ri. fettp diet of powdered milk, sugar and dried meat powder was sufficient for maintenance of adult...

LABORATORY REARING, TOXICITY OF CYROMAZINE AND THE

EFFECT OF TEMPERATURE AND MANURE MOISTURE ON OPHYRA

AENESCENS (WIEDEMANN) (DIPTERA: MUSCIDAE)

by

Lorraine Marie Koller

Thesis submitted to the Faculty of the Virginia Polytechnic Institute and State

University in partial fulfillment of the requirements for the degree of

APPROVED:

L. T. Kok

MASTER OF SCIENCE

Ill

Entomology

E. C. Turner, Jr., Chairman

May, 1989

Blacksburg, Virginia

I . fettp ri. a. Pfei~r

LABORATORY REARING, TOXICITY OF CYROMAZINE AND THE

EFFECT OF TEMPERATURE AND MANURE MOISTURE ON OPHYRA


by,

Lorraine Marie Koller

E. Craig Turner, Jr., Chairman

Entomology

(ABSTRACT)

The effect of protein in adult and larval diets for Ophyra aenescens

(Wiedemann) (Diptera: Muscidae ), a facultative predator of the house fly, Musca

domestica L., was examined. A larval diet of coarse wheat bran, vermiculite and

dried meat powder was found adequate for rearing 0. aenescens larvae. Protein

content was important for maximum larval emergence and for Fl adult longevity

and fecundity. Adult diet of powdered milk, sugar and dried meat powder was

sufficient for maintenance of adult 0. aenescens flies. Protein was needed in adult

diet for optimal fecundity.

Cyromazine was toxic to 0. aenescens at high levels (1.0 ppm), but at 0.75

ppm 0. aenescens tolerated cyromazine better than a susceptible strain of house

flies. At these cyromazine levels, mass release of 0. aenescens into poultry houses

is possible one to two days after cyromazine has been removed from the chicken

feed.

The effect of temperature and manure moisture on 0. aenescens was

studied. At temperatures of 18°C, emergence of Ophyra aenescens was

significantly lower than at temperatures of 21 and 27°C. Predation by 0.

aenescens at 27°C on house fly larvae was significant at ratios of 3:1, 2:1and1:1

(house fly to 0. aenescens). A constant manure moisture was important in the

development of 0. aenescens larvae and its ability to prey on house fly larvae. At

constant levels of 50, 60, and 70% manure n;ioisture, 0. aenescens substantially

reduced house fly larval numbers at ratios of 3:1, 2:1and1:1.

ACKNOWLEDGEMENTS

I wish to thank Dr. E. C. Turner, Dr.,L. T. Kok, and Dr. D. G. Pfeiffer for

being members on my committee.

I am grateful to and for their technical

assistance, logical thinking and advice; Dr. Kok for use of an environmental

chamber; for building the fly cages used in the experiments;

of the Poultry Science Department for his never ending supply of chicken

manure; Dr. Ruszler of the Poultry Science Department for use of his chickens in

the cyromazine experiment; Dr. Ray Noblet of Clemson University for analyzing

the different larval media types; and Dr. Birch, Dr. Krutchkoff and Dr. Pirie of the

Statistics· Department for their advice.

Financial support was made possible by the Virginia Agriculture Council,

grant number 4-37043 and by Dr. Turner.

I wish to thank the following people: and

who were a constant source for inspiration. Special thanks goes to

for his advice, encouragement, friendship and his enthusiasm for science.

Finally, I would like to thank my Mom and Dad for calling me every Sunday

night to listen to me and to cheer me onand for sending care packages when I

needed it.

iv

! '

TABLE OF CONTENTS

ABS'ffi.ACT : ........... ~ .................. · ...... ~ ......................................................................... ii

ACKNOWLEDGEMENTS ...............................................•................................. iv

INTRODUCTION:· ..........•............• : .•.. : .••... ~ .. ~.~ ••..•.. ~ •............................................... 1

I. UTERATURE REVIEW ..•.•. ~ .... ·~ ..................................................................... 3

II. THE EFFECT OF DIFFERENT PROTEIN LEVELS IN LARY AL

AND ADULT DIETS ON THE DEVELOPMENT AND

REPRODUCTION·OF•OPHYRAAENESCENS (WIEDEMANN)

(DIPTERA: 'MUSCIDAE) ...........• ~: ..... ; ... ~~ ............... ;; ........................................ 13

ill. THE TOXICITY OF CYROMAZINE TO OPHYRA AENESCENS

(WIEDEMANN}(DIPTERA: MUSCIDAE} ..........•....................................... 28

IV. THE EFFECT OF TEMPERATURE AND MANURE MOISTURE

ON THE PREDATORY HABITS OF OPHYRA AENESCENS

(WIEDEMANN} ON MUSCA DOMESTICA L. ........................................... 37

LITERATURE CITED ...................................................................................... 5 0

VITA ............................................................. .' ............... ~ .......................................... 57

v

1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

LIST OF TABLES

Mean number of flies emerged and standard error of Ophyra aenescens reared on different larval diets placed into the rearing room.. . ............................................................... 23

Mean number and standard error of flies emerged from 150 first instar Ophyra aenescens seeded into larval diets with varying protein levels. . ................................................ 24

Fecundity and longevity with standard error for Fl male and female Ophyra aenescens reared from different protein levels. . ................................................................................... 25

Fecundity.and longevity with standard error for males and female Ophyra aenescens fed adult diets with varying protein levels. . .................................................................... 26

Percent mortality of Musca domestica and Ophyra aenescens from cyromazine in rearing media. . ............................................ .32

Slope, LC90 and fiducial limits from probit analysis or cyromazine in rearing media. . .................................................... .32

Percent mortality of Musca domestica and Ophyra aenescens from cyromazine in chicken manure. . ......................................... .33

Slope, LC and fiducial limits from probit analysis ofOcyromazine in chicken manure. . ................................................... 34

Percent emergence of Musca domestica and Ophyra aenescens from chicken manure one day after and one week after cyromazine was removed from food. . ................................. 35

Effect of manure moisture and competition with Musca domestica on emergence of Ophyra aenescens. . ............................... .43

Effect of manure .moisture and competition with Ophyra aenescens on emergence of Musca domestica. . ............................... .44

Effect of temperature and competition with Musca domestica on emergence of Ophyra aenescens. . ........................................... .45

Effect of temperature and competition with Ophyra aenescens at different ratios on the emergence of Musca domestica ............... : .......... ~ ..................................................................... 46

vi

LIST OF FIGURES

Figure Page

1. House fly emergence at 70, 60 and 50% manure moisture at different house fly to Ophyra aenescens ratios ..................................... : ............................................................ 47

2. House fly emergence at 27, 21and18°C at different house fly to Ophyra aenescens ratios. ····••••••n••·····································································································48

vii

INTRODUCTION

Poultry systems today are providing greater efficiency in animal production.

At the same time these systems also increase problems in manure disposal and fly

control. Manure pits in caged layer poultry houses provide an ideal environment

for the development of the house fly, M-usca domestica L. (Diptera: Muscidae ).

The house fly, primarily a nuisance pest, can be a severe problem when

populations reach high levels. This fly disturbs farm workers and frequently

disperses to nearby residential areas. Large numbers of house flies in residential

areas can prompt complaints from neighbors and may be a potential health threat

(Greenberg 1971).

Traditionally, pesticides are used in house fly control, but with insect

resistance becoming a problem in many poultry houses, an Integrated Pest

Management system (IPM) is becoming more popular. This system involves

cultural and biological control methods with minimal chemical input. Within this

system an alternative approach in biological control of the house fly is through the

use of a facultative predator, Ophyra aenescens (Wiedemann) (Diptera: Muscidae ).

The larvae of 0. aenescens are predators of house fly larvae and mass releases of

0. aenescens into poultry houses can reduce house fly populations (unpublished

data). Mass releasing an insect requires knowledge about rearing the insect. Little

information exists about rearing 0. aenescens for mass release.

After using the proper cultural and biological control practices there is still

often a need to use insecticides to control house flies. One of the best ways to

control flies is through the use of feed-through larvicides. This is an ideal method

to control house flies because it eliminates labor costs and uses no expensive spray

equipment. Cyromazine (Larvadex™) (Ciba-Geigy Corp., Greensboro, NC), a

1

2

feed-through insect growth regulator, is widely used for larval control in caged

layer poultry houses. Although cyromazine is known to affect only dipterous

insects, its toxicity to 0. aenescens is unknown.

Because of the predatory habits of th~ larva, 0. aenescens has been

proposed as a biological control agent for use in an IPM program (Nolan &

Kissam 1985). Thus, egg producers would benefit financially because 0. aenescens

would reduce the amount of chemicals required to· obtain satisfactory house fly

control. The implementation of an IPM program using 0. aenescens may also

retard the occurrence of insecticide resistance. .

The information from this research will be used to.integrate 0. aenescens

into an IPM program for house fly control. The specific objectives of this study are

to determine the:

1. effect of varying protein levels in both larval and adult diet on fly

emergence, fecundity and longevity.

