FACTORS AFFECTING MATING, MONITORING AND PHENOLOGY  

OF GRAPE BERRY MOTH, PARALOBESIA VITEANA,  

IN MICHIGAN VINEYARDS 

By 

Keith Scott Mason 

 

A DISSERTATION 

 

Submitted to 

Michigan State University 

in partial fulfillment of the requirements 

for the degree of 

 

Entomology – Doctor of Philosophy 

2018  

 

 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

ABSTRACT 

FACTORS AFFECTING MATING, MONITORING, AND PHENOLOGY  

OF GRAPE BERRY MOTH, PARALOBESIA VITEANA,  

IN MICHIGAN VINEYARDS 

By 

Keith Scott Mason 

Paralobesia viteana (Clemens), the grape berry moth (GBM), is a major economic pest of 

cultivated grapes in Eastern North America. Although pheromone lures and traps are available 

for monitoring this pest, male moth captures in these traps are not consistent between Michigan 

grape-growing regions, and male captures decline as the infestation increases through the 

multiple generations that occur during a season. This makes it difficult to use traps to monitor 

this pest’s population dynamics and complicates the timing of pest management activities.  

Substantial regional variation exists in the magnitude of the response of male GBM to sex 

pheromone-baited traps in Michigan vineyards. Males are readily captured in traps in the 

southwest region, whereas in the northwest very few males are captured. However grape berry 

moth larval infestation is found in fruit in both regions. Using Y-tube choice tests and trapping 

trials with captive females, I determined that males from Southwest and Northwest Michigan 

responded similarly to the standard pheromone blend, and males did not preferentially choose 

females from the same population. From these results I conclude that the regional differences in 

male captures are not due to differential responses of males in these respective areas. I postulate 

that the reason fewer males are trapped in Northwest Michigan is because the P. viteana 

population is much smaller than in Southwest Michigan.  

To test whether seasonal changes in the plant canopy affect captures of male grape berry 

moth, I manipulated grapevine fruit density or canopy structure in multiple growing seasons, and 

 

 

measured male captures under these conditions. Removal of either 50 or 100% of the fruit 

clusters from vineyard plots did not consistently affect captures in pheromone traps. In a separate 

canopy manipulation experiment, I detected significant differences in male captures between 

unaltered and open canopies for some sample periods, and there was a trend toward numerically 

more male captures in unaltered than in open canopies. I conclude that fruit presence, fruit 

density and canopy fullness do not reduce male P. viteana captures late in the season, and thus 

do not explain the seasonal pattern of development and abundance of this insect. 

Experiments that measured the frequency, intensity and duration of mating and 

reproductive behaviors in colonies held under different temperature and photoperiodic conditions 

were used to determine that temperature is the likely driving force behind the seasonal variation 

in male P. viteana captures, and thus shapes the observed phenology of this pest. The frequency 

of male flights, mating and oviposition increased with temperature. This amplified activity helps 

to explain the intensification of oviposition and subsequent larval feeding damage in vineyards 

during the summer and early fall when conditions are warm. My data also show the proportion of 

male flights that occur when females are not receptive to mating is greater at lower temperatures, 

which helps explain why more males are trapped in the spring when temperatures are cool.  

Traps baited with lures that contained different quantities of P. viteana sex pheromone 

were used to determine that the increased amount of pheromone released by lures during hot 

periods can reduce male captures. My research shows that temperature is an important factor that 

governs the behaviors associated with mating and reproduction, and also influences the main tool 

for monitoring this pest, the pheromone trap. Taken as a whole, the effects of temperature on 

behavior and trapping strongly shape the observedphenology of this pest. 

 

 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

For my wonderful family, Julienne, Lindsey and Justin, and my parents, Gail and Charles 

Mason, I dedicate this dissertation to you with all my love and many thanks 

for your constant support and encouragement during this process. 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

iv 

 

 

 

ACKNOWLEDGMENTS 

 

First, I thank my wonderful wife Julienne and our beautiful children, Lindsey and Justin. The 

love and support that you have given to me through these past few years has been a great help 

and potent motivator to keep me focused and help me finish. I also thank my parents, Gail and 

Charles Mason, who have been behind me all the way, in mind, body and spirit. 

I could not have asked for a more engaged guidance committee in Drs. Jim Miller, Jim 

Smith and Randy Beaudry. I thank you for your ideas and input as my research progressed. You 

challenged me to think broadly and deeply about all the intricacies of my research projects. This 

includes proper interpretation of my data, identification of the meaningful implications of my 

results, and wrapping it all up to present a good story.  

Rufus Isaacs, my major professor, my boss, my friend. I can’t thank you enough for your 

patient guidance, sound advice and unwavering support in all my times of need. In all of our 

interactions, whether as an employee, student or colleague you have made me feel that my ideas 

and opinions are valuable, and that my work is appreciated. It has been an absolute pleasure, and 

you have been an incredible influence for me personally and professionally, and I know this is a 

similar story with others that have passed through your lab. 

 

Natalia Botero-Neerdaels, thank you for providing the seed that developed into my own 

work with grape berry moth. I have also modeled my interactions with collaborating growers 

after what I learned from you. Zsofia Szendrei, I greatly appreciate your help and guidance with 

the GC-MS analysis that was an integral part of my research, and thanks also for your assistance 

with my initial attempts to use PCR.   

 

Chris Adams and Phil Fanning have been my in-house support system during my PhD. I 

thank you both for picking up my slack and for your help, advice, encouragement, friendship and 

 

v 

juicy departmental gossip. Juan Huang and Adam Ingrao, thanks to both of you for the GC-MS 

methods and advice that I used to analyze pheromone samples. I thank Angie Zhang for help 

with GIS data, and Bing Tong from the MSU Center for Statistical Training and Consulting for 

statistical advice. 

 

I must thank my Isaacs Lab comrades and the farm staff at Trevor Nichols Research 

Center and Northwest Michigan Horticulture Research Center for help with experimental set up 

and collecting data. In particular, I want to thank the student workers that I have had the chance 

work with and mentor during my PhD: Alexander Apostle, Laura Bizzarri, Jordan Brandel, 

Therese Costantini, Holly Drankan, Jeremiah Eaton, Matt Hiles, Nolan Jahn, Rachel Labby, Ian 

McCririe, Josh Paavola, Dan Pickard, Guy Procopio, Trisha Samota, Hayley Sisson, Chris Worst 

and Zach Yarost. I hope you were able to learn something useful from me; as I know I have 

learned from you. 

I have had the good fortune to work with many Michigan grape growers during my time 

at MSU, and I am thankful for all that you have taught me about the practical side of viticulture, 

and for allowing me to do research in your vineyards. I thank the following grape producers 

along with their families and employees that have been an important part of my research: Ed 

Oxley, Bryan Cronenwett, Rick Brown, Francis Ryan, Bill Mihelich, Chuck Felcyn, Bob and 

Jason Pagel, Jeff Lemon, Jim Shafer, Larry Mawby, Shady Lane Winery and Leorie Vineyards. 

I also gratefully acknowledge the Ray and Bernice Hutson Trust Fund, Project GREEEN, The 

Michigan Grape and Wine Industry Council, The National Grape Cooperative and the US 

Department of Agriculture for providing funding for my research. 

 

vi 

TABLE OF CONTENTS 

 

LIST OF TABLES……………………………………………………………………………….. x 

LIST OF FIGURES.………………………………………………………………………………xi 

CHAPTER 1 NATURAL HISTORY, ECONOMIC IMPORTANCE, AND VARIATION IN 
MONITORING PARALOBESIA VITEANA  ……………………………........................................1 
Taxonomy and biology…...……………………………………………………………….1 
Nomenclature……………………………………………………….......................1 
Hosts, habitat and distribution……………………………………………….........1 
Life cycle and reproductive biology………………………………………………2 
Economic importance....……………………………………………...................................3 
History of P. viteana management….………..……..……………………………………..4 
The rise of IPM.……...………………………………………...………….…….....5 
Monitoring...……….…...……………………………………………………….................7 
Thresholds….………………………………………………...…………………....7 
The MSU Enviroweather model..………….……………………………..………..7 
The importance of pheromones in monitoring….………….………………….......8 
The sex pheromone of P. viteana.…..………………………...……...……............8 
Geographic variation in sex pheromones..………….….…………………….……………9 
Variation between P. viteana populations...….….……………………………......9 
Regional variation in other species….………………………………...................10 
Seasonal variation in male captures…...……………………………………....................11 
The paradox between moth captures and infestation……………….....................11 
Plant volatiles as insect attractants...………………………………………..........12 
Do grape clusters influence male captures?...........................................................13 
Does the grape canopy reduce male captures?.......................................................14 
Temperature and photoperiod effects on P. viteana…….…………..………...................15 
Relationships between male captures, temperature and photoperiod…….....…...15 
Temperature and insect physiology……………………………………………...16 
Longevity………………………………………………………………………...16 
Activity and movement………….…………..……………………...................................17 
Effects on flight…………………………………………………………………..17 
 
Oviposition and temperature………………………………………......................18 
Effects of temperature and photoperiod on activity cycles………....................................18 
Temperature and activity.………………………………………………………...18 
Photoperiod and activity.…......….…………………...…………………....….….19 
Pheromone release and temperature…...……...………………………….............20 
Research goals.……………..…………………….……………………………...……….21 
 
 

 
 

 

vii 

CHAPTER 2 LOW CAPTURES OF MALE PARALOBESIA VITEANA IN MONITORING  
TRAPS ARE NOT DUE TO GEOGRAPHIC VARIATION IN MALE RESPONSE TO 
PHEROMONES.…………………………………………………………………………………22 
INTRODUCTION...……….………………………………………………………………...22 
METHODS.…….......………………………………………………………………………..25 
Study insects……………………………………………………………………………..25 
Bioassays.………………………………………………………………………………..25 
Field trials.……………………………………………………………………………….29 
RESULTS….………………………………………………………………………………...32 
Bioassays.………………………………………………………………………………...32 
Field trials.………………………………………………………………………………..33 
DISCUSSION..….……………………………………………………………........................35 

CHAPTER 3 JUICE GRAPE CANOPY STRUCTURE AND CLUSTER AVAILABILITY DO 
NOT REDUCE MIDDLE AND LATE SEASON CAPTURES OF MALE GRAPE BERRY 
MOTH, PARALOBESIA VITEANA (LEPIDOPTERA: TOTRICIDAE) IN SEX PHEROMONE 
TRAPS…………………………………………………………………………………………....41 
INTRODUCTION…………………………………………………………………………...41 
METHODS…………………………………………………………………………………..46 
RESULTS……………………………………………………………………………………49 
DISCUSSION………………………………………………………………………………..53 

CHAPTER 4 RESPONSE OF PARALOBESIA VITEANA TO TEMPERATURE PROVIDES 
INSIGHT INTO SEASONAL PATTERNS OF MOTH FLIGHT AND VINEYARD 
INFESTATION…………………………………………………………………………………..58 
INTRODUCTION…….…………………………………………………..............................58 
METHODS………….…………………………………………………………...……..........66 
Insect rearing….…………………………………………………………...……………..66 
Moth longevity...…..……………………………………………………………………..67 
Minimum flight temperature.....…………………………………………………….........68 
Oviposition.…………………………………………………………………………........70 
Duration and frequency of the mating period and male flight period…….……...………71 
Response to pheromone lures at different times of the season….….………....................74 
RESULTS .…………………………………………………………………………………...80 
Moth longevity…………………………………………………………………...……....80 
Minimum flight temperature…………..………………………………………………....81 
Oviposition…………………………………………………………………………….....83 
Diel patterns of mating and male activity in colonies…..…….….....................................84 
Constant temperature...……………………...……………....................................84 
Day length.....…………………………………………………………….............89 
Diurnal temperature cycles........………………………………………………….95 
Response to pheromone lures at different times of the season…..……………………..100 
DISCUSSION...…………………………………………………………………………….106 

 

 

 

viii 

CHAPTER 5 SYNTHESIS AND FUTURE RESEARCH NEEDS………………....................118 

APPENDIX……………………………………………………………………………………..126 

LITERATURE CITED.………………………………………………………………………....128 

      

 

ix 

LIST OF TABLES 

 

Table 4.1 Average daily temperatures and day lengths for April to October 2010 – 2014 for 
Lawton, Michigan..………………………………………………………………………............66 
 
Table 4.2. Stock solutions, dilutions and loading volumes to make lures for field testing……...75 
 
Table 4.3. Summary of mating and male flight measurements for colonies held at constant 
temperatures. Values in the same column with different letters are significantly different  
(P < 0.05).………………………………………………………………………………………..87 
 
Table 4.4. Summary of mating frequency and male flight measurements for colonies of 
Paralobesia viteana held under different day length regimes. Values in a given column with 
different letters are significantly different (P < 0.05).…………………………………………...92 
 
Table 4.5. Summary of mating frequency and male flight measurements for colonies held under 
diurnal temperature regimes. Values in a column values with different letters are significantly 
different (P < 0.05).……………………………....……………………………………………...99 
 
Table 4.6. Analysis of covariance to determine if the relationship between male captures of P. 
viteana and pheromone release differs between samping periods ……………………………..103 
 
Table 4.7. Comparison of least squares means for captures of P. viteana in different sample 
periods (Tukey’s HSD). Means with the same letter are not significantly different …………..103 
 
Table 4.8. Analysis of variance and parameter estimates from linear regression of residuals from 
the analyses in Figure 4.22 to evaluate the effect of pheromone release on captures of male P. 
viteana after removing the effect of temperature……………………………………………….105 
 

 

x 

LIST OF FIGURES 

 

Figure 1.1. Pyramid of IPM tactics……………………………………………………………….6 

Figure 1.2 Geographic variation in the response of P. viteana males to pheromone-baited traps 
and incidence of grape berry moth feeding damage at representative vineyards in the major grape 
growing regions of Michigan in 2015. Note difference in Y-axes between graphs. Blue solid line 
indicates male moth capture and orange dashed line denotes P. viteana damaged cluster..……...9 
 
Figure 1.3. Phenology of P. viteana in southwest Michigan. Captures of males (gray solid line) 
are highest during the first generation, when berry infestation (green dashed line) is lowest. In 
the second and third generations, male capture is lower, but infestation increases until harvest. 
Data are averages from eight commercial vineyards during 2015.Temperatures at the top of the 
figure are the range of average daily temperatures for each generation in 2015………………...12 
 
Figure 2.1. Y-tube apparatus to test behavioral responses of male P. viteana to a standard 
pheromone blend or to females from different populations. Left) Y-tube set up showing 
experimental enclosure; middle) close-up of Y-tube; right) male moth in one arm of the Y-
tube……………………………………………………………………………………………….27 
 
Figure 2.2. Captive female traps and lures for comparing the response of males in northwestern 
and southern Michigan vineyards. Left to right: Captive females in a mesh cage inside a trap. 
Standard pheromone lure loading set-up (inset in upper left shows orientation of septa for 
loading). Pherocon VI (Delta) trap with a standard pheromone lure deployed in a 
vineyard.………………………………………………………………………………………….29 
 
Figure 2.3. Percentage of P. viteana males from northwest and southwest Michigan that chose 
the Y-tube olfactometer arm containg a pheromone sample. This was not significantly different 
between regions………………………………………………………..……………………………....32 
 
Figure 2.4. Percentage of P. viteana males from northwest and southwest Michigan that chose 
the Y-tube olfactometer arm containg a female from the same or different regions. Males did not 
prefer females from the same 
region……………………………………………………..………...…………………………....33 
 
Figure 2.5. Response of resident male P. viteana to traps deployed in vineyards in Northwest- 
and Southwest-Michigan. Traps were baited with pheromone lures or captive P. viteana females 
from Northwestern or Southwestern Michigan. Columns labeled with the same letters are not 
significantly different (P > 
0.05).……………………………………………………………………………..........................34 
 
Figure 3.1. Vineyard plot containing a triangular tunnel designed to keep grape canopy open. 
Photograph was taken early in the season before the canopy was fully developed……………...47 
 

 

xi 

Figure 3.2. Effect of cluster removal on capture of male P. viteana. Captures of male P. viteana 
in plots with 0, 50% or 100% of clusters removed in 2013, 2014 and 2015. Columns with the 
same letter are not significantly different; “NS” indicates no significant differences were found 
among treatments, P > 0.05……………………………………………………………………...50 
Figure 3.3. Effect of manipulating canopy structure on captures of male P. viteana. Male 
captures in plots with unaltered, dense juice grape canopies (Unaltered) or canopies held open 
with a triangular tunnel (Open) in 2012, 2014 and 2015. Asterisks indicate treatments were 
significantly different (P <0.05). This experiment was run in a Concord vineyard in 2012 and in 
a Niagara vineyard in 2014 and 2015.………...…………………………………………………52 
Figure 4.1 Model of changing female pheromone production (purple dashed line) and male 
response to pheromone (solid black line). The gray rectangle denotes the dark phase of the light 
cycle. The area between the purple dashed and solid black line represents the proportion of time 
males are receptive to pheromone, but females are not emitting pheromone (i.e. not receptive to 
mating).…………………………………………………………………………………………..64 
Figure 4.2 Catapult used to propel moths into the air at different temperatures to determine the 
lower temperature threshold for flight. Inset in upper left shows a moth ready to be launched…69 
Figure 4.3. Longevity of moths held at different temperatures. Survival of males and females 
were not significantly different so data from the sexes were pooled, and all data were log 
transformed before analysis. Columns headed with different letters are significantly different  
(P < 0.05).……………………………………………………………………………………………………………………80 
Figure 4.4. Flight behaviors exhibited by (a) female and (b) male P. viteana that were launched 
into the air at different temperatures. See text for descriptions of behaviors.……………………...81 
Figure 4.5. Average proportion of female and male P. viteana that exhibited full flight in the 
temperature range 10 to 19°C. The solid line indicates the line of best fit for pooled male and 
female data. The vertical dashed line shows the FT50 for all moths (pooled) is estimated to be 
15ºC.……………………………………………………………………………………………...82 

Figure 4.6 Oviposition at different temperatures in bioassay cages with (a) grapes suspended, or 
(b) attached to the floor of the cage. Columns with the same letter within each graph are not 
significantly different (P > 0.05). ……………………………………………………………….83 

Figure 4.7. Effect of temperature on mating frequency (a) and flight frequency (b) in colonies 
held at different temperatures. Data are the average number of behaviors observed per hour 
averaged over all sampling hours. Points with different letters are significantly different (P < 
0.05). Only one flight was observed in colonies at 10ºC so those data were excluded from the 
analysis………………...…………………………………………………………………………84 

 
 

 

xii 

Figure 4.8. Average time of the first observation of mating pairs (a) and male flights (b), and 
average time of last mating pair (c) and male flight (d) in colonies reared at different 
temperatures. Times of first and last behaviors were averaged over all days where at least 2 
behaviors were observed in the 24 h period from 12:00 on the first day of recording to 11:59 the 
following day. Male flight data from colonies reared at 10ºC were not included in the analysis 
because only one flight was observed across all samples. In each graph, columns with different 
letters are significantly different (P < 0.05)……………………………………………………...85 
Figure 4.9. Average duration of the mating period (a) and flight period (b). In each graph, 
columns with different letters are significantly different (P < 0.05). The flight period was 
significantly longer than the mating period for all temperatures except 15ºC (P < 0.05). See text 
for statistics. Male flight data from colonies reared at 10ºC were not included because only one 
flight was observed across all samples…………………………………………………………..86 
Figure 4.10 Proportions of male flights and mated pairs of P. viteana observed each hour in 
colonies held at constant temperatures under 17:7 L:D and 60-75% RH. The shaded rectangle 
covering the period from 2000 to 0300 hours on the x-axis indicates the scotophase. The 
proportion of male flights that occurred when mating was not observed is given in the bold 
numbers on the left hand side of each graph. Proportions with the same letter are not statistically 
different (Q0.05, ∞, 6 > 4.03, P < 0.05, arcsine transformed data, using multiple comparison of 
proportions (Zar 1999)). Data from colonies reared at 10°C (shown in red) were not used in this 
analysis because only one flight was observed in all samples.………………………..................88 

