion weights are signiﬁcantly different: Fisher’s
protected LSD test (P<0.05).

Figure 20. Insecticide treatment effects on onion yield in 2001. A) Number of onions and
B) harvest weight. *Mean onion weights with different letters are signiﬁcantly different:
Fisher’s protected LSD test (P<0.05).

CHAPTER 1:

INTRODUCTION

ONION PRODUCTION

Onions, Allium cepa L., is a biennial usually planted as seeds by commercial
growers (Jones and Mann 1963). Onions are thought to be among the ﬁrst plants to be
cultivated by early humans. Garlic, Allium sativum L., is a closely related species and was
heavily used in ancient times for its pungent ﬂavor and medicinal properties. There are
many onion cultivars in production today varies in characteristics such as day-length
requirement, skin color (white, brown, yellow, red, or purple), size (3-15 cm diameter),
shape (globe-shaped, ﬂattened or spindle-shaped), and pungency and sweetness. The
variety and the chemical characteristics of the soil where they are grown mainly
determine the expression of pungency and sweetness.

Typical onion production in Michigan takes place on high organic (muck) soils
that contain sufﬁcient nutrients for bulb production. Planting in Michigan begins in mid
to late April and ends in early May. Harvest usually begins in early September and ends
in mid to late October. Most production of onions in the northeastern United States
occurs in New York and Michigan, and in the United States, approximately 70,000 ha of
onions are harvested each year (NASS 2000). In 1999, Michigan growers harvested 1619

ha of dry bulb onions with a production value of $10.8 million (NASS 2000).

ONION PESTS

There are major and minor insect pests that affect onions. Major pests include the
onion thrips, Thrips tabaci L. and onion maggot, Delia antiqua (Meigen). Onion thrips
feed on newly emerged leaves by damaging leaf cells with their rasping mouthparts and
feeding on the sap released at the point of injury. If thrips populations become high
enough, girdling occurs and severe leaf damage causes the leaf to die. Heavy infestation
of onion thrips can kill seedlings early in the growing season and can reduce yields and
bulb quality (Hoffman et al. 1996). Few control methods are available for control of
onion thrips. Physical factors such as heavy rains can wash out thrips populations in neck
of the onion plant. Growers rely heavily on chemical control strategies for management
of this pest. Other minor pests include Western ﬂower thrips (F rankliniella occidentalis
(Pergande)), cutworrns, aster leaﬂiopper (Macrosteles quadrilineatus Forbes), mites and
several species of aphids (Hoffman et el. 1996).

The second major pest of onions and perhaps the most important is the onion
maggot. It is the most serious and economically signiﬁcant pest of onions in Michigan
and much of the northeastern US. and Canada (McEwen et a1. 1981, Ellis and Eckenrode
1979, Wells and Guyer 1966). Onion maggot is a specialist herbivore on onions (Ellis
and Eckenrode 1979b) and a few other minor Allium species. Michigan has three distinct
onion maggot generations each season, with the initial spring emergence of adults
occurring in late April or early May (Eckenrode et al. 1975, Loosjes 1976). First
generation larvae are usually considered to have the most impact economically, because

the onion plant is in its most vulnerable stage (Miller and Cowles 1990). Small onion

seedlings cannot withstand heavy feeding by onion maggot due to extensive vascular
tissue damage. A single maggot can destroy as many as 12-15 seedlings before pupating
(Loosj es 1976); onion maggot has the potential of causing a 40-80% reduction in yield
without proper chemical or cultural control strategies (Zandstra et al. 1996).

ONION MAGGOT

Distribution. Because the onion maggot is such a major pest in commercial
onions, its geographic distribution has been reviewed extensively. Onion maggot is
mainly limited to the northern latitudes (3 5-60° N) in the temperate zone of the Holarctic
region (Finch 1989, Hill 1987). The onion maggot was originally a palaearctic species
but was introduced into eastern North America during the early 1800’s in cargos of
onions. From its original point of introduction it spread to the western region of the
United States and Canada (Loosjes 1976). A general compilation of information was
supplied by Scott (1969) after the original description of onion maggot in the late 18205.
Loosj es (1976) also went on to describe the geographical distribution of the onion
maggot by mapping general occurrence and local observations cited in annual reviews
and bulletins.

Life history. The onion maggot has six distinct stages in its life-cycle: egg, 3
larval instars, pupa, and adult. Onion maggots overwinter as pupae. Initial spring adult
emergence occurs approximately after an accumulation of 200 degree-days above a base
temperature of 4.4°C (Eckenrode et a1. 1975). A temperature-dependent preoviposition
period of 103 degree-days, base 44°C, is required. Gravid females deposit their eggs at

bases of onion stems or leaf axils of onion plants. Newly deposited eggs require 50

degree-days, base 388°C, before eclosion (Carruthers 1979). Newly hatched larvae feed
on the roots and the developing onion bulb. As feeding progresses, secondary invasion of
soft-rot organisms occurs and this plus direct damage of plant tissue quickly produces
physical evidence of plant stress (Doane 1953).

Onion maggot has three distinct larval stages. First, second and third larval instars
complete development in 37, 89, and 161 degree days (base 4.4°C), respectively
(Carruthers 1979). Following the completion of the third instar, the larva exits the onion
plant and burrows into the soil. Pupal depths range ﬁ'om 4 to 15 cm below the surface of
the soil (Carruthers 1979, Rygg 1960, Loosjes 1976). Whitﬁeld et al. (1986) reported
survival of overwintering pupae was not dependent on pupal depth or habitat, and
suggested moisture and temperature were the critical factors.

Male onion ﬂies oﬁen emerge a few days earlier than the females (Rygg 1960),
and this emergence is reported to coincide with the ﬂowering of dandelions in early
spring (Baker 1925). This may give males a competitive edge in discovering newly
emerged unmated females. Male insects oﬁen develop more rapidly or at lower
developmental thresholds to accommodate for this early emergence (Price 1997). After a
3-4 d post-eclosion period (McDonald and Borden 1995), copulation occurs and the life-
cycle continues.

Univoltine and multivoltine insect populations are highly dependent on many
biotic and abiotic factors, but the major abiotic stimuli determining the number of onion
maggot generations per year is temperature. Onion maggot is typically a multivoltine

species averaging 3-4 generations per year depending on seasonal temperature ranges

(Loosjes 1976). Southwestern France has as many as 5 generations per year (Loosjes
1976). In places with low seasonal degree-day accumulations such as northern Norway,
onion ﬂy populations are univoltine (Rygg 1960). The ﬁnal generation in multivoltine
populations are incomplete and pupae from these generations go into a facultative
diapause (Loosjes 1976).

Diapause induction seems to be strongly age dependent in the onion maggot and
the third instars of the late season generation usually undergo diapause. Short day length
in combination with low temperatures during the third instar induces diapause
(Drummond 1982). There is a low percentage of diapause at longer day lengths, if the
temperature is < 18°C, and a high percentage diapause at shorter day lengths even if the
temperature is high (Loosj es 1976). The correct balance of temperature and daylength is
needed to stimulate or inhibit onion maggot diapause.

Photoperiod also inﬂuences ﬂight activity. When the photoperiod is longer than 8
h, diurnal adult onion maggot exhibit a major peak of activity in the evening (W atari and
Arai 1997). Finch et al. (1986) showed that adult onion ﬂies spend most of the day
resting in shaded habitats provided by surrounding foliage and avoid the onion crop. The
late afternoon/evening peak in ﬂight activity is mainly females searching for suitable
ovipositional sites (Havukkala and Miller 1987). Results from a study by Watari and Arai
(1997) shows most of the egg deposition occurs after 10-12 h of light and suggests that
this major peak in activity is controlled by a circadian pacemaker. They defended their
hypothesis by shifting the grth chamber photoperiod and found egg-laying coincided

with the photoperiod of the chamber.

A post-eclosion interval of several days is oﬁen required by many Diptera before
mating. There are considerable biotic and abiotic factors that determine this post-eclosion
interval and the interactions are complex in nature. Usually, this time delay for both sexes
is dependent on meeting physiological criteria for processes such as oogensis and
accessory gland maturation (Chen 1984). Having female spermatozoa present in the
female reproductive tract often will inhibit sexual receptivity for both sexes (Adams and
Hintz, 1969). The time of occurrence is usually correlated with distinct stages in the
morphological development of the ovaries (McDonald and Borden 1995). The post-
eclosion interval lasts for 1-2 wks and as the adults age, mating begins (Loosjes 1976).
This usually occurs after dispersal to suitable host plants and ovariole maturation (Judd
and Borden 1988). Research by McDonald and Borden (1995) does not support the
hypothesis that mating occurs only in the presence of mature ovarioles. However, they
showed a strong age to sexual receptivity correlation. Age of the female onion maggot
adult had a strong effect on its probability of being fertilized (McDonald'and Borden
1995), and no adults of either sex mated before 3 d of age.

Mating. Mate location and acceptance is an important aspect to the mating
biology of many insect species. The ability of one species to recognize a conspeciﬁc and
the sex of a conspeciﬁc is important in producing future generations. A well-studied
phenomenon in onion maggot is their courtship behavior. McDonald and Borden (1996)
categorized seven courtship behaviors expressed by onion maggot adults: inspection from
the substrate, aerial inspection, contact from the substrate, contact from the air, genital

alignment, copulation, and male-male interaction. The sequence of events that make up

this unique mating behavior relies primarily on indiscriminate visual recognition of
potential mates. This is then followed by a detection of semiochemicals that inform the
receiver of species-speciﬁc and sex-speciﬁc information. Elements such as genital
alignment and attempted copulation illustrates this ability by males to discriminate
between sexes, sexually immature and mature females, and between other species
(McDonald and Borden 1996).

When a male creates a species-speciﬁc proﬁle by detecting unique cuticular
hydrocarbons, this activity might also function as a reproductive isolation mechanism
(Blomquist et al. 1987). The speciﬁcity of this so-called cuticular hydrocarbon
“blueprint” increases qualitatively and quantitatively in conjunction with female age
(Blomquist et al. 1987). This could ultimately reduce the time spent searching or
copulating with unsuitable mates and increase the amount of time spent searching for
more suitable female onion maggot adults.

The amount of time spent copulating may also have an affect on the reproductive
success of onion maggot. Insemination may ultimately be effected by the male’s ability
to grasp and remain in copulo. This could impart some competitive advantage to the
most-ﬁt males. On the other hand, females may also beneﬁt from shorter copulation
events by being able to mate with several males. It is unclear, however, which sex ends a
copulation event, thus making it difﬁcult to assess which sex is receiving the competitive
advantage. Regardless, McDonald and Borden (1996) showed copulation duration in

onion maggot to be brief and highly variable.

Female reproductive behavior is affected by extracts from mature male
reproductive tracts. Spencer et a1. (1995) illustrated this in the lab. Purely virgin females
receiving a fraction of an equivalent male extract remained “unmated in the presence of
males and began laying unfertilized eggs at a normally mated rate.” When such extracts
are transferred to the female aﬁer copulation, these sex peptides are believed to act as
mate-guarding substances (Miller et a1. 1994). Male extracts appear to be a potent
behavioral modiﬁer and may have permanent effects on the behavior of sexually mature
females (Spencer et al. 1995). This sexual adaptation seems to be an advantage for the
male onion ﬂy in helping reduce sperm competition with other males when fertilizing
eggs.

Host plants. Perhaps the most important biotic factor inﬂuencing onion maggot
distribution and population dynamics is its host plant. Onion maggot attacks only Allium
species and the onion is the preferred host (Ellis et al. 1979). Other species attacked by
onion maggot include Allium ascolonicum L. (shallot), Allium sativum L. (garlic), and
Allium schoenoprasum L. (chives) (Ellis and Eckenrode 1979b). The presence of onion
maggot is in direct correlation with areas of high onion production and there is no
important wild host for the onion maggot in Michigan or for other onion maggot
populations across the United States. This is perhaps the most important factor limiting
onion maggot distribution.

The temporal occurrence of host plants in a particular habitat also inﬂuences
onion maggot populations. A well-accepted method of protecting crops against Delia

species is to vary planting times. This helps to reduce migrant ﬂies from entering the ﬁeld

or to reduce crop susceptibility to female onion ﬂies during peak egg-laying (Coaker
1987). Onion seedlings that sprout early are at a greater disadvantage, which could select
for late-germinating Allium plant species. Late planting is a management option, although
it may cause lower yields due to possible host dry conditions during germination and less
time to reach maturity.

