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thesis entitled

FACULTATIVE DISPERSAL OF THE APPLE MAGGOT,
RHAGOLETIS POMONELLA, (WALSH)
(DIPTERA: TEPHRITIDAE)

presented by
JANYCE MARIE RYAN

has been accepted towards fulfillment -
of the requirements for

Masters degree in Entomology

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FACULTATIVE DISPERSAL OF THE APPLE MAGGOT,
RHAGOLETIS POMONELLA, (WALSH)
(DIPTERA: TEPHRITIDAE)

By

Ianyce Marie Ryan

A THESIS

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

MASTER OF SCIENCE

Department of Entomology

1990

o -
(f;

(355

(0.

ABSTRACT

FACULTATIVE DISPERSAL OF THE APPLE MAGGOT,
RHAGOLETIS POMONELLA (WALSH)
(DIPTERA: TEPHRITIDAE)

BY

Ianyce Marie Ryan

Apple maggot damage in commercial orchards is often caused by
emigrant flies from unmanaged apple trees. Understanding this dispersal
can lead to more effective management. This study examines temporal and
spatial dynamics of movement, and factors initiating apple maggot dispersal.
Apple maggot flies immigrating into an unsprayed orchard were captured on
red sticky spheres and yellow Pherocon ®AM traps for 3 summers. Females
and males were caught in similar proportions. Overall preferences for red
spheres, and the predominance of gravid females suggested that flies were in
search of sites for mating and oviposition rather than food. Fruit drop was
indicated as the single most important factor initiating dispersal, as changes
in host fruit density were highly correlated with declines in trap catch. Lastly,
flies were attracted to sticky traps within a circular arena of potted apple trees,
but no clear directedness in movement could be concluded from angles of

recapture.

To Gus, who saw me through it all

iii

ACKNOWLEDGEMENTS

This thesis is the product not only of those who had direct input, but
also of the environment in which I was able to work. I am grateful to the
many people at Michigan State who made that a rich environment. Thanks
are extended to my major professor Dr. Stuart Gage, for providing material
and financial resources, generous amounts of time and thought, and much
encouragement. I would also like to thank members of my guidance
committee, Dr.s Mark Whalon, Jim Flore, Graeme Hamilton and George
Ayers for their expressed interest in the project, and their most helpful
suggestions. It was Dr. Hamilton who conceived of this project, and I am
grateful for his insight and guidance in getting me started. Dr. George Ayers
was invaluable in taking the time to work through some challenging areas
with me. His creativity, pragmatic goals and dedication (in and out of the
classroom) were a major source of inspiration throughout my program. Ellie
Groden and Frank Drummond were also advisors, and their insights over
many mealtime discussions were most helpful. In addition, I am grateful for
their model of unselfish commitment to the biological enrichment of
agriculture.

I would also like to acknowledge the following people: Dr. Frank
Drummond, for providing generous assistance with statistical analysis; Dr.
Ed Grafius for his enormously constructive advice and straight answers to
questions; Dr. Todd Bierbaum for sharing his knowledge of Rhagoletis as

well as reference materials; Tim Wirth, Karlis Kaugers and Bill Morgan, for

iv'

providing assistance with computers and many useful suggestions; Becky
Mather, for her calm competence in rescuing me from computer traumas;
and the Upjohn Company, for their accomodation in letting me use their
orchard for field studies.

Lastly, I would like to thank the friends who listened, and who
provided advice, inspiration and moral support, particularily Debbie Miller,
James N itao, Jude Sirota, Ned Walker and Joel.

TABLE OF CONTENTS

LIST OF TABLES ......................................................................................................... viii
LIST OF FIGURES .......................................................................................................... ix
INTRODUCTION ............................................................................................................ 1
Apple Maggot Dispersal ..................................................................................... 3
Apple Maggot Biology ........................................................................................ 7

CHAPTER 1. Temporal Dynamics and Composition of Dispersing

Populations of Apple Maggot Flies .................................................................. 8
Materials and Methods ......................................................................... 9

Results and Discussion ...................................................................... 11

CHAPTER 2. Factors Initiating Dispersal of Apple Maggot Flies ...................... 22
Part 1. Monitoring Apple Maggot Fly Activity ........................................... 24
Materials and Methods ........................................................................ 24

Results and Discussion ........................................................................ 26

Part 2. Effect of Host Fruit Density on Dispersal .......................................... 32
Materials and Methods ........................................................................ 32

Results and Discussion ........................................................................ 33

Part 3. Distribution of Eggs Among Apples as an Index of Oviposition

Deterring Pheromone Activity ......................................................... 39
Materials and Methods ....................................................................... 39
Results and Discussion ........................................................................ 40

vi

vii

CHAPTER 3. Directional Movement of Apple Maggot Flies .............................. 47
Materials and Methods ....................................................................... 47
Results and Discussion ...................................................................... 50
APPENDD< 1. Record of Deposition of Voucher Specimens ............................... 58
APPENDD< 1.1 Voucher Specimen Data .................................................................. 59
APPENDIX 2. Effects of Rainfall on Apple Maggot Fly Activity ......................... 60

LITERATURE CITED .................................................................................................... 67

Table 1.

Table 2

Table 3.

Table 4.

Table 5.

Table 6.

Table 7.

Table 8.

Table 9.

LIST OF TABLES

Timing of peak apple maggot fly activity and total numbers of flies
caught in the KBS orchard and unmanaged apple tree sites
in 1987 .............................................................................................................. 20

. Sample dated showing significant differences among apple varieties,

and mean comparisons for the number of apple maggot flies caught
day '1 on sticky traps in the Upjohn orchard ........................................... 27

No. of apple maggot eggs in relation to activity period, apple variety
and tree strata .................................................................................................. 41

Differences between means for the no. of apple maggot eggs per cm2
apple surface .................................................................................................... 42

Statistics for 5 releases of apple maggot flies at the Kellog Biological
Station by release, including total numbers released, numbers of
immature and mature flies, and percent recaptured ............................. 51

Actual and critical values of U for determining significance in the
directedness of apple maggot fly dispersal using Rao's spacing
test .................................................................................................................. 53

Angular deviation of mean angle of apple maggot fly capture from
the mean wind vector ................................................................................... 54

Dates and degree day accumulations for days following rainfall vs.
those not following rainfall ......................................................................... 63

Differences in activity and values of T for "rain" vs. "no-rain"
days ................................................................................................................... 64

viii

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

LIST OF FIGURES

Map of Kellog Biological Station study site showing the orchard,
unmanaged apple tree sites, and grid boundaries .............................. 10

Map of the Kellog Biological Station showing layout of the grid of
apple maggot traps ..................................................................................... 12

Apple maggot fly trap catch for each of 3 years at the Kellog
Biological Station orchard. a. Proportion of female and male flies
caught on red and yellow traps. b. Proportion of females captured
on red and yellow traps according to stage of reproductive maturity
(S=stage). SZ-immature, slight ovarian development; S3-
immature, eggs in 2 discrete bundles; S4-gravid, abdomen full of
mature eggs; SS-spent, (<10 eggs in abdomen) .................................... 14

Numbers of female and male apple maggot flies caught on red and
yellow traps, for 3 years in the Kellog Biological Station
orchard ......................................................................................................... 16

Cumulative number of apple maggot flies caught in 1987, on red
and yellow traps in the Kellog Biological Station orchard, and for
individual trees in unmanaged apple sites (B. Avenue and Duck
Lake) .............................................................................................................. 17

Numbers of gravid and immature female apple maggot flies caught
on red and yellow traps for 3 years in the Kellog Biological Station
orchard ......................................................................................................... 19

Diagram of Upjohn Co. orchard showing apple trees containing
apple maggot traps ..................................................................................... 25

Mean number of apple maggot flies caught clay‘1 on red and yellow
sticky traps, for different apple varieties in the UpJohn
orchard ......................................................................................................... 28

Mean number of apple maggot flies caught day‘1 by trap type (red or
yellow) for apple varieties in the Upjohn orchard ............................... 30

Figure 10. Cumulative percent apple drop for individual trees of different

apple varieties in the Upjohn orchard ................................................... 34

ix

Figure 11.

Figure 12.

Figure 13.

Figure 14.

Figure 15.

Figure 16.

Figure 17.

Figure 18.

Figure 19.

Figure 20.

Figure 21.

Relationship between trap catch and apple density for apple
varieties in the Upjohn orchard .............................................................. 35

Relationship between trap catch and apple density for early apple
varieties in the Upjohn orchard. Apple density within a tree was
calculated for each date by taking the total number of drops for a
tree minus cumulative drops to that date ............................................ 36

Relationship between mean trap catch of apple maggot flies and
cumulative percent apple drop for apple varieties in the Upjohn
orchard. Arrows indicate hypothesized beginning of fly

dispersal ...................................................................................................... 38

Relationship between mean and variance of the number of apple
maggot eggs apple’1 for 3 periods of apple maggot fly activity in the
Upjohn orchard .......................................................................................... 45
Diagram of release site for apple maggot flies at the Kellog
Biological Station ....................................................................................... 49
Locations of potted apple trees that caught apple maggot flies, and
the number of flies caught for each of 5 releases ................................. 52
a. Diagram showing division of release site into 8 directional

sectors. b. Proportion of apple maggot flies caught in each of 8
sectors for dates where distribution was significantly different from
randomness, and for all releases combined ......................................... 55

Number of apple maggot flies caught day’lin release arena at the
Kellog Biological Station. Arrows indicate days on which flies were
released ......................................................................................................... 57

Combined red and yellow trap catch of apple maggot flies for
indivual trees of different apple varieties in the Upjohn
orchard ........................................................................................................ 61

Mean (combined red and yellow) trap catch of apple maggot flies
for 3 replicates of each apple variety. Arrows indicate selected
sample dates that were preceeded by rainfall ("rain" dates) ............. 62

Mean (combined red and yellow) trap catch of apple maggot flies
for 3 replicates of each apple variety, with "rain" dates
omitted ......................................................................................................... 65

Introduction

Dispersal is fundamental to animal movement in that it allows
individuals to maximize their resources and respond to adversity.
Ecologically, it functions in the regulation of population density (Taylor &
Taylor 1977). Dispersal also provides an evolutionary mechanism for gene
flow among populations (Levins 1964) which allows animals to exist in
heterogeneous and changing environments (Southwood 1962).