 Figure 4.11. Matings per hour (a) and male flights per hour (b) in Paralobesia viteana colonies 
reared under short (12h), moderate (14h), or long (17h) day lengths. Values labeled with 
different letters are significantly different (P < 0.05)………………………………………...….89 
Figure 4.12. Average time of the first observation of mating pairs (a) and male flights (b), of 
Paralobesia viteana and average time of last mating pair (c) and male flight (d) in colonies 
reared under 3 different day length treatments. Times of first and last behaviors in the 24 h 
period from 12:00 on the first day of recording to 11:59 the following day on all days the 
behavior was observed. All colonies were reared at 28°C. Columns with different letters are 
significantly different (P  < 0.05)……...…………………………………………………….…..90 
Figure 4.13. Mating period duration (a), and flight period duration (b) of Paralobesia viteana, in 
colonies reared under different day lengths. Averages are taken only where a given behavior was 
observed at least twice during the 24 hour period from 12:00 on the first day to 11:59 on the 
second day of recording. Columns labeled with different letters are significantly different  
(P < 0.0001).……………………………………………………………......................................91 
 

 

 

 

 

xiii 

Figure 4.14. Proportion of mated pairs and male flights of P. viteana observed each hour in 
colonies reared under different day length treatments at 28°C and 60 - 75% RH. Numbers in the 
plot area of each graph indicate the proportion of male flights that occurred when no mating pairs 
were detected. The shaded rectangles in each graph indicate the scotophase of the light: dark 
cycle. No significant differences in the proportion of male flights that occurred when mating was 
not observed were detected among day length treatments (Q 0.05, ∞, 3 < 3.31, P > 0.05, Multiple 
comparison of proportions, Zar 1999)..……………………………………………………….....94 

Figure 4.15 Mating frequency (a) and male flight frequency (b) of Paralobesia viteana recorded 
in colonies reared under three diurnal temperature regimes. Cool treatment colonies were reared 
in a temperature scheme that changed from 20°C during the day to 10°C at night. Day:night 
temperature cycles in the Warm and Hot treatment were 28°C:10°C and 28°C:18°C respectively. 
All treatments incorporated a 17:7 light: dark (day:night) cycle. “ns” denotes no significant 
differences were detected between treatments (P < 0.05)……………………………………......95 
 
Figure 4.16. Average time of the first observation of mating pairs (a) and male flights (b), and     
average time of last mating pair (c) and male flight (d) in colonies reared under 3 different 
diurnal temperature regimes. Treatments are the same as described in Figure 4.15. “ns” denotes 
no significant differences were detected between treatments (P >0.05).………….………….....96 
Figure 4.17. Mating period duration (a) and flight period duration (b), in colonies of P. viteana 
reared under different diurnal temperature regimes. Treatments are the same as described in 
Figure 4.16. “ns” denotes no significant differences were detected between treatments  
(P > 0.05).……………………………………………..................................................................97 
Figure 4.18 Proportion of mated pairs and male flights of P. viteana observed each hour in 
colonies reared under diurnal temperature treatments and constant day length 17:7 and 60 % RH. 
The shaded rectangle surrounding the time from 20:00 to 03:00 shows the scotophase. 
Proportions of male flights that occurred when mating was not observed are given in bold on the 
left hand side of the graphs. Proportions with the same letter are not statistically different 
(Q0.05, ∞, 3 > 3.31, P < 0.05, Multiple comparison of proportions, Zar 1999).………………….....99 
Figure 4.19 Total male moth captures of P. viteana for the entire season in traps loaded with 
different amounts of pheromone per lure. Data are averages from seven replicate vineyards in 
southwest Michigan. Columns labeled with different letters are significantly different  
(P  < 0.05).……...……………………………………………………………………...........….100 
Figure 4.20. Captures of male P. viteana in traps baited with lures containing different amounts 
of pheromone in different sampling periods. The legend gives the amount of pheromone per lure 
in µg. In any sampling period, columns with different letters are significantly different  
(P < 0.05). ………………………………………………...……………………………………101 
Figure 4.21 Relationship between captures of Paralobesia viteana and pheromone release for 
different sampling periods in 2017. Each point represents the average male capture and 
pheromone release for each lure load (15, 60, 75, 100, 125 µg/lure) at 7 southwest Michigan 
vineyards. Blank lures were not included in this analysis because they did not contain 
pheromone.……………………………………………………………………………………...104 

 

xiv 

Figure 4.22 Regression of P. viteana captures (a) and pheromone release (b) on accumulated 
heat units (GDD8.41). Residuals from (a) were regressed on the residuals in (b) to test the effect of 
pheromone release on captures with the effect of temperature removed (Table 4.8)…………..105 

 

xv 

CHAPTER 1 

PARALOBESIA VITEANA 

 

 

NATURAL HISTORY, ECONOMIC IMPORTANCE, AND VARIATION IN MONITORING 

Taxonomy and biology  

Nomenclature. The grape berry moth (GBM), Paralobesia viteana (Clemens) 

(Lepidoptera:Tortricidae), is a specialist herbivore found in woods and vineyards across Eastern 

North America (Johnson and Hammar 1912) that feeds primarily on wild and cultivated plants in 

the genus Vitis (Vitaceae). The original taxonomic determination was made in 1860 as Endopiza 

viteana Clemens. Prior to that it was considered to be the polyphagous fruit pest Lobesia botrana 

(Denis and Shiffermüller) known commonly as the European grape vine moth. It was determined 

that P. viteana  was a separate species after observations that it was reared only from grapes, and 

in addition, P. viteana larvae pupated on rolled leaves and not on grape shoots, trunks or canes as 

is known for L. botrana (Slingerland 1904). Over time P. viteana has been classified in different 

genera including Polychrosis, Lobesia, Endopiza and Paralobesia, all with the specific epithet 

viteana. In a review of the discrepancies in the nomenclature of the Tortricidae (Brown 2006), 

the disparities within this species were clarified and it is currently classified as Paralobesia 

viteana (Clemens).  

Hosts, habitat and distribution. Twelve species of wild grape (Vitis) occur in deciduous woods 

in Eastern North America (Galet 1979, Gilbert 2012) and these are thought to be ancestral hosts 

of P. viteana (Morano and Walker 1995). Wild grapes are common components of the woodland 

flora throughout North America, and are often found on the borders of wooded areas or in areas 

of disturbed habitat (Fergusson-Kolmes and Dennehy 1993, Morano and Walker 1995). In 

Michigan four species of Vitis occur naturally, Vitis riparia Michaux, V. aestivalis Michaux, V. 

labrusca L. and V. vulpina L., and of these species, V. riparia and V. aestivalis are the most 

 

1 

common in Michigan woodlands (Voss 1985, K. Mason personal observation). The presence of 

wild grapes is an important determinant of the large scale distribution of P. viteana, and records 

and reports of this insect from wild and cultivated sites range from Ontario to Texas and from the 

Rocky Mountains eastward to New England (Slingerland 1904, Johnson and Hammar 1912, 

Isley 1917, Pfeiffer et al. 1990). At the local scale, the abundance, distribution and risk of 

infestation of cultivated grapes is determined in large part by the density of wild grapes in the 

habitat adjacent to a vineyard (Hoffman and Dennehy 1989, Dennehy et al. 1990, Botero-Garcés 

and Isaacs 2003, 2004a, Jenkins and Isaacs 2007a).   

Life cycle and reproductive biology. Paralobesia viteana exhibits multiple generations in a 

year, depending on the location and length of the growing season, e.g., three and sometimes four 

generations in Michigan and other parts of the Great Lakes region (Tobin et al. 2003, Teixeira et 

al. 2009, 2011). In these regions, first generation adults typically emerge from overwintering 

pupae beginning in late April or early May. Mated females begin to lay eggs around dusk on 

warm nights in early to mid-June (Clark and Dennehy 1988, Teixeira et al. 2009, 2011). After 

larvae hatch, they feed on multiple adjacent flowers or young berries and produce webbing that 

encloses the feeding site (Johnson and Hammar 1912, Jenkins and Isaacs 2007b, Isaacs et al. 

2012b). Larvae of subsequent generations excavate a tunnel into the fruit, and also web together 

and feed on multiple berries. 

 

Upon maturation, a larva leaves the feeding site, moves onto a leaf and forms a 

hibernaculum by using its mandibles to cut a small semi-circle on the leaf and then folding it 

over its body and sealing the edges with salivary silk. The larva then spins a cocoon in this parcel 

and pupates (Johnson and Hammar 1912, Taschenberg 1951). Eggs that are laid in the late 

summer and fall are increasingly likely to enter diapause, and eggs and young larvae that are 

exposed to day lengths shorter than 14 h (Nagarkatti et al. 2001, Tobin et al. 2002) will 

 

2 

overwinter as pupae on leaves. These leaves drop from the vine in late fall and may remain in the 

litter on the vineyard floor or be blown by wind into adjacent habitats (Johnson and Hammar 

1912, Isley 1917, Taschenberg 1951, Botero-Garcés and Isaacs 2003, Matlock et al. 2016). 

These pupae then emerge the following spring to resume the cycle. 

 

Economic importance 

The economic impact of the first generation is minimal, but larvae of later generations can cause 

significant economic losses due to reduced fruit yield, lowered fruit quality, or rejection of 

contaminated fruit by fruit processors (Hoffman et al. 1992, Teixeira et al. 2009, Roubos et al. 

2013). Paralobesia viteana infestation is higher in vineyards adjacent to deciduous woods that 

contain wild grape (Hoffman and Dennehy 1989, Botero-Garcés and Isaacs 2003, 2004a, Jenkins 

and Isaacs 2007a) with grape berry moth infestation consistently higher at wooded edges 

compared to the vineyard interior (Hoffman and Dennehy 1989, Trimble 1993, Botero-Garcés 

and Isaacs 2003, Mason et al. 2016). Left unmanaged, grape berry moth can infest 100% of 

clusters on vineyard borders by harvest, and larval contamination of the harvested fruit can lead 

to rejection of the crop by processors or wine makers. Larval feeding can also reducing cluster 

weight and increase susceptibility to fungal infections. Larval feeding by P. viteana is similar to 

that of the closely related European species, Lobesia botrana (Denis & Schiffermüller) that also 

affects yield and quality by increasing susceptibility to bacterial and fungal infections (Fermaud 

and Le Menn 1992, Mondy et al. 1998, Ioriatti et al. 2011). Because of the risks of direct yield 

loss, larval contamination of fruit and reduced quality due to pathogens, P. viteana is the target 

of the majority of insecticides used in vineyards east of the Rocky Mountains (Hoffman et al. 

1992, Teixeira et al. 2009). 

 

 

 

3 

 

Paralobesia viteana was first noted as a pest soon after the start of commercial grape 

production in the Midwestern and Northeastern United States, when in 1869 yield losses of up to 

50% of the crop were reported in Ohio, Missouri and Illinois (Johnson and Hammar 1912). It 

was noted that P. viteana infestation was not uniform at local or regional scales, and high levels 

of infestation were found only in a small number of vineyards, especially in Pennsylvania and 

New York (Isley 1917). In Michigan it was reported that this insect was found in many vineyards 

in Van Buren County, but there were few cases where P. viteana caused losses of economic 

significance (Isley 1917). It was not until 1922 that the first widespread P. viteana infestations 

were reported in Michigan, but the actual loss was not quantified in economic terms (Pettit 

1922). By 1932 P. viteana was considered a “serious enemy of Michigan grapes” (Pettit 1932). 

 

History of P. viteana management 

Early measures used for P. viteana management were dominated by cultural controls to bury or 

damage the overwintering pupae by tilling, and mounding or hilling soil onto the vine trunk 

(Johnson and Hammar 1912, Isley 1917, Pettit 1932). The advent of chemical controls for 

agriculture began in the late 19th and early 20th century, and inorganic compounds containing 

toxic heavy metals such as lead arsenate and Paris green (copper acetoarsenite) added to either 

water or Bordeaux mixture (Clark 1902), proved to be very effective at controlling this pest 

(Johnson and Hammar 1912, Isley 1917). Starting in the immediate post-World War II era and 

continuing through the 1950s and early 1960s, highly toxic chlorinated hydrocarbon insecticides, 

including dichloro-diphenyl-trichloroethane (DDT), dieldrin and thiodan were used to control P. 

viteana and other pests. Later and into the 1980s organophosphates, such as azinphos-methyl and 

methyl parathion saw widespread use for pest control in grapes (Taschenberg 1948, 1950, 

Taschenberg and Avens 1960, Taschenberg et al. 1964, Dennehy et al. 1990). These compounds 

 

4 

were all part of the “Green Revolution” in which synthetic pesticides and fertilizers were seen as 

the solution to world hunger. During this period many cost-effective tools were developed, and 

global food production was increased greatly. However, high chemical inputs into some 

agricultural systems produced unforeseen adverse environmental consequences, such as surface 

water contamination, detrimental effects on non-target species and the development of pesticide 

resistance (Henny 1972, Devonshire and Moores 1982, Brattsten et al. 1986). The insecticides of 

this era typically had a broad spectrum of activity, and because they were contact poisons with 

high volatility and long residual activity, could be applied without precise timing either 

prophylactically, or as a “rescue” or “clean up” application after P. viteana infestation was 

established. Additionally these chemicals were deemed less hazardous and more economical than 

previous options such as lead arsenate, or Paris green, and this led to the overuse of insecticides 

for control of P. viteana and other pests (Pimentel 2012). As these compounds were lipophilic 

molecules, they were prone to bio-accumulate in sediments and then in fatty tissues in organisms 

at low trophic levels. These substances then bio-magnified upward into higher trophic levels 

resulting in widespread environmental effects including population reductions in fish, 

amphibians and birds of prey (Henny 1972). 

The rise of IPM. The declines across many taxa that were linked to the overuse of pesticides 

were brought into public view in the seminal work, Silent Spring, (Carson 1962). In addition to 

the ensuing public backlash against existing agricultural practices that was incited by Carson 

(1962), multiple cases of insecticide resistance were linked to the indiscriminate and repeated use 

of some of these compounds (Devonshire and Moores 1982, Brattsten et al. 1986, Nagarkatti et 

al. 2002b). These led to the development of new insecticides including novel chemistries that 

were designed to be used in rotation to limit the buildup of insecticide resistance. However many 

of these chemicals had similar environmental and worker/consumer safety concerns as the 

 

5 

chlorinated hydrocarbons. This led to the eventual passage of the Food Quality Protection Act 

(FQPA) (Anon 1996), that mandated the review and ultimate restriction of several 

organophosphate and carbamate insecticides, not only in grapes, but in all food crops. 

 

The decade following Silent Spring (Carson 1962) also saw the development and 

adoption of many new tools and strategies to control P. viteana and other pests. These tactics 

taken as a whole became known as integrated pest management (IPM) (Figure 1.1, from 

Fleischer et al., 2014). The components of IPM include: efforts to better understand pest biology 

and ecology to improve control tactics; implementation of methods for monitoring pest 

abundance and phenology; derivation of economic and action thresholds to determine if and 

when to apply pesticides; advancement of 

weather-based models to predict disease 

and insect pest development; formulation 

and use of novel chemistries that are 

selective for a narrow range of organisms 

with reduced risks to the environment and 

the health of agricultural workers and 

consumers; and the promotion of 

Figure 1.1. Pyramid of IPM tactics 

sustainable pest management approaches such as cultural and biological control  (DeBach and 

Rosen 1991, Dent 2000, Jenkins and Isaacs 2007a, 2007b) (Figure 1.1). All of these control 

methods have seen some adoption in P. viteana management programs, however control of this 

insect remains dominated by the use of synthetic insecticides (Isaacs et al. 2012b). 

 

 

 

 

6 

Monitoring 

Thresholds. Pest monitoring is an important component of IPM. Information gathered from 

regular visual sampling and the use of passive or baited traps can be used to determine when 

susceptible stages of a pest are present, and if pests are in high enough abundance to warrant 

control (Binns and Nyrop 1992, Knight and Light 2005a, Roubos et al. 2013). This is done by 

comparing the cost of applying a given treatment to the dollar value that the crop would lose if it 

was left untreated (economic threshold). In general, if the cost of treatment is less than the 

potential loss of crop value, then the treatment should be used. In practice the treatment is 

applied when the action threshold is reached. This is a level of pest damage or abundance that 

triggers treatments to be applied to maintain pest abundance below the economic threshold. 

Monitoring can also be used to develop predictive models that estimate when a pest is likely to 

reach the action threshold (Binns and Nyrop 1992, Knight and Light 2005a).  

The MSU Enviroweather model. In the case of P. viteana, multiple years of scouting to 

determine when eggs and larval damage were present in clusters were used to create a model 

posted on Michigan State University’s Agricultural weather online service, MSU Enviroweather 

(Isaacs 2017). This model predicts when oviposition will begin in different areas of the state 

based on the accumulation of growing degree days (base temperature 8.41ºC) after bloom of wild 

grape (V. riparia) at multiple remote weather stations in regions of grape production. This model 

has helped improve P. viteana management in Michigan using reduced-risk insecticides, such as 

the ecdysone agonist methoxyfenozide and the anthranilic diamide chlorantraniliprole. These 

compounds need to be ingested by the target insect, so they need to be applied to grapes at the 

start of the ovipositional period to be most effective (Isaacs et al. 2005, Jenkins and Isaacs 

2007b, Teixeira et al. 2009, 2011, Mason et al. 2016).  

 

 

7 

The importance of pheromones in monitoring. Traps baited with sex pheromone are often 

used to monitor specific insects, and hundreds of insect sex pheromones have been identified 

(Arn et al. 1992, El-Sayed et al. 2009). The sex pheromones of several economically important 

tortricid fruit pests have been synthesized and are available commercially for use in traps to 

monitor males of specific species (Baker 2009, Witzgall et al. 2010). Most of these pheromones 

are either single hydrocarbon compounds with 9 to 16 carbon atoms, one or two double bonds 

and a single functional group; or they are blends of two or three such compounds (Arn et al. 

1992, El-Sayed et al. 2009). Males of a given species are sensitive to not only the specific ratios 

of different pheromone components, but typically they only respond to sex pheromone when it is 

present in a range of acceptable concentrations (Roelofs and Comeau 1969, Arn et al. 1992, Linn 

and Roelofs 1995, El-Sayed et al. 2009).  

The sex pheromone of P. viteana. The female sex pheromone of P. viteana is a mixture of a 

two monounsaturated acetates. The major component in this standard blend is (Z)-9-dodecenyl 

acetate (Roelofs et al. 1971), and the minor constituent is (Z)-11-tetradecenyl acetate. This  

blend is attractive to males in compositions from 20:1 to 5:1 (Witzgall et al. 2000), but the major 

component alone is also effective at attracting males (Roelofs et al. 1971, Witzgall et al. 2000). 

 

Lures loaded with 100µg of the two-component blend of this pheromone are available for 

monitoring traps in the integrated management of this pest (Botero-Garcés and Isaacs 2003, 

Isaacs et al. 2012b, Jordan et al. 2013).  However the consistency of male captures can vary 

greatly with time of year (Taschenberg et al. 1974, Taschenberg and Roelofs 1977, Hoffman et 

al. 1992, Mason and Isaacs 2018), lure manufacturer (Jordan et al. 2013), location in the  

vineyard, or in relation to adjacent habitat (Hoffman and Dennehy 1989, Botero-Garcés and 

Isaacs 2003, 2004a). Exploring the factors that affect male captures of this species are important 

to inform decision-making regarding the need for treatment, and may allow for the development 

 

8 

Figure 1.2 Geographic variation in the response of P. viteana males to 
pheromone-baited traps and incidence of grape berry moth feeding damage at 
representative vineyards in the major grape growing regions of Michigan in 
2015. Note difference in Y-axes between graphs. Blue solid line indicates male 
moth capture and orange dashed line denotes P. viteana damaged clusters. 

of lures or trapping strategies that improve moth monitoring, potentially improving timing of 

insecticide applications or other management strategies. 