Allium species including A. cepa contain unusually high amounts of organic
sulfur. This sulfur takes the form of alkylcesteine sulfoxides and gamma-glutamyl
peptides (Miller and Harris 1985). Chemicals such as n-propyl disulﬁde and n-propyl
mercaptan are effective attraction and oviposition stimulates for adult onion maggots
(Matsumoto 1970) and these chemicals are unique to Allium plant species.

Host selection and host quality. Insects use many physical and chemical cues to
select the best suitable host for oviposition and food allocation. Because chemical cues
are important for plant-herbivore interactions, adult onion maggots use these cues to
detect the most suitable hosts. Selecting a suitable host for oviposition often involves the
use of behavioral sequences triggered by a particular stimulus (Shorey 1977). Chemical
stimuli, such as the n—propyl disulﬁde compound found in Allium species, can often
trigger female ovipositional behavior repertoires. For example, a typical ovipositional
sequence or repertoire includes running up and down leaf surfaces, sitting, grooming,
extension of the proboscis so the labellum contacted leaf and soil surfaces, movements of
the tip of the abdomen over surfaces (surface probing), subsurface probing of soil

crevices with the ovipositor, and ﬁnally oviposition (Harris and Miller 1991).

Long-range host orientation is also dependent on chemical cues. However,
interpreting the inﬂuence of host odors on long-range host location in the ﬁeld can be
complicated. Local weather variations (Vernon et al. 1981), compositional changes in
odors over time (Miller et al. 1984), host and non-host olfactory interference (Vernon and
Borden 1983), and variability in onion maggot populations (Martinson et al. 1989) can all
inﬂuence the success of onion maggot in ﬁnding a suitable host. In the ﬁeld, females
searching for ovipositional sites are strongly attracted to decomposing onions (Dindonis
and Miller 1980).

Tactile stimuli also play a role in ﬁnding suitable host plants. When a young
onion seedling is blown by the wind, the stem of the small plant creates a space between
the soil and the base of the stem. The length and depth of this space is an important
ovipositional stimulus for females. Mowry et a1. (1989) found that onion maggot females
oviposite most eggs in holes >4 mm deep and 0.6 mm diam. Not only was length and
depth important, but the preferences in substrate quality was also stressed. Penetrability
of the substrate rather than particle size was the dominant factor when selecting
ovipositional substrates (Mowry et al. 1989). Soil type can potentially inﬂuence the
distribution of this economically important pest species.

Other host cues used by the onion maggot in locating a suitable host plant are
visual. Leaf shape, color, hue, and brightness inﬂuence the attractiveness of a host plant.
Onion maggot adults favor long leaf blade models that are similar in structure to their

natural host (Degen and Stadler 1996). Color hue or saturation determines attractiveness

10

to onion maggot adults in the ﬁeld and the magnitude of a response is determined by the
attractive key wavelength intensity (Vernon and Bartel 1985).

Host age can also determine its attractiveness. Optimal visual, olfactory,
gustatory, and tactile stimuli that solicit strong ovipositional responses resemble those
from a small onion plant at the 3-4 leaf stage (Mowry et al. 1989). All stimuli are equally
important in generating a positive ovipositional response, and work by Harris and Miller
(1991) supports the hypothesis that temporal smnmation of inputs ﬁ'om multiple sensory
organs can trigger egg-laying.

Because onion maggot relies heavily on the success of its host, host quality
becomes an important biotic factor affecting onion maggot ﬁtness. There are many
components that are associated with host quality and the most important is nutrition.
Blaine and McEwen (1984) showed low concentrations of chlorine to be essential for
. pupation. Proteins and sucrose are essential for longevity in onion maggot males and ﬂies
of any species lacking protein in their diets reduce their overall success (McDonald and
Borden 1996b). Females especially depend on proteinaceous and carbohydrate nutrients
for normal ovarian development, with the preferred carbohydrate source being sucrose
(Blaine and McEwen 1984).

The adult is not the only life-stage that relies on proper nutrition. Larvae are also
dependent on host plants providing proper nutrients at effective levels. Proteins, lipids
and nucleic acids in cells can be affected negatively by activated forms of oxygen (Harris
1992), and this oxidative stress occurs in all organisms. However, most organisms exhibit

adaptive defense mechanisms for these oxidative stresses, usually in the form of

11

superoxide dismutase (Fridovich 1983). Superoxide dismutase activity is strongly
affected by diet. When larvae are fed a strict synthetic diet void of copper or zinc, they
exhibit lower superoxide dismutase activity (Matsuo et al. 1997). This micronutrient
dependency becomes essential for successful larval development and selects for larvae
that are able to obtain these essential nutrients.

The onion maggot is morphologically adapted for microbe grazing (Marshall and
Eymann 1981), and this probable microbial dependence is even recognized in nature. In
the ﬁeld, females searching for ovipositional sites are strongly attracted to decomposing
onions (Dindonis and Miller 1980). Onion maggot larvae can fully develop on alternate
substrate (i.e. substrate comprised only of microbes), but this event is usually rare
(Eymann and Friend 1983). Though this phenomena is not selected for in nature, it
cannot be discounted (Schneider et al. 1983). Doane (1953) reported onion maggot larval
damage was commonly accompanied by soft-rotting bacteria such as Erwinia carotovora
(Jones), and thought this relationship to be mutualistic.

Bacteria or possibly their products play major developmental roles in onion
maggot survival (Marshall and Eymann 1981). Friend et al. (1959) showed that the
presence of microorganisms on artiﬁcial medium can accelerate larval growth and onion
maggots seem to require some nutrients not present on sterilized onion tissue. Sterile
onions reduce maggot development considerably and larvae may even die when reared on

sterile onions (Marshall and Eymann 1981).

12

CONTROL STRATEGIES

Currently, there are few effective pest management tactics for controlling onion
maggot. Cultural and physical controls include crop rotation, removal of overwintering
sites, delayed planting, minimization of mechanical damage, and planting windbreaks
(Hoffrnann et al. 1996, Martinson et al. 1988, Finch and Eckenrode 1985). Hoffman et
al. (2001) effectively used nonwoven ﬁbers as a physical barrier to prevent onion maggot
adults from ovipositing eggs at the base of onion seedlings resulting in reduced numbers
of larvae on onions. Other possible strategies include the use of olfactory repellents such
as phenolics and monoterpenoids and pungent spices (Cowles and Miller 1992, Cowles et
al. 1989).

Chemical control is the most commonly used method for onion maggot
suppression and is the most effective. Commercial growers in regions of high onion
maggot damage use a soil insecticide at planting (Harris et al. 1982). Of twelve
insecticides registered since 1955 for control of onion maggot, only one, chlorpyrifos
(Lorsbana, Dow AgroSciences LLC, Indianapolis IN) is currently labeled for use, and
resistance to it is increasing (Graﬁus and Pett 1991). In 1998, chlorpyrifos was applied to
930 ha in Michigan (47% of the acreage used for dry bulb onion production) at a rate of
2.32 kg/ha with a total of 2160 kg of chlorpyrifos on onions in Michigan (MASS 1998).
Resistance occurs with the continual usage of a select group of soil insecticides
(Eckenrode and Nyrop 1995) over an extended period of time. To avoid resistance,
frequent shifts to new materials is important. However, concerns raised by the Food

Quality Protection Act of 1996 strictly limits registration of new soil insecticides

l3

(Walters and Eckenrode 1996), and this creates a problem for a management system that
heavily relies on chemical management strategies. Also, the very small market potential
for onions makes insecticide registration unproﬁtable for chemical manufacturers. This
has forced the onion industry to look for new alternatives in managing onion maggot.

Chemical control methods. Despite its economic importance, management
options for this herbivorous insect are limited and heavy reliance on a single broad
spectrum chemical generates a cause for concern. Because of the Food Quality Protection
Act of 1996, this insecticide and its usage are at risk. Chlorpyrifos has been withdrawn
from use in all indoor and outdoor urban markets. But even if use on onions is not
restricted, development of resistance by onion maggot to chlorpyrifos is a concern (Harris
and Svec 1976, Walters and Eckenrode 1996). New chemical alternatives to onion
maggot control must be developed to maintain onions as a viable crop for Michigan
vegetable farmers. Some of these management options include development of new
chemicals for managing pest populations.

A chemical that is currently in the process of replacing chlorpyrifos is an insect
growth regulator, cyromazine (Trigarda, Ciba Plant Protection, Greensborro NC).
Cyromazine has had Section18 emergency registration status for treatment of onion seed
to be used in Michigan since 1996 (Hayden and Graﬁus 1990). It is an insect growth
regulator that disrupts the molting process of some Diptera larvae (El-Oshar et al. 1985).
Its low toxicity to beneﬁcials and its effectiveness at low levels makes it a viable
candidate for controlling onion maggot (Robbins et al. 1991, Davis and Graﬁus 1997,

McComack et al. 2001). Cyromazine’s narrow range of activity (El-Oshar et al. 1985)

14

also makes it more compatible with biological control strategies. Graﬁus et al. (1997)
showed predatory carabid beetle counts to be higher in cyromazine treated sections of the
ﬁeld than in areas treated with chlorpyrifos. Its specific range of activity helps to
conserve beneﬁcial soil arthropods and potential biological control agents within onion
agroecosystems (Ebert 1999).

Biological control. Non—chemical strategies also need to be considered when
designing a pest management strategy. Natural enemies and biological control agents are
key components in managing pest populations. Tomlin et al. (1985) built miniature mass
rearing beds containing onion maggot to attract local parasites and predators. They found
20 carabid species, 42 staphylirrids, and 17 other predators (total 79) associated with the
onion maggot in or near the rearing beds and they found 7 species of parasitoids (Tomlin
et al. 1985). In the ﬁeld, carabids prey on a variety of insect pests including: aphids
(Hance 1990), codling moth, Cydz'a pomonella (L.) (Hagley and Allen 1988), onion
maggot (Graﬁus and Warner 1989), black cutworrn, Agrotis ipsilon (I-Ifrr.) (Lund and
Turpin 1977), European corn borer, Ostrinia nubilalis (Hﬁbner) (Brust et al. 1986),
armyworrn, Spodoptera exigua (Hﬁbner) (Clark et al. 1994), and wheat midge,
Sitodiplosis mosellana (Gehin) (Floate et al. 1990). However, the economic impact of
carabids on onion maggot populations is poorly understood. Graﬁus and Warner (1989)
showed that Bembidion quadrimaculatum L. consumes onion maggot eggs in ﬁeld arenas
artiﬁcially infested with eggs. Ebert (1999) showed the importance of carabids in
reducing onion maggot numbers late in the season, thus reducing the amount of

ovipositioning by females in the spring. Data on the number of prey consumed by a

15

population of carabids in ﬁeld conditions is needed to evaluate the impact of beneﬁcial
arthropods, and dispersal rates can give an indication on the effectiveness of a predator
migrating to an area of outbreak (Best et al. 1981).

Other biological control agents include the parasitoids Aleochara bilineata
(Gyllenhal) (Staphylinidae) and Aphaereta pallipes (Say) (Braconidae), the predatory
ﬂies Coenosia tigrz'na and Scatophaga stercoraria and a ﬁrngus Entomopthora muscae
(Groden 1982, Ritcey 1991, Watson et al. 1995, Failes et al. 1992, Majchrowicz et al.
1990, Hagar 1978). However, the costs involved in mass rearing these agents and the
need for innundative releases make them very costly to farmers and economically
unfeasable for use in commercial onion production systems.

CARABIDS

Carabidae are found throughout the world and are the third-most diverse family of
insects with over 30,000 described species (Larochelle and Lariviere 2001, Lorenz 1998,
Ball 1979). Carabid beetles inhabit a wide range of environments including terrestrial and
arboreal habitats. They often show strong habitat-speciﬁcity and because of this, they are
excellent bioindicators of habitat quality or changes in quality due to disturbances in the
environment (Kavanaugh 1992). Ground beetles are usually classiﬁed as either spring or
autumn breeders; spring breeders overwinter as adults and mate in the spring while
autumn breeders overwinter as larvae with the adults mating in the fall. Carabids mainly
prefer moist, well-irrigated ﬁeld conditions and seek shelter from the harsh winter

conditions by burrowing below the soil surface and by hiding under crop residues or

16

surface trash (Kirk 1976). The seasonal abundance of ground beetles depends on
nutrition, moisture, temperature, and beetle age.

Carabids are generalist predators in many agricultural landscapes. They feed on a
variety of insect pests including onion maggot (Graﬁus and Warner 1989, Ebert 1999).
However, little is known about their overall impact on onion maggot populations in onion
cropping systems. In other systems, the exclusion of generalist predators such as carabids
results in greater armyworrn damage to the corn plants (Clark et al. 1994). Laub and Luna
(1992) suggested that the presence of several carabid species in high numbers was
followed by a decrease in abundance of armyworm. Augmenting carabid beetle
populations in a ﬁeld is likely to increase predation pressure on targeted pest species
(Chiverton 1986, Menalled et al. 1999).

