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thesis entitled

INSECT GROWTH REGULATOR, CYROMAZINE, CONTROL
OF ONION MAGGOT (DELIA ANIYQUA (MEIGEN)) AND
EFFECTS ON POSSIBLE BIOLOGICAL CONTROLS

presented by

Sheila Ebert

has been accepted towards fulfillment
Of the requirements for

Masters degree in Entomology

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1M c/CIMMM

INSECT GROWTH REGULATOR, CYROMAZINE, CONTROL OF
ONION MAGGOT (DELIA ANTIQUA (MEIGEN)) AND EFFECTS ON POSSIBLE
BIOLOGICAL CONTROLS
By

Sheila M. Ebert

A THESIS

Submitted to
Michigan State University
In partial fulfillment of the requirements
For the degree Of

MASTERS OF SCIENCE
Department Of Entomology

1999

ABSTRACT

INSECT GROWTH REGULATOR, CYROMAZINE, CONTROL OF
ONION MAGGOT (DELIA ANHQUA (MEIGEN)) AND EFFECTS ON POSSIBLE
BIOLOGICAL CONTROLS
By

Sheila M. Ebert

Total carabid counts were generally higher in the cyromazine treated area versus the
chlorpyrifos treated area Of a field. However, each Of the carabid species counted did not
have higher numbers in the cyromazine areas. Total staphylinid counts were also more
numerous in the cyromazine areas at all sites in the second year. Count comparisons Of other
coleopterans and other arthropods were made. The patterns Of beetle activity peaks were '
examined.

Trenches were used to increase and decrease ambient carabid concentrations in an
onion field. The relative survival Of onion plants on which maggot eggs had been placed did
not differ between the high and low carabid concentrations. At harvest, the number Of eggs
that survived did not depend on the carabid concentration treatments. However, eighty
percent fewer maggots survived in the treatments with higher carabid concentrations.

Cyromazine and chlorpyrifos were tested on a variety Of soils for control of onion
maggot and for possible effects on onion germination and growth. These tests were done by
growing onions with these insecticides and with a no insecticide control on different soils in
two greenhouse studies and one field study. These results indicate that cyromazine does not
differ from chlorpyn'fos in its efficacy at the different soil organic matter contents tested.
However, soil organic matter content does effect the growth Of onions and the performance

Of the insecticides.

DEDICATION

T o the memory of F IoreIda Kraemer and Rosella Ebert

iii

ACKNOWLEDGEMENTS

Thank you to:

O

O

O
0..

O
0..

Maria Davis and Ed Grafius who gave me this Opportunity to learn “how to do
science.”

My committee members Doug Landis and Darryl Warncke who listened to my ideas
and guided me through onions and beetles,

Walter Pett, Beth Bishop, and everyone in who worked in the Grafius lab during my
time at Michigan State University,

Karim Maredia and Melanie Kaeb who expanded my time as a masters student into a
larger experience,

Jim Miller and his egg rearing lab members, in particular, Adam Peters for insight
into onion maggot behavior,

The students, staff and professors who helped, taught, inspired, listened, and made
my time at MSU a good experience,

Ilka and Steve Gilmer, Piera Giroux, Nathan Seigert, and my mother,

Ron Gnaggy who was patient with the number Of weeds in my plots and with me.

I would like to extend a special thank you to the people who let me onto their land and

graciously let me “muck” With their muck, the onion growers Mr. Dave Brink, Mr. Bruce

Schreur, Mr. Bernard Emelander, Mr. Don Krummrey and their families.

iv

TABLE OF CONTENTS

LIST OF TABLES ................................................................................ vi
LIST OF FIGURES .............................................................................. vii
INTRODUCTION .............................................................................. 1

LITERATURE REVIEW
Onion Maggot ............................................................................ 4
Management of Onion Maggot ...................................................... 5
Predatory Natural Enemies ............................................................ 7
Pitfall Trapping ........................................................................... 9
Profiles Of Carabids Frequently Caught ............................................. 12

Activity Density of Carabidae and Staphyllnidae in onion fields treated with
cyromazine and chlorpyrifos for control of onion maggot Delia antiqua (Meigen)

Abstract .................................................................................. 20
Introduction ............................................................................ 21
Materials and Methods .................................................................. 21
Results and Discussion ................................................................. 25
Conclusions ............................................................................... 61

Carabidae predation on onion maggot Delia antiqua (Meigen) and subsequent maggot
damage to onions

Abstract .................................................................................. 62
Introduction .............................................................................. 63
Materials and Methods .................................................................. 63
Results and Discussion ................................................................ 71
Conclusions ............................................................................... 79

Efficacy of insecticide treatment and soil organic matter content
on onion growth and damage by onion maggot Delia antiqua (Meigen)

Abstract .................................................................................. 80
Introduction .............................................................................. 8 1
Materials and Methods .................................................................. 83
Results and Discussion ................................................................. 87
Conclusions ............................................................................... 93
LITERATURE CITED .......................................................................... 94
APPENDICES
APENDIX A: Field Diagrams for Chapter II ....................................... 104
APENDIX B: Record Of Deposition Of Voucher Specimens ...................... 108

LIST OF TABLES

Activity Density of Carabidae and Staphylinidae in onion fields treated with

cyromazine and chlorpyrifos for control of onion maggot Delia antiqua (Meigen)

Table

1. Farm field Sites and descriptions .....................................................

2. Total number of carabids and staphylinids caught in all traps per insecticide
treatment over the entire trapping time ...............................................

3. Chi square values for comparisons Of total seasonal pitfall catches in
chlorpyrifos and cyromazine in four different onion field sites in

1996 and 1997 ............................................................................

4. Total number of selected non-carabids caught in all traps per insecticide

treatment over the entire trapping time ..............................................
Carabidae predation on onion maggot Delia antiqua (Meigen) and subsequent
maggot damage to onions

Table
1. Mean number of Delia antiqua eggs and maggots eaten by carabids in a
laboratory feeding study ................................................................
2. Mean number of eggs on the soil surface or below the soil surface eaten
by P. lucublandus and B. quadrimaculatum .......................................

Elcacy of insecticide treatment and soil organic matter content
on onion growth and damage by onion maggot Delia antiqua (Meigen)
Table
1. Greenhouse study 1: Mean comparisons Of onions grown on muck soil
of 20%, 40% and 60% organic matter content and with insecticide
treatments cyromazine, chlorpyrifos and no insecticide ..........................
2. Greenhouse study 1: Mean comparisons Of onion maggot control by
insecticides cyromazine and chlorpyrifos in mucksoils Of 20%, 40%
and 60% organic matter ................................................................
3. Greenhouse study 2: Mean comparisons Of onions grown on sand, organic
sand, or pest humus with cyromazine, chlorpyrifos or no insecticide
treatment ..................................................................................
4. Field study in Newaygo Co.: Mean comparisons of onions grown on
organic sand or peat with cyromazine, chlorpyrifos, or no insecticide
treatment ..................................................................................

vi

Page
23
26

29

49

Page
77

78

Page

88

90

91

92

LIST OF FIGURES

Activity Density of Carabidae and Staphylinidae in onion fields treated with cyromazine
and chlorpyrifos for control of onion maggot Delia antiqua (Meigen)
Figure Page
1. Field sites in Michigan ................................................................ 22
2. Total numbers Of all carabids caught per trap in chlorpyrifos and

cyromazine treated areas in four different onion field sites during the

1996 and 1997 growing season ....................................................... 28
3. Number of all carabids caught per trap per week in chlorpyrifos and

cyromazine treatments at four different onion field sites in 1996 and

1997 ...................................................................................... 3O
4. Total numbers Of Poecilus chalcites caught per trap in chlorpyrifos

and cyromazine treated areas in four different onion field sites

during the 1996 and 1997 growing seasons. ....................................... 31
5. Number Of Poecilus chalcites caught per trap per week in

chlorpyrifos and cyromazine treatments at four different onion field

sites in 1996 and 1997. ................................................................ 33
6. Total numbers OfAnisodacozlus sanctaecrusis caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 34
7. Number OfAnisodactylus sanctaecrusis caught per trap per week in

chlorpyrifos and cyromazine treatments at four different onion field

sites in 1996 and 1997 ................................................................. 35
8. Total numbers Of all Pterostichus melanarius caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 36
9. Number of Pterostichus melanarius caught per trap per week in

chlorpyrifos and cyromazine treatments at four different onion field

Sites in 1996 and 1997 ................................................................. 37
10. Total numbers of Clivim'a impressifi'ons caught per trap in

chlorpyri fOS and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................. 39
l 1. Number Of Clivinia impressifi‘ons caught per trap per week in

chlorpyrifos and cyromazine treatments at four different onion field

sites in 1996 and 1997 ................................................................. 40
12. Total numbers of Stenolophus comma and lecontei caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 41
13. Total numbers Of Poecilus lucublandus caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 42
14. Total numbers of Bembidion quadrimacutlum caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 43

vii

15.

16.

17.

18.

19.

20.

21.

22.

23.

24.

25.

26.

Number of Stenolophus comma and lecontei caught per trap per

week in chlorpyrifos and cyromazine treatments at four different

onion field sites in 1996 and 1997. .................................................. 44
Number Of Poecilus lucublandus caught per trap per week in

chlorpyrifos and cyromazine treatments at four different onion field

sites in 1996 and 1997. ............................................................... 45
Total numbers Of all staphylinids caught per trap in chlorpyrifos and

cyromazine treated areas in four different onion field sites during the

1996 and 1997 growing seasons. .................................................... 48
Number Of all staphylinids caught per trap per week in chlorpyrifos

and cyromazine treatments at four different onion field sites in 1996

and 1997. .............................................................................. 49
Total numbers of all anthicids caught per trap in chlorpyrifos and

cyromazine treated areas in four different onion field sites during the

1996 and 1997 growing seasons ...................................................... 50
Number of all anthicids caught per trap per week in chlorpyrifos and

cyromazine treatments at four different onion field sites in 1996 and

1997. .................................................................................... 5 1
Total numbers Of all spiders caught per trap in chlorpyrifos and

cyromazine treated areas in four different onion field Sites during the

1996 and 1997 growing seasons ...................................................... 53
Number Of all spiders caught per trap per week in chlorpyrifos and

cyromazine treatments at four different onion field sites in 1996 and

1997 ...................................................................................... 54
Total numbers Of Coleomegilla macultata caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 55
Total numbers Of Coccinella septumpunctata caught per trap in

chlorpyrifos and cyromazine treated areas in four different onion

field sites during the 1996 and 1997 growing seasons ............................ 56
Total numbers of Hippodamia spp. caught per trap in chlorpyrifos

and cyromazine treated areas in four different onion field sites

during the 1996 and 1997 growing seasons. ....................................... 57
Composition Of the carabid populations in chlorpyrifos and
cyromazine at four farms in 1996 and 1997 ........................................ 59

Carabidae predation on onion maggot Delia antiqua (Meigen) and subsequent
maggot damage to onions

Figure Page
1. Cross-section through trench around plot showing the plastic

sheeting that restricts beetle movement .............................................. 65
2. Diagram Of onion field at Michigan State University Muck Soils

Research Farm, Clinton CO ............................................................. 66
3. Number Of carabids caught per attempted treatment (decreased,

existing and increased carabid densities) in an onion field during the
growing season .......................................................................... 72

viii

4. Ratio of the number onions one month after placing onion maggot

eggs in the field to the number Of onions the day the eggs were

placed in the field ....................................................................... 73
5. Ratio Of the number onions three months after placing onion maggot

eggs in the field to the number Of onions the day the eggs were

placed in the field ....................................................................... 73
6. Number Of onion maggots and pupae found in or beneath an onion in

an field 4 weeks afier placing 20 onion maggot eggs on the onions

within different carabid densities ..................................................... 75
7. Number Of onion maggots and pupae found in or beneath an onion in

an onion field 4 weeks after placing 20 onion maggot eggs on onions

accessible or not accessible to ground dwelling predators ........................ 75
8. Number Of onion maggots and pupae found in or beneath an onion in

the field 4 weeks after placing 7 onion maggots on the onion within

different carabid densities ..................................................... 76
9. Number Of onion maggots and pupae found in or beneath an onion in

an onion field 4 weeks after placing 7 onion maggots on onions

accessible or not accessible to ground dwelling predators ........................ 76
Apendix A
Figure Page
1. Ottawa County 1 Site 1997 ........................................................... 105
2. Newaygo County Site 1997 ......................................................... 106
3. Ingham County Site 1997 ............................................................. 107

ix

INTRODUCTION

Onions (Alliaceae: Allium cepa) are a major vegetable crop in the United States, second
only to lettuce production by weight (Kortier-Davis et a1. 1995). In 1996, Michigan
growers planted 2511 ha of dry bulb onions with a prodUction value of $15.5 million
(MASS 1997). Most Of these onions were directly seeded into histosols, commonly
referred to as “muck” soils which have high organic matter content (Lucus 1982).
Histosols typically have good water retention, high nitrogen content, and simple nutrient
management and harvest practices (Zandstra et al. 1996).

The insect pest complex in onion production is relatively simple in Michigan.
Onion thrips, Thrips tobaci (Lineman), scrape the leaves and feed on the sap causing
damage to the leaves; large enough numbers can result in reduced onion yields and
increased incidences Of bacterial rot (Cornell University 1983). However, the most
significant insect pest Of onions in Michigan is the onion maggot, Delia antiqua Meigen
(Diptera: Anthomyiidae). In severe years, onion maggot can reduce onion stand in
commercially treated fields by 40-80% (Zandstra et a1. 1990).

Foliar insecticide sprays have been used to kill adult flies; soil drenches and
granular insecticides have been used to kill larvae. Historically, the common practice
was to apply granular insecticides in the seed furrow at planting and then follow with
foliar sprays as Often as once a week starting in June (Lin et a1. 1982). The result Of this
intensive exposure is that the onion maggot is now resistant to many insecticides (Howitt

1958, Guyer & Wells 1959, Harris & Svec 1976, Harris et a1. 1981, and Carroll et a1.

1991). Chlorpyrifos (Lorsban, Dow Elanco, Indianapolis, Indiana), an organophosphate
insecticide, and cyromazine (Trigard, Novartis, Greensboro, North Carolina), an insect
growth regulator, are the only remaining chemicals registered and effective for use
against onion maggot.

Cyromazine is an insect growth regulator that stiffens the larval cuticle via an
undetermined mode Of action and prevents melting (Kotze & Reynolds 1991). In the
early 1980’s, cyromazine was found to be useful against species Of flies. It has been used
against leaf miners, Liriomyza trifolii (Burgess), cultivated mushroom pests, Lycoriella
auripila, and has been fed to cattle and fowl to kill flies in feces (Shen & Plapp 1990).
Hayden and Grafius (1990) reported the potential of cryromazine as a management tool
for onion maggot. Cyromazine was first used against onion maggot as a soil drench; it is
now being incorporated into an onion seed treatment which results in the low dosage Of
50g of active ingredient per kg seed (Grafius et al.1984, Grafius & Boylan-Pett 1991 ,
Davis & Grafius 1992).