 

Geographic variation in sex pheromones 

Variation between P. viteana populations.  In the previous decade, variation in male response 

to P. viteana sex pheromone baited traps has been observed during routine scouting during 2015 

in different regions of Michigan (Mason unpublished - Figure 1.2). In Northwest Michigan, 

standard pheromone traps capture very few male moths during the growing season, yet 

 

9 

infestation is found in some vineyards at harvest. These observations raises the possibility that 

Northern and Southern Michigan populations of this pest may have diverged physiologically or 

behaviorally, leading to the observed differential responses of males to the standard pheromone 

blend. Variation in P. viteana male captures between Michigan grape growing regions is yet to 

be reported in the literature. 

Regional variation in other species. There are several examples of variation in composition of 

the pheromone released by females and in the male response between geographically separated 

populations of several species of lepidopteran pests. In the turnip moth Agrotis segetum (Denis 

and Schiffermüller), the relative proportions of the three pheromone components varies among 

European populations, and the relative abundance of sensillae on male antennae that are sensitive 

to these blends also varies between geographic areas (Hansson et al. 1986, Löfstedt et al. 1986). 

Pheromone trapping of A. segetum across Eurasia and Africa has shown that populations north of 

the Sahara desert have distinctly different pheromone composition to populations south of the 

Sahara, and males from these regions respond preferentially to the pheromone blend of females 

from the same region (Tòth et al. 1992). In field tests using pheromone blends from Japanese, 

Indian and Philippine populations of the rice leaffolder, Cnaphalocrocis medinalis Guenée, 

Kawazu et al.(2009) showed male C. medinalis from Balinese and Javanese populations were 

attracted to the Japanese blend, but were not attracted to the Indian or Philippine blends. While 

researching geographic variation in male captures of two tortricid pest species, Planotortrix 

excessana Walker and Ctenopseutis obilquana, Walker in New Zealand, Foster et al. (1986) 

showed that sibling species in each of these pests had become reproductively isolated, and 

sibling species had slightly different pheromone blends. In the obliquebaded leafroller, 

Christoneura rosaceana (Harris) male response to sex pheromone is stronger when males and 

females are from the same geographic regions in North America (El-Sayed et al. 2003, Stelinski 

 

10 

et al. 2007b). These studies and subsequent research led to the development of eastern and 

western pheromone lure blends that are used for this species in those respective regions of North 

America (El-Sayed et al. 2003, Stelinski et al. 2007b).  

One objective of this dissertation was to explore the factors that may be involved in the 

differences in P. viteana male captures that have been observed between northern and southern 

growing regions in Michigan. Behavioral tests in the lab and the field were used to compare male 

responses to different pheromone sources to determine if males from different regions of 

Michigan respond similarly to a standard pheromone blend. This study also tested whether males 

from northern and southern regions respond preferentially to females from the same region. 

 

Seasonal variation in male captures  

The paradox between moth captures and infestation. Paralobesia viteana pheromone lures 

are available commercially, however in Southwestern Michigan males of this species are only 

captured consistently during the first generation that is active around bloom. This generation 

causes little larval feeding damage, but during the second and third generations that occur in the 

early and late summer, respectively, the level of oviposition on berries, and subsequent larval 

infestations increase greatly, yet few males are caught in monitoring traps (Figure 1.3) (Snyder et 

al. 1992, Teixeira et al. 2009, Isaacs et al. 2012b, Mason and Isaacs 2018). This incongruence 

between male moth captures and larval infestation prevents development of action thresholds 

based on captures in pheromone traps as has been done for other lepidopteran fruit pests (Binns 

and Nyrop 1992, Bradley et al. 1998, Reddy and Manjunatha 2000, Knight and Light 2005a). 

The temporal variation in P. viteana male response to traps is concurrent with substantial 

changes that occur in the grapevine during seasonal growth. One hypothesis is that the observed  

 

 

11 

Figure 1.3. Phenology of P. viteana in southwest Michigan. Captures of males (gray solid line) 
are highest during the first generation, when berry infestation (green dashed line) is lowest. In 
the second and third generations, male capture is lower, but infestation increases until harvest. 
Data are averages from eight commercial vineyards during 2015.Temperatures at the top of the 
figure are the range of average daily temperatures for each generation in 2015. 

 
differences in male captures are related to the phenology of the host plant. The underlying 

chemical and structural changes in the grapevine may affect the behavior of P. viteana such that 

the number of males that are caught in pheromone traps is reduced as the season progresses. 

Plant volatiles as insect attractants. Volatile host plant chemicals can influence host-finding in 

some key crop pests (Bruce et al. 2005, Leskey et al. 2008, Piñero and Dorn 2009, Saveer et al. 

2012). Most previous studies in this area have focused on the behavior of females, but either sex 

can respond to host plant volatiles in the laboratory or field (Stelinski et al. 2003, Knight and 

Light 2005b, Faraone et al. 2013). Within species, odorant receptors and neural pathways are 

also similar between sexes (Jordan et al. 2009, Varela et al. 2011). Female codling moths, Cydia 

pomonella L., are attracted to apple odors, and in laboratory studies show increased oviposition 

and flight response compared to an odorless control (Wearing et al. 1973, Yan et al. 1999, 

 

12 

Coracini et al. 2004). In addition, C. pomonella males are attracted to compounds derived from 

pear, and these can be used in monitoring traps resulting in higher captures than with pheromone 

alone (Light et al. 2001, Knight et al. 2005, Il’ichev et al. 2009). 

In the oriental fruit moth, Grapholita molesta (Busck), females are attracted to a combination of 

green leaf volatiles and other aromatic compounds that are derived from peach shoots (Piñero 

and Dorn 2007). In addition, male and female G. molesta are attracted to monitoring traps baited 

with volatiles derived from peach and pear (Lu et al. 2012). Female European grapevine moth  

(L. botrana), consistently flew upwind and landed on unripe grape clusters in wind tunnel tests 

(Tasin et al. 2006). In subsequent studies, L. botrana females were also attracted to a four-

component blend of volatile compounds collected from the headspace around confined grapes 

clusters, and females were attracted to synthetic grape volatiles in field studies (Tasin et al. 

2009). 

In similar studies, P. viteana females oriented toward grapevine components in wind 

tunnel tests, and this response was stronger for leaves and shoots than for flowers, unripe berries 

or mature fruit (Cha et al. 2008a). Male P. viteana were also attracted to a blend of grape shoot 

volatiles in the wind tunnel and in field tests (Cha et al. 2008b, Loeb et al. 2011). These latter 

studies show that grape shoot volatiles are important and attractive cues for both male and 

female P. viteana, and they also suggest that the volatile-rich grape canopy may influence the 

interaction between male P. viteana and monitoring traps.  

Do grape clusters influence male captures? The size and chemical composition of grape 

clusters and the vine canopy change considerably during seasonal growth and development 

(Hrazdina et al. 1984, Mullins et al.1992, Schultz 1995). Early in the season, few leaves and 

small flower or berry clusters are present on vines. As the growing season proceeds, the clusters 

increase in weight 100 fold, and as the berries soften and become ripe, physiological changes 

 

13 

lead to increased soluble solids, lower organic acids (e.g. tartaric, malic and citric), and, 

depending on grape variety, an increase in pH to a final value between 2.8 and 3.7 at harvest 

(Hrazdina et al. 1984, Jackson and Lombard 1993). The concurrent increase in phenolic 

compounds, such as flavonoids and anthocyanins, can impart distinctive odors and flavors to 

ripening grape clusters (Singleton and Trousdale 1983), and volatile terpenes that increase 

greatly after veraison (fruit coloring) also change the aroma and flavor characteristics of grapes 

(Dimitriadis and Williams 1984, Rosillo et al. 1999). These physiological transformations 

contribute to an odor landscape that varies consistently through the growing season, and these 

changing host plant cues may provide information that P. viteana could use to orient to its host 

plant, and find potential mates and oviposition sites. If P. viteana mating occurs on the grape 

clusters, or if females spend the majority of their time on clusters, males would have an increased 

chance of finding females, and mating successfully, if they can detect and orient toward the 

volatiles produced by grape clusters. This could lead to a “competition” between clusters and 

traps that might lead to a reduction in the number of male captures in traps. In addition the 

combination of grape volatiles and sex pheromone may be more attractive to male P. viteana 

than sex pheromone alone, as has been shown for C. pomonella (Light et al. 2001). This 

preference could result in reduced P. viteana male captures in pheromone traps because the 

amount of grape cluster volatiles increases during the season due to the increase in cluster size 

and the ripening of the crop. 

Does the grape canopy reduce male captures? In addition to changes that occur as clusters 

develop, the physical structure of the juice grapevine canopy is also transformed through each 

season. In varieties that are bred and managed to maximize crop yield, such as juice grapes (V. 

labrusca, cvs. Concord and Niagara), the vines are typically cane-pruned and trained to a single 

wire top-cordon system. The resulting trailing habit of shoot growth causes the canopy to 

 

14 

become increasingly dense, and it creates a thick matrix of shoots and leaves as the season 

progresses (Smart et al. 1982a, Miller and Howell 1998, Dry 2000, Bates 2008). The quantity 

and quality of grape shoot and leaf volatiles that are present in a vineyard change as the canopy 

grows and becomes more dense (Tasin et al. 2006). The dense canopy imposes challenges on 

disease and insect management by forming an impediment to air flow and reducing spray 

coverage (Wise et al. 2010). The increase in canopy density may also affect monitoring P. 

viteana with pheromone traps by altering trap findability (Miller et al. 2006), making it less 

likely that male moths find traps. The canopy could physically block males from reaching traps, 

it may disrupt the structure of the pheromone plumes from lures, or the naturally occurring grape 

shoot volatiles may draw moths away from traps.  

 

Temperature and photoperiod effects on P. viteana  

Relationships between male captures, temperature and photoperiod. In temperate regions, 

there are consistent patterns of variation in temperature and photoperiod over a growing season, 

and these correspond to the observed phenology of P. viteana (Figure 1.3). Typically in 

Michigan, the spring is cool with average daily temperatures around 10-15ºC, and the 

photoperiod increases from ~13 to 15 hours. Over this time P. viteana male captures are high and 

cluster infestation is low (Figure 1.3). The highest average daily temperatures (20 to 23ºC) occur 

in the middle to late summer and the longest day lengths (14.5 to 15.5 hours) also occur during 

this period. P. viteana male captures are typically at the lowest for the season, and in contrast 

cluster infestations begin to sharply increase (Figure 1.3). In the late summer and early fall 

cluster infestation is usually at its highest point and male captures increase, but remain much 

lower than in the spring (Figure 1.3). Average daily temperatures range from 17 to 21ºC and are 

 

15 

intermediate to those of spring and summer, and the photoperiod decreases during this time from 

about 14.5 to 12.5 hours (Table 4.1).  

Temperature and insect physiology. Most insects are ectothermic, and consequently many 

aspects of insect physiology, development, behavior and reproduction are dependent on ambient 

temperature (Ratte 1985, Honek 1996, Frazier et al. 2006). For a diverse group of insects, the 

rate of enzymatic processes involved in physiological functions such as metabolism, hormone 

production, and digestion approximately doubles for each 10°C increase in ambient temperature 

(Rao and Bullock 1954, Ratte 1985). The range of temperatures where this Q10 doubling occurs 

is limited to temperatures between a critical minimum and a critical maximum, and although this 

differs somewhat between species and climatic regions, this temperature range is typically close 

to 10 to 30°C for species living in temperate zones (Nielsen et al. 1999, Nespolo 2003). 

Longevity. The effect of temperature on adult longevity has been studied in several insect 

orders, and across all taxa, longevity decreases with increasing temperature (Graham et al. 1967, 

Emana 2007, Gómez et al. 2009). In field tests, Asaro and Berisford (2001) showed males of the 

first generation of the Nantucket pine tip moth, Rhyacionia frustrana (Comstock) lived 

significantly longer than males in the second and third generations. The authors also 

demonstrated in the lab that there is a significant reduction of longevity with increasing constant 

temperature. Longevity of codling moth, Cydia pomonella (L.) in northern European populations 

was shorter for males and females held in a warm temperature regime (18°C day and 15°C night) 

compared to those in a cool temperature scheme (13°C day and 10°C night) (Sæthre and 

Hofsvang 2002).  

 

 

 

 

16 

Activity and movement 

The frequency and intensity of insect movement and activity are also dependent on temperature. 

Between critical minimum and maximum temperatures, thermal performance, measured as 

cricket (Acheta domesticus L.) running speed and jumping distance, increases with temperature 

(Lachenicht et al. 2010). Similarly, locomotor activity of the tenebrionid, Gonocephalum simplex 

(Fabricius) increases with temperature up to a critical maximum temperature, and then activity 

decreases rapidly as the insect succumbs to heat stress (Klok et al. 2004).  

Effects on flight. Insect flight shows a similar response to temperature, occurring above a 

critical minimum and decreasing at temperatures at and above a critical maximum. In early 

studies, Taylor (1963) found the minimum temperature for flight to be 15.5°C for Vespula 

germanica (L.) queens, 17.5°C for alates of the bean aphid Aphis fabae (Scopoli) and 16.5°C for 

the soldier beetle Rhagonycha fulva (Scopoli). However, (Taylor 1963) also found the minimum 

temperature for flight for the large bodied noctuids (~30-40mm wing span) Agrochola lychnidis 

(Denis & Schiffermüller) and Amphipyra tragopoginis (Clerck) to be considerably lower at 9 and 

10.5°C, respectively. For smaller moths such as the tortricids (wing spans ~10-20mm) the critical 

minimum temperatures for flight are in the range of 12-15°C. For example the minimum 

temperature for flight in the eastern spruce bud worm, Choristoneura fumiferana (Clemens) is 

14°C (Greenbank et al. 1980) and for oriental fruit moth Grapholita molesta (Busck), that 

temperature was 15°C (Rothschild and Minks 1974). Codling moth minimum flight temperature 

was found to be 12.7°C (Batiste et al. 1973), and for the light brown apple moth, Epiphysis 

postvittana (Walker) the minimum temperature for flight ranged from 8 to 11°C 

(Danthanarayana 1976).  

 

 

17 

The critical maximum temperature for flight has been quantified less often, but for 

codling moth the maximum was found to be 26.7°C (Batiste et al. 1973), and for the light brown 

apple moth, the maximum temperatures for flight ranged from 27 to 28°C (Danthanarayana 

1976). 

Oviposition and temperature. Oviposition is also highly dependent on temperature. In pink 

bollworm, oviposition increases 10-fold between females held at 15.5°C and those reared at 

18.3°C. Over the range from 18.3 to 26.7°C oviposition was similar. At 32°C oviposition 

decreases by about half and at temperatures of 37.8°C and above oviposition is reduced a further 

100-fold (Graham et al. 1967). Sæthre and Hofsvang (2002) showed northern European 

populations of codling moth begin to lay eggs at temperatures as low as 12.3°C, and the amount 

of oviposition increases steadily through a range of temperatures ending at 25°C (the highest 

temperature measured). Oriental fruit moth oviposition is highest from 22 to 30°C, and drops off 

rapidly at 33°C, while no egg-laying is observed at 35°C (Notter-Hausmann and Dorn 2010). 

 

Effects of temperature and photoperiod on activity cycles.  

The influence of temperature and photoperiod on daily and seasonal cycles of growth, 

development, activity, and reproduction have been studied in several insect families (Tauber and 

Tauber 1981, Beck 1983, Régnière et al. 2012, Tonnang et al. 2017). Moths in the family 

Tortricidae have been the subjects of much of this work owing to the status of some members of 

this family as economically important fruit pests.  

Temperature and activity. In moth species where mating occurs at the beginning of the 

scotophase (dark phase), females emit pheromone (call) earlier in the day at lower temperatures. 

At higher temperatures, the female calling period is generally shorter, and occurs in the 

scotophase (Cardé et al. 1975b, Baker and Cardé 1979a, Delisle and McNeil 1987, Webster 

 

18 

1988). Male responsiveness to pheromone also occurs earlier in cool temperatures (Cardé et al. 

1975a, b) Thus for some species the current air temperature, or changes in temperature dictate 

when mating behaviors will occur. In other species, ambient temperature in the period 

immediately before the scotophase determine the periods of female calling and male 

responsiveness (Baker and Cardé 1979a, Haynes and Birch 1986, Delisle and McNeil 1987).  

Photoperiod and activity. Day length can also be an important cue for determining seasonal or 

daily patterns of activity (Delisle and McNeil 1987). For example decreasing day length in the 

autumn can trigger physiological changes that can alter insect development and lead to diapause 

(Riedl and Croft 1978, Gangavalli and Aliniazee 1985, Nagarkatti et al. 2001, Saunders 2001). 

Photoperiod can influence mating behavior, although relatively few studies have examined the 

effect of day length on mating, and the effect varies across species and sexes. As day length 

decreases, the female calling period is lengthened (Kanno 1981, Gerber and Howlader 1987), but 

decreasing day length in the late summer and fall reduce male responsiveness to sex pheromone 

(Delisle and McNeil 1986, 1987, Mulder et al. 1989). In cases where there is an effect of 

photoperiod on either male or female mating behavior, the effect is typically minor compared to 

the effect of temperature (McNeil 1991).  

Identification of the patterns of daily mating activity can inform other management 

approaches such as mating disruption, mass trapping and attract and kill (McNeil 1991, El-Sayed 

and Suckling 2005, El-Sayed et al. 2006, 2009, Baker 2009, Rodriguez-Saona and Stelinski 

2009). For example, in mating disruption of some tortricid pests, automated pheromone 

dispensers can be programmed to emit pheromone only during the period when females are 

calling, and this could reduce the costs of deploying mating disruption (Isaacs et al. 1999, 

Fadamiro and Baker 2002, Stelinski et al. 2007a, Jones and Wiman 2012).  

 

19 

Pheromone release and temperature. In developing sex pheromone lures for monitoring, the 

optimal amount of pheromone to use in a lure is often determined by comparing male captures in 

traps that contain a range of concentrations of an active compound (Roelofs et al. 1969, 1971, 

Witzgall et al. 2000, Suckling et al. 2005). Traps with too low of a pheromone concentration will 

not be attractive to males and lower captures will result (Roelofs et al. 1971, Taschenberg et al. 

1974, Linn and Roelofs 1995). Adding more pheromone can increase the longevity of activity, 

but traps that have a higher than optimal concentration of pheromone can repel male moths, 

resulting in reduced catch compared to lower concentrations (Linn and Roelofs 1995, Witzgall et 

al. 2000, Suckling et al. 2005).  The rate of pheromone release from lures increases with 

increasing temperature (McDonough et al. 1989), and the increase of pheromone release at high 

temperatures may suppress male catch in periods of hot weather (Sanders 1981, Cork et al. 2003, 

Cork 2016, Cardé et al. 2018).  

The effect of temperature and photoperiod on the phenology and behavior of P. viteana 

were investigated to determine when mating activity and reproductive behaviors occur during the 

growing season. This is an essential component of integrated management of tortricid pests 

(Riedl et al. 1976, Damos and Savopoulou-Soultani 2010, Jones and Wiman 2012), yet little is 

known about the role of temperature and day length in regulating P. viteana mating activity or 

periodicity, and less is known about how temperature affects male response to sex pheromone 

traps.  

 

 

20 

Research goals  

Some of the primary challenges of P. viteana management are due to the limited understanding 

of the factors that affect chemical communication between the sexes in this pest, and how these 

factors in turn govern mating and reproductive behaviors. This dissertation explored the variation 

in male P. viteana response to sex pheromone between geographic regions and over the course of 

a growing season. The results of this work help to explain some of the inconsistencies inherent in 

monitoring this important pest and how these factors interact to produce the observed phenology 

of P. viteana.  

The specific goals of this research were to:  

1) Determine the cause of low male captures in standard pheromone traps in northwest Michigan 

vineyards where P. viteana infestations occur. 

2) Determine whether the seasonal changes in the grape canopy or cluster development influence 

male captures to produce the observed phenology of P. viteana. 

3) Characterize the role of temperature and photoperiod in daily and seasonal patterns of P. 

viteana reproduction. 

4) Improve understanding of how temperature can influence the biology of P. viteana and affect 

the function of pheromone traps, and how this ultimately produces the observed phenology.   