Dispersal is a broad term, meaning the scattering of members of a
population so that the mean distance between individuals is increased. It
may include movements within as well as those away from a habitat. For
flying insects, movement within a habitat is usually termed 'trivial' or
'appetitive', and is characterized by relatively short flights and a
responsiveness to vegetative stimuli (Kennedy 1961, Southwood 1962,
Johnson 1969). Dispersal away from a habitat is termed migration, and
usually involves sustained, undistracted flight; often by pre-reproductives
(Kennedy 1961, Southwood 1962, Johnson 1969).

Distinctions between migratory and non-migratory movement are not
always clear. For example, differences may involve only levels of thresholds
for responsiveness to stimuli (Kennedy 1961), or the scale of movement
(Hughes 1979). The criterion that migration must involve a change of habitat
is somewhat ambiguous, since what constitutes a habitat. varies among
species (Hassell 8: Southwood 1978, Whalon & Croft 1987). There is likely a
continuum of dispersal between short-range appetitive movements and the
long-range, persistent flight of migration (Johnson 1969), that might be

termed medium-range dispersal. Little is known about this level of

movement. Most studies have focused on migration, perhaps because it is
often spectacular, involving large numbers of individuals. However,
medium-range dispersal may result in a change of breeding habitat, and
therefore provide the same ecological and evolutionary functions as
migration (Taylor & Taylor 1977).

The evolutionary significance of insect dispersal is that it allows a
species to keep pace with changes in the locations of its habitat. Evidence for
this theory comes from observations that dispersing insects tend to be
occupants of temporary habitats (Southwood 1962). The nature and frequency
of environmental patterns in these habitats, and the species involved
determine what type of dispersal is utilized (Hughes 1979). Changes that
occur regularly over time tend to produce obligate dispersal, meaning that it
occurs independent of factors in the immediate environment (Southwood
1962). This situation may result, for example, due to seasonal changes in the
environment, or in some cases because of management, as in agricultural
systems.

Habitat changes that are irregular tend to produce facultative dispersal,
where emigration is triggered by some factor in the immediate environment
that indicates the advance of unfavorable conditions (Southwood 1962,
Johnson 1969). This is proposed to be a highly evolved mechanism for
movement rather than an immediate response to adversity, particularly
when long-range, persistent flight is produced. In some instances a
facultative response to crowding may produce increased trivial movements
resulting in inadvertent dispersal of vagrants beyond the original breeding
habitat (Southwood 1962).

Dispersing insects tend to be r-selected, in that they are rapid colonizers

with a high potential for population increase (Begon 8: Mortimer 1981). That

insect pests as a group are apt to be r-selected (Stinner et al. 1983) is not
surprising, since this is an effective strategy for coping with the
impermanence of agricultural ecosystems. In commercial agricultural,
damage by insect pests is often dependent on recolonization each year,
because intensive use of insecticides prevents insects from overwintering
within the system. Whalon 8: Croft (1987) demonstrated the effect
surrounding habitat has on the numbers of pest insects caught in orchards.
For Michigan, these include such major pests as apple maggot, Rhagoletis
pomonella; codling moth, Cydia pomonella; and plum curculio,
Conotrachelus nenuphar, all of which typically reside in unmanaged fruit
trees or other habitats at variable distances from the potential target orchard.

Determining factors that regulate movement from source habitats is
necessary for understanding the ecology of dispersing insects. From a
practical standpoint, including source habitats in management
considerations can provide new opportunities for management. These might
include increased capabilities for scouting or warning providing lead time
before economic levels are attained, the modification of source habitats, or
management along invasion routes (Rabb 1985).

Apple Maggot Dispersal

The importance of apple maggot fly (AMF), Rhagoletis pomonella
dispersal was recognized early in the history of commercial orcharding,
because of observations that neglected, unmanaged apple trees were often
sources of AMF infesting commercial orchards (Phipps 8: Dirks 1932, Bourne
et al. 1934).

Apple maggot is usually described as a poor disperser (Whalon 8: Croft
1985), as in mark-recapture studies most flies are captured close to the release

site (Reissig 1977, N eilson 1971, Maxwell 1968). These results probably reflect

the facultative nature of AMP dispersal and not a lack of ability, since AMF
can travel over fairly large areas (e.g. up to 1 mile, Maxwell and Parsons 1968)
when fruit is absent at the release site. Experiments on foraging behavior also
indicate that AMF will not disperse when fruit is abundant (Roitberg 8:
Prokopy 1982). The facultative nature of apple maggot dispersal is further
suggested by the often episodic nature 'of infestations of commercial orchards
(Leroux and Mukerji 1963, Hamilton and Gage in review), and by the
variability in delay times from emergence in unmanaged apple sites until
arrival in commercial orchards (Olsen 1982).

A number of authors have postulated that AMF dispersal is dependent
on factors related to host fruit quality and / or density (Prokopy 8: Hauschild
1979, Olsen 1982, McNeil 8: Roitberg 1985). The density of host fruit and the
level of oviposition deterring pheromone (ODP) both affect the giving up
time (sensu Krebs et al. 1974) of an AMF within a host tree (Roitberg et al.
1982).

Host fruit density is highly variable in nature due to differences in the
phenologies of different apple varieties, which causes fruit to mature and
drop at different times. Apple variety also affects alternate bearing patterns,
susceptibility to frost (determining fruit set) and pest damage, which may
affect the rate of fruit drOp (Keck 1934, Dean 8: Chapman 1973). Variability
among unmanaged apple trees, and from year to year may explain variation
in the frequency and tinting of apple maggot infestation commercial orchards.

Quality of host fruit may also play a role in AMF dispersal. Prokopy
(1972) suggested that the exodus of female flies from a tree harboring ripe fruit
may be due at least in part to the buildup of ODP over time. In the laboratory,
females tethered to flight mills and exposed to infested, ODP marked fruit
displayed long distance flight (>1000m) more frequently and flew further than

those exposed to clean fruit (Roitberg et al. 1984). Dispersal in nature is
proposed to result from the exhaustion of suitable fruit, due to partitioning of
foraging and oviposition by females. This system appears to function for
AMF in hawthorns (Crataegus spp.), based on observed uniformity in the
distribution of eggs among fruit (Averill 8: Prokopy 1989). Uniformity in the
distribution of eggs has been noted among apple tree quadrants (Leroux 8:
Mukerji 1963, Stanley et al. 1987), and has been attributed to the role of ODP as
an epideictic (dispersal) pheromone.

Most studies of the influence of ODP on apple maggot behavior have
used Crataegus as the host, where usually only one apple maggot per fruit
will develop to maturity (Prokopy 1981). ODP is likely to be less effective in
deterring multiple ovipositions in apples for several reasons: greater size of
apple fruits allow several maggots to develop to maturity, and is reflected in
multiple ovipositions (Prokopy 1972); the longer a female is deprived of fruit
the greater the tendency for her to accept fruit marked with ODP (Roitberg et
al. 1983); and environmental parameters such as rainfall are known to alter
the residual activity of ODP (Averill 8: Prokopy 1987). ODP may have little
effect on oviposition in apples in nature, where weather conditions and the
availability of fruit are highly variable.

In addition to factors relating to host fruit quality and density, residence
time for an AMF within a tree is positively related to the distance to
neighboring trees (Roitberg 8: Prokopy 1982). This would be predicted from
foraging behavior theory where optimum residence time in a patch (tree) is
positively related to the time spent traveling between patches (Parker 8:
Stuart 1976). This result suggests movement away from a source habitat will
occur when considerable time has elapsed since locating a suitable fruit.

Moreover, it represents an efficient foraging strategy where the probability of

locating suitable hosts, after leaving the source habitat will be highly variable.
The above led McNeil and Roitberg (1985) to postulate a model for apple
maggot dispersal where frequencies of distance traveled have a bimodal
distribution as most movement is short range but under certain conditions
longer flights are initiated.

Lack of information on factors regulating facultative dispersal of the
apple maggot results in inefficient and sometimes ineffective management of
this pest. Area-wide control measures are often based on the timing of
emergence in a particular site, which fails to account for variability in pest
pressure for individual orchards. This variability was shown for Michigan
orchards by the fact that no apple maggot flies were captured in ca. one-half of
388 commercial orchards sampled between 1981 and 1984 (Hamilton 8: Gage
in review).

Variability in the timing of arrival of AMF in commercial orchards
makes prediction difficult, and many growers follow a calendar spray regime.
Because of the low market tolerance for apple maggot damage, this may result
in 5 pesticide applications aimed at apple maggot. In at least some instances
these result in unnecessary economic and ecological costs, because arrival of
flies in the orchard may be significantly delayed in relation to activity in
unmanaged sites. This delay is often greater than that attributable to '
reproductive maturation, and is therefore probably dependent on resources in
the source habitat. Understanding how these factors affect emigration of
AMF from source habitats may enable prediction of both timing and severity
of apple maggot attack in commercial orchards (Hamilton 8: Gage in review).

The main objective of this study was to determine what factor(s)
initiate facultative dispersal of AMP by examining 1) the composition of

immigrating populations, and 2) the role of fruit density and ovipositon

deterring pheromone in the emigration of AMP from apple trees. A second
objective was to examine the temporal dynamics of movement of AMP from
unmanaged apple trees into an experimental orchard.

Apple Maggot Biology

The apple maggot is endemic to eastern and midwestern United States,
breeding originally in the fruits of native hawthorns (Crataegus spp.). A host
shift to cultivated apple first occurred in New England in the middle of the
last century (Bush 1969). The species presently exists as both apple and
hawthorn infesting races.