2. level of toxicity of cyromazine to 0. aenescens larvae.

3. effects of different moistllre levels and temperature on 0. aenescens

ability to prey on house fly larvae.

LITERATURE REVIEW

Ophyra aenescens. Ophyra aenescens was first described by Wiedemann in

1830 (Johnson & Venard 1957) and placed~ the genusAnthomyia. According to

Johnson & Venard (1957), Stein in 1897 transferred it toDphyra Robineau-

Desvoidy. The genus Ophyra was first placed in the family Anthomyiidae but

Crampton (1944) after examiningthe terminalia statedthatOphyra was a typical

muscid and placed it in the family Muscidae where it remains today.

Where is 0; aenescens found?. According to Greenberg (1971), Ophyra

aenescens occurs in the United States from Oregon to Arizona, Illinois to the East

Coast. This fly is also neotropical and oceanic. Ophyra aenescens has spread to

Europe (Adams 1984, Skidmore 1985). Ophyra aenescens has been found in Texas

around animal.confinement areas (Robertson & Sanders 1979) and in poultry

houses in South Carolina (Nolan & Kissam 1985) and Florida (Hogsette 1979).

Mail & Schoof{1954) found 0. aenescens moving around actively in refuse

dumping areas in West Virginia. Hill & Williams (1980) found 0. aenescens to be

the most numerous fly in high rise poultry houses in Indiana.

In lab experiments performed by Johnson & Venard (1957), the eggs of 0.

aenescens hatched in 12 to 16.hours·at 28°C. The development period for the

three larval instars averaged 9 days while the pupal stage averaged about 4 days at

27°C. The adult is shiny black and slightly smaller than the house fly. The male

fly has contiguous eyes while the female's eyes are separated. The females hold

theirwings parallel to each other and the male~s wings are crossed half way

between the fifth and sixth veins (Johnson & Venard 1957). Adult males lived an

average of 15 days while females lived an average of 20 days (Johnson & Venard

3

4

1957). Hogsette (1979) reported similar results in that females lived for an

average of 20 days and outlived males by an average of 3 to 4 days. One pair of

adults can produce 300:-400 offspring (Johnson & Venard 1957).

Rearing. Little information on Ophy~a spp. rearing exists. Roddy (1955)

used a larval media consisting of whole milk, Brewer's yeast, bacto-agar and water

for rearing 0. aenescens. Johnson & Venard (1957) used the Chemical Specialties

Manufacturing Association ( CSMA) preparation medium, fish meal diamalt, cake

yeast, and brewer's yeast. Hogsette (1979) used a similar media, consisting of

CSMA, wheat flour, fish meal, N31C03, alfalfa meal and water. Olckers & Hulley

(1984) reared colonies of Ophyra capensis (Wiedemann) on lucerne meal, wheat

bran, molasses, yeast, powdered milk and a fungus. suppressor. Nolan (1987) used

a diet consisting of CSMA medium, soybean meal, two whole chicken eggs and

water.

Johnson & Venard (1957) used fish meal for adult food of 0. aenescens.

Hogsette (1979) gave adult 0. aenescens .flies cane sugar, dry fish meal and

nasogastric mix. Nolan (1987) used a mixture of powdered milk, table sugar and

egg for the adult food. Olckers & Hulley (1984) used sugar and whole milk

powder for adult food of 0. capensis.

In basic biological studies on 0. aenescens by Hogsette (1979), a fortified

larval diet (CSMA medium plus alfalfa meal, N31C03, fish meal and wheat flour)

did not shorten larval development time as compared·with an unfortified diet

(CSMA media). The fortified diet did increase the number of pupae that formed

and the number of adults thatemerged. Size of emerging adults was the same for

both fortified and unfortified diets. Sugar in adult food increased the adult life

span 9 times. The life span for flies without sugar in the adult food was 2 days

5

while the life·span was 18 days for flies feeding on sugar.

Predaceous behavior. The larvae of Ophyra spp. are predaceous on other

dipterous larvae (Anderson & Poorbaugh 1964a, Peck 1969, Peck & Anderson

1969) but not cannibalistic (Anderson & Poqrbaugh 1964b, Hogsette 1979).

Hogsette (1979) examined the cephaloskelton of the third-instar larvae of 0.

aenescerzs and concluded that the larvae can live either in a saphrophagous manner

or they can be carnivorous. Similar findings were reported by Schumann(1982).

Anderson & Poorbaugh (1964a, 1964b) reportedthat Ophyra leucostoma

(Wiedemann) larvae may kill 2 to 20 Musca domestica L. maggots per day. In

laboratory studies by Olckers & Hutley (1984), 0. caperzsis consumed 4-5 house fly

larvae per day. Nolan & Kissam (1985) observed 0. aenescerzs feeding onM.

domestica, Phormia regina (Meigen) and Sarcophaga sp. larvae in laboratory

colonies. Hogsette (1979) found thatO. aenescerzs could destroy more than 20

first-instar house fly larvae per day during larval development. Muller (1982)

discovered that joint breeding of 0. aenescerzs and M. domestica led to a high

mortality rate of M. domestica. 0. aenescerzs was a facultative predator and

developed normally without consuming fly larvae.

Because of the predaceous habit of the larvae of the genus Ophyra, it has

been suggested. they could be used as biological control agents against the house

fly (Derbeneva-Ukhova 1943, Conway 1973, Muller et al. 1981, Olckers & Hulley

1984, Nolan & Kissam 1985, Ribbeck et al. 1987). Many researchers feel the

adults of 0. aenescerzs are pestiferous and excessive numbers of this fly are just as

annoying as the house fly (Hogsette 1979, Axtell 1986a, Axtell & Rutz 1986). The

nuisance potential of adult Ophyra flies was examined by Nolan & Kissam (1987).

They found that dispersal from poultry houses with high populations of 0.

l

.6

aenescens was minimal. This agrees with other workers (Anderson & Poorbaugh

1964a, 1964b, Legner & Dietrick 1974)in thatOphyra spp: adults tend to hide in

secluded places.to mate -and.congregate.

House Fly. Linnaeus described the h<;mse fly .in 1758 (West 1951). It is an

ubiquitous insect (West 1951 ), is cosmopolitan in· distribution and meets all

conditions requfred of a disease vector (Greenberg 1971). Jt is important because

it coexists with m~ consuming·both contaminated~an:d;non~cdntaminated·food,

has great flight activity .and dispersal and alternates between feces and Jood

(Greenberg 1971); ·

The development of this fly is highly.dependent upon temperature which

influences both survival and time required for development(Harwood & James·

1979). The egg stage takes·8~12 hours'to hatch, larval.stage takes 5 days, pupal

stage.takes 4-5.days, with a total of 10 days from egg tc>' adultat3o0c. Under

temperate·conditio:risit woUldtake3weeks•(Harwood.&JamesJ979) .. During the

srinnller in the southeastern United States; generation times are between ·six and·

ten days. (Axtell 1986b )>The average life span• of the adult can range-from· 14· to 70

days (Harwood&James1979); House flies can overwinterin•any.stage

(Greenberg1971). ·

The house fly is vecy prolific (Harwood & James 1979); A· female mates

and beginslaying .. eggs 3-4 days afteremerge11ce· (Axtelt1986a). Some housefly

females can lay over 1000 eggs (LaBrecque: etaL 1972) ·in• the laboratory but

usually females will .lay 4-6 batches of 100-150 eggs in her lifetime• (Axtell l986a ).

Greenberg {1973)reported a dispersion. of 2.3 km to lL8 km per day. They

mostly stay within lto 3 km-of: their breeding place butcan: fly 5 or 6 km in large

7

numbers (Harwood & James 1979). Mark recapture traps have indicated that the

house fly can go as far as 20-32 km from their source (Linquist et al. 1951) using

wind drift to increase the distance (Oldroyd 1965).

Resting spots of house flies were also, investigated. Traps held overnight

caught 85% ofhouse flies.within houses (Anderson & Poorbaugh 1964b).

Larvae of house flies can be found in refuse areas (Mail & Schoof 1954)

and inhorse, cow and chicken manure (Harwood & James.1979). In chicken

manure, a temperature of 27°C and a moisture of 60-75 % was determined to be

optimum for house fly larval development (Miller et al. 1974).

Fly Control. Manure management and fly control are closely related

problems for poultry facilities (Barth 1986). The moisture content of fresh manure

that accumulates beneath cages ranges from 70-80% (Hart 1963, Card & Nesheim

1975) and has a pH of 6butincreases due to bacterial growth after a few hours

(Beard & Sands 1973). This is optimal for house fly larval development(Miller et

al. 1974). Keeping the manure dry (below 60%) reduces.the habitat for fly larval

development (Axtell 1986a, 1986b ). Maintaining watering systems and preventing

moisture from entering into the fly breeding areas is critical in fly control (Axtell

1986b, Barth 1986). If this cannot be done, increasing the moisture level higher

than 80% where manure becomes anaerobic will render it unsuitable for house fly

development (Miller et al. 1974) but this may create conditions that favor other

noxious flies (Axtell 1986b ). Keeping the manure dry will also encourage natural

fly predator and parasite populations to develop (Axtell 1986b ). The activities of

predators and parasites in accumulated manure in Florida resulted in a 97%

reduction in the number of house flies recovered from artificially infested

8

containers (Propp & Morgan 1985).