Predator density is not the only factor inﬂuencing rates of predation. Predator
activity and searching behavior can also affect predation rates (Barney and Pass 1986).
Rather than make generalizations about carabids at the family level, Barney and Pass
(1986) suggested that foraging and feeding strategies should be examined at the species
level. Factors that can inﬂuence these subtle differences in behavioral responses within
the Carabidae families include morphological and physiological adaptations, predator
density, and resource distribution (Bell 1990, Evans 1990). Habitat structure and
complexity and community diversity might also contribute to the effectiveness of
carabids as a management tactic. Clark et a1. (1994) found community structure of

generalist predators to be important in altering pest populations in agroecosystems.

17

CONSERVATION BIOLOGICAL CONTROL

The goal of any biological control program is to suppress and stabilize the target
pest population below an economic threshold with the use of natural enemies (i.e.
parasitoids, predators, pathogens, antagonists, or competitor populations) (van Driesche
and Bellows 1996). Protection of predator and parasitoid populations is crucial for both
native and exotic natural enemies and is key to the success of a conservation program.
Successful programs are able to shift the predator-prey or parasitoid-host ratio to favor
natural enemies (Johnson et al. 1986). There are three main approaches to biological
control: introduction, augmentation, and conservation of natural enemies. Conservation
biological control is the only method that seeks to indirectly alter existing natural enemy
populations through manipulation of their environment. Conservation strategies seek to
reduce the negative environmental inﬂuences while increasing positive inﬂuences.
Tactics used in conservation biological control include: modiﬁcation of pesticide
applications (i.e. lower rates and frequency and use of insecticides with narrow host-
range speciﬁcity); changes to the crop and non-crop habitats (i.e. intercropping, cover
crops, preservation of ﬁeld margins/borders, and creation of refuge habitats); and changes
to cultural practices (i.e. use of no-till, reduced tillage, and crop rotation) (Landis et al.
2000)

One way conservation biological control practices increase natural enemy
populations is by providing alternate foods sources for natural enemies when pest
populations are low and not able to support the biological control community. For

example, when coccinellids are provided ﬁeld borders with alternate food sources or food

18

supplements when aphid numbers are declining in the crop habitat, these alternative food
resources support growing coccinellid populations (Obrycki and Kring 1998). Adult
syrphids need nectar and pollen sources for egg production (Schneider 1969). In
sugarcane ﬁelds ﬂoral nectar sources are routinely unavailable for adult parasitoid wasps,
so cane growers have attempted to remedy this by providing suitable shelter and plants in
the ﬁelds for parasitoids (J epson 1954). Wild carrot nectar provides food for an
introduced parasitoid of the Japanese beetle, Papilla japonica (Newman) (Johnson et al.
1986). Enhancing natural enemy survival, longevity, and fecundity through conservation
practices will ultimately inﬂuence their efﬁciency at controlling the target pest species
(Gross 1987).

Another way conservation practices increase natural enemy populations is
through the use of refuge habitats. These habitats may provide alternative food sources as
described above and also provide sites for overwintering and a place for refuge from
pesticides and from disturbances caused by farming practices (Desender 1982).
Intensiﬁcation of farming has reduced hedge size and number of grassy ﬁeld borders,
which are natural reservoirs for many polyphagous predators such as carabid beetles
(Esau and Peters 1975). By introducing refuge habitats as successional strips, a diverse
natural enemy fauna can be created (Thomas et a1. 1991).

Carabids are generalist predators in many agricultural landscapes. They feed on a
variety of insect pests including onion maggot (Graﬁus and Warner 1989, CHAPTER 2).
Augmenting beetle populations in a ﬁeld is likely to increase predation pressure on

targeted pest species (Chiverton 1986, Menalled et al. 1999). In corn, the exclusion of

19

generalist predators such as carabids resulted in increased armyworrn damage (Clark et
al. 1994). However, little is known about their overall impact on onion maggot
populations.

. Carabids are very sensitive to disturbances in the environment and are easily
affected by cultivation practices (Kromp 1999). In turfgrass, insecticide applications
affect surface-foraging arthropods such as carabids through multiple routes of exposure:
topical, residual, and dietary exposure (Kunkel et al. 2001). Refuge strips can increase the
numbers and activity of carabids and other biological control agents in com and soybeans
(Carmona 1998, Menalled and Landis 1997, Lee et al. 2001). Grassy refuge habitats can
also help replenish communities reduced by heavy insecticide use (Lee et al. 2001) and
provide overwintering sites (Thomas 1990). In addition, they can provide alternate food
resources for predators when pest populations in the ﬁeld are low (Hawthome and
Hassall 1995).

Luff (1 982) investigated the impact of stable environments on carabid beetle
densities and found little ﬂuctuation in carabid abundance from year to year, thus acting
as a constant mortality factor in suppressing some pest species. Application of soil
insecticide treatments and tillage practices lower the density of all predators in an
agroecosystem by an order of magnitude (Brust et al. 1985). Refuge habitats that remain
undisturbed are needed to maintain beetle populations. Strip vegetation can offer
abundant food sources and suitable overwintering sites (Thomas 1990), promoting the
survival of the natural enemy (Den Boer 1981). Field borders, grassy strips, or hedgerows

can then become important shelters for these predators at certain times of the year (Best

20

et al. 1981). Jones (1979) found that several species would migrate to and from ﬁeld
borders into a crop area during the season and after harvest. Overall, ecologists recognize
the need to study individual movements quantitatively, to better understand the spatial
dynamics of any given population (Bell 1991).

Determining habitat suitability for natural enemies is a large concern. Aspects that
affect habitat suitability include: single large or several small refuge areas, corridors (how
habitats are connected), and refuge shape (circular versus long and narrow areas
designated for preservation of the desired species) (Simberloff 1988). Even though
determination of suitability is the ﬁrst step in species conservation, many studies fail to
thoroughly examine the habitat needs of speciﬁc natural enemies (Simberloff 1988). The
success of any conservation biological control program relies on deﬁning the biology and
habitat needs of the control agent, but the research required for accurate data describing
these aspects is costly, intensive, and time consuming (Zimmerman and Bierregaard
1986)

By understanding how a species uses a refuge habitat, we can ﬁnd better ways of
creating habitat structures that can be use in effective pest management strategies. One
strategy in manipulating population densities of natural enemies, such as carabids, is to
modify the habitat to favor recruitment (Gross 1987). Also, crop rotation can play a more
important part in managing an agroecosystem than tillage practices when building a
suitable habitat for promoting establishment of carabid communities (Weiss et a1. 1990).
Carcamo and Spence (1994) investigated the effects of crop types on carabid density and

suggested that altering crop canopies changed the microclimate. This diversiﬁcation in

21

the agroecosystem doesn’t always promote higher rates of colonization. Instead,
Letourneau (1990) suggested architectural complexity may inﬂuence or attract beetle
migration into a speciﬁc community. Beetle abundance and species richness were higher
in organic farms than chemically managed farms (Carcamo et al. 1995).

Though conservation biological control practices increase natural enemy
populations, the amount of control they provide is not well understood and is somewhat
limited. Systems where disturbances to the landscape occur regularly (i.e. cultivation of
an annual crop) have less of a chance for success due to the discontinuous interactions
between the pest and biological control agents (Gubbins and Gilligan 1997). Also,
conservation is not a quick remedy or replacement for chemical control strategies.
Conservation tactics are sometimes limited to cropping systems that have a high tolerance
for direct damage and often restricted to pest species that cause indirect damage to the
crop. For example, some crops have a no-tolerance level for pest infestation such as some
small ﬁ'uits. Onions also have a low tolerance for onion maggot damage since any
damage to small plants causes stand loss and later damage will cause quality problems
and loss at harvest. These systems often require high inputs of pesticides that can
negatively affect the natural enemy community.

Natural enemy biology and the densities required for effective pest control are
unknown for many biological control agents. How a species interacts, behaves, and uses a
refuge habitat, its prey, or the landscape is not well understood in many cropping

systems. The life history of the natural enemy needs to be well deﬁned so that the timing

22

of supplemental sprays, pesticide applications, and planting of ﬂowering nectar species
can be effective at suppressing the pest population.

Conservation and augmentation of onion maggot natural enemies requires an
integrative approach to onion maggot control. The incorporation of narrow spectrum
insecticides (Graﬁus et al. 1997) can help conserve existing predator populations.
Preservation of refuge habitats such as ﬁeld margins and hedgerows (Menalled and
Landis 1997) could potentially augment carabid communities in onion ﬁelds, thus
increasing the importance of biological control. Integrating multiple aspects of onion
maggot control will provide a more efﬁcient and sustainable approach to managing onion
maggot populations in Michigan onions.

Pest management costs also need to be considered when evaluating the role of
conservation in biological control programs. Modiﬁcation of pesticide schedules can
reduce the amount of sprays by encouraging farmers to apply pesticides only when pest
populations exceed speciﬁed levels (Hoy 1988). This can beneﬁt natural enemy
populations and could signiﬁcantly decrease pesticide costs by using fewer sprays but
still provide some level of control.

A major concern about the use of conservation tactics is the limited acceptance by
the farming community. Reconstructing the landscape and incorporation of natural
enemy refugia often requires land to be put out of production (Thomas et al. 1991). If the
crop happens to be of great cash value, this could cause ﬁnancial stresses to the farming

operation. Herbicide programs may also need to be modiﬁed to protect the refuge strips.

23

Measures that illustrate the effectiveness of a given natural enemy are needed to justifty
the area needed for reduction of pest populations in the ﬁeld.

Even though refuges may provide excellent sources of food and shelter, they may
also act as sinks for plant pathogens and pest insects. For example, incorporating grassy
refuge strips into onion agroecosystems increases carabid abundance, however, there is a
possibility for the harboring of onion maggot adults (Finch et al. 1986), which could
affect onion maggot damage in the ﬁeld. Both positive and negative effects relating to the
control of a particular pest species need to be critically assessed before carrying out a
management regime.

Natural enemy conservation coincides with the ideals deﬁned by integrated pest
management (IPM) approaches in agricultural systems. A true integrative approach to the
management of a pest includes the use of a broad spectrum of chemical, cultural, and
biological control practices to reduce a pest population below economically damaging
levels. IPM also reduces the risk the insect resistance by spraying/applying control
measures when the target pest population reaches an economic threshold. The objectives
of any IPM program is to provide many control methods in designing a sustainable
agroecosystem. However, chemical control is the most utilized tactic in managing pest
outbreaks in most agroecosystems, especially in onion production. There are many
reasons for its desirability: low cost, high efﬁciency, availability, a long history of
success and low labor inputs are only a few examples.

Heavy reliance on insecticides such as chlorpyrifos in onions can select for

resistant individuals within a population and the probability for failure increases. Adding

24

another chemical component like cyromazine would aid in reducing the chance for onion
maggot resistance. Conservation biological control incorporates multiple chemical
strategies and cultural practices, and it enhances the reliance on the biological control
communities within existing agroecosystems.

If pesticides continue to be a major part of the system, understanding their impact
on biological control agents is important. A key component to a sustainable management
system is the added pest control received from biological control agents or natural
enemies and other cultural practices and increased stability of the agroecosystem. By
focusing on the overall impact of a particular management tactic or system, we can
achieve a better evaluation of its effectiveness and efﬁcacy.

Conservation and augmentation of onion maggot natural enemies requires an
integrative approach to onion maggot control. The incorporation of narrow spectrum
insecticides (Graﬁus et al. 1997) and preservation of refuge habitats such as ﬁeld margins
and hedgerows (Menalled and Landis 1997) can augment carabid communities.
Integrating multiple aspects of onion maggot control will provide a more efﬁcient and
sustainable approach to managing onion maggot populations in Michigan onions.

The objectives of this study were to 1) measure the impacts of several carabid
species on onion maggot larvae and pupae; 2) determine the effects of refuge habitats on
carabid communities in Michigan onions; and 3) evaluate the combination of cyromazine

and grassy refuge strips as a new tool for management of onion maggot.