This thesis investigated three questions:

1. What is the impact Of cyromazine versus conventional insecticide controls on non-
pest, surface dwelling insects? Cyromazine is an insect growth inhibitor that may
have fewer negative impacts than conventional insecticides on natural enemies Of the
onion maggot (Miller et a1. 1981, Samsoe-Petersen 1985, Wills et a1. 1990) and,
therefore, might lend itself to a more integrated approach to control onion maggot.

2. What impact do these surface insects, particularly members of the family Carabidae,
have on the survival Of the immature stages Of D. antiqua? Does carabid predation

affect the level of maggot damage to the onion plants?

3. HOW effective are cyromazine and chlorpyrifos on soils Of different organic matter
content? Despite the success Of cyromazine for onion maggot control, there have
been some reports of failures. During the growing season of 1995, Grafius and
Davis (1996) found cryromazine ineffective at one field site. They suggested that
this might have been due to dry conditions, failure of pellet breakdown, or soil with

low organic matter content.

LITERATURE REVIEW

Onion maggot. The onion maggot, Delia antiqua Meigen (Diptera:
Anthomyiidae), is a serious onion pest. In Michigan, onion maggots have three
generations per year; the third generation over-winters in the soil as pupae and emerges
as adult flies in May. Fifty percent emergence occurs at approximately 400 DDMoC
(Carruthers 1979, Whitfield 1981). Newly emerged flies require a day for the
exoskeleton to dry and harden (Carruthers 1982). In the period before oviposition, the
flies forage and are commonly found in field borders visiting dandelions, Taraxacum
officinale Weber (Baker 1927) or other wild flowers (Carruthers 1982).

After a preovipositional period of about 10 days, the flies mate (Carruthers 1979).
The females lay their eggs at the base of onion seedlings. Perron and LaFrance (1961)
found in field cage experiments in Quebec that the mean numbers Of eggs laid per female
of each generation were 57.8, 36.2, and 24.3 respectively. Havukkula et a1. (1992)
reported that on average a D. antiqua female lays 15% Of her eggs on the surface to 2 mm
below, 24 % 2-4 mm deep, 22% 4-6 mm deep, 13% 6-8 mm deep, 7% 8-10 mm deep,
18% 10-15 mm deep, and a few deeper.

Onion maggot eggs require 50 1313333120 hatch (Carruthers 1979). Larvae feed on
the onion bulbs for 2 to 3 weeks, passing through three instars. One maggot destroys an
average of 28 small seedlings (onions in the loop stage with diameter at the soil surface
of 1 mm) before completing development (Workman 195 8). The larvae then pupate, and
adults emerge in July. By this time, the onions have developed a papery skin over the
bulbs that is more resistant to onion maggot attack. Therefore, summer generation

female flies prefer to lay their eggs on previously damaged onions (Finch & Eckenrode

1985, Hausmann & Miller 1989). Second generation flies emerge in August and
September and lay eggs on onions left behind in the field after the harvests in August-
October. The first generation larvae, therefore, have the greatest direct effect on the yield
and quality Of the onion crop. In severe years, onion maggot can reduce onion stand in
commercially treated fields by 40-80% (Zandstra et a1. 1996).

Management of onion maggot. Historically, onion maggot has been managed
primarily with chemical controls. The common practice was to apply granular
insecticides in the seed furrow at planting and then follow with foliar sprays as often as
once a week starting in June (Liu et a1; 1982). The result of this intensive exposure is that
the onion maggot is now resistant to cyclodiene, organophosphate, carbamate, and
pyrethroid insecticides (Howitt 1958, Guyer & Wells 1959, Harris & Svec 1976, Harris et
a1. 1981, and Carroll et a1. 1991). Foliar sprays used against adults are ineffective and
may have contributed to resistance development (F inch et a1. 1986). Application of
granular insecticides in the seed furrow by itself is effective against the very damaging
first generation of onion maggot (Ritcey et a1. 1991). Chlorpyrifos (Lorsban, Dow
Elanco, Indianapolis, Indiana), an organophosphate insecticide, and cyromazine (Trigard,
Novartis, Greensboro, North Carolina), an insect growth inhibitor, are the only remaining
chemicals effective registered for use against onion maggot.

Resistance to chlorpyrifos is increasing in Michigan (Grafius and Pett 1991), and
soil insecticides such as chlorpyri fOS are known to be toxic to many species Of carabids
(Mowat & Coaker 1967, Critchley 1972, Tomlin 1975, Clements et a1. 1988, Asteraki
1991, Bale et al. 1992), potential predators Of the onion maggot. Clements (1988)

concluded that chlorpyrifos sprays reduce total adult and larval carabid populations with

some variations between species and that some of the insecticide effects persist at least 18
months. In a non-replicated study by Warner (1986), soil applied chlorpyrifos may have
reduced the numbers Of the carabid Bembidion quadrimaculatum L.. F loate et a1. (1989)
found that while chlorpyrifos was toxic to Bembidion obscurellum Motschulsky and B.
quadrimaculatum in the lab, in the field Bembidion spp. mortality was lower in sprayed
plots between 3-16 days but not significantly lower between 17-47 days. Funderburk et
a1. (1990) found in peanut fields that spiders but not carabid numbers were significantly
reduced by chlorpyrifos. In Michigan, most onions are grown on organic soils.
Organophosphate pesticides maintain a higher concentration in organic soils than in
mineral soils (Szeto & Price 1991).

In the early 1980’s, cyromazine, an insect growth inhibitor, was found to be
useful against species Of flies. It has been used against leaf miners, Liriomyza trifolii
(Burges), cultivated mushroom pests, Lycoriella auripila, and has been fed to cattle and
fowl to kill maggots in feces (Shen & Plapp 1990). Hayden & Grafius (1990) reported
the potential Of cryromazine as a management tool for onion maggot. Cyromazine was
first used against onion maggot as a soil drench; it is now being incorporated into an
onion seed treatment which results in the low dosage Of 50g active ingredient (AI) / kg
seed (Grafius et al.1984, Grafius & Boylan-Pett 1991, Davis & Grafius 1992).

Cyromazine stiffens the larval cuticle via an undetermined mode Of action and
prevents molting (Kotze & Reynolds 1991). The physiological effects Of cyromazine
have been studied in the Mediterranean fruit fly, Ceratitis capitata (W iedemann)
(Diptera: Tepritidae), by Vinduela & Budia (1994). They found in cyromazine treated

flies a conspicuous swelling of the integument in the anterior region of the body, with a

local thinness Of the cuticle due to the gap between the epicuticle and the procuticle. In
the exoskelton there was discontinuity between the procuticle layers, abnormal
thickening Of the cuticle and disorganization and elongation Of the epidermic layer; only
the epicuticle was unaffected. There were also some effects on the muscles such as
altered mitochondria, distorted area Of fiber arrangement, and less fiber packing. They
concluded that cyromazine acts at the hormonal level, but its effects on the skeletal
muscles also indicate a protein involvement in the mode Of action.

Cyromazine is a pesticide that may have fewer negative impacts than
conventional pesticides on natural enemies Of the onion maggot (Miller et a1. 1981,
Samsoe-Petersen 1985, Friedel 1986, Wills et a1. 1990) and therefore, might lend itself
well to a more integrated approach to control onion maggot.

Predatory natural enemies of the onion maggot. The predators of D. antiqua
adults and immatures that have been investigated include birds (Kastner 1930, LOOSjes
1976), toads Bufo bufo L. (Loosjes 1976), the tachinid fly Coenosia tigrina (L.) (Perron
et a1. 1956), and Scatophaga stercoraria (L.) (Loosjes 1976). Carabidae and
Staphylinidae are the most researched predators Of the immature stages of D. antiqua and
its relatives, the cabbage maggot Delia radicum (L.) (=Hylemya brassicae Bouche) and
the turnip maggot Delia floralis (L.). Trehem (1916) Observed in the laboratory that
carabids attack cabbage maggot eggs. Wishart et a1. (1956) showed predacious beetles
destroy up to 70% Of cabbage maggot eggs and concluded that carabids are more
important predators than staphylinids. Hughes (1959) and Hughes & Salter (1959) found

that carabids destroy more than 90% Of D. radicum eggs. Coaker & Williams (1963)

found that although carabids are important D. radicum egg predators, staphylinids were
more effective.

Coaker (1965), using barriers drenched in pesticide to alter carabid densities,
showed that the survival of D. radicum is inversely related to the numbers of the
predatory carabids present. He stated that the carabids are responsible for up to one third
of the total egg mortality, though it varies from Site to site and with species composition.
Later in the cabbage maggot life cycle, Coaker suggested that mortality is due tO other
sources, staphylinids being an important source. Wayman et al. (1976) found that the
ground beetle, Stenelophus comma (F abr.) in addition to being an efficient predator of
immature D. radicum in the laboratory, when attracted to cabbage plots by black lights
could reduce cabbage maggot damage.

However, Van Dinther (1972) investigating Bembidion species by radioactive
monitoring estimated that the role of carabids as natural enemies Of cabbage root flies is
minimal. Uba Yaman (1990) stated that in the Netherlands 97% Of cabbage root flies are
destroyed prior tO their adult stage when natural enemies are present; without natural
enemies the mortality is 80%. Thus mortality due to predation is only 17%.

Work by Wishart et al. (1956), Coaker & Williams (1963) Coaker (1965), Perron
(1972), Drummond (1982), Andersen & Shannan (1983), Tomlin et al. (1985) all thought
that the genus Bembidion tO be a promising Delia spp. egg predator. Haynes et a1. (1980)
developed a conceptualization of the onion agroecosystem showing levels Of interaction
within the object Of control (D. antiqua) and the monitored environment. The only
carabid named in the model was Bembidion Sp. Grafius and Warner (1989) reported that

B. quadrimaculatum could potentially remove 60% Of D. antiqua eggs from the field.

B. quadrimaculatum predation is higher when eggs are placed on the soil surface
than when eggs are placed 1 cm deep (70% versus 17.5%). However, large portions Of
D. antiqua eggs are laid beneath the soil surface. Waymann et a1. (1976) compared over a
24 h period S. comma predation on D. radicum eggs that were either exposed or covered
with sand. They found that when unstarved S. comma found 65% Of the covered and
92% Of the uncovered eggs. When starved, S. comma found 85% Of the covered and
94% Of the uncovered eggs.

Haynes et a1. (1979), Drummond (1982), and Motyka and Edens (1984) have
found many species Of carabids inhabit onion fields in Michigan. Tomlin et a1. (1985) and
Drummond (1982) conducted feeding trials with some of these species that showed an
ability to eat onion maggot eggs and larvae.

Pitfall trapping. Pitfall traps have been used extensively to monitor the number
and activity of surface-active invertebrates, especially Coleoptera and Araneida (Halsall
1988). However, pitfall traps have some important shortcomings. Surrounding
vegetation may impede carabid movement and affect trap catches (Greenslade 1964).
Weather may influence the amount of carabid locomotor activity and therefore trap
catches (Briggs 1961). Greenslade (1964) found that different Species vary in
susceptibility to pitfall traps; smaller beetles were less susceptible to traps. However,
Halsall (1988) found capture rates between a sample Of species were unrelated to beetle
size, speed Of movement or diurnal behavior. Pitfall trap Size, shape, and composition
also have been found to affect trap catch (Luff 1973, Spense et a1. 1994). Chiverton

(1984) demonstrated that the content Of the gut affected capture Of a carabid Species.

These reports support Briggs’s (1961) conclusion that pitfall traps are Of little value for
the direct estimation Of absolute populations.

Baars (197 9) demonstrated that the use Of continuous pitfall sampling could be
used as a relative measure Of the Size Of carabid populations. In the present work,
comparisons of populations were made within individual fields with the same vegetation
and under the same management practices. Against these arguments, pitfall traps seemed
adequate.

There is some question as to the reliability of pitfall traps for assessing the impact
Of pesticides on populations Of ground-dwelling arthropods. Edwards and Thompson
(1975) found that the neurologically active insecticides cause hyperactivity that enhances
catches in sprayed plots relative to unsprayed ones and that pitfall catches are influenced
by beetle immigration. Chiverton (1984) concluded that reducing prey populations by
the application Of insecticides results in hungrier carabid beetles with consequently
higher activity. Since pitfall trap catches are determined not only by population size but
also activity, he argues that, “pitfall-trap catches alone cannot give a true measure Of the
effects of insecticides on carabid populations in the field.” In a peanut field, Dixon &
McKinlay (1992) hypothesized that after being sprayed with insecticide the pest (aphids)
falls Off plants. The beetles then ate the aphids and were less hungry therefore less active
and less likely to be trapped; later increases in catches may have been due to hungry and
thus more active beetles. In the onion system, the availability Of eggs or maggots, which
are already on or in the ground, is probably not increased due to the insecticides. Floate
et a1. (1989) found much higher toxicity Of chlorpyrifos to Bembidion species in the

laboratory than in the field and suggested that adult immigration and residual toxicity

10

influence pitfall catches and recovery Of carabid populations after spraying. These
arguments against the use Of pitfall traps except Dixon and McKinley (1992), result from

higher numbers Of carabids caught in sprayed areas.

11

Profiles of carabids frequently caught during the course of these studies
Poecilus chalcites Say

Size 10.5-13 cm

Feeding. In a feeding study by Best and Beegle (1977), Poecilus chalcites fed on
larvae but did not feed on any vegetable material. Kirk (1975) reported that P. chalcites
eats eggs of western corn rootwonn (Diabrotica virngera LeConte) and pursues and eats
larvae and adults in the laboratory. There is little cannibalism among adults but larvae
ate eggs Of the same species and were a quite cannibalistic stage (Kirk 1975).

Habitat. P. chalcites occurs throughout Eastern North America (Lindroth 1969).
It prefers low, poorly drained fields where the soil is moist but not waterlogged. These
fields retain clods and cracks that provide living places. P. chalcites will remain in a field
year after year regardless Of crop being grown. Kirk (1975) speculated that this presence
in some fields year after year and none in other fields indicates favorable breeding sites
are limited. Very rainy and wet conditions are favorable for larvae.

Life cycle (IO-23°C) (Kirk 1975)

Stage Days

Egg 6.8

1st staditun 9

2'“I stadium 10.4
3rd stadium 14.1

 

Prepual 2.4
urinal 7.8
Total 50.5

12

The following is a summary from Kirk (1975) except where noted.

In South Dakota, P. chalcites overwinters 5-15 cm below the soil surface as an
adult and emerges as early as mid April if the soil thaws. There is increasing activity
from May until about mid-July after which there is a decrease until mid August when an
equal size second activity period starts and lasts through September. The second peak
includes the new generation adults.

Oviposition occurs in late May to mid August by overwintered adults. Peak
ovipostion is in mid-June with most ovaries spent by late July. Females place their eggs
in earthen cells beneath the soil surface. After eclosion the larvae probably live in the
existing spaces between soil agglomerates or make temporary burrows by pushing their
way between loose soil. The larvae pupate 2-15 cm below the surface. Females of the
new generation remained sexually immature until the following spring.