Three families of mites are known to prey upon house fly eggs or larvae:

Macrochelidae, Uropodidae and Parasitidae (Axtell 1963, .1986b ). Macrocheles

muscaedomesticae (Scopoli), a phoretic mite,, can kill house fly eggs and first instar

larvae by piercing the chorion or integument and sucking out the contents (Axtell

1963, 1964 ) .. Other important predatory mites in poultry manure are the uropodid

mite Fuscruopoda vegetans (DeGeer), and. the parasitid mites, Poecilochirus spp.

(Geden et al. 1988). Many chemicals used to control house flies are harmful to

mites (Axtell 1966). Larvicides were reported to destroy mites but adulticides left

them unharmed (Axtell 1970) ..

Many beetles especially Histeridae and Staphylinidae are common in

poultry manure (Peck1969, Pfeiffer & Axtell 1980). Carcinops pumilio (Erichson)

and Alphitobius diaperinus (Panzer) were consistently the most abundant species in

three regions of North Carolina (Pfeiffer & Axtell 1980). Carcinops pumilio adults

are known predators of house fly eggs (Peck1969, Geden et al. 1988) while the

larvae wiHfeed on house fly instars (Geden et al. 1988). The role of A. diaperinus

as a predator of house fly larvae was examined by Despins et al. (1988). Both

adults ~d late instar A. diaperinus larvae had a significant impact on house fly

emergence in the laboratory. Not enough research has been conducted to reveal

the importance of other species of beetles found in poultry manure (Pfeiffer &

Axtell 1980).

The major parasites of house flies in confined animal systems are small

wasps (Hymenoptera) which belong to the family Pteromalidae. These parasites

are common biological control. agents of flies in poultry houses (Legner & Brydon

1966, Morgan & Patterson 1975, Rutz & Axtell 1980, Rueda & Axtell 1985). Mass

I

releases of these parasites -can result in a decrease 'in .house fly populations (Ables

& Shepard 1974,,0lton&Legner 1975, Rutz &.Axtell 1981, Shepard & Kissam

1981) although some.species of parasites were not active.throughout the year

(Olton & Legner 1975, Rutz & Axtell 19~0) and~perfotmed better in dry manure

than wet manure {Rutz & Axtell 1980). Parasites were also required to be

climatically adapted to the ateawhere they are released (Axtell & Rutz 1986).

Manure removal schedules. can affect abundance of house fly and predator

populations. Monthly or biweekly removal of manure favored fly populations

while the. predators studied were most abundant in ;Unremoved manure (Peck &

Anderson 1970)~ Lower numbers .offlies emerging from: poultry manure was

correlated with increasing masses of breeding habitat due to increased populations

of scavengers, predators and parasites,(Legner et al~ 1973). If manure must be

removed, ·leaving a base of old,manure .. behind in the pit would favor beneficial

arthropod predators and also absorb excess.moisture from new droppings (Legner

& Brydon.1966, Peck &Anderson1970, Axtell 1986a).

Environmental conditions in manure pits were measured to see what role

theymight playonthe developmentof flies and beetles:(Stafford & Collison 1987).

Temperatures in the pits had weekly means of 18.l.to 20.o0 c which is adequate for

fly development all year round. ·Mean temperatures in upper manure layers were

near optimum (29 .5~35.8°C) for beetle development. Relative humidity was found

to be around.65% .and no seasonal trends were found. In British poultry houses,

moisture content of manurewas in.dependent of temperature and relative humidity

(Bills 1973)~

· Chemical Larvicides •. Larvicides are an effective way to control livestock

pests,. either applied directly to manure or as a feed additive• (Miller 1970).

10

Larvicides should only be used after biological and cultural controLtactics have

been applied and a high level of fly control is desired (Axtell 1986b ). Insecticides

are effective if they complement biological and cultural controls (Axtell 1986a).

A chemical should not be 'routinely used if it is known to be toxic to

parasites and predators (Axtell 1986a). When spraying manure directly, the

chemical should only be applied· to those areas in which abundance of flyJarvae is

observed (Axtell 1986b). Bailey et al. (1968) stated that sprayinglarge quantities

of manure is ineffective due to larval movement mixing the chemical with the

mediumand quickly making the concentrationtoolmy. Major insecticides

currently used as larvicides are: stirophos (Rabon™), dimethoate (Cygon ™) and

cyromazine (Larvadex™) (Axtell 1986b)~.

Pathogens. The fungus Entomophthora muscae (Cohn) Fresenius is a

widely known natural enemy of adult muscoid flies. ·This pathogen can be

transmitted within house fly populations during periods of comparatively dry and .

cool weather and when the relative humidity within the boundary layer

surrounding the fly's body is at or near the saturation point (Kramer 1980).

Kramer & Steinkraus (1987) achieved 100% mortality of house flies in a small

poultry house by placing infected flies into the house.

Hall & Arakawa (1959)successfullyusedB. thuringiensis vaL thuringiensis.

Berliner to kill house fly maggots in laboratory tests~ The pathogen Bacillus

thuringiensis Berliner was fed to caged layers for fly control buta reduction in feed

consumption, body weight and egg production was noted (Burns et al. 1961).

Insect Growth Regulators. Insect growth regulators (IGR) have been

tested for control of the housefly. ·Several chemicals.have.been effective

experimentally for feed-through fly control buthave not been registered for use

11

due to residues in animals or products (Axtell 1986b )~ Laboratory bioassays using

encapsulated methoprene, anIGR, resulted in good control of house fly

emergence at a rate of 5.0 ppm after the chickens were fed treated feed for eight

days (Breeden et al. 1975). Similar results were found by Morgan et al. (1975) and

birds did not experience a weight loss. However, methoprene was not effective as

atopical spray on poultry droppings under field conditions (Morgan et al. 1975)

and in field studies, satisfactory fly control was not achieved· due to existing cross

resistance to methoprene (Breeden et al. 1980).

Diflubenzuron (Dimilin ™) has also been tested as a feed'-through larvicide

for control of the face fly and the house fly (Miller 1974). In field and laboratory

studies, Diflubenzuron affected intermediate to late stage larvae but had no effect

on house fly eggs or fly pupae (Ables et al. 1975). Diflubenzuron also had no

effect on the parasitoid Muscidifurax raptor Girault and Sanders or its ability to

parasitize house fly pupae (Ables et al. 1975). When Diflubenzuron was applied to

fly resting surfaces in conjunction with releases of the parasitoid, M. raptor, a

significant reduction in the number of house flies on the poultry farm resulted

(Shepard & Kissam 1981). When Diflubenzuron was fed to chickens, fly control

was obtained but residues were found in all egg samples (Miller et al. 1975).

Cyromazine is the only registered feed-through insect growth regulator for

caged poultry to control the house fly and other Diptera. Numerous studies on its

effect on dipterous insects have been performed (Hall & Foehse 1980, Williams &

Berry 1980, Mulla & Axelrod 1983a, 1983b, Meyer et al. 1987). Cyromazine had

no adverse effects on populations of manure-inhabiting mites which prey on fly

eggs and larvae (Axtell & Edwards 1983). Populations of beneficial Staphylinidae

and Histeridae were also unaffected by treatments of

12

cyromazine (Meyer et al. 1984 ). Cyromazine was found to be the most cost

effective treatment and provided the highest level of control in small commercial

caged layer poultry houses (Quisenberry & Foster 1984).

In laboratory studies, a 10% soluble concentrate of cyromazine in rearing

media caused 100% mortality of 0. aenescens at levels between 0.025 - 0.10%

(Hogsette 1979). No pupae were found; all flies died in the larval stage. A 1.5

ppm level of feed-through cyromazine had no effect on the 0. aenescens ' ' '

population in a poultry house in South Carolina (Nolan & Kissam 1985).

In laboratory studies, tolerance to cyromazine was detected in a wild,

organophosphate-resistant house fly strain (Bloomcamp et al. 1987). In field

studies at poultry farms in southern New England, cyromazine was ineffective after .

one and a half years of intermittent use at one farm and at a second farm,

adequate fly control was never achieved {Anderson et al. 1986). Reasons for this

were not understood but resistance was suggested.

1 . I

1

I ,I

/.