25

CHAPTER 2:
CARABIDAE PREDATION ON ONION MAGGOT, DELIA ANT IQUA
(DIPTERA: ANTHOMYIIDAE), LARVAE AND PUPAE IN THE GREENHOUSE
AND LABORATORY

ABSTRACT

Carabids are generalist predators in many agricultural landscapes and are capable
of feeding on a variety of insect species and weed seeds. Many carabids feed on both
plant and animal material and use a wide host range, thus being able to feed on live prey,
carrion, and plant material. Research studies have focused on evaluating effectiveness of
adult carabids as predators of signiﬁcant agricultural pests including onion maggot (Ebert
1999, Graﬁus and Warner 1989). In ﬁeld observations, high activity-densities for P.
chalcites, P. lucublandis, and P. melanarius appear to coincide temporally with onion
maggot oviposition and larval development. Carabid beetle predation of onion maggot
larvae and pupae were examined using greenhouse and laboratory studies. In this study,
Chlaenius sericeus (Forster), Poecilus lucublandis (Say), Pterostichus melanarius
(Illiger), and Poecilus chalcites (Say) consumed more onion maggot larvae per day than
Harpalus aﬂinis (Schrank) or Harpalus pennsylvanicus (DeGeer). Scarites quadriceps
Chandoir consumed the most pupae per day and was the largest carabid species assessed.
In a laboratory study, more pupae were consumed at 0 cm and 1 cm depths than at 4 cm

or 8 cm depths.

KEY WORDS Delia antiqua, ground beetle, natural enemies, generalist predators,

biological control agents

26

Carabidae are found throughout the world and are the third-most diverse family of
insects in North America with over 30,000 described species (Kavanaugh 1992, Borror et
al. 1981, Ball 1979). Carabid beetles inhabit a wide range of environments including
terrestrial and arboreal habitats. They often show strong habitat-speciﬁcity and, because
of this, they are excellent bioindicators of habitat quality or changes in quality due to
disturbances in the environment (Kavanaugh 1992). Ground beetles are usually classiﬁed
as either spring or autumn breeders; spring breeders overwinter as adults and mate in the
spring while autumn breeders overwinter as larvae with the adults mating in the fall
months of the growing season (Lindroth 1969). Carabids mainly prefer moist, well-
irrigated ﬁeld conditions and seek shelter ﬁ'om the harsh winter conditions by burrowing
below the soil surface or by hiding under crop residues or surface trash (Kirk 1976). The
seasonal abundance of ground beetles often depends on nutrition, moisture, temperature,
and beetle age.

Carabids are generalist predators in many agricultural landscapes and are capable
of feeding on a variety of insect species and weed seeds. Many carabids feed on both
plant and animal material and use a wide host range, thus being able to feed on live prey,
canion, and plant material. Adults and larvae are mostly carnivorous, however, a few
carabid species are known to damage crops. Some carabid species are known to feed on
seeds of oats, barley, wheat, corn and even parsley (Thiele 1977). However, the damage
is insigniﬁcant.

Research on predation by carabids has focused on evaluating effectiveness of
carabid adults as predators of agricultural pests. Some carabid species are capable of
consuming high numbers of aphids (Hance 1990), codling moth, Cydia pomonella (L.)
(Hagley and Allen 1988), black cutworrn, Agrotis ipsilon (an.) (Lund and Turpin 1977),
European corn borer, Ostrinia nubilalis (Hﬁbner), (Brust et al. 1986), armyworrn larvae,

Spodoptera exigua (Hilbner) (Clark et al. 1994), diarnondback moth larvae Plutella

27

xylostella (L.) (Suenaga and Hamamura 1998), and different life stages of carrot weevil,
Listronotus texanus (Stockton) (Baines et al. 1990).

Ebert (1999) examined the impact of increased carabid beetle populations on
onion maggot egg densities with ﬁeld studies. She concluded that predation was higher
in plots containing greater numbers of carabid beetles. However, the experimental design
did not allow for possible inferences pertaining to onion maggot egg survival. Graﬁus
and Warner (1989) demonstrated that arenas containing greater numbers of Bembidion
quadrimaculatum L. was correlated with less damage and fewer onion maggot eggs, thus
showing the ground beetles potential as biological control agents of onion maggot in
Michigan onion ﬁelds.

In ﬁeld observations, high activity-densities for P. chalcites, P. lucublandis, and
P. melanarius appear to coincide temporally with onion maggot oviposition and larval
development (Figure 3). Carabid activity starts to increase early in the season with the
presence of spring breeders (i.e. carabids that overwinter as adults and lay eggs). As this
occurs, onion maggot adults emerge from overwintering puparia. These begin to
oviposite shortly after their emergence and peak oviposition occurs between late May to
late June. This ﬁrst generation of onion maggots has the greatest damage potential
because onion seedlings are in their most vulnerable stage. As onion maggot larvae are
developing, carabid populations are at their highest. This same trend is also seen during
the second onion maggot generation (mid to late July) and the occurrence of fall breeding
carabids (i.e. carabids that overwinter as eggs and are now emerging in mid-summer as
adults). But carabid impacts on onion maggot populations in commercial farming
operations are not well understood. Future research on carabid predation and the use of
refuge strips to increase populations in commercial ﬁelds will indicate whether carabids
and refuge strips can signiﬁcantly contribute to onion maggot population management.

The objective of this study was to examine carabid beetle predation of onion

maggot larvae and pupae in greenhouse and laboratory studies.

28

MATERIALS AND METHODS

Adult carabids trapped from commercial onion ﬁelds in Clinton County MI
between May and July 2001 were used for the studies. Carabids were kept at 21°C in
plastic boxes supplied with a diet of dry dog food and water for a week prior to the
experiments. An onion maggot colony was started from ﬁeld-collected larvae during the
summer of 2000 and was maintained by the J .R. Miller lab, Michigan State University,
East Lansing MI. Onion maggot larvae and pupae were collected from the colony and
used for the experiments.

No-choice predator bioassays.

Larval predation by carabids. To determine the daily predation rates of
commonly collected beetles found in commercial onion ﬁelds, I used a predator arena of
ten second-instar onion maggots placed in petri dishes (150 mm diam.) along with a
moist cellulose sponge (5 x 10 x 10 mm). There were seven treatments: six carabid
species (Chlaenius sericeus, Harpalus aﬂinis, Harpalus pennsylvanicus, Poecilus
lucublandis, Pterostichus melanarius, and Poecilus chalcites) and one group without
predators to account for larval mortality and escape during the experiment. One beetle or
no beetle (control) was put into each arena. The arenas were kept in a growth chamber at
21°C, photoperiod of 16:8 (lightzdark). Daily for 6 d the number of onion maggot larvae
consumed or attacked in each arena was recorded and all larvae were removed and
replaced with new larvae from the lab colony. Data were analyzed with one-way
ANOVA (PROC GLM, SAS Institute, version 8.1) blocked by day. Means were
separated with Fisher’s protected LSD test (a=0.05).

Papal predation by carabids. To determine predation rates on pupae, onion
maggot pupae were placed into petri dishes as described above. There were ﬁve carabid
species tested (H. aﬂinis, H. pennsylvanicus, P. lucublandis, P. melanarius, P. chalcites
and Scarites quadriceps). One beetle was put in each arena. The arenas were arranged in

a randomized complete block design and kept in a grth chamber at 21°C, photoperiod

29

of 16:8 (lightzdark) and were blocked by day. The number of pupae eaten or partially
eaten in each arena was recorded daily for 5 d. Eaten or partially eaten pupae were
removed and replaced with new pupae from the lab colony. Data were analyzed as
before.

Greenhouse and laboratory experiments.

Larval predation by carabids in onion pots. A greenhouse study was conducted
to test the effects of carabid beetles on onion maggot larval numbers in a controlled
environment. Eight fungicide treated onion seeds (BejoO Seeds, Inc.) were planted in
square plastic pots (10 x 10 x 20 cm) at a depth of 3 cm in sifted organic muck soil from
the Michigan State University Muck Soils Research Farm, Clinton County MI. The
arenas were placed in the greenhouse in early May of 2001 and the pots were watered and
weeded when needed. When the onion plants reached the 3-leaf stage, they were thinned
to 4 onion plants per pot.

In August 2001, ten second instar onion maggots were placed in each arena and
were allowed to acclimate to the greenhouse and arena conditions for 2 d. The four
treatments tested included three carabid species (P. chalcites, P. lucublandis, and P.
melanarius) and a control group without carabids to account for natural larval death,
larval escape, and/or handling loss. After the 2 d acclimation period one beetle or no-
beetle (control) was placed in each experimental arena and all arenas were arranged in a
completely randomized design in a greenhouse with temperatures ranging from 21-27°C
and a photoperiod of 16:8 (lightzdark). The larvae were exposed to predators for 1 wk.
Then the soil was searched and the number of larvae remaining in each arena was
recorded and analyzed with one-way AN OVA (PROC GLM, SAS Institute, Version 8.1).
Fisher’s protected LSD test was used to separate mean differences between treatments
(a=0.05). Data from arenas containing dead or missing predators were not used in the

analysis.

30

Predation inﬂuenced by depth and carabid species. A lab study was conducted
to measure the ability of carabid species captured in commercial onion ﬁelds to consume
onion maggot pupae at different soil depths. This experiment tested consumption rates of
buried pupae (0 cm, 1 cm, 4 cm, or 8 cm) by two common predator species (P.
lucublandis or P. melanarius) found in onion agroecosystems.

The arena consisted of two 1 liter plastic cups (11.5 cm diameter, 14 cm height),
one inverted on top of the other (Figure 1). Next, two 8 x 8 cm sections from the top cup
were removed and replaced with a mesh screen (screen size = 1 x 1 mm). This allowed
for air ventilation and light penetration into the arenas. Ten pupae were placed at the
speciﬁed depths (0 cm, 1 cm, 4 cm, or 8 cm) and covered with muck soil, collected and
sifted to remove all other potential food or predators from the Michigan State University
Muck Soils Research Farm, Clinton County MI. A 2 dram vial ﬁlled with water and
plugged with a moist cotton ball was used to maintain the humidity levels within the
arena; it also provided a source of water for the predators. After the onion maggot pupae
were placed in the arenas, a single beetle was added to each arena. Top and bottom halves
of the arenas were secured together with tape. Predator arenas were placed on a bench at
room temperature (approximately 21°C) with a photoperiod of 16:8 (lightzdark).

The pupae were exposed to the predators for 1 wk and the numbers of onion
maggot pupae remaining in each arena were recorded. Because depth is a continuous
variable, a regression analysis was used (PROC REG and PROC UNIVARIATE, SAS
Institute, Version 8.1) (a=0.05). Shapiro-Wilks tests for normality were used and data
were transformed with log(x+1) to normalize the data before regression analysis. Arenas
containing dead or missing predators were not used in the analysis. A parallel test group
using no predatory beetles was used as a control to measure efﬁciency in pupae recovery

techniques and all pupae were recovered. The control group was not used in the analysis.

31

RESULTS AND DISCUSSION
No—choice predator bioassays.

Larval predation by carabids. C. sericeus, P. lucublandis, P. melanarius, and P.
chalcites consumed signiﬁcantly more larvae per day than H. aﬁinis or H. pennsylvanicus
(p<0.05) (Table 1). H. aﬂinis and H. pennsylvanicus are mainly phytophagous (Hagley et
al. 1982, Kirk 1973), explaining the lower consumption rates for these two species. The
mean number of onion maggot larvae consumed by H. aﬂinis and H. pennsylvanicus was
not different from numbers dead or missing in the control (p>0.05). These consumption
rates represent what is occurring in a no-choice laboratory test with no limits to access to
the larvae by the carabids.

Finch (1996) suggests that predator size plays a crucial role when it comes to
cabbage root ﬂy, Delia radicum L., egg predation. The relationship between prey and
mandible size is key to the efﬁciency of carabids to consume cabbage root ﬂy eggs. Total
lengths of C. sericeus, P. chalcites, P. lucublandis, and P. melanarius range ﬁom 10. l to
13.5 mm, 10.5 to 13.0 mm, 9.0 to 14.0 mm, and 12.0 to 18.0 mm, respectively (Lindroth
1969). Finch (1996) found that the predator size had an inﬂuence on predator
consumption of root ﬂy eggs; the largest and smallest beetles consumed fewer eggs than
medium sized beetles. The results from that study suggest that the ideal cabbage root ﬂy
egg predator ranges ﬁ'om 27-10 mm in length (Finch 1996).

This might also be the case when discussing onion maggot larvae predation by the
species tested. Future bioassays that could address this question of size might be relevant
to the incorporation of refuge strips in onion cropping systems. Since larger beetles have
a tendency to consume more larvae (i.e. P. lucublandis and P. melanarius), the

importance of these and other similar sized beetles as generalist predators in onion

32

agroecosystems needs to be evaluated. The relationship between predator and prey is
essential to understanding the success of the intended biological control agent.

