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ABSTRACT

Bembidion guadrimaculatum
PREDATION ON THE

EGGS OF THE ONION MAGGOT
(Delia antiqua (Meigen))
By

Frederick W. Warner

Bembidion cmadrimaculatum L. is a small (2.7-3.8 mm), diurnal ground beetle
that preys on the eggs of the onion maggot, Delia antiqua (Meigen) and other
arthropods. This study investigates the role these beetles can play in the Michigan
onion agroecosystem in the absence of insecticides. In addition, the relative
impact of pesticides on Q. quadrimaculatum and onion maggot eggs and adults was
examined.

Q. quadrimaculatum overwinter as adults in the soil and under plant debris.

 

They become active in the spring and peak activity occurs in June, with a second
peak in August or September. These activity peaks correspond roughly with spring
and fall generation Q. m egg laying.

_B_. quadrimaculatum adults can consume up to 25 onion maggot eggs per day
in the laboratory. These beetles forage actively on the soil surface but are not
very effective predators if eggs are laid in the soil. In a field experiment, Q.
(madrimaculatum adults reduced Q. m larval numbers by 5796 compared to the
controls (absence of beetles).

_B_. quadrimaculatum adults are highly intolerant to foliar insecticides and are
almost completely absent from commercial fields. Concentrations sufficient to
kill onion maggot eggs and adults in the laboratory, killed these carabids quickly.
However, soil insecticides do not appear to be very toxic to the adults in the field.

In conclusion, _B_. quadrimaculatum adults presently appear to play no role in
reducing onion maggot numbers in commercial fields. However, if allowed to reach

natural population densities, they are capable of reducing maggot numbers.

Bembidion quadrimaculatum L.
PREDATION ON THE
EGGS OF THE ONION MAGGOT
(Delia antiqua (Meigen))

By

Frederick W. Warner

A THESIS

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

MASTER OF SCIENCE
Department of Entomology

1986

To my parents,
for their financial and moral support
and to my wife, Glenys, and son, Steve,
for backing all of my endeavors

ii

ACKNOWLEDGEMENTS

I would first and foremost like to thank my major professor, Dr. Edward
Grafius, for his support, guidance and encouragement during my study. I'd also like
to thank my committee members, Dr. Dean Haynes, Dr. Richard Merritt and Dr.
Frederick Stehr for their assistance. Special thanks also to Dr. James Bath, the
department chairman, for overlooking a department that made this a rewarding and
enjoyable experience.

Thanks also to the members of the prestigious Grafius empire: Ms. Elizabeth
Morrow, Mr. Tony May, Mr. Dave Prokrym, Ms. Dana Hayakawa, Mr. Mark Otto,
Ms. Martha Otto, Mr. Leeroi Panella, Mr. Ralph Fax and Ms. Lisa Harris. Thanks
for all the good times and assistance. Keep up the good work. I am especially
indebted to Ms. Melinda Mitchell and Mrs. Susan Jawitz for their time and effort
on this project.

I would also like to acknowledge Dr. James Miller and his staff for their
consideration and for kindly supplying onion maggot eggs, often on short notice.
Thanks also to Dr. George Bird, Mr. John Davenport and other nematologists for
employing me during my undergraduate days. Appreciation is also extended to Mr.
Tom Ellis, for occasional good words, and to my fellow graduate students and other
members of the faculty and staff for always making me feel welcome and at home.

My very best friends, Mr. Jeff Milbrath, Mr. Bob Hanley, Mr. Dave George
and Mr. Craig Krisan also deserve thanks for many good times and those to come.
If it wasn't for these guys, I probably would have completed this thing in 1983. But,

it was always worth it.
iii

Thanks also to Mr. Ron Gnagey for his assistance and to the Michigan Onion
Commodity Committee, Mr. Dave Brink, Mr. Peter Brink and Mr. Peter Plaisier for
their support.

I would also like to thank Becky Mather and Susan Battenfield for editing and

typing parts of this manuscript.

iv

TABLE OF CONTENTS

 

ACKNOWLEDGEMENTS .......................................... iii
LIST OF TABLES ................................................ vii
LIST OF FIGURES .............................................. viii
INTRODUCTION . . ............. . ................................. 1
RESEARCH OBJECTIVES ......................................... 4
LITERATURE REVIEW ............................................ 5
Onion Maggot ......................... . ....................... 5
Ground Beetles ........ ' ....... . .............. . .......... . ...... 7
The Genus Bembidion ............................ . ..... . . ..... 10
Bembidion quadrimaculatum ................... . ............... 13
PitfallTraps ......... . ....... . ................ 16

ACTIVITY OF BEMBIDION QUADRIMACULATUM L. AND PREDATION
ON EGGS OF THE ONION MAGGOT, DELIA ANTIOUA (MEIGEN) - - - - - 18

 

Abstract“ ................ .......... lg
Introduction .......................... . ...................... 1 9
Materials and Methods ........................................ 19
Results and Discussion . ....................................... 24
Acknowledgements . ........... . .............................. 41
ReferencesCitedHHHHHH-H' .......... . ................. . (,2

EFFECTS OF INSECTICIDES ON BEMBIDION QiJADRIMACULATUM L.

 

 

AND DELIA ANTIQUA (MEIGEN) EGGS AND ADULTS ------- - - - - as
Abstract .......... . ......................................... 45
Introduction . ..................... . .......................... 45
Materials and Methods .............. . . . . . . ..... . .............. 47

Results and Discussion oooooooooooooooooooooooooooooooooooooooo 53

Acknowledgements ......... . . . . .......... . ................... 67
References Cited .......................................... . . . 68
CONCLUSION'------ ....................................... 70
Summary-"on”- ........... ....... . ......... . ..... 70

Augmenting naturally occurring E. mdrimaculatum
pOPUIationS000000000 000000000000 0.....0000... ................ 71

Bembidion quadrimaculatum and other carabids as

 

biological control agents 0 0 0 0 0 . . . 0 0 0 0 0 . . 0 0 0 .................... 74
APPENDIX............... ............... 0 oooooo 0 ............... 76
REFERENCES CITED oooooooooooo 0 ....... 0 oooooooo 0 0 0 . 0 ...... . 0 0 . 83

vi

.‘l Ii 1 I I III ll [ {ll I‘ll [.[(II\ (II (I ll

LIST OF TABLES

Activity of Bembidion quadrimaculatum L. and Predation on Eggs
of the Onion Maggot, Delia antklua (Meigen)

Table I. Number of onion maggot eggs and first instar larvae
consumed daily by Bembidion quadrimaculatum adults
at constant temperatures of 15, 20, 25 C over 60
days ooooooooooooooooooooooooooooooooooooooooooooooooooooooo 26

 

Table 2. Foraging ability of Bembidion quadrimaculatum adults ----------- 29

Table 3. Percent survival of onion maggot larvae in the absence
of predation in field experiments conducted at the
M.S.U. Muck Soils Experimental Farm, 1983 - - - . - . . - ------------ 36

Table 4. Egg data obtained from sampling cut and sprouted cull
onions from 2 commercial fields in Grant, Michigan, 1983 - - ------ 40

Effects of Insecticides on Bembidion quadrimaculatum L. and Delia
antigg (Meigen) Eggs and Achilts

Table 1. Treatment levels for onion production pesticides
applied to Bembidion quadrimaculatum in laboratory
studies .................................................... 51

Table 2. Treatment levels for onion production pesticides
applied to Delia antiqua eggs and adults in laboratory
Studies 000.00.00.0000000000000..00....0..0.000.00..0 ....... 52

Table 3. Mean numbers per replication of Bembidion quadrimaculatum
adults trapped in plots sprayed with diazinon and
fenvalerate’ 1982 oooooooooooo 0 oooooooooooooooooooooooooooooo 55

Table 4. I Mean numbers per replication of Bembidion quadrimaculatum
adults trapped in plots sprayed with diazinon and
fenvalerate, 1983 0..0..00...0.0000000000000000..0000. ....... 58

Table 5. Response levels and LC 50 values with 95%
confidence limites for all pesticide treatments
applied in the laboratory studies . 0 0 . . 0 0 . . . . ................... 60

Thesis Conclusions

Table 1. Pesticides utilized by commercial onion growers
known to be toxic to natural enemies of the onion
maggot, Delia antiqua (Meigen), in Michigan . - ------------------ 72

 

vii

LIST OF FIGURES

Thesis Introduction

Figure l. Conceptualization of the onion agroecosystem
showing levels of interaction within the object
of control and the monitored environment. Numbers
refer to footnotes in Appendix A (after Haynes
et al., 1980). Arrows highlight role of
Bembidion 5p. oooooooooooooooooooooooooooooooooooooooooooooo 12

Activity of Bembidion quadrimaculatum L. and Predation on Eggs
of the Onion Maggot, Delia anticya (Meigen)

Figure 1. Proportion of attacks (number of times attacked/75)
by Bembidion quadrimaculatum adults on 6 food items
inapreference study 00000.00....00000000000000. ............. 25

Figure 2. Seasonal trap catch of Bembidion quadrimaculatum
adults in an onion plot located at the M.S.U.
Muck Soils Experimental farm, I982 - . ~ - - - - - - - - - - -------------- 30

Figure 3. Seasonal trap catch of Bembidion quadrimaculatum
adults in an onion plot located at the M.S.U.
Muck Soils Experimental farm, I983 - - - - - - - - ----- - ------------- 31

Figure 4. Number of Bembidion quadrimaculatum adults trapped
per day during 1982 and 1983 in an onion plot
located at the M.S.U. Muck Soil Experimental
farm ..... 0 oooooooooooooooooooooooooooooooooooooooooooooooo 33

Figure 5. Proportion of Bembidion quadrimaculatum adults
active at various temperatures ..... 0 0 . 0 . 0 . 0 0 oooooo 0 ooooooooooo 34

Figure 6. Relationship between the number of Bembidion
‘ (madrimaculatum adults and the number of
survival Delia antiqua larvae (with 95%
confidence interval) per enclosure in the
second of four field experiments, 1983 - - - ---------------------- 37

 

Figure 7. Relationship between the number of Bembidion
quadrimaculatum adults and the number of
surviving Delia antiqua larvae (with 95% confidence
interval) per enclosure in the third of four
field experiments, 1983 0 0 . . . 0 0 0 0 ........ . .................... 38

viii

Effects of Insecticides on Bembidion quadrimaculatum L. and Delia
gm (Meigen) Eggs and Adults

Figure 1. Plot diagrams of large plot insecticide experiments
at the M.S.U. Muck Soils Experimental farm during
the summers of 1982 and 1983 . . . . . . oooooooooo . . . . oooooooooooo 49

Figure 2. Comparative numbers of Bembidion quadrimaculatum
adults trapped from July 13 to August 18, 1982
in plots treated with 2 soil insecticides
compared to an untreated plot . . . . . . . . . . . . . . . . oooooooooooooooo 56

Figure 3. Comparative numbers of Bembidion quadrimaculatum
adults trapped from July 16 to August 24, 1983 in
an untreated plot and a plot treated with
fonofos.. ..... ................. ..... .. ooooooooooooooooooooo 59

Figure 4. Ratio of LC 50 values obtained for Bembidion
quadrimaculatum, Delia antiqua eggs, Q
antigua field-collected adults and Q. antigua
laboratory-reared adults during laboratory
studies ................. ...... ........... ooooooooooooooo ...62

Figure 5. Log dose-probit mortality regressions for
Bembidion quadrimaculatum, Delia antim
eggs, Q. antigua field-collected adults and
Q. antigua laboratory-reared adults exposed
todiazinon ..... ....... .......... ....... .................... 6Q

Figure 6. Log dose-probit mortality regressions for _B_________embidion
quadrimaculatum, Delia antiqua eggs,_ D.a antigua
field-collected adults and Q. antigua laboratory-
reared adults exposed to fenvalerate - - - - - ~ - - - - - - - -------------- 65

Figure 7. Log dose-probit mortality regressions for Bembidion
quadrimaculatum, Delia antiqua eggs, Q. antigua
field-collected adults and Q. antigua laboratory-
reared adults exposed to naled .. . . . . .. . . . .. . . ............ . . . . .66

ix

INTRODUCTION

There has typically been a heavy reliance on chemicals for control of soil
insect pests (Harris et a1. 1981). Extreme measures have been taken to control the
onion maggot (Delia antiqua (Meigen)) in North America. As a result, the onion
maggot frequently indicates problems that probably will arise with other soil insect
species (Harris et al. 1981). '

'Insecticides have been used to control the onion maggot since the 1930's
(Kendall 1932). Until the 1950's, however, 30-8096 control was typical (Harris et al.
1981). At that time (1950's), the development of the chlorinated hydrocarbon
complex (DDT, aldrin, heptachlor, dieldrin) revolutionized soil insect control.
Unfortunately for onion growers, the effectiveness of the cyclodiene insecticides
was short-lived. By the late 1950's, the onion maggot had become resistant to all
cyclodiene insecticides in the northern U.S. and Canada (Drew and Guyer 1958).
Resistance to these insecticides occurred in England in the late 1960's (Gostick,
Powell and Slough 1971).

Organophosphorus (OP) compounds were then employed to control the onion
maggot. These insecticides were very effective from 1960 until the early 1970's.
By 1972, the onion maggot had become somewhat resistant to all OP insecticides
and carbofuran (a carbamate) although the latter was rarely applied for maggot
control (Harris and Svec 1976). Resistance levels have continued to increase
(Harris et al. 1981). Due to these resistance problems, growers sprayed for adults
more frequently and at higher application rates. Some growers were applying 20
applications of parathion and diazinon during the growing season by 1975 (Harris et

1

2
al. 1981). Presently, moderate spray programs in Michigan consist of 7-10 sprays
during the growing season, even though foliar sprays are not effective in reducing
maggot damage (Warner and Grafius 1981, Whitfield 1981). Recently, the effects of
a post-harvest spray of naled for adults have been studied (Chambers 1984).