The number Of teneral adults peaked in early August. Teneral adults are fully
colored within one day of eclosion and are soft for one week. They become active on
surface and some fly at night. Lindroth (1969) reported that repeated captures in drift
material suggested good powers Of flight. Kirk (1975) thought that they only occasionally
fly in low numbers. He believed flight to be limited and with little dispersal from
favorable breeding sites. Poecilus chalcites can travel a maximum distance Of 91 m/day
but most individuals disperse relatively little averaging m/d (Best et al 1981). P. chalcites

does not burrow.

13

Anisodactylus sanctaecrucis (Fabr.)

Size. 83-105 mm

Feeding. Adults are not very canabalisitic. ..

Habitat. A. sanctaecrucis is transamerican (Lindroth 1969). A, sanctaecrucis
prefers moist soil such as crop land moist and poorly drained and is found in soil trash
and clods with Poecilus lucublandus, Poecilus chalcites, Stenolophus comma, Harpalus
herbivagus (Say), Clivinia inpressiforons (LeConte), and Evarthrus alernans (Casey)
(Kirk 1977).

Life cycle (20-23°C) (Kirk 1977)

Stage Days

Egg 5.7

1“ stadium 7.52

2“‘1 stadium 7.6

3rd stadium 8.7

prepupal 3.41

pupal 7.1
Mean developmental period takes 40 days

 

The following is a summary from Kirk (1975) except where noted.

Anisodactylus sanctaecrusis hibernate as adults and are active from spring thaws
to late September. From early June through August, the adults are good fliers. Kirk
(1977) noted that, “in the Spring, those disturbed in the field readily took flight, and I saw
them in May flying in the midst of heavy daytime flights Of Stenolophus comma.” These
adults probably lay eggs during May, June and early October. Eggs are more fragile than
most other carabid species. The teneral adults overwinter before ovipositing. Females
are known to produce eggs for as many as 3 years. Adults prepare overwintering

chambers beneath the soil surface by early October

14

ll

f:

Stenolophus comma Fabr.

Size. 5.5-7.7mm

Habitat. S. comma is widely distributed in North America. Lindroth (1969)
reported that S. comma was found in Open, usually sandy but not very moist places near
water. However, Rivard (1964) found that the species preferred moist, Open ground with
sparse vegetation. Kirk (1975), in a more in-depth investigation, found S. comma in
rangelands, pastures, and in fields Of the commonly grown crops. He found the largest
populations in cropland where the organic content Of the soil was high and the SOil
moisture was above average for the general area. Kirk found that S. comma is common
in soil cracks, the series Of Spaces in the soil beneath soil clOds, in tunnels in the soil and
under the surface trash in moist situations. When conditions are dry the beetles were
found deeper in soil cracks

Feeding. S. comma has been suspected of causing damage tO corn, however Kirk
(1975) did not find strong evidence for this behavior. Pausch (1979) found S. comma and
S. Iecontei to be primarily carnivorous (prefer insect eggs or small larvae) but they will
feed on nonanimal food when animal food is not available. Larvae, which are highly
cannibalistic, apparently feed on microorganisms that enter or grow in the burrows. In
the laboratory, adults eat only dead or weak adults unless overcrowded (Kirk 1975).
In a laboratory feeding study, S. comma would feed on the eggs and newly hatched larvae
of house flies and on dead western corn rootwonns (Diabriotica virgifera) adults, but not

live rootworm larvae (Pausch 1979).

15

 

or
by

tel

We

to r
hea
Flig

Spa:

With

cabb

Life cycle (20-23°C) (Kirk 1975)

Stage Days
Egg 5.4
1“t stadium 10.5
2"‘1 stadium 9.3
31rd stadium 12.8

Erna 9.4
Total 47.4

 

The following is a summary from Kirk (1975) except where noted.

Adult S. comma are present in the field during all months Of the year in South
Dakota Maximtun activity on the soil surface is during June and early July with minimal
activity during August and September. Adults hibernate in burrows 2-20 cm beneath the
soil surface. All females remained sexually immature until after overwintering. The first
oviposition occurs 15 days after the beetles emerge from hibernation, unless inactivated
by cold weather. Ovipostion peaks between mid May tO July. Eggs are laid singly in
cells located Off burrows that the females create in moist soil. Teneral adults appear from
Mid June to mid October. Newly emerged adults congregate, perhaps waiting until
weather conditions are suitable for flight.

When temperatures are over 15°C and the wind not over 10 knots from late April
to mid June, heavy dispersal flights occur during the day. The flights are especially
heavy when the field has been disturbed. After mid June, dispersal flights occur at night.
Flights are correlated with damp soil, higher RH, warm air, and not more moderate wind
speed.

S. comma is attracted tO light. Wayman et a1. (1976) found in cabbage plots lit
with black lights that S. comma numbers were higher and subsequent damage due tO

cabbage maggot (Delia radicum) was less.

16

Pterosticlrus melanarius Illiger

Size. 12-19mm

Habitat. Barlow (1970) found P. melanarius in Open or semi-Open areas and in
both cultivated and uncultivated land. He thought that it avoided barren places and
preferred areas with deep, rich soil.

Lifecycle. P. melanarius hibernate mainly in the larval stage, although some
adults overwinter. Adults have one activity-abundance cycle per year, which begins in
May and ends in October with the greatest numbers in July and August. P. melanarr’us
are summer-autumn breeders and females are gravid mainly in August and September.
Gravid females were present throughout the activity cycle but the proportion of gravid to

temeral females vary during the cycle. Some Of the teneral females are not gravid until

late July.

Clivinia impressifi'ons Lecont
Size. 5.9-7.0 mm
Habitat. Found in Eastern North America south to Texas. Lindroth 1968

reported them found in sandy lake Shores (Lindroth 1969).

17

The following summary is from (Pausch and Pausche 1980) except Where noted:

Feeding. Adults and larvae are primarily carnivorous but will feed on corn seed
when their primary food is absent or in short supply. They eat house fly eggs and larvae
as well as corn rootworm eggs and larvae, which they prefer over vegetation, seeds and
artificial diets. The larvae are extremely cannibalistic.

C. impressrfrons hibemates as an adult and is found active in soil in Illinois as
early as the end Of March. It is trapped through the summer until the temperature is
below 20C, with very few found after July. When spring temperatures are above normal,
C. impressifions activity peak occurs during May or June. However, when spring
temperatures are below normal, they peak in June or July. Lindroth (1968) reported that
C. impressifoms is apparently an excellent flier, caught at light traps. Pausch and

Pausche (1980) also found this species at light traps.

Poecilus lucublandus Say

Size. 9-14 mm

Habitat. P. lucublandus is found across North America and is commonly found
in cultivated fields with high moisture (Kirk 1971) and is most abundant in fields that are
damp but not waterlogged and is common in soil cracks. It is Often in close association
with S. comma (F .), P. chalcites (Say), Harpalus herbivagus Say, Amara carinata (Le

Conte) (Kirk 1971).

18

I61

ha]

Feeding. P. lucublandus feeds on insects and prefers dead invertebrates over live
ones (Best and Beegle 1977). Adults are cannibalistic when crowded in the laboratory

(Kirk 1971).

Life cycle (20-23°C) (Kirk 1971)

 

Stage Days
Egg 7
1“ stadium 1 1
2"6 stadium 13
3rd stadium 31
prepupal 4
meal 10
Total 76

P. lucublandus are spring breeders and have one generation per year. Adults
overwinter beneath the soil under crop residues in cultivated fields or pastures. There are
two periods Of activity during the season. Kirk (1971) measured the activity Of P.
lucublandus and found it slightly active at 5° C and quite active at 10-15°C. Teneral
adults are found in traps during August to September and early October. The first period
Of activity is in the spring, greater than fall activity. Adults do not fly.

Kirk (1971) surmised that they probably lay eggs in cells Off Of soil cracks or
clOds and have peak oviposition in June (May-Sept). The late summer period of adult
activity is from late August through September. They have continual egg production and

renewed production if conditions are favorable. The larvae are more subterranean in their

habits than adults.

19

ACTIVITY DENSITY OF CARABIDAE AND STAPHYLINIDAE IN ONION
FIELDS TREATED WITH CYROMAZINE AND CHLORPYRIF OS FOR
CONTROL OF ONION MAGGOT DELM AN TIQUA (MEIGEN) (DIPTERA:

ANT I-IOMYIIDAE)

ABSTRACT
Pitfall trap sampling Of commercial onion fields in southern Michigan in chlorpyrifos and
cyromazine treated areas was done over the 1996 and 1997 growing seasons. Total
carabid numbers were generally significantly higher in the cyromazine treated areas
compared to numbers in the chlorpyrifos treated areas Of fields. However, not all species
had higher numbers in the cyromazine areas. Total staphylinid numbers were also more
numerous in the cyromazine areas at all sites in the second year. Comparisons Of numbers
of other coleopterans and other arthropods were made and the seasonal patterns of

activity were examined.

20

Introduction
TO construct an integrated pest management strategy for onion production, it is important
to understand the impacts Of chlorpyrifos and cyromazine, the two currently available
chemical controls of onion maggot, on ground dwelling natural enemies. There have been
few studies on the impacts Of cyromazine on non-pest Species, though it is not toxic to the
adult coleopterans tested (Miller et a1. 1981, Friedel 1986, Wills et a1. 1990, Samsoe-
Petersen 1993). However, cyromazine is toxic to Colorado potato beetle (Leptinotarsa
decemlineata Say) larvae (Sirota & Grafius 1994).

The Obj ective of this study was to compare the carabid and staphylinid
populations in commercial fields treated with the organophosphate chlorpyrifos, or with
cyromazine, an insect growth regulator. It was our hypothesis that the newer and
“softer” insect grthh inhibitor would be less disruptive to the natural biological controls.
Pitfall traps were used to compare the soil surface fauna, the group of arthropods most
likely to come into contact with controls applied to the soil (See literature review). Baars
(1979) demonstrated that the use of continuous pitfall sampling could be used as a
relative measure of the size of carabid populations. In the present work, comparisons of
populations were made within individual fields with the same vegetation and under the

same management practices.

Materials and Methods

Sites. F our commercial onion fields in southern Michigan were used as field
sites, one near Grant (Newaygo CO.), two (one in 1997) near Hudsonville (Ottawa CO.),
and one near Stockbridge (Ingham CO.) (Figure 1). Farm and field descriptions are listed

in Table 1. The crops Of the previous season were different at each farm. All Of these

21

 

 

Figure 1. Map Of field sites in Michigan

22

Table 1. Farm field Sites and descriptions. Different fields were used in

successive years at each farm.

 

 

Experiment year:

Farm previous rotation Farm description

Ottawa 1 1996 : Celery NO raised beds. Four onion rows per
1997 : Celery bed. Limited cultivating during

season. NO foliar insecticide sprays
for adult onion maggots. Used spray
threshold for thrips. High organic
muck.

 

Ottawa 2 1996 : Onions

NO rotation. High pesticide usage
including foliar insecticides and
extra soil drenches for onion maggot
larvae. Cultivated frequently.

 

Newaygo 1996 : Carrots
1997 : Carrots

Raised beds. Three onion rows per
bed. NO foliar insecticide Sprays for
adult onion maggot. Used spray
threshold for thrips. Sandy muck
soil.

 

 

Ingham 1996 :PotatO
1997 :Onions

 

 

Raised beds. Three onion rows per
bed. NO foliar insecticide Sprays for
adult onion maggots. Used spray
threshold for thrips. Marl patches in
muck soil. Spirea planted as
hedgrows.

 

23

 

crops are full season crops. Potatoes form a full canopy cover and, therefore, there is
probably little pesticide penetration to the soil. Celery and carrot canopies are not as
continuous, though may inhibit pesticide penetration to the soil especially late in the
season.

At each farm, the grower had a field in which he had planted a portion Of the area
with cyromazine coated seed (50g active ingredient (AI) per kg seed) and a portion with
untreated seed and granular chlorpyrifos (5.7g AI per 1000 row m) placed in the seed
furrow (Ottawa CO. 1996, Site 1 fonofos was used instead of chlorpyrifos). It was in
these adjacent chlorpyrifos and cyromazine field areas that comparisons Of fauna were
made.

Sampling methods. Activity densities, the number Of beetles that enter the trap
per unit time, were measured using pitfall traps that were protected from rain and
irrigation by covers of aluminum flashing suspended 2-3 cm over the traps by nails. The
pitfall traps were made out of two plastic containers. The outer container remained in the
soil for the duration Of the experiment and limited soil disruption when traps were
checked. In 1996, the traps were made from Solo brand cups (9.5 cm dia., 10.5 cm deep)
that contained 5 cm of 50% ethylene glycol. In 1997, the plastic cups (11 cm dia., 14 cm
deep) contained 5 cm soapy water.

Traps were placed in diagonal lines in the fields. In 1996, there were five traps
placed in two diagonal lines 12-18 raised beds apart. The space between traps within a
line was 30 m. In 1997, there were nine traps in three diagonal lines 46 m apart. The
space between traps within a line was 8-9 m. The trapped fauna was sorted to family;

most carabids were identified to species level (Lindroth 1968).

24

Statistics. The numbers Of a species, family, or group per insecticide treatment
per field location was totaled for the entire trapping season. Means of seasonal catch per
trap in the two treatments were compared via a 2-sample Poisson comparison test that
was run as a log linear model with a Chi square table to Obtain a critical value (PROC
GENMOD, SAS Institute 1994). Since each field represented a single non-replicable
experimental unit, numbers were not compared between fields. In the figures that follow,
the arithmetic means are used.

Results and Discussion

Carabids. In 1996, P. chalcites (Say) was the most numerous carabid species at
the two Ottawa CO. Sites and the Ingham CO. Site in the cyromazine, chlorpyrifos, fonofos
areas (Table 2). In 1997, A. sanctaecrucis was the most numerous species in the
chlorpyrifos areas, while P. chalcites was most numerous in the cyromazine areas at the
Ottawa 1 and Ingham CO. sites. In both years, the most numerous species at the
Newaygo site was P. melanarius in both insecticide treatments. It is interesting to note
that in pitfall surveys Of Michigan onion fields in the late 19703 and early 19803 report a
different species composition. From early June to early September of 1981 and 1982,
Motyka and Edens ( 1984) pitfall trapped carabids at two commercial fields in Newaygo
CO. Only A. sanctaecrucis numbers averaged between 3-9 per collection date, while the
rest of the carabid species including P. chalcites (=Pterostichus chalcites) and P.
melanarius were rare (average <3 per collection date) or were absent. Drummond (1982)
in 1978 and 1979 pitfall trapped carabids in commercial onion fields and found
Stenolophus spp. (=Agnoderus spp.) and A. sanctaecrucis the most common. The

numbers of Amara spp., B. quadrimaculatum (L.), C. impressifrons,

25

 

 

 

 

 

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26

and Pterostichus spp. were up to an order of magnitude lower than the number of
Stenolophus spp. and A. sanctaecrucis. Since the time Of these studies, onion production
systems have changed. There is now interplanting with barley or rye, more crop rotation,
and less foliar insecticide use (Grafius 1999).