Apple maggots typically have one generation per year. Adults emerge
from pupae that have overwintered in the soil underneath infested trees.
Emergence in Michigan usually begins in mid to late June and lasts until mid
August. Adult females are sexually immature upon emergence and are
presumed to feed on primarily honeydew and leaf exudates for a period of 1
to 2 weeks. Mating takes place on the fruit, and may occur throughout adult
life. Once eggs are mature, they are deposited just under the surface of the
skin of susceptible fruits. Insertion of the ovipositor causes a characteristic
puncture ("sting") which remains as a record of probing. The female then
drags her ovipositor on the fruit surface laying down an oviposition deterring
pheromone (ODP) which deters subsequent oviposition by herself and other
females (Prokopy et al. 1976). Eggs hatch in 3—7 days and the small larva
begins tunneling in the fruit leaving characteristic brown trails. This damage
causes fruit to drop prematurely. Larvae pass through 3 instars within the
fruit requiring 2-4 weeks for development. At the end of the third instar, the

larva exits the fallen apple and passes a final instar in the soil before pupating.

Chapter 1.

Temporal Dynamics and Composition of Dispersing Populations

of Apple Maggot Flies

A study of dispersing populations of apple maggot flies (AMF) was
conducted at the Michigan State University Kellog Biological Station (KBS) in
Kalamazoo Co., MI. AMF were caught on traps set in the KBS orchard for the
first time in the summer of 1986. Because this was the first season the
orchard had produced fruit, no AMF could have overwintered in the orchard,
and those captured were certain to have resulted from immigration. The
nearest potential host trees outside the orchard were ca. 500 m away, a
distance that would have required inter-habitat movement of AMF. This
situation provided an opportunity to study medium-range dispersal of AMF
through non-orchard environments, a subject about which little was known.

The short time (15 days) during which AMF were trapped in 1986
suggested two possible scenarios for the emigration of flies from unmanaged
apple trees around the orchard: 1) environmental factors produced
conditions favorable for dispersal so that flies emigrated from a number of
sources at ca. the same time, or 2) a relatively large number of flies emigrated
from one location in response to conditions particular to that site. An
answer to this question would help determine factor(s) that initiate
emigration of AMP.

Objectives of this study were: 1) to examine factors regulating
facultative dispersal by determining a) which members of AMP populations
dispersed (in relation to sex and age), and b) which host trees were sources of
immigrant AMF in the KBS orchard; and 2) to study spatial and temporal

dynamics of inter-habitat movement of AMF.

Materials and Methods

The KBS orchard was a 5 year old 1.5 hectare orchard of mixed disease-
resistant apple varieties in which insecticides had never been used. In 1987,
the study site also included unmanaged apple trees in the vicinity of the
orchard, and non-orchard habitat between these trees and the orchard (Figure
1).

Activity in the KBS orchard was monitored for 3 consecutive years
using two types of visual attractant traps: 2.5-inch diameter plastic red sticky
spheres (fruit mimics) coated with Tanglefoot®, and yellow Pherocon AM®
traps (foliage mimics) baited with an ammonium stearate feeding attractant.
In addition to providing information for the timing of control strategies,
these traps have been used to estimate seasonal trends in the abundance of
flies (Prokopy 1968), and to monitor dynamics of adult activity for
comparative studies (Reissig and Tette 1979, Olsen 1982, Aliniazee and
Westcott 1987). One of each trap type was hung in trees throughout the
orchard. Traps numbered 36, 51 and 72 in 1986, 1987 and 1988, respectively.

Six sites outside the orchard, comprising 41 unmanaged apple trees
were identified as possible hosts for AMF. One red and one yellow trap was
hung in each tree in foliage containing fruit clusters. Irregularity in the
distribution of fruit in trees was common, but an attempt was made to
position traps so as to maximize AMF attraction (Reissig 1975a, Drummond
et. a1 1984).

Monitoring in the non-orchard environment between unmanaged
apple trees and the orchard consisted of the erection of T-shaped
wooden "trees" (2m tall x 1m across) which were placed in holes drilled into

the ground lined with a piece of 30 cm PVC pipe. These traps were similar to

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Figure 1. Map of Kellog Biological Station study site showing the orchard,
unmanaged apple tree sites, and grid boundaries.

II

those used by Johnson (1983). One red and one yellow trap was hung on
either side of the trap cross-piece. Traps were arranged in a grid configuration
which encompassed a 62ka area, including 92 traps (ca. 50 m apart) within
an hypothesized immigration corridor, and 121 traps (ca. 100 m apart) placed
in the area surrounding the corridor (Figure 2). An effort was made to
construct as complete a grid as possible, though some areas were inaccessible.

Traps hung in apple trees, both in the orchard and in unmanaged trees
were sampled 2-3 times per week during the main period of AMP activity.
Traps within the corridor were sampled 2 times per week, and those within
the grid surrounding the corridor 1 time per week. All Pherocon AM traps
were replaced every 2 weeks. Red sticky spheres were replaced when
tackiness of the Tanglefoot was diminished due to rainfall or debris.

Date of capture, foraging intent, trap preference and sex were recorded
for all AMF caught on traps. Females were dissected to determine
reproductive stages, which were classed into 1 of 5 categories: 1) immature
(no definite structure within the abdomen), 2) immature (slight ovarian
development), 3) immature (obvious ovarian development, eggs in two
discrete bundles), 4) gravid (abdomen full of mature eggs) and 5) spent (<10
eggs in abdomen).

Air temperature degree days (base 50 °F) were estimated from
measurements of maximum and minimum temperatures (Baskerville 6:
Emin 1969).

Results and Discussion
Composition of Immigrant Apple Maggot Ply Populations

The pattern of trap catch for apple maggot flies in the orchard was
similar for all 3 years of the study (Figure 3a). The majority of flies was caught
on red spheres rather than yellow traps, suggesting that AMF immigrating

 

Figure 2. Map of the Kellog Biological Station showing layout of the grid of
apple maggot traps.

13

into the orchard were in search of apples as sites for mating and oviposition,
rather than food. This assumption is supported by data from the dissection of
females, which showed that most females trapped in the orchard were
reproductively mature (stages 4 825, Figure 3b). Reproductive maturity of
females on yellow traps was not evaluated in this study because of the small
number of flies caught.

These results suggest that the majority of dispersing apple maggot
females are capable of damaging fruit by the time they arrive in orchards.
Management in commercial orchards includes removal of most fruit (by
picking), and the use of insecticides for apple maggot control. Therefore, most
AMF found in commercial orchards are thought to result almost exclusively
from immigration, rather than from pupae overwintering in the orchard.
This assumption is supported by most studies of trap preferences in
commercial orchards. Monitoring by pest management scouts in Michigan
from 1981-1984 showed red traps were more effective (caught flies when
yellow traps did not) in 62.7% of orchards where both trap types were used,
and in ca. 58% of these orchards no flies were caught on yellow traps
(Hamilton 8: Cage in review). Similar results were obtained by Prokopy and
Hauschild (1979), in that red spheres in commercial orchards consistently
caught greater numbers of AMF than Pherocon AM traps.

Red spheres were also more effective in capturing gravid females in
the KBS orchard (Figure 3b). Olsen (1982) found that in commercial orchards,
yellow Zoecon® AM traps caught a greater proportion of gravid females than
red spheres, but this result was apparently related to the greater proportion of
males caught on red spheres in his study. Females and males in our study

were caught in roughly equal proportions for all 3 years (Figure 3a), indicating

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YELLOW TRAPS [:3 RED TRAPS

Figure 3. Apple maggot fly trap catch for each of 3 years at the Kellog
Biological Station orchard. a. Proportion of female and male flies caught on
red and yellow traps. b. Proportion of females captured on red and yellow
traps according to stage of reproductive maturity (S=stage). SZ-immature,
slight ovarian development; S3-immature, eggs in 2 discrete bundles; S4-
gravid, abdomen full of mature eggs; SS-spent, (<10 eggs in abdomen).

15

that males as well as females dispersed. Dispersal of both sexes may result in
increased reproductive success, since multiple matings in the laboratory
increased both fertility (egg hatch) and fecundity (egg-laying rate and
longevity) of apple maggot females (Opp 8: Prokopy 1986). Assuming that
flies responded to traps upon arrival in the orchard, the coincidence in timing
of catch for females and males suggests that both sexes emigrated from
unmanaged sites at the same time (Figure 4).

Reissig (1975b) and Johnson (1983) reported that yellow traps caught
more flies than red spheres early in the season in abandoned orchards. Olsen
(1982) reported this result for commercial orchards, though the difference was
not significant. The assumption of yellow traps capturing AMF early in the
season is often used by pest managers, who hang yellow traps to detect AMF
before they are capable of damaging fruit. Our results raise a question as to
the validity of this assumption, since first catch occurred earlier for red traps
(July 4 and 8) vs. yellow traps (July 13 and 20) in 1987 and 1988, respectively
(almost no flies were caught on yellow traps in 1986). Prokopy and Hauschild
(1979) also found that first catch in commercial orchards occurred on red

spheres in 14 out of 16 commercial orchards studied.

Timing of apple maggot fly activity

AMF activity plotted as a function of degree days (DD, base 50°F.)
showed considerable variance in the pattern and timing of catch among the 3
years of this study (Figure 4). Activity began earlier in 1987 and 1988 (ca. DD
1100-1250) compared to 1986 (ca. DD 1500). Comparison of early activity in the
orchard vs. unmanaged apple trees in 1987 showed little difference in the

time of first catch (Figure 5). These observations raised the question of

7o-
sol
sol
40:
3o-
20-

10‘

1986

 

0
1000
70-
601
50-
40-
30-
20-
10"I
d
04
1000
70-

NUMBER OF FLIES

60‘
50-
40-

30-

 

1000

' I
1500 2000

l - gigggfi
2500 3000

1987

'9' MALES
+ FEMALES

    

1500 2000 2500 3000

1988

 

. . . . . I
1500 2000 2500 3000

DEGREE DAYS >50°F.