Pupal predation by carabids. P. chalcites, P. lucublandis, P. melanarius, and S.
quadriceps consumed signiﬁcantly more pupae per day than H. aﬂinis and H.
pennsylvanicus (p<0.05) (Table 2) . Predation was observed in H. aﬁinis and H.
pennsylvanicus, but variability was high and their mean pupae consumption rates were
not signiﬁcantly different from zero. The species that consumed the most pupae per day
was also the largest carabid species assessed, S. quadriceps (16.0 to 20.0 mm). Again,
this suggests that predator size might have .an inﬂuence in the choices pertaining to prey
size and consumption rates.

Greenhouse and laboratory experiments.

Larval predation by carabids in onion pots. A large number of onion maggot
larvae were lost or disappeared in the absence of predators. Larvae
consumption/disappearance ranged from 47-57 %, however, there were no signiﬁcant
differences observed (p>0.05) (F 3,102=1 .77, P=0.16). These carabids apparently were
not able to ﬁnd and consume larvae buried in the soil or hidden within the onion plant
tissue. Other possible reasons for the lack of differences include experimental design, the
difﬁculty in retrieving larvae from the onion plants, natural larval death, and the
probability of larvae escaping from the arena. Plant size could have also contributed to
the low level of predation observed. Second instars were used and were placed in the pots
when the onions were at the 3-4 leaf stage. Individual onion plants were large enough to
support the growth of a developing larva. Since the larvae had all the resources needed to
complete their development, their need to search for a new host plant was minimized and
little plant-to-plant movement probably occurred. Therefore the probability of larvae
moving onto the soil surface and potential predation by generalist predators such as

carabids was low. Future behavioral studies would be needed to support this hypothesis.

33

Research on predation on onion maggot eggs and other closely related species has
been well documented (Graﬁus and Warner 1989, Ebert 1999, Finch 1996). Finch and
Elliott (1993) showed carabids to be effective predators of cabbage root maggot when the
eggs were on the soil surface; none of the beetles they tested were able to ﬁnd the eggs
buried below the soil surface. However, little research has been done on the effectiveness
of carabids on predation on onion maggot larval stages. Brust (1991) developed a method
for observing below-ground arthropod predators and concluded that carabid larvae were
signiﬁcant predators of ﬁrst, second, and third instars of southern corn rootworm,
Diabrotica undecimpunctata howardi Barber. Brust (1991) was able to show a strong
correlation between the number of southern corn rootworrn larvae that disappeared and
the number of predators observed.

Evaluating the impact of variables such as plant size, life stage of the prey items
(egg vs. larvae vs. pupae), soil moisture, host quality, soil type, and duration of the study
will be necessary to determine the role of these generalist predators in reducing onion
maggot populations in the ﬁeld.

Carabid predation inﬂuenced by depth and species. There was a signiﬁcant
relationship between pupae depth and rate of predation by both predators P. lucublandis
(F 1,22 = 20.28, P=0.001) and P. melanarius (F1,22 =25.27, P<0.0001). A parallel series
was run without predators and all pupae were recovered. The zero consumption observed
in the control group was expected and it validated the techniques used to recover the
pupae. As pupal depth increased, the predation rates of onion maggot pupae for both
species tested (P. lucublandis and P. melanarius) was signiﬁcantly lower; the most pupae
were consumed at 0 cm (p<0.05) (Figure 2). Variation in pupae consumption rates
explained by the regression model was low for each species tested; r2 values for P.
melanarius and P. lucublandis were 0.45 and 0.43 respectively. No pupae were
consumed at the 4 cm and 8 cm depths, but high numbers of pupae were consumed at the

soil surface. There was deﬁnitely a strong correlation between depth and the number of

34

pupae consumed, but 40-45% of the variation in consumption rates could be explained by
my model.

The observed predation/depth relationship for these carabid species could be
explained by their prey-searching behavior. Carabids are generalist predators and they
use a variety of mechanisms for prey allocation: random search, sight, and cherrrical cues
(Lovei and Sunderland 1996). They spend most of their time on the soil surface, and they
most commonly search for prey using a random walk or search. As cues become stronger,
they increase their turning angles, thus increasing the probability for ﬁnding the prey
item. As the strength of the signal decreases, they resume a random, but a more straight
walk. Since the pupae at 0 cm were exposed and the beetles were conﬁned to small
arenas, the probability of a beetle coming into contact with the pupae increased and
number of onion maggot pupae consumed was high. As the depth of the buried pupae
increases, the probability of a beetle ﬁnding pupae decreased.

Some carabid species such as P. melanarius have burrowing behaviors that could
bring them into contact with pupae located below the soil surface (Wallin 1988).
Burrowing was observed at 1 cm in this study, but few buried pupae were consumed by
P. melanarius. This suggests that locating pupae by burrowing was a rare occurrence and
it was not a common behavior used by P. melanarius for resource allocation. In the ﬁeld,
onion maggot rarely pupate at the soil surface; factors such as moisture and temperature
affect onion maggot pupation depths.

The results from this experiment suggest that the probability of a carabid
consuming onion maggot pupae decreases as the depth of the pupae increases. When
examining the life history of the onion maggot, female onion maggot adults lay their eggs
at the base of onion seedlings early in the season. As the egg hatches, maggots make their
way into the root zone of the onion plant and eventually into the stem of the onion. As
they grow and develop through 3 larval instars, they eventually pupate 5-8 cm below the

soil surface. From my experiment I observed no predation of onion maggot pupae at this

35

depth. This does not, however, rule out the importance of carabids at reducing the
number of pupae in the ﬁeld because carabid larvae spend a majority of their
developmental time in close contact with the soil (Lindroth 1969). Although little is
known about carabid larvae prey preference and feeding behaviors. Future predation
studies should address the role of immature carabids in the predator-prey complex in any
biological control program using carabids for control of important soil arthropods.

Generalization about carabids and their potential ability to reduce pest populations
in the ﬁeld should be made with caution. Predator activity and searching behavior can
also affect predation rates in the ﬁeld (Barney and Pass 1986). Rather than make
generalizations about carabids at the family level, Barney and Pass (1986) suggested that
foraging and feeding strategies should be evaluated at the species level.

Factors that can inﬂuence these subtle differences in behavioral responses within
the Carabidae family includes morphological and physiological adaptations, predator
density, and resource distribution (Bell 1990; Evans 1990). Clark et al. (1994) found the
community structure of generalist predators to be an important factor in altering pest
populations in agroecosystems. Future ﬁeld studies that tried to understand community

diversity might contribute to the effectiveness of carabids as a management tactic.

36

  
 

A
‘— cage (top)
E
O
00
N screen
Pu ae
Depths
(1) cm soil surface
cm
4 cm onion maggot
pupae
8 cm
cage (bottom)
v

 

Figure 1. Arena design for pupal predation by carabids, Pterostichus melanarius
and Poecilus lucublandis. One 1 liter plastic cup (11.5 cm diameter, 14 cm height)
was inverted on top of another 1 liter plastic cup. The top cup had 2 sections (8 x 8

cm) removed and replaced with screen mesh (mesh size = 1 x 1 mm).

37

Table 1. Mean number of onion maggot larvae consumed per day by various carabid species

captured in commercial onion ﬁelds.

 

 

Species n Larvae/day' i SE
Chlaenius sericeus 20 5.1 i 0.41 a
Harpalus afﬁnis 12 1.2 i 0.53 b
Harpalus pennsylvanicus 16 0.5 i 0.46 b
Poecilus Iucublandis 20 3.6 :t 0.46 a
Pterostichus melanan'us 16 4.6 i 0.46 a
Poecilus chalcites 16 3.5 i 0.41 a
Control (No-predator) 16 0.1 2 i 0.46 b

 

1 Means within a column followed by different letters are signiﬁcantly
different (P<0.05, Fisher's protected LSD test).

2 Arenas that contained no—predators (control) were used to account for larval
death and larval escape during the experiment.

38

Table 2. Mean number of onion maggot pupae consumed per day by various carabid species

captured in commercial onion ﬁelds.

 

 

Species n Pupaelday’ t SE
Harpalus afﬁnis 36 0.4 i 0.38 d
Harpalus pennsylvanicus 6 1.2 i 0.95 cd
Poecilus aha/cites 24 2.3 i 0.47 c
Poecilus Iucablandis 90 4.0 i 0.24 b
Pterostichus melanarius 18 4.9 i 0.54 b
Scarites quadriceps 6 8.2 i 0.94 a

 

1 Means within a column followed by different letters are signiﬁcantly
different (P<0.05, Fisher's protected LSD test).

39

 

9
i A) Poecilus Iucablandis

 

 

 

 

\ = -0.7376x + 4.6473

 

/

Consumption rate (pupae/wk)

 

 

 

 

 

 

 

 

 

 

 

 

 

0 2 4 6 8 1O
10
B) Pterostichus melanarius

9
S?
E 8
8
Q 7
:3
5 a
a _.
E 5 \ y--0.8237x+ 5.2602
c \
.2 4
E \

3
3
3 2 \
8 \

1 if \

o . é . 4

 

o 2 4 6 8 10
Depth (cm)

Figure 2. Correlation between mean number of onion maggot pupae consumed by A)
Poecilus lucublandis and B) Pterostichus melanarius at varying depths (0 cm,

1 cm, 4 cm, or 8 cm).

40

**********

8

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errageme
—> Peakon’onn'amot

 

8

 

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2
8
§

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,0\ Ah meme

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/ \ i
I \ - .3

 

 

 

 

 

 

 

 

 

a s a a

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A"

<
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/
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Total number of beetles captured

 

 

A

0”U\ o’ \ g.
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Od—Siiilliﬁ4iiiiiiliu
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—<>-Poeduschdcites-~X- Poedrslrnﬂaﬁs-O-Ptemstidisnelm

Figure 3. Carabid beetle activity-density for the species Poecilus chalcites, Poecilus

Iucablandis, and Pterostichus melanarius at the Michigan State UniversityMuck Soils

Research Farm, Clinton County MI in 2000.

41

CHAPTER 3:
GRASSY REFUGE STRIPS AND A NARROW SPECTRUM INSECTICIDE
(CYROMAZINE) CON SERVE GROUND BEETLE (COLEOPTERA:

CARABIDAE) POPULATIONS IN MICHIGAN ONIONS

ABSTRACT

Onion maggot, Delia antiqua (Meigen), is the most economically important insect
pest in Michigan onions (Allium cepa L.). In years of severe outbreak it can cause a 40-
80% reduction in yield. Effective management of this pest relies on the use of
chlorpyrifos, a broad-spectrum insecticide, for control. Michigan onion growers need
additional control methods for managing onion maggot. My objectives were to 1)
determine the effects of refuge habitats on carabid communities in Michigan onions, and
2) evaluate the combination of cyromazine and refuge strips in onions as a new tool for
management of onion maggot. We looked at the effect of newly established grassy
refuges on carabid beetle populations in a Michigan onion ﬁeld. The carabid activity-
density within 3.6 m wide grassy refuge strips during 2000 was not signiﬁcantly different
from the activity-density within similar onion control strips. Pterostichus melanarius
(Illiger) was the only species more abundant in the newly established refuges than in the
onion habitats. However, the presence of a grassy reﬁrge increased carabid populations in
the adjacent crop habitat, including entomophagous predators such as Poecilus chalcites
(Say) and Bembidion quadrimaculatum L. In 2001, signiﬁcantly more Elanphropus

anceps (LeC.) were captured in untreated or crop areas treated with cyromazine than crop

42

areas treated with chlorpyrifos; E. anceps was the only species directly affected by the
insecticide treatments. Conservation practices including the use of narrow-spectrum
insecticides and refuge strip habitats will help to deﬁne the role of generalist predators in
the control of onion maggot.

KEY WORDS Delia antiqua, onion maggot, ground beetles, refuge habitats,

conservation biological control, carabids, generalist predators

The onion maggot, Delia antiqua (Meigen), is the most serious and economically
important insect pest of onions (Allium cepa L.) in Michigan and much of the
northeastern United States and Canada (McEwen et al. 1981, Ellis and Eckenrode 1979,
Wells and Guyer 1966). Onion maggot is a specialist herbivore on onions (Ellis and
Eckenrode 1979b) and a few other minor Allium species. In Michigan the onion maggot
has three distinct generations each year, with the initial spring emergence of adults
occurring in late April or early May (Zandstra et al. 1996, Eckenrode et al. 1975, Loosjes
1976). First generation larvae have the most impact economically, because the onion
plant is in its most vulnerable stage and a single maggot can destroy up to 12-15
seedlings before pupating (Miller and Cowles 1990, Loosjes 1976). Onion maggot has
the potential of causing a 40-80% reduction in yield without proper chemical or cultural
control strategies (Zandstra et a1. 1996).