The mean total number Of carabids was higher in the cyromazine area than in the
chlorpyrifos fonofos area at all four farm Sites in 1996 (Figure 2). This difference was
significant in three Of the four fields (Table 3). In 1997, at the Ottawa and Newaygo field
Sites there were Significantly more carabids in the cyromazine areas than in the
chlorpyrifos areas, however, at the Ingham site there were significantly more carabids in
the chlorpyrifos area than in the cyromazine area. This difference between the 1997
Ingham county site and the other sites was due to A. sanctaecrucis and will be discussed
later. The largest peak of carabid activity during the trapping period was in late June
(Figure 3).

The number of P. chalcites, a common carabid at all field Sites, was higher in the
cyromazine treated areas than in the chlorpyrifos or fonofos treated areas at three Of the
four sites in 1996 (Figure 4). In 1997, there were fewer P. chalcites found even though
the number of trapping days was higher in 1997. P. chalcites was Significantly more
numerous in the cyromazine treated area than in the chlorpyrifos treated area at Ottawa 1
and significantly less numerous in the cyromazine treated area than in the chlorpyrifos
treated area at the Newaygo site. Reed et a1. (1992) found that chlorpyrifos was more
toxic to P. chalcites than fonofos and terbufos. The reported effects of terbufos and

caroburan on P. chalcites

27

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

130 , *
1‘: 160 1_ I Chlorpynfos ____,
g: m 2140 -2 I Fonofos __
8 a,“ §120 -2 El Cyromazine ._
g 1' E 100 —
E E s 80 * 66
C t to 60 I * __
C
3 8 3. 4o .—
2 20 ~ ~—
,_ 3 i
Ottawa 1 Ottawa 2 Newaygo Ingham
Site
B. 1997
180
E 160 I—IChlorpyrifos
3’ LI] 9 140 ‘4 UCyromazine
8 05 *3 120
o :5 - 100
E ‘3- 2 80 f
a g 8
C <0 60 -
c: E 3’,
8 av 40
2 20 -
0 _
Ottawa 1 . Newaygo Ingham
Site

 

 

 

Figure 2. Total numbers of all carabids caught per trap in

chlorpyrifos and cyromazine treated areas located in four different onion

field Sites during the 1996 and 1997 growing seasons

(Poisson means = variance; * =Significantly different, p<0.05)

 

Table 3. Chi square values for comparisons Of total seasonal pitfall catches in

chlorpyrifos and cyromazine in four different onion field sites in 1996 (5 traps per

insecticide treatment) and 1997 (9 traps per insecticide treatment).

 

All carabids

Poecilus
chalcites

Anisodactylus
sanctaecrucis

Pterostichus
melanarius
Clivinia
impressifrons
Stenolophus

comma &
Iecontei

Poecilus
lucublandus

Bembidon

quadrimacu-
Iatum

Staphylinids

Coleomegilla
maculata

Cocinella
septumpuntata

Hippodamia
spp.

Anthicids
Spiders

Earthworm

x2

 

< 0.05

Ottawa 1 Newaygo Ingham

1226 - 1.222 122fi 1226 1221 1220 1221
0.1 9.7 7.0 95.4 17.4
< 0. 05 < 0.05 < 0. 05 < 0. 05 < 0. 05
101.9 82.8 9.7 79.9 3.5
< 0. 05 < 0.05 < 0. 05 < 0.05 0.06
0.2 3.7 2.0 6.0 127.1
0.65 0. 05 0.15 < 0.05 < 0.05
1.3 11.0 3.0 17.4
0.24 < 0. 05 0.08 - < 0.051

2.7 8.3 13.1
- 0.10 < 0.05 - < 0.05
4.1 0.1 1.0 1 .0 9.8
< 0. 05 0.75 0.30 0. 31 < 0.05
1.9 1.1 0.2 0.6 0.5
0.16 0.26 0.59 0. 41 0.45
1.3 2.7 11.8 18.5 6.9
0.24 0.10 < 0.05 < 0.05 < 0.05
0.3 7.7 53.4 40.4 23.0
0.58 <0.05 <0.05 < 0.05 < 0.05
4. 8 0.8 0.2 5.8 1. 5
< 0. 05 0.36 0.62 < 0. 05 0.21
3.3 14.5 1. 3
- 0.07 < 0.05 - 0.25
4.1 5.2 0.0 5.0
< 0. 05 < 0.05 0.94 - < 0. 05
72.3 9.1 5.3 18.4 68.1
< 0.05 < 0. 05 < 0.05 < 0. 05 < 0. 05
23.3 9. 2 2.5 4.0 7. 0
<0.05 <0.05 0.1] <0.05 <0.05
24.161

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

    

 

 

 

 

 

 

 

 

A. Ottawa] B. Ottawa 2
37 25 1996 '25 20 1996
I
2 ..
E 0 E 15 I]
a. 15 a '1
g 10 g 10 4“
g 5 E 5 '1
E 0 E
2 2 ° - L .
125 15° 1753 20° 225 25° 125 150 175 200 225 250
Julian day Julian day
3 25 1997 1997, Site not used
§ 20
a 15
g 10
: 5
3 0
g 125 150 175 200 225 250
2 Julian day
C. N ewaygo D. Ingham
.2 12 x 40 1996
8 8
E 9 E 30
Q Q
g 6 g 20
‘ 3 t 10
E S
g 0 g 0
Z 125 150 175 225 250 Z 125 150 175 200 225 250
Julian day Julian day
1997 1997
E 12 § 4°
\ 9 E 30
I Q
E 6 g 20
g 3 . >4; 3 10
a 0 6 1 m 1 g 0 - ‘ . v 1
z 125 150 175 200 225 250 z 125 150 175 200 225 250
Julian day Julian day

 

 

 

 

     

 

 

 

 

Figure 3. Number Of all carabids caught per trap per week in chlorpyrifos

and cyromazine treatments in four different onion field sites in 1996 and 1997.

(4_ = chlorpyrifos, _._ = f0n0f08,_... = cyromazine, I = insecticide spray)

30

 

 

A. 1996

 

 

  

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

160 *,

g, 140 - orpyn 08 +4
3 ui 7.; 120 _ [Fonofos I

{E <0 ‘5 100 DCyromazine _ I T
Q \' Z d F—
.o + m 30 ___1
§ 3?. 60 * __
c t 3 40 T *

w 2. r c
2 0 J ,

Ottawa1 Ottawa 2 . Newaygo Ingham
Site
B. 1997
160 .

E 140 WfiIChlorpynfos

g“; :5 120 ____uCyromazine

a f _.9_. 100

£11380 .

g 1: 3 60

c a 40 _ r
g 9.8% 20 * ' t

F—
o -
Ottawa 1

 

 

Newaygo Ingham
Site

 

 

Figure 4. Total numbers of Poecilus chalcites caught per trap in

chlorpyrifos and cyromazine treated areas located in four different onion

field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; " =significantly difl‘erent p<0.05)

31

have ranged from toxic to no effect (Gholson et a1. 1978, Hsin et a1. 1979, Lesiewicz et a1
1984)

Kirk (1975) reported two equal size activity peaks of P. chalcites in South
Dakota, one starting in May and peaking to July and a second in mid August tluough
September. The second peak, normally made up of teneral adults was absent or occurred
after the traps were removed from the fields in this study (Figure 5).

Many more A. sanctaecrucis were trapped in 1997 than in 1996. In both years
there were field sites with significant differences between the numbers in the two
treatments, but there was no prevailing pattern of A. sanctaecrucis numbers being higher
in the cyromazine or chlorpyrifos areas (Figure 6). A. sanctaecrusis adults are good fliers
from early June through August (Kirk 197 7) and therefore may not have made contact
with the insecticide or could immigrate quickly into the field. Activity peak occurred
between 150-175 Julian days (Figure 7). Drummond (1982) found three peaks of adult
activity in Michigan, though the largest peak was between 190-230 Julian days.

P. melanarius was the most common species found at the Newaygo site;
significantly more were trapped in the cyromazine areas at the Newaygo site in 1996, the
Ottawa 1 site in 1997, and the Ingham site in 1997 than in corresponding chlorpyrifos
areas (Figure 8). While not statistically significant, the mean number of P. melanarius
was higher in the cyromazine area than in the chlorpyrifos area at Newaygo in 1997.

Bale et al. (1992) found P. melanarius to be susceptible to chlorpyrifos. The activity

peak matched that reported by Barlow (1970) in July and August. (Figure 9).

32

A. Ottawa 1 B. Ottawa 2

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

x 18 1996 x 20 1995
i 3 -l
\ E 15
5 :1 10 “vi
\ : 5 '.
g s
3 ~ g o . , -‘s . .
z 125 150 175 200 225 250 z 125 150 175 200 225 250
Julian day Julian day l
§ ,8 1997 1997, Site not used
3 15
3 12
g 9
t 6
3 3
g 0
Z 125 150 175 200 225 250
Julian day
C. Newaygo D. Ingham
x x 1996
\ 3 \
Q Q
E 2 8
E 3
.8. ° 5
Z 125 150 175 200 225 250 Z 125 150 175 200 225 250
Julian day Julian day
.2 1997 x 1997
3 4 g 40
3. 3 .3 30
Q Q
20
g 2 A E .
g i“.'. ‘\ é O ‘l—Jr TV.
3 0 -—I-l-I" 1 1 ‘ MCJ :1 125 150 175 200 225 250
Z 125 150 175 200 225 250 Z Junan day
Julian day

 

 

 

 

 

 

Figure 5. Number of Poecilus chalcites caught per trap per week in chlorpyrifos

and cyromazine treafinents in four different onion field sites in 1996 and 1997.

( + = chlorpyrifos, _._ = fonofos,_-_. = cyromazine, l = insecticide spray)

33

 

A. 1996

 

 

   

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

l
i
l 50
[E orpyn os
lg)“.i :40 — .Fonofos
l8 <15 {95 [jCyromazine
11;, \- :30
in + 2
E 8 820
C t 8 *
1§ 8. £110 7!,-
‘2

o __.*i____+l --| {Fl
‘ Ottawa 1 Ottawa 2 _ Newaygo Ingham

Site

B 1997

60 _ .
jg 50 - .Chlorpyrltosl T *
3 LL] ’2 UCyromazmei
§ as g 40
g :g 30
3 g g 20 -
= '1‘:
g Q3 10 -_ Q

0 _ fl

Ottawa 1 Site Newaygo Ingham

 

 

 

Figure 6. Total numbers of Anisodactylus sanctaecrusis caught per
trap in chlorpyrifos and cyromazine treated areas located in four different
onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

34

A. Ottawa 1 B. Ottawa 2

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

 

 

 

 

 

 

 

 

 

 

 

 

 

   

1996 1996 ‘
-§ 15 1:: 1.5
3 12 3 \-
-~ 9 K 1 -"
Q Q . 2
g 6 g 05 . ‘
5 ‘25 15° ‘7? 20° 225 25° 5: 125 150 175 200 225 250
“'3" days Julian days
x 1997 1997, Site not used
15
i 12
a 9
g 6
: 3
3 o
:5, 125 150 175 200 225 250
2 Julian day
C. Newaygo D. Ingham
1996
25 2 35 18
a 1.5 E 15
a. a. 12
E 1 g 9
t 0.5 t g
3 3
E 0 E 0 '
5 125 150 175 225 250 2 125 150 175 200 225 250
Julian day Julian day
1997 1
g 2 a; 18 997
0
\ 1.5 315
a a 12
g g 9
2‘: t 6
g 3 3 .
n . .-
3 - Sui-'4‘. g 0
125 150 175 200 225 250 z 125 150 175 200 225 250
Julian day Julian day

 

 

 

 

 

Figure 7. Number of Anisodactylus sanctaecrusis caught per trap per week
in chlorpyrifos and cyromazine treatments in four different onion field sites in 1996

and 1997.

(4. = chlorpyrifos, _._ = fonofos,... = cyromazine, | = insecticide spray)

35

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

14
E 12 dfl'Chlorpyn'fos
3’ uj 1‘; 10 DCyromazme ..
M :5 8 =5
a) \ -—
.o + <0 .—
5 55 6 F
c '3 ‘“ 4 .
5 3:3, ' r
g 2

0 —-—

Ottawa 1 Ottawa 2 Newaygo Ingham
Site

B. 1997
‘ , A ,7 , Q Q 7 -
‘ 18
1E 15 _ .Chlorpyrifos
ESim z: 14 — DCyromazine T
i8 05 g 12 T“
12 is 1°
*5 a 8 8
C C m 6
C o O a]:
‘8 0.3 4 :52.
2 2 ‘TIT

o [—51

Ottawa 1 Newaygo Ingham
Site

 

Figure 8. Total numbers of Pterostichus melanarius caught per
trap in chlorpyrifos and cyromazine treated areas located in four different
onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly difi‘erent, p>0.05)

36

 

A. Ottawa 1

 

 

 

 

 

 

 

 

 

 

 

None caught

A. Ottawa 1

x 05 1997

§ 0.4

E 0.3

g 0.2

r 0.1

2 125 150 175 200 225 250
Julian day

C. Newaygo

E 5

g 4

g 3

E 2

:3

Z 1

0
125 150 175 200 225 250

Julian day
1997

§ 5

E 4

O- 3

22

g 1

g o

2 125 150 175 200 225 250
Julian day

 

 

 

B. Ottawa 2
None caught

B. Ottawa 2
1997, Site not used

 

 

 

 

 

 

 

D. Ingham
None caught
a: 1997
8 0.6 -
3 .I lie
‘ 0.4 ' - - .
Q ,' 1. I
g l- . _ .' z -'
t 0-2 "I %:
8 ." '- ."
Z 125 150 175 200 225 250
Julian day

 

 

Figure 9. Number of Pterostichus melanarius caught per trap per week in chlorpyrifos

and cyromazine treatnents in four different onion field sites in 1996 and 1997.

(4_ = chlorpyrifos, _._ .= cyromazine, l = insecticide spray)

37

 

Another species that tended to be more prevalent in the cyromazine areas was
Clivina impressifi'ons (Lecont). Two of the three fields had significantly more of C.
impressifrons in 1997 (Figure 10). Drummond (1982) and Pausch & Pausch (1980)
found that C. impressifrons had two generations per year, a summer peak (140-210 Julian
day) and a fall peak (250-280 Julian day) which is similar to the 1997 catches in this
study (Figure 11). C. impressrfrons is a good flier, but it does have large fossorial legs
and may come into contact with pesticides while digging in the soil.