 

 

21 

CHAPTER 2 

 

INTRODUCTION 

 

 

LOW CAPTURES OF MALE PARALOBESIA VITEANA IN MONITORING TRAPS ARE 
NOT DUE TO GEOGRAPHIC VARIATION IN MALE RESPONSE TO PHEROMONES 

Insect species with distributions that cover large geographic ranges often show variation in traits 

such as body size, physiology, coloration, or behavior among subpopulations that reside along 

that range (Futuyma and Moreno 1988, Hill et al. 1999, Goropashnaya et al. 2001, Eckert et al. 

2008, Cruz-Esteban et al. 2017). Widespread planting of crops has helped to artificially increase 

the range of many pest insects, such as Colorado potato beetle, Leptinotarsa decemlineata (Hare 

1990), fall armyworm, Spodotera frugiperda (Takahashi et al. 2012, Dávila et al. 2013, Chen et 

al. 2015), and tephritid fruit flies (Yee and Goughnour 2008, Hood et al. 2013). Pest populations 

can diverge so much across the host plant range that the phenotypic or genetic differences 

between geographically separated populations lead to the formation of races, subspecies or 

distinct species (Foster et al. 1986, Roderick 1996). These populations can show considerable 

variation in physical and behavioral characters, even though the sub-groups remain 

reproductively compatible (Hsiao 1978, Ramaswamy et al. 1988, Goropashnaya et al. 2001; 

Cruz-Esteban et al. 2017).   

 

There are many examples of variation in the composition of the pheromone released by 

females and in the male response between geographically separated populations of several 

species of lepidopteran pests. In the turnip moth Agrotis segetum (Denis and Schiffermüller), the 

relative proportions of the three pheromone components varies among European populations, 

and the relative abundance of sensillae on male antennae that are sensitive to these blends also 

varies between geographic areas (Hansson et al. 1986, Löfstedt et al. 1986). Pheromone trapping 

of A. segetum across Eurasia and Africa has shown that populations north of the Sahara desert 

 

22 

have distinctly different pheromone composition to populations south of the Sahara, and males 

from these regions respond preferentially to the pheromone blend of females from the same 

region (Tòth et al. 1992). In field tests using pheromone blends from Japanese, Indian and 

Philippine populations of the rice leaffolder, Cnaphalocrocis medinalis Guenée, Kawazu et al. 

(2009) showed male C. medinalis from Balinese and Javanese populations were attracted to the 

Japanese blend, but were not attracted to the Indian or Philippine blends. While researching 

geographic variation in male captures of two tortricid pest species, Planotortrix excessana and 

Ctenopseutis obilquana, in New Zealand, Foster et al. (1986) showed that sibling species in each 

of these pests had become reproductively isolated, and sibling species had slightly different 

pheromone blends. In the obliquebanded leafroller, Christoneura rosaceana (Harris), male 

response to sex pheromone is stronger when males and females are from the same geographic 

regions in North America (El-Sayed et al. 2003, Stelinski et al. 2007b). These studies and 

subsequent research has led to the development of eastern and western pheromone lure blends 

that are used for this species in those respective regions of North America.  

 

The female sex pheromone of Paralobesia viteana (Clemens) is a mixture of two 

monounsaturated acetates, with a major component of (Z)-9-dodecenyl acetate, and a minor 

constituent, (Z)-11-tetradecenyl acetate. This blend is attractive to males in compositions from 

20:1 to 5:1 (Witzgall et al. 2000), but the major component alone is also effective at attracting 

males (Roelofs et al. 1971, Witzgall et al. 2000). Lures loaded with 100 µg of this pheromone are 

available for monitoring traps in the integrated management of this pest (Botero-Garcés and 

Isaacs 2003, Isaacs et al. 2012a, Jordan et al. 2013).  The consistency of male captures can vary 

with time of year (Taschenberg et al. 1974, Taschenberg and Roelofs 1977, Hoffman et al. 1992, 

Mason and Isaacs 2018), lure manufacturer (Jordan et al. 2013), location in the vineyard, or in 

relation to adjacent habitat (Hoffman and Dennehy 1989, Botero-Garcés and Isaacs 2003, 

 

23 

2004a). However, variation in P. viteana male captures between growing regions has not been 

previously documented. 

 

Variation in the response of males to P. viteana sex pheromone baited traps has been 

observed during routine scouting between different regions of Michigan (see Chapter 1, Figure 

1.2). In Northwest Michigan, standard pheromone traps capture very few male moths during the 

growing season, yet infestation is found in some vineyards at harvest. These observations 

suggest that Northern and Southern Michigan populations of this pest may have diverged 

physiologically or behaviorally, leading to the observed differential responses of males to the 

standard pheromone blend. 

 

Developing monitoring programs that consider the regional differences in male response 

to pheromone traps and allow accurate detection and monitoring of Northern Michigan 

populations would greatly improve management of this important pest. This study tested the 

hypothesis that the observed difference in the number of males captured in pheromone traps in 

Northwest and Southwest Michigan is due to differences between regions in male response to the 

standard pheromone. I posed two questions to test this hypothesis: 

1) Do male P. viteana from Northwest and Southwest Michigan respond differently to a 

standard pheromone blend?  

2) Do male P. viteana from Northwest and Southwest Michigan respond differently to 

females from these two regions?  

 

24 

 

Study insects 

METHODS 

Male and female P. viteana were obtained for behavioral testing and for captive female 

field trapping studies by opportunistically collecting P. viteana-infested fruit from six 

Southwest- and four Northwest-Michigan vineyards during July-September in 2014, 2015 and 

2016. Following the methods of Taschenberg (1951, 1969), fruit from each site was held in a 

separate plastic bin containing strips of clear plastic for developing larvae to use as a substrate on 

which to pupate. Pupae were collected every three days from each bin, and then placed in 

individual 30 ml deli cups and held in an environmental chamber (28°C, 17:7 L:D and 56-60% 

RH) until the moths emerged. Upon emergence, moths were anesthetized with CO2 and 

examined with a dissecting microscope to determine the sex. Adults were used within 5 days 

after emergence.  

 

Bioassays 

A Y-tube olfactometer (Figure 2.1) was used in all experiments. This apparatus was 

custom built by the Michigan State University Chemistry Glass shop (East Lansing, MI, USA) 

using 1.5 cm i.d. glass tubing. The body of the Y-tube was made by heat-joining a 13 cm length 

of glass tubing to two 7 cm arms, each positioned 30o from the longitudinal axis of the 13 cm 

tube with all three tubes positioned in the same plane. The body of the Y-tube had ends with 

female connections, each with a ground glass interior surface to connect the upper arms of the Y-

tube to sample chambers. A moth transfer tube connected to the third opening facilitated 

introduction of male moths into the apparatus. Sample chambers/transfer tubes were constructed 

from a single piece of 2 cm (o.d) glass tubing, a porous glass partition that divided the lumen of 

the tube so it could be used as a sample chamber or a moth transfer tube. The upper compartment 

 

25 

(sample chamber) was topped by a 3 cm threaded collar and this held either a pheromone sample 

or a female P. viteana. Threaded open-top bushings (McMaster-Carr, Elhurst, IL, USA) were 

used to connect the air supply to the sample chambers (Figure 2.1). The compartment below the 

glass partition was made with a ground glass outer surface that fit into the female ends of the Y-

tube body. After each run the Y-tubes were washed in methanol and hexane and dried before the 

next set of runs. Five sets of Y-tube bodies and sample chambers/transfer tubes were constructed 

to allow for changing out the apparatus periodically without having to wash the Y-tube 

component parts and wait for them to dry.      

Air from the pressurized building air supply was purified with activated carbon, and 

hydrated by passing the airflow through 0.83 cm food grade tubing (McMaster-Carr, Elhurst, IL, 

USA) into a glass air stone submerged in de-ionized water inside a stoppered 250 ml Erlenmeyer 

flask with an outflow port. The hydrated outflowing airstream was split with a branched 

connector (McMaster-Carr, Elhurst, IL, USA) and each branch flowed through additional similar 

tubing (~0.5 m) into a 300 ccm flowmeter (Analytical Research Systems, Gainesville, FL, USA). 

The flow through each sample chamber on the upper arms of Y-tube apparatus was held at 25 

ml/min.  

To test whether male moths from Northwestern and Southwestern Michigan respond 

differently to a standard pheromone blend, a 1 µg/ml stock solution of P. viteana pheromone 

(10:1 mix of (Z)-9-dodecenyl acetate and (Z)-11-tetradecenyl acetate) in hexane was blended 

from pure pheromone components (Bedoukian, Danbury, CT, USA). A 5µl aliquot (5ng) of this  

 

26 

Figure 2.1. Y-tube apparatus to test behavioral responses of male P. viteana to a 
standard pheromone blend or to females from different populations. Left) Y-tube set up 
showing experimental enclosure; middle) close-up of Y-tube; right) male moth in one 
arm of the Y-tube. 

pheromone solution was pipetted onto a 0.5 x 0.5cm piece of filter paper and allowed to dry. The 

treated filter paper was then placed in a sample chamber attached to one arm of the Y-tube. A 

similar piece of filter paper treated with 5µl of hexane was placed in the sample chamber in the 

other arm of the Y-tube. A small ball of glass wool was placed at the top of each sample chamber 

to separate the end of the air supply tubing from the contents of the sample chamber and prevent 

contamination of the air-supply tubing.  

All assays were performed in a walk-in environmental chamber set to 28°C and 60% RH 

and during the scotophase when males and females are most active (Cha et al. 2008a, Cha et al. 

2008b, see also Chapter 4), and when female P. viteana have the highest pheromone titer 

(Witzgall et al 2000). A run began when a 2 to 3 day old male P. viteana moth was moved into a 

transfer tube that was then attached to the base of the Y-tube. The male was able to move freely 

in the Y-tube and chose an arm. A choice was scored when the test insect moved through the Y-

tube, continued at least half way up one arm of the tube, and remained in the arm for at least 5 

seconds. Males that did not move into an arm after 3 minutes were scored as “no choice”, and 

these runs were excluded from the analysis. Each male was used only once, and the location of 

 

27 

the arm where the pheromone sample was presented was alternated every 5 to 10 runs to reduce 

positional bias. The Y-tube apparatus was washed with methanol and then hexane and allowed to 

dry between trials. To test whether Northwest or Southwest Michigan males chose the Y-tube 

arm with the pheromone sample more or less often than by chance, a two-tailed Fisher’s exact 

test was used (JMP v13.1.0, 2016 SAS Institute, Cary NC, USA). 

To compare the responsiveness of Northwest and Southwest Michigan male P. viteana to 

females from the same or different region, a series of Y-tube bioassays were conducted. 

Individual moths were obtained in the collections described above, and the Y-tube olfactometer 

was the same as described previously (Figure 2.1). These assays were performed during the 

scotophase in a walk-in environmental chamber set to 28°C and 60% RH. One two to three day 

old female P. viteana from a Northwest Michigan vineyard and one similarly aged female from a 

Southwest Michigan vineyard were placed in sample chambers in separate arms of the Y-tube, 

and a small ball of glass wool was positioned in each sample chamber above the female. For 

each run, a two to three day old naïve male P. viteana moth was transferred to the base of the Y-

tube and allowed move in the tube. Choices were scored as above, and the sides of the Y-tube 

that contained females from the two regions were alternated to reduce positional bias. Females 

were used for 5-10 runs and then replaced, and males were used only once. The proportion of 

moths that chose a female from the same population was compared using a two-tailed Fisher’s 

exact test (JMP v13.1.0, 2016 SAS Institute, Cary NC, USA). 

 

 

 

 

 

28 

Figure 2.2. Captive female traps and lures for comparing the response of males in 
northwestern and southern Michigan vineyards. Left to right: Captive females in a mesh 
cage inside a trap. Standard pheromone lure loading set-up (inset in upper left shows 
orientation of septa for loading). Pherocon VI (Delta) trap with a standard pheromone lure 
deployed in a vineyard. 

Field trials 

To determine the response of resident males to a standard pheromone blend and to 

females from Northwestern and Southwestern Michigan, a trapping experiment was established 

in 2015, 2016 and 2017 at three Southwest and three Northwest Michigan vineyards, each with a 

history of grape berry moth infestations. At each vineyard, white Pherocon VI traps (Trece Inc, 

Adair, OK, USA) were baited with captive females or lures containing the standard P. viteana 

pheromone blend described above.  

Female P. viteana for these experiments were obtained from the collections described 

previously. On the day prior to deploying traps, individual 2 to 3 day old female moths were 

anesthetized with CO2 and transferred, in groups of 5, into a metal mesh cage (Figure 2.2) along 

with a 1.27 cm piece of moistened dental wicking (Absorbal, Wichita, Kansas, USA). Cages 

were then closed and held in an environmental chamber at 10°C, 60% RH overnight. The 

following day, these females were transported to field sites in a cooler with ice packs for 

deployment in traps 

 

29 

Lures for this experiment were made using the standard P. viteana pheromone blend 

described above. The stock solution of P. viteana pheromone in hexane (1µg/ml), a 10-fold  

dilution of this solution, and pure hexane as a negative control were used to make solutions of 

1.0,  0.1, or 0µg/ml.  Small rubber septa (West Pharmaceuticals, Exton, PA, USA) were arranged 

open side up in aluminum mesh racks with 0.64cm2 openings (Figure 2.2), and septa were filled 

with 1 ml of the approriate dilution in four 0.25ml aliquots to produce a set of lures that 

contained 1.0,  0.1, or 0µg of pheromone per lure. These quantities are well below the 100 µg 

that is used in commercial lures (Jordan et al. 2013), and I chose these reduced levels to make the 

lures more comparable to the 1 ng of pheromone produced by female P. viteana (Witzgall et al. 

2000). The mesh racks were held in a fume hood during loading, and then septa were stored in 

the hood until the solutions evaporated. An additional 0.25ml of hexane was then pipetted into 

each septum to help the pheromone adsorb onto the septum wall. The lures were dried in the 

fume hood and then grouped by pheromone load and each group was placed in a separate 200ml 

labeled glass jar, sealed with teflon tape and stored in a freezer (-5°C) until the lures were 

deployed in traps. On the day of deployment, the lures were transported to field sites in a cooler 

with ice packs separate from the females.  

At each vineyard, white Pherocon VI traps (Trece Inc, Adair, OK, USA) were baited with 

one of the following treatments: five caged Northwest Michigan females, five caged Southwest 

Michigan females, a 1µg P. viteana pheromone lure, a 0.1µg pheromone lure or a blank lure as a 

negative control. Traps were hung from the trellis wire (1.5m above the ground) next to vineyard 

end posts that were adjacent to a woodlot. Traps were separated by 10m, and deployed for one 

week. Trapping dates varied between years with traps in the southwest deployed 11 to 25 August 

2015; 17 to 31 May, 12 to 19 July and 5 to 12 August 2016, yielding a total of 17 vineyard x date 

combinations. Traps in the northwest were deployed for a total of 15 vineyard x date 

 

30 

combinations with dates of 22 to 29 August 2015, 17 June to 1 July 2016 and 9 to 29 August 

2017. When traps were checked, sticky trap liners, caged females and lures were removed and 

replaced, and the location of traps was re-randomized.  

Due to previous knowledge about the differences in captures between Northwestern and 

Southwestern Michigan vineyards, I expected region to be a strong and significant predictor of 

male captures, and inclusion of this factor in our statistical analysis would cause a significant 

interaction between lure treatment and region. In addition to complicating the interpretation of 

the results, this would reduce the main effect of bait type. Thus, I chose to compare traps within 

regions. The documented variation in male captures between times of year (Botero-Garcés and 

Isaacs 2003, Mason and Isaacs 2018), resulted in considerable variation between sample dates. 

Therefore, I chose to compare the sum of male captures in each lure treatment over the entire 

experiment. The total number of male captures was compared between treatments with a mixed 

model ANOVA with vineyard as a random factor and lure type as a fixed factor separately by 

region using vineyards as replicates (JMP Pro Ver 13.1 2016, SAS Institute Inc 2016). 

 

 

31 

Bioassays 

RESULTS 

 

In Y-tube tests of male regional response to a standard pheromone sample, 69% of the tested 

males moved in the Y-tube olfactometer and made a choice between arms containing pheromone 

or plain air. Males from northwestern vineyards chose the arm with the pheromone sample in 

39% of the runs, while southwestern males chose the arm with the pheromone sample in 60% of 

the runs, and these percentages were not significantly different between regions (Figure 2.3, χ2 = 

1.8, n=43 df =1, P = 0.22).  

Figure 2.3. Percentage of P. viteana males from northwest and southwest Michigan that 
chose the Y-tube olfactometer arm containg a pheromone sample. This was not 
significantly different between regions. 

 

In bioassays that tested whether males respond preferentially to females from the same 

region, 84% of the tested males moved in the Y-tube olfactometer and made a choice between 

arms that contained a northwestern or southwestern female. Northwestern and southwestern 

males responded similarly to females from either population in Y-tube assessments. Males from  

 

 

 

 

32 

 

 

 

 

 

 

 

 

 

Figure 2.4. Percentage of P. viteana males from northwest and southwest Michigan that 
chose the Y-tube olfactometer arm containg a female from the same or different regions. 
Males did not prefer females from the same region. 

 

northwestern vineyards chose the arm with the northwestern female in 57% of the runs, while 

southwestern males chose the arm with the southwestern female in 50% of the runs (Figure 2.4), 

and male response was not significantly different between regions ( χ2 = 0.42 , n=83, df =1, P = 

0.66). 

 

Field trials 

 

In the field trial to test the response of resident males in different regions to traps baited with 

captive females from Northwest or Southwest Michigan and to a standard pheromone blend, the 

total number of males captured in traps deployed in Southwest Michigan vineyards was over 45 

times higher than those in Northwest Michigan. In Southwest Michigan, male captures in the 1 

µg lure treatment were at least 20 fold higher than captures in either of the captive female traps 

or in the control traps, and these differences were statistically significant (F4, 8 = 14.84, P = 

0.0009). There was a similar pattern of captures across bait treatments in Northwest and 

Southwest Michigan vineyards. Traps containing the standard pheromone lure caught a greater  

 

33 

number of moths than the traps loaded with either Southwest or Northwest Michigan females or 

the control (0 µg) lure (Figure 2.5). However, male captures in the 1 µg lure in vineyards in 

Northwest Michigan were only 2 to 4 fold higher than in other traps and captures were not 

significantly different across trap treatments (F4, 8 = 2.12, P = 0.17; Figure 2.5).  

Pheromone lures

     NW                    SW 

Females 

Figure 2.5. Response of resident male P. viteana to traps deployed in vineyards in 
Northwest- and Southwest-Michigan. Traps were baited with pheromone lures or 
captive P. viteana females from Northwestern or Southwestern Michigan. Columns 
labeled with the same letters are not significantly different (P > 0.05). 

 

34 

Paralobesia viteana males from different regions had similar responses to a standard pheromone, 

DISCUSSION 

 

and they also responded similarly to females from their own and different geographical areas. In 

Y-tube choice tests, the percentage of Northwestern males that chose the standard pheromone 

sample was not different than that for Southwestern males. When allowed to choose between 

females from Northwestern and Southwestern Michigan in a Y-tube olfactometer, males showed 

no preference for females from the same region. In vineyards in Northwest and Southwest 

Michigan, there was a similar pattern in the relative numbers of resident males captured in traps 

baited with a standard pheromone blend or with captive females from Northwest or Southwest 

Michigan. In both regions, more males were caught in traps baited with a 1µg pheromone lure 

than in those baited with a 0.1µg lure, a 0µg lure or with captive females from either Northwest 

or Southwest Michigan. Although there were only significant differences in male captures 

among trap bait treatments in Southwest Michigan, there were no significant differences in the 

total number of males captured in traps baited with females from Northwestern or Southwestern 

Michigan. That is, resident males did not preferentially chose females from the same region, and 

males from both regions are captured in traps containing the standard pheromone blend. The fact 

that P. viteana males from different regions had similar responses to a standard pheromone and 

responded similarly to females from different geographical areas suggests that variation in male 

captures between Southwest and Northwest Michigan is not caused by regional differences in 

male response to pheromone or to regional differences in pheromone blend.  