Despite its economic importance, management options for this pest are limited.
Heavy reliance on a single broad-spectrum insecticide by growers generates a cause for
concern. Chlorpyrifos (Lorsbana, Dow AgroSciences LLC, Indianapolis IN) is the only

chemical currently registered for control of onion maggot in Michigan onions. Because of

43

the Food Quality Protection Act of 1996, chlorpyrifos has been withdrawn from use in all
urban markets and from minor uses in other crops. Even if use on onions is not restricted,
development of resistance by onion maggot to chlorpyrifos is a concern (Harris and Svec
1976). Cyromazine (Trigarda, Ciba Plant Protection, Greensborro NC) has had
emergency registration (Section 18) status as a seed treatment for control of onion
maggot since 1996. It is an insect growth regulator that disrupts the molting process of
some Diptera larvae (El-Oshar et al. 1985). This speciﬁc range of activity helps to
conserve beneﬁcial soil arthropods within onion agroecosystems (Ebert 1999). New
alternatives for onion maggot control must be developed to maintain onions as a viable
crop for Michigan vegetable farmers.

Carabids are generalist predators in many agricultural landscapes. They feed on a
variety of insect pests including onion maggot (Graﬁus and Warner 1989, CHAPTER 2).
Augmenting carabid beetle populations in a ﬁeld is likely to increase predation pressure
on targeted pest species (Chiverton 1986, Menalled et al. 1999). In com, the exclusion of
generalist predators like carabids results in increased armyworrn damage (Clark et al.
1994). However, little is known about their overall impact on onion maggot populations.

Carabids are very sensitive to disturbances in the environment and are easily
affected by cultivation practices (Kromp 1999). Refuge strips can increase the numbers
and activity of carabids and other biological control agents in corn and soybeans
(Carrnona 1998, Menalled and Landis 1997, Lee et al. 2001). Grassy refuge habitats can
also help replenish communities reduced by heavy insecticide use (Lee et al. 2001) and

provide overwintering sites (Thomas 1990). In addition, they can provide alternate food

resources for predators when pest populations in the ﬁeld are low (Hawthorne and
Hassall 1995).

Conservation and augmentation of onion maggot natural enemies requires an
integrative approach to onion maggot control. The incorporation of narrow spectrum
insecticides can help conserve existing predator populations (Graﬁus et al. 1997).
Preservation of refuge habitats like ﬁeld margins and hedgerows (Menalled and Landis
1997) could also potentially augment carabid communities in onion ﬁelds, thus
increasing the importance of biological control. Integrating multiple aspects of onion
maggot control will provide a more efﬁcient and sustainable approach to managing onion
maggot populations in Michigan onions.

My objectives were to 1) determine the effects of refuge habitats on carabid
communities in Michigan onions, and 2) evaluate the combination of cyromazine and
refuge strips in onions as a new tool for management of onion maggot.

MATERIALS AND METHODS
1999 ﬁeld study.

Predator enclosures were established in an onion ﬁeld located at the MSU Muck
Crops Research Farm, Clinton County MI in August 1999. This was a one-factor
treatment design with three treatments: full-enclosure plot, partial-enclosure plot, and a
grassy border. Plots were arranged along the edge of an established grassy border. Plots
(10 x 10 m) were surrounded by a 20 cm high plastic barrier that was secured 20 cm deep
into the ground to reduce carabid migration between plots (Lee et al. 2001). The plastic
barrier was secured into the soil using wooden stakes. Full enclosure plots were

surrounded by plastic barrier on all sides to prevent carabid movement into or out of the

45

plots (Figure 4). On the partial-enclosure plots, the side closest to the grassy border
remained open to encourage carabid migration into the plot from the grassy border. The
grassy border plots were adjacent to the full enclosure plots and were used to monitor the
carabid populations; no physical barrier was constructed.

Pitfall traps were used to monitor carabid activity—density. Traps (4/plot) were
located in the second and forth rows of each onion plot (2 m from the barrier wall and 6
m between each trap) and in similar locations in the grassy border plots (Figure 4). Traps
were checked 4-5 times/wk between 1 Aug and 8 Sept 1999 and carabids in the traps
were identiﬁed to species and released on site.

Trap catches were totaled over the entire trapping period. The data was analyzed
with one-way ANOVA (PROC GLM, general linear model, SAS Institute 8.1) (P=0.05).
Activity-densities for each carabid species that accounted for >5% of the total trap catch
were analyzed. All data were normalized with a log(x+l) transformation before analysis.
Established grassy refuges within an onion field.

Field experiments were conducted at the Michigan State University Muck Soils
Research Farm, Clinton County MI in 2000 and 2001. The overall ﬁeld dimension was
30 m long by 183 m wide. The south side of the ﬁeld was adjacent to a well-established
grassy border, and the north edge was adjacent to a tree line running east and west. I
created raised beds (30 m x 1.7 m x 0.3 m high) with a standard commercial onion
bedder. A 3.6 m wide grassy refuge treatment consisted of a mixture of three cover crop
species: orchard grass (Dactylus glomerata L.), white clover (T rifolium repens L.), and
red clover (T rifolium pratense L.); I rounded and hand-raked the raised beds assigned to

the grassy refuge strip treatment. The orchard grass, white clover, and red clover were

46

sown with a hand-spreader at the recommended seed application rates of 5-7 kg/ha, 1-2
kg/ha, and 2-7 kg/ha, respectively. Onion control strips were planted to onions and were
not treated with an insecticide; the control strip mimicked normal onion ﬁeld conditions
and canopy cover. We measured the impact of newly seeded refuge strips on carabid
beetle populations in 2000 and the effects of established refuges, insecticides, and
interactions between refuges and insecticides in 2001. The same ﬁeld and refuge strips
were used in both years, arranged in a randomized complete block design.

Newly established grassy refuges. A one factor experiment with two treatments
was planted in early May 2000 and was blocked by location. There were 4 blocks with 2
plots per block. Each plot contained ten beds; four onion beds on either side of a two-bed
(3.6 m wide) treatment strip (Figure 5). Treatments consisted of refuge strips or onion
control strips as described above. Crop areas on both sides of the treatment strips (four-
bed crop areas) were planted to onions. Herbicides, fungicides, fertilizer, and irrigation
were applied throughout the growing season according to standard commercial practices;
no insecticide was used in this experiment.

Carabid activity-density was measured with dry pitfall traps for 4 consecutive
days every other week from 9 May — 18 September 2000. There were 36 traps/plot (24
traps in the adjacent crop areas and 12 traps in each treatment strip); traps were evenly
spaced throughout the refuge and crop areas (Figure 5). Traps were checked daily and the
carabids were identiﬁed to species and released; traps were covered with plastic lids
when not in use. I took specimens to the lab when specimens could not be identiﬁed in
the ﬁeld. Catches within the crop areas, within the treatment strips, and within the entire

plot (traps located within the crop area plus traps in treatment strips) were analyzed with

47

one-way AN OVAs with subsamples (PROC GLM, SAS Institute version 8.1) (P=0.05).
Activity-densities for carabid species that accounted for >5% of the total trap catch were
analyzed. All data were normalized with a log(x+1) transformation before analysis.

Insecticide and refuge habitat effects on predator populations. In 2001, I
evaluated the impacts of a combination of insecticide application and reﬁrge habitat on
carabid populations using predator inclusion/exclusion plots. I used a split-plot design
with the whole-plots arranged in a randomized complete block design. The whole-plot
factor was the same treatment strips as in 2000 (3.6 m wide grassy refuge strip or two-
bed onion control strip), and the sub-plot factor was an insecticide treatment
(chlorpyrifos, cyromazine, or untreated) applied to onions in the three-bed crop areas
adjacent to the 3.6 m wide refuge treatment strips (Figure 6). Each whole-plot (30.5 x 17
m) was sectioned off lengthwise into three sub-plots (10 x 17 m) and I randomly assigned
sub-plot treatments within each whole-plot (Figure 6). To prevent predator movement
between sub-plots, all sub-plots were completely and individually enclosed with a 20 cm
high plastic barrier secured 20 cm into the soil and supported by corner and side-wall
stakes (Lee et al. 2001).

Ground-dwelling predators were monitored in the insecticide treated or untreated
crop area and within treatment strip habitats using dry pitfall traps (11.5 cm diam., 15 cm
ht.). Each sub-plot contained 12 traps (8 traps in the crop area and 4 in the treatment
strip) arranged as in the previous experiment. A total of 288 pitfall traps were arranged
and monitored as in 2000.

Catch for each trap was totaled over the whole season and catch/trap were

analyzed with a split-plot AN OVA (P=0.05) (PROC GLM, SAS Institute, Version 8.1).

48

Catches within the crop areas, within the treatment strips, and within the entire plot (traps
within the crop area plus the traps in treatment strips) were analyzed. Activity-densities
from individual carabid species that accounted for >5% of the total trap catch were also
analyzed. All data were normalized with a log(x+1) transformation.

Species richness within the entire plot, within the crop area, and within the
treatment strips was analyzed. Shannon Weaver’s index (I-I’) was used to assess species
diversity. Species diversity (H’) is a measure of uncertainty for species within the
community (Hayek and Buzas 1997). When more species are present and the individuals
are more evenly spread divided across these species, the value for H’ will be higher than
for fewer species or a more uneven distribution (Hayek and Buzas 1997). Shannon
Weaver’s indices (H’) and the total number of species captured within the refuge or
control strips, within the crop areas, or within in the entire plot were used to access
refuge, insecticide, and reﬁrge*insecticide effects on species diversity and species
richness. Treatment effects on onion harvest weights and numbers within the crop areas

were also determined.

RESULTS AND DISCUSSION
1999 field study.

Signiﬁcantly more carabids were captured in the grassy border plots than in the
full-enclosure or partial-enclosure plots (p<0.05). However, the total number of carabids
captured in plots that had sides open to the grassy ﬁeld border were not signiﬁcantly
different from plots that were fully enclosed (p>0.05) (Table 3) (Figure 7). At the species

level, there were signiﬁcant differences within the ﬁve carabid species tested (p<0.05)

49

(Figure 8). Pterostichus melanarius (Illiger), Poecilus chalcites (Say), and Harpalus
pennsylvanicus (DeGeer) were more abundant in the grassy ﬁeld border (p<0.05) (Figure
8). There were no signiﬁcant differences in the mean activity-densities between full-
enclosure and partial-enclosure plots for Bembidion quadrimaculatum L., P. melanarius,
P. chalcites, H. pennsylvanicus, and Amara aenea (DeG.) (p>0.05) (Figure 8). The mean
number of carabids captured per plot was the highest in the grassy border plots compared
to onion plots for all the species tested except B. quadrimaculatum (Figure 8). Larger
beetles such as P. melanarius, P. chalcites, and H. pennsylvanicus are better dispersers
and would be expected to be common in the partial-enclosure plots, especially since they
were collected in the nearby grassy border. Conversely, the opposite was observed in the
much smaller species B. quadrimaculatum. In this species signiﬁcantly more beetles were
captured in the full-enclosure and partial-enclosure plots than in the grassy border
(p<0.05 (Figure 8). A longer sampling period and more replicates from grassy ﬁeld
borders from multiple ﬁelds would help to clarify the role of grassy borders in
contributing to in-ﬁeld carabid communities.

Established grassy refuges within the ﬁeld.

Newly established grassy refuges. A total of 6,194 carabids representing 25
species was captured during the 2000 trapping period (Table 4). The total catch of all
carabids per trap within the treatment strips was not signiﬁcantly affected by the presence
of reﬁrge vegetation (p>0.05) (Table 7) (Figure 9). Anisodactylus sanctaecrusis (F.), P.
melanarius, A. aenea, Stenolophus comma (F.), P. chalcites, B. quadrimaculatum,
Elaphropus anceps (LeC.), Stenolophus ochrapezus (Say), and Poecilus Iucablandis

(Say) each accounted for >5% of the total catch. However, P. melanarius was the only

50

species with a signiﬁcantly greater activity-density per plot and per trap in the refuge
strips than in the onion control strips (p<0.05) (Table 8) (Figure 10B). The total numbers
of E. anceps captured was signiﬁcantly higher in the onion control strip habitat than in
the refuge strips (p<0.05) (Figure 10B). Carrnona and Landis (1999) also found P.
melanarius to have a greater activity-density in newly established refuge strips than in the
crop area (com). This very large and mobile species can disperse 2-90 m/day (Wallin and
Eckbom 1988). Because of its great dispersal rate and freedom of movement for beetles
between treatment and crop in this experimental design, the greater P. melanarius
numbers in the refuge strip appears to be due to a preference for this habitat.