Future control of the onion maggot by the use of agrochemicals seems
precarious at best. The development of new soil insecticides aimed at onion
maggot control does not seem to be a primary objective of the pesticide industry
(Harris et al. 1981). Due to the high costs associated with pesticide production,
screening and registration, companies are interested in developing new products for
corn, cotton, small grains, soybeans and tobacco only (Matsumura 1983).
Therefore, it appears that future onion maggot control will be obtained with
limited or no chemical input. Future control will rely heavily on cultural practices
aimed at reducing pest populations and increasing the population of natural
enemies and/or on the use of non-insecticidal tactics such as sterile insect
releases.

The carabid, Bembidion quadrimaculatum L. was felt to be highly intolerant

 

to insecticides due to its extremely low numbers in commercial compared to
organic fields (Motyka and Edens 1984). Ground beetles, as a rule, are highly
intolerant to insecticides applied at normal concentrations (Freitag 1979).
However, insecticides are known to produce differential kills of ground beetles
when applied at equal concentrations (Mowat and Coaker 1967, Critchley 1972,
Tomlin 1975, Thiele 1977). For this reason, the relative toxicities of various
insecticides to ground beetles (as well as other predators and parasitoids) and
noxious insect species should be investigated. When this information is available,
sound management decisions can be made concerning chemical input into an

agroecosystem.

3

Predators, such as Q. quadrimaculatum, and parasitoids are less likely to
become tolerant to insecticides than pests. Because of this, a common
phenomenon associated with buildup of insecticide resistance by a pest is an
increase in damage in chemically treated plots as opposed to untreated areas
(Mowat and Coaker 1967, Chapman and Eckenrode 1973). This increase in damage
is usually correlated with a decrease in predator and parasitoid numbers in the
treated plots. Therefore, it appears that, unwarranted insecticide use can be
detrimental by destroying beneficial species.

The preservation of beneficial insect species should be a major concern when
implementing pest management spray programs. In the onion agroecosystem, _B_.
quadrimaculatum is felt to be a beneficial insect species although its role at this
time is not fully understood. These beetles are known to be predators on the eggs
of Q. antigua (Perron 1972, Drummond 1982). Therefore, management practices

aimed at increasing their abundance in onion fields should be advantageous.

RESEARCH OBJECTIVES

Study the feeding habits of Bembidion quadrimaculatum adults in the
laboratory.
Investigate the impact these carabids have on onion maggot larvae numbers
in the field.
Examine the relative impact of pesticides on Q. quadrimaculatum and onion

maggot eggs and adults.

LITERATURE REVIEW

Onion Maggot

The onion maggot, Delia (=Hylemya) antiqua (Meigen) is an important pest of
onions in Michigan as well as other parts of the United States and Canada. It has
been a major pest in onions for over 100 years (Fitch 1867). Annually, in Michigan,
crop loss due to the onion maggot is estimated to be 1-2096. Losses can be as high
as 95% if onions are left untreated or insecticides fail. This insect is only known to
attack Allium species, with the bulbing onion, Allium c_eQa I.., the preferred host
(Ellis and Eckenrode 1979).

There are three distinct generations of the onion maggot per year in
Michigan, although the generations do overlap (Carruthers 1979). It overwinters as
a pupa in the soil. As the soil warms in the spring, adults emerge. Fifty percent
emergence occurs at approximately 400 DD4.4°C (Eckenrode, Vea and~ Stone 1975,
Carruthers 1979, Whitfield 1981).

Newly emerged flies require a day to dry and harden (Carruthers 1981). A
preovipositional period follows and the flies forage. They are commonly found in
field borders visiting dandelions, Taraxacum officinale Weber (Baker 1927) or other
wild flowers (Carruthers 1981).

After the preovipositional period (about 10 days, 103 DD3.88°C’ Carruthers
1979), flies mate. Gravid females lay their eggs in the soil around the base of
onion plants, on the leaves, or in the leaf axils (Doane 1953, Workman 1958).
Females from this spring generation have the highest reproductive potential
(Perron and LaFrance 1961). In field cages in Quebec, the mean numbers of eggs

5

6
laid per female of each generation were 57.8, 36.2 and 24.3 respectively for the
three generations.

The placement of eggs, especially early in the growing season, is often
dictated by the presence of volunteer onions (onion bulbs left in the field after
harvest the previous fall that sprout and grow the next spring). These volunteer
onions attract onion maggot females (Whitfield 1981, Chambers 1984). Females
alight on the volunteers and lay their eggs on these sprouting onions or on nearby
seedlings. Cull onions were suggested as a trap crop in Wisconsin as early as 1924
(Dudley 1925). He felt large numbers of onion maggot larvae could be eliminated
by destroying these cull onions after maggots had infested them.

Onion maggot eggs require 50 003.88 to hatch (Carruthers 1979). After
eclosion, first instar larvae feed directly on onion tissue, usually initiating feeding
at the root zone. Positioning of the eggs adjacent to the host plant appears to be
extremely important because first instar larvae have a migration distance and
detection radius of only ca. 2.5 cm. (Drummond 1982). Drummond suggested that
60-80% larval mortality could be induced if the eggs could be dislodged from the
plant in some manner.

One onion seedling may not be sufficient to sustain a developing larva. One
maggot destroys an average of 28 small seedlings (onions in the loop stage with a
diameter at the soil surface of 1 mm.) before completing development (Workman
1958). The larger the onion, the more larvae it can support (Workman 1958,
Loosjes 1976, Carruthers 1979). One larva can sustain itself on an onion with a
diameter of 4-5 mm. (Workman 1958) and onion maggot adults actually prefer to
oviposit on onion plants with a stem diameter of 4-8 mm. and heights of 10 cm. or
more (Harris 1982). Larval population densities can be reduced up to 9596 by late
plantings of onions compared to early plantings, with or without insecticide

treatment (Chambers 1984).

7
Developmental times of the three instars are 37, 89 and 161 DD3 88’

respectively (Carruthers 1979). Carruthers (1979) found pupae from the spring (and
summer) generation 0 to 15 cm. deep in muck soil. Fifty percent emergence of
summer generation adults is correlated with the accumulation of approximately
990 DDT”! (Whitfield 1981).

The summer generation larvae cause little or no damage to the existing onion
crop. Ninety-six percent of summer generation flies reinfest previously infested
onions (Kendall 1932). This behavior probably increases larval survival because
first instar larvae are frequently unable to penetrate and establish themselves on
healthy bulbs (Drummond 1982).

Fifty percent emergence of fall generation adults is correlated with the
accumulation of 1769 DDW‘ (Whitfield 1981). However, 10-67% of summer
generation pupae enter diapause and remain in the ground until the following spring
(Perron and LaFrance 1961, Ellington 1963, Loosjes I976, Whitfield 1981).

A large proportion of the overwintering onion maggot population develops in
cull onions left in the field (Drummond 1982). He demonstrated the importance of
cut and sprouted culls as attractants to onion maggot adults. He also reported
onion maggot pupae of the fall generation to pupate at deeper depths (up to 28 cm.)

than reported for the spring and summer generations (Carruthers 1979).

Ground Beetles
The immature stages of the onion maggot are very susceptible to predation
by various species of Carabidae and Staphylinidae. The impact the staphylinid,
Aleochara bilineata (Gyll.) has on Michigan onion maggot populations has been well
documented (Whitfield 1981, Groden 1982). Carabids, however, have received little
attention.
Ball (1960) lists approximately 2500 species of Carabidae in America north of

Mexico. Allen (1979) states that the majority of North American carabids can best

8
be described as opportunistic. Depending on what is available they may act as
general predators, herbivores, or scavengers. However, a few species specialize as
predators on specific taxa. Lindroth (1969) lists carabid larvae as being predatory
with very few exceptions. Two North American ground beetle genera, however,
are known to have species that are host specific ectoparasitoids as larvae.

Ground beetles are present in most, if not all, agricultural croplands (Allen
1979). Although little is known about the biology of North American carabids or
their role in cultivated fields (Kirk 1971a, Thiele 1977), there has been an increased
interest in ecological and biological studies on the Carabidae within the past
several years (Allen 1979).

Carabids are generally regarded in the literature as being beneficial. They
have been known, however, to be minor pests of some crops such as strawberries
(Johnson and Cameron 1969) and corn (Pausch and Pausch 1980). Their usefulness
comes from their consumption of vegetable and animal material. They have been
shown to consume the seeds of many noxious weed species of cultivated land
(Johnson and Cameron 1969, Lund and Turpin 1977). As predators, they feed
principally on the eggs and larvae of many forest and agricultural pests (Davies
1953, Best and Beegle 1977, Allen 1979).

Much of the literature concerning the usefulness of carabids in
agroecosystems deals with their predation of root maggots, Qe_l_i§_ s22. (Treherne
1916, Wishart, Doane and Maybee 1956, Hughes 1959, Wright, Hughes and Worrall
1960, Mitchell 1963, Coaker and Williams 1963, Coaker I965, Wyman, Libby and
Chapman 1976, Drummond 1982, Andersen et al. 1983, Andersen and Sharman
1983). Treherne (1916) demonstrated in the laboratory that carabids found in
cabbage fields consumed eggs of the cabbage maggot, Delia radicum L. (=Hylemya
brassicae (Bouche)). Carabids have also been shown to be very important predators

of Q. radicum eggs in the field (Wishart et a1. 1956). Hughes (1959) listed five

9
species of carabids (along with three species of staphylinids) as predators of Q.
radicum eggs. He found that predation accounted for over 9096 of the mortality
experienced by cabbage maggot eggs during the first generation. Wright et al.
(1960) demonstrated that the number of carabids (of the most abundant species)
was inversely proportional to the number of surviving Q. radicum eggs and larvae.
Mitchell (1963) found two carabid species feeding on cabbage maggot eggs and
determined that the stage of crop growth affected the densities of the two beetle
species. Coaker and Williams (1963) estimated the daily intake of four common
carabid species to be a minimum of 16 Q. radicum eggs, larvae or pupae per day.
They felt, however, that staphylinids were more effective predators than carabids.
Coaker (1965) determined carabids were responsible for up to 3396 of the total egg
mortality of Q. radicum. Wyman' et al. (1976) demonstrated that damage
occurring in cabbage plots could be significantly reduced by artificially increasing
populations of Stenolophus (=Agonoderus) lecontei Chandoir and _S_. m (F.)
using blacklights. They also reported that these two species can consume large
numbers of cabbage maggot eggs. Finlayson et al. (1970) found more Q. radicum

pupae in plots where the carabid, Bembidion lampros (Herbst) had been removed

 

than in plots where they were present. Andersen et al. (1983) and Andersen and
Sharman (1983) also showed carabids and staphylinids to be important predators on

the eggs of the turnip root fly, Delia floralis Fallen. They concluded, however,

 

that predation alone did not reduce the pest population as greatly as granular
insecticides.

Drummond (1982) reported on the importance some carabid species play in
the onion agroecosystem. He found six species of ground beetles to feed on the
eggs of the onion maggot, Q. m. In addition to Drummond (1982), the
importance carabids may play in the Michigan onion agroecosystem was exhibited

by results obtained in a pitfall trap study during the growing seasons of 1981 and

10
1982 (Motyka and Edens 1984). The four fields studied ranged in pesticide use from
"organic" (no pesticide use for at least three years) to "intensive" (soil insecticide
at planting and approximately 15 foliar insecticide applications plus fungicides and
herbicides during the growing season). The "organic" field yielded catches of ten
times more carabids than any of the other three onion fields, but the combined

numbers of trapped adult onion and seedcorn maggots, Delia Llatura (Rond), were

 

almost two times less in the "organic" field. This strong negative correlation
suggests that carabids may play a role in reducing root maggot numbers in

Michigan.

The Genus Bembidion

Bembidion is the largest genus of carabids, with 162 species (Lindroth 1969).
Adults have a rather uniform appearance, small and slender (< 8.5 mm) with long
antennae and legs. Metallic reflection is common and the elytra are often spotted.
They move very rapidly.

Lindroth (1969) states that most species of Bembidion live close to water.
Thiele (1977) asserts that there are many similarities between littoral regions and
cultivated fields, the most important being that both are subject to drastic changes
in climatic factors. According to Thiele (1977) then, it should come as no surprise
to find large numbers of Bembidion in cultivated fields. Lindroth (1969), however,
further states that a few species of Bembidion are rather xenophilous and run about
on bare spots in the sunshine. Bembidion eat a variety of living, dying or dead
arthropods (Lindroth 1969, Allen 1979). Collembola, Acarina, Araneida, fragments
of other arthropods, fungal spores and other plant material comprised the diet of
14 species found in England (Davies 1953). Allen (1979), in his list of materials
reportedly consumed by North American Carabidae, lists eight species of
Bembidion. All were reported to feed on the eggs of the red-backed cutworm,

Euxoa ochrogaster Guenee in the laboratory.

11

When the consumption rates of insect eggs by various carabids are reported,
Bembidion s29. usually receive high rankings (Wishart et al. 1956, Wright et al.
1960, Coaker and Williams 1963, Perron 1972, Drummond 1982, Andersen et al.
1983). Wishart et al. (1956) state that Bembidion quadrimaculatum @positum Say
was the most important carabid attacking Q. radicum eggs in the field in Ontario.
They assigned it the highest ranking in egg-eating capacity and relative abundance.
Another species, Bembidion nitidum (Kby.), received the fifth highest ranking in

egg-eating‘capacity. Wright et al. (1960) report Bembidion lampros (Herbst) to be

 

the most important predator in their experiments in Wellesbourne, England.
Coaker and Williams (1963), also in Wellesbourne, gave Q. 'lamRros the highest
relative predator value during their studies of consumption of cabbage maggot
eggs. Q. quadrimaculatum was given the fifth highest value. Perron (1972)
mentions that Q. quadrimaculatum adults can destroy large numbers of onion

maggot eggs in Quebec. Q. quadrimaculatum adults consumed 8 onion maggot eggs

 

in two days in a greenhouse study at Michigan State University (Drummond 1982).
Only one of seven other species of carabid adults tested consumed more. Finally,

Andersen et al. (1982) showed Q. lamQros and Q. quadrimaculatum can eat large

 

numbers of turnip root fly eggs in Norway. Q. lamgros received the highest
predator value; Q. quadrimaculatum received the fourth highest value compared
with eight other carabids and four species of staphylinids.