Figure 4. Numbers of female and male apple maggot flies caught on red and
yellow traps, for 3 years in the Kellog Biological Station orchard.

17

:20 '. ORCHARD-1987
too 1
80'

60-

 

 

‘ T

 

”0 I ' I I I I
1000 1500 2000 2500 3000 3500

120-
. DUCK LAKE SITE

100'l
so:
so:
40:

20‘

 

 

0- u.- .p
1000 1500

 

' I V

I ' I i
2500 3000 3500

12° ‘ B. AVENUE SITE

I
2000

CUMULATIVE FLIES (%)

moi
so!
601
40:

1

20‘

 

 

 

0' ° I ' I . I ' I ' I
1000 1500 2000 2500 3000 3500
DEGREE DAYS > 50°F.

Figure 5. Cumulative number of apple maggot flies caught in 1987, on red
and yellow traps in the Kellog Biological Station orchard, and for individual
trees in unmanaged apple sites (B. Avenue and Duck Lake).

18

whether apple maggots had overwintered in the orchard. Examination of
the timing of catch for apple maggot females showed that the first flies caught
included mature as well as immature females (Figure 6), which suggested that
at least some AMF caught early in the season could have been immigrants.
Early emigration of AMF from unmanaged apple trees may have occurred
because of biennial bearing patterns which were noted for a number of
unmanaged apple trees in this study. Traps within trees having an "off" year
failed to capture AMF, even though large numbers of flies were captured the
previous year when fruit was abundant. The source of early AMF in the KBS
orchard in 1987 and 1988 could not be positively determined from this study.
However, resident flies, if any, should have been few in number, because the
proportion of immature females did not change appreciably from that in 1986,
when a resident AMF population was not possible. Proportions were 15.7,

12.7 and 19.3 for 1986, 1987 and 1988, respectively (Figure 3b).

Monitoring Inter-Habitat Movement of Apple Maggot Flies

The most likely sources of AMF immigrating to the KBS orchard were
two sites to the NW of the orchard (Figure 1), where activity peaked earlier (B.
Avenue, ca. DD 1700; Duck Lake, ca. DD 1850-2050) than in the orchard (ca.
DD 2150, Table 1, Figure 6). This observation is speculative, since efforts to
trap flies en route to the orchard failed. The grid of traps placed in the area
between the orchard and unmanaged apple trees caught only 2 flies; a mature
female and a male, ca. 200 m West of the orchard on 23 July (1858 DD, base
50°F.). It is not known whether trap density was a factor in traps not
capturing flies. The fact that this trap design was successful in capturing flies
within a non-orchard habitat (Johnson 1983) but not in this study suggests

19
4o-

' 1986
30'-

20"

 
  

 

H)“

 

   

r:
I
.1
o

2000

 

 

 

 

' I I - I
1000 1500 2500 3000

40'-

1987

 
 
 
 
 

‘9' ININIATURE
+ GRAVID

  

 

   

 

1000 1500 2000 2500 3000
40'-

NUMBER OF FEMALES

1988

30'-

20"

H)-

 

 

0 - « v .
1000 1500 2000 2500 3000

DEGREE DAYS > 50° F.

Figure 6. Numbers of gravid and immature female apple maggot flies caught
on red and yellow traps for 3 years in the Kellog Biological Station orchard.

20

Table 1. Timing of peak apple maggot fly activity and total numbers of flies
caught in the KBS orchard and unmanaged apple tree sites in 1987.

Location No. of trees Total Flies Caught Peak ActivitygDD)2

 

Orchard 511 320 2150
Duck Lake 18 769 1850-2050
B. Avenue 1 93 1700
Kettle Hole 6 305 2250-2300
School 2 64 2170
Wintergreen L. 13 44 *

1 51 out of the total 373 trees contained traps.
2 Peak activity = 50% cumulative catch in degree days (DD) base 50 °F.

" Peak activity not determined because of the small number of flies

caught/ tree.

21

that stimuli eliciting attraction of AMF might differ for intra-habitat vs. inter-
habitat movement. This study suggests that AMF do not engage in the
persistant, undistracted flight of true migrants, since this is usually
accomplished by immature females (Johnson 1969), and most females caught
in the orchard were gravid. Though little is known about longer-range
movement of AMF, there is some indication that flight may occur at heights
greater than the typical height (<2 m) for shorter-range movement. Moericke
et al. (1975) found that the flight of AMF, as measured by response to 2-
dimensional vertical rectangles, tended to be higher further from the nearest
host trees. It is possible then, that the 2m height of traps used in this study
was too low to capture AMF.

Visual stimuli provided by real trees have been shown to be important
in the attraction of AMF (Moericke et al. 1975). Such stimuli were not
essential for attracting AMF moving within a habitat in Johnson's (1983)
study, but may be necessary for the attraction of AMP moving longer
distances between habitats.

This study supports the idea that AMF immigrating to commercial
orchards are reproductively mature and in search of sites for mating and
oviposition rather than food. It also suggests that initiation of emigration
from unmanaged apple habitats is related to the lack of of suitable host fruit

in these sites.

Chapter 2.
Factors Initiating Dispersal of Apple Maggot Flies

In the summer of 1987, differences in late season apple maggot fly
(AMF) activity, as measured by trap catch, were noted in the Upjohn® Co.
orchard in Kalamazoo Co., MI. Activity declined first in early apple varieties,
suggesting that flies were dispersing from these trees. The decline in trap
catch also suggested that dispersal was related to abundance or quality of fruit
as an ovipositional resource, since these factors differ between early and late
varieties.

Differences in the rate of mortality of AMF among apple varieties
might also account for differences in late season activity. This was not
thought to be the case in the Upjohn orchard, since the timing of emergence
of AMF from different apple varieties in the orchard was not significantly
different (Hamilton et al. in review). To further explore this possibility,
however, the temporal dynamics of AMF activity among apple varieties was
compared.

Because AMF dispersal occurs during late summer when seasonal
weather changes are taking place, the possible influence of certain weather
parameters on fly activity could not be discounted. Rainfall, temperature and
windspeed were examined because they have been shown to affect trap catch
of other Dipterans (Burnett 8: Hays 1974, Dale 8: Axtell 1975, Whitfield 1981).
Barometric pressure was thought to be a potentially important variable based
on its effect on the trap catch of Tabanids (Burnett & Hays 1974), its influence
on apple maggot fly behavior (Averill & Prokopy 1987), and on
unsubstantiated claims that fly catch in commercial orchards is related to rain

storms (Hamilton & Cage in review). Data on barometric pressure was not

22

23

available for this study. Relative humidity was instead correlated with fly
activity, because of its expected relationship to storm activity.

The objectives of this study were to 1) monitor apple maggot adult
activity to examine seasonal dynamics in relation to apple variety, and to
determine the timing of fly dispersal; 2) examine the effect of host fruit
density over time on the dispersal of apple maggot flies, and 3) use the
distribution of apple maggot eggs among apples as an index for ODP activity,
to determine if egg distribution was uniform at the time of apple maggot fly

dispersal.

Part 1. Monitoring Apple Maggot Fly Activity

Materials and Methods

The Upjohn orchard comprised ca. 5 ha. of 30—40 year old standard,
unpruned apple trees, representing 5 varieties. Three varieties were used in
this study: Wealthy, McIntosh and Northern Spy, all of which had substantial
fruit loads. No insecticides had been used in the orchard for 8 years and the
orchard supported a large apple maggot population. Orchard boundaries
included woods and pasture to the West, and open fields to the North, East
and South.

Timing apple maggot fly dispersal

The timing of AMF dispersal was determined by monitoring adult
activity with Pherocon® AM traps and plastic red 2.5-inch diameter spheres
coated with Tanglefoot® (The Tanglefoot Co., Grand Rapids, MI.) One of
both trap types was hung in each of three trees for Wealthy and Northern Spy
varieties (Figure 7). Six trap pairs were hung in McIntosh trees since this
variety had two locations in the orchard (3 trees x 2 locations). McIntosh
trees were designated McIntosh 1 and McIntosh 2 to account for possible
differences in activity that might have occurred due to differences in location
and adjacent apple varieties. Traps were hung ca. 1 m apart at eye level, near
the periphery of the tree canopy and were located in the directional quadrant
where fruit was most abundant. This criteria was thought to be more
important than directional position of the tree quadrant (Reissig 1975a ) since

fruit were sometimes absent or sparse in parts of a tree.

24

25

UPJOHN ORCHARD

000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
000000000000
WMM JJ SNNNNMM
200m

237.5 m

W=Wealthy 0 apple trees

M=McIntosh . apple trees containing traps
J =Jonathon
S =Snow

N =Northern Spy

non-fruiting

Figure 7. Diagram of Upjohn Co. orchard showing apple trees containing
apple maggot traps.

26

Apple maggot flies were counted and then removed from traps every
2-3 days beginning 8 July until 9 September, 1988. Traps were also sampled on
13, 17 and 27 September. Pherocon traps were replaced at least every 2 weeks;
more often during periods of rain. Red spheres were replaced when tackiness
of the Tanglefoot decreased due to rain or when the trap became cluttered
with debris.

Statistics were performed on combined catches for red and yellow traps.
This total was thought to be less biased than catch on either trap alone, since
effectiveness of the two traps in unmanaged apple trees differs depending on
the time of season (Reissig 1975b, Johnson 1983). The mean number of AMF
caught per day was subjected to an ANOVA for each day that traps were
sampled to compare activity between apple varieties. Air temperature degree
days (base 50 °C) were estimated from measurements of maximum and

minimum temperatures (Baskerville 8: Emin 1969).

Results and Discussion

Comparison of trap catch among apple varieties for each sample date
showed an initial difference on 8 July (672 DD, Table 2, Figure 8). After this
date, no significant difference was found until fairly late in the season on 10
August (1131 DD). Differences between early (Wealthy and McIntosh) vs. late
(N. Spy) varieties were consistent through late season activity until 2
September (1371 DD).