THE EFFECT OF DIFFERENT PROTEIN LEVELS IN LARVAL AND ADULT

DIETS ON THE DEVELOPMENT AND REPRODUCTION OF OPHYRA


Ophyra aenescerzs (Wiedemann) (Diptera: Muscidae ), a facultative

predator, has beeh.proposed as a biological control agent for house flies in caged

layer poultry houses (Nolan & Kissam 1985). When introducing predators for use

in an IPM program, it is important to produce sufficient numbers of the predator

efficiently and economically. Various diets have been used to rear the 0.

aenescerzs larvae using the Chemical Specialties Manufacturing Association

preparation (CSMA). Johnson & Venard (1957) usedCSMAwith diamalt, fish

meal, yeast and brewer's yeast while Hogsette (1979) used a similar diet containing

CSMA, wheat flour, fish meal, N<liC03, and alfalfa meal. Nolan (1987) simplified

the ingredients by using CSMA with soybean meal and chicken eggs.

Ingredients for the adult food have also varied; the adult food used by

Johnson & Venard (1957) consisted of dry fish meal, but Hogsette (1979) used a

nasogastric mix with fish meal. Nolan (1987) used a different mixture consisting of

powdered milk, sugar and· a chicken egg.

Because the diets were either costly or time consuming to produce, a less

expensive diet with simple ingredients was needed to rear 0. aenescerzs. Following

a suggestion by Robert D. Hall (personal comm.), a larval diet of coarse wheat

bran, vermiculite, dried meat powder (50% protein) and a chicken egg was used.

Preliminary tests indicated that this diet worked well. The ingredients for the adult

diet consisted of powdered.milk, sugar and dried meat powder .

Since the dried meat powder is an important part of both diets, the

13

14

objective was to. determine the optimum amount of protein needed in the diet to

rear healthy flies without reducing the number offlies emerging. Experiments

conducted were todetermine : (1) the number of flies emerging from media types

with varying levels of protein thathad been a) placed in the 0. aenescens rearing '

room, and b) seeded with a. known number of first instar 0. aenescens larvae,· (2)

the .effect of varying levels of protein in larval media on the Fl adult 0. aenescens

longevity and fecundity, and (3) the effectof different levels ofprotein in adult

food on longevity andfecundity of adultO. aenescens.

Materials and Methods

Effect of different protein levels in larvaldiet on the number of flies

emerging from. the media. The standard. diet for rearing larvae consists of, by

volume,. eight parts vermiculite, twelve parts wheat bran, one part dried meat

powder (protein supplement), and one chicken egg. The proteinleveland the

presence of the chicken egg were varied in this test. The proteinJevelswere: (1)

dietwith no protein supplement (OX); (2) dietwith half the protein supplement

(1/2X); (3} the standard diet (lX) and (4) dietwith twice the protein supplement

(2X). Because the egg might supply additional protein to the larvae, the presence

of eggs was also .examined using these four diet types (EOx, El/2x, Elx and E2x).

Individual diets (237ml) andwater (enoughto moisten diet)were

combined in small containers (474 ml) and replicated three times. Inthe egg

treatments, 10 ml of raw beaten egg was mixed into the top of the medium. Cups

were placed randomly in a walk-in rearing room, which had a controlled

temperature (27°C) with continuous light and constant air flow. Only one diet

type was.placed into the rearing room at a time. Females were allowed free access

15

to oviposit in the cups for 24 h. To allow for larval growth, the medium was

transferred to a larger container which held· an additional 4 7 4 ml of the wet

corresponding medium. A layer of vermiculite was added on top to prevent mold

growth (Born 1954). The containers were coyered with a screen top and placed

into an environmental chamber (27°C) and the emerging flies counted. Data were

analyzed by the Kruskal-Wallis test (SAS Institute· 1985); ·Amino acid analysis was

determined for larval diets 2x, 1x, and Ox from the Food Science Department,

Clemson University; Clemson, South Carolina.

Effect of different protein levels in larval diet on the adult fly·emergence

from a known number of 0. aenescens larvae. In a similar experiment, diets

containing different protein levels were mixed as before and one hundred and fifty

first-instar 0. aenesceris were seeded into each diet. A layer of vermiculite was

added on top. Containers were covered with a screen top and placed into an

environmental chamber (27°C). Emerging adults were counted. Data were

analyzed using two factor ANOV A and the LSD test for means separation (SAS

Institute 1985).

Effect of different protein levels in the adult diet on longevity and fecundity

of .Q. aenescens adults. The standard adult diet consisted of two parts dried milk,

two parts sugar and one.part dried meat powder. The amount of dried meat

powder in the food was varied in this test as follows: (1) A2 with 480 ml of dried

meat powder; (2) Al with 240 ml of dried meat powder; (3) Al/2 with 120 ml of

dried meat powder; and ( 4) AO with dried milk and sugar and no dried meat

powder; The final treatment used no adult food, just oviposition medium and

water (AH20). Qviposition medium was coarse wheat bran and vermiculite.

16

When the medium was taken out of the adult cages and transferred to bigger

containers, a protein supplement was added to provide a source of nutrition for the

developing larvae.

ln·adult experiments, ten newly·emer~ed male.and female flies were

anesthetized with C02 and placed into rearing cages (30x30x35 ml). Each adult

diet was replicated three times. Cages were kept in a cabinet with a constant

temperature of 30°C. Adult food was provided (120 ml) in 240 ml cups and

changed when needed. Water was alsoprovided in paper cups with Styrofoam™

shavings to reduce mortality due to drowning. Dead flies were recorded and

removed from the cage each day. Oviposition medium was provided on day 2 and

transferred the following day to a bigger container. It was then placed into a

cabinet with a constant temperature of 30°C. The medium was changed everyday

until all females were dead. After five days,. larvae were counted and recorded.

Larvae were counted because it was difficult to count accurately the eggs deposited

in the medium. It was realized that some egg and larval mortality could occur but

since all treatments were similarly evaluated, the results should be comparable

(Turner & Hair 1967).

The· number of larvae per female fly-days was based on the total number of

larvae collected, divided by the total.number of days the females lived. Longevity

for. each replicate was determined by using the median age of the flies in each

cage. Data were analyzed using two factor ANOV A and the LSD test for means

separation (SAS Institute 1985).

Fecundity and longevity of.Fl O. aenescens flies reared from different levels

of protein. In a final experiment, the flies that emerged from the larval media. test

(rearing room test) were collected to determine if they produce viable offspring.

17

Ten newly emerged male and female flies were anesthetized with co2 and placed

into rearing cages (30x30x35 ml); These first generation flies were treated in a

similar manner as the flies in the previous adult food experiment. Adult food was

a 2-2-1 ·ratio of the sugar, powdered milk and.dried meat powder respectively.

Results

Based on amino acid analysis, the percent of crude protein in the diets,

using.amino acid analysis, was 12% for Ox, 17.1% for lx, and 245% for2x.

Although 1/2x medium was not analyzed, extrapolating from the results of the

other diets, 1/2xwould contain approximately 14.Sto 15% crude protein.

Effect of different protein levels in larval diet on the number of emerged

flies. Flies oviposited in all media types (Table 1). Significant differences were

found between diets (Chi-square =0.0056). Due to the small number of replicates,

a mean separation test was not possible. There are trends that can be observed

from the· data. Diets E2xand El/2x had large numbers offlies·emerging from the

diet while diets Ox and 1/2x had the smallest number emerging. ·The addition of 10

ml of raw beaten chicken egg to the diets increased the number of flies emerging

except for dietElx. ·Reasons for. this poor performance of Elx are· unclear.

Effect of different protein levels in the larval diet on adult fly emergence

from a known number of 0. aenescens larvae. Two factor analysis on larval diets

indicate a significantinteraction between larval media with protein and the

presence of eggs (Table 2). For media with an egg on top, EOx was significantly

different from diets El/2x, Elx and E2x. There were similar findings with the

diets with no egg on top (diet Ox was significantly different from diets 1/2x, 1x and

2x). Comparing the media with egg to the media without egg, only EOx and Ox ·

18

were significantly different. Lack of protein in the larval medium can affect the

emergence of flies. A protein source is thus needed because a lack of protein will

reduce the number of flies emerging. The addition 10 ml of raw beaten chicken

egg to the medium increased the number ·of t;lies emerging when no other protein

source was present (EOx vs. Ox).

Fecundity and longevity of Fl adults 0. aenescens reared·from different

larval protein levels. Statistically, .there were no differences in fecundity

(P=0.0836) for the Fl generation 0. aenescens flies reared from the different

larval diets (Table 3). Numerically, the larvae per female fly-days were similar in

diets 2x, 1x and l/2x (21, 20 and 2llarvae per female fly-days respectively).

Although the Ox diet was lower ( 4 larvae per female fly-days) it was not

significantly different.

Two factor analysis indicates a significant difference in longevity of Fl

generation flies reared on different larval diets (P = 0.0016). Diets 2x and lx were

significantly different from l/2x and Ox (Table 3). Fl male flies lived significantly

longer than Fl females (P=0.0001) (Table 3). Longevity of Fl males due to the

larval diets (P=0.0399) was statistically different (Table 3). Fl males reared in lx

media lived the longest (32 days). Males reared in diets 2x, l/2x, and Ox were not

significantly different, having longevities of 24, 16, and 20 days respectively.