The combined per trap catch for all carabids within the crop areas adjacent to
refuge habitats was higher, however, it was not signiﬁcant (p>0.05) (Table 6) (Figure 9).
Trap catches for the common carabid species captured within the adjacent crop area were
signiﬁcantly affected by the presence of a refuge strip (p<0.05) (Table 8). Activity-
density for P. chalcites was signiﬁcantly higher in crop areas adjacent to refuges than in
the crop areas adjacent to control strips (p<0.05) (Figure 10A).

The combined activity-density of all carabids captured per trap within the entire
plot (carabids captured in the treatment strips plus those captured within the crop areas)
was not signiﬁcantly affected by the presence of the refuge vegetation (p>0.05) (Table 5)
(Figure 9). The trap catch for E. anceps was signiﬁcantly lower in the control treated
plots than in the refuge treated plots (p<0.05) (Figure 10C). P. melanarius and S.

ochropezus were higher in the refuge treated systems, however, it was not signiﬁcant

(p>.05) (Figure 10C).

51

When looking at the seasonal carabid activity within the adjacent crop areas and
within the entire plot, there are no signiﬁcant differences between the refuge strips or the
onion control strips (p>0.05) (Figure 11A,C). However, this was not the case for trap
catches within the refuge strips or control strips. Signiﬁcantly more beetles were captured
in the refuge strips around 1 June 2000 than in the onion control strips (Figure 11B).
Because the refuges were established in the spring of 2000, it is hard to interpret the
differences in activity-densities observed early in the season.

Pitfall trap data needs to be interpreted with caution because of unknown trapping
efficiencies and uncontrolled migration of insects across the landscape (Greenslade 1964,
Southwood 1966, Luff 197 5). In 2000 there were no physical barriers used to separate the
treatment areas. For trapping areas that had signiﬁcantly higher beetle catches, it is not
clear what caused the increased catch. Gist and Crossley (1975) found estimates made
with pitfall trapping showed good agreement with hand sorting techniques. The
experiment in 2001 controlled for migration of carabids between plots and the results
ﬁ'om that experiment will help in determining the overall effects observed in the activity-
densities of the species tested in 2000.

Insecticide and refuge habitat effects on predator populations. A total of 2,91 l
carabids representing 25 species was captured in pitfall traps in 2001 (Table 4). A. aenea,
A. sanctaecrucis, B. quadrimaculatum, E. anceps, Harpalus aﬂinis (Schr.), P. chalcites,
P. melanarius, and S. comma each accounted for >5% of the total catch. Seasonal mean
carabids captured per trap within the treatment strips ranged from 6-10 beetles per trap,

while trap catches within the adjacent crop areas ranged ﬁ'om 9-18 beetles per trap (Table

52

13). The most beetles captured per trap was in traps located in crop areas treated with
cyromazine and adjacent to a refuge strip.

The number of carabids captured per trap within the crop areas was signiﬁcantly
higher with the presence of a refuge strip than for plots without an adjacent refuge strip
(p<0.05) but was not affected by the insecticide treatments (p>0.05) (Table 10) (Figure
12A—B). Both the refuge treatment and the insecticide treatment affected the trap catch.
More beetles were captured in the crop areas treated with cyromazine than crop areas
treated with chlorpyrifos, however, it was not signiﬁcant (p>0.05) (Figure 12B). P.
chalcites, H. aﬁinis, and A. aenea per trap catches were higher in the crop areas adjacent
to refuge strips than onion control strips (p<0.05) (Figure 13A). The species where catch
within the adjacent crop area was affected by insecticide included E. anceps and H.
aﬂinis (p<0.05); E. anceps trap catch in both the untreated and cyromazine treated crop
areas was signiﬁcantly higher than in the chlorpyrifos treated areas and there was no
difference in catch between the untreated or cyromazine treated onions (p<0.05) (Figure
15A). H. afﬁnis was signiﬁcantly higher in the cyromazine treated crop area than in the
untreated crop area, however, trap catch was not signiﬁcantly different than the
chlorpyrifos treated crop area Q)<0.05) (Figure 15A).

The activity-density of carabids within refuge strips and onion control strips were
not signiﬁcantly affected by the presence of a refuge strip or by the application of
insecticides (p>0.05) (Table 11) (Figure 12A-B). At the species level, trap catches for P.
melanarius were signiﬁcantly higher within the refuge strips than in the onion control
strips (p<0.05) (Table 12) (Figure 138). The number of P. melanarius captured per trap

within the refuge treatments was unaffected by the insecticide treatment (p>0.05) (Figure

53

15B). A. aenea was the only species captured within the refuge strips affected by the
treated adjacent crop area (p<0.05) (Table 12) (Figure 158). Signiﬁcantly more beetles
were captured within the reﬁrge strips that were adjacent to the untreated (control) crop
areas than in refuge strips adjacent to chlorpyrifos treated areas (p<0.05) (Table 12).

The total number of beetles captured within an entire plot containing a refuge
strip was higher than in plots having an onion control strip but the difference was not
statistically signiﬁcant (p=0.07) (Table 9) (Figure 12A). Chlorpyrifos appeared to
reduced the number of carabids captured per trap within entire plots when compared to
catches in plots containing untreated or cyromazine treated cr0p areas, however, the
differences were not signiﬁcant (p>0.05) (Figure 12B). The activity-densities for H.
aﬂinis, A. aenea, A. sanctaecrucis, and P. chalcites were signiﬁcantly higher in plots
containing refuge strips than in plots with onion control strips (p<0.05) (Table 12)
(Figure 13C). Fewer E. anceps were captured per trap within plots where the crop areas
were treated with chlorpyrifos than in cyromazine treated or untreated (control) plots
(p<0.05) (Figure 15C). B. quadrimaculatum was also affected by the insecticide
treatment. Fewer beetles were captured in chlorpyrifos treated plots than in untreated
plots, however, it was not signiﬁcantly lower than cyromazine treated plots (p<0.05)
(Figure 15C).

The total number of carabids captured over the entire season within crop areas
and within entire plots were signiﬁcantly different between plots treated with refuge
strips or plots treated with onion control strips (p<0.05) (Figure 14A,C). During the
month of August, signiﬁcantly more beetles were captured within the crop areas adjacent

to refuge strips than in crop areas adjacent to onion control strips (p<0.05). In general,

54

activity-densities of captured carabids were higher throughout the entire trapping period,
but this is not the case when comparing trap catches within refuge strips. Trap catches
were signiﬁcantly higher within the refuge strips at the beginning of the season and then
numbers start to decline (Figure 148). This same trend was also observed in 2000 (Figure
11B). Although there were differences observed between insecticide treatments, no
general trends or patterns could be concluded when examining the trap catches at
different times during the trapping period (Figure 16A-C). Signiﬁcantly more beetles
were captured at the beginning of August within plots containing cyromazine treated crop
areas than in untreated or chlorpyrifos treated plots (p<0.05) (Figure 16C). P. melanarius
and B. quadrimaculatum were the only two species that exhibited differences at speciﬁc
trap periods during the 2001 ﬁeld season. B. quadrimaculatum activity-density was
generally higher within the onion control strip for almost the entire season (Figure 17),
while P. melanarius activity-density was generally greater in systems that contained
refuge strips (Figure 18).

Entire plots containing refuge strips had signiﬁcantly more carabid species
captured than systems containing onion control strips (p<0.05) (Table 14). Insecticide
treatments had no effect on the total number of species captured (p>0.05). However, there
was signiﬁcant interaction between refuge and insecticide treatments. Trap catches from
the entire plot comprised of refuge strips and crop areas treated with cyromazine had
signiﬁcantly more species than systems comprised of onion control strips and crop areas
treated with chlorpyrifos (p<0.05) (Table 14). There were no signiﬁcant differences
observed between the other treatment combinations (p>0.05). Reﬁrge strips exhibited

signiﬁcantly greater diversity (greater H’ value) than the onion control strips (p<0.05)

55

(Table 15); there were no other differences observed for insecticide effects or interaction
between refuge and insecticide effects (p>0.05).

Both refuge and insecticide treatments signiﬁcantly affected the mean number of
onions and harvested weight (p<0.05) (Table 16). Number of small (<4 cm diam.) and
medium (4-10 cm diam.) sized onions were higher in plots with onion control strips than
in plots with refuge strips (p<0.05) (Figure 19A). Harvested weights were only
marginally higher (p=0.09) for small sized onions in plots containing onion control strips
(Figure 19B). Plots treated with chlorpyrifos had signiﬁcantly higher onion numbers and
weights for small and medium sized onions than in plots cyromazine or untreated
(control) plots and the total number of onions harvested were also signiﬁcantly higher in
the chlorpyrifos treated plots (p<0.05) (Figure 20A-B). There were no differences
observed between the untreated (control) or cyromazine treated plots (p<0.05) (Table 16).
In a ﬁeld study comparing cyromazine, chlorpyrifos and untreated onions, no signiﬁcant
onion maggot damage was present at the MSU Muck Research Farm during 2001
(McComack et al. 2001).

My results indicate that carabid populations can be manipulated with refuge strip
habitats and certain species of carabids (A. aenea and E. anceps) can be conserved with
the use of a low spectrum insecticide like cyromazine. It is well documented that carabids
are very sensitive to disturbances in the environment and are easily affected by
cultivation practices (Kromp 1999). It has been shown that refuge strips can increase the
numbers and activity of carabids and other biological control agents in corn and soybeans
(Carmona 1998, Menalled and Landis 1997, Lee et al. 2001). Critchely (1972) showed

carabids that burrowed into soil treated with insecticides were more susceptible than

56

those that didn’t burrow. Brust et al. (1985) correlated an increase in cutworrn-damage to
com plants with a decrease in predator densities in insecticide treated plots. Application
of an insecticide only affected a couple of species captured in the onion ﬁeld (A. aenea
and E. anceps) but harvest weights were higher in chlorpyrifos treated plots. Future
studies that would address the issue of plant damage or stand loss (% onion damage)
during the growing season would help explain this relationship. However, in this ﬁeld
study, if the onion maggot population at the MSU Muck Soils Research Farm was high, I
would expect biological control to be reduced due in chlorpyrifos treated plots to high
insecticide activity. This does not appear to be the case. I saw greater beetle numbers and
lower harvest weights and onion numbers in plots treated with refuges than in plots
without refuge strips.

Michigan onion growers must be able to effectively and economically control
onion maggot to remain in business. Registration of new and effective chemicals is just
one part of this task. There is a need for an effective, safe, and environmentally sound
pest management system that includes all aspects of integrated pest management
(chemical, biological, cultural, etc.), so growers can prevent future development of
insecticide resistance and reduce the potential impact of onion maggot on onion yields.
Currently, there are few management options available to growers. Development of new
control tactics and increased effectiveness of biological control agents such as carabids
will beneﬁt growers by increasing the stability of the onion production system while
reducing the risks associated with crop loss. Conserving natural enemies natural enemies
in an agroecosystem is an effective way to increase biological control in the targeted

system (Hull and Beers 1985). As the role conservation biological control in an onion

57

agroecosystem is better deﬁned, the use of carabids for control of onion maggot may

become a crucial component to onion pest management programs.

58

 

 

 

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Figure 4. Plot layout for evaluating the effects of a grassy ﬁeld edge on carabid beetle
populations in 1999 at the MSU Muck Soils Research Farm in Clinton County, MI. A)

Full-enclosure plot, B) partial-enclosure plot, and C) a grassy ﬁeld edge.

59

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Figure 5. Plot layout for evaluating the effects of newly established refuge strips on
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60

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refuge strips, insecticide treatments (A-untreated, B-cyromazine, and C-chlorpyrifos) and
interaction between refuge and insecticide on carabid beetle populations at the MSU
Muck Soils Research Farm, Clinton County MI in 2001. Pitfall traps were used to

monitor beetle activity-densities.

61

Table 3. Analysis of variance for activity-densities of common carabid species captured in

enclosure plots at the Michigan State University Muck Soils Research Farm, Clinton County

MI in 1999. Tests for enclosure effects on carabid activity-densities are shown.

 

 

Species d.f. F P
Amara aenea 2,6 73.03 <0.0001
Harpalus pennsylvanicus 2,6 9.77 0.013
Poecilus aha/cites 2,6 25.51 0.0012
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62

 

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Mean number of carabids captured during the trapping period are shown. Means with a

different letter are signiﬁcantly different: Fisher’s protected LSD test, (P<0.05).