In addition to Drummond's research (1982), Haynes and co-workers (Haynes,
Tummala and Ellis 1980) felt Bembidion size. may play an important role as
predators in the Michigan onion agroecosystem. In their conceptualization of the
onion ecosystem (Figure l) the general nature of predation by these beetles is
depicted. They are not only shown to be first order predators of three pest species,

but also interact with five beneficial organisms.

12

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8.2.200 to #0560 53520536 enacts;

l3
Bembidion qurimaculatum
The most common species of Bembidion found in Michigan onion fields is
Bembidion quadrimaculatum L. (Drummond 1982, Motyka and Edens 1984). Adult
beetles are 2.7-3.8 mm. in length and black with two yellow lateral spots on each
elytron. They occur throughout North America (Lindroth 1969) and at least in
some European countries (Coaker and Williams 1963, Thiele 1977, Andersen 1982).

There are two recorded subspecies of Q. quadrimaculatum, Q.

 

quadrimaculatum ggpositum Say and Q. quadrimaculatum dubitans LeConte. B

quadrimaculatum opoositum occurs east of the Rocky Mountains and Q.
quadrimaculatum dubitans occurs west of the Rockies (Lindroth 1969). Lindroth
(1969) states, however, that he is unable to find any difference between the two
subspecies other than color. Since the two forms are almost allopatric and their
occurrence is apparently not governed by climate (both occurring in humid coastal
as well as in dry inland country), Lindroth (1969) felt that the two forms were
genetically fixed and regarded both as subspecies of Q. quadrimaculatum.

Q. quadrimaculatum adults are commonly found on bare or almost bare soil,
usually fine-sand or clay that is dry or slightly damp (Rivard 1964a, Lindroth 1969).
Andersen (1982), however found that they preferred clay soils over sandy soils.
This is not unusual and is a general phenomenon associated with carabids (Thiele
1977). Clay generally has higher plant productivity which in turn ensures a better
food supply of herbivores and detritivores. In addition, Perron (1972) found
populations of predators and parasitoids to be almost ten times higher on organic
soil (e.g. muck) than on clay soils.

Q. quadrimaculatum are often common in cultivated fields (Lindroth 1969).
Esau and Peters (1975) actually collected more adults in pitfall traps placed in
disturbed habitats (cornfields) than fence rows or prairies in Iowa. Q.

fladrimaculatum frequently occur in large numbers in cultivated fields (Wishart et

14
al. 1956, Rivard 1964a, Frank 1971, Kirk 1971a, Perron 1972, Pimentel and Wheeler
1973, Esau and Peters 1975, Hsin, Sellers and Dahm 1979, Drummond 1982,
Andersen 1982, Los and Allen 1983). Frank (1971a) recorded a density of 20 Q.
quadrimaculatum adults per square meter from an arable field in central Alberta.
In these agricultural settings, Q. mdrimaculatum adults are reported to be
predators on the eggs of several DLlia s22. (Wishart et al. 1956, Perron 1972,
Drummond 1982, Andersen et a1. 1983), the eggs of the western corn rootworm,
Diabrotica virgifera virgifera LeConte, the northern corn rootworm, Q. longicornis

(Say) (Kirk 1982) and the eggs of the red-backed cutworm, Euxoa ochrogaster

 

Guenee (Frank 1971b).

Similar to almost all other Bembidion s22” Q. yadrimaculatum overwinters
as an adult. As the soil warms in the spring, they become active, although the time
of peak activity is uncertain. Perron (1972) reports that they do not build up to
significant numbers in Quebec until late June or early July. Drummond (1982)
reports peak captures of adults in Michigan from mid-April through early June. He
mentions, however, that the activity response is unclear, possibly due to low
population densities. Andersen (1982) shows peak activity ranging from mid-May to
late July in Norway. The most reliable indication of the activity response in
Michigan comes from the M.S.U. pitfall trap study (Motyka and Edens 1984).
Results of trap catches from the organic field showed the first activity peak to
occur from mid-June to early July.

Egg laying occurs in the spring (Rivard 1964b, Lindroth 1969, Frank 1971a,
Andersen 1982). Rivard (1964b) reports only one breeding period and collected
gravid females in May, June and July in eastern Ontario, with the highest
percentage of gravid females taken in early July. Frank (1971a) also records
collecting gravid females only during May-July but he reports two distinct breeding
periods in central Alberta. He states this is a common phenomenon associated with

beetles in the genus Bembidion.

15
From dissections, Rivard (1964b) found that the maximum number of eggs

present per gravid female was 16. He used a maximum of ten eggs per female as a

cutoff point to separate carabid species with a high reproductive potential from
those having a low reproductive potential. Although not recorded specifically for
Q. quadrimaculatum adults, carabid females frequently lay their eggs singly in the
soil at random, a few centimeters below the soil surface (Allen 1979).

Teneral Q. quadrimaculatum adults occur in the fall (Andersen 1982), another

 

indication of spring and early summer reproduction (Goulet 1976). The second
adult activity peak ranges from early August to early September in Michigan
(Motyka and Edens 1984). These adults eventually overwinter.

Most adult Bembidion are reported to be excellent fliers (Lindroth 1969).

However, the wings of Q. gladrimaculatum adults are not always functional,

 

although these beetles have been observed flying in Europe (Lindroth 1969). Thus,
Q. quadrimaculatum may have limited dispersal capabilities.

Very little is known about carabid immature stages in general (Lindroth 1969,
Kirk 1972). Little information is available concerning the larvae of Q.
quadrimaculatum. The larvae were described by Kirk (1972). They typically occur
from mid-August through October (Lindroth 1969).

For carabids in general, eggs usually hatch in three to ten days depending on
environmental factors (Kirk 1972, Allen 1979). There are generally three instars
with the duration of each stadium varying with the species and environmental
factors (Allen 1979). They are subterranean (Kirk 1972) and generally predaceous
(Lindroth 1969). Third instars construct a cell in the soil prior to pupation (Kirk
1972). The duration of the pre-pupal and pupal stages also vary with environmental
temperature and species involved. Adults upon emerging are extremely soft-bodied
and require a period to harden. At this time, they are relatively inactive and are

very susceptible to predation by other carabid adults (Goulet 1976).

l6
Pitfall Traps

Pitfall traps are the most commonly used instrument to study ground beetle
populations. They are inexpensive, quick and easy to operate and they yield large
amounts of data (Southwood 1978). Also, because ground beetles are frequently
present in low numbers in certain habitats and have secretive habits, daytime
searching and collecting activities are tedious and inefficient (Durkis and Reeves
1981). In an evaluation of various trapping devices available, pitfall traps were
found to be superior to all other methods for sampling populations of Carabidae
(Thiele 1977).

There are also numerous disadvantages associated with the use of pitfall
traps and data obtained with these traps must be interpreted with caution. They do
not yield an accurate assessment of the density of a population (unless other
techniques such as mark-recapture techniques are employed), but measure the
activity density of a population (Andersen 1982) (Le. pitfall trap catches are not
only dependent on the population density of a species, but also on its activity,
Thiele 1977). The activity of soil dwelling arthropods is affected by many factors
such as temperature, soil moisture and other weather conditions, food supply, the
characteristics of the habitat (e.g. the amount of impedance by vegetation) and the
sex, age, behavior and condition of the individuals (Greenslade 1964, Thomas and
Sleeper 1977, Southwood 1978).

Pitfall trap designs and trapping methods have been shown to affect trap
catches. Comparison of trap catch data from different habitats or between various
researchers is therefore difficult. For example, the type of trap used, greatly
influences trap catches, especially when no preserving fluid (e.g. ethylene glycol) is
used in the traps. Glass and plastic traps have a higher retaining efficiency than
metal ones (Luff 1975). The diameter of the traps is also important. Traps are

generally circular and catch size should be theoretically related to the length of

17
the perimeter (Southwood 1978). However, it has been demonstrated that smaller
aperture traps seemed to have higher efficiencies for smaller beetles while larger
traps caught a higher proportion of the larger beetles that encountered the trap
boundary (aperture) (Luff 1975).

Trapping methods that have been found to influence trap catches are
plentiful. The number of traps used and the distance between traps are important.
Traps standing close together will overlap in their effective catching-area and thus
catch less than traps farther apart (Andersen 1982). The use of barriers has been
shown to increase trap catches (Durkis and Reeves 1982). The number of times a
trap is replaced also affects catches. The catches immediately after a pitfall trap
is placed in position are commonly found to be higher than those subsequently
achieved ("digging-in effects", Greenslade 1973).

It seems that the adoption of a universally accepted pitfall trapping scheme
would be beneficial so that trap data obtained by different researchers could be
more adequately compared. Inferences could be made about the size of a carabid
population in a particular habitat compared to a similar habitat if the number of
traps, the size of the traps and the distances between them within each location

were identical.

ACTIVITY or BEMBIDION QUADRIMACULATUM I...1
AND PREDATION ON EGGS OF THE ONION MAGGOT,
DELIA ANTIQUA (MEIGEN)2

 

Abstract
Bembidion quadrimaculatum L. (Coleoptera: Carabidae), one of the most
common ground beetles in Michigan onion fields, feeds on the eggs of the onion

maggot (Delia antiqua (Meigen) (Diptera: Anthomyiidae)). Laboratory and field

 

experiments were conducted to determine how well Q. quadrimaculatum prey on Q.

 

m eggs. In the laboratory, these carabids consume up to 25 onion maggot
eggs per day. Q. m larval numbers were reduced more by Q. quadrimaculatum
when eggs were on the soil surface (7096 reduction) than when eggs were under the
soil surface (17.596 reduction). In a field cage study, Q. quadrimaculatum reduced

onion maggot larval numbers 5796. Q. quadrimaculatum, therefore, may be an

effective biological control agent of Q. antigua.

 

lColeoptera: Carabidae

2Diptera: Anthomyiidae

18

19
Introduction

Bembidion quadrimaculatum L. is one of the most abundant carabid species
found in onion fields in Michigan (Motyka and Edens 1984). The adults prey on root
maggot (M spp.) eggs, reducing pest populations (Wishart et al. 1956, Coaker
and Williams 1963, Coaker 1965, Perron 1972, Drummond 1982, Andersen et al.
1983, Andersen and Sharman 1983). The onion maggot, Delia antiqua (Meigen), is a
major pest of onions in the northern United States and Canada. Q.
quadrimaculatum preys on eggs of Q. m (Perron 1972, Drummond 1982) and
might be a potential biological control agent of this pest.

The objectives of this study were to study Q. quadrimaculatum feeding and
the impact these beetles have on onion maggot numbers in the field. Information is

also presented on dispersal and activity of these insects.

Materials and Methods

Feeding Studies. Bembidion quadrimaculatum adults were collected from the soil
surface at the M.S.U. Muck Soils Experimental Farm (Laingsburg, MI) and kept in
the laboratory at 20-25°C(15hL:9hD) in cake pans (34 cm x 24 cm x 5.7 cm) filled
with muck soil or a vermiculite and silica sand mix. Fifty to one hundred beetles
were placed in each pan. They were fed and given water three times a week. The
diet consisted of onion maggot eggs and first instar larvae, sections of Tenebrio
larvae, and small pieces of boiled ham.

Food Preference. In a preliminary study, Q. quadrimaculatum adults were

 

 

housed in petri dishes for ten days with radish (Rapharus sativus (L.)), barnyard-
grass (Echinochloa crusgalli (L.) Beauv.) and redroot pigweed (Armaranthus

retroflexus (L.)) seeds -- none were fed on. Q. quadrimaculatum adults also did not

 

feed on lettuce leaves, although Q. raEidum LeConte (found in moderate numbers

at the M.S.U. Muck Soils Experimental Farm) did.

20

Seventy-five Bembidion giadrimaculatum adults were individually housed at
20°C in petri dishes (100 mm x 15 mm) containing moist filter paper. Six food
items: Delia antiqua eggs, one-day-old Q. m larvae, a section of Tenebrio sp.
larva, onion bulb mites (Rhizoglyphus echinopus (Fumouze and Robin», green peach
aphid adults (MJZUS persicae (Sulzer)), and pea aphid adults (Acyrthosiohon pisum
(Harris)), were offered simultaneously to each beetle. The beetles were checked 48
hours later and the remaining food was recorded.

Feeding Rate Study. Beetle adults were individually housed in petri dishes
(100 mm x 15 mm) with moist filter paper at 15°, 20°, and 25°C (fifteen beetles
per temperature). Each received a known number (15, 20, 25, or 30) of onion
maggot eggs daily for 60 days. The eggs were fertile and viable and often hatched.
Eggs and first instar larvae consumed were recorded daily.

Foraging Ability. A piece of chemically untreated onion (15 mm x 15 mm x
3-4 mm) was placed at the bottom of 40 petri dishes (60 mm x 15 mm) and covered
with 1 cm of field-collected muck soil. Twenty Q. antique eggs were placed in
each dish in two clumps of ten, ca. 1.5 cm apart. They were placed adjacent to the
onion, (covered with 1 cm of soil) or left on top of the soil. Beetles were collected
three days before the experiment, stored at 25° and not fed. One Q.
quadrimaculatum adult was placed in half the dishes; the other half served as
controls to estimate maggot survival in the absence of predation. The onion
sections were kept at 25°C for 96 hours, and then examined for the presence of

first instar larvae.

Dispersal & Activity. Q. quadrimaculatum populations were sampled with pitfall
traps. (See Durkis and Reeves 1982 and Warner 1986 for the use of these traps.)
Glass canning jars (Mason jars, 473 ml, 7.6 cm ID) were used as pitfall traps in

1982. They were modified in 1983 by placing a plastic cup (414 ml) inside each jar.

21
A roof (aluminum flashing material, 11.4 cm x 14.0 cm) was constructed ca. 8 cm
above each trap to keep rain out. The beetles were trapped alive, identified in the
field, and brought to the laboratory for further studies.