Differences were also found in female longevity (P=0.0230) (Table 3). Female

longevity was longest on lx media (17.8 days). Results from diets2x and l/2x were

similar and Ox diet yielded the shortest lived flies (9 days).

Effect of different protein levels in the adult diet on longevity and fecundity

of Q. aenescens adults. No significant difference in the number of larvae produced

due to different levels of protein in adult diets was.found (P=0.0545) (Table 4).

19

Fecundity ranged from. 27 larvae per female fly-days to 11 larvae per female fly-

days for diet AO; even in the treatment with no adult food (AH20), the flies still

laid eggs (13 larvae per female fly-days).

Two factor analysis on adult diets indi~ate a significant difference in

longevity between diets for 0. aenescens.flies (P=0.0001) (Table 4). Diets A2, Al,

Al/2 and AO were significantly different from the AH20treatment (Table 4).

Male flies lived significantly longer than did female flies (P=0.0001). There was

also a significant interaction between adult dietand sex (P=0.0016). For the

treatment of no adult food (AH20), the longevity for male flies was lower than the

female longevity for that treatment.

Longevity was not significantly different between females feeding on the

different adult diets (P=0.0631} (Table 4). Male longevity differed between adult

diets (P=0.0002) (Table 4). The male 0. aenescens lived the longest time on diet

Al/2 (33.6 days) but was not significantly different from diets Al .and A2 (27.8 and

25.3 days respectively) .. Longevity for males significantly decreasedtothree days

when given no adult food (AH20).

DISCUSSION

Larval diet. Female 0. aenescens show a preference for media with high

protein levels with a chicken egg on top. Media containing diets 2x, E2x, lx and

El/2x all produced similar numbers of emerging flies. Diet Elx had enough

protein, .even more than El/2x diet, but it did not attract as many ovipositing flies

as the others. It is uncertain why this occurred. Conditions within the rearing

room such as humidity and temperature, may change from day to day. These

20

conditions may affect the fly's abilitytoJay eggs or they may· not be favorable for

the fly to.lay eggs atthattime;· The number of ovipositingfeniales in the rearing

room also may vary from day to day to cause the difference in the.number of Fl

flies emerged~ The amount ofprotein in the <!iet and the presence of eggs appears

to affect female 0.: aenescens choice of;oviposition site but :because there was

considerable variation. in the·.·experiment .this ·is not conclusive .. ·

... • Proteili levels.in:the. larval media:is important in the development of .the

instars and emergence of the fly. The 10 ml of raw beaten chicken egg placed on

top of the media was not enough to, make a significant difference .in the number

emerged. The one exception was EOx medium (10R67.) which had significantly

more flies emerging thariOx (30.17)~

The.longevity of Fl generation adults was significantly greater when the

larvaewerereared on diets 2x andlx~ Flies lived20.:25 days:onthose diets while

adults livedorily 14 days oll'diets 1/2x and.Ox.·.The Fl males lived significantly

longer (23 days) than the. female flies• (13 days) .. Adult males emerging from the

different larval media lived the longest on the lx media{33 days) and was .

significantly differentfromthose exposed: to diets l/2x (16 days).and Ox (20 days).

Females lived the longestwhen reared.from diets J.X,(17.8 days) and:2x (163 days).

These diets were significantlydifferentfrom Ox diet(9days). < ·.

Fecundity was similar for diets 2x/lx and l/2x (21.2, 20.021.0.larvae per ·

female fly-days, respectively);, Females reared on Ox. had.a lower fecundity ( 4.4

larvae per female fly-days), but was not significantly different fromthe other diets.

A minimum amount of protein· in the larval dietis needed forlongevity and

fecundityofadultO~ aeriescens flies~ . ·

·. Adult Diet· 'J'herewas no difference inJoilgevity offlies.reated on different

l I

21

adult diets but these diets were significantly differentfrom the treatment with no

food; Adult male longevity was similar for diets Al/2, A2 and A1(34, 28, 25 days

respectively) and was notdifferentfromdietAO (20 days).; However; longevity was

significantly reduced when flies were not give:µ adult ·food at all (A.HiO, 3 days). ··

Varying thelevels.ofprotefu in theadultdietmadelittle difference in the female

fly longevity. Female longevity decreased with protein levels but when not given

any adult food, the female flies stilllived an average of8 days~ Diets were not

significantly different for female fongevity at all levels. Varying the protein

amount (ie. dried meat powder) in adult diets has little effect on adult longevity. It

may be that dried milk and sugar are adequate for maximum longevity.

Fecundity of the flies for diet A2 was 27 larvae per female fly-days but was

not significantly different from diets AO and AH20 (11, 13 larvae per female fly-

days respectively). It seems that fecundity of adult flies is not influenced by the

protein in adult diets. In the AHzO treatment, female 0. aenescens still laid viable

eggs even when no protein source was given. The oviposition media contained

only wheat bran and vermiculite. ·In contrast, Johnson and Venard ( 1957) reported

that no eggs hatched until flies fedonanimal flesh. Glaser (1924) stated that sugar

or starch together with protein are necessary oviposition factors for house flies. A

diet of protein was needed for the maturation of ova for blowflies (Mackerras

1933). My results indicate that protein content in the vermiculite and wheat bran

must be adequate for maturation of the ova in the 0. aenescens female.

Both Johnson and Venard (1957) and Hogsette (1979) reported that

females lived 3-4 days longerthan the males (reared at26.6°C). This opposes the

results presented here. In all my experiments the males lived longer than the

females. The rearing temperature (30°C) might be the reason for this. Similar

22

results occurred with the adult house fly when reared at high temperatures (35°C)

(M. G. Fletcher, personal communication). The higher temperature did affect the

fecundity of the house flies but 50% of the eggs were laid sooner at this

temperature than at 30°C. 0. aenescens fem~es would probably outlive males at

temperatures lower than 30°C. Research is needed to confirm this.

23

Table 1. Mean number of flies emerged and standard error (SE) of Ophyra aenescens reared on different larval diets placed into the rearing room.a

Diet Mean SE(±)

E2x 1908.7 236.6

El/2x 1818.7 126.1

2x 1123.7 340.8

lx 923.7 231.9

Elx 170.3 79.4

EOx 141.0 101.4

Ox 54.3 33.8

1/2x 27.7 11.3

aDue to the small number of replicates (n=3), a means separation test was not carried out. ·

24

Table 2. Mean number and standard error (SE) of flies emerged from 150 first instar Ophyra aenescens seeded into larval diets with varying protein levels.

Diet Type

Ox 1/2x 1x 2x

Mean Emergence0 ±SE

Egg 108.7 ±7.87b * 125.7±4.53a 130.2±4.61a 135. 7 + 2.57 a

No egg 30.2±8.16c 113.3±15.06a 121.3±8.77a 128.7±3.47a

0 Means with the same letterin rows are not significantly different.

*Means in this column were found to be significantly differenL There were no differences in the other columns.

LSD test used to separate means (P = 0.05).

Table 3. Fecundity and longevity with standard error (SE) for Fl male and female Ophyra aenescens reared from different larval protein levels.

Fecundity" Diet Meanb

Mean Longevity (days)+ SE Males Females

Mean Longevity+ SE of adult flies

2Jf 21.24+3.84a 24.16± 4.68ab 16.33±0.33ab 20.25±3.87a

lx 20;04±5.99a 32.83±4.04a 17.83±1.92a 25.33 ±5.53a

1/2x 21.03±5.32a 16.33±0.92b 11.16±2.52bc 13.75 +2.36b

Ox 4.44±2.14a 19.83±2.45b 9.00±l.52c 14.42±3.89b

, Meand 23.29a 13.58b

acalculationmade by dividing the total number of larvae produced by the total number of days the female Ophyra aenescens lived (Larvae/female fly-days).

bMeans with the same letter in each column are not significantly different. LSD test used to separate means (P = 0.05).

c2x, lx and 1/2x represent decreasing amounts of protein in larval diets. Diet Ox contains no protein, only vermiculite and wheat bran.

d Average longevity of male and of female 0. aenescens for all diets. Means with different letters are significantly different.

N V1

Table 4. Fecundity and longevity with standard error (SE) for male and female Ophyra aenescens fed adult diets with varying protein levels.

Fecundity" Mean Longevity (days )±SE Mean Longevity±SE Media .Mean±SEb Males Females of adult flies

A2c 26.87±1.94a 27.83±4.26ab 19.33±2.03a 23.59 +4.0la

Al 20.75±5.05a 25.33±3.38ab 15.16±1.59a 23.58±3.99a

Al/2 17.84±1.35a 33.66±1.74a 13.50±2.93a 20.25±6.73ab

AO ll.13±4.36a 19.50±3.0lb 13.50±2.93a 16.51 +3.27b

AHzO 13.32±2.75a 2.66±0.33c 8.33±0.88a 5.50+ 1.89c

Meand 21.80a 13.97b

°Calculation made by dividing the total number of larvae produced by the total number of days the female 0. aenescens lived (Larvae/female fly-days). ·

bMeans with the same letter in each column are not significantly different. LSD test used to separate means (P = 0.05). ·.

c A2, Al and Al/2 represent decreasing amounts of protein in adult diets, AO diet contains only sugar and dried milk, and AH20 represents treatment with no adult food given.

d Average longevity of male and of female 0. aenescens for all diets. Means with different letters are significantly different.