My results contrast other studies reporting geographic differences in pheromone 

composition and male response to pheromone in other tortricid species (Foster 1986, El - Sayed 

et al. 2003, Stelinski et al 2007b). In previous studies that showed divergence in pheromone 

composition or male response to pheromone, thousands of kilometers separated the observed 

 

35 

populations. For example, the populations of C. rosaceana in the Eastern and Western US that 

were compared by El - Sayed et al (2003) and Stelinski (2007b) were separated by over 4,000 

km. Given there is a negative relationship between geographical distance and gene flow between 

populations (Manel et al. 2003), the likelihood of local adaptations that result in trait divergence 

increases with the distance between populations. Likewise, physical barriers that restrict 

movement between populations would be more likely to occur between widely separated 

populations compared to nearby populations. Northwestern and Southwestern P. viteana 

populations in Michigan are separated by 400km, and this may not have been sufficient to retard 

gene flow and movement of individuals between northwestern and southwestern populations, 

and therefore prevented differentiation of pheromone composition or male response to 

pheromones between these regions.  

Additionally, the observation in Y-tube assays and field trapping that males do not prefer 

females from their region of origin supports the premise that the composition of the female sex 

pheromone has not diverged between southwestern and northwestern populations of P. viteana to 

such a degree that we can observe differential responses in males. Additional research that 

includes collecting and comparing the sex pheromone from females in northwest and southwest 

Michigan using gas chromatography and mass spectrometry would more directly address this 

question. If different pheromone compositions were present, the response of males to these 

different blends could be tested using electro-antennography and behavioral assays in flight 

tunnels, but these experiments were beyond the scope of the current study. The similar response 

of males to the standard pheromone and females in Y-tube assays, and the similar pattern of male 

captures in field studies suggest geographic variation in pheromone composition is unlikely to be 

present.  

 

36 

The results of bioassays and field studies do not support my prediction that the low P. 

viteana male captures observed in most vineyards in Northwestern Michigan are caused by 

regional differences in male response to the standard pheromone used in commercial lures, and 

the basis of this difference must lie elsewhere. There are several distinct differences between 

grape production areas in Michigan that align with the observed regional differences in male 

captures. The growing season is shorter and typically drier in Northwest Michigan, and these two 

factors may limit P. viteana population growth in that area relative to the warmer and wetter 

southwest portion of the state. In addition there are contrasts in the size and composition of the 

grape industry between northwest and southwest Michigan. There are about 13,100 acres of 

grapes in Michigan and approximately 75% of this acreage is planted in juice grapes (Vitis 

labrusca L. cv. Concord and cv. Niagara) in Southwest Michigan. The remaining acreage is 

planted in wine grapes with a little over half of the acreage is in Northwest Michigan and 

consists of a mix of European wine grape varieties of V. vinifera L. and French hybrids (Anon 

2016). There are marked differences in the intensity and types of management practices used in 

wine and juice grape production in Michigan. The high value of wine grapes provides a margin 

of profit that allows growers to invest more capital in pest and disease management and vineyard 

maintenance than in lower value juice grape varieties. Although these differences may result in 

lower rates of cluster infestation in wine grape vineyards, it is unlikely to produce the observed 

difference in male captures between regions, because insecticide applications in grapes typically 

target larvae, and not adults (Isaacs et al. 2005, Isaacs et al. 2012b, Mason et al. 2016). It is also 

not likely that the difference in species and varieties of grape cultivated between Northwest and 

Southwest Michigan contributed to this phenomenon, because in areas where both juice and wine 

grapes are grown there are similar levels of P. viteana male captures and cluster infestation in 

 

37 

wine and juice grape vineyards (Slingerland 1904, Johnson and Hammar 1912, Biever and 

Hostetter 1989, K. Mason. personal observation). 

Although the incidence of P. viteana infestation (i.e. % damaged clusters) can be similar 

between varieties or between regions as is shown in Chapter 1, (Figure 1.2), my personal 

observations over the past two decades show that the severity of P. viteana infestations (the 

number of damaged berries per cluster) in southwest Michigan is much higher than the severity 

of damage in northwest Michigan. My research results and observations lead me to conclude that 

the regional difference in the number of male P. viteana captured in pheromone traps in 

Michigan reflects the relative population sizes of P. viteana in these two production areas. 

Although population size was not exhaustively measured in the current study, the results of the 

field trial provide some evidence for this possibility. Across all bait types more males were 

captured in southwest Michigan compared to captures in traps in northwest vineyards. This 

includes captures in the control traps baited with a blank lure, which can be considered passive 

traps that would measure the activity/density of P. viteana in a given area without the possible 

interactive effect of an attractant. Over the course of the current study in traps that contained 0 

µg lures, there was an average of 0.3 males per trap per vineyard in Northwest Michigan and 1.7 

males per trap per vineyard in Southwest Michigan. This six fold difference in captures in un-

baited traps indicates there is likely a difference in the size of P. viteana populations between 

regions.  

The argument that the variation in P. viteana captures between regions in Michigan is a 

reflection of different population sizes is strengthened by considering the history of the grape 

industry in Michigan. Commercial grape production in southwest Michigan dates back to the late 

19th century (Slingerland 1904, Johnson and Hammar 1912, Pinney 1989), whereas in Northwest 

Michigan, the first commercial plantings were established in 1970 (Anon 2016). Given that wild 

 

38 

grapes (Vitis spp.) are common in wooded areas throughout North America (Johnson and 

Hammar 1912, Galet 1979, Morano and Walker 1995), including Michigan (Voss 1996, Botero-

Garcés and Isaacs 2004a, Jenkins and Isaacs 2007a), it is likely that P. viteana populations exist 

in these areas and these populations could increase if vineyards were planted near wooded areas. 

I postulate that P. viteana populations are much larger in commercial grape plantings in 

Southwest Michigan because of the increased amount of available resources in the form of 

cultivated grapes.  

Landscape composition varies between production regions. In the northwest region of 

Michigan (Leelanau and Grand Traverse counties) 12% of the land area is forested, and this is 

much greater than in the southwestern region (Allegan, Van Buren and Berrien counties) where 

2% of the land area is forested (Homer et al. 2015). Wild grapevine density may also vary 

between regions, and this could contribute to different population sizes in Northwest and 

Southwest Michigan. This premise could be further explored with a trapping and mapping study 

that compares P. viteana captures in commercial vineyards and adjacent woodlots in Southwest 

Michigan to similar measures in vineyards and adjacent woodlots in Northwest Michigan. Traps 

would also need to be placed in wooded areas away from any grape production to estimate the 

background population of P. viteana. I would expect that captures in woodlots in Northwest 

Michigan would be similar to those in wooded areas that are not close to commercial vineyards. 

In addition, captures in the northern region would be much lower than those in wooded areas 

adjacent to vineyards in Southwest Michigan. Given that there is a large difference between 

regions in the percentage of area covered in woodland, it would be critical to conduct vegetation 

surveys and landscape analysis to measure the abundance and density of wild grape and 

characterize the landscape surrounding the areas where grape berry moth traps are deployed.  

 

39 

Independent of any underlying factors that may be responsible for potential regional 

differences in P. viteana population sizes, my results have important implications for future 

management of P. viteana in Michigan. This is particularly salient in Northwest Michigan, and 

in other areas where commercial grape production is beginning or expanding into uncultivated 

areas with high proportions wooded habitat where wild grape (Vitis spp.) is prevalent. 

Paralobesia viteana is a native insect that will likely be present at low levels in these areas, and 

if left unchecked can develop into a major economic pest.  

Given that southwestern and northwestern males respond similarly to the standard 

pheromone, my advice to growers and fruit extension agents in areas where grape plantings are 

increasing would be to start monitoring for this pest by using pheromone traps and by 

quantifying infestation in newly planted vineyards. Effective control tactics have already been 

developed and tested in areas where P. viteana is a serious pest, and these tools could be used 

when population buildup is first detected to reduce the likelihood that P. viteana causes 

substantial economic losses.  Educational programming in areas where viticulture is expanding 

should start while wild populations of P. viteana are at low levels. This could easily be 

accomplished with minimal funding through university extension or grower industry 

collaboratives that are already in place.  

 

40 

JUICE GRAPE CANOPY STRUCTURE AND CLUSTER AVAILABILITY DO NOT 

REDUCE MIDDLE AND LATE SEASON CAPTURES OF MALE GRAPE BERRY MOTH, 
PARALOBESIA VITEANA (LEPIDOPTERA: TOTRICIDAE) IN SEX PHEROMONE TRAPS 

Published as: Mason, K.S. and Isaacs, R. (2018) Juice grape canopy structure and cluster 

availability do not reduce middle and late season captures of male grape berry moth,  

Paralobesia viteana (Lepidoptera: Totricidae) in sex pheromone traps.  

Environmental Entomology Vol. 74:3 707-714 

INTRODUCTION 

CHAPTER 3 

 

 

 

 

The grape berry moth, Paralobesia viteana (Clemens) (Lepidoptera:Tortricidae), is a specialist 

herbivore found in woods and vineyards across eastern North America, feeding primarily on wild 

and cultivated plants in the genus Vitis (Johnson and Hammar 1912). This moth is a primary pest 

of cultivated grapes (Vitis labrusca L. and Vitis vinifera L. and their hybrids), and it has 

challenged grape growers since the beginning of commercial grape production in this region 

(Johnson and Hammar 1912, Hoffman et al. 1992, Isaacs et al. 2012b). 

 

There are multiple generations of P. viteana in a growing season depending on location 

and the length of the growing season, with three and sometimes four generations in Michigan 

(Tobin et al. 2003, Teixeira et al. 2009, 2011). First generation adults begin to emerge from 

overwintering pupae in late April or early May, and mated females start to lay eggs on warm 

nights in early to mid-June (Clark and Dennehy 1988, Teixeira et al. 2009, 2011). After larvae 

hatch, they feed on multiple adjacent flowers or young berries and produce webbing that 

encloses the feeding site (Johnson and Hammar 1912). Larvae of subsequent generations 

excavate tunnels into the fruit, and web together and infest multiple berries (Johnson and 

Hammar 1912). The economic impact of the first generation is minimal, but larvae of later 

generations can cause significant economic losses due to reduced yield, lowered fruit quality or 

rejection of contaminated fruit by fruit processors (Hoffman et al. 1992, Teixeira et al. 2009, 

 

41 

Roubos et al. 2013) (Hoffman et al. 1992. Larval feeding by P. viteana is similar to that of the 

closely related European species, Lobesia botrana (Denis & Schiffermüller) that also affects 

yield and quality by increasing susceptibility to bacterial and fungal infections (Fermaud and Le 

Menn 1992, Mondy et al. 1998, Ioriatti et al. 2011). Because of the risks of direct yield loss, 

larval contamination of fruit and reduced fruit quality due to pathogens, P. viteana is the target of 

the majority of insecticide applications to vineyards east of the Rocky Mountains (Hoffman et al. 

1992, Teixeira et al. 2009). 

 

Flight activity of male grape berry moth can be monitored using traps containing lures 

baited with synthetic sex pheromone, but the males of this species are only captured in 

pheromone traps consistently during the first generation that is active around bloom. The first 

generation causes little larval feeding damage, but in the second and third generations in the 

early and late summer, respectively, the level of oviposition on berries, and subsequent larval 

infestations increase greatly, yet few males are caught in monitoring traps (Snyder et al. 1992, 

Teixeira et al. 2009 - Figure 1, Isaacs et al. 2012a). This disconnect between male moth captures 

and larval infestation at harvest prevents development of action thresholds based on captures of 

male moths as has been done for other lepidopteran fruit pests  (Binns and Nyrop 1992, Bradley 

et al. 1998, Reddy and Manjunatha 2000, Knight and Light 2005a). Exploring factors that affect 

male captures of this species will inform the development of lures or trapping strategies that 

improve moth monitoring, potentially allowing for better timing of insecticide applications and 

improving decision-making about the need for treatments.  

 

Volatile host plant chemicals can influence host-finding in some key crop pests (Bruce et 

al. 2005, Leskey et al. 2008, Piñero and Dorn 2009, Saveer et al. 2012). Most previous studies in 

this area have focused on the behavior of females, but either sex can respond to host plant 

volatiles in the laboratory or field (Stelinski et al. 2003, Light and Knight 2005, Faraone et al. 

 

42 

2013). Within species, odorant receptors and neural pathways are also similar between sexes 

(Jordan et al. 2009, Varela et al. 2011). Female codling moth, Cydia pomonella L., are attracted 

to apple odor, and show increased oviposition and flight response in laboratory studies (Wearing 

et al. 1973, Yan et al. 1999, Coracini et al. 2004). In addition, C. pomonella males are attracted 

to compounds derived from pear, and these can be used in monitoring traps resulting in higher 

captures than with pheromone alone (Light et al. 2001, Knight and Light 2005b, Il’ichev et al. 

2009)). In the oriental fruit moth, Grapholita molesta (Busck), females are attracted to a 

combination of green leaf volatiles and other aromatic compounds that are derived from peach 

shoots (Piñero and Dorn 2007). In addition, male and female G. molesta are attracted to 

monitoring traps baited with volatiles derived from peach and pear (Lu et al. 2012). Female 

European grapevine moth (L. botrana), consistently flew upwind and landed on unripe grape 

clusters in wind tunnel tests (Tasin et al. 2006). In subsequent studies, L. botrana females were 

also attracted to a four-component blend of volatile compounds collected from the headspace 

around confined grapes clusters, and females were attracted to synthetic grape volatiles in field 

studies (Tasin et al. 2009). In similar studies, P. viteana females oriented toward grapevine 

structures in wind tunnel tests, and this response was stronger for shoot tips and mature leaves 

than that for flowers, unripe berries or mature fruit (Cha et al. 2008a). In further tests using wind 

tunnels, females consistently flew to lures loaded with blends of grape shoot volatiles that were 

collected from the headspace around grape shoots (Cha et al. 2008b). Male P. viteana were also 

attracted to this blend as males were captured in traps baited with the same volatile blends in 

field tests (Cha et al. 2008b, Loeb et al. 2011). These latter studies show that grape shoot 

volatiles are important and attractive cues for both male and female P. viteana, and they also 

suggest that the volatile-rich grape canopy may influence the interaction between male P. viteana 

and monitoring traps.  

 

43 

 

The size and chemical composition of grape clusters and the vine canopy change 

considerably during seasonal growth and development (Hrazdina et al. 1984, Mullins et al. 1992, 

Schultz 1995). Early in the season, few leaves and only small flower or berry clusters are present 

on vines. As the growing season proceeds, the clusters increase in weight 100 fold, and as the 

berries soften and become ripe, physiological changes lead to increased soluble solids, lower 

organic acids (e.g. tartaric, malic and citric), and, depending on grape variety, an increase in pH 

to a final value between 2.8 and 3.7 at harvest (Hrazdina et al. 1984, Jackson and Lombard 

1993). The concurrent increase in phenolic compounds, such as flavonoids and anthocyanins, 

can impart distinctive odors and flavors to ripening grape clusters (Singleton and Trousdale 

1983), and volatile terpenes that increase greatly after veraison (fruit coloring) also change the 

aroma and flavor characteristics of grapes (Dimitriadis and Williams 1984, Rosillo et al. 1999). 

These physiological transformations contribute to an odor landscape that varies consistently 

through the growing season, and these changing host plant cues may provide information that P. 

viteana could use to orient to its host plant, and find potential mates and oviposition sites. If P. 

viteana mating occurs on the grape clusters, or if females spend the majority of their time on 

clusters, males would have an increased chance of finding females, and mating successfully, if 

they can detect and orient toward the volatiles produced by grape clusters. This could lead to a 

“competition” between clusters and traps that might lead to a reduction in the number of male 

captures in traps. In addition the combination of grape volatiles and sex pheromone may be more 

attractive to male P. viteana than sex pheromone alone, as has been shown for C. pomonella 

(Light et al. 2001). This preference could result in reduced P. viteana male captures in 

pheromone traps because the amount of grape cluster volatiles increases during the season due to 

the increase in cluster size and the ripening of the crop.  

In addition to changes that occur as clusters develop, the physical structure of the juice 

44 

 

 

grapevine canopy is also transformed through each season. In varieties that are bred and 

managed to maximize crop yield, such as juice grapes (Vitis labrusca, cvs. Concord and 

Niagara), the vines are typically cane-pruned and trained to a single wire top-cordon system. The 

resulting trailing habit of shoot growth causes the canopy to become increasingly dense, and it 

creates a thick matrix of shoots and leaves as the season progresses (Smart et al. 1982b, Miller 

and Howell 1998, Dry 2000, Bates 2008). The quantity and quality of grape shoot and leaf 

volatiles that are present in a vineyard change as the canopy grows and becomes more dense 

(Tasin et al. 2006). The dense canopy imposes challenges on disease and insect management by 

forming an impediment to air flow and reducing spray coverage (Wise et al. 2010). The increase 

in canopy density may also affect monitoring P. viteana with pheromone traps by altering trap 

findability (Miller et al. 2006), making it less likely that male moths find traps. The canopy could 

physically block males from reaching traps, it may disrupt the structure of the pheromone plumes 

from lures, or the naturally occurring grape shoot volatiles may draw moths away from traps. 

 

To better understand the observed phenology of P. viteana in vineyards, this study 

explored the interaction between P. viteana and two host plant characteristics, cluster density and 

canopy structure. We determined if these factors reduce moth captures in pheromone traps by 

testing two hypotheses: 1) grape clusters reduce captures of P. viteana males in pheromone traps, 

and 2) the juice grape canopy reduces male P. viteana moth captures in pheromone traps.  

 

 

45 

Field trials measured the effect of the presence and density of grape clusters on captures of male 

METHODS 

 

P. viteana at six (2013) or five (2014 and 2015) commercial juice grape vineyards (c.v. 

'Concord') in Van Buren and Berrien counties in southwest Michigan (42.25 to 41.75ºN, 86.5 to 

85.75ºW). All vineyards were grown on a 1.8m (6ft) tall trellis with a single-wire, top-cordon 

training system, and vineyards were cane pruned to ~75 buds per vine. At each vineyard, three 

15x15m plots (5 rows x 5 vines), separated by at least 15m, were set up on the vineyard border 

adjacent to a woodlot containing wild grape (Vitis spp). Plots received one of the following 

randomized treatments: 100% of the clusters removed, 50% of the clusters removed or 0% of the 

clusters removed (control). Pruning shears were used to remove clusters between the 26th of May 

and the 18th of June, before the end of bloom in all three years. 

One Pherocon VI monitoring trap baited with a sex pheromone lure (Trece Inc, Adair, 

OK) was hung inside the grape canopy with the long axis of the trap parallel to the row. Traps 

were attached to the trellis wire in the middle row of each plot between the third and fourth vines 

in the row when clusters were removed in late May or early June. Captures of males were 

recorded weekly until the end of the experiment. For each season, lures from a single lot were 

used, and lures were changed every 6 weeks to coincide with the start of each generation. Sticky 

trap liners were changed every 2 to 4 weeks when they became water-logged or excessively 

soiled. P. viteana generations were determined using the MSU Enviroweather grape berry moth 

model (Isaacs 2017) that employs an egg to adult development time of 423.9 DD8.41ºC and local 

bloom of wild grape (Vitis riparia L.) as the biofix (Tobin et al. 2001, Teixeira et al. 2009). 

Using this model, moths that emerged from overwintering pupae and were caught in May and 

June were classified as the first generation, those caught in July through mid-August comprised 

the second generation, and the third generation consisted of moths that were captured from mid-

 

46 

August until harvest in late September. In each year, the total number of males captured during 

each of three generations and the total number captured per season were square root transformed 

before analysis to stabilize error variance in order to meet the normality assumptions of the 

analysis of variance. Captures were then compared among treatments with analysis of variance 

using vineyard as a random variable and plots as replicates followed by means separation using 

Tukey’s HSD test (JMP Pro ver 13.1.0, SAS Institute Inc 2016). 