These results suggest that prior to late season, all three apple varieties
were similarly attractive to apple maggot flies. This is somewhat surprising
since apple maggot flies are reported to attack earlier varieties first (Dean 8:
Chapman 1973, Neilson et al. 1981). However, the high level of attractiveness

of Northern Spy early in the season was shown in this study both by the

27

Table 2. Sample dates showing significant differences among apple varieties,
and mean comparisons for the number of apple maggot flies caught day”1 on

sticky traps in the Upjohn orchard.

Apple Varieties3

gate 202 Muse} W___xea1th Mc-_1 Esra: M92
7/ 8 672 4.17‘ 25a 0.5a 0.2a 0.6a
8/ 10 1131 424* 36.3a 13.0a 29.0a 4.8a
8/ 15 1210 8.09“ 27.5ab 12.5a 34.2b 8.8a
8/ 20 1271 13.1“ 6.7a 4.2a 24.4b 3.7a
8/22 1287 8.39" 7.3a 2.2a 24.7b 2.5a
8/ 25 1313 9.81“ 1.2a 5.0a 28.4b 3.7a
9/2 1371 31.2“ 6.2a 3.3a 26.3b 1.3a

1 from ANOVA a‘(P>0.05), “(P>0.01).
2 Degree Days >10°C.

3 Means in a row (not column) followed by the same letter are not

significantly different from each other (Tukey's HSD). Mc-l and Mc-2 =

McIntosh variety.

28

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29

numbers of flies caught and by apple maggot damage. Mean numbers of
oviposition punctures per apple counted for apple collections made on 28-29
July were 3.02, 3.44, and 6.96 for Wealthy, McIntosh and Northern Spy,
respectively.

Differences in late season activity between early and late varieties were
likely the result of AMF dispersal from early varieties for a number of
reasons. Temporal synchrony for early to mid season activity among apple
varieties suggests that a significant difference in the rate of fly mortality
among varieties was unlikely. Similarity in temporal dynamics would be
expected based on studies of emergence, where no differences were found in
time of emergence between apple varieties in the Upjohn orchard (Hamilton
et al. in review). This result has been noted in other orchards as well (Dean 8:
Chapman 1973). Also, because of the close proximity of different varieties in
the orchard, it is unlikely that flies emerging from under a tree of a particular
variety were limited to that variety in their activity.

Distributions of AMF for all apple varieties were apparently bi-modal
(Figure 8). This raised a question of whether a second emergence of AMF,
perhaps in relation to rainfall, might have occurred that would have
accounted for the second peak. Examination of plots separating catch on red
and yellow traps (Figure 9) showed that second peaks were due mainly to
increased catch on red traps, indicating that bi-modal distributions were not
likely due to emergence. A sudden increase in emergence of flies should
have been reflected in an increase in the number of flies caught on yellow
traps, since immature AMF are more likely to respond to the feeding

stimulus provided by yellow Pherocon AM traps (Prokopy 8: Hauschild 1979).

um N0. IDES/DAY

.30

 

co~ -

l0

 

   

WEALTHY
+ Rad’trap

* Yellow trap

 

l l

 

 

 

 

 

  
     

 

 

 

 
 

0 ..
050 750 050 050 1050 1150 1250 1850 1450 1550
25
MCINTOSH 1
2°»- ..,.,. .-...
+ Rad trap
15 .- .-_-_..- 2-2..”
"" Yellow trap
10 r» ,
5 In- .... H
0 57 5
050 750 050 050 1050 1150 1250 1350 1450 1550
25
MCINTOSH 2
20.... .. .. -.-... -
'9' Rad trap
15 ~

10

 

  

+ Yellow trap '

  

 

 

 

 

 

5
0 . .
850 750 050 050 1050 ll 50 1250 1350 I450 [550
50
Northern Spy
00 t' I . , .
‘9‘ Red trap
30 1- . .
+ Yellow trap
20 >- '
10 ~ . . . . - - .
o i : _ l 1 m4
050 750 050 050 1050 I 1 50 1250 1350 1450 1550

DEGREE DAYS >50°c.

Figure 9. Mean number of apple maggot flies caught day”1 by trap type (red or
yellow) for apple varieties in the Upjohn orchard.

31

Weather related factors are a possible explanation for patterns of trap
catch in this study, though little is known about their influence on trap catch
of AMF. Understanding the influence of weather on the dynamics of activity
was not thought to be crucial in this study, since a comparison between apple
varieties was the primary objective. This study assumed that weather
influences on trap catch should not have differed greatly among varieties.

The results of this study support the theory that declines in trap catch
for early apple varieties was due to dispersal of flies. Continued AMF activity
in the (late) Northern Spy variety may have represented either a movement
of flies from early to a late variety, or the lack of dispersal of flies present in
Northern Spy trees. Regardless, it indicates a difference in "attractiveness"
between early and late apple varieties that is important in terms of the quality
and or density of host fruit.

Part 2. Effect of Host Fruit Density on Dispersal

Materials and Methods

Fruit drop in the Upjohn orchard was monitored for a total of 9 trees of
Wealthy and McIntosh varieties (Figure 7). Northern Spy trees were not
included because the late timing of apple drop prevented total numbers from
being counted. Also, factors other than apple drop were thought to influence
declines in AMF activity for this variety because declines occurred before any
substantial number of fruit had dropped.

On each day that traps were monitored for AMF, all apples falling into
a 2m X 2m area under the tree were counted and then removed. The area of
fruit collection was located in the same directional quadrant of the tree in
which traps were placed. Apple collection continued until all of the fruit
within a tree had dropped.

Stepwise linear regression analysis was used to examine effects of apple
density, maximum temperature, windspeed and relative humidity on the
number of apple maggot flies caught per day. Rainfall was considered
separately because its influence on trap catch was not thought to be linear (see
Appendix 1). Other variables were omitted one at a time by selecting the
variable with the largest (non-significant, P>0.05) value of P and re-
computing the regression. A separate analysis was conducted for Wealthy,
McIntosh 1 and McIntosh 2 varieties. Apple density within a tree was
calculated for each date by taking the total number of drops for a tree minus
cumulative drops to that date. All data points z 1104 DD were included in
the regression, as this point was estimated to be the beginning of dispersal
from Wealthy trees (Figure 8) and therefore the earliest that dispersal should

have occurred in the orchard.

32

33

Results and Discussion

The pattern of apple drop was similar among Wealthy trees, with peak
drop (50 % cumulative drop) occurring at ca. 1075 DD (Figure 10). The pattern
of apple drop for McIntosh trees was somewhat less synchronous, but all
replicates peaked later than Wealthy trees, between 1125-1225 DD. No
consistent difference in time of peak drop was apparent between McIntosh 1
and McIntosh 2.

Examination of number of apples in trees vs. number of flies caught
showed similarities in the overall magnitude of these two factors within
varieties (Figure 11). This suggests that the number of flies foraging within a
tree was proportional to fruit density, though possible differences in the
effectiveness of traps based on fruit density was not assessed.

Stepwise linear regression analysis eliminated the weather variables
maximum temperature, wind speed and relative humidity from the model.
Apple density, however, was found to be a good determinant of the decline in
AMF activity (P>0.001, R=.95, .84, and .85 for Wealthy, McIntosh 1 and
McIntosh 2, respectively, Figure 12). Solar radiation contributed significantly
(P=0.05) to the model for McIntosh 2, accounting for 7% of the variation
(R=.91, P>0.001) in the model containing variables for apple density and solar
radiation.

Because apple density is based on cumulative drop, this study
suggested that a threshold of apple density may have been important for the
initiation of dispersal. This is somewhat difficult to ascertain from this study,
since fluctuations in fly activity make the precise time of dispersal
ambiguous. However, inspection of plots of apple maggot fly activity
suggested that dispersal probably began later than 1104 DD for the McIntosh
trees, possibly at ca. 1179 and 1211 DD for McIntosh 1 and McIntosh 2,

100 "

60

60

‘0 ...... .. .. .. .. .. . . ... .. ..

 

100

60

60

 

0
760

vomo mrpv> i m<—q>rc:co

100

 

 

...-..Wl'lt??? 2,, , . ‘ -

34

 

 

 

1460 1660

 

 

20 _, -—

I I I J I I I

860 060 1060 1160 Q60 1360 1460 1660

     

l L J. I I I I

860 950 1060 150 1250 1350 14 60 1550

Degree Days >50°C.

Figure 10. Cumulative percent apple drop for individual trees of different

apple varieties in

the Upjohn orchard.

35

   

 

 

   

 

 

 

 

      

 

 

 

   

60 - F500
. Wealthy _
5° ‘ -400
40 -
q '300
30 '-
' '200
20 '-
10 _ - 100
:3 '
a 0 " U I ‘ I ' I ‘ I ' '0
o 600 800 1 000 1 200 1 400 1600
\ 60 - F500 (0
(o ' McIntosh I 2
0’ 5° ' --400 a.
: 40 l ' 2
t q ”300
. V-
L -200 L. '0' APPLES
0) d)
a a
3 3
z ~ ~ -0 2
C 600 800 1000 1 200 1400 1600
0 60 - r500
a) . I.
Z 50 " "CIDtOSh 2 .. 400
40 ..
. ~ 300
30 '-
' ' 200
20 '-
10 _ - 100
0 ‘1 a I ' I ' I ' n D ' 0
600 800 1000 1200 1400 1600

DD BASE 50

Figure 11. Relationship between trap catch and apple density for early apple
varieties in the Upjohn orchard. Apple density within a tree was calculated
for each date by taking the total number of drops for a tree minus cumulative

drops to that date.