N

°'

27

LITERATURE CITED

Born, D. E. 1954. Mold control in fly rearing media. J. Econ. Entomol. 47: 367.

Glaser, R. W. 1924. The effect of food on longevity and reproduction in flies. J. Exp. Zool. 38: 383-412. '

Hogsette, J. A., Jr. 1979. The evaluation of poultry pest management techniques in Florida poultry houses. Ph.D dissertation U. of Fla. Gainesville, Fl 307 pp.

Johnson, W. T. & C. E. Venard~ 1957. Observations on the biology and morphology of Ophyra aenescens (Diptera: Muscidae). Ohio J. Sci. 57: 21-26.

Mackerras, M. J. 1933. Observations on the life-histories, nutritional requirements and fecundity of blowflies. Bull. Entonml. Res. 24: 353-362.

Nolan III, M. P. 1987. Development of an integrated pest management program for the control of the house fly Musca domestica L., in caged layer poultry houses in South Carolina. Ph.D dissertation Clemson Univ. Clemson, S. C. 179 pp.

Nolan III, M. P. & J.B. Kissam. 1985. Ophyra aenescens: A potential bio-control alternative for house fly control in poultry houses. J. Agric. Entomol. 2: 192-195.

SAS Institute. 1985. SAS user's guide: statistics, 5th ed. SAS Institute, Cary, N. C.

Turner Jr., E. C. & J. A. Hair. 1967. Effect of diet on longevity and fecundity of laboratory-reared face flies. J. Econ. Entomol. 60: 857-860.

THE EFFECT OF CYROMAZINE ON OPHYRA AENESCENS (WIEDEMANN)

(DIPTERA: MUSCIDAE)

Accumulated manure of deep pit poultry houses is an ideal environment for '

the development of the house fly, Musca domestica L. Dispersal of this fly into

nearby residential areas has become both a nuisance and a public health threat.

This has resulted in new regulations governing the suppression of these insects

(Anderson et al. 1986).

Feed-through insect growth regulators are an ideal way to control house flies

because this method eliminates most labor and equipment costs of house fly control

(Mulla & Axelrod 1983b, Miller 1970); Cyromazine (Larvadex™) (Ciba-Geigy

Corp., Greensboro, NC), an insect growth regulator, is incorporated into chicken

feed and prevents development of house flies (Hall & Foehse 1980, Williams &

Berry 1980, Mulla & Axelrod 1983, Anderson et al. 1986).

Cyromazine activity is thought to be limited mainly to dipterous insects and

has been shown not to affect manure-inhabiting predaceous mites and beetles

adversely (Axtell & Edwards 1983). Ophyra aenescens (Wiedemann) (Diptera:

Muscidae ), a facultative predator, has been proposed as a biological control agent

against house flies in caged layer poultry houses (Nolan & Kissam 1985). They also

reported that use of cyromazine at a high rise poultry farm appeared to have no

effect on 0. aenescens.

It is important to determine if 0. aenescens and cyromazine can be used

together in an IPM program to control house flie.s. The objective of this study was

to determine the toxicity ofcyromazine to 0. aenescens and compare it to the

toxicity of a susceptible house fly strain.

28 ! I '

29

Materials·and Methods

Cyromazine toxicity in artificial media. Cyromazine was incorporated into

artificial larval media. The larval media consi~ted of eight parts vermiculite, twelve

parts wheat bran and one part dried meat powder. Weighed amounts of

cyromazine from a 1 % premix were added and mixed to 100 g of artificial rearing

media to obtain concentrations of 0.0, 0.75,1.0, 1.5, 2.0, 25 and 3.0 ppm. Each

concentration was replicated three times. About 250 ml of water was mixed into

each container to provide a suitable substrate for larvae. One hundred first instar

0. aenescens (from laboratory colony) were seeded into each container (800 ml),

covered with a screen top and placed into temperature controlled cabinets

maintained at 27°C. Emerging adults were counted and removed. This experiment

was also conducted using susceptible house fly.larvae .. The laboratory colony of

house flies consisted of flies from a poultry farm that did not use cyromazine. Data

were analyzed using probit analysis on the Statistical Analysis System (SAS Institute

1985).

Cyromazine toxicity in chicken manure. Cyromazine was tested as a feed-

through larvicide in chicken feed. Various dosages of a 1 % premix of cyromazine

were mixed into.22.5 kg (50 lbs) of standard layer chicken feed for 10 min. using a

H600 Hobart feed mixer. Dosages were: 0.0, 0.5, 0.65, 0.85, 1.0 and 1.5 ppm. The

experiment was conducted at the Virginia Tech Poultry Research Center using 61

week-old White Leghorn chickens. Five.birds represented a replicate and four

replicates were used for each treatment rate. The feedwas given to the birds for

seven days, after which the food.trough and water system were cleaned and refilled

with untreated food and water. Samples of manure were collected one day before I I l' ,, I

11

30

treatment, days 1, 3, and 7 during treatment and days 8 and 14 post treatment. The

manure samples were collected separately from each replicate (total manure of five

birds), placed in labeled plastic bags and frozen. Prior to bioassay, samples were

thawed for 24 h to room temperature. An eqqal amount of manure (237 ml) from

each sample was placed into two plastic containers (474 ml)and seeded with either

100 first instar 0. aenescens or with 100 first instar.house·flies. Containers were

held at ambient temperature (21-27°C) and relative humidity. All flies that

emerged were allowed to die before counting. Data were analyzed using probit

analysis on the Statistical -Analysis System (SAS Institute 1985).

Results and Discussion

There were too many data points above the 60% mortality range in the

lower treatments. This caused the pro bit analysis to estimate the LC50 value with

large fiducial limits. Thus, the LC90 value was used to compare 0. aenescens and

M. domestica.

Test using artificial media. Ophyra aenescens tolerated higher

concentrations of cyromazine thanM. domestica(Table 5). Fewer 0. aenescens

died at 0.75 ppm (27%) compared with the house fly (65%). As the dosage of

cyromazine increased, mortality increased for both species. The LC90 value for 0.

aenescens was 1.27 and 1.11 for M. domestica (Table 6). Fiducial limits did overlap

for the LC90 values, indicating that they are_ not significantly different. Percent

mortality was high (Table 5) in the 0.75 ppm and 1.0 ppm treatment. 0. aenescens

may be more tolerant of lower doses of cyromazine (below 0.75 ppm) compared

with the house fly but mortality increases with cyromazine dosages above 0.75 ppm.

------

I. 1:

31

Test using chicken manure. Ophyra aenescens and house fly mortality

increased from day 3 to day 7 (Table 7). The LC90 values for 0. aenescellS tested on

days 3 and 7 were 0.68 and 0.58, respectively (Table 8). Musca domestica bioassay

resulted in LC90 values of 0.58 and 0.45 for days 3 and 7. The fiducial limit values

for 0. aenescellS and the house fly did not overlap.indicating they are significantly

different. The house fly percent emergence was lower in the post treatment (day 8)

compared with the control suggesting that some cyromazine was present in the

manure (Table 9). The percent emergence in 0. aenescellS (day 8) remained the

same in all treatments. One week after cyromazine was removed (day 14 ), no

differences were found in percent emergence between the control and treatments

for either the house fly or 0. aenescellS.

The data indicate that 0. aenescellScan tolerate higher dosages of

cyromazine thanthe house fly. This would agree with the findings Nolan & Kissam

(1985) where 0. aenescellS became the dominant fly in poultry houses after

cyromazine was used as a control for house flies. In an IPM program using 0.

aenescellS and cyromazine at doses of 1.0 ppm and lower, releases of 0. aenescellS

might be possible one day after cyromazine use has stopped. More detailed

research is needed to investigate the effects of cyromazine on 0. aenescellS at lower

doses. Also field studies need to be performed to understand how cyromazine

affects the dynamics of the 0. aenescellS population over time in poultry houses.

32

Table 5. Percent mortality of M-usca domestica and Ophyra aenescerzs from cyromaz~e in rearing media.

Concentration % Mortalitya of~omazine

pm) M. domestica 0. aenescerzs

0.0 0.0 0.0

0.75 65.1 26.7

1.0 81.3 74.4

1.5 98.1 94.7

2.0 100.0 99.4

2.5 100.0 100.0

3.0 100.0 100.0

avalues adjusted using Abbott's Formula (Abbott1925).

Tab~e 6~ SloJ?e,. LC90 and fiducial limits (FL) from pro bit analysis of cyromazine in rearing media. · •· ·

Slope±.SEM

M. doinestica 2.45+0.31

0. aenescerzs 3.34_±_0.26

LC a 90

.. • 1.11

1.27

avalues adjusted with Abbott's Formula (Abbott 1925).