63

 

 

 

 

 

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Table 5. Analysis of variance for traps catches within the entire plot at the MSU Muck Soils

Research Farm, Clinton Co MI in 2000.

 

 

Source d.f. SS MS F p-value
Total 287 9.25
Block 3 1 .569 0.523
Refuge Effect 1 0.018 0.018 0.15 0.72
Experimental Error 3 0.353 0.118

Observational Error 280 7.31 0.026

 

68

Table 6. Analysis of variance for trap catches within the crop areas adjacent to refuge or

control strips at the MSU Muck Soils Research Farm, Clinton Co MI in 2000.

 

 

Source d.f. SS MS F p-value
Total 191 5.981
Block 3 1.181 0.394
Refuge Effect 1 0.131 0.131 1.02 0.39
Experimental Error 3 0.385 0.128

Observational Error 184 4.284 0.023

 

69

 

Table 7. Analysis of variance for traps within reﬁJge or control strips at the MSU Muck

Soils Research Farm, Clinton Co MI in 2000.

 

 

Source d.f. SS MS F p-value
Total 95 3.243
Block 3 0.419 0.14
Refuge Effect 1 0.078 0.078 0.81 0.44
Experimental Error 3 0.291 0.097
Observational Error 88 2.455 0.028

 

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[Dwrmu refugestrips lWith name 5mg]

- Figure 9. Seasonal activity-density for all carabid beetles captured per trap during the 2000
ﬁeld season. *Means within a pitfall trap location are statistically signiﬁcant: Fisher’s

protected LSD test, (P<0.05).

74

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Figure 10. Grassy refuge effects on carabid activity-densities of common carabid species
captured within an onion ﬁeld in 2000. Mean number of carabids captured within a location
are shown: A) within the crop area, B) within the refuge strip or onion control strip, and C)
within the entire plot. *Means within a species are statistically signiﬁcant: Fisher’s protected

LSD test, (P<0.05).

76

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Figure 1 l. Grassy refuge effects on activity-densities of carabids captured throughout the

2000 trapping period (30 May-18 September) within an onion ﬁeld. Mean number of carabids

captured per trap date: A) within adjacent crop area, B) within the reﬁige or onion control

strips, and C) within the entire plot. *Means within a trapping period are statistically signiﬁcant:

Fisher’s protected LSD test, (P<0.05).

78

Table 9. Analysis of variance for traps catches within the entire plot at the MSU Muck Soils

Research Farm, Clinton Co MI in 2001.

 

 

Source d.f. 88 MS F p-value
Total 23 959.53
Block 3 609.27 203.09
Refuge 1 152.09 152.09 7.74 0.07
Block*Refuge 3 58.95 19.65
Insecticide 2 30.12 15.06 2.06 0.17
Refuge*|nsecticide 2 21.21 10.61 1.45 0.27
Error 12 87.88 7.32

 

79

Table 10. Analysis of variance for trap catches within the crop areas adjacent to reﬁige or

control strips at the MSU Muck Soils Research Farm, Clinton Co MI in 2001.

 

 

Source d.f. SS MS F p-value
Total 23 1498
Block 3 884.27 294.76
Refuge 1 373.08 373.08 32.1 1 0.01
Block*Refuge 3 34.85 1 1.62
Insecticide 2 41.06 20.53 1 .77 0.21
Refuge*lnsecticide 2 25.33 12.67 1 .09 0.37
Error 12 139.36 11.61

 

8O

Table 1 1. Analysis of variance for traps within refuge or control strips at the MSU Muck

Soils Research Farm, Clinton Co MI in 2001.

 

 

Source d.f. SS MS F p-value

Total 23 546.83

Block 3 226.65 75.55

Refuge 1 2.67 2.67 0.04 0.86
Block*Refuge 3 205.69 68.56

Insecticide 2 24.54 12.27 2.02 0.18
Refuge*lnsecticide 2 14.47 7.23 1 .19 0.34
Error 12 72.82 6.07

 

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Table 13.Effects of refuge treatment and insecticide on seasonal mean carabids/trap in 2001.

 

 

Trap Location Treatement carabids/trap i SE
Treatment strip Control Strip + untreated 10.00 i 1.35
Control Strip + cyromazine 7.13 i 1.35
Control Strip + chlorpyrifos 6.13 i 1.35
Refuge Strip + untreated 7.19 :1: 1.35
Refuge Strip + cyromazine 7.94 i 1.35
Refuge Strip + chlorpyrifos 6.13 i 1.35
Adjacent crop areas Control Strip + untreated 11.08 i 1.79
Control Strip + cyromazine 8.88 i 1.79
Control Strip + chlorpyrifos 5.83 i 1.79
Refuge Strip + untreated 14.25 i 1.79
Refuge Strip + cyromazine 18.06 1: 1.79
Refuge Strip + chlorpyrifos 13.88 i 1.79
Entire plot Control Strip + untreated 9.35 i 1.63
Control Strip + cyromazine 7.60 i 1.63
Control Strip + chlorpyrifos 5.81 i 1.63
Refuge Strip + untreated 11.90 i 1.63
Refuge Strip + cyromazine 14.69 i 1.63
Refuge Strip + chlorpyrifos 11.29 i 1.63

 

87

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8

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Plot Area Strip
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Seasonal mean carabids/trap t SE

 

 

 

 

 

 

Entire Adjacent Crop Treatment
Plot Area Strip

Pitfall Trap location

 

B)

Figure 12. Seasonal mean carabid beetles per trap captured during 2001. A) Effect of

refuge strip habitats (*means within a location are statistically signiﬁcant: Fisher’s protected

LSD test, P<0.05), and B) insecticide treatments on carabid beetles captured in the total plot,

within the crop areas, and within the refuge strips (different letters denote signiﬁcant differ-

ences within a location, Fisher’s LSD tests, P<0.05). ns=no signiﬁcant differences.

88

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Figure 13. Grassy refuge effects on activity-densities of common carabid species captured
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2001 trapping period (6 June - 17 September). Mean number of carabids captured per trap
date: A) within adjacent crop area, B) within the refuge or onion control strips, and C)
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Figure 15. Insecticide effects on activity-densities of common carabid species captured
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A) within adjacent crop area, B) within refuge or onion control ships, and C) within the
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protected LSD test, (P<0.05).

96

 

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97

 

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affected by the presence of refuge or onion control strip during the 2001 ﬁeld season.

*Means within a nap date are statistically signiﬁcant: Fisher’s protected LSD test, (P<0.05).

98

 

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Table 16. Analysis of variance of onion harvest weights and number of onions 5 in 2001.

Tests for refuge, insecticide, and refuge*insecticide effects are shown.

 

 

Bulb Category Effect d.f. F P
Small weight refuge 1,12 6.01 0.09
(<4 cm)

insecticide 2,12 5.88 0.02

refuge*insecticide 2,12 0.65 0.54
Small count refuge 1,12 10.01 0.05
(<4 cm)

insecticide 2,12 4.45 0.04

refuge*insecticide 2,12 0.38 0.69
Medium weight refuge 1,12 2.59 0.21
(4-10 cm)

insecticide 2,12 3.03 0.09

refuge*insecticide 2,12 1.21 0.33
Medium count refuge 1,12 5.09 0.11
(4-10 cm)

insecticide 2,12 3.81 0.05

refuge*insecticide 2,12 1.21 0.33
Large weight refuge 1,12 0.07 0.81
(>10 cm)

insecticide 2,12 0.46 0.64

refuge*insecticide 2,12 2.20 0.15
Large count refuge 1,12 0.01 0.91
(>10 cm)

insecticide 2,12 0.43 0.66

refuge*insecticide 2,12 2.31 0.14

105

Table 16 (cont’d).

Total weight

Total count

refuge

insecticide
refuge*insecticide
refuge

insecticide

refuge*insecticide

1,12
2,12
2,12
1,12
2,12

2,12

0.75

1.67

1.78

4.00

3.91

1.57

0.45

0.23

0.21

0.14

0.05

0.25

 

106

0)
O
O

A) Number of onions

:“5’

M
8

Mean number of onlons t SE
8 8

OI
O

 

(<4) (410) (>10)

01
O

B) Harvest weight

Mean harvest welght t SE (kg)
—I -A N N (a) 00 h A
O 01 O 01 O 01 O 01

0|

 

Small Medium Large Total
(<4) (4-10) (>10)
Bulb diameter (cm)

 

IDWithout refuge strips IWith refuge stripsl

 

Figure 19. Grassy refuge or control strip effects on onion yield in 2001. A) Number of
onions and B) harvest weight. *Mean onion weights are signiﬁcantly different: Fisher’s

protected LSD test (P<0.05).

107

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

In 350 A) Number of onions a
cg 300 7
g 250 Z
'2 200 /
5 150 . %
2 . %
21m /
5 50 b b " , Z
Small Medium Large Total
(<4) (4-10) (>10)
B) Harvest weight I

 

01
O

 

A
C

 

 

(a)
O

 

N
O

 

 

Mean onion weight 1 SE (kg)

 

 

 

 

 

 

 
   

 

b b 3
Small Medium Large
(<4) (4-10) (>10)

Bulb diameter (cm)
[D untreated I cyromazine chlorpyrifos ]

 

 

Figure 20. Insecticide treatment effects on onion yield in 2001. A) Number of onions and
B) harvest weight. *Mean onion weights with different letters are signiﬁcantly different:

Fisher’s protected LSD test (P<0.05).

108

CONCLUSIONS

Despite its economic importance, management options for this pest are limited. Heavy
reliance on a single broad-spectrum insecticide by growers generates a cause for concern.
Chlorpyrifos has been withdrawn from use in all urban markets and ﬁom minor uses in
other crops. Even if use on onions is not restricted, development of resistance by onion
maggot to chlorpyrifos is a concern. Conservation and augmentation of onion maggot
natural enemies requires an integrative approach to onion maggot control. The
incorporation of narrow spectrum insecticides can help conserve existing predator
populations (Graﬁus et al. 1997), while preservation of refuge habitats such as ﬁeld
margins and hedgerows (Menalled and Landis 1997) could potentially augment carabid
communities in onion ﬁelds, thus increasing the importance of biological control.
Integrating multiple aspects of onion maggot control will provide a more efﬁcient and
sustainable approach to managing onion maggot populations in Michigan onions.
Carabids have signiﬁcant potential for biological control of onion maggot. In ﬁeld
obServations, high activity-densities for P. chalcites, P. Iucablandis, and P. melanarius
appear to coincide temporally with onion maggot oviposition and larval development
(Figure 3). In my experiments I was successful at conserving and augmenting carabid
populations in the ﬁeld. However, this is not enough to merit them as a good biological
control agents of onion maggot. Research focused on describing the species that
contribute most to the biological control of onion maggot is needed. Finch et al. (1986)
found in a related prey species (D. radicum) that beetle size was correlated with prey
size; medium-sized beetles consumed more eggs than larger beetles. If the important
carabid species are egg predators, chances are it will be small in size (i.e such as the
predator B. quadrimaculatum). In my ﬁeld experiments, larger beetles (i.e. P. melanarius
and P. chalcites) were more affected by the presence of refuge strips than smaller species

(i.e. B. quadrimalucatum and E. anceps). Deﬁning the role of immature carabids is also

109

important to the understanding of their importance in controlling various pests in the
ﬁeld. The next step would be to incorporate refuges in commercial farms and evaluating
onion maggot control in the ﬁeld.

Though the integrative approach to managing onion maggot is much needed in
Michigan, growers are in need of new and immediate forms of control that would bring
onion maggot populations below some economic threshold. Creating a more stable
system with the use of stable habitats like refuge strips and increasing the abundance of

generalist predators like carabids is just one part of the picture.

110

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122

APPENDIX 1
Record of Deposition of Voucher Specimens’
The specimens listed on the following sheet(s) have been deposited in the named museum(s) as
samples of those species or other taxa, which were used in this research. Voucher recognition
labels bearing the Voucher No. have been attached or included in ﬂuid-preserved specimens.
Voucher No.2 2002-02
Title of thesis or dissertation (or other research projects):

increasing biological control of onion maggot, Delia antiqua (Meigen), with integrative approaches
and methods.

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

lnvestigator’s Name(s) (typed)
Brian P. McCornaLck

 

 

Date 22 March 2002

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

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

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

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

123

Appendix 1.1

Voucher Specimen Data

 

Page 1 of 3 Pages

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124

Appendix 1.1

Voucher Specimen Data

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125

Appendix 1.1

Voucher Specimen Data

 

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126

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