Periods of Activity. Fifteen pitfall traps were placed in an onion plot (22.86

 

m x 15.24 m in 1982 and 30.48 m x 15.24 m in 1983) at the M.S.U. Muck Soils
Experimental Farm during May of 1982 and 1983. The traps were placed in a 3 x 5
grid measuring 10.98 m (each trap 5.49 m apart) by 12.2 m (each trap 3.05 m
apart). The traps were checked three times a week and remained in position until
beetle activity had ceased. They were removed temporarily if field activities
necessitated their removal.

Population Density Estimates and Dispersal Measures. Mark-recapture

techniques were used to study the fall population levels of Q. quadrimaculatum

 

during 1983. Before releasing marked beetles in the field, the marking procedure
was evaluated in the laboratory.

Thirty Q. quadrimaculatum adults were marked on the right elytron with
model airplane paint (Testors‘D) in the laboratory the previous spring. The paint
was applied with a No. 2 Entomological pin. After the mark dried, the beetles
were housed individually in petri dishes (60 x 15 mm) containing muck soil for 21
days. Thirty unmarked beetles were individually housed and served as controls.

To obtain the desired estimates in the field, a release point was chosen on
September 6 in a fallow area (30.48 m x 15.24 m) adjacent to an onion plot.
Eighteen pitfall traps were placed in three concentric rings around this release
point (4 traps 3 m from the release point, 6 traps 7.6 m from the position of
release, and 8 traps 15.2 m from the release point).

100 marked Q. quadrimaculatum adults were released at 5 p.m. EDT. The

 

time corresponded to the beginning of a period of inactivity (Drummond 1982).
Animals frequently show a high level of activity immediately after release, which

could bias dispersal estimates (Southwood 1978).

22

Estimates of the population density of Q. gmadrimaculatum adults were
derived from collecting beetles at the M.S.U. Muck Soils Experimental Farm
during 1983. The collections were made from a fallow area adjacent to two onion
plots. Early summer densities were estimated to be 6-9 adults/m2; fall densities
were estimated at 2-5 beetles/m2. Densities as high as 20/ m2 have been reported
(Frank 1971).

Effects of Rainfall and Temperature. The effects of rainfall on Q.
quadrimaculatum activity were evaluated with pitfall traps and rainfall records.
To determine the lower threshold temperatures for activity, 16 beetles were
individually housed in petri dishes and placed in an environmental chamber at 15°C.
The temperature was lowered l-2°C every 48 hours. The proportion able to walk
at each temperature was recorded.

Habitat Study. Twelve pitfall traps were monitored at the M.S.U. Muck Soils
Experiment Farm, 15 August to 9 September, in each of four locations: an onion
plot, a windrow comprised of pine trees, a Sudan grass plot, and a large fallow
area. The traps were placed in a 2x6 array measuring 5.49 m by 27.45 m and were
examined 2x/week.

Overwintering Habitats. Two hundred samples (30.5 cm x 30.5 cm x 10 cm
deep) were taken in each of the four locations described above. The samples were
taken on 7 to 8 November 1983 when virtually all adult Q. quadrimaculatum

activity had ceased.

Impact on Onion Maggot Larval Numbers. Four field experiments were conducted
at the M.S.U. Muck Soils Experimental Farm during the summer and fall of 1983.
Experiments 1 and 2 were conducted during the growing season; experiments 3 and

4 simulated conditions after harvest.

23

Thirty-six enclosures (clay drainage tile covered with insect screen, 20.32 cm
in diameter placed 16 cm beneath the soil surface with 15 cm protruding above)
were placed at random in an onion plot. The plot received no soil insecticide
treatment at planting and no foliar applications during the growing season.

All arthropods were trapped to extinction within each enclosure before the
experiments began. A pitfall trap (Mason jar, 473 ml. 7.6 cm ID), partially filled
with antifreeze, was used for this purpose. This trapping was accomplished in 7 to
10 days.

Two to four non-maggot infested onions were transplanted into each
enclosure. Q. mug eggs (obtained from Jim Miller, Dept. of Entomology,
M.S.U.) were then placed in clusters of 6-10 (25/enclosure), approximately 1 cm
below the soil surface; 0, 1, 3, or 5 Q. cmadrimaculatum adults were then added
randomly to each enclosure (4 treatments, 9 enclosures/treatment). The beetles
were field-collected on the day of the experiment except for experiment 4
(collected in mid-September and kept at 15°C).

Six to eleven days later, the onions and surrounding soil within each enclosure
were sampled for surviving Q. _a_n_t_i_gu_a_ larvae. Carabid mortality was not

monitored during the experiments since soil and plants could not be disturbed.

Placement of Eggs by Onion Maggot Females. To determine the percentage of
eggs accessible to Q. fladrimaculatum adults, cull onions were sampled from two
onion fields in Grant, Michigan, on September 28 and October 11. Eggs were
considered available if they were (1) attached to an onion at the soil surface, (2)
lying on the soil adjacent to an onion, or (3) under a cull onion at the onion-soil
interface.

Only cut or sprouted cull onions were sampled because eggs are most

frequently found around them (Drummond 1982). Cut culls were sampled by

24
removing them from the soil and scraping away small portions of soil beneath them

to a depth of approximately 5 cm. Sprouted culls were sampled by pulling them
from the ground, searching along the stem and bulb and then searching in the

cavity left in the ground.

Results and Discussion

Feeding Studies. Delia antiqua eggs, mealworms, and one-day old Q. antigua larvae

 

were the most frequently attacked of the items presented (Figure 1). However, no

 

food was entirely avoided. Q. quadrimaculatum adults were never seen killing a
healthy green peach or pea aphid during the study, but fed on dead individuals.
Furthermore, Q. quadrimaculatum were never seen attacking and killing another
healthy beetle. If,however, one or more healthy beetles encountered a dead or
dying individual, they would quickly overwhelm it. These observations agree with
Lindroth (1969) who found the staple food of Bembidion adults to be dead or dying
insects, which could include insect stages with limited mobility such as eggs or
maggots.

Feeding Rate Study. Q. cuiadrimaculatum adults can consume up to 25 onion

maggot eggs per day at 25°C (Table 1). When Q. quadrimaculatum adults locate

 

eggs, they usually remain in the vicinity of the eggs and continue feeding, unless
disturbed. This behavior is noteworthy because, in the field, onion maggot eggs are
typically laid in groups of 2-12 (Doane 1953). Therefore, if these beetles encounter
a group of eggs they can consume them all before resuming active foraging.
Foraging Ability. There was no significant difference in larval survival when
eggs were on or under the soil surface in the absence of predation (Table 2). In the

presence of Q. quadrimaculatum, onion maggot larval numbers were significantly

 

25

Proportion attacked

 

0.8

0.6

0.4

0.2

0 . .
OM OM meal- mites green pea
eggs. larvae worm peach aphids
aphids
Food Sources
Figure 1. Proportion of attacks (number of times attacked/75) by Bembidion

quadrimaculatum adults on 6 food items in a preference study.

26

Table 1. Numbers of onion maggot eggs and first instar larvae consumed daily by
Bembidion quadrimaculatum adults at constant temperatures of 15°, 20°
and 25°C over 60 days.

 

 

 

 

 

Temperature (°C) Eggs Larvae Eggs and Larvae
x : S.E. Range 2 1 S.E. Range 31 1 S.E.
15 .96 i .12 0-8 1.77 I. .16 0-8 2.73 _+_; .21
20 1.30 i. .12 0-10 2.78 i .18 0-9 4.08 1'. .24

25 4.53 i .52 0-25 4.06 1 .24 0-12 8.59 _+_ .61

 

27
reduced (70%)when the eggs were on top of the soil but not when the eggs were
under the soil surface (17.5% reduction). This agrees with Kirk (1982) who reported
that Q. quadrimaculatum adults feed on corn rootworm eggs, but make no effort to
dig the eggs out of the 5011.
Possible explanations are that the beetles are not effective excavators, or
they cannot detect the presence of eggs under the soil surface. Q.

quadrimaculatum adults forage actively on the soil surface, but randomly.

 

Therefore, they may not possess an effective mechanism for sensing prey at any
distance. Searching is undoubtedly more rapid on top than beneath the soil surface
(depending on the amount of vegetation to impede their movement).

The surface foraging behavior of Q. quadrimaculatum adults may reduce
competition between adults and larvae. Most carabid larvae, including Q.
gadrimaculatum larvae, are subterranean (Kirk 1972). From laboratory
obserations and pitfall trap catches, it seems that these larvae rarely forage on the
soil surface. Although larvae are felt to outnumber adults in the field by a ratio of
10 to 1 (Tomlin 1982), they are infrequently caught in pitfall traps (Kirk 1971).
Thus, this diversification of feeding habits may increase survival of both larvae and

adults.

Dispersal and Activity. Q. quadrimaculatum adults exhibit two periods of peak

 

activity (Figures 2 and 3). Overwintering adults become active in the spring and
breed. The larvae spend the summer in the soil, and the adults become active
again in late summer and early fall (Andersen 1982, Motyka and Edens 1984).

Q. quadrimaculatum adults are predators of onion maggot eggs, but their
impact is limited by low their densities during first generation Q. _a_r_1t_igi_1_a egg-
laying (Perron 1972). Because the onion crop is damaged most at this time

(Whitfield 1981), a decrease in onion maggot larvae numbers would be extremely

28
beneficial. During 1982 and 1983, Q. quadrimaculatum adults became active in
May. Drummond (1982) found these carabids in April of 1979. Therefore, Q.
quadrimaculatum adults may possess the potential to reduce spring onion maggot
larval numbers in Michigan.

Population Density Estimates and Dispersal Measures. No significant
difference in mortality was found between marked beetles (13.3% mortality) and
the controls (10% mortality). However, 3 of the 26 surviving marked beetles
(11.54%) lost their mark, a common occurrence when marking with paints
(Southwood 1978). Because other marking procedures were tedious or impossible,
paint was still used.

Actual field densities were not obtained because only two marked beetles

were captured during the study (2.7% of the total number of Q. quadrimaculatum

 

adults collected over 23 days). One marked Q. quadrimaculatum adult traveled 7.6
m on the soil surface in a day. Q. lamgros adults, a species slightly larger than Q.
(madrimaculatum, wandered an average of 1.6 m/day (maximum 10.0, minimum
0.15 m/day) (Thiele 1977). Although Q. quadrimaculatum adults can fly, they
seldom do (Lindroth 1969).

Effects of Rainfall and Temperature. Beetle activity decreased significantly
(difference test, p > 0.05; 1982, t = 5.13; 1983, t = 3.04) after periods of moderate
to heavy'rainfall (> 1.25 cm during a trapping period) (Figure 4), which agrees with
previous reports (Freitag et. al. 1969). Data analyzed in this study were collected
prior to the use of irrigation. The effects of irrigation on Q. quadrimaculatum
activity were not studied.

The effect of temperature on Q. quadrimaculatum is shown in Figure 5. All
beetles did not cease being active until 5°C. The lower temperature range for
individual beetle activity was 6-11°C, suggesting large individual variability within
the population. This may be genetically determined or due to the condition of the

beetle (e.g., age and body fat).

29

Table 2. Foraging ability of Bembidion giadrimaculatum adults.

 

 

Placement of Eggs Beetles Present Percent Survivall
No 87.0
On Soil Surface
Yes 26.02
No 91.0
Under Soil Surface
Yes 75.5

 

l. (#larvae/Ifeggs) x 100
2. Significantly different from controls (SNK test, P < 0.01)

No. beetles trapped/traplweek

30

 

 

 

4 —1
2 .—

° IIIIIIIIIIIIIIIIT
130 150 170 190 210 230 250 270 290
Julian Days

M | J J A I s l c
Figure 2. Seasonal trap catch of Bembidion quadrimaculatum adults in an onion

 

plot located at the M.S.U. Muck Soils Experimental farm, 1982.

No. beetles trapped/traplweek

31

 

 

ITIIIIIIII 111117

130 150 170 190 210 230 250 270 290

Figure 3.

JulianDays
MI .1 [J '11 | s | 0

Seasonal trap catch of Bembidion guadrimaculatum adults in an onion
plot located at the M.S.U. Muck Soils Experimental farm, 1983.

32

Habitat Study. More Q. cmadrimaculatum adults were caught in the windrow
(wind break of pine trees) than in other locations. Only 1% of the beetles were
collected from the onion plot; 19% were found in the fallow area, 21% in the Sudan
grass and 59% in the windrow (n = 269 beetles). These results were unexpected,
because carabids have strong habitat preferences (Thiele 1977), and Q.
quadrimaculatum prefer the relatively dry and sunny nature of a cultivated field
with low vegetation (Lindroth 1969). Possible explanations could be (1) extremes in
heat (the soil surface temperature of onion fields in Michigan frequently reaches
50°C or higher) and low soil surface moisture killed the beetles or forced them to
aestivate, (2) higher larval mortality in onion fields than in adjacent habitats, or (3)
adult dispersal from onion fields to more suitable adjacent habitats. Carabids can
distinguish small differences in air humidity (Thiele 1977). The humidity level in
the windrow may have been more suitable. The low levels of moisture present in
the onion plot during this study is best exemplified by the large numbers of
cicindelid beetles (they prefer very dry conditions, Thiele 1977) trapped over this
period. Thirty-four cicindelids were trapped in the onion plot, whereas they were

not trapped in the other 3 habitats.

Overwinterirm Samples. The number of Q. quadrimaculatum adults found

 

overwintering in the four locations were: 0.25 adults/m2 in the fallow plot, 0.18
adults/m2 in the Sudan grass plot and 0.15 adults/m2 in the onion plot and windrow
Q. quadrimaculatum adults overwinter in the soil and under plant debris. Soil
samples were taken to a depth of 10 cm; most adults (77.3%) were taken at 0-6 cm.
When found deeper in the soil, they were frequently associated with Stenolophus
c_o_rQ_m_a_ adults. Q. quadrimaculatum adults probably followed burrows dug by these

beetles.