95%FL

1.06-i.17

1.17-1.49

33

Table 7. Percent mortality of Musca domestica and Ophyra aenescens from cyromazine in chicken manure .... ·

34

Table 8. Slope, LC90 and fiducial limits (FL) from probit.analysis of cyromazine in chicken manure.

Day Slope±SEM LC90 a 95%FL

Ophyra aenescerzs

3 4.44±0.52 0.68 0.64-0.75

7 2.85±0.21 0.58 0.56-0.61

Musca domestica

3 6.81±1.37 0.58 0.57-0.60

7 4.07+0.91 0.45 0.38-0.48

avalues adjusted using Abbott's Formula (Abbott 1925).

35

Table 9. Percent emergence of Musca domestica and Ophyra aenescens from chicken manure one day after and one week after· cyromazine was removed from food.

Dosage

0.0 0.5 0.65 0.85 l.O l.5

Musca domestica Day8

93.0 100.0 89.0 29.0 48.0 8.5

Day 14

85.0 87.0 85.0 97.0 86.0 77.0

Ophyra aenescens Day8

60.0 60.0 63.0 62.0 67.0 41.0

Day 14

75.0 63.0 61.0 63.0 56.0 94.0

'I i 1.

36

LITERATURE CITED

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

Anderson, J. F., A. Spandorf, L.A. Magnarelli and W. Glowa. 1986. Control of house flies in commercial poultry houses in Connecticut. Poultry Sci. 65: 837-844.

Axtell, R. C. & T. D. Edwards. 1983. Efficacy and nontarget effects of Larvadex™ as a feed additive for controlling house flies in caged-layer poultry manure. Poultry Sci. 62: 2371-2377.

Hall, R. D. & M. Foehse. 1980. Laboratory and field tests of CGA-72662 for control of the house fly and face. fly in poultry, bovine,. or swine· manure. J. Econ. Entomol. 73: 564-569.

Miller, R. W. 1970. Larvicides for fly control-A review. Bull. Entomol. Soc. Am. 16: 154-158.

Mulla, M. S. & H. Axelrod. 1983b~ Evaluation of the IGR Larvadex™ as afeed-through treatment for the control of pestiferous flies on poultry ranches. J. Econ. EntomoL 76: 515-519. ·

Nolan III, M. P~ & J.B. Kissam. 1985. Ophyra aenescens: A potentialbio-control alternative for house fly control in poultry houses. J. Agric. Entomol. 2: 192-WS. .


Williams, R. E. & J. G. Berry. 1980. Evaluation of CGA 72662 as a topical spray and feed additive for controlling house flies breeding in chicken manure. Poultry Sci. 59: 2207-2212.

THE EFFECT OF TEMPERATURE AND MANURE MOISTURE ON THE

PREDATORYliABITS OF OPHYRA AENESCENS (WIEDEMANN) ON MUSCA

DOMESTICA L.

Temperature and manure moisture are important factors regulating the

development of arthropod pest populations in caged layer poultry houses.

Temperature and accumulated manure in high.rise poultry houses provide

favorable conditions for development offlies year round (Stafford & Collison

1987). Optimum conditions for house fly, Musca domestica L., development are

21°c (Miller et al. 1974) and a manure moisture content of 7.0% (Peck and

And~rson 1969). Optimum development of Ophyra aenescens {W,iedemann), a

facultative predator ofthe house fly, was 26.6°C(Johnson & Venard 1957). Ophyra

leucostoma (Wiedemann), a i:elated species, was most abundant in areas with a 63% c

· manure moisture content in poultry houses in California (Peck & Anderson 1969). . . .

Temperatures in pits of poultry houses in Bent Mt., Virginia ranged from a

maximum of 21°c to a minimum of 14.8°C, and an average temperature of 21.8°C

which will support a house fly population (unpublished data).

The larvae of Ophyra spp. are predaceous on.other dipterous larvae

(Anderson & Poorbaugh 1964a, Peck 1969, Peck & Anc.lerson 1969),but not

cannibalistic (Anderson & .Poorbaugh 1964b, Hogsette 1979). In laboratory studies,

Nolan &Kissam (1985) observed.O. aenescens feeding on Musca domestica,

Phormia regina (Meigen) and Sarcophaga sp.larvae. Hogsette (1979) found that D.

aenescens could destroy more than20 first-instat house fly larvae per day during

larval development.

Ambient temperature and moisture content. of the manure may affect. 0.

37

38

aenescens' ability to control house fly larvae. The purpose of this study was to

determine the effect of temperature and manure moisture levels on the ability of 0.

aenescens larvae to control house flies.

Materials and Methods

Varying house fly to 0. aenescens ratios and manure moisture. Fresh

poultry manure was collected from the Virgiriia Tech Poultry Research Center.

The manure was taken to Price's Fork Research Facility, frozen for 24 h and then

dried in an oven at 90°C for two days. One hundred grams of oven-dried manure

was added to a plastic container. Based on the weight of the manure, moisture

levels were prepared by adding a measured amount of water to the cup to condition

the manure to obtain three percentage moisture levels, 50, 60, and 70%. The

experiment was replicated three times for each moisture level. At these levels,

house fly and 0. aenescens larvae were added at different ratios, 3:1, 2:1and1:1,

(house fly to 0. aenescens) and controls were set up, 1:0, 2:0, 3:0 and 0:1. A top

layer of vermiculite was added to prevent mold growth. All containers were

weighed and put into a cabinet which maintained a temperature of 27°C and 50%

RH. The containers were weighed each day for five days (when pupae were

noticed) and water was added to maintain the proper percent moisture level. The

number of emerging flies was recorded;

Varying house fly to 0. aenescens ratios and ambient temperature. Fresh

poultry manure was collected from the Virginia Tech Poultry Research Center and

then frozen for 24 h. The manure was thawed and a 237 ml sample was put into

containers ( 474 ml). Percent moisture of fresh manure was between 60 and 70%.

39

House fly and 0. aenescens larvae were seeded into the containers at different

ratios, 3: 1, 2: 1 and J: 1 {house fly to 0. aenescens) and controls were used, 1 :0, 2:0,

3:0 and 0:1. Ratios were replicated three times. A layer of vermiculite was added

to the surface. The containers were put into ~o cabinets which had constant

temperatures of 21and27°C respectively. For a third temperature, 18°C, a cabinet

witha constant, low temperature was not available, therefore, containers were

placed into a cool roomwhere the temperature was recorded each day. The

temperature ranged from 17-20°C with an average of 18°C;·adequately

representing the effect of low temperature onO. aenescens; .Emerged flies were

collected and the numbers recorded. Data were analyzed using two factor

ANOV A, ttestand LSD means separation (SAS Institute 1985).

Results

Moisture test: Effect of. manure moisture and competition with M.

domestica on emergence of 0. aenescens. No differences in percent emergence

were found for 0. aenescens when combined with varying ratios of M. domestica

(3:1, 2:1, 1:1) as compared with the control (0:1) (P=0.8047). There was a

significant manure moisture effect. Emergence of Ophyra aenescens at 70 and 60%

moisture level was 84 and 77%, respectively (Table 10) which was significantly

differentfrom 46% emergence at the 50% moisture level (P = 0.0001 ).

Effect of manure moisture on percent emergence of M •. domestica in

controls. House fly emergence in the controls was 81.3, 68.8 and 74.1 % at moisture

levels 50,. 60 and 70% respectively (Table 11 ). Two factor analysis indicated a

significant interaction(P=0.0363) between moisture and controls for house fly

40

emergence .. Atthe 2:0control for 60% moisture, emergence was 51%(Table11).

This percent emergence was lower than any control at any moisture level. Reasons

. for this are unclear. At the other moisture levels percent emergence between

controls did not differ more than 8%.

Effect .of manure• moisture and competition with 0. aenescens on emergence

ofM. domestica. Eniergence forthe house flieswhen combined withO. aenescens

was significantly lower from the house fly controls. At the 70% moisture level,

differences in house fly emergence were found at all three ratios (3:1, 2:1, 1:1)

(P=0.0011, P=0.0004, P=0.0001) (Fig. 1). At the 60%1evel, house fly emergence

was significantly different from the controls (P=0.0001, P=0.0139, P=0.0002 for

ratios 3:1, 2:1, 1:1, respectively) (Fig. l). Significant differences from the controls

were also found for house fly emergence at the 50% moisture level (P=0.0017,

P=0.0332, P=0.0003 for ratios 3:1,2:1, 1:1, respectively) (Fig. 1). The 0. aenescens

predation rate was significantly lower at the 50% moistureJevel (P = 0.0341) than at

other levels (Table 11 ). I tis assumed house flies died due to 0. aenescens

predation rather than other causes because the house fly emergence in controls was

at its highest in the 50% moisture level (Table 11).