36

5°“ WEALTHY

g = - 2.1942 + 0.0833x R = 0.95

 
   
     

30-

20'

10"

 

 

0 100 200 ' 300 ' 400 ' 500 600
MCINTOSH l

g .-. - 0.006 + comm R = 0.04

  
   
     

 

 

v I a I I I I I
O 100 200 300 400

NO. OF FLIES / DAY

MCINTOSH 2
g = - 0.3226 + 0.0738x R = 0.85

 

 

 

0 I l ' l ' ' l
0 50 100 150 200

1

NO. OF APPLES

Figure 12. Relationship between trap catch and apple density for apple
varieties in the Upjohn orchard. Apple density within a tree was calculated
for each date by taking the total number of drops for a tree minus cumulative
drops to that date.

37

respectively (see arrows, Figure 13). If these times are accurate, then a
threshold effect was evident since dispersal would have begun at ca. 50—60%
apple drop for both varieties.

This study shows the importance of apple phenology for the
timing of AMF dispersal. Apple density is apparently the predominant factor
regulating the tinting of dispersal, given the amount of variation explained
by regression, and the lack of significance of all but one weather variable. The
significant effect of solar radiation for the McIntosh 2 variety indicates the
need for a better understanding of the influence of weather on AMF trap
catch.

Number of Flies / Day

20'-

10"

 

20"

10"

 

 

38

Wealthy

   
  

 

U U

I I I L“
000 1000 1200 1400
’ McIntosh l

 

  

 

 

l ' I
1000 1200 1400

V

800

McIntosh 2

 

 

 

' I ' t V

I
800 1000 1200 1400

DD BASE 50

  
  

  

1 600

   

1600

 

D
0‘00 o

P 120

I'

~100
loo
~60
".40
120
lo
F120
-lOO
-80
".60
L40

P

'20

b

'0

 

Cumulative 2 Apple Drop

r120
:100
'80
".60
:40

~20

 

1600

Figure 13. Relationship between mean trap catch of apple maggot flies and
cumulative percent apple drop for apple varieties in the Upjohn orchard.
Arrows indicate hypothesized beginning of fly dispersal.

Part 3. Distribution of Eggs Among Apples as an Index of Oviposition

Deterring Pheromone Activity

Materials and Methods

Three collections of apples were made corresponding to "early", "peak"
and "declining" apple maggot fly activity. These periods were estimated from
the number of flies caught in traps. The first (early season) samples of apples
for dissection were collected on 27 July for Wealthy and 28 July for McIntosh
and Northern Spy, the second (peak activity) on 8 August for all three
varieties, and a third (declining activity) on 22 and 26 August for Wealthy and
McIntosh, respectively. A third (declining) sample was not collected for
Northern Spy since most fruit remained on these trees when sampling was
concluded in late September. Because of the late date, decline in fly activity
was thought to reflect seasonal mortality rather than dispersal related to fruit
quality or density. Five fruit were randomly selected from both a lower (0-2
m) and upper (24 m) strata, from each of 10 trees (early and peak samples) or
8 trees (declining sample), for each apple variety. Fruit was refrigerated at 5°
C. until dissection.

Circumference of each fruit was recorded as a measure of relative fruit
size. Apples were examined with a binocular microscope for oviposition
punctures, and the number of unhatched eggs (or newly eclosed first instars)
was recorded. These eggs and larvae represented a limited period of female
egg laying activity since eggs usually hatch within a week (Dean and
Chapman 1973).

Apples were grouped into units of 5 to meet requirements for
ANOVA and LSD mean comparisons. The number of eggs per cm2 surface of

apple was compared for different activity periods, varieties, and tree strata, to

39

40

take into account increases in apple size as the season progressed.
Distribution of eggs among apples was assessed by calculation of b from
Taylor's Power Law ( Elliot 1977).

Results and Discussion
Comparison of parasitism by R. pomonella between activity periods, apple
varieties and tree strata 5
Overall trends in the number of eggs per apple and per cm2 apple 1
surface suggested that designation of fly activity periods was meaningful in
that the largest numbers of eggs generally occured during the peak activity

period (Table 3). LSD comparisons of means, however, showed differences

 

between activity periods were significant only for Wealthy trees (4 out of 6
contrasts, Table 4).

Comparisons of the mean number of eggs per cm2 apple surface
showed no significant differences between upper and lower tree strata, with
the exception of one sample (N. Spy, peak season). Sampling constraints in
this study prevented the collection of apples from the very tops of trees. It is
not likely that this influenced results, since previous studies have indicated
that representative samples for apple maggot damage can be taken from any
part of the tree (Stanley et al. 1987, Leroux 8: Mukerji 1963).

Differences in numbers of eggs between apple varieties were significant
during peak activity in 4 out of 6 contrasts which suggested that apples differed
in "attractiveness", in terms of suitability for oviposition during this time. In
order to compare numbers of eggs between apple varieties, it must be assumed
that rates of oviposition were not affected by differences in the number of
apples present in trees. This assumption is based on the fact that flies could

move easily between varieties, and on the indication that the number of flies

41

Table 3. No. of apple maggot eggs in relation to activity period, apple variety

and tree strata.

 

Sample Variety Stratum Tmt. N Eggs/apple N E gsI/cm2

 

 

(mean:SE) X 10E-3)
(mean+SE)

Early Wealthy 1 1 49 .37 : .53 10 1.7 : .91
2 2 49 .27 : .32 10 1.0 : .33‘

McIntosh 1 3 50 .38 : .44 10 1.1 : .29

2 4 48 .46 : .51 10 1.2 : .24

N. Spy 1 5 46 .78 : .93 9 2.5 : .52

2 6 47 .58 : .95 10 1.7: .53

Peak Wealthy 1 7 41 1.50 : .28 8 4.3 :1.00
2 8 '42 1.50 : .19 9 5.2 : .12

McIntosh 1 9 50 1.00 : .09 10 2.3: .15

2 1o 48 .17 31.18 10 4.0: .71

N. Spy 1 11 48 1.00 :20 10 3.2: .22

2 12 49 .53 : .42 10 1.5 _+_ .22

Decli- Wealthy 1 13 38 .13 :.12 8 3.2: .13

ning

2 14 34 .24 : .25 7 5.6: .18

McIntosh 1 15 40 .18 :25 8 3.0: .12

2 16 38 .21 :33 8 4.0: .19

1 N 0. eggs / cm2 apple surface

42

Table 4. Differences between means for the no. of apple maggot eggs per cm2
apple surface.

 

Comparisons between:

Fly Activity Periods

y_a_ri_e_2_ty 13:51 Contrast Mean Difference2

Wealthy 1- 7 .0260 "
7—13 .0040 "
1-13 .0014 NS
2— 8 .0042 "
2-14 .0005 NS

McIntosh 3- 9 .0008 N 5
9-15 .0001 NS
3-15 .0008 NS
4-10 .0008 NS
10-16 .0000 NS
4-16 .0008 NS

N. Spy 5-11 .0007 NS
6-12 .0002 NS

 

1 Upper and lower strata were examined separately.
(see Table 3 for treatment descriptions)

2 " Significant (P>0.05, LSD test for mean comparisons)

43

Table 4. (continued)

Comparisons between:

 

Apple Varieties Tree Strata
Mean Mean
Tmt. Contrast Difference Tmt. Contgait Difference
Early 1 -3 .0006 NS 1- 2 .0007 NS
3- 5 .0014 * 3 -4 .0008 NS
1 -5 .0007 NS 5 -6 .0007 NS
2 -4 .0001 NS
4 -6 .0006 NS
2 -6 .0007 NS
Peak 7 -9 .0041 " 7 -8 .0009 NS
9-11 .0030 " 9-10 .0002 NS
7-11 .0011 NS 11-12 .0017 *
8-10 .0048 *
10-12 .0011 NS
8-12 .0035 "
Declining 13-15 .0000 NS 13-14 .0002 NS
1416 .0002 NS 15-16 .0000 NS

44

present in trees (based on trap catch), appears to be a function of the number
of apples (Figure 11) varieties, and the number of flies present in trees (based

on trap catch) appears to be a function of the number of apples (Figure 11).

Distribution of eggs among apples

Distribution of eggs among apples was random for all three sample
periods: early, b=1.05 : .197; peak, b=.79 : .294; and declining, b=1.49 : .660
(Figure 14). No uniformity in egg distribution was found. This suggests that
ODP was not a factor in the dispersal of flies from trees, or in regulating
oviposition during the other times that apples were collected.

This result does not agree with a study conducted by Cameron and
Mukerji (1974) which examined egg distribution among apples that were non-
uniformly distributed within trees. Though the authors claimed that egg
distributions were uniform, b values they provided indicated that
distributions were clumped (Taylor 1961). Visual observations indicated that
apple distribution among trees in our study was also not uniform. However,
differences in egg distribution between Cameron and Mukerji's study and
ours may have been the result of differences in the distributions of apples.

The conclusion that ODP was not at work in the Upjohn orchard
during the time periods examined is supported by the high levels of apple
maggot damage present. Total numbers of oviposition punctures were
counted only for the first collection of apples, and therefore underestimate
seasonal damage. Mean numbers of punctures per fruit were 3.02 (Wealthy),
3.44 (McIntosh), and 6.96 (N. Spy). It is possible that ODP was not present long
enough to deter oviposition, since significant rains occurred prior to apple
collections on 23 July (46mm); and on 5 (46mm), 15 (34mm), and 23 (10mm)

of August. It is also possible that ODP is ineffective in an orchard situation

- 1 .368-20 '1

-l.OOe-l -

‘2.008-1 "

-3.00e-l

-4.00e-l

I

. EARLY ACTIVITY

 

-S.OOe-l

45

    

g = 0.1242 + 1.04541: R = 0.94

   

  

 

 

 

' I I I I ' I
-0.6 -0.5 -0.4 -0.3 -0.2 -0.1
"°j PEAK ACTIvrrY
05 q = - 0.1641 + 0.79851: R = 0.81
. El
0.0 -
B

LOG VARIANCE

 

‘ I j I fi " i _l I l ‘I I U I

-1.2 -1.0 -0.8 -0.6 -0.4 -0.2 -0.0 0.2

—0.4 -

.1

-0.5 -
-0.6 -
-o.7 -

.1

-0.8 '1

 

 

DECLINING ACTIVITY
9 = 0.4415 + 1.49on R = 0.85

  

 

I j I ' I

-o.8 -0.7 -0.6
LOG MEAN

Figure 14. Relationship between mean and variance of the number of apple
maggot eggs apple'1 for 3 periods of apple maggot fly activity in the Upjohn

orchard.