Figure 4.

33

1982

PER DRY

TRRPPEO
2:

 

 

 

N0.

Y

 

Y T t I ' I ' I
135 155 175 195 215
JULIHN DRYS

r ' 4r
235 255

“T 1983

.. ”UH

PER DRY

 

 

TRRPPED
6
l

 

NO.

 

 

o Y I f T V I Y Tifi jA Y T
135 155 175 195 215 235 255

JULIRN ORYS

Number of Bembidion quadrimaculatum adults trapped per day during
1982 and 1983 in an onion plot located at the M.S.U. Muck Soils
Experimental farm. Arrows indicate periods of moderate to heavy
rainfall (> 1.25 cm) during the trapping period.

34

 

 

 

 

 

 

 

 

 

 

 

 

 

‘ 7

0.8-
O
.2
a
0 —-1
c 0.6
C A._.
.2
‘5’
a 0.4 .-
2
a .——-J

0.2 4

0 5 ' 10
Temperature (‘0)
Figure 5. Proportion of Bembidion quadrimaculatum adults active at various

 

temperatures.

35
Impact on Onion Maggot Larval Numbers. Only experiments 2 and 3 yielded
substantial onion maggot survival in the absence of beetles (Table 3). In these
experiments, the number of surviving onion maggot larvae was inversely
proportional to the number of Q. quadrimaculatum adults. The highest beetle
density reduced larval numbers by 55% in experiment 2 (Figure 6) and 57% in
experiment 3 (Figure 7). Wishart et. al. (1956) found no relation between the

number of Q. quadrimaculatum adults and Delia radicum L. pupae in a laboratory

 

experiment using cages (17.8 cm x 19 cm x 7.9 cm) with 125 Q. radicum eggs
placed on and slightly below the soil surface around a turnip. In this study, they
used 0, 5, 10, and 20 beetles, but found the largest reduction (91%) in pupal
numbers in the cages with 5 beetles. They concluded that 5 predators could devour
all the accessible eggs in each cage during the time it took them to hatch
(approximately 3 days). Thus, Q. quadrimaculatum adults may be able to reduce
root maggot numbers more than shown in the two field experiments reported here.
The beetle treatment that best represents a natural field density is unknown
because density estimates were unsuccessful. However, Q. cmadrimaculatum adults
are very sparse in commercial onion fields (Motyka and Edens 1984) and are much
more common in "organic" fields and at the M.S.U. Muck Soils Experimental farm.
Regardless of density, however, all the beetle treatments reduced onion maggot
larval numbers. Therefore, Q. quadrimaculatum adults, if present, can reduce

onion maggot numbers in the field.

Placement of Eggs by Onion Maggot Females. Data obtained from the fall
sampling of onion culls is presented in Table 4. The data is similar to Drummond's
(1982), except he found fewer eggs on the foliage of sprouted culls (only 5%). The
percentage of eggs found on the foliage may increase with increasing soil moisture

(Doane 1953, Miles 1953, Workman 1958).

36

Table 3. Percent survival of onion maggot larvae in the absence of predation in
field experiments conducted at the M.S.U. Muck Soils Experimental
farm, 1983.

 

 

Initial Condition # Eggs Placement

Date of Onions per tile of eggs % Survival

July 14 - not damaged 25 in 5011 3.56
July 20

August 11 - damaged 40 in soil 18.33
August 18

September 19 - damaged 30 on soil 37.41
September 26

October 18 - damaged 30 on 5011 1.11

October 29

 

37

 

 

 

ID
" Y=6.731-.7815x
L1J f-2=.16
a:
>
a:
c:
_1 :11
223 l x
S
>
a:
3 at at 11:
(n
.. s s 7.
11!
c3 .
z
i 1!
0+; at: 3F
0 l 3 5
N0. BEETLE HDULTS

Figure 6. Relationship between the number of Bembidion quadrimaculatum adults
and the number of surviving Delia antiqua larvae (with 95% confidence
interval) per enclosure in the second of four field experiments, 1983.

38

.3 .. Y=10.98-1.286x
r3. .43

 

SURVIVING LRRVHE

 

N0.

 

 

I I a
0 1 3 5

N0. BEETLE RDULTS

Relationship between the number of Bembidion quadrimaculatum adults
and the number of surviving Delia antiqua larvae (with 95% confidence
interval) per enclosure in the third of four field experiments, 1983.

Figure 7.

39
On the average, ca. one quarter of the total eggs laid around cut and sprouted

culls were deemed accessible to Q. quadrimaculatum adults. Although these

 

beetles reduced onion maggot larval numbers 17.5% (Table 2) when eggs were
placed 1 cm under the soil surface, they are much more efficient predators of eggs
on the soil surface. Eggs below the soil surface, however, may be preyed on by Q.

quadrimaculatum larvae. As this aspect was not studied, their impact on onion

 

maggot numbers is unknown.

Onion maggot eggs are felt to be most accessible to Q. quadrimaculatum

 

adults in the spring and fall. Eggs are often attached to young seedlings at the air-
soil interface during the spring; these would be vulnerable to predation by Q.
quadrimaculatum adults. Many eggs (Table 4) are also present on the soil surface
in the fall. Therefore, Q. quadrimaéulatum adults should reduce populations of
onion maggots to a greater degree at these times, rather than in mid-summer when
most eggs are laid beneath the soil surface (Workman 1958) and adults are not so
prevalent.

In conclusion, Q. quadrimaculatum adults are capable of reducing onion
maggot numbers in the field. However, this study investigated the role these
beetles might play in the Michigan onion agroecosystem in the absence of
insecticides. Heavy insecticide pressure is exerted upon Q. antigua by
commercial growers. The effects of insecticides on these carabids should be
determined for a better understanding of the impact Q. quadrimaculatum have on

maggot populations in commercial settings.

40

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ACKNOWLEDGMENTS

Special thanks to Jim Miller and his staff for their consideration and for
kindly supplying Delia antiqua eggs, often on short notice. Thanks also to Dean
Haynes, Rich Merritt, and Fred Stehr for their input. We are indebted to Melinda
Mitchell for her assistance and also gratefully acknowledge the Michigan Onion
Commodity Committee fortheir financial support. Thanks are also in order for

Ron Gnagey and Susan Battenfield.

(ll

REFERENCES CITED

Andersen, A. 1982. Carabidae and Staphylinidae (Col.) in swede and cauliflower
fields in south-eastern Norway Fauna Norv. Ser. B. 29:#9—6l.
Andersen, A., A. G. Hansen, N. Rydland and G. Oyre. 1983. Carabidae and

Staphylinidae (Col.) as predators of eggs of the turnip root fly Delia floralis

 

Fallen (Diptera, Anthomyiidae) in cage experiments. Z. ang. Ent. 95:499-
506.

Andersen, A. and J. A. Sharman. 1983. Effect of chlorfenvinphos and isofenphos
on Carabidae and Staphylinidae (COL), and their predation of eggs of D_elg
floralis Fallen (Diptera, Anthomyiidae) in field experiments. Z. ang. Ent.
95:206-213.

Coaker, J. M. 1965. Further experiments on the effect of beetle predators on the
numbers of the cabbage root fly, Erioischia brassicae (Bouche), attacking
brassicae crops. Ann. Appl. Biol. 56:7-20.

Coaker, J. M. and D. A. Williams. 1963. The importance of some Carabidae and
Staphylinidae as predators of the cabbage root fly, Erioischia brassicae
(Bouche). Entomol. Exp. Appl. 6:156-1614.

Doane, C. C. 1953. The onion maggot in Wisconsin and its relation to rot in
onions. Ph.D. Thesis. University of Wisconsin. 125 pp.

Drummond, F. A. 1982. Post-harvest biology of the onion maggot, Hylemya
1012993 (Meigen). M.S. Thesis. Michigan State University. 353 pp.

Durkis, J. J. and R. M. Reeves. 1982. Barriers increase efficiency of pitfall traps.
Ent. News 93(1):9-12.

#2

43

Frank, J. M. 1971. Carabidae (Coleoptera) of an arable field in Central Alberta.
Quaest. Entomol. 7(2):237-252.

Freitag, R., G. W. Ozburn and R. E. Leech. 1969. The effects of sumithion and
phosphamidon on populations of five carabid beetles and the spider Trochosa
terricola in northwestern Ontario and including a list of collected species of
carabid beetles and spiders. Can. Entomol. 101:1328-1333.

Johnson, N. E. and R. Scott Cameron. 1969. Phytophagous ground beetles. Ann.
Entomol. Soc. Amer. 62(#):909-914.

Kirk, V. M. 1971. Biological studies of a ground beetle, Pterostichus lucublandus.

 

Ann. Entomol. Soc. Amer. 64(3)5#0-544.

Kirk, V. M. 1972. Identification of ground beetle larvae found in cropland in South
Dakota. Ann. Entomol. Soc. Amer. 65(6):1349-1356.

Kirk, V. M. 1975. Biology of Stenolophus (=Agnoderus) comma, a ground beetle of
cropland. Ann. Entomol. Soc. Amer. 68(1):135-l38.

Kirk, V. M. 1982. Carabids: minimal role in pest management of corn rootworms.
Environ. Entomol.. 11(1):5-8.

Lindroth, C. M. 1969. The ground beetles of Canada and Alaska—parts 1-6. Opusc.
Entomol. Suppl. 20, 2Q, 29, 33, 314 and 35.

Lund, R. D. and F. T. Turpin. 1977. Carabid damage to weed seeds found in
Indiana cornfields. Environ. Entomol. 6(5):695-698.

Miles, M. 1953. Study of British anthomyiid flies. V. The onion fly, Delia antiqua.
Bull. Ent. Res. l54:583-588.

Motyka, G. and T. C. Edens. 198“. A comparison of heterogeneity and abundance
of pests and beneficials across a spectrum of chemical and cultural controls.
Prepared for submission to the E.P.A.

Perron, J. P. 1972. Effects of some ecological factors on populations of the onion
maggot, Hylemya antiqua (Meig.), under field conditions in Southwestern

Quebec. Ann. Ent. Soc. Quebec 17:29-05.

144 ‘

Southwood, T. R. E. 1978. Ecological methods, 2nd ed. Chapman and Hall, London.
524 pp.

Thiele, H. U. 1977. Carabid beetles in their environments. Zoophysiology and
Ecology 10. Springer-Verlag, Berlin, Heidelberg, New York. 369 pp.

Tomlin, A. D. 1982. Personal communication. Research Centre, Agriculture
Canada. London, Ontario.

Warner, F. 1986. Bembidion quadrimaculatum L. predation on eggs of the onion
maggot (Delia antiqua (Meigen)). M. S. Thesis. Michigan State University.

Whitfield, G. H. 1981. Spatial and temporal population analysis of the onion
maggot, (Hylemya antiqua (Meig.)) in Michigan. Ph.D. Thesis. Michigan
State Univeristy. 379 pp.

Wishart, G., J. F. Doane and G. E. Maybee. 1956. Notes on beetles as predators of
eggs of Hylemya brassicae (Bouche) (Diptera: Anthomyiidae). Can. Entomol.
88:634-639.

Workman. R. B., Jr. 1958. The biology of the onion maggot, Hylemya antiqua
(Meigen), under field and greenhouse conditions. Ph.D. Thesis. Oregon State

College, Corvallis. 82 pp.

EFFECTS OF INSECTICIDES ON BEMBIDION QUADRIMACULATUM 1..1
AND DELIA ANTIGUA (MEIGEN)2 EGGS AND ADULTS

Abstract

The effects of insecticides on Bembidion Luadrimaculatum L., Delia antiqua
(Meigen) eggs and Q. m adults were studied. Field experiments were
conducted to determine the impact of foliar insecticides on _B_. quadrimaculatum.
Laboratory studies were also performed on B. gladrimaculatum adults, Q. m
eggs, field-collected Q. m adults and laboratory-reared adults to obtain LC 50
values for various pesticides utilized in Michigan onions. In large plots, B.
quadrimaculatum numbers were not reduced by insecticides in 1982, but were
significantly reduced by diazinon in 1983. In field cages, diazinon killed 100% of _B_.
quadrimaculatum and fenvalerate killed 51% in 2 weeks. All of the insecticides
tested were extremely toxic to the beetles in the laboratory. Insecticides (with the
exception of fenvalerate) were found to be toxic to Q. m eggs, but the adults
were quite tolerant. Field-collected Q. a_n_t_i_q_ua adults were 14x more tolerant to
diazinon, 8x more tolerant to fenvalerate and #.7x more tolerant to naled than
laboratory-reared flies. Insecticides were 65 - #92x more toxic to _B_. ‘

quadrimaculatum than to field-collected Q. antigua adults.

 

lColeoptera: Carabidae

2Diptera: Anthomyiidae

45

#6
Introduction

The onion maggot, Delia antiqua (Meigen) is a major pest of onions in the
northern United States and Canada. Insecticides have been used to control this
insect since the 1930's due to the extensive damage it may cause (Kendall 1932).
Resistance, however, is a primary concern. The onion maggot has become resistant
to virtually all insecticides used for its control (Drew and Guyer 1958, Harris and
Svec 1976, Harris et. al. 1981). Due to resistance problems, growers spray for
adults more frequently and at higher application rates (Harris et. al. 1981).
Presently, moderate spray programs in Michigan consist of 7-10 sprays during the
growing season, even though foliar sprays are not effective in reducing maggot
damage (Warner and Grafius 1981, Whitfield 1981).

Unwarranted insecticide use can be detrimental by destroying beneficial
insect species. Ground beetles, as a rule, are highly intolerant to insecticides
applied at normal concentrations (Freitag 1979). However, insecticides are known
to produce differential kills of ground beetles when applied at equal concentrations
(Mowat and Coaker 1967, Critchley 1972, Tomlin 1975, Thiele 1977). Insecticides
less toxic to ground beetles (as well as other predators and parasitoids) should be
utilized to control pest insect species when implementing pest management spray
programs.