To determine whether mid and late-season P. viteana male captures are reduced by a 

dense juice grape canopy, a field trial was established during the spring of 2012 at a commercial 

Concord vineyard in Lawton, MI (42.15°N, 85.83°W). This experiment was repeated in 2014 

and 2015 in a vineyard (cv Niagara) at the Trevor Nichols Research Center in Fennville, MI 

(42.58°N, 86.14°W). Ten 15 x 15m plots (5 rows x 5 vines) were marked on the edge of the 

vineyard adjacent to a woodlot containing wild grape (Vitis spp.). The vineyard was grown on a 

Figure 3.1. Vineyard plot containing a triangular tunnel designed to 
keep grape canopy open. Photograph was taken early in the season 
before the canopy was fully developed. 

 

47 

1.8m (6ft) tall trellis and trained to a single-wire, top-cordon system, and vines were cane pruned 

to ~75 buds per vine. We did not collect canopy measurements such as shoot length, cluster 

density leaf density, etc., as our study only included two levels of canopy density, “Open” or 

“Unaltered”. Treatments were arranged in blocked pairs with the two different treatments applied 

in adjacent plots that were separated by at least 9m. In the center row of one randomly chosen 

plot in each pair, we used bamboo stakes, snow fence and zip ties to hold the canopy open by 

constructing a 15m long triangular tunnel (0.5m on a side) that was open at the bottom (Figure 

3.1), and this treatment was designated as “Open”. The second plot in the pair was left unaltered, 

and this treatment was referred to as “Unaltered”, and was used as a control. Treatments were re-

randomized each year to reduce location effects. In mid-May of each year, a monitoring trap as 

described above was hung on the trellis wire with the long axis of the trap parallel to the row and 

between the 3rd and 4th vines in the middle row of each plot. Traps were within the canopy in 

“Unaltered” plots, or inside the tunnel in “Open” plots. The number of P. viteana males captured 

was recorded each week from mid-May through September. Each year, lures came from a single 

lot and were changed every 6 weeks to coincide with the start of each generation. Sticky trap 

liners were changed at least every 4 weeks when they became waterlogged or soiled with insects. 

Generations were determined as described above, and the total number of males captured during 

each generation and the total captured in a season were compared between treatments with 

analysis of variance using square-root transformed data and included blocked pairs as a random 

variable and vineyards as replicates (JMP Pro 13.1.0, SAS Institute Inc, 2016). In 2015, data 

transformation did not satisfy the normality assumptions for analysis of variance, so these data 

were not transformed and were compared between treatments using a Wilcoxon Test of summed 

ranks (JMP Pro 13.1.0, SAS Institute Inc 2016). 

 

 

 

48 

RESULTS 

 

In 2013, significantly more P. viteana males were caught in traps in plots where clusters were 

retained compared to plots where they were removed. This was true for the number of moths 

trapped during each generation (Generation 1: F2,10 = 4.67, P < 0.037; Generation 2 F2,10 = 7.48, 

P < 0.01; Generation 3: F2,10 = 7.73, P < 0.01), and for the total captured during the entire season 

(F2,10 = 9.04, P < 0.006; Figure 3.2). However, in 2014 and in 2015 after experimental plots were 

re-randomized, no significant differences were detected among cluster removal treatments in the 

total number of male P. viteana captured during the entire season (F2,8 = 2.53, P > 0.14, Figure 

3.2). There was also no difference in the number of males captured during any of the three 

generations in 2014 (F2,8 < 2.52, P > 0.14), or 2015 (F2,8 < 0.86, P > 0.45). The contrasting 

results between the first year and subsequent years indicate there was a confounding location 

effect in 2013, most likely because our control plots were inadvertently situated in areas of high 

grape berry moth pressure. 

No significant differences were found between male captures in plots where all of the 

clusters were removed compared to captures in plots where 50% of the clusters were removed. 

The absence of a cluster removal rate effect suggests that removing clusters triggered vegetative 

growth, and this may have led to a similar increase in leaf volatiles in the canopy in the 50% and 

100% cluster removal treatments. This may have led to similar male moth captures between 

those treatments.  

 

49 

 

Figure 3.2. Effect of cluster removal on capture of male P. viteana. Captures of 
male P. viteana in plots with 0, 50% or 100% of clusters removed in 2013, 2014 
and 2015. Columns with the same letter are not significantly different; “NS” 
indicates no significant differences were found among treatments, P > 0.05. 

50 

 

 

The number of male moths captured in open canopies was similar to moth capture in 

unaltered canopies in 2012 (Figure 3.3). No significant differences in total number of male moths 

captured during the entire season were detected between canopy treatments in 2012 (F1,4 = 0.22, 

P > 0.65). Similarly, there were no significant differences between treatments in the number of 

moths caught during any of the three generations in 2012 (Generation 1: F1,4 = 0.05, P > 0.84; 

Generation 2: F1,4 = 0.65, P > 0.46; Generation 3: F1,4 = 0.12, P > 0.74). In 2014, significantly 

more male moths were captured in unaltered canopies than in open canopies during the second 

generation (F1,4 = 15.22, P < 0.018; Figure 3.3). However we found no significant differences in 

the number of male moths captured between canopy treatments during the first (F1,4 = 5.74, P > 

0.07) or third generation (F1,4 = 3.59, P > 0.13). The sum of moth captures over the entire season 

was also similar between canopy treatments (F1,4 = 5.72, P > 0.07). Moth captures in unaltered 

canopies were significantly greater than captures in open canopies only during the third 

generation in 2015 (Figure 3.3 Generation 3: Χ2 = 5.12, df = 1, P < 0.03).  Although the average 

number of males captured in unaltered canopies was arithmetically greater than captures in open 

canopies in the second generation, these differences were not statistically significant because of 

considerable variability within treatments (Generation 1: Χ2 = 2.45, df = 1, P > 0.11; Generation 

2: Χ2 = 3.55, df = 1, P < 0.06). Similarly, total captures for the season were not different between 

canopy treatments (Figure 3.3, Season total: Χ2 = 0.53, df = 1, P > 0.46). The consistent pattern 

of numerically higher male captures in unaltered canopies during the second and third 

generations shows the canopy does not reduce moth capture, and it suggests that shoots and 

leaves may be used by males to find traps or calling females.  

 

51 

Figure 3.3. Effect of manipulating canopy structure on captures of male P. viteana. 
Male captures in plots with unaltered, dense juice grape canopies (Unaltered) or 
canopies held open with a triangular tunnel (Open) in 2012, 2014 and 2015. 
Asterisks indicate treatments were significantly different (P <0.05). This experiment 
was run in a Concord vineyard in 2012 and in a Niagara vineyard in 2014 and 2015.
 

 

 

52 

These experiments showed that captures of male P. viteana are not consistently affected by 

DISCUSSION 

 

cluster density or by the vine canopy structure in juice grape (cv Concord and cv Niagara) 

vineyards. When we did observe treatment effects on moth captures, the results did not help to 

explain the previously documented reduction in male P. viteana captures in monitoring traps in 

the middle and late season.  

In the cluster density experiment in 2013, we caught significantly more males in plots 

where clusters were left intact than in plots with 50 or 100% of the clusters removed. This effect 

was not present in the following years when treatment locations were re-randomized, as there 

were no significant differences between cluster removal treatments in 2014 or 2015. We interpret 

this as evidence of a location effect in 2013, likely because by chance our control plots were near 

areas of high male moth activity/density. The results from all three years of our study falsified 

our original hypothesis that cluster density reduces male P. viteana capture in traps. Therefore, 

the presence or density of fruit does not cause the reduction of male captures of P. viteana in 

pheromone traps that occurs during the second and third generations (Snyder et al. 1992, 

Teixeira et al. 2009). Even though clusters increase greatly in size and the volatile chemicals 

produced by fruit clusters change markedly through the season, it appears they are not a critical 

cue used by male P. viteana. This contrasts the behavior of some other fruit feeding tortricids 

such as C. pomonella, G. molesta and L. botrana, that are attracted to volatiles derived from fruit 

(Knight and Light 2005b, Piñero and Dorn 2007, Tasin et al. 2009). However these three species 

all feed on multiple hosts, so we cannot rule out some contribution of diet breadth to the 

difference between these pests and the specialist, P. viteana. A meta-analysis comparing the 

responses of males of different species to host plant volatiles derived from fruit to those present 

 

53 

in shoots may help explain these differences, but that is beyond the scope of the present work. 

Our results are also consistent with previous research that shows fruit is less attractive than grape 

shoot tips and leaves to P. viteana (Cha et al. 2008a). Males are strongly attracted to shoot tips 

and leaves in addition to sex pheromone, and we saw that a change in the density of fruit does 

not affect male moth capture. We would expect an increase in vegetative growth when clusters 

are removed, and this presumably would lead to an increase in the amount of leaf volatiles in 

areas where clusters are removed. It is conceivable that an increase in leaf volatiles could draw 

more males into the cluster removal plots, but these males may be attracted to leaves and not to 

traps. Unfortunately, we did not measure vegetative growth or leaf volatile titers in our research 

plots, so we cannot directly assess the effect these factors had on male capture. 

In two of the three years of our canopy structure study, we found consistent numerical 

differences between male captures in vineyard plots with an unaltered canopy and those that 

were opened using an artificial tunnel. In 2012, the effects of these treatments did not differ, 

whereas in the second generation in 2014 and in the third generation in 2015, the number of 

males captured in unaltered canopies was significantly higher than in open canopies. These 

results show that the canopy does not impede the movement of male moths to traps. Captures of 

P. viteana in dense, unaltered grape canopies were higher than in open canopies, which 

highlights the possible importance of shoots and leaves in male trap finding behavior. As volatile 

compounds are attractive to male P. viteana, (Cha et al. 2008b), we may have caught more males 

in unaltered canopies because traps were in closer proximity to leaves in the unaltered vs open 

treatments. We were unable to assess the effect of the seasonal increase in leaf volatile titer on 

male captures because we did not manipulate the amount of leaf area in experimental plots with 

pruning, leaf removal, etc., but we expect the titer of leaf volatiles would have been similar 

between treatments. Still the results of our experiment refute the hypothesis that canopy structure 

 

54 

reduces male moth capture, and does not support the prediction that low captures of male P. 

viteana in traps at the end of the season are due to physical interference from the canopy. 

 It may be advantageous for a grape specialist such as P. viteana to respond more 

strongly to leaf volatiles than to fruit volatiles due to the climbing, spreading growth of 

grapevines in a natural setting. The total area of leaves of a grapevine is much greater than the 

area of the fruiting zone, and growing shoots may be several meters away from fruit clusters, 

particularly in uncultivated habitats (Mullins et al. 1992). We would therefore argue that P. 

viteana moving through wooded areas are more likely to encounter leaves than fruit, so detecting 

leaf volatiles may be the optimal strategy for finding host plants within the dense deciduous 

habitats of eastern North America.  

Paralobesia viteana has limited capacity for long flights and it seems well adapted to 

movement within the dense vegetation of its natural habitat (Botero-Garcés and Isaacs 2004b). A 

series of short flights between shoots may be advantageous for an organism like P. viteana that 

must find mates and food resources in a structurally complex environment such as a contiguous 

forest or vineyard canopy. If P. viteana uses short flights between shoots to move around its 

environment, we would expect to see lower numbers of males in traps in open canopies, because 

the trap is outside of the space where the moths are moving. Movement in the canopy was not 

addressed in our study, but it could be explored using video recordings (Grieshop et al. 2012) in 

open and unaltered canopies to compare the movement behavior of moths in relation to varying 

habitat structure.  

Some possible confounding factors may have influenced the canopy experiment, but it is 

unclear how important these were for our results. The experiment was performed at two different 

locations over three years, and two closely related grape varieties were used. In 2012, the trial 

was performed in a commercial vineyard (Vitis labrusca L. cv ‘Concord’) in Lawton Michigan, 

 

55 

while in 2014 and 2015, we used a V. labrusca L. (cv ‘Niagara’) vineyard 80 km away at the 

Trevor Nichols Research Center in Fennville, MI. High temperatures (25 - 30°C) in the spring of 

2012 led to an early start of growth, and made this one of the warmest years on record for the 

region. Subsequent spring freezes reduced the crop load by 30- 40% in the section of the 

vineyard we used, and the owner of the vineyard reduced his disease and insect management 

program, as is common practice in freeze years. The 2014 and 2015 growing seasons did not 

have a major freeze event, but they were some of the coolest seasons in the previous twenty 

years, and the experimental vineyard did not receive insecticide in 2014 or 2015. In any given 

year, all of the treated plots were exposed to these factors to the same degree, so we conclude 

that there were no confounding effects from weather, location or variety.  

The fencing material that we used to construct the tunnels to create open canopies may 

have produced repellent odors, or created a visual pattern that could have deterred male moths 

from entering plots that contained the tunnels. Although we did not directly test for the effect of 

the fencing on male moth captures, our data suggest there was not a repellent effect. There were 

no significant differences in captures between plots with fencing (Open) and plots without this 

material (Unaltered) in the first generation. During this period, the grape canopy was not fully 

grown and the tunnels were visible and any odors from the fencing would also be present (Figure 

3.1). Our results show the juice grape canopy affects captures of male grape berry moth, but the 

observed effect does not explain the previously reported reduction of male P. viteana captures in 

pheromone traps during the second and third generations (Teixeira et al. 2009, Isaacs et al. 

2012a). We postulated that the unaltered juice grape canopy interferes with a male’s ability to 

find traps. However, we caught more males in traps that we placed in unaltered as opposed to 

open canopies, and from this, we propose that the canopy is an important component of trap and 

presumably mate finding. Surprisingly, fruit cluster presence or density did not consistently 

 

56 

affect male captures, so we conclude that any effect the fruit may have does not contribute to the 

reduction of male captures during the middle and late season generations. There remains a need 

to explore the factors that cause reduced moth captures at the time when oviposition by P. 

viteana is increasing, and this could help to improve monitoring of this key vineyard pest. 

Additional studies that examine the reduction of captures during the second and third generation 

flights when oviposition and infestation increase will be reported later as separate publications. 

Other areas of research focus on testing the effects of temperature on some important aspects of 

mating behavior such as: female calling/receptivity to mating; male diurnal activity; the timing 

and frequency of mating; the duration of the mating period; moth longevity; and oviposition. We 

are also testing the effect of seasonal temperature changes on the release rate of sex pheromone 

lures to determine if second and third generation males are repelled by monitoring traps due to 

higher pheromone release rate at high temperatures.  

 

 

57 

CHAPTER 4 

 

INTRODUCTION 

 

 

RESPONSE OF PARALOBESIA VITEANA TO TEMPERATURE HELPS DETERMINE 

SEASONAL PATTERNS OF MOTH FLIGHT AND VINEYARD INFESTATION 

Most insects are ectothermic, and consequently many aspects of insect physiology, development, 

behavior and reproduction are dependent on ambient temperature (Ratte 1985, Honek 1996, 

Frazier et al. 2006). For a diverse group of insects, the rate of enzymatic processes involved in 

physiological functions such as metabolism, hormone production, and digestion approximately 

doubles for each 10°C increase in ambient temperature (Rao and Bullock 1954, Ratte 1985). The 

range of temperatures where this Q10 doubling differs somewhat between species and climatic 

regions, but is typically close to 10 to 30°C for species living in temperate zones (Nielsen et al. 

1999, Nespolo 2003). 

The effect of temperature on adult longevity has been studied in several insect orders, and 

across all taxa, longevity decreases with increasing temperature (Graham et al. 1967, Emana 

2007, Gómez et al. 2009). In field tests, Asaro and Berisford (2001) reported males of the first 

generation of the Nantucket pine tip moth, Rhyacionia frustrana (Comstock) lived significantly 

longer than males in the second and third generations. The authors also demonstrated in the lab 

that there is a significant reduction of longevity with increasing temperature. Longevity of 

codling moth, Cydia pomonella (L.) in northern European populations was about 25% shorter for 

males and females held in a warm temperature regime (18°C day and 15°C night) compared to 

those in a cool temperature scheme (13°C day and 10°C night) (Sæthre and Hofsvang 2002). 

The frequency and intensity of insect movement and activity are also dependent on 

temperature. Between critical minimum and maximum temperatures, thermal performance, 

measured as cricket (Acheta domesticus L.) running speed and jumping distance, increases with 

 

58 

temperature (Lachenicht et al. 2010). Similarly, locomotor activity of the tenebrionid, 

Gonocephalum simplex (Fabricius), increases with temperature up to a critical maximum 

temperature, and then activity decreases rapidly as the insect succumbs to heat stress (Klok et al. 

2004).  

Insect flight shows a similar response to temperature above a critical minimum and 

decreasing at temperatures at and above a critical maximum. In early studies, Taylor (1963) 

found the minimum temperature for flight to be 15.5°C for Vespula germanica (L.) queens, 

17.5°C for alates of the bean aphid Aphis fabae (Scopoli) and 16.5°C for the soldier beetle 

Rhagonycha fulva (Scopoli). However, (Taylor 1963) also found the minimum temperature for 

flight for the large bodied noctuids (~30-40mm wing span) Agrochola lychnidis (Denis & 

Schiffermüller) and Amphipyra tragopoginis (Clerck) to be considerably lower at 9 and 10.5°C, 

respectively. For smaller moths such as the tortricids (wing spans ~10-20mm) the critical 

minimum temperatures for flight are in the range of 8-15°C. For example the minimum 

temperature for flight in the eastern spruce bud worm, Choristoneura fumiferana (Clemens) is 

14°C (Greenbank et al. 1980) and it is 15 oC for oriental fruit moth Grapholita molesta (Busck) 

(Rothschild and Minks 1974). Codling moth minimum flight temperature was found to be 

12.7°C (Batiste et al. 1973), and for the light brown apple moth, Epiphysis postvittana (Walker) 

the minimum temperature for flight ranged from 8 to 11°C (Danthanarayana 1976). The critical 

maximum temperature for flight has been quantified less often, but for codling moth the 

maximum was found to be 26.7°C (Batiste et al. 1973), and for the light brown apple moth, the 

upper limit of temperatures for flight ranged from 27 to 28°C (Danthanarayana 1976). 

Oviposition is also highly dependent on temperature. In pink bollworm, oviposition 

increases 10-fold (from 22 to 236 eggs per female) between females held at 15.5°C and those 

reared at 18.3°C. Over the range from 18.3 to 26.7°C oviposition was similar (range 228 to 280 

 

59 

eggs per female). At 32°C, oviposition decreases to 157 eggs per female and at temperatures of 

37.8°C and above oviposition is less than one egg per female (Graham et al. 1967). Særthre and 

Hofsvang (2002) showed northern European populations of codling moth begin to lay eggs at 

temperatures as low as 12.3°C, and the amount of oviposition increases steadily through a range 

of temperatures ending at 25°C (the highest temperature measured). Oriental fruit moth 

oviposition is highest from 22 to 30°C, and drops off rapidly at 33°C while no egglaying is 

observed at 35°C (Notter-Hausmann and Dorn 2010). 

The influence of temperature and photoperiod on daily and seasonal cycles of growth, 

development, activity, and reproduction have been studied in several insect families (Tauber and 

Tauber 1981, Beck 1983, Régnière et al. 2012, Tonnang et al. 2017). Moths in the family 

Tortricidae have been the subjects of much of this work owing to the status of some members of 

this family as economically important fruit pests.  

In moth species where mating occurs at the beginning of the scotophase (dark phase), 

females emit pheromone (call) earlier in the day at lower temperatures. At higher temperatures, 

the female calling period is generally shorter, and occurs in the scotophase (Cardé et al. 1975b, 

Baker and Cardé 1979a, Delisle and McNeil 1987, Webster 1988). Male responsiveness to 

pheromone also occurs earlier in cool temperatures (Cardé et al. 1975a). Thus for some species 

the current air temperature, or changes in temperature, dictate when mating behaviors will occur. 