Carabids such as Stenolophus spp. Poecilus lucublandus (Say), and B.
quadrimaculatum had seasonal means that were not consistantly higher in either
treatment (Figures 12-14). In South Dakota, S. comma has two peaks of adult activity,
one in June and one in September (Kirk 1875), and in Wisconsin it has three peaks
(W aymann et a1. 1976). Drummond (1982) found in early spring a third peak in
Michigan as well. The trapping period in this study only caught the second activity
period (Figure 15). Poecilus lucublandus, in South Dakota, has a large spring activity
peak and a smaller fall peak. In this study there does not appear to be a definite pattern
(Figure 16).

While Bembidion spp. have been implicated as good Delia spp. egg predators in
many studies, ( Wishart et a1. 1956, Coaker & Williams 1963, Coaker 1965, Perron 1972,
Drummond 1982, Andersen et a1. 1983, Andersen & Shannan 1983, Tomlin et al.1985,
Grafius & Warner 1989) they are not the most frequently seen or caught carabid in the
commercial onion fields. In a habitat study done by Warner (1986), more B.
quadrimacutlatum were caught outside of an onion field than inside of it.

1 Stenolophus comma (F .)and Stenolophus Iecontei Chaudoir have similar biologies and can only
be taxonomically separated by the relative shape of the penis sac armature (Lindroth 1969).
Therefore, they were not distinguished as two different species.

38

 

1997

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

 

 

 

9
E 3 - Chlorpyrifos *
3’ uj c7 DCyromazine T
§w§6 if
3 t a 5 i ~——~——*——
E 3 §4 _ T
g b m 3 I 1 .l.
5 2.1.2 Si *
d)
2 1 .

0 -

Ottawa 1 Newaygo Ingham
Site

 

Figure 10. Total numbers of Clivinia impressifrons caught per trap in
chlorpyrifos and cyromazine treated areas located in four difi'erent onion
field sites during the 1997 growing season.

(Poisson means = variance; * =significantly different, p<0.05)

39

 

A. Ottawa 1 B. Ottawa 2

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Site not used
is 1997
3
Q
g
'5
.0
g 125 150 175 200 225 250
2 Julian day
C. Newaygo D. Ingham
1 97 1997
1 2 9 i 3
E 1.5 E I
Q 2 : .
I .
E 1 " g "
x ." . -_ \ 1 -' -
g 0.5 1 O .I. . 5‘ "v. ‘ l. E .6. e. .
g 0 4H1 1 f r W E o - '. . .
z 125 150 175 200 225 250 Z 125 150 175 200 225 250
Julian day Julian day

 

 

 

 

 

Figure 11. Nurrber of Clivinia impressifions caught per trap per week in
chlorpyrifos and cyromazine treatments in four different onion field sites in 1997.

= chlorpyrifos, _ .= cyrormzine, = insecticide spray)
I- l

40

 

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

 

 

 

5
E ChlorpyrITos
gm- 9 4 . [Fonofos
8 <15 1‘3 3 DCyromazine
ii? i
a E 8 2
C a: m '
§ 33. 1 * I T]
2
O -
Ottawa1 Ottawa 2 ‘ Newaygo Ingham
Site
8. 1997
7
fig . 6 __‘.Chlorpyrifos
5 a 3:3)- 5 __0Cyromazme
5 g g 4
5 a 8 3
g t 3 2 -
53 312.1 _
2
o _
Ottawa 1 Site Newaygo ingham

 

 

 

Figure 12. Total numbers of Stenolophus comma & Iecontei caught
per trap in chlorpyrifos and cyromazine treated areas located in four
different onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

41

A. 1996

 

 

 

 

 

 

 

 

 

   

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

5
35 Chlorpyrifos
9.4.; c 4 - [Fonofos
§03 g 3 UCyromazine
o r — *
5 a 2
g a 8 2 I
C t 8
g a $1 - - ._ «-
2 A .
o - J fl
Ottawa 1 Ottawa 2 Site Newaygo Ingham
B. 1997
4
U) . .
a u; r: 3 .mUCyromazme
3 a) £3
:3 i 2
ED 3% 2 .t
a g 8
c m 1
8 a. £9
2 i
0 - _.
Ottawa 1 Site Newaygo Ingham

 

 

 

Figure 13. Total numbers of Poecilus Iucublandus caught per trap in

chlorpyrifos and cyromazine treated areas located in four different onion

field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

42

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 
 
   

 

 

 

 

6 :1:
E 5 Chlorpyrifos I
3’ LL] 2 I Fonofos '
§ 03' g 4 - [jCyromazine ——1
o \' 2:
"E: a 2 3 _
3 g g 2 _~
= 8
é ‘13 1 __
0 Mi
Ottawa 1 Ottawa 2 Newaygo Ingham
Site
B. 1997
6
E 5 .Chlorpyrifos
3’ uj :5 DCyromazine
8 05 L5 4
g $ '5 3
§§§ *1 *
c: t 8 2
saw 1 I
2
0 d—a - ll
Ottawa 1 Newaygo Ingham
Site

 

 

 

Figure 14. Total numbers of Bembidion quadrimaculatum caught per

trap in chlorpyrifos and cyromazine treated areas located in four difierent
onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

43

A.Ottawal

 

 

 

 

 

 

 

1997
fig 2
31.5
a.
1
g
:05
g o
3 125 150 175 200 225 250
Z .
Julian day
C. Newaygo
x 1 1997
“0.6
E
\ 0.4
0.2
E
g 0
125 150 175 200 225 250
Julian day

 

 

 

 

B. Ottawa 2
None caught
D. Ingham
3 1997

 

>

 

 

Number I trap I week
‘ . \o
,'
/

O
l
I
-.
I
I
O
O
I
O

 

 

1 25 1 50 1 75 200 225

Julian day

 

m

 

250

 

Figure 15. Number of Stenolophus comma & Iecontei caught per trap per week in

chlorpyrifos and cyromazine treatments in four different onion field sites in 1997.

( = chlorpyrifos, _'j-' cyromazine, l = insecticide spray)

 

A. Ottawa 1

 

 

 

 

 

 

B. Ottawa 2

 

0.5
0.4
0.3
0.2
0.1

0

 

 

 

 

Number I trap I week

 

125

150

1996

1

 

200 225 250

Julian day

 

 

1997, Site not used

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

'§ 15 1996

3 ' 1

‘ 1

n.

E 0.5. I

5 125 150 175 200 225 250
Julianday
1997

E 1.5

\ 1

a.

E 0.5

é 0.1—W

g 25 150 175 200 225 250
Julianday

C.Newaygo
1996

'33? 1.5

3 a

a 1 34*

g It N.

t 0.5 ' ‘

3 1 V 1'

E o

3 r rv [I 1

125 150 175 200 225 250

Julianday

i 1.5 1997

3

\ 1

E

\0.5

2 9 .'.

Z 125 150 175 200 225 250
Julianday

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Dlngham

x 1996

£15

3. 1

g

:05 '

: 0~——r——o-i+I-AI1

Z 125 150 175 200 225 250
Julianday
1997

131.5

0

3

Q 1

g

:05

8

g o_ . ...

Z 125 150 175 200 225 250
Julianday

 

 

Figure 16. Number of Poecilus lucublandus caught per trap per week in

chlorpyrifos and cyromazine treatments in four different onion field sites in 1996 and 1997.

(_._ = chlorpyrifos, . = fonofos,_-_' = cyromazine, l = insecticide spray)

45

 

Staphylinids. In 1996, staphylinids were significantly more numerous in
the cyromazine treated area than in chlorpyrifos treated area at the Ingham site. At the
Ottawa 2 site there were more staphylinids in the cyromazine treated area than in the
fonofos treated area.(Figure 17). Moreover, in 1997 they were significantly more
numerous in the cyromazine treated areas than in the chlorpyrifos treated areas in all
three sites. The activity peaks during the season are composed of many different species
and differ between years and fields (Figure 18).

Other arthropods. Table 4 lists some of the other organisms that were found in
the pitfall traps. The numbers of organisms such as weevils, elaterids, grasshoppers and
crickets do not differ regularly nor much between the two areas of the fields sampled.
Even though all the chlorpyrifos traps were on one side of the field and all the
cyromazine traps on the other, there does not appear to be a large difference in the
numbers or taxonomic composition of other arthropods.

Anthicids. In 1996, Anthicidae (Coleoptera) were more numerous in the
chlorpyrifos areas than in the cyromazine areas in two sites, more numerous in the
cyromazine than in the chlorpyrifos at the Ottawa 2 site, and in equal numbers in both
cyromazine and chlorpyrifos in the fourth site (Figure 19). The timing of peak activity
varied between years and sites (Figure 20). However, in 1997 anthicids were more
numerous in the chlorpyrifos areas at all three sites than in the cyromazine areas.
Anthicids are small beetles that are found in many locations and habitats. Adults of many
species are found in association with decaying vegetation on the surface of the ground.
Adults are probably omnivorous (Young 1991) though some are predacious with reports

of attack on mites, scales or other small invertebrates on cotton and pine vegetation

46

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

60
.. mlorpyrifos
g” "j 9 5° IFonofos
8 :15 g 40 DCyromazine
g E E 30
3 g 8 *
c b 8 20
C
E 33 1o :1; i E
O L—‘E—I ".1
Ottawa 1 Ottawa 2 Newaygo Ingham
Site
B. 1997
70 .
35-) 60 M.Chlorpynfos at: .1
: uj 5: gCyromazine
.2 ? E 40
§ % 3 3° 1:
c b °° 20 ’k
1:: fig 3 .
g -10 f j:
0 . ,
Ottawa 1 Newaygo Ingham
Site

 

 

 

Figure 17. Total numbers of all staphylinids caught per trap in
chlorpyrifos and cyromazine treated areas located in four different onion field

sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

47

A. Ottawa 1

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

'§ 2.5
E 2
a.‘L5
g 1
.. 0.5
E o
5 125 150 175 200 225 250
Julianday
1997
1:5 2.5
3 2
E 1.5
E 1
s 0.5
12 o
g 125 150 175 200 225 250
Julianday
C.Newaygo
1996
g e
I; 6
g .
2 2
E I
3 o u‘
z I 'II—7 I
125 150 175 200 225 250
Julianday
a 1997
g ~'. .I.' I :1
E 6 T}. ,. 1 ., '-
.. 4 f ‘i /1-, W
E 2 . " 1'
E - V
2 0 r. r 1 l
125 150 175 200 225 250
Julianday

 

 

 

B. Ottawa 2

 

Number I trap I week
0 .5 N
O OI A 0| N at

125

150

 

 

175 200 225 250
Julian day

 

 

1997, Site not used

D. Ingham

 

Number/traplweek
O N «In a: G

125 150

 

1996

 

175

200 225

250

Julian day

 

 

1997

 

 

 

 

 

 

 

 

T

150

Number/trap/week
O N h 0) (D

 

175 200 225 250
Julian day

 

 

Figure 18. Number of all staphylinids caught per trap per week in chlorpyrifos

and cyromazine treatments in four different onion field sites in 1996 and 1997.

(.Q_ = chlorpyrifos... = fonofos,.... = cyromazine,| = insecticide spray)

48

 

 

 

 

 

 

 

 

N o - - .N NN N N - - N N o _ Eggs
- - N N - - N : o N 3.23
_ a _ _ - - N v gamma
_ N - - _ o - - o _ N N - - 8255
_ N N N N_ N N NN - - - - - - Sages
N N - - N N - - - - N a. a _ £8320
N N_ - - N N - - - - N N - - Neofieaz ”0823
N N N : N N - - N N N S - - ”83:2
3. NN N _ N o _ N - - N N - - 325%:
N 2 N N N _ _ N o - - NN 2 N N seaoaaau
NN N: N S NNN NNN NN NN N _ N 3. N N 93385 3.;
N_ N N N «N NN N _ o o 2 N N N .& easeuofii
N N_ o N N: No o N N N Na N - - assuage... £8389
NN NN N 2 2 N z N_ N a NN NN N N 3382. enamusoaoo
N_ N_ NN 8 N N S N NN N_ NN NN 2 2 3.5.5 as...
NN N N_ N 2 N N N N N N N N o E... 550
N_ N_ NN 8 N N 2 N NN 2 NN NN E 2 35a... 38w
N _ - - N N - - - - N _ - - 998855 usage
NN NN NNN NN. NNN N2 Na. Na. NN Nv E N NE N4 @82va 0852
2: SN NN Nv N— :2 NN NN 3 NN N: NNN NN N: 32935. 3.;
8 NE a N N a. NN NN Na N _ N N NN .& 3882
_N N2 NN :. 3; NN_ _N NN NN NN NE SN Na NN .283 cases 55o
L— < N? < _ _ m c T e m _ n i; 1 _ n < n fl Fl
IE: 1.5.... _ _ 5: 1.52 _ _ be: _ _ 3.: NE”—
IlEauE _ _ E r Pk E _ _ E

 

 

 

Nouoaomuo 63%!”on .8bi9efiou<
.08: 9:3an 2:3 ufl .95 Each 03882: Ba Nag aw a 39.8 83823 3823 we boa—E :53. .v 033.

49

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

35
E 30 TChlorpyrifos
g,”- c T * [Fonofos
3 05 g 25 DCyromazine
g 8- 3 15 _
C b (u
c a Q) 10 ..
M Q 9’
g 5-
0 _
Ottawa 1 Ottawa 2 Newaygo Ingham
Site
B. 1997

0)
0|

- Chlorpyrifos
g Cyromazine

OD
010

01

2
20
1
1

C

"j:
«6%
4'...
“2
a.
98
“m
5d)
83;

Mean number caught

OUI

Ottawa 1 Site Newaygo Ingham

 

Figure 19. Total numbers of all anthicids caught per trap in
chlorpyrifos and cyromazine treated areas located in four different onion

field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

50

A.0ttawal

 

.A
O

Number/traplweek
O N «b O) on

125 150

 

1 996

175 200 225 250
Julian day

 

 

 

10

125 150

Number! trap/week
O N .b O) on

 

 

1997

175 200 225 250
Julian day

 

 

C. N ewaygo

 

Number/trapreek
O N hr 03 G

1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

125 150 175 225 250
Julianday
1997
§ 8
E 6
E4
‘ 2
I, .
to. a T
2 125 150 175 200 225 250
Julianday

 

 

B. Ottawaz

 

1996

 

Number/traplweek
O N «b a: on

 

 

 

 

 

 

 

 

 

 

 

Figure 20. Number of anthicids caught per trap per week in chlorpyrifos

and cyromazine treatments in four different onion field sites in 1996 and 1997.

( = chlorpyrifos, = fonofos,_ , = cyromazine,
4— -O- I- |

125 150 1 200 225 250

Julian day

1997, Site not used

D.Ingham

x 10 1996

§ 8

a 6

g 4

T. 2

g 0

3 125 150 175 200 225 250

2 Julian day

-§ 10

3 8

3 6

g 4

- 2

é o

g 125 150 175 200 225 250
Julian day

= insecticide spray)

51

(Werner & Chandler 1995). Larvae are generally associated with decaying vegetative
materials where most are omnivorous or mycetophagous; there are a few reports of
anthicids feeding on insect eggs and pupae (Young 1991). In this study, the anthicids
were frequently observed on the soil surface, but never on the onion plants. Motyka &
Edens (1984) collected an Anthicus sp. consistently in Michigan onion fields, but never in
large numbers; they noted a peak of activity in August.