46

where large apple maggot populations may foster strong "drives" to oviposit

among females.

Chapter 3.
Directional Movement of Apple Maggot Flies

A number of experimental releases of apple maggot flies (AMF) was
conducted at the Kellog Biological Station in the summer of 1988. Flies were
released into an arena containing 24 potted apple trees arranged in 3
concentric circles. The objective was to determine if there was a directedness
to AMF dispersal, and if so, whether direction was related to wind.
Information on the directional movement of AMF would be helpful in
predicting the pest threat potential of unmanaged apple trees, and might also
provide insight into behavioral aspects of apple maggot dispersal.

Materials and Methods

Apple maggots for release were obtained from infested Wealthy and
McIntosh apples collected from the Upjohn Company orchard in the Fall of
1987. Apples were placed on one-half inch mesh hardware cloth set over
plastic trays containing moist vermiculite. Vermiculite was sifted once a
week to collect and count apple maggot pupae, which were then stored at 3° C.
in plastic containers until the following Summer. Pupae were removed from
cold storage and held at ca. 25 °C. until adult emergence. When the first flies
emerged, vermiculite containing pupae was transfered to a pan of water
where floating pupae were collected by skimming the surface. These were
allowed to air dry on paper towels. Once dry, pupae were transfered to a paper
bag containing a small amount of Dayglo® fluorescent powder and were
gently shaken to distribute the dye. Dye-coated pupae were placed ca. 200 each
in plastic petrie dishes filled with vermiculite kept moist by periodic

additions of water. These were set inside emergence cages.

47

48

Apple maggot adults were held at 22 °C. on a 16:8 light: dark regime.
Flies fed ad lib on filter paper that had been dipped in a liquid mixture of
brown sugar and yeast hydrolysate. At least twenty four hours before release,
cages containing flies were moved to an outside shelter, to allow some time
for acclimatization.

The release site was a 200 X 225 m alfalfa field bordered on the North by
a tree-lined road, on the South by an open grass pasture, and by woods to the
West and East (woods to the east began at ca. 90 ° and ran south along the east
edge of the field, Figure 18). Apple trees were arranged in 3 concentric circles
at distances of 33, 66 and 100 m from the center. Each circle contained 8 non-
fruiting, 7-8 year old crab apple trees (Malus sargenti sp.) ranging from 1.5 to 2
m in height. One ZS-inch red sticky sphere and 1 yellow Pherocon® AM trap
(cut in half) were placed in each tree. Each tree also contained a vial of
synthetic apple volatile. The release point consisted of 5 crab apple trees

without apple maggot traps, in the center of the arena.

Statistical Analysis

Data in the form of measurements of angles are considered circular
variables and require methods in circular statistics for analyses. Rao's spacing
test was used to determine if AMF catch distributions indicated a directedness
to movement. This test is suitable for multimodal as well as unimodal
distributions (Batschelet 1981). Mean angle of capture (based on tree location)
and mean wind direction were calculated for each date that distribution
differed from randomness (Batschelet 1981). Data for wind came from
weather stations at the Kellog Biological Station. Wind direction for a given
date represented the mean of hourly wind vectors for that date from 0800—

2000 hours.

49

tree-lined road

 

 

225 m

WOOOS

200 m

woods

 

33m

 

alfalfa

 

 

chain-link fence

OOOOOOOOOOOOOOOOOOOOOOOOOOOOOO

........................................
........................................
........................................
OOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOOO

IIIIIIIIIIIIIQQQ".9CQ$S.D§$t.UT?IIIIIIIIIIII'

 

 

N
. potted apple trees /I\

Figure 15. Diagram of release site for apple maggot flies at the Kellog
Biological Station.

50

Results and Discussion

A total of 154 AMF were recaptured from the 5 releases. Percentage of
recapture within a release ranged from 2.6 to 7.0 % (Table 5). All of the 24
potted apple trees caught AMF at some point in the study, though catch for
individual trees varied among releases (Figure 16). More flies were caught in
the innermost (33m) circle of traps, but this result was not surprising because
these traps were more dense in relation to area than those further from the
release point.

Distributions of AMF capture were examined for 10 different dates and
for all releases combined to determine whether there was deviation from
randomness. Significance was found for 4 dates on 1, 8, 14, and 15 September,
and for the overall distribution of AMF for the combined releases (Table 6).
Examination of individual dates to determine if directedness was related to
wind direction showed no apparent relationship between mean angle of
capture and mean wind direction (Table 7). Orientation into the wind
(anemotaxis) might be expected to show a small angular deviation between
angles of capture and wind direction. On the other hand, displacement due to
wind acting as a medium for movement should show an ca. 180° difference
in angular deviation. Neither of these situations was indicated by these data,
though some caution must be exercised because of the small number of
samples. It is also possible that anemotaxis operated only within a short
distance, after considerable displacement had already occurred, in which case
it would not have been shown by this study.

The proportion of AMF moving in a given direction was determined
by dividing the arena into 8 225° sectors, each containing 3 trees (Figure 17).

For dates where directedness was significant, most flies were captured in

51

Table 5. Statistics for 5 releases of apple maggot flies at the Kellog Biological

Station by release, including total numbers released, numbers of immature

and mature flies, and percent recaptured.

females/
release date _r_r_1_ale_s_1
Aug. 21 196/ 102
Aug. 26 "'
Sept. 1 "'
Sept. 8 "'
Sept. 14 "'

immature/
mature2

0/ 196

254/211
251/186
527/517
322/540

total

298
465
437
1044
862

released recaptured

 

number
%
21 7.0
12 2.6
25 5.7
57 5.2
39 4.5

1 sex ratios determined for the first release only

2 immature flies 1-7 days old
mature flies >7 days old

52

No. 1 (21 flies) NO- 2 (:2 flies)

  
  

   
   
 

 

 

 

i
a 2 a
l
a a T a
270 I—O—I
a 111 a
I
2
I
180 180
N0. 3 (25 flies) N0. 4 (57 flies)
0 o

T a a
fl—N— 3-0 -u—~—0:

 

270

 

180 180

270

 

180

Figure 16. Locations of potted apple trees that caught apple maggot flies, and
the number of flies caught for each of 5 releases.

53

Table 6. Actual and critical values of U for determining significance in the
directedness of apple maggot fly dispersal using Rao's spacing test.

12:13 No. of flies g1 U(alpha=.05)
8/21 11 84.0 170.3
8/22 7 77.0 177.8
8/26 6 173.0 180.7
9/1 12 172.5: 169.2
9/2 9 115.0 173.5
9/8 27 240.0: 158.9
9/9 12 120.0 169.2
9/10 8 112.5 112.5
9/14 25 230.4: 158.9
9/15 13 193.8" 167.8
All

Releases 150 321 .6" 144.7

1 " indicates significant difference from randomness, U > U (alpha).

54

Table 7. Angular deviation of mean angle of apple maggot fly capture from

the mean wind vector.

 

 

Mean angle Mean wind Angular
Date of capture° directi0n° deviation°1
9/1 289.2: 21.2 171.8 : 4.4 117.4
9/8 51.5:10.1 174.1 :3; 3.8 122.6
9/14 290.4 3; 12.0 284.1 114.8 6.0
9/15 44.2 i 17.1 84.7 1; 3.5 40.5

1 Based on the smallest angular distance given that 0°= North and angles are

numbered clockwise.

55

 

 

 

 

    

“ o
1 September 1 (12 flies)
.
30 -
90’ E i
20 -
10 -
IBO‘ o -
s 1 2 3 4 5 6 7 8
so . 30 - ,
- September 8 (26 flies) September 14 (25 flies)
20 -

 

 

Percent

September 15 (13 flies)

   

Direction

Figure 17. a. Diagram showing division of release site into 8 directional
sectors. b. Proportion of apple maggot flies caught in each of 8 sectors for

dates where distribution was significantly different from randomness, and for
all releases combined.

56

sectors 3 and 7, while the fewest were caught in sectors 4 and 5. This was also
the pattern for all releases combined. The reason for this is not known, but
may have been related to visual cues provided by large trees, which were
present on all field borders except the south. There is also the possibility that
AMF left the field, perhaps to feed in adjacent areas, and then returned,
which might bias the direction of capture. The possibility that AMF entered
the release arena from outside areas can not be excluded because fluorescent
marks on flies were not always discernable. This is likely a remote possibility,
however, because traps hung in apple trees near the release site were no
longer catching AMF at the time of releases. It is possible that AMF could
have come from the adjacent woods, but the coincidence in timing of capture
with releases indicates that most flies were likely the result of releases (Figure
18).

Studies using distributions resulting from trap catch are always limited
by the fact that trap catch is an end result that does not track actual insect
movement. This study therefore assumes a relationship between angle of
capture and direction of orientation. Based on the number of distributions
that did not differ from randomness and the apparent lack of correlation
between angles of capture and wind direction, direction of AMF dispersal
appears to be independent of wind direction. The degree to which
directedness in AMF dispersal occurs is not clear from this study since
randomness was indicated for ca. one—half of the distributions examined.
Results may have been limited by the number of flies released. Releases of
larger numbers of flies in an arena similar to the one in this study might
provide an answer to this question. In addition, the success in captures of
flies at all distances in this study indicates that this experimental set-up may

be useful in studying possible long range cues in the attraction of AMF.

 

57

 

30 -
d
g 20 '-
1.1..
O
o'
t: 10 , *
1
1
1
0 1
2122232425262720301 2 3 5 6 7 0 9101112131415

August September

Figure 18. Number of apple maggot flies caught day'lin release arena at the '
Kellog Biological Station. Arrow indicate days on which flies were released.