In other species, ambient temperature in the period immediately before the scotophase limit the 

periods of female calling and male responsiveness (Baker and Cardé 1979a, Haynes and Birch 

1986, Delisle and McNeil 1987). Photoperiod can also be an important cue for determining 

seasonal or daily patterns of activity (Delisle and McNeil 1987). For example decreasing day 

length in the autumn can trigger physiological changes that can alter insect development and 

trigger diapause (Riedl and Croft 1978, Gangavalli and Aliniazee 1985, Nagarkatti et al. 2001, 

 

60 

Saunders 2001). Photoperiod can influence mating behavior, although relatively few studies have 

examined the effect of day length on mating, and the effect varies across species and sexes. As 

day length decreases, the female calling period is lengthened (Kanno 1981, Gerber and Howlader 

1987), but decreasing day length in the late summer and fall reduce male responsiveness to sex 

pheromone (Delisle and McNeil 1986, 1987, Mulder et al. 1989). In cases where there is an 

effect of photoperiod on either male or female mating behavior, the effect is typically minor 

compared to the effect of temperature (McNeil 1991).  

Identification of the patterns of daily mating activity can inform other management 

approaches such as mating disruption, mass trapping and attract and kill (McNeil 1991, El-Sayed 

and Suckling 2005, El-Sayed et al. 2006, 2009, Baker 2009, Rodriguez-Saona and Stelinski 

2009). For example, in mating disruption of some tortricid pests, automated pheromone 

dispensers can be programmed to emit pheromone only during the period when females are 

calling, and this could reduce the costs of deploying mating disruption (Isaacs et al. 1999, 

Fadamiro and Baker 2002, Stelinski et al. 2007a, Jones and Wiman 2012). 

In developing sex pheromone lures for monitoring, the optimal amount of pheromone to 

use in a lure is often determined by comparing male captures in traps that contain a range of 

concentrations of an active compound (Roelofs et al. 1969, 1971, Witzgall et al. 2000, Suckling 

et al. 2005). Traps with too low of a pheromone concentration will not be attractive to males and 

lower captures will result (Roelofs et al. 1971, Taschenberg et al. 1974, Linn and Roelofs 1995). 

In addition, the rate of pheromone release from lures increases with increasing temperature 

(McDonough et al. 1989), and increased pheromone release at high temperatures may also 

suppress male catch in periods of hot weather (Sanders 1981, Cork et al. 2003, Cork 2016, Cardé 

et al. 2018). In this study, the effect of temperature and photoperiod on the behavior of P. viteana 

were investigated to determine how daily periods of mating activity and reproductive behaviors 

 

61 

change during the growing season, and how these changes can influence P. viteana phenology. 

This is an essential component of integrated management of tortricid pests (Riedl et al. 1976, 

Damos and Savopoulou-Soultani 2010, Jones and Wiman 2012), yet little is known about the 

role of temperature and day length in P. viteana. 

The grape berry moth, Paralobesia viteana (Clemens) (Lepidoptera:Tortricidae), is a 

specialist herbivore found in woods and vineyards across eastern North America, feeding 

primarily on wild and cultivated plants in the genus Vitis (Johnson and Hammar 1912). This 

moth is a primary pest of cultivated grapes (V. labrusca L. and V. vinifera L. and their hybrids), 

and it has challenged grape growers since the beginning of commercial grape production in this 

region (Johnson and Hammar 1912, Hoffman et al. 1992, Isaacs et al. 2012b). 

 

Flight activity of male grape berry moth can be monitored using traps that contain lures 

baited with synthetic sex pheromone, but the males of this species are only captured in 

pheromone traps consistently during the first generation that is active around bloom. The first 

generation causes little larval feeding damage, but in the second and third generations in the 

early and late summer, respectively, the level of oviposition on berries, and subsequent larval 

infestations increase greatly, yet few males are caught in monitoring traps (see Chapter 1, Figure 

1.3) (Snyder et al. 1992, Teixeira et al. 2009, Isaacs et al. 2012b). This complicates P. viteana 

management because action thresholds based on captures of male moths cannot be used for all 

generations as has been done for other lepidopteran fruit pests (Binns and Nyrop 1992, Bradley 

et al. 1998, Reddy and Manjunatha 2000, Knight and Light 2005a). Exploring factors that affect 

male captures of this species will inform decision-making about the need for treatment and the 

development of lures or trapping strategies that improve moth monitoring could lead to better 

timing of insecticide applications or other management strategies. 

A model was developed to predict how different temperatures during the three grape 

 

62 

berry moth generations produce the observed pattern of P. viteana phenology (Figure 4.1). Male 

response through the diurnal cycle is shown by the solid black lines, and it is assumed that the 

period of this response changes little between the three generations. The period of female calling 

changes with temperature and is the shortest when temperatures are the lowest, during 

Generation 1. The female calling period is expected to be longest in the second generation 

(Figure 4.1) when temperatures are the highest. The area between the lines of male response and 

female calling indicates the time that males are responsive to pheromone and females are not 

emitting pheromone. This is the period when males would be most likely to be caught in traps, 

and this would the longest in Generation 1 (Figure 4.1). Thus this model predicts the highest 

male catch in this generation. Conversely, the lowest number of males would be caught in 

Generation 2 (Figure 4.1) because females are calling for the entire period that males are 

responsive, and traps would thus be in competition with calling females as is seen the tea tortrix 

(Noguchi and Tamaki 1985) and spruce budworm (Palanisawamy and Seabrook 1978, Sanders 

1987). Male capture in Generation 3, would be lower than in Generation 1, but higher than in 

Generation 2. This is expected to occur because the lower temperatures during this time would 

create periods in Generation 3 when males are responsive but females are not calling. Thus the 

effect of temperature on female calling period may be responsible for reduced male captures 

  

 

63 

Photophase 

Scotophase 

Figure 4.1 Model of changing female pheromone production (purple dashed line) 
and male response to pheromone (solid black line). The gray rectangle denotes the 
dark phase of the light cycle. The area between the purple dashed and solid black line 
represents the proportion of time males are receptive to pheromone, but females are 
not emitting pheromone (i.e. not receptive to mating).  

 

64 

during the second and third grape berry moth generations that occur in the middle and late 

season, respectively.  

 

The purpose of this study was to determine the roles of temperature and day length in the 

levels and timing of mating behavior, oviposition, and activity of P. viteana and to ascertain 

whether these relationships explain the phenology observed in Michigan vineyards. My research 

focused on the following eleven questions: 

1) How are longevity, flight ability and oviposition affected by temperature? 

2) Does the frequency of mating or male flights increase with temperature?  

3) Does the time of first mating or the time of first male flight change with temperature?  

4) Do the durations of the mating period and the period of male flight vary with temperature?  

5) Are there more male flights when females are not receptive in colonies reared at low 

temperatures than in colonies reared at high temperatures?  

6) Does day length affect the frequency of mating frequency of male flights, the time of first 

mating or the time of first male flight, the duration of the male flight or mating period?  

7) Does day length affect the number of male flights when females are not receptive?  

8) Do diurnal temperature regimes affect timing or duration of mating period and male flights?  

9) Do diurnal temperature regimes affect the proportion of male flights that occur when females 

are not receptive to mating?  

10) Does the rate of pheromone release from lures change with temperature?  

11) Do high pheromone release rates reduce male capture? 

 

 

65 

 

To determine a range of temperatures for testing their effects on mating behaviors, average daily 

METHODS 

 

temperatures were determined for April to September based on 2010-2014 weather data from 

Lawton, Michigan (enviroweather.msu.edu). Those values were used to choose the temperatures 

used in all experiments (Table 4.1). I also selected day length values that encompass the range of 

day lengths in Michigan during the growing season (Table 4.1).  

 

 

 

 

 

 
 
 
Insect rearing 

Temperature °C SEM Day length* 

Table 4.1 Average daily temperatures and day lengths for 
April to October 2010 – 2014 for Lawton, Michigan. 
Month 
0.9 
April 
0.4 
May 
0.3 
June 
1.2 
July 
0.4 
August 
September 
0.3 
*Day length on 15th day of the month 

13:22 
14:35 
15:15 
14:58 
13:53 
12:30 

9.1 
16.1 
20.5 
22.8 
21.4 
16.7 

Insects used in these experiments were obtained from a colony of freely mating P. viteana that 

has run continuously for over a decade. The rearing methods were based on those of 

(Taschenberg 1951, 1969). Paralobesia viteana infested fruit was collected from multiple 

agricultural and natural sites in Berrien and Van Buren counties in southwest Michigan and 

adults reared from these collections were used to start the colony. In the summer and fall of each 

year, individuals from similar collections were added to the colony to reduce potential selective 

effects of laboratory rearing (Chambers 1977, Cha, et al. 2008a). Adult moths (100 – 400 

individuals in a 50:50 sex ratio) were held in 30cm3 Bugdorm-1 cages (MegaView Science Co., 

Ltd, Taichung City, Taiwan) and reared in a walk-in chamber set at 28°C; 60-75% RH and a 

17L:7D light cycle. Deionized water and a 10% sucrose solution were provided ad libitum in 200 

 

66 

ml glass bottles each containing a 15 cm piece of dental wicking (Absorbal Inc. Wheat Ridge, 

CO, USA) and sealed with Parafilm so that a 3 cm piece of wicking extended above the 

bottleneck. Fluorescent lamps provided all lighting in the rearing chamber except for two 10W 

incandescent bulbs that were continually illuminated to provide twilight conditions to encourage 

mating and egglaying in the colony chambers during the scotophase. To provide oviposition sites 

and food for hatching larvae, I used fresh seedless grape clusters that were purchased weekly 

from a local grocer. To prepare them for the colony, I soaked the clusters for 5 min in 5% bleach 

solution, and then rinsed exhaustively and allowed them to air dry. Three times per week, 2 to 3 

grape clusters (300-400g total) were hung in the rearing chambers and the previous set of 

clusters were removed and placed in 17L plastic rearing bins with fine nylon mesh lids. The 

grapes were placed in the bins on 25 x 30 x 5 cm platforms made from aluminum metal mesh 

with 0.64cm2 openings. Pieces of cellulose sponge (5 x 8cm) that were placed under the metal 

mesh absorbed liquid that leaked from the grapes. Ten to fifteen strips of clear plastic (2 x 10cm) 

were placed on the bottom of the bin and around the grapes to provide pupation substrate for 

mature larvae that leave the clusters. Rearing bins were held in the same walk-in chamber as the 

adult cages. After 2-3 weeks mature larvae start to drop from the fruit and form a pupal cocoon 

by cutting a small disc from a plastic strip and wrapping themselves up and sealing it using 

salivary silk. These pupae were then collected every two or three days and put in small bins until 

the adults emerged. Adults were aspirated out of these bins and divided up among the active 

oviposition cages. 

 

Moth longevity  

To quantify the effect of temperature on moth longevity, pupae from the colony were placed in 

29.6ml plastic deli cups (Solo, Urbana, IL, USA). A 1cm piece of moist dental wicking 

 

67 

(Absorbal, Wheat Ridge, CO, USA) was placed in the cup, and was covered with a perforated lid 

and held at 28°C, 60% RH and 17L:7D until adults emerged. Newly emerged moths were then 

moved to an environmental chamber set at either 10°C, 18°C or 28°C, and 60% RH and 17L:7D. 

Moths were checked daily for viability and touched with a small paintbrush to determine if they 

were still alive. At least 15 (maximum 34) replicate moths of each sex were assessed at each 

temperature. The sex of each moth and the number of days from emergence to death were 

recorded, and their longevity was compared between the sexes and across temperatures with a 

two way analysis of variance (ANOVA) followed by means separation with Tukey’s Honest 

Significant Difference test (HSD) (JMP 13.1.0, SAS Institute. Cary, NC). 

 

Minimum flight temperature 

The minimum temperature required for flight by male and female P. viteana was determined 

using a catapult to propel moths into the air at different temperatures and record their flight 

behavior. This experiment was performed in a walk-in environmental chamber that was set to 

temperatures between 10 and 19°C and under 50-60% RH, fluorescent lighting on a 17:7 L:D 

cycle.  

The catapult (Figure 4.2) was constructed from a 42 x 24 x 2.5cm wooden platform, and 

a 4.5 x 23 x 0.2cm strip of semi- rigid plastic with one end attached to the platform with wood 

screws. The other end of the plastic strip was raised above the platform using a large binder clip 

attached to the platform with wood screws so it was positioned underneath the strip to serve as a 

fulcrum. This allowed the suspended end of the plastic strip to be pressed down to a standard 

height above the platform (3cm). An inverted 29.6ml plastic deli cup was glued to the platform 

so the strip could be set before releasing the strip to launch a moth into the air. A scintillation 

 

68 

vial cap was glued to the upper side of the suspended end of the strip to serve as a holding basket 

for a moth before it was launched.  

Before testing, one to five day old moths from the colony were held in an environmental 

chamber at 10°C, 75% RH and 17:7 L:D in individual 29.6ml (1oz) plastic deli cups (Solo, 

Urbana, IL, USA) containing moist cotton wicking and covered with a perforated lid. On the day 

of testing, moths were held in the walk-in chamber at test temperatures for at least 30 min prior 

to measurement to allow their bodies to equilibrate with that temperature. I launched individual 

moths at temperatures between 10 and 19°C at 0.5°C increments starting at the lowest 

temperature to be tested. In total, 147 female and 155 males were tested and at least 5 moths of 

each sex were tested at each temperature during each round of tests.  

 

Figure 4.2 Catapult used to propel moths into the air at 
different temperatures to determine the lower temperature 
threshold for flight. Inset in upper left shows a moth ready to 
be launched. 

 

 

69 

For each moth, I classified the flight behavior as either: 1) Glide – following a parabolic 

path without moving wings. 2) Flutter – wing movement is visible but moth follows a parabolic 

path without a change of direction. 3) Partial – wing beating is visible and moth flight veers from 

the parabolic path, or changes direction, but sustained or upward flight is not seen. 4) Full – moth 

shows wing flapping and non-parabolic upward or extended flight.  

The threshold temperature for flight was defined as the temperature at which 50% of 

moths were able to fly (FT50). I determined the FT50 by fitting a line to the average proportion of 

moths that were able to fly in the range of 14°C to 16°C, and calculated the FT50. This was 

determined separately for males and females, and I pooled male and female flight data to 

determine the FT50 for all moths. 

 

Oviposition  

The effect of temperature on P. viteana oviposition was determined using a series of bioassays in 

mesh cages made by rolling a 30 x 60cm piece of aluminum window screen into cylindrical 30 x 

15cm diameter mesh cage. The vertical seam of the cage was sealed with hot glue and the cage 

was covered on the top and bottom with 15cm plastic Petri dishes. I placed five female and five 

male 3 to 5 day old lab reared P. viteana adults along with three table grapes into the cages. 

Grapes were either threaded on a wire, fixed in place by applying hot glue between the grapes 

and then suspended in the middle of the cage, or they were glued, stem end down, onto a 6cm 

Petri dish and placed on the cage bottom. I randomly assigned cages to one of three different 

temperature treatments, and placed them in environmental chambers at 10, 18 or 28°C with 60% 

RH and a 17L:7D light cycle, and with lighting provided as described above. The trial using 

grapes suspended in cages was replicated at least 27 times at each temperature, and the trial 

where grapes were placed on the cage floor was replicated 10 times at each temperature. After 48 

 

70 

hours the berries from each cage were removed and, using a dissecting microscope, the number 

of eggs were counted and recorded. I compared the average number of eggs laid per female 

among temperatures with one-way ANOVA followed by means separation with Tukey’s Honest 

Significant Difference test (JMP 13.1.0, SAS Institute. Cary, NC). I did this separately for cages 

with grapes suspended and those with them on the bottom. 

 

Duration and frequency of the mating period and male flight period 

To determine whether the frequency, timing and length of the mating period, or the male flight 

period are affected by temperature, day length or patterns of diurnal temperature changes, I 

conducted timed observations of freely mating P. viteana moths in colonies held under specific 

conditions. A colony consisted of 150 to 200 adults with an approximate 1:1 sex ratio held in a 

30cm3 Bugdorm-1© clear plastic cage with mesh walls (MegaView Science Co., Ltd, Taichung 

City, Taiwan). Newly emerged moths were added to the rearing cages and dead moths were 

removed every other day to keep colonies at a standard density of 150 to 200 moths. Fresh 

seedless table grapes, water and sucrose solution were available in the colony, and these were 

replaced and handled as described above.  

Experimental conditions were similar to the conditions for colony rearing described 

above except that I varied temperature or day length according to experimental requirements. I 

used walk-in (EGC, Chagrin Falls OH, USA) and reach in (Percival Scientific, Perry IA, USA) 

environmental chambers so that I could collect data simultaneously from multiple colonies under 

different conditions. I kept the intensity of light at comparable levels between all chambers (550 

lux - light phase, 0.5 lux - dark phase).  

The insects in the cages were video recorded during different temperature and day length 

regimes through multiple daily cycles using Panasonic HC-V160 (Panasonic Corp. Newark, NJ, 

 

71 

USA) portable camcorders with low light recording capabilities. I was not able to record at all 

hours of the daily cycle in a single recording session due to video memory and staffing 

constraints, so to ensure that data were collected during each hour of the 24-hour cycle, I 

periodically shifted the start of the dark phase in the rearing chambers by 6 or 12 hours. Colonies 

were allowed to acclimate to new conditions for 3 to 5 days before video recording. I 

standardized the time of observations relative to the dark phase of the sampling period by 

subtracting the time the sample occurred from the start time of the dark phase using this simple 

equation: Trdp = 24 – (Tdp - Ts). Where Trdp is time relative to dark phase, Tdp is the time the dark 

phase starts, and Ts is the time the sample was taken. To simplify data interpretation by humans, 

all times were then standardized to a 24 hour cycle in which the dark phase began at 20:00. 

The video recordings were sampled at approximately 30 min intervals by replaying the 

recording and observing the colony for 30 second samples. I used Windows Media Player 

version 10 or VLC Media Player version 2.26 for video playback, and made a minimum of 12 

samples from different cages of moths for each hour and temperature or day length combination. 

At each 30 second sample, the number of mating pairs, the number of male flights, and the time 

that each sample was taken (calculated from the video file information and the video timer) was 

recorded. Similarly, the start and end of the dark phase of the light cycle was recorded from the 

video timer. For each recording session, mating pairs and male flights were averaged for each h 

of observation to yield matings per hour (mph) and flights per hour (fph). Observations that 

occurred during the 24h period from 12:00 on the first day of recording to 11:59 the following 

day were grouped into replicates for statistical analyses. I counted all observed flights as male 

flights based on the results of a pilot test where I used 5 P. viteana colonies and captured 10 

moths in each colony that were flying during the scotophase. Captured moths were anesthetized 

 

72 

with CO2, and after examination using a dissecting microscope, all of the captured moths were 

determined to be male.  

The data collection protocol described below was used for all observations in three 

experiments. In the first experiment, the effect of temperature on male flight and mating 

frequency and period was tested by placing colonies in environmental chambers set at constant 

temperatures of 10, 15, 18, 23, 28 or 35°C, 60% RH and a 17L:7D light cycle. In the second 

experiment the effect of day length on moth mating and male flight was tested by placing 

colonies in chambers set at 28°C and 60% RH and programmed with either a long, 17 hour 

light:7 hour dark (17L:7D), moderate (14L:10D), or short (12L:12D) day length regime. In the 

final set of experiments, colonies were observed under three diurnal temperature regimes that 

were loosely based on temperatures that occur during the growing season. The diurnal regimes 

consisted of a hot weather cycle (28°C day - 18°C night), a warm weather regimen (28°C day - 

10°C night) and a cool weather treatment (20°C day - 10°C night), and all colonies experienced 

the same photoperiod 17L:7D and 60% RH. This was repeated for 3 colonies and each one 

received one of the three diurnal weather treatments on successive weeks, and I randomized the 

order that the diurnal temperature regimes were presented. For each of the three experiments 

explained above, I compared the start time, end time, length of the mating period and mating 

frequency across temperature, day length and diurnal pattern treatments in experiment sets 1, 2 

and 3, respectively, with one-way ANOVAs followed by Tukey’s HSD for mean separations. I 

did similar comparisons of start time, end time, period length and frequency for male flight 

activity in those same experiments. In all analyses, data were square root or natural log 

transformed as needed to stabilize error variance and to meet the assumptions of analysis of 

variance (ANOVA). In cases where transformations did not satisfy the assumptions of ANOVA, 

a Wilcoxon ranked sums test was used on untransformed data to determine if treatment 

 

73 

differences existed, and to separate the mean treatment effects (JMP 13.1.0, SAS Institute. Cary, 

NC). Specific transformations that were used for statistical analyses are reported in the Results 

section.  