The carabid, Bembidion quadrimaculatum L. was felt to be highly intolerant

 

to insecticides due to its extremely low numbers in commercial compared to
organic fields (Motyka and Edens 1981:). These beetles are predators of onion
maggot eggs (Perron 1972, Drummond 1982, Warner 1986), therefore, management
practices aimed at increasing their abundance in commercial onion fields should be
beneficial.

The primary objective of this study was to examine the relative effects of

insecticides on _B_. quadrimaculatum and _D_. antigua eggs and adults. The effects of

#7
soil and foliar insecticides on Q. quadrimaculatum in the field were observed.
Laboratory studies were performed to obtain relative toxicities of various
agrochemicals utilized in Michigan onion production to Q. quadrimaculatum adults,
Q. antigua eggs, field—collected Q. antigua adults and laboratory-reared Q. antigua

adults.

Materials and Methods
Field Research. Field research was conducted at the M.S.U. Muck Soils
Experimental Farm (Laingsburg, MI) during the summers of 1982 and 1983. A large
plot experiment and a cage study were conducted in 1982 and a large plot study
was conducted in 1983.

' Pitfall traps (MasonO jar, 473 ml, 7.6 cm ID) were used to monitor the
activity of Q. cmadrimaculatum adults. Beetles were trapped alive and returned to
their respective plots as far from the traps as possible to reduce the probability of
immediate recapture (beetles are known to become "trap happy," Thomas and
Sleeper 1977). The traps were checked 3-5 times per week.

Diazinon (.56 kg ai/ha, #1796 solution, 280 l/ha) and fenvalerate (.11 kg ai/ha,
.13996 solution, 280 l/ha) were applied every 7-10 days, similar to commercial

programs for onion maggot and onion thrips (Thrips tabaci (Lind)) control. Soil

 

insecticide (fonofos or chlorpyrifos granules) was applied in-row at planting to

portions of the plot to reduce Q. antigua damage.

Large Plot Experiment 1982. Plots were separated by placing aluminum flashing
(23 cm high) ten centimeters in the ground between plots arranged in a completely
randomized design with 6 replications per treatment (Fig. 1). The plots were not
enclosed over the top, but Q. quadrimaculatum movement from these plots was

minimal because they rarely fly. Insecticides were applied as described above.

as
Cage Study 1982. Nine cages (6.7 cm x 6.7 cm) were constructed of aluminum

flashing with 1 mm mesh screen tops, and placed into the ground. All vegetation

(weeds and onions) was removed from the cages.

All insects present when the cages were placed in the ground were removed
or killed by drenching the soil with a 1596 Clorox® mixture followed by pitfall
trapping (with ethylene glycol) for approximately three weeks. Ten or fifteen
field-collected Q. quadrimaculatum adults were then placed in each cage. The
beetles were fed onion maggot eggs and given water daily with a small sponge.
Insecticides were applied with a hand sprayer August 3, 10 and 18.

Q. wadrimaculatum adults were monitored daily using one pitfall trap per
cage and by disturbing the top two centimeters of soil. The number of living and

dead beetles was recorded, although dead beetles were difficult to locate.

Large Plot Experiment 1983. Plots were arranged in a randomized complete block
design with 4 replications per treatment (Fig. 1). The treatments were not
separated using aluminum flashing as in 1982. This allowed beetles to move freely
from treated to untreated plots. The insecticides were applied as before on July

28, August 4 and August 18.

Laboratory Studies. Laboratory LC 50 values were obtained with various pesticides
for Q. quadrimaculatum adults, Q. m eggs, field-collected Q. m adults
and laboratory-reared adults. Pesticides tested were: diazinon, fenvalerate
(Pydrin), naled (Dibrom), chlorpyrifos (Lorsban), fonofos (Dyfonate), maneb (a
fungicide) and glyphosate (Roundup, an herbicide). LC 50 values were not obtained

for every chemical tested due to the limited numbers of insects available.

#9

1982
115i-

 

.
_a
N
(D
.a
N
N
0)
_a

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0'

 

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-——-—--—--—1
-

 

 

 

 

 

 

 

 

 

 

 

eoll treated aoll aoll treated

 

 

 

 

 

 

 

 

 

 

with untreated with
chlorpyrltoa tonotoe
1 =- control
2 = sprayed with ' 1933
diazinon E'H—7‘m—l'
a = sprayed with E 1 1
fenvalerate “'
2 3
O = plttall trapa 3 2
1 2
3 1
:aaa;s;2:aegsz+s 3
3 31:11 ii! ::i 1::
soil untreated aoll treated with
tonotoe

Figure 1. Plot diagrams of large plot insecticide experiments at the M.S.U. Muck
Soils Experimental farm during the summers of 1982 and 1983.

50
Pesticide solutions were prepared using commercial pesticide formulations

and distilled water. Filter papers (WhitmanO #2) were then dipped into the

respective solutions for five seconds and allowed to dry for ten minutes (when
testing Q. antigua eggs, the filter papers were only allowed to drip dry). After
drying, the papers were placed into containers and insects or eggs added. The tests

were conducted at 25°C. Containers were checked every 24 hours for four days.

Effects of Pesticides on B. quadrimaculatum Adults. Beetles used in these tests
were collected at the M.S.U. Muck Soils Experimental farm and stored in the
laboratory for 2-3 weeks at 25°C. These beetles were fed and watered three times
a week.

Testing was performed by placing an insecticide-treated filter paper (5.5 cm)
in a baby food jar (130 ml) covered with screen. Thirty adults (6 replications (jars);
5 beetles/rep) were tested at each concentration (Table l). The beetles were fed

Q. antigua eggs and watered after 24 hours.

Effects of Pesticides on D. antiqua Eggs. Eggs used in these tests were obtained
from a laboratory culture of Q. m maintained by the staff of Dr. Jim Miller,
located at the Pesticide Research Center, M.S.U. These flies, collected from
Guelph, Ontario, have completed approximately 20 generations in the lab.

Testing was performed by placing an insecticide-tainted filter paper (5.5 cm)
in a petri dish (60 mm x 15 mm). One hundred and fifty eggs (6 replications; 25
eggs/ rep) were tested at each concentration (Table 2).

An additional experiment was completed to determine if insecticide
resistance is present in the eggs of Q. m. For this study, eggs collected from
the aforementioned laboratory culture were compared to eggs oviposited by flies

recently captured (0 generations removed from the field) from Grant, Michigan.

51

Table 1. Treatment levels (percent solution) for onion production pesticides

applied to Bembidion quadrimaculatum in laboratory studies.

 

 

 

 

F = fungicide

H = herbicide

diazinon fenvalerate naled chlorpyrifos maneb glyphosate
(I) (I) (I) (I) (F) (H)
.125 .04 .0025 .5 .1 1.25
.025 .01 .001 .25 .01
.01 .001 .0005 .125 .001
.005 .00015 .00025 .025
.0025 .0001 .0001 .0025
.001 .000025 .00025
.0005 .000025
.00025
.0001
.00005
.000025
.417f .139f .417f .375f 1.25f
.250d .osad .500d
d = normal drench treatment concentration at 467 l/ha
f = normal foliar application concentraton at 280 l/ha
I = insecticide

52

 

 

 

 

 

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53
Flies from Grant were chosen because they are known to be resistant to a large
number of insecticides (Harris and Svec 1976, Harris et al. 1981). Filter papers
were dipped in a .0025% diazinon solution and placed in petri dishes. Two hundred

and fifty eggs (10 replications; 25 eggs/rep) of each strain of flies were tested.

Effects of Insecticides on D. antiqua Adults. The testing procedure was identical
for the field-collected and laboratory-reared flies. The tests were done by placing
an insecticide-tainted filter paper (7.0 cm) in a one pint Mason jar. The jar was
covered by insect screen. Forty-five adults (3 replications; l5 flies/rep) from each
culture were tested at each insecticide concentration (Table 2). The flies were fed
a mixture of 20 parts enzymatically hydrolyzed yeast, 10 parts table sugar and 10

parts powdered milk and given water daily.

Results and Discussion
Large Plot Experiment 1982. The foliar applications of diazinon and fenvalerate
produced no significant differences in the mean numbers of Q. quadrimaculatum
trapped (Table 3). However, more beetles were actually trapped in the sprayed
plots than in the unsprayed plots. There were equivalent densities of Q.
quadrimaculatum adults in all the plots prior to spraying (Table 3). Therefore,

there may have been a slight increase in activity of Q. quadrimaculatum adults in

 

the insecticide—treated plots, especially the plots sprayed with fenvalerate.
Sublethal doses of insecticides are known to stimulate carabid activity (Critchley
1972).

These results were unexpected because the rates of insecticide applied were
felt to be toxic to Q. quadrimaculatum adults. However, many broad-leaved weed
species (e.g. redroot pigweed, Amaranthus retroflexus L. and lambsquarters,

Chenopodium album L.) colonized these plots and probably prevented many

54
insecticide droplets from reaching the soil surface. Therefore, it is possible that
only a small proportion of the insecticide applied settled on the soil.

Although non-replicated, the soil insecticide may have reduced Q.
quadrimaculatum numbers (Figure 2). Soil insecticides are known to be toxic to
many species of carabids (Mowat and Coaker 1967, Critchley 1972, Tomlin 1975),
so these results were not surprising. However, it is unknown whether the adults,
larvae or both stages were adversely affected by these insecticides.

Chlorpyrifos and fonofos produce excellent onion maggot control when
applied at planting (Grafius, Warner and Mitchell 1983a). However, because
fonofos appears to be more toxic to Q. quadrimaculatum, chlorpyrifos would be

preferable.

Cage Study 1982. The first application of diazinon produced 83% mortality of Q.
gadrimaculatum adults within 24 hours. Eventually, all of the diazinon—treated
beetles succumbed. The first application of fenvalerate produced 33% mortality
within 24 hours (calculated after Abbott (1925)). The three applications of
fenvalerate caused 51% mortality.

The cage study probably represents an amplification of the results that would
be obtained in commercial onion fields. Because all of the vegetation (onions and
weeds) was removed from 'the cages, all of the insecticide droplets probably
reached the soil surface. In commercial fields, a great deal of the insecticide
applied would settle on the onion foliage and not on the soil. However, weed
control in commercial onion fields is intensive so weeds would not be present to

intercept the remaining droplets.

55

Table 3. Mean numbers per replication of Bembidion Qadrimaculatum adults
trapped in plots sprayed with diazinon and fenvalerate, 1982.

 

)2 numbers of Q. quadrimaculatum adults trappedl

 

Treatments Prior to foliar Post applications

applications (7-20)

 

 

diazinon 2.53 11.333
fenvalerate 2.5a 21.67a
untreated 2.67a 10.33a
1

Means followed by the same letter are not significantly different (Student-

Newman-Keuls' multiple range test, P > 0.05).

56

g untreated
' [D chlorpyrifos
120 —

D fonofos
100- g

 

 

80"

60-

 

BEETLES TRAPPED

40-

NO.

20-

 

 

 

 

 

 

 

 

 

 

O

 

Figure 2. Comparative numbers of Bembidion quadrimaculatum adults trapped
from July 13 to August 18, 1982 in plots treated with 2 soil insecticides
compared to an untreated plot.

57

Large Plot Experiment 1983. Fewer Q. quadrimaculatum adults were trapped in
the plots receiving applications of foliar insecticides than in the untreated plots.
Significantly fewer beetles were caught in the diazinon-treated plots than in the
untreated plots (Table 4). As in the cage study, diazinon appeared to be more toxic
to Q. (madrimaculatum than fenvalerate. Both foliar insecticides produce
comparable control of onion thrips (Grafius, Warner and Mitchell 1983b), therefore,
fenvalerate would be preferable.

It appears that the application of fonofos at planting did not reduce Q.
quadrimaculatum numbers in this study (Figure 3). However, in this experiment,
beetles were allowed to move from one plot to another, unlike the 1982 study.
Therefore, although the adults did not appear to be affected by the soil insecticide

treatment, the effects on the larvae are uncertain.

Laboratory Studies.

Effects of Pesticides on B. quadrimaculatum Adults. All of the insecticides tested

were extremely toxic to Q. quadrimaculatum adults (Table 5). The herbicide,

 

glyphosate, produced 100% mortality. This was not unexpected because carabids
are known to be intolerant to many herbicides (Thiele 1977, Freitag 1979). Maneb
produced only 40% mortality at 0.196 solution, but this dose is 3.75x less than the
recommended field rate. Foliar pesticides, in general, are probably extremely

detrimental to Q. quadrimaculatum adults. Populations of these carabids will

 

almost surely be drastically reduced in fields where these pesticides are routinely
applied.

Comparing the LC 50 values of diazinon, fenvalerate and naled obtained for
Q. m eggs, field-collected adults and laboratory-reared adults with values

found for Q. quadrimaculatum adults indicates the relative toxicity of these three

58

Table 4. Mean numbers per replication of Bembidion gadrimaculatum adults
trapped in plots sprayed with diazinon and fenvalerate, 1983.

)2 numbers of Q. cmadrimaculatum adults trappedl

 

Treatments Prior to foliar Post application

applications (8-1 )

 

diazinon 17.25a 2.5a
fenvalerate 15.25a 4.25ab
untreated 17.5a 5.5b

 

lMeans followed by the same letter are not significantly different (Student-
Newman-Keuls' multiple range test, P > 0.05).

59

 

E untreated

.,__W
fonofos

 

 

 

140A

 

 

120-“

100-

80-1

60—

BEETLES TRAPPED

NO.

40 —1>

20—

 

 

 

 

 

 

0

Figure 3. Comparative numbers of Bembidion quadrimaculatum adults trapped
from July 16 to August 24, 1983 in an untreated plot and a plot treated

with fonofos.

6O

 

 

 

 

 

 

 

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6.0%: w 339.32 05 5 Biz?
3:253: 0287.2. =m Low SUV «.th oucooacou 83 5:3 33? no.— Ucm £22 oncoamom .a 033.

61
insecticides to the pest organisms and the beetle. Some of the ratios are
extremely high (Figure ‘1). For example, fenvalerate was found to be 492x more
toxic to g. quadrimaculatum adults than to field-collected onion maggot adults.