Spiders. There were more spiders in the fonofos area than in the cyromazine
treated area at the Ottawa 2 site in 1996; at the two other sites there were more spiders in
the cyromazine treated areas than in the chlorpyrifos treated areas (Figure 21-22). This
pattern continues into 1997 with more spiders in the cyromazine treated areas and
chlorpyrifos treated areas at Ottawa 1 and Ingham sites. There appeared to be the most
spider activity in the middle of the season (Figure 22).

Coccinelids. Coleomegilla maculata (DeG.) was significantly more numerous in
the chlorpyrifos treated area than in the cyromazine area in two sites in 1996 (Figure 23).
In 1997, there were no significant differences between treatments, however there
appeared to be a trend of more C. maculata in the chlorpyrifos areas than in the
cyromazine areas. No pattern of relative abundance appears in Figure 24 for Coccinella
septumpunctata (L.). The Hippodamia spp. were more numerous in cyromazine areas at
two sites in 1997, but at other sites the species was not common or was of the same

abundance in both treatments (Figure 25).

52

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

60

z Chlorpyrifos *
a, 50 -

: uj E lFonofos

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60

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Figure 21. Total numbers of all spiders caught per trap in
chlorpyrifos and cyromazine treated areas located in four difl‘erent onion
field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

53

 

A. Ottawa 1

 

Number/trap/week
O N h a: m

1996

 

 

 

 

 

 

 

 

125 150 175 200 225 250

Julian day
1997

g a

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2 Julian day

C. Newaygo
1996

Number/traplweek
O -I N 0) ¢

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175 200
Julian day

225

 

250

 

 

 

Number/traplweek
O -I N (d b

125

150

 

1 997

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Julian day

225

 

250

 

 

B. Ottawa 2

 

125

150

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0 -I N w h

 

1996

 

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225 250

 

 

1997, Site not used

D. Ingham

 

.L
O

Number/trap/week
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125 150

 

175 200
Julian day

225 250

 

 

1O

Number/trap/week
O N h 0) on

125

150

 

1997

 

175 200
Julian day

225 250

 

Figure 22. Number of spiders caught per trap per week in chlorpyrifos and cyromazine

treatments in four different onion field sites in 1996 and 1997.

(4_ = chlorpyrifos, _._ = fonofos,_... = cyromazine, I = insecticide spray)

54

 

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

   

 

 

 

 

 

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Figure 23. Total numbers of Coleomegilla maculata caught per
trap in chlorpyrifos and cyromazine treated areas located in four difl‘erent

onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

55

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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Ottawa 1 SitG’Newaygo Ingham

 

 

Figure 24. Total numbers of Coccinella septumpunctata caught per
trap in chlorpyrifos and cyromazine treated areas located in four different

onion field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; * =significantly different, p<0.05)

56

 

A. 1996

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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e

 

 

 

 

 

 

 

 

Figure 25. Total numbers of Hippodamia spp. caught per trap in

chlorpyrifos and cyromazine treated areas located in four different onion

field sites during the 1996 and 1997 growing seasons.

(Poisson means = variance; "' =significantly different, p<0.05)

57

 

Figure 26 shows the relative numbers of the most common carabid species. When P.
chalcites was the most common species, carabids as a group were more numerous in the
cyromazine areas. However, A. sanctaecrusis, was the most numerous at the Ingham site
in 1997 and its numbers did not appear to be decreased by chlorpyrifos, although the total
number of carabids was reduced. P. melanarius was the most common species at the
Newaygo site and appeared to be less numerous in the chlorpyrifos area and reduced the
total number of carabids caught.

Conclusions
There is some question as to the reliability of pitfall traps for assessing the impact

of pesticides on populations of ground-dwelling arthropods. Edwards and Thompson
(1975) found that the neurologically active insecticides cause hyperactivity that enhances
catches in sprayed plots relative to unsprayed ones and that pitfall catches are influenced
by beetle immigration. Chiverton (1984) concluded that reducing prey populations by

' the application of insecticides results in hungrier carabid beetles with consequently
higher activity. Since pitfall trap catches are determined not only by p0pulation size but
also activity, he argues tha , “pitfall-trap catches alone cannot give a true measure of the
effects of insecticides on carabid populations in the field.” In a peanut field, Dixon &
McKinlay (1992) hypothesized that after being sprayed with insecticide, the pests
(aphids) fall off plants. The beetles then ate the aphids and were less hungry, therefore,
less active and less likely to be trapped; later increases in catches may have been due to
hungry and thus more active beetles. In the onion system, the availability of eggs or
maggots, which are already on or in the ground, is probably not increased due to the
insecticides. Floate et al. (1989) found the toxicity of chlorpyrifos on Bembidion species

much higher in the

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laboratory than in the field and suggested that adult immigration and residual toxicity
influence pitfall catches and recovery of carabid populations after spraying. These
arguments against the use of pitfall traps except Dixon and McKinley (1992), result from
higher numbers of carabids caught in sprayed areas.

In the present experiment, cyromazine is compared to chlorpyrifos. Cyromazine,
which affects larvae, should not directly cause adult carabid mobility. The first year data
showed that if there was a difference in trap catches between treatments, the number of
carabids or staphylinids caught were lower in chlorpyrifos than in the cyromazine treated
area. Therefore, while not perfect, pitfall traps seemed adequate and were used in the
second year of the experiment.

The total number of carabids was nearly always higher in the cyromazine areas
than in the chlorpyrifos areas, but each of the species that made up the carabid population
exhibited its own relative abundance. Insecticides are known to produce differential kills
of ground beetles when applied at equal concentrations (Mowat & Coaker 1967,
Critchely 1972, Tomlin 1975, Gholson et a1. 1978, Los & Allen 1983, Thiele 1997,
Hassan et a1. 1991). These differences might be due to physiology, behavior, or size.
However, in these experiments, no species of carabid was always more numerous in the
chlorpyrifos area than in the cyromazine area.

The results of this study indicate that cyromazine may be less toxic than
chlorpyrifos to adult carabids, staphylinids and spiders, however, there is question about
the relative effects on the immature stages of the beetles which are soil inhabiting.
Bartlett (1964) generalized that it is the adult stages of predators and parasites that were

the most susceptible to insecticides, while eggs the least. He thought that holometabolist

6O

larvae were intermediately susceptible and heterometabolous nymphs were more prone to
be poisoned than adult forms. Tomlin (1975) using topical application found that
chlorfenvinphos, an organophosphate pesticide, was fairly innocuous to carabid larvae
although it had a wide range of effects upon adult carabids.

The effects of cyromazine on the immature stages of onion maggot predators have
not been tested. Cyromazine, may not be Diptera specific. Cyromazine has been shown
to affect Colorado potato beetle (Coleoptera: Chrysomelidae) (Sirota & Grafius 1994)
and Manduca spp. (Lepidoptera: Sphingidae) larvae (Kotze & Reynolds 1991).
Therefore, when the effects of chlorpyrifos and cyromazine on larvae are compared, the
results might be different.

The introduction of an insect growth regulator into the onion system may
allow increased biological control, contributing to reduced pest damage, greater pest/crop
stability, and reduced risk of crop loss. These kinds of changes are essential if producers

are to reduce reliance on pesticides, as is desired by environmental and consumer groups.

61

Carabidae predation on onion maggot Delia antiqua (Meigen) (Diptera:

Anthomyiidae) and subsequent maggot damage to onions

ASTRACT

Trenches were used to increase and decrease existing carabid beetle densities in an onion
field. The relative survival of onion plants on which maggot eggs had been placed did
not differ between the high and low carabid densities. In a second experiment, the
number of eggs placed in the field that survived to third instar or to pupate did not depend
on the carabid concentration treatments. Reasons for the lack of treatment effects are
discussed. Fewer maggots placed in the field did, however, survive in the treatments
with higher carabid concentrations.

In no-choice feeding studies, carabid beetles commonly found in Michigan onion
fields ate onion maggot eggs and onion maggots. Mean number of maggot eggs

consumed per beetle ranged from <10 to >90 per day.

62

 

Introduction

Carabidae and Staphylinidae predation on the immature stages of D. antiqua
(Drummond 1982, Grafius & Warner 1989, and Tomlin et al. 1985) and its relatives
Delia radicamCBouche) (W ishart 1959, Hughes 1959, Hughes & Salter 1959, Coaker &
Williams 1963, and Coaker 1968, Mowat & Martin 1981, Uba Yaman 1990) and Delia
floralis (Fallen) (Andersen et al. 1983) has been documented in North America and
Northern Europe. Depending on the species composition in the field, these studies have
estimated that these predators may eat 17 -90% of the eggs laid by D. radicum, the
cabbage maggot. Grafius and Warner (1989) reported that one species of carabid,
Bembidion quadrimaculatum L., at high enough population densities could potentially
remove 60% of D. antiqua eggs from the field. However, as Varis (1989) noted upon
reviewing several of the studies cited above, carabids can destroy considerable number of
root fly eggs, the resultant effects on crop loss are often indistinct.

The objective of this study was to determine the predatory impact of carabids and
staphylinids on D. antiqua in an onion monoculture and subsequent impacts on the onion
stand.

Methods
Field experiments. In 1998 two field experiments were done to test the impact of

predators on survival of immature D. antiqua at the Michigan State University Muck
Soils Research Farm, Clinton Co. Michigan. The soil at the farm has an organic matter
content of 80%. In the spring, an experiment tested the impact of carabids on onion

survival. In the late summer, when the onion tops had died back and the onions were

63

ready to harvest a study was done to assess predation on onion maggots and on onion
maggot eggs.

The field used in this experiment was 61 m long (N-S) by 15.2 m wide (E-W)
consisting of 36 planting beds that were 1.2 m wide and were raised 15 cm higher than
the surrounding soil with 30-45 cm between beds. An early variety onion was planted in
three rows on each bed. No insecticide was used at planting nor during the course of the
experiment. Within the field, 12 plots (6.1 x 6.1 m) were arranged in a randomized
complete block design with four blocks of three treatments. In the three treatments the
density of beetles was a) same as existing b) decreased relative to existing, or c)
increased relative to existing. The altered beetle density plots were created by digging a
15 cm deep trench around each plot. In the decreased density plots, the inner walls of the
trench were lined with a continuous piece of black plastic thereby permitting beetles to
crawl out of but not into the plots (Wright 1960); pitfall traps were used to filrther reduce
beetle numbers. In the increased density plots, the outer walls of the trenches were lined
with plastic thereby permitting beetles to crawl into but not out of the plots. In both
treatments, the upper and lower edges of the plastic were anchored every 1 m with
sections of bent wire. These edges were then buried under about 3-5 cm of soil. To
determine whether the three treatments resulted in significantly different beetle densities,
each whole plot treatment was sampled using four pitfall traps (Figure 1).

An irrigation pipe that had pivoting heads ran lengthwise down the center of the
field. The farm manager irrigated the field in the mornings when necessary. Each whole

plot had one edge of the treatment bordering the pipe (Figure 2).

64

 

Figure 1. Cross-section through trench around plot showing

the plastic sheeting (P) that restricts beetle movement.

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All sides of the field were bordered by 4 m bare soil. Beyond the bare soil, the west side
was bordered by another field of onions and the east wide was bordered by a field of
mint. The shorter north and south ends bordered respectively a thick hedgerow of shrubs,
and a fence that marked the edge of the cultivated area and the start of weeds and trees

Spring Field Predation Experiment. Four subplot treatments were as follows a)
20 eggs placed on the soil surface within 1 cm of an onion, b) 10 eggs placed on the soil
surface and 10 eggs placed 1 cm below the surface within 1 cm of the onion c) 20 eggs
placed in the crack in the soil created by and around the base of the onion plant d) no
eggs placed (control). Treatments were applied to the 25th onion from the center of the
plot.

Three weeks after the trenches were put in the field and the onions had reached
the 2 leaf stage the onion maggot eggs were placed on onions in the plots. To reduce
edge effects, the 4 subplot treatments were applied to the inner two raised beds each
divided into two 2.7 m sections with the outer 30 cm of each bed not included. In each of
the subplots, two of the three rows of onions were chosen at random and any onions that
were not in the 2 leaf stage were removed. Onions in a randomly-selected l m of a row
were counted to measure initial stand. A 50 plant section of onions was marked by stakes
with the following restrictions: no gaps between onions greater than 15 cm, no gaps
within the center 17 plants of onions greater than 10 cm, the entire length of the section
was between 125-170 cm. These restrictions were used to standardize the rows of onions
used. If a section of onions did not meet the criteria, a different 1 m of onions was used.

The eggs and maggots were obtained from the culture maintained in the lab of Dr.

James Miller at Department of Entomology, Michigan State University. Before being

67

placed in the field, the eggs were counted in an air-conditioned room. Ten or 20 eggs
were counted out in the lab with a watercolor brush and placed in 6 cm sections of clear
plastic drinking straws. The straw ends were folded over and taped shut. Egg counting
was finished at mid-afternoon, and the straws with eggs were placed in a cooler and
transported to the field. The eggs were removed from the opened straws with a 2 ml
burst of water from an oral syringe and the placement of the eggs was checked to be sure
the eggs were within 1 cm of the plant base. The eggs were placed in the field between 6
and 9 pm. to simulate natural timing of oviposition (Perron & LaFrance 1960).

The beetle populations were monitored via live pitfall traps (11 cm dia., 14 cm
deep) located within each subplot. The pitfall traps were made out of two plastic
containers. The outer container remained in the soil for the duration of the experiment
and limited soil disruption when traps were checked. Traps were opened for 24 h and
then the contents collected. On May 15, the contents of the depressed beetle density plots
were moved to the increased plots. On May 29, the day the eggs were placed on the
onions, the beetles were returned to the area sampled. On June 19 the beetles were
removed and placed in alcohol.

Onion survival was counted on June 19 and August 28 (harvest time). Carabid
and staphylinid numbers were log (count+ l) transformed and then analyzed to determine
whether whole plot treatments were statistically significant (PROC GLM, SAS Institute
1994). Ratios of onions that survived to original number counted were calculated,
arcsine converted, and then analyzed as a splitplot random complete block design using
PROC GLM (general linear model) AN OVA (SAS Institute 1994). Arithmetic means are

used in the result section figures.

68

Late Summer Field Experiment. In late summer, the black plastic trenches
around the plots were inspected and mended where needed. Plastic food grade containers
(11 cm diam. and 14 cm deep) with two 0.5 cm holes covered with plastic screening in
the bottom were filled to the rim with muck soil. The soil had been sieved to remove
most insects and other visible arthropods. In each plot, two of these containers were
buried so that their rims were covered with soil. A 5 cm diam. onion with its basal plate
cut off was placed cut end down into a 2 cm deep depression in the soil in the center of
the container. Seven second and third instar D. antiqua were placed under one of the
onions. Twenty onion maggot eggs were placed on the side of the onion at the point
where the onion met the soil so that half the eggs were above ground and half were
below.