 

APPENDICES

 

58

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.: 1990-02

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

Facultative Dispersal of the Apple Maggot, Rhagoletis

 

Pomonella (Walsh)(Diptera: Tephritidae).

 

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

Investigator's Name (5) (typed)
.danyce MarieLRYan

 

 

Date May 12, 1990

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

Deposit as follows:

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

Copies: 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 MDseum.

59

APPENDIX 1.1

Voucher Specimen Data

Page 1 of 1 Pages

 

 

11K 1k mumn HJMMMWWW
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.E honoEoucm

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pom mawfiwomnm wwumwa m>onm ozu vm>wmumm
Nelomma .oz umnuao>

 

 

00ml .2 .8: mama

 

 

 

:mhm wand: schema
Acmamuv Amvmsmz m.u0umwfium0>cH
Amummmooma ma muomnm Hmcowuavvm omsv

 

 

 

 

 

 

 

 

 

 

 

.D.m.z a CH nwofi .uonsmumom Hz ..oo oonmamam MHHmaoaom,mfiuoHowmam
m<nHHHm:AMH "<MMBAHQ

406+ vmuwwomov paw pom: no pmuumaaou aoxmu umcuo no mmwummm

m e r r m m e .m % mcmeauoam new sump Henna

e r 0.0 e .1 .1 a p. w s

s e p.e .n u u p. m. .6

u.n e t t .d .d u a 20

M w.d.1 “U .A AA D. N .L “E a

 

“mo Hmassz

 

 

 

Appendix 2
Effects of Rainfall on Apple Maggot Fly Activity

Inspection of plots of apple maggot fly (AMF) activity showed frequent,
rapid declines in trap catch that occurred at ca. the same time for most trees
(Figure 19). Since declines corresponded with sample dates preceeded by
rainfall, this relationship was examined by conducting paired T-tests of trap
catch following rain vs. that not following rain. Five days following rainfall
were selected within the main period of apple maggot fly activity; ca. 850-1200
DD (Figure 20), and these were paired with the day closest in DD that was not
preceeded by rainfall (Table 8). Each pair served as a replicate within blocks
(apple varieties) . Dates within a pair differed by <50 DD accumulations so
that fly density, excluding the influence of environmental parameters, was
assumed to be similar.

Results of paired T-tests were significant (P>0.05) for all varieties,
indicating that apple maggot fly activity was significantly reduced on days
immediately following rainfall (Table 9). Omission of data points for all
"rain" days (11 sample dates were preceeded by rain and therefore omitted)
had the effect of "smoothing out " curves, (Figure 21).

Rainfall appears to decrease AMF activity. This result seems
reasonable, since flies might be expected to take cover during rains. It should
be considered with some caution, however, since other weather parameters
(e.g. windspeed and solar radiation) are likely to be correlated with rainfall. In
addition, the relationship between rainfall and trap catch is probably more
complex, and depends on intensity and duration of rainfall as well as
accumulation. A light rainfall in some instances may increase trap catch

(Looses 1976). This study indicates that there is a need for more information

60

61

No. 01 "ha/day
so

 

 

 

 

 

 

 

 

 

 

McIntosh 2

 

 

 

 

 

60"

40

20

 

 

 

 

O .
660 760

Degree days 2 50°C.

Figure 19. Combined red and yellow trap catch of apple maggot flies for
indivual trees of different apple varieties in the Upjohn orchard.

62

0mm:

 

 

.333 :52.» :82?" .3 60380.5 0.83 “85
83.6 295.6. 83020» 88:05 250.54 .5854, 03% :08 mo 858:8.” m .48
85 Lomwnfi made no :38 nab A3028» can no." 885803 :82 .om 0.5me

m 8888: 1mT .am 56582 ll ._ .8356: IT 3:8: 11
.o 6 on A manna monwma
one onno onme onoa onoa ono onn one onn

u widow/u .13.}. _
(AV A... -

 

al.; 11111115111111. 7.1111111...

_ . - _ 1*
fin
». /

 

 

 

 

 

 

 

 

 

 

nop\m0:m .08 9802

63

Table 8. Dates and degree day accumulations for days following rainfall vs.

those not following rainfall.

 

Actual date

 

 

Rep "No rain" day 122 "Rain” day 122 of rain - Amount
1 7-26 899 7-24 877 7—23 46 mm
2 7-28 926 7-30 957 7-30 2 mm2
3 8—1 989 8-3 1027 8—3 0.5 mm
4 8-8 1104 8-6 1074 8-5 46 mm
5 8-13 1179 8-10 1131 8-9 27 mm
1 Degree Days > 50 F°

2 Rain accompanied by avg. daily winds of 2.3 m/s

64

Table 9. Differences in activity and values of T for "rain" vs. "no-rain" days.

Differences in

 

Block Variety pg Activity 1(X-1-SE) I
1 Wealthy 4 17.53 _t 6.19 283*
2 McIntosh 1 4 9.61 : 1.80 5.34"
3 McIntosh 2 4 11.07 i 2.59 427*
4 N. Spy 4 21.88 i 3.59 6.10"

1 measured as mean no. flies caught/ day (N =3)
" significant (P>0.05) Paired T-test

65

 

 

63:80 8.3 :58: firs Snow—g 03mm :08 no 85828: n no»
88 6&me 2%? mo :38 nab 35mg 98 pm." 85988 502 .3 933.3

N 83562 lmT 2m .z 1.1 a 8356: IT 2:8; ll.

.0 o omA manna 00.4me

o9; coma coma on: omofi com com own.

 

 

_ _ 1

 

 

 

 

 

 

 

 

 

 

--.. < 1.1-1-1111...

 

 

engines.“ dd :80:

ca

ON

on

04

on

ow

66

on the effects of weather on apple maggot behavior. A better understanding

of these influences will allow more accurate interpretation of trap catch data.

 

1H .

LITERATURE CITED

LITERATURE CITED

Aliniazee, M..T 8: R..L Westcott. 19871;.h Flight period and seasonal
development of the apple maggot, hagoletis pomonella (Walsh)
(Diptera: Tephritidae), in Oregon. Ann. Entomol. Soc. Am. 80(6): 823-28.

Averill, A.L. 8: RI. Prokopy. 1989. Distribution patterns of Rhagoletis
pomonella (Diptera: Tephritidae) eggs in hawthorn. Ann. Entomol. Soc.
Am. 82(1): 38-44.

Baskerville, CL 8: P. Emin. 1969. Rapid estimation of heat accumulation
from maximum and minimum temperatures. Ecology 50: 514-17.

Batschelet, E. 1981. Circular Statistics in Biology. Academic Press, Inc. New
York.

Begon, M. 8: M. Mortimer. 1981. Population Ecology: A Unified Study of
Animals and Plants. Blackwell Scientific Publications. Oxford.

Bourne, A.I., W.H. Thies 8: FR. Shaw. 1923. Some observations on long
distance dispersal of apple maggot flies. J. Econ. Ent. 27: 352-55

Burnett, A.M. 8: K.L. Hays. 1974. Some influences of meteorological factors
on flight activity of female horse flies (Diptera: Tabanidae). Environ.
Entomol. 3: 515-21.

Bush, CL. 1969. Sympatric host race formation and specialization in
frugivorous flies of genus Rhagoletis (Diptera: Tephritidae) Evolution 23:
237-51.

Cameron, R]. 8: F0. Morrison. 1974. Sampling methods for estimating the
abundance and distribution of all life stages of the apple maggot,
Rhagoletis pomonellg (Diptera: Tephritidae). Can. Ent. 106: 1025-34.

Dale, W.E. 8: RC. Axtell. 1975. Flight of the salt marsh Tabanidae (Diptera),
Tabanus n_igrovittatus, Chrysops atlanticus and _C__. fugliginosus:
correlation with temperature, light, moisture and wind velocity. J. Med
Ent. 12, 5: 551-57.

67

68

Dean, R.W. 8: RI. Chapman. 1973. Bionomics of the apple maggot in eastern
New York. NY St. Ag. Exp. Sta. Search 7. 63 pp.

Dingle, H. 1972. Migration strategies of insects. Science 175: 1327-35.

Drummond, F., E. Groden 8: R]. Prokopy. 1984. Comparative efficacy and
optimal positioning of traps for monitoring apple maggot flies (Diptera:
Tephritidae). Environ. Entomol. 13: 232-35.

Elliot, J.M. 1977. Some Methods for the Statistical Analysis of Samples of
Benthic Invertebrates. Freshwater Biological Association Scientific
Publication No. 25.

Hamilton, J.C. 8: SH. Gage. Apple maggot, Rhagoletis pomonelfi (Walsh)
occurrence and damage in Michigan apple orchards: a case study in
analysis of the CCMS regional crop monitoring data base. In review.

Hamilton, J.G., S.H. Gage, 8: ME. Whalon. Effect of soil moisture on adult
emergence of apple maggot Rhagoletis pgmonella (Walsh) (Diptera:
Tephritidae). In review.

Hassell, MP. 8: T.R.E. Southwood. 1978. Foraging strategies of insects. Ann.
Rev. Ecol. Syst. 9:75-98.

Hughes, RD. 1979. Movement in population dynamics. Pp. 14-34 In R.L.
Rabb 8: (3.6. Kennedy eds. Movement of Highly Mobile Insects: Concepts
and Methodology in Research.

Johnson, CG. 1969. Migration and Dispersal of Insects by Flight. Methuen,
London.

Johnson, RC. 1983. Response of adult apple maggot (Diptera: Tephritidae) to
Pherocon AM traps and red spheres in a non-orchard habitat. J. Econ.
Entomol. 76: 1279-84.

Keck, CB. 1934. Relation of oviposition punctures of the mediterranean fruit
fly to the premature dropping of citrus fruits. J. Econ. Ent. 28: 908-914.

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