Temperature Test. Effect of Temperature and competition with Musca

domestica on emergence ofOphyra aenescens. There were no differences between

0. aenescens emergence at the different ratios (3:1, 2:1, l:l)compared withthe

control (0:1). The developing house fly larvae had no detrimental effects on 0.

aenescens. There was however, a significant temperature effect(P=0.0001). The

percent emergence ofO. aenescens inthe 18°Ccontainers was 14.6% while at 27°

and 21°c the rate of emergence was 87 and 83.3% respectively (Table 12).

Effect of temperature on M. domestica inthe controls. For the house fly

41

controls, there was a decrease in the number of flies emerging at the 18°C level

(P = 0.0002). The percent emergence at 18°C was 67% as compared with 87 and

86% at 27° and 21°c, respectively (Table 13).

Effect of temperature· and competition, with 0. aenescens at different ratios

on the emergence ofM. domestica. House.fly emergence vary at the.three

temperatures (Table 13). At 18°C, there were no differences in house fly

emergence betweenthe controls (3:0, 2:0, 1:0) and the ratios (3:1, 2:1, 1:1),

(P=0.2858, P=0.0927, P=0.1802, respectively)•(Fig.2). At 21°c, there was no

difference in emergence at the· 3: 1. ratio (P = 0.1093), but there. were. differences at

the 2:1and1:1 ratiosas compared with the controls (P=0.0041, P=0.0018) (Fig. 2).

At the 27°C, differences in house fly emergence were found at all three ratios (3:1,

2:1, 1:1) (P=0.0005, P=0.0080, P=0.0145) (Fig. 2).

Ophyra aenesceru develops and emerges at 27° and 21°c but not as well at

18°C. This in turn affects its ability to prey on house fly larvae. The house fly also

had a decrease in emergence at 18°C but it is not clear whether this reduction was

due to 0. aenesceru predation or due to the effects of temperature.

The data indicate that 0. aenesceru emergence is influenced by temperature

and also by a constant moisture level. Emergence of 0. aenesceru was highest at

27°C and at constant moisture levels of 70% in chicken manure. Predation on

house fly larvae by 0. aenesceru seems to follow these conditions as the highest

predation of house fly maggots was found at 27°C and at 70% moisture level.

House fly emergence was better than 0. aenesceru in 50% moisture; in fact

M. domestica emergence was highest at 50% moisture while 0. aenesceru

emergence was lowest at the 50% moisture level. It seems M. domestica has a

greater moisture range for development than 0. aenesceru.

42

Although there was significant difference for house fly emergence between

controls and treated containers in the temperature test, there wasn't a dramatic

reduction in house fly emergence as was the case in the moisture test. Temperature

might be a factor for this in the 21° and 18°C ~est, but a lack of constant moisture

in the 27°C could be the reason for the increase in the house fly emergence. The

drying of manure in the temperature test may have hampered 0. aenescens's ability

to seek out house fly larvae. Since they are facultative predators, this would not

hurt 0. aenescens emergence. It would seem constant moisture (as in the moisture

test) helps with 0. aenescens predation on house fly larvae while the lack of

moisture (as in the 27°C temperature test) seems to.hinder predation. Thus, 0.

aenescens would be a more effective predator in areas of wet manure.

43

Table 10. Effect of manure moisture and competition with Musca domestica on emergence of Ophyra aenescens.

Manure Moisture(%)

Ratioa 70 60 50

Percent Emergence

3:1 '77.3 77.3 46.4

2:1 85.3 82.6 34.4

1:1 85.3 62.6 60.0

0:1 90.4 85.3 42.4

Meanb 84.6a 77.0a 46.0b

aRatio of M. domestica to 0. aenescens.

bMeans with the same letter are not significantly different. LSD test used to separate means (P = 0.05).

l ~··

44

Table 11. Effect of manure moisture and competition with Ophyra aenescens on emergence 'Of Musca dome~tica.

Ratioa

3:1

3:0

2:1

2:0

1:1

1:0.

Meanb

Ratio

Controls

70

2.6

73.0

1.3

74~6

2.6

74.6

2.2a

74.lab

Manure Moisture ( % )

60'

Percent·Emergence

io 74.0

5.3

51.3

4.0

81.3

3.7a

68.8b


50

10.1

79.3

18.6

86.0

9.3

78.6

12.7b

81.3a

bMeans with the same letter in rows are not significantly different. LSD test used to separate means (P = 0.05).

,,

45

Table 12. Effect of temperature and competition with Musca domestica on emergence of Ophyra aenescens.

Temperature (°C)

Ratioa 27 21 18

Percent Emergence

3:1 88.0 76.0 21.2

2:1 85.2 94.4 16.0

1:1 86.4 73.2 5.2

0:1 88.0 89.2 16.0

Meanb 86.8a 83.2a 14.4b

aRatio of M .. domestic a to 0. aenescerzs.

bMeans with the same letter are not significantly different. LSD test used to separate means (P = 0.05).

46

Table 13. Effect of temperature and competition with Ophyra aenescens at different ratios on the emergence of Musca domestica.

Ratioa

3:1

3:0

2:1

2:0

1:1

1:0

Ratio

Controls

27

60.4

85.6

60.6

88.0

57.3

88.0

59.4a

87.2a

Temperature (°C)

2r

Percent Emergence

53.3

84.0

42.6

89.3

29.3

85.3

41.Tu

86.2a


18

54.6

61.3

54.0

68.6

56.0

70.1

54.8a

66.8b

bMeans with the same letter in rows.,are not significantly different. LSD test used to separate mean~ (~~-0.05).\

100

75 w u z w 0 50 °' w :::; w 00!

25

0

100

I 60% MOISTURE

80

w u

60 z w '-' £1: w :::; 40 w ~

20

0 3-0 3-1 2-0 2-1 1-0 1-1

RATIO OF HOUSE FLIES TO 0. AENESCENS

70% MOISTURE

3-0 3-1 2-0 2-1 1-0 1-1 RATIO OF HOUSE FLIES TO Q., ~~N!~CJ:~~-

UJ u z w

- --------100..--~~~~~~~~~~~~~~~~~~~---,

50% MOISTURE

75

~ 50 w :::; w 00!

25

0 +----'---'-r 3-0 3-1 2-0 2-1 1-0 1-1 RATIO OF HOUSE FLIES TO Q., ~q.l_E;~~E!l~-

Fig. 1 House fly emergence at 70, 60 and 50% manure moisture at different house fly to Ophyra aenescens ratios.

+:--....::..

w (J z w 0 0:: w :::!! w <>11

100 27 <t

75

50

25

0

3-0 3-1 2-0 2-1 1-0 1-1 RATIO OF HOUSE FLIES TO Q. ~~ti_E.§!'.2~N_?_

~

I

'

,,

3-0 3-1 2-0 2-1 1-0 1-1 RATIO OF HOUSE FLIES TO 0. AENESCENS - --------

' 100

75 w (J z ~ 0:: 50 w :::< w <>11

25

0

21 "C

I I I I I I I

3-0 3-1 2-0 2-1 1-b 1-1

RATIO OF HOUSE FLIES TO 0....: ~E_!Jf~CJ:.!::I~-

Fig. 2 House fly emergence at 27, 21 and 18° C at different house fly to Ophyra aenescens ratios.

.!;--00

I

49

LITERATURE CITED

Anderson, J. R. & J. H. Poorbaugh. 1964a. Biological control possibility for house flies. Calif. Agric. 18: 2-4.

, Anderson, J. R. & J. H. Poorl>augh. 1964b. Observations on the ethology and

ecology of various diptera associated with northern California poultry ranches. J. Med. Entomol. 1: 131-147.

Hogsette, J. A., Jr. 1979. The evaluation of poultry pest management techniques . in Florida poultry houses. Ph.D dissertation U. of Fla. Gainesville, Fl 307

pp.

Johnson, W. T. & C. E. Venard. 1957. Observations on the biology and morphology. of Ophyra aenescens (Diptera: Muscidae). Ohio J. Sci. 57: 21-26. .

Miller, B. F., J. S. Teotia & T. 0. Thatcher. 1974. Digestion of poultry manure by Musca domestica. Br. Poultry Sci. 15: 231-234.

Nolan III, M. P. & J.B. Kissam. 1985. Ophyra aenescens: A potential bio-control alternative for house fly control in poultry houses. J. Agric. Entomol. 2: 192-195.

Peck, J. H. 1969. Arthropod predators of immature diptera developing in poultry droppings in northern California. Part II. Laboratory studies on feeding behavior and predation potential of selected species. J. Med. Entomol. 6: 168-171.

Peck, J. H. & J. R. Anderson. 1969. Arthropod predators of immature diptera developing in poultry droppings in northern California. Part I. Determination, seasonal abundance and natural cohabitation with prey. J. Med. Entomol. 6: 163-167.


Stafford HI, K. C. & C. H.Collison .. 1987. Manure pit temperatures and relative humidity of Pennsylvania high rise poultry houses and their relationship to arthropod population development. Poultry Sci. 66: 1603-1611.

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50

I i

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51

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