After 3 weeks, the containers with maggots added were removed. After 4 weeks
the containers where the maggots eggs were placed were removed. The onions were
dissected and the soil in the cup sieved and carefully inspected for onion maggots and
pupae.

In addition, in each increased beetle density plot two more containers of soil were
added. One had the same placement of eggs, and the other the same placement of
maggots as above. However, these containers were only buried halfway into the soil.
Therefore the onion and D. antiqua were approximately 5 cm above the soil surface and
protected from predators. Each container was paired with its firlly buried counterpart and
the numbers of onion maggots found at the end of the experiment statistically analyzed

with a paired t-test.

69

Pitfall traps, arranged as in the spring experiment, were used to determine beetle
densities in each whole plot. In this experiment, the number of beetles caught in the four
pitfall traps per whole plot were pooled. The data was log (count + l) transformed and
then analyzed as a randomized complete block design to determine whether there were
significant whole plot effects. Again, arithmetic means are used in the figures.

Laboratory feeding studies. The carabids used in this study were field collected
in August and September from the Michigan State University Muck Soils Research Farm,
Clinton Co. and from a non—cultivated field at the Collins Road Entomology Research
Farm, East Lansing. The onion maggots and eggs were again obtained from the lab of
Dr. James Miller.

Three day study on predation of eggs. Eggs (100) were counted out onto a 2 cm
square of wet filter paper in the center of a petri dish and one carabid beetle was placed
into each dish. The dishes were then closed and placed in a growth chamber at 25°C with
a photoperiod of 15:9 (LzD) d. The number of eggs eaten, eggs hatched and remaining 1St
instars were recorded after 24 h. The filter paper and all remaining eggs and larvae were
removed and replaced with 100 new eggs every 24 h for 3 d. The number of eggs each
individual beetle consumed per 24 h was averaged over the 3 d assay and combined to

calculate a mean SE. per beetle.

 

I
II.

One day study on predation of maggots. Third instars and a section of onion were
placed on wet filter paper in petri dishes (seven/dish). One carabid beetle was placed into
each dish. The dishes were then closed and placed in a growth chamber at 25°C with a
photoperiod of 15:9 (LzD) d. The number of maggots eaten or attacked was recorded

after 24 h and mean number eaten i S.E. per species was calculated.

70

Foraging study. In 1998, a small study was done to determine the ability of
carabids to find eggs on the soil surface versus below the surface. A similar study was
done by Grafius and Warner (1989) with Bembidion quadrimaculatum L. For this study
100 ml soufflé cups (6 mcm dia. top, 4 cm diam. bottom, 3.5 cm high) were filled to a
depth of 2 cm with sieved muck soil. Twenty eggs were placed either on the soil surface
or 1 cm below the surface. To the cups one B. quadrimaculatum, one P. lucublandus or
no carabids were added. After 24 h (20-23°C) the numbers of remaining eggs were
recorded.

Results and Discussion

Field studies. In the spring experiment, the beetle densities were never
significantly different between ambient, increased or decreaed predator plots. The global
ANOVA for the spring experiment was not significant for carabids (May 29, F = 2.14, df
=2,6, P = 0.19; June 19 (F = 1.96, df =2,6, P = 0.2177) (Figure 3) or for staphylinids (
May 29, F = 3.38, df =2,6 , P = 0.0851, June 19, F = 1.74, df=2,6, P = 0.2597). When
onion stands were counted at the global AN OVA was not significant for the numbers at
third week (F = 1.12 , df = , P = 0.3984 ) or for numbers at harvest(F = 0.93, df = , P =
0.5647) (Figures 4 and 5). The populations were not trapped more often for fear that the
trapping and the movement in and out of the plots would disturb the carabid populations.
A control to measure egg survival in the field disintegrated and the data could not be

collected.

71

 

 

25 Beetle treatment

 

 

 

 

 

 

 

 

 

 

     
 

 

 

 

 

 

 

 

 

 

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Figure 3. Number of carabids caught per attempted treatment +/- SE.
(decreased, existing and increased carabid densities) in an onion field
during the growing season.

Different letters indicate significantly different means, P <0.05.

72

 

 

 

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decreased existing increased
Egg placement

Beetle concenfratlon levels

 

 

 

 

Figure 4. Ratio of the number onions one month after placing onion maggot
eggs in the field to the number of onions the day the eggs were placed in the field
+/- S.E. (A = 20 eggs on soil surface, B =10 eggs on soil surface and 10 eggs
below soil surface, C = 20 eggs place in soil crack at onion base, D = no eggs)
No corrrparisons were significantly difi‘erent at P<0.05.

 

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Figure 5. Ratio of the number onions three months after placing onion
maggot eggs in the field to the number of onions the day the eggs were placed
in the field +/- S.E. (A = 20 eggs on soil surface, B =10 eggs on soil surface
and 10 eggs below soil surface, 'C = 20 eggs place in soil crack at onion base,
D = no eggs). No comparisons were significantly different at P<0.05.

73

By the end of the growing season, the increased and decreased beetle density plots
were significantly different from each other (August 20, F = 8.28, df = 2, 6, P = 0.0031,
August 28, F =8.95, df = 2, 6, P = 0.0094) (Figure 3). Common species were P.
chalcites, P. lucublandus, P. melanarius, S. comma, and some B. quadrimaculatum.
Staphylinids means were not significantly different on August 20, (F = 0.59, df = 2,6, P =
0.7086) and only two beetles were caught on August 28. Where the eggs were added
there were no differences in the number of onion maggots or onion maggot pupae found
(toms = 3.18, df = 3, P < 0.05; F = 1.08, df= 2,6, P = 0.4558) (Figures 6 and 7). Where
onion maggots were added, significantly more onion maggots were found in the
decreased carabid treatment than in the increased treatment (F = 5.63, df = 2, 6, P =
0.0289) (Figure 8). Moreover, more maggots were found in the control cups where
maggots were not accessible to the ground insects than were found in the treatment where
the eggs were accessible (toms = 12, df= 3, P < 0.05) (Figure 9).

From these experiments it appears carabid levels impact the number of maggots
that survive. However, due to the nature of the experimental design it is not possible to
make conclusions about the impact on egg survival.

Laboratory feeding study. As shown by others (Tohnin et al 1975, Drummond
1982, Grafius & Warner 1989), carabids will eat onion maggots and onion maggot eggs
when offered to them under laboratory conditions (Table l). The sample size in the

foraging study was not large enough to make an assessment (Table 2).

74

 

 

 

 

 

 

 

 

 

 

 

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Figure 6. Number of onion maggots and pupae found
in or beneath an onion the field 4 weeks afier placing 20 onion
maggot eggs on the onion, (+/- S.E.) within different carabid
densities. Different letters indicate means significantly
different, P<0.05.

 

 

 

 

 

 

 

 

 

 

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Figure 7. Number of onion maggots and pupae found in
or beneath an onion in an onion field 4 weeks afier placing 20
onion maggot eggs on the onion, +/- S.E.; A= accessible to
ground dwelling predators. Control = not accessibile to
ground dweeling predators. Different letter indicate means
significantly different, P >0.05

75

 

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Figure 8. Number of onion maggots and pupae found
in or beneath an onion in the field 4 weeks after placing 7
onion maggots on the onion (+/- sd) within different carabid
densities. Different letters indicate means significantly
different, P<0.05.

 

 

 

 

 

 

 

 

 

 

 

 

7
m.
roUJ6
a.“ b
335
+
is“
883 a
$52
40.
1
0

 

 

   

 

 

Treatment control

 

 

 

Figure 9. Number of onion maggots and pupae found
in or beneath an onion in an onion field 4 weeks afier placing
7 onion maggots on the onion, +/- S.E.; A= accessible to
ground dwelling predators. Control = not accessbile to
ground dwelling predators. Different letters indicate means

significantly different, P<0.05.

76

 

Table 1. Mean number of Delia antiqua eggs and maggots eaten by carabids in a

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

laboratory feeding study.
3 Day Egg Study 1 Day Maggot Study
# Mean # Mean #
offered eaten per # eaten
Species n per day day :l: S.E. n offered is S.E.
Poeeilus chalcites '7 100 69 i 11 9 7 5 i 2
P. lucublandus 3 100 99 :t 1* 4 7 6 i 1
Pterostichus 3 100 71 i 13 8 7 7 :i: l
melanarius
Anisodactylus 1 100 96 1 7 4
sanctaecrucis
Stenolophus comma & 5 100 92 :l: 3 11 3 2 :l: 1
Iecontei
Harpalus spp. 3-6 100 84 :i: 12 10 7 6 i l
Scarites spp. 4 70 10 :t 5 "‘ - - -
Cicindela spp. 3 To 8 :i: 4 4 6 5 1:1
*2 d

77

 

Table 2. Mean number of eggs on the soil surface or below the soil surface eaten by P.

lucublandus and B. quadrimaculatum.

 

 

 

 

 

 

Number of eggs not found i S.E.
eggs placed 1 cm
Species eggs placed on surface below surface
Poecilus lucublandus 10 j; 2 (5) 6 j; 4 (4)
Bembidion quadrimaculatum 12 j: 3 (4) 11 :i: 5 (3)
Control (no carabids) 3 i 3 (3) 3 i- 1 (3)

 

 

 

 

78

Conclusions

The first half of this experiment is inconclusive. When looking at the mean
number of beetles caught per treatment (Figure 3) there appeared to be a trend of more
carabids in the high beetle density plots. There may have been significantly different
carabid densities in the plots but the trapping method may not have been effective. Traps
should have been left open for a longer period of time or more often. In addition, a better
control was needed to monitor the fate of the eggs placed in the field. Knowing the
number of eggs that hatched was important to determine whether there was a difference
between the sub-plot treatments.

The second half of the experiment indicates that at the end of the growing season

carabids may reduce onion maggot numbers by half and thereby reducing the number of

females ovipositing in the spring when the crop is most susceptible to damage.

79

Effect of Insecticide Treatment and Soil Organic Matter Content
on Onion Growth and Damage by Onion Maggot, Delia antiqua Meigen

(Diptera: Anthomyiidae)

ABSTRACT
Cyromazine and chlorpyrifos were tested on soils of differing organic matter content for
control of onion maggot and for effects on onion germination and growth. Onions
received one of three treatments: cyromazine in a seed coating, chlorpyrifos at planting,
or no insecticide and were gown in soils differing in organic matter content or other
composition. Onion maggot eggs were placed on half of the treatments and allowed to
develop. The first greenhouse study showed that cyromazine and chlorpyrifos were
equally effective at controlling onion maggot (99 and 85% plant stand after germination
respectively), compared to the control (17% plant stand) on muck soil of 20, 40, and 60%
organic matter content. The soil with 20% had a negative effect on onion growth, with
decreased survival after germination and lower stands. The second greenhouse study also
showed cyromazine and chlorpyrifos were equally effective in controlling onion maggot
(89% and 92% plant stand respectively), compared to the control (39%) on a sandy loam,
an organic sand, and a peat humus. Both insecticides performed better on the sandy loam
(94%) than on either the organic sand (69%) or the peat humus (57%). However, the
onion size was significantly smaller on the sandy loam. In the field, the insecticides were
equally effective, however, the resulting yields were not the same; cyromazine had the
greatest yield and the control the smallest. The efficacy of both insecticides was higher

than the control on the organic sand (63% plant stand) than on the peat humus (43% plant

80

stand). These results indicate that cyromazine does not differ from chlorpyrifos in its
efficacy at different soil organic matter contents. However, soil organic matter content

does affect the growth of onions.
Introduction

Onions (Alliaceae: Allium cepa) are a major vegetable crop in the United States, second
only to lettuce production by weight (Kortier-Davis et al. 1995). In 1996, Michigan
growers planted 2511 ha of dry bulb onions with a production value of $15.5 million
(MASS 1997). Most of these onions were directly seeded into histosols, commonly
referred to as “muck” soils which have high organic matter content (Lucus 1982).
Histosols typically have good water retention, high nitrogen content, and simple nutrient
management and harvest practices (Zandstra et al. 1996). In Michigan, muck farming
areas were created by draining lakes and swamps resulting in muck soils that vary in
organic matter content within and between fields (W arncke, personal communication).
The onion maggot, Delia antiqua Meigen (Diptera: Anthomyiidae), is a serious
onion pest. In Michigan, onion maggots over-winter in the soil as pupae and emerge as
adult flies in May. The females lay their eggs at the base of onion seedlings. After
hatching in 3-5 days, the larvae feed on the onion bulbs and roots for three instars (2 to 3
weeks). The larvae then pupate, and adults emerge in July. By this time, the onions have
developed a skin over the bulbs that is more resistant to onion maggot attack, and the
female flies prefer to lay their eggs on previously damaged onions (Finch & Eckenrode
1985, Hausmann & Miller 1989). The offspring of the July generation emerge in August

and September and lay eggs on onions left behind in the field after the harvests in

81

August-October. The first generation larvae, therefore, have the greatest direct effect on
the yield and quality of the onion crop. In severe years, onion maggot can reduce onion
stand in commercially treated fields by 40-80% (Zandstra et al. 1996).

Historically, the common practice for onion maggot management on commercial
farms was to apply granular insecticides in the seed furrow at planting and then follow
with foliar sprays as often as once a week starting in June (Liu et al. 1982). The result of
this intensive exposure is that the onion maggot is now resistant to cyclodiene,
organophosphate, carbamate, and pyrethroid insecticides (Howitt 1958, Guyer & Wells
1959, Harris & Svec 1976, Harris et al. 1981, and Carroll et al. 1991). Foliar sprays used
against adults are ineffective and may have contributed to resistance development (Finch
et a1. 1986). Application of granular insecticides in the seed furrow by itself is effective
against the very damaging first generation of onion maggot (Ritcey et a1. 1991).
Chlorpyrifos (Lorsban, Dow Elanco), an organophosphate insecticide, and cyromazine
(Trigard, Novartis), an insect growth inhibitor, are the only remaining effective chemicals
registered for use against onion maggot.

Cyromazine (Trigard, Novartis) is an insect growth regulator that stiffens the
larval cuticle via an undetermined mode of action and prevents molting (Kotze &
Reynolds 1991). It will be registered for use against onion maggot for the 1999 growing
season (Bishop, personal communication). In the early 1980’s, cyromazine was found to
be useful against species of flies such as leaf miners, Liriomyza trzfolii (Burges) and
cultivated mushroom pests, Lycoriella auripila, and it has been fed to cattle and fowl to
kill flies in feces (Shen & Plapp 1990). Hayden and Grafius (1990) reported the potential

of cryromazine as a management tool for onion maggot. Cyromazine was first used

82

against onion maggot as a soil drench; it is now being incorporated into an onion seed
treatment at the the low dosage of 50g of active ingredient kg of seed (Grafius 1984,
Grafius & Boylan-Pett 1991).