Obviously, doses of insecticide required to control [_D_. antigua (especially the adults)

are going to kill Q. quadrimaculatum adults.

 

Effects of Pesticides on D. antiqua Eggs. All of the insecticides tested, with the
exception of fenvalerate were extremely toxic to _D_. m; eggs (Table 5).
However, glyphosate and maneb produced no significant mortality at any solution
tested (S.N.K. multiple range test, P = 0.05). From these results, it would seem
possible to achieve excellent control of onion maggot populations by the use of
well-timed insecticide applications (e.g. drench applications of diazinon) aimed at
the eggs. However, only marginal control is obtained in the field (Grafius, et al.
1983a). Insecticide resistance may be present in the eggs of Q. antigua. However,
a comparison of eggs obtained from laboratory-reared flies and eggs oviposited by
field-collected flies did not support this (Student's t-test, P = 0.01). Therefore,
other phenomena (e.g. degradation of the insecticide, binding of the insecticide by
soil particles, etc.) account for the less than anticipated onion maggot control

achieved by soil drenches.

Effects of Insecticides on D. antiqua Adults. Q. antigua adults, most notably field-
collected adults, appear tolerant to the insecticides tested (Table 5). In fact, the
field-collected adults were 14x more tolerant to diazinon, 8x more tolerant to
fenvalerate and l4.7x more tolerant to naled than the laboratory-reared flies. This
was not surprising because flies from Grant, Michigan are known to be resistant to

many insecticides and this resistance is rapidly increasing (Harris et al. 1981).

500-

450—

400-

M 0) 00
0| 0 0|
‘P ‘P ‘1’

200-

Ratio of LC50 Values

.5
01
‘13

1ooj

50-

62

- . antiqua eggs:
D B. quadrimaculatum

FFF . (T?— D. antiqua field adults:

8. quadrimacula tum

g D. antiqua lab adults:
8. quadrimaculatum

 

Figure 1!.

 

 

 

 

 

 

 

 

 

 

H E} Ell];

diazinon fenvalerate naled

Ratios of LC5 values obtained for B___embidion guadrimaculatum, Delia
antigua eggs,_ 58.21 antigua eggs,_ D. antigua afield-collected adults and D.
antigua alaboratory- reared adults during laboratory studies.

 

63
Examination of the log dose-probit mortality regression equations obtained

for the two strains of flies reveals nearly identical slopes (Figures 5-7). This may

be an indication that resistance is already a serious problem. Often, when testing
insects that are developing insecticide resistance, the slope of the line changes and
the line moves to the right compared to a line obtained for a non-resistant strain.
If the onset of a resistance problem is detected, resistance management can be
employed (Matsumura 1983). However, once resistance has become fixed,
management is much more difficult.

It appears obvious that no insecticide spray programs should be employed
against Q. antigua adults in the field. The flies are difficult to kill and additional
insecticide pressure favors resistance buildup. In fact, the use of foliar sprays to
reduce Q. antigua damage has been shown to be ineffective (Warner and Grafius
1981, Whitfield 1981). In addition, this heavy insecticide pressure is detrimental to
the natural enemies of the pest such as Q. quadrimaculatum, the braconid,
Aphaereta pallipes (Say) and the tigerfly, Coenosia tigrina (Fabricus) (Carruthers

1981).

64

D.anthuo egg.

    
  
   
  
  

 

 

 

7'5 1 Y: .062 +1.603x
B. quadrimaculatum '1: .90
7.0 _ Y--2.518 + 3.6 511
15.34
6.5 —
- 90
6.0 -—
>- >-
- 1-
S 5.5 - .. 70 3
(
‘ 1-
" " 1:
S o
1 5'0 _. D. antiqua _ 50 E
5 field adults " 5
0 4.5- — 0
E 0. mm“ Y=-1.675+ 30 5
lab adults r‘ 1347" - “-
‘-° " Y: .5947 + = '95
1.16x _ 10
3.5 J R: .90
3.0 w
a --... ........ ”W- -fi-..
2'5 "l l 1 1
.0000 1 .0001 .001 .01 .1 1 10

PERCENT SOLUTION

Figure 5. Log dose-probit mortality regressions for Bembidion (wadrimaculatum,
Delia antiqua eggs, Q. antigua field-collected adults and Q. antigua
laboratory-reared adults exposed to diazinon.

 

65

B. quethnacula tum

    
 

    
   

 

 

 

7'5 ‘1 Y: 2.535 + 1.537):
I“: .88
7.0 -
6.5 —
D. antiqua eggs — 90
6.0 — =-1.527 +1.666x
r‘: .33 " 1’.”

z 2
a 5'5_ D. anthua _ 70 E
g lab adults D. nnthuo 2
2 5-°- Y: 2.283+ field adults " 5° '5
,_ u
a Y=1.225 + 0

4 5 — fi
3 ' .903x _ 3° a
“ r‘:.94 _

4.0 —

- 10

3.5 -

3.0 -

2.5 1W1 l’ v 'll'I'l v v 'IIYIII’ v - v-uu' *rw v—rv

.0001 .001 .01 .1 1 10

PERCENT SOLUTION

Figure 6. Log dose-probit mortality regressions for Bembidion quadrimaculatum,
Delia antigua eggs, Q. antigua field-collected adults and Q. antigua
laboratory-reared adults exposed to fenvalerate.

66

B. quaddmocula tum

     
 

  
   
     
       
  
 
 
  

D. antiqua
7.5 — Y: 1.‘ ‘02 2.6.5x .99.
r‘. .64 D. antiqua Y=3.403
7.0 Q lab adults +.832x
Y:2.0051 + ”-1-“
1.28511
8.5 .— E's-.95
*- 90
3.0 _ D. antiqua
field adults - >
>- 1-
' = .7803 + —
5 5.5 a Y 1— 70 g
2‘ 1.2111 ._
'- f‘: 93 1- m
5 ° 2
5.0 _‘ l—I-
, 50 ._
’2 r 2
m i“:
“- a
1..
4.0 .5
-— 10
3.5 "‘
3.0 -*
2.5 -—H'IWHT-r-r-nwmr—1-n-rrml—rw-rrmr—r-FW

 

 

.0001 .001 .01 .1 1 10
PERCENT sotunou

Figure 7. Log dose-probit mortality regressions for Bembidion quadrimaculatum,
Delia antigua eggs, Q. antigua field-collected adults and Q. antigua
laboratory-reared adults exposed to naled.

ACKNOWLEDGMENTS

Special thanks to Jim Miller and his staff for their assistance. Thanks also to
Dean Haynes, Rich Merritt and Fred Stehr for their input. We are indebted to
Melinda Mitchell and Susan Jawitz for their hard work on this project. We also
gratefully acknowledge the Michigan Onion Commodity Committee for their

financial support. Thanks are also in order for Ron Gnagey and Susan Battenfield.

67

REFERENCES CITED

Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide.
J. Econ. Ent. 18:265-267.

Carruthers, R. I. 1981. The biology and ecology of Entomophthora muscae (Cohn)
in the onion agroecosystem. Ph.D. Thesis. Michigan State University, East
Lansing. 238 pp.

Critchley, B. R. 1972. A laboratory study of the effects of some soil-applied
organophosphorus pesticides on Carabidae (Coleoptera). Bull. Ent. Res.
62:229-262.

Drew and Guyer. 1958. Test method for evaluating insecticides against the onion
maggot. Proc. North Cent. Branch Entomol. Soc. Amer. 13:413-44.

Drummond, F. A. 1982. Post-harvest biology of the onion maggot, Hylemya
M (Meigen). M.S. Thesis. Michigan State University. 353 pp.

Freitag, R. 1979. Carabid beetles and pollution. Pages 507-521 _i_r_1_ Carabid
beetles: their evolution, natural history and classification. Proc. of the First
Int.‘ Symp. of Carabidology. Smithsonian Institution, Washington, D. C.
August 21, 23 and 25, 1976. Dr. W. Junk bv Publishers, The Hague-Boston-
London.

Grafius, E. 3., F. W. Warner and M. Mitchell. 1983a. Onion maggot control, 1983.
Insecticide and Acaricide Tests 8:155-158.

Grafius, E. J., F. W. Warner and M. Mitchell. 1983b. Thrips control in onions,

1983. Insecticide and Acaricide Tests 8:159-160.

68

69
Harris, C. R. and H. J. Svec. 1976. Onion maggot resistance to insecticides. J.
Econ. Ent. 69(5):6l7-620.
Harris, C. R., H. J. Svec, J. H. Tolman, A. D. Tomlin and F. L. McEwen. 1981. A
rational integration of methods to control onion maggot in southwestern
Ontario. Proc. Br. Crop Protection Conf.--Pests and Diseases. 789-799.

Kendall, E. W., Jr. 1932. Notes on the onion maggot (Hylemya antiqua (Meig.)).

 

Rep. Entomol. Soc. Ont. 62:82-84.

Matsumura, F. 1983. Personal communication. Department of Entomology,
Michigan State Universty.

Mowat, D. J. and T. H. Coaker. 1967. The toxicity of some soil insecticides to

carabid predators of the cabbage root fly (Erioischia brassicae (Bouche)).

 

Ann. Appl. Biol. 59:369-35‘1.

Thiele, H. U. 1977. Carabid beetles in their environments. Zoophysiology and
Ecology 10. Springer-Verlag, Berlin, Heidelberg, New York. 369 pp.

Thomas, D. B., Jr. and E. L. Sleeper. 1977. The use of pitfall traps for estimating
the abundance of arthropods with special reference to the Tenebrionidae
(Coleoptera). Ann. Entomol. Soc. Amer. 70:2112-248.

Tomlin, A. D. 1975. The toxicity of insecticides by contact and soil treatment to
two species of ground beetles (Coleoptera: Carabidae). Can. Entomol.
107:529-532.

Warner, F. W. 1986. Bembidion quadrimaculatum L. predation on the eggs of the
onion maggot (Delia antiga (Meigen)). M.S. Thesis. Michigan State
University.

Warner, F. W. and E. J. Grafius. 1981. Unpublished data. Department of
Entomology, Michigan State University.

Whitfield, G. H. 1981. Spatial and temporal population analysis of the onion
maggot, (Hylemya anticma (Meig.)) in Michigan. Ph.D. Thesis. Michigan

State Univeristy. 379 pp.

CONCLUSION

Summary

Bembidion quadrimaculatum L. is one of the most abundant carabids found in
Michigan onion fields (Motyka and Edens 1984). These beetles are opportunistic
feeders, but do show a preference for onion maggot eggs and first instar larvae. In
the laboratory, Q. quadrimaculatum adults consumed up to 25 Delia antiqua
(Meigen) eggs per day.

Q. quadrimaculatum adults do not apparently exploit the subterranean
habitat. In a laboratory study, onion maggot larval numbers were reduced 70%
when eggs were placed on the soil surface but only 17.5% when eggs were in the
soil. These beetles do not appear to possess an effective mechanism for sensing
prey, so searching is undoubtedly more rapid on than beneath the soil surface.

Q. quadrimaculatum adults exhibit two periods of peak activity per year in
Michigan. Overwintering adults become active in the spring; the second period of
activity occurs in the fall (August-October). These activity peaks correspond
roughly with spring and fall Q. m egg laying.

In a field cage study, Q. gadrimaculatum adults reduced onion maggot larval

 

numbers 5796. In this study, regardless of the number of beetles placed in each
enclosure, maggot numbers were reduced. However, at best, only l13% of the
variation in the numbers of surviving onion maggot larvae was explained by beetle
numbers.

Insecticides are extremely toxic to Q. quadrimaculatum. In the field,

diazinon was more toxic than fenvalerate. The soil insecticides, fonofos and

70

7l
chlorpyrifos, reduced Q. quadrimaculatum numbers in 1982. In the laboratory,
diazinon was l185x, fenvalerate ll92X and naled 65X more toxic to Q.
quadrimaculatum adults than to field-collected Q. M adults. It was concluded
that, because these flies are difficult to kill, spray programs aimed at Q. m
adults should be avoided. This unwarranted insecticide use can drastically reduce

numbers of Q. quadrimaculatum and other natural enemies of the pest (Carruthers

1981).

Augmenting naturally occurring
B. quadrimaculatum populations

Heavy insecticide pressure (soil insecticide at planting and 0-15 foliar
applications during the growing season) is exerted upon the onion maggot by
commercial onion growers. The majority of this insecticide use is unwarranted for
onion maggot control because foliar sprays are not required to reduce damage
caused by this pest (Warner and Grafius 1981, Whitfield 1981). This misuse of
insecticide is unfortunate because while not reducing crop damage, it has all but
obliterated many natural enemies of the maggot in commercial fields, including Q.
quadrimaculatum (Motyka and Edens 1986).

In order to attain and sustain a significant natural population of Q.
quadrimaculatum in commercial onion fields in Michigan, a drastic reduction in the
use of pesticides is necessary. Presently, however, this does not appear to be
acceptable to commercial onion growers. Therefore, the establishment of
substantial Q. quadrimaculatum and other beneficial insect populations capable of
checking onion maggot outbreaks in onion fields is highly unlikely. The fact
remains, that Q. gmadrimaculatum adults, and other beneficial organisms, are killed
by concentrations of pesticides utilized by onion growers to control insects, weeds

and fungal diseases (Table l).

72

.52 265:th Eo:N

. a mg 2033:? Soc:

 

 

 

 

 

* c393:
* mummocabw
1: 9:10.530
* <<OU
moEoELo:
* * * nocmE
* * 36:3 Loaaou
* * _EoEEoLo—co
822mg"—
: 60.6:
* * c2529:
* 03 monocou
* - OMEN 8.6.6.623
* . Owe eofinflo
* Um: 33.33320
* 323385
”:88 58:8": .3 <33 238
0382: main: Sam—sumEIomau mo 56 8605—3
NmLocanEoEm ~m_mocooU coBEEom Nmmuolmmmfl alt—IQ

q

 

 

 

.cmeBE E .AcowEEV median 6:60 .339: :oEo
05 Ho ""2805 .836: 8. ? 3 63:80.60: 2on on 3 5505. 30303 :28 _m_u._oEEoo .3 SEE: moEutmom ._ 633.