Despite the success of cyromazine for onion maggot control, there have been
some reports of failures. During the growing season of 1995, Grafius and Davis (1996)
found cryromazine ineffective at one field site. They suggested that this might have been
due to dry conditions, failure of pellet breakdown, or soil with low organic matter
content. Sandy soils have been implicated in low onion stands in New York (Taylor,
personal communication).

Cyromazine may have fewer negative impacts than conventional insecticides on
natural enemies of the onion maggot (Miller et a1. 1981, Samsoe-Petersen 1985, Wills et
al. 1990) and, therefore, might lend itself well to a more integrated approach to control
onion maggot. Determining the effectiveness of cyromazine is important in constructing
reliable integrated pest management strategies. This study was designed to test
cyromazine and chlorpyrifos effects on onion germination, plant development, and onion

maggot control in soils of different organic matter content.

Methods

Greenhouse studies. Two studies were conducted in the Center for Integrated
Plant Systems greenhouses at Michigan State University. Both were randomized
complete block designs with a split-plot arrangement of treatments, insecticide treatments
within soil type. In both greenhouse studies, each soil flat (51 x 25 cm) was physically

divided lengthwise with double layer of PVC duct tape into 3 equal sub-plot sections, 8

83

cm wide. Twenty-five onion seeds were sown in 1 cm deep fin'rows that ran the length of
each sub-plot. Treatments were randomly assigned: cyromazine coated on the seeds,
granular chlorpyrifos in the furrow, or no insecticide.

Greenhouse Study 1. Whole plots consisted of a muck soil amended to create one
of three different organic matter levels. The plots were arranged into 8 blocks. The
muck soil, categorized as “Houghton muck,” was from the Michigan State University
Muck Soils Research Farm, Clinton Co. Michigan. The unamended soil had an organic
matter content of 80%, which is higher than that of most commercial onion fields. The
soil was mixed with pure silica sand to achieve three different organic matter contents:
20%, 40%, and 60% by weight. These levels were within the range of organic matter
contents of muck soils farmed in Michigan. Each seedling flat contained 3 l of soil.

The onion seed (‘Legacy,’Sun Seeds) used in this study came from a single seed
lot. A portion of the lot was thinly coated with cyromazine (appox. 0.16 mg of active
ingredient per seed) by Dr. Alan Taylor, Cornell University. The chlorpyrifos treatment
received granular Lorsban 156, at the label rate of 3.7 oz. per 1000 row foot. All seeds
had been treated with the fungicide thiram (ProGro). Every other day during the
experiment, each seedling flat received 0.5 to 1 l of water via a sprinkling can.

When the onions had reached the two leaf stage (42 days post planting), sub-sub
plots were assigned: halfreceive onion maggot eggs, the other half did not. In the
maggot egg treatments, two eggs were placed on the base of each onion. Eggs came from
a culture maintained in the lab of Dr. James Miller, Department of Entomology,

Michigan State University.

84

Greenhouse Study 2. Whole plots consisted of two muck soils and one mineral
soil. The plots were arranged into 4 blocks. The muck soil used in this study came from
a commercial farm in Newaygo Co Michigan where cyromazine had reportedly failed in
a field trial. The two different muck soils were collected fi'om locations 90 m apart within
the same field. One muck soil was “peat humus” with 73% organic matter and a 6.2 pH;
the other was “organic san ” with 20% organic matter and 5.9 pH. The inorganic soil
came fiom the Michigan State University Potato Research Farm in Montcalm Co.
Michigan. The soil was sandy loam (66% sand, 24% silt, 10% clay) with 2% organic
matter and 7.2 pH. Each seedling flat contained 4.26 L of soil.

Novartis Crop Protection, Inc (Hillard, Ohio) supplied the seed for this study. A
portion of the seed (‘Quantum’) was pelleted with a clay coat that contained cyromazine
(50g/kg seed).

All onion plants received onion maggot eggs 53 d after planting. The eggs were
applied as in the first study. Each seedling flat received 0.5 to 1.5 l of water every l-2d
via a sprinkling can.

Field study. A field plot study was planted in the same location at the farm in
Newaygo Co. where the muck soil of higher organic matter content had been acquired for
the second greenhouse study. The study was an incomplete block design with a split plot
arrangement of treatments. As in the studies above, soil was the whole plot and the same
three insecticide treatments were the subplots. Each of the five blocks was 3.7 m long and
consisted of two adjacent raised onion beds 0.45 m wide. In one bed of each block, the
soil was removed to a depth of 10 cm. This soil was replaced with 90 [1 organic sand from

the sandy area of the field (described in second greenhouse study). The onion seeds were

85

planted May 12, 1997, using the same as in the second greenhouse study) with 100 onion
seeds per sub-plot sown 1 cm deep.

Data collection and analysis. The number of emerged onion plants were
counted on eight dates during the first greenhouse study and on four dates during the
second greenhouse study. Two ratios were calculated from these counts for each
treatment: 1) maximum number of seeds germinated / number of seeds planted and 2)
number of plants alive at the two leaf stage / maximum number of seeds germinated.
Onion plant size was measured as total length of photosynthetic cotyledon or leaf above
ground. Measurements were taken on six dates in the first study and on four dates in the
second study. The relative efficacy of insecticide treatments was evaluated by the ratio of
healthy plants at the end of the study (11 d after eggs were placed on the onion plants in
the first study and 14 d afier in the second study) to the number of plants present the day
the eggs were placed on the plants.

In the field study, the onion stand was counted on seven dates before harvest. At
harvest (August 21,1997) the onions were counted and weighed. The ratio of number of
plants at harvest to maximum number of plants counted during the season was calculated.

Ratios were arcsin transformed and count data were log(count+1) transformed.
Comparisons were made by general linear model procedure, AN OVA (SAS Institute

1994) at the 5% level. HSD comparisons were done on least square means.

86

Results and Discussion

Greenhouse study 1. Soil organic matter affected the number of onions that
survived from germination to the two leaf stage (F = 5.37, df = 2,14, P = 0.0185);
survivorship was lower in the sandier soil (Table 1). This may have resulted in a soil
effect on onion stand at the two leaf stage (F = 4.04, df = 2,14, P = 0.0412) in which
onion stands were lower on the sandier soil. There was no significant soil or insecticide
treatment effect on the number of onions germinated nor on the size of the onions at the
two leaf stage.

The differences between insecticide treatments (F = 32.92, df =2, 18, P = 0.0001),
between the treatments with onion maggots added and with no onion maggots (F = 75.05,
df = 1,27, P = 0.0001), and the interaction of these two factors (F = 47.52, df = 2,27, P =
0.0001) were significant. Soil organic matter content, though it affected onion growth,
did not affect efficacy of either insecticide. In plots with no onion maggot added, the
survival of onions was the same on the three soils and for the three insecticide treatments
(Table 2). In plots with onion maggots added, the stands of onions with the cyromazine
and chlorpyri fos treatments were not different, and both were higher than onions planted
without insecticide. The level of onion maggot damage in the cyromazine and
chlorpyrifos treatments was not different to the controls without onion maggot. The
interaction between soil and insecticide treatment was not significant, therefore, cell

comparisons were not done.

87

Table 1.

Greenhouse study 1: Mean comparisons of onions grown on muck soil

of 20%, 40%, and 60% organic matter content and with insecticide treatments

cyromazine, chlorpyrifos, and no insecticidel.

 

 

% organic
matter in Cyromazine Chlorpyrifos No Mean
soil insecticide
20% IIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIII
40% 0.77 0.67 0.69 0.71
60% 0.77 0.74 0.72 0.74
Mean 0.76 0.67 0.68
W. l . l:
20% 0.72 0.67 0.77 0.72 a
40% 0.89 0.72 0.82 0.81 b
60% 0.76 0.84 0.89 0.83 b
Mean 0.79 0.74 0.83
WM:
20% 12.9 11.3 12.0 12.1a
40% 17.3 11.8 14.5 14.5 ab
60% 16.3 15.5 15.1 15.6b
Mean 15.5 12.9 13.9
Iotalnnicnleaflengthfcm)
20% 91.8 90.3 93.3 91.8
40% 91.8 79.5 90.1 87.1
60% 99.0 85.6 96.5 93.7
Mean 94.2 85.1 93.3

 

fMeans followed by a different letter within a column (a, b, c) are significantly different

at p < 0.05

88

Greenhouse study 2. Onions grown on sandy loam were smaller than those
grown on either of the two muck soils; soil effect (F = 47.19, df = 2,6, P = 0.0002) (Table
3). Onions grown on sandy loam were observed to grow not as robustly as the onions
grown on muck soils.

Cyromazine and chlorpyrifos had the same level of efficacy which was higher
than that of no insecticide, ANOVA (F = 25.01, df = 2,16, P = 0.0001) (Table 3). The
survival of onions was also affected by the soil organic matter content (F = 13.89, df =
2,6, P = 0.0056). Onions grown on sand had a higher survival than those did on either
muck type. The plots with sand appeared to develop a silt layer over the soil surface and
to be more compacted than the muck soils. The survival of the onion maggots in this
study may have been lower and therefore maggot damage was less.

Field study. In the field study, both insecticide treatment (F = 16.25, df = 2,12, P
= 0.0004) and soil type (F = 12.40, df = 1,4, P = 0.0244) effected onion survival (Table
4). Onion stands were higher on the organic sand than on the peat humus (Table 4).
Cyromazine and chlorpyrifos had the same level of efficacy, higher than with no
insecticide. There was no interaction between insecticide treatment and soil. The size of
each onion was not affected by soil or insecticide treatment. However, the total yield per
row was affected. Cyromazine yield was the highest, followed by the chlorpyrifos and

with no insecticide yields being the lowest (F = 20.74, df = 2,12, P = 0.0001).

89

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Table 3. Greenhouse study 2: Mean comparisons of onions grown on sand,
organic sand, or peat humus with cyromazine, chlorpyrifos, or no insecticide treatment‘.

 

 

Soil Cyromazine Chlorpyrifos No insecticide Mean
Sand III-III...III-OI...-IIIIIOIIIIIIIIIIIIIIIIIIIIIIIIIIIIIII
Organic 0.52 0.50 0.55 0.52
sand
Peat 0.54 0.53 0.58 0.55
humus
Mean 0.48 0.43 0.51
WW 1 . 1]
Sand 0.78 0.94 0.92 0.88
Organic 0.72 0.95 0.85 0.84
sand
Peat 0.94 0.91 0.87 0.91
humus
Mean 0.81 0.93 0.88
WW
Sand 9.0 5.0 8.8 7.6
Organic 12.3 9.0 11.8 11.0
sand
Peat 12.3 12.3 12.3 12.3
humus
Mean 11.2 8.8 11.0
W
Sand 7.3 5.2 6.8 6.4 a
Organic 21.0 18.1 19.0 19.4 b
sand
Peat 16.5 18.8 22.8 19.4 b
humus
Mean 14.9 14.0 16.2
Efficacy (number of onions afier onion maggots/
l E . l E . 2
Sand 0.98 1.00 0.83 0.94 a
Organic 0.95 0.92 0.20 0.69 b
sand
Peat 0.73 0.83 0.15 0.57 b
humus
Mean 0.89 x 0.92 x 0.39 y

 

lMeans followed by a different letter within column (a,b,c) or row (x,y,z) are

significantly different at p < 0.05

91

Table 4. Field Study in Newago Co.: Mean comparisons of onions grown on organic

sand or peat humus with cyromazine, chlorpyrifos, or no insecticide treatment].

 

Soil Cyromazine Chlorpyrifos No Mean
insecticide

 

S'lfilE' 18,. l

germinated)

Organic 0.74 0.69 0.46 0.63 a
sand
Peat humus 0.66 0.42 0.22 0.43 b
Mean 0.70 0.56 0.34

D . . l l I] 1
Organic 4.8 3.8 3.2 3.9
sand
Peat humus 5.3 2.7 1.5 3.2
Mean 5.1 x 3.3 y 2.4 2

D . . 3 3
Organic 0.074 0.072 0.073 0.073
sand
Peat humus 0.090 0.063 0.076 0.076
Mean 0.082 0.068 0.075

 

rMeans followed by a different letter within a column (a, b, c) or row (x, y, z) are

significantly different at p < 0.05

92

Conclusions

The results of these studies indicate cyromazine does not differ from chlorpyrifos in its
control of onion maggot in muck soils that range in organic matter content from 20%
to70%. The comparison of soils from the farm where cyromazine had failed, indicated
thatthe organic content was probably not the causal factor for the failure. Soil type has an

effect on the survival or size of an onion independent of the insecticide used.

93

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102

APPENDICES

103

APPENDIX A

Field Diagrams for Chapter 1.

 

104

+
N

 

0
Industrial 0 a
bu1ld1ngs aTrees '
a 0 a
/’A I
Low wet ff, l
area
{/Fallow
\ I
Dirt road Chlorpyrifos
Irrigation ditch
Grass Onions

Figure 1. Ottawa 1 Site 1997

105

Residential area

 

 

Irrigation ditch
i
Onions I Onions
.C:
3
‘3
'6'
I .
. l
l
' l
,-___________ l________._-
g B Cyromazrne
fi'
3 1———1
g' = 400fi

= Diagonal line of
3 pitfall traps

 

Newaygo Site 1997

 

 

 

 

 

 

 

 

3;
M
+
Carrots
N 8‘
Carrots
Onions Carrots Onions Corn Potatoes
I I
I l
Irrigation ditch
Gravel road ' | I = Diagonal line of
3 pitfall traps
O 0
$3 g Grain
Onions g E g i—____l
84 E, 3* = 400 a.
U) U)

Figure 2. Newago site 1997

106

 

 

 

Potatoes

 

 

 

 

 

 

 

Irrigation ditch
N
Potatoes Onions Potatoes
3
a. s
*3 if
g .-
s 2
E a.
m
I m I
E"
I 3‘ I
.0
I 5 I ._
Dirt road > ! .
L l Q
J F .
Irrrgatron drtch Chlorpyrrfos Cyromazrne I = Diagonal line of
Soybean 3 pitfall traps

i———7 =4UUII

Figure 3 . Ingham County site 1997.

107

APPENDIX B

Record of Deposition of Voucher Specimens

108

APPENDIX 1

Record of Deposition of Voucher Specimens“
The specimens listed on the following sheet(s) have been deposited in the named
museum(s) as samples of those species or other taxa which were used in this research.
Voucher recognition labels bearing the Voucher No. have been attached or included in
fluid-preserved specimens.
Voucher No: 12:28
Title of thesis or dissertation (other research projects):
INSECT GROWTH REGULATOR, CYROMAZINE, CONTROL OF ONION

MAGGOT (DELIA ANTIQUA (MEIGEN)) AND EFFECTS ON POSSIBLE
BIOLOGICAL CONTROLS

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

Investigator’s Name (s) (typed)

Sheila Ebert
Date

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

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

Museum(s) files.
Research project files.

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

109

 

 

 

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