 

73
What the future holds, however, for commercial onion growers is uncertain.

Growers may be forced to look for alternative control measures due to the lack of

effective insecticides (the onion maggot has eventually become resistant to
virtually every insecticide used for its control) and to the economics associated
with future insecticide use (e.g. increasingly high costs of fossil fuels). If this
situation occurs, beneficial insects may hold the key for onion maggot control.

The invasion of onion fields by beneficial organisms will not occur overnight.
Because these beneficials have been reduced to extremely low numbers by
pesticides, recruitment must occur. Beneficial insects must disperse from adjacent
habitats to onion fields to establish natural populations, or large numbers of insects
can be released to accelerate this process. However, at this time, the rearing and
release of large numbers of Q. mdrimaculatum is highly improbable. These
carabids are extremely difficult to culture due to the cannibalistic nature of the
larvae. To rear large numbers of these insects, the larvae must be housed
individually (Goulet 1976). This would not be an efficient use of resources and
probably would not be economically feasible (cost of environmental chambers,
labor, etc.). In addition, these beetles cannot be handled and released as easily as
parasitoids.

_B_. quadrimaculatum adults rarely fly, so recruitment from neighboring
habitats into onion fields may require a great deal of time, possibly 6 or 7 years
(estimates used in this calculation; starting population = .1 _B_. quadrimaculatum
adult/m2, desired natural population = 6 adults/m2, immigration from adjacent
habitats = .2 adult/m2, sex ratio 1:1, each female lays 16 eggs with 4 surviving to
the adult stage, adult mortality = 5096). So, to aid in the recruitment of Q.
quadrimaculatum and other natural enemies into commercial onion fields,
"nurseries" should be established adjacent to these fields. A nursery should be an

area where beneficial insects are allowed to thrive. It could consist of a block of

74
land (30 m x 30 m) where onions would be planted (maggots would surely infest the

onions to ensure a food and host supply for the beneficials and the onions could

possibly serve as a trap crop), weeds would be allowed (they would offer shelter and

would serve as sites for flies infected by Entomophthora muscae (Cohn) (Carruthers

 

1981) to die) and most importantly these areas would be free of pesticides. In the
fall, this block of land could be disked along with the neighboring onion fields and
subsequently replanted in the spring. Carabid populations would not be disrupted
because species that commonly inhabit cultivated fields are unaffected by
cultivation practices or harvesting (Thiele 1977). Eventually this nursery area

could serve as an index for the potential of biological control.

Bembidion quadrimaculatum and other carabids
as biological control agents
B. quadrimaculatum adults (and possibly the larvae) can reduce onion maggot

larval numbers in the field. However, _B_. quadrimaculatum is only one of over 50

 

species of Carabidae known to inhabit Michigan onion fields (Motyka and Edens

1980. Many of these carabids (e.g. Stenolcmhus comma and Anisodactylus

 

 

sanctaecrucis) are known to feed on root maggot eggs and larvae (Wyman et al.

 

1976, Drummond 1982). Therefore, all of these species in combination may be
capable of checking onion maggot populations.

Carabids are found in virtually all agricultural croplands (Allen 1979). They
are an extremely successful group of insects (£10,000 species described, Thiele 1977)
largely due to the fact that they are almost uncontested in their ecological niche
(their niche is partially overlapped by staphylinids and centipedes and shared by
lycosid spiders, Thiele 1977). Because they are beneficial and quite frequently
occur in large numbers in agricultural croplands (i.e. _B_. quadrimaculatum densities

as high as 20/m2 have been reported, Frank 1971a), it seems reasonable to suggest

75
that they warrant attention when implementing integrated pest management

programs. The impact carabids have on pest populations, especially root maggot

populations, should not be overlooked.

APPENDIX

(Footnotes for Figure l)

APPENDIX
(Footnotes for Figure l)

Footnote 1:

Nye, P. H. et a1. 1975. The possibility of predicting solute uptake and plant
growth response form independently measured soil and plant characteristics.
Plant and Soil 42:161-70.

Robinson, J. C. 1973. Studies on the performance and growth of various short-day
onion varieties (Allium cepa L.) in the Rhodesian low veld in relation to date
of sowing. Rhod. J. Agric. Res. 11:51-69.

Footnote 2:

Hancock, J. G. and J. W. Lorbeer. 1963. Pathogenesis of Botrytis cinerea, _B_.
guamosa and _B_. §l_li_i_ on onion leaves. Phytopathology. 53:669-73.

Footnote 3:

Ellington, J. J. 1963. Field and laboratory observations on the life history of the
onion maggot, Hylemya antglua (Meigen). Ph.D. thesis, Cornell University.
124 pp.

Kendall, E. W. 1932. Notes on the onion maggot, HylemLa antiqua (Meigen).
Entomol. Soc. Ontario Rep. 62:82-84.

Footnote 4:

Lewis, T. 1973. Thrips, their biology, ecology and economic importance. New
York: Academic, 366 pp.

Footnote 5:

Martin, G. C. 1958. Root-knot nematodes (Meloidogyne spp.) in the federation of
Rhodesia and Nyasaland. Nematologica #:122-25.

76

77
USDA. 1960. Index of Plant Diseases in the United States, Agriculture Handbook,
No. 165. Crops Research Division, Ag. Research Service, USDA. p. 365.
Footnote 6:
Sprague, R. 1950. Diseases of Cereals and Grasses of North America. Ronald
Press, New York.
Footnote 7:
Perron, J. P. 1972. Effects of some ecological factors on populations of the onion

maggot, I-Memya antiqua, under field conditions in southwestern Quebec.

 

Ann. Soc. Entomol. Que. l7(l):29-#7.
Footnote 8:
Perron, J. P. 1972. Effects of some ecological factors on populations of the onion

maggot, Hylemya antiqua, under field conditions in southwestern Quebec.

 

Ann. Soc. Entomol. Que. l7(1):29-l:7.

Footnote 9:

Stoffolono, J. G. 1969. Nematode parasites of the face fly and the onion maggot
in France and Denmark. J. Econ. Entomol. 62:792-95.

Footnote 10:

Perron, J. P. and R. Crete. 1960. Premieres observations sur le champignon,

Empusa muscae Cohn. (Phycomycetes: Entomophthora) parasitant la mouche

 

de 'l'oignon, Hylemya antiqua (Meig.) (Dipteres: Anthomyiidae) dans le

 

Quebec. Ann.Entomol. Soc. Quebec 5:52-56.

Footnote ll:

Perron, J.P. 1972. Effects of some ecological factors on populations of the onion
maggot, Hylemya antiqua, under field conditions in southwestern Quebec.
Ann. Soc. Entomol. Que. 17(1):29-#7.

Footnote 12:

Russell, H. M. 1912. An internal parasite of Thysanoptera. Tech. Ser. Bur. Ent.

U.S. 23:25-52.

78

Footnote 13:

Charles, V. K. 1941. A preliminary checklist of the entomogenous fungi of North
America. Tech. Bull. U.S. Dep. Agric. 21:707-85.

Footnote l4:

Cobb, N.A. 1917. The Mononchs, a genus of free-living predatory nematodes. Soil
Science. 3:431-86.

Footnote 15:

Mankau, R. et al. 1975. The life cycle of an endoparasite in some tylenchid
nematodes. Nematologica 21:89-94.

Footnote l6:

Connard, M. H. and P. W. Zimmerman. 1931. Origin of adventitious roots in

cutting of Portulaca oleracea. Contrib. Boyce Thompson Inst. Plant Res.

 

3:331-46.
Zimmerman, C. A. 1969. The causes and characteristics of weediness in Portulaca
oleracea L. Ph.D. Thesis, University of Michigan. 248 pp.

Footnote 17:

 

Shorthouse, J. D. and A. K. Watson. Plant galls and the biological control of
weeds. Insect World Digest, pp. 8-11.

Footnote 18:

Sawyer, A. J. 1976. The effect on the cereal leaf beetle of planting oats with a
companion crop. M.S. Thesis, Michigan State University. 145 pp.

Footnote 19:

Perron, J. P. 1972. Effects of some ecological factors on populations of the onion

maggot, Hylemya antiqua, under field conditions in southwestern Quebec.

 

Ann. Soc. Entomol. Que. 17(1):29-47.
Footnote 20:
Webster, J. M. 1972. Nematodes and biological control, pp. 469-96. In: Webster

(Ed.) Economic Nematology. Academic Press, N.Y.

79
Footnote 21:
Gorske, S. F. 1973. The bionomics of the purslane sawfly, Schizocerella pilicornis.
M.S. Thesis, University of Illinois. 108 pp.
Footnote 22:
USDA. 1960. Index of plant diseases in the United States. Agriculture Handbook
No. 165. Crops Res. Div., Agric. Res. Ser. 531 pp.

Footnote 23:

 

USDA. 1960. Index of plant diseases in the United States. Agriculture Handbook
No. 165. Crops res. Div., Agric. Res. Ser. 531 pp.

Footnote 24:

USDA. 1960. Index of plant diseases in the United States. Agriculture Handbook
No. 165. Crops Res. Div., Agric. Res. Ser. 531 pp.

Footnote 25:

Goeden, R. D. et a1. 1974. Present states of projects on the biological control of
weeds with insects and plant pathogens in the United States and Canada.
Weed Science 22:490—95.

Footnote 26:

Breeland, S. G. 1958. Biological studies on the armyworm, Pseudaletia unipuncta
(Haworth) in Tenessee. J. Tenn. Acad. Sci. 33:263-347.

Footnote 27:

Helgesen, R. G. and D. L. Haynes. 1972. Population dynamics of the cereal leaf

beetle, Oulema melanopus (Coleoptera: Chrysomelidae): a model for age

 

specific mortality. Can. Entomol. 104:797-814.
Tummala, R. L. et al. A discrete component approach to the management of the

cereal leaf beetle ecosystem. Environ. Entomol. 4:175-86.

80
Footnote 28:

Perron, J. P. .1972. Effects of some ecological factors on populations of the onion

maggot, Hylemya antiqua, under field conditions in southwestern Quebec.
Ann Soc. Entomol. Que. 17(1):29-47.

Footnote 29:

Webster, F. M. and C. W. Mally. 1900. The purslane sawfly -- Schizocerus
zabreskei. Can. Entomol. 32:51-55.

Footnote 30:

Gorske, S. F. 1973. The bionomics of the purslane sawfly, Schizorella pilicornia
(Meig.). M.S. Thesis, University of Illinois. 108 pp.

Footnote 31:

Mankau, R., J. L. Imbiani. 1975. The life cycle of an endoparasite in some
tylenchid nematodes. Nematologica 21:89-94.

Footnote 32:

Webster, J. M. 1972. Nematodes and biological control, pp. 469-496. In: J. M.
Webster (ed.) Economic Nematology. Academic Press, N.Y.

Footnote 33:

Cobb, N.A. 1913. Notes on mononchus and tylenchulus. Washington Acad. Sci.
3:287-88.

Cobb, N.A. 1917. The mononchs, a genus of free-living predatory nematodes.
Soil Science 3:431-486.

Footnote 34:

Raulin, F. W. 1975. A revision of the genus Archytas (Diptera Tachindae) for
America north of Mexico. M.S. Thesis. Michigan State University. 80 pp.

Footnote 35:

Danks, H. V. 1975. Factors determining levels of parasitism by Winthemia
rufopicta (Diptera: Tachinidae), with particular reference to Heliothis spp.

(Lepidoptera: Noctuidae) as hosts. Can. Entomol. 107:555-684.

81
Danks, H. V. 1975. Seasonal cycle and biology of Winthemia rufopicta (Diptera:

Tachinidae) as a parasite of Heliothis spp. (Lepidoptera: Noctuidae) on

tobacco in North Carolina. Can. Entomol. 107:639-54.

Footnote 36:

 

Gage, S. H. and D. L. Haynes. 1975. Emergence under natural and manipulated

conditions of Tetrastichus julis, an introduced larval parasite of the cereal

 

leaf beetle, with reference to regional population management. Environ.
Entomol. 4(3):425-34.

Footnote 37:

 

Maltby, H. I., F. W. Stehr, R. C. Anderson, G. E. Moorehead, L. C. Barton and J. D.
Paschke. 1971. Establishment in the United States of Anaphes flavipes
(Foerster), an egg parasite of the cereal leaf beetle, Oulema melanopus (L.)
J. Econ. Entomol. 64:693-97.

Footnote 38:

Perron, J. P. 1972. Effects of some ecological factors on populations of the onion
maggot, HJLlemya antiqua (Meig.), under field conditions in southwestern
Quebec. Ann. Soc. Entomol. Que. 17(1):29-47.

Footnote 39:

Thompson, W. R. 1943. A catalogue of the parasites and predators of insect pests.
Sect. 1, Pt. 2. Belleville, Ontario, Canada. The Imperial Parasite Service. 99
PP-

Footnote 40:

USDA. 1960. Index of plant diseases in the United States. Agriculture Handbook

No. 175. Crops Res. Div., Agric. Res. Ser., p. 280.

82
Footnote 41:

Gorlenko, M. V., I. V. Voronkevich and T. S. Maksimova. 1956. Mutual relations

between the onion fly and onion syrphid and the bacteria that cause damp
rots in plants. (in Russian) Zool. Zh. 35 pt. 1, pp. 16-20, 6 refs. Moscow,
1956. (With a summary in English, Suppl. p. 4).

Footnote 42:

 

Newhall, A. G. and B. G. Chitwood. 1940. Onion eelworm or bloat caused by the

stem. or bulb nematode, Ditylenchus dipsaci. Phytopathology 30:390-400.

 

Footnote 43:

 

USDA. 1960. Index of plant diseases in the United States. Agriculture Handbook

No. 165. Crops Res. Div., Agric. Res. Ser., p. 365.

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