To determine how often male flights occurred when females were not receptive to mating 

(i.e. outside of the mating period), I calculated the proportion of all male flights and mating pairs 

that occurred during each hour of the 24 cycle for each experimental treatment. These data were 

graphed together by treatment, and then the area under each portion of the graph where male 

flight occurred but mating pairs were not observed was integrated using Microsoft Excel. For 

each experiment (constant temperature, day length or diurnal temperature regime), I then 

compared the proportion of male flights in each treatment that occurred outside of the mating 

 

period across treatments using the comparison of multiple proportions test (Zar 1999). These 

proportions will be discussed as percentages for clarity. 

 

Response to pheromone lures at different times of the season 

A field trial to test the response of male P. viteana to sex pheromone lures at different times of 

the season was conducted from May to October 2017. Lures with custom pheromone loads were 

made for this experiment using a 10:1 ratio of analytical grade (Z)-9-dodecenyl acetate and (Z)-

11-tetradecenyl acetate (Bedoukian, Danbury, CT, USA). I first mixed stock solutions of 300 and 

500µg/ml using hexane as the solvent, and then further diluted these with hexane to yield loading 

solutions of 60, 300, 400 and 500µg/ml (Table 4.2). Small rubber septa (West  

 Pharmaceuticals, Exton, PA, USA) were arranged open side up in aluminum mesh racks with 

0.64 cm2 openings and filled with either 0.20 ml or 0.25ml of the approriate dilution to produce 

lures loaded with 0, 15, 60, 75, 100 or 125 µg of P. viteana pheromone. 

 

74 

 The mesh racks were held in a fume hood until the solutions evaporated. An additional 

0.25ml of hexane was then pipetted into each septum to help the pheromone adsorb onto the 

septum wall. The lures were dried in the fume hood and then grouped by pheromone load and 

each group was placed in a separate 200ml labeled glass jar, sealed with teflon tape and stored in 

a freezer (-5°C) until the lures were deployed in traps.  

 

 

 

 

 

 
 
 
 

Stock solution 

(µg/ml) 

Dilution 
factor 

(µg/ml) 

Loading 

aliquot (ml) 

Loading concentration

Table 4.2. Stock solutions, dilutions and loading volumes to make lures for 
field testing. 
Lure load 
(µg/lure) 
0 
15 
60 
75 
100 
125 

    0 
300 
300 
300 
500 
500 

  0 
60 
300 
300 
500 
500 

1 
5 
1 
1 
1 
1 

0.25 
0.25 
0.20 
0.25 
0.20 
0.25 

The field trial to test the response of male P. viteana to traps baited with different 

pheromone loads was performed in seven juice grape vineyards in Lawton, Michigan. Each 

vineyard had a history of grape berry moth infestation and was adjacent to a woodlot containing 

wild grape (Vitis spp.). At each site, the trial was established along a 50m section of vineyard 

border adjacent to a woodlot. All vineyards were planted on single wire, top-cordon trellis, with 

3 or 3.5m between vineyard rows and 3 or 3.5m between vines. Six vineyard posts situated at 

least 10m (3 rows) apart and along the border were flagged and these locations were used to 

hang traps throughout the season. To record the temperature and calculate accumulated growing 

degree days at each site, a Hobo UA-001-08 data logger (Onset Computer Corp., Bourne, MA, 

USA) was hung on the inside of an inverted 240ml (8oz) white styrofoam cup and suspended 

from the trellis wire 1.7m (5.5ft) above the ground. Hobo data-loggers were deployed at the 

approximate center of the 50m section of vineyard border used for this experiment. White 

 

75 

Pherocon VI large plastic delta traps (Trece Inc., Bend, OR, USA) were baited with one of the 

lures listed in Table 4.2. A 4cm sewing pin was inserted through the side wall of each trap and a 

lure was skewered on the pin and held near the middle of the open space inside the trap. Sticky 

trap liners were inserted into the bottom of baited traps and these were then hung on the vineyard 

trellis wire. Traps were removed from the trellis each week and the number of P. viteana males 

captured on the sticky trap liners were recorded. Trap liners were replaced, and the relative 

location of the traps was re-randomized before the traps were reattached to the trellis wires. 

Traps were set up on 9 May (early vine growth) and removed from the vineyards on 14 

November 2017 (postharvest). Lures were changed approximately every 3-4 weeks, except that 

one set of lures was deployed for 8 weeks during the harvest period in September and October. 

The length of time each lure set was deployed constituted a trapping period, so there were five 

trapping periods (May, June, July, August and September/October). As the length of the trapping 

period was not the same for all lure sets, prior to analysis, male captures were divided by the 

number of days in the trapping period to give captures per day.  

For each lure change, the jars of lures described above were transported to the field in a 

cooler filled with ice packs. After traps were checked, the used lures were removed, placed 

separately in labeled 29.34 ml plastic deli cups (Solo, Urbana, IL, USA), and a new lure of the 

same pheromone load was hung on the pin inside the trap. The cups with used lures were then 

placed in a cooler, returned to the laboratory and stored in a freezer (-5°C) until the pheromone 

in the lures could be extracted and analyzed using GC-MS. Nitrile gloves were used for all trap 

and lure handling, and gloves were changed between checking individual traps and between 

changing different lures. 

To estimate the quantity of pheromone released from lures during each trapping period, I 

soaked each lure in 5 ml of hexane in individual 20ml glass scintillation vials (RPI, Mt. Prospect, 

 

76 

IL, USA), for 10 days to extract the pheromone remaining in the lure. For each lure set, one 

unused lure from each level of lure load was selected to be used as a control on the day that the 

extractions were set up, and the pheromone was extracted using the same method. A one ml 

sample of solvent from each lure extraction was then pipetted into separate 2ml clear glass screw 

top GC vials (Wheaton, Millville, NJ, USA). To calculate the concentration of target compunds 

in each sample, a 50µl aliquot of methyl myristate (methyl tetradecanoate) (Bedoukian, Danbury, 

CT, USA) in hexane (500µg/ml) was added to each GC vial as an internal standard with a final 

concentration of 25µg/ml (Rodriguez-Saona and Stelinski 2009). The amount of pheromone in 

each lure was analyzed using an Agilent 7890A gas chromatograph (GC) paired with an Agilent 

5975C mass spectrometer (MS) (Agilent Technologies, Santa Clara, CA, USA) following the 

methods reported in Hufnagel et al. (2017). An Agilent HP-5 column (30m length, 0.320mm ID, 

film thickness 0.25µm) was used for all GC-MS analyses with helium used as the carrier gas at 

30cm s-1 flow velocity. Aliquots (1 µl) of each sample were injected into the GC-MS and 

separated using a program of 1 min at 40°C followed by increasing temperature at a rate of 10°C 

min-1 to 260°C. Isobutane was used as the reagent gas for chemical ionization. Ion source 

temperature was 250°C in chemical ionization mode and was 220°C in electron impact mode. 

GC-MS results were analyzed using MSD ChemStation v.2.00 (Agilent Technologies, Santa 

Clara, CA, USA). (Z)-9-dodecenyl acetate, (Z)-11-tetradecenyl acetate and methyl myristate 

were identified from the samples by comparing the mass spectrum of each compound to those in 

a reference library, NIST 11 (National Institute of Standards and Technology, Springfield VA, 

USA). Compound identifications were confirmed by analyzing standard solutions of single 

compounds and mixtures of (Z)-9-dodecenyl acetate, (Z)-11-tetradecenyl acetate and methyl 

myristate with concentrations ranging from 0.5 to 500µg/ml using the GC method described 

above to determine retention times, and the range of response for each of these compounds. The 

 

77 

amount of each target compound in each sample was then calculated using the ratio of the peak 

area of that compound to the peak area of the known amount of internal standard in the sample 

using this equation:  

Amount of compound A(µg) = (Peak area A/Peak area IS) x [IS] (µg/ml) x extraction volume 

(ml). 

I then determined the amount of pheromone components, (Z)-9-dodecenyl acetate and 

(Z)-11-tetradecenyl) released from each lure during the trapping period by subtracting the 

amounts of these compounds in the lure sample from the average amounts of these compounds 

extracted from the corresponding unused control lures. Only the major component, (Z)-9-

dodecenyl acetate was used in subsequent analyses because the GC-MS was not able to 

accurately measure the very low amounts of the minor pheromone component, (Z)-11-

tetradecenyl acetate) in these samples. The amount of (Z)-9-dodecenyl acetate released was 

calculated as the difference in the mass of pheromone in the deployed lures and the average mass 

in the undeployed control lures. As the length of the trapping period was not the same for all lure 

sets, values are presented as µg released per day.  

To test the effect of different lure load treatments on the total number of males captured 

in a trapping period and all season, I used a mixed model ANOVA with male captures/d as the 

dependent variable, vineyard as a random or blocking factor and lure load as a fixed factor. In 

this analysis vineyards were considered replicates, and a separate analysis was performed for 

each trapping period. The mixed model analysis was followed by mean separation with Tukey’s 

Honestly Significant Difference test (JMP 13.1.0, SAS Institute. Cary, NC).  

To determine the relationships between male captures and pheromone release at different 

times of the season, I first regressed the average captures for each lure load on the average 

amount of pheromone released from those lures during each sampling period. To determine if the 

 

78 

relationship between captures and pheromone release was similar during different times of the 

year, I used analysis of covariance with male captures as the dependent variable, pheromone 

release as the main factor and sampling period as the covariate, and this analysis was followed 

by Tukey’s HSD on least square means for sampling period to detect differences in the effect of 

pheromone release on captures across periods. As male capture is likely to be correlated with 

both temperature and pheromone release, I used residual regression analysis to tease apart the 

relationship between moth captures, pheromone release and temperature. I first used linear 

regression to determine the relationships between captures and pheromone loss and captures and 

temperature. I used growing degree day (GDD) accumulations based on the developmental 

threshold for P. viteana of 8.41°C (Tobin et al. 2001) as the measure of temperature. GDDs are a 

sum of accumulated heat during a sample period, and this better represents the totality of 

temperature conditions that lures and moths experienced during a sample period than does 

average daily temperature. I used averages pooled across replicate vineyards of male captures 

and pheromone release for each lure load/sampling period. I saved the residuals from the 

regressions of captures on GDD8.41°C and from the regression of pheromone release on 

GDD8.41°C. By regressing these residuals, the effect of pheromone release on captures was 

assessed with the effect of temperature removed (JMP® 13.1.0., SAS Institute, Cary, NC, USA). 

 

79 

Moth longevity  

RESULTS 

Average P. viteana longevity was 57.5 ± 3.5 days at 10°C, 17.8 ± 0.9 days at 18°C, and 8.9 ± 0.7 

days at 28°C. This represents an almost six-fold decrease in survival length from lowest to the 

highest temperature; and, moths held at 18°C lived twice as long as those held at 28°C. There 

was a strong statistically significant effect of temperature on longevity, and the effect was similar 

for males and females (F1,136 = 0.0006; P = 0.94, log transformed data). Longevity data were 

pooled for the two sexes for one-way analysis of variance (Figure 4.3). Longevity at 10°C was 

significantly longer than at 18°C, and longevity at 18°C was significantly lower than at 28°C  

(F2,135 = 134.0; P < 0.0001, log transformed data, Figure 4.3). 

a 

Figure 4.3. Longevity of moths held at different temperatures. Survival of males 
and females were not significantly different so data from the sexes were pooled, 
and all data were log transformed before analysis. Columns headed with different 
letters are significantly different (P < 0.05).  

 

 

80 

Minimum flight temperature 

Male and female P. viteana showed similar characteristic flight behaviors when launched into 

the air at different temperatures (Figure 4.4). They were unable to fly at temperatures below 

11°C, and at this temperature all launches resulted in gliding on a parabolic path in the vertical 

plane of the launching strip, with no wing movements. In the range from 11 to 13.5°C, 

catapulted moths displayed wing movements and fluttering flight, without deviating from a 

similar parabolic trajectory. Partial flight, where moths were able to move their wings  

(a) 

(b) 

 

 

 

81 

sufficiently to change direction from the normal parabolic path but without powered level or 

upward movement, occurred from 13°C to 15.5°C for female moths and from 13.5°C to 16.5°C  

for males. Full powered flight, where moths were able to change direction and fly upward or  

 

Figure 4.5. Average proportion of female and male P. viteana that exhibited full flight 
in the temperature range 10 to 19°C. The solid line indicates the line of best fit for 
pooled male and female data. The vertical dashed line shows the FT50 for all moths 
(pooled) is estimated to be 15ºC. 

level after launch was first seen at 14.5°C for both sexes. The FT50 or the temperature at which 

50% of moths were able to fly upward, level or change direction after launch, was determined to 

be 15°C for males and 14.9°C for females (Figure 4.5).  

 

 

 

 

82 

Oviposition  

Paralobesia viteana female moths held with grapes suspended in cylindrical cages laid 

significantly more eggs on grapes at 28°C than at either 18°C or 10°C (χ2 = 69.3, P <0.0001). At 

28°C, 4.5 ± 0.8 eggs were laid per female, while at 18°C there was less than one egg per female 

(0.05 ± 0.05). Female moths maintained at 10°C did not oviposit. In trials with grapes affixed to 

a Petri dish that was placed on the cage floor, the results were very similar to the experiment 

above, as temperature had a strong significant effect on oviposition (F2,27= 25.8; P < 0.0001, log-

transformed data). At 28°C, I found females laid an average of 7.9 ± 1.6 eggs per moth, and that 

was reduced to 1.4 ± 0.7 eggs per female when cages were held at 18°C. No eggs were laid on 

grapes in the 10°C cages (Figure 4.6).  

(a) 

(b)

TemperatureºC 

Figure 4.6 Oviposition at different temperatures in bioassay cages with (a) grapes 
suspended, or (b) attached to the floor of the cage. Columns with the same letter within 
each graph are not significantly different (P > 0.05).  

 

83 

Diel patterns of mating and male activity in colonies 

Constant temperature. In colonies held at constant temperatures, the frequency of mating, 

expressed as matings per hour (mph) averaged over the entire 24-hour cycle, ranged from 0.01 

mph at 10°C to 0.52 mph at 28°C. This is an exponential increase from 10 to 28°C, but mating 

frequency was reduced at 35°C (Figure 4.7a). At 28°C the frequency of mating was significantly 

higher than mating at any of the other temperatures (χ2 = 62.9, P <0.0001, Figure 4.7a). The 

number of male flights observed per hour (fph) also increased significantly in the range of tested 

temperatures (F4,122 = 27.9; P <0.0001, log transformed data, Figure 4.7b). The frequency of 

male flights ranged from 0.001 at 10°C to 9.8 fph at 28°C, and there were significant differences 

in male flight frequency between treatments. 

(a) 

(b) 

b 

Figure 4.7. Effect of temperature on mating frequency (a) and flight frequency (b) in colonies held 
at different temperatures. Data are the average number of behaviors observed per hour averaged over 
all sampling hours. Points with different letters are significantly different (P < 0.05). Only one flight 
was observed in colonies at 10ºC so those data were excluded from the analysis. 

 

             

 

 

84 

Across all temperatures, the average time of the first observed mating pair occurred during 

the dark phase (20:00 to 03:00), and this time ranged from 21:26 to 0:34. Despite this large 

range, temperature had no significant effect on the time of first mating (F5,102 = 2.29; P = 0.052, 

log transformed data, Figure 4.8a). The average time of the first male flight ranged from 06:59 to 

14:14, and thus occurred much earlier in the day than the first mating (Figure 4.8b). Significant 

differences among temperature treatments were detected in the time of first male flight (χ2 = 

17.3, P = 0.0017, Figure 4.8b). Flights began significantly later in colonies reared at 23°C and 

35°C compared to flights in colonies held at 18°C or 28°C. The last mating pair was observed  

(a) 

(c) 

 

C
°
 
e
r
u
t
a
r
e
p
m
e
T

 

 

 

 

 

 

 

 

 

 

 

 

(b) 

(d) 

Time of occurrence ± SEM

 
Figure 4.8. Average time of the first observation of mating pairs (a) and male flights (b), and 
average time of last mating pair (c) and male flight (d) in colonies reared at different 
 
temperatures. Times of first and last behaviors were averaged over all days where at least 2 
behaviors were observed in the 24 h period from 12:00 on the first day of recording to 11:59 
the following day. Male flight data from colonies reared at 10ºC were not included in the 
analysis because only one flight was observed across all samples. In each graph, columns 
with different letters are significantly different (P < 0.05).  

85 

 

 

from 03:09 to 06:22, and mating was observed significantly later in colonies reared at 28°C 

compared to colonies held at 23°C or 15°C. The last mating in colonies held at 18°C occurred 

later than in colonies reared at 15°C (F5,102 = 5.51; P = 0002, log transformed data, Figure 4.8c). 

The average time of the last male flight ranged from 09:18 to 17:30, and there were no 

significant differences among temperature treatments (F4,97 = 1.97; P = 0.10, log transformed 

data, Figure 4.8d). 

The average duration of the mating period ranged from 69 minutes at 10°C to 294 minutes at 

28°C and there was a significant effect of temperature on the duration of the mating period (F5,102 

= 5.7, P <0.0001, log transformed data, Figure 4.9a). The mating period was significantly longer 

at 28°C than at 10°C, 15°C or 18°C. Temperature significantly affected the duration of the male 

flight period (F4,98 = 5.11, P  = 0.0009, log transformed data, Figure 4.9b). Male flight period  

Temperature˚C

Figure 4.9. Average duration of the mating period (a) and flight period (b). In each graph, 
columns with different letters are significantly different (P < 0.05). The flight period was 
significantly longer than the mating period for all temperatures except 15ºC (P < 0.05). See 
text for statistics. Male flight data from colonies reared at 10ºC were not included because only 
one flight was observed across all samples.

 

86 

duration ranged from 0 to 1147 minutes, and flight period duration for colonies held at 18, 23, 28 

and 35°C were all significantly longer than for colonies reared at 15°C (Figure 4.9b). Figure 4.9 

shows that the male flight period was longer than the period when mating pairs were observed. 

For all constant temperature treatments except 15°C, the flight period was significantly longer 

than the mating period (15°C - F1,18 = 1.09, P = 0.3107; 18°C -  F1,33 = 30.5, P <0.0001; 23°C -  

F1,42 = 14.5, P = 0.0005; 28°C -  F1,85 = 5.5, P = 0.0215; 35°C -  F1,20= 12.8, P = 0.0019; all 

analyses used log transformed data). The duration of the mating period and flight period at 10°C 

was not used in the analysis because only one male flight was observed.  

Table 4.3. Summary of mating and male flight measurements for colonies held at 
constant temperatures. Values in the same column with different letters are significantly 
different (P < 0.05). 
Temp 
°C 

Proportion 
male flights 

Hours 
observed

Hours 
observed

mph* 

fph** 

# times 
behavior 
observed 

# times 
behavior 
observed

outside 
mating 
period 

1 

10 
15 
18 
23 
28 
35 

 0.01 
0.03 b 
0.04 b 
0.14 a 
0.52 a 
0.06 b 

0.58 a 
0.35 a 
  0.34 ab 
0.12 b 
0.63 a 

0.002 
0.31 c 
2.51 bc 
6.82 a 
9.78 a 
5.79 ab 
       * mph = Average number of mating pairs per hour averaged across all hours. 
       ** fph = Average number of male flights per hour averaged across all hours. 
 
 

 7 
19 
30 
    114 
    639 
30 

763 
584 
737 
833 
1227 
495 

    1 
375 
   1666 
   5985 
   8751 
   2864 

 405 
798 
569 
   1089 
650 
472 

The proportion of male flights that occurred outside of the mating period was lowest in 

colonies reared at 28°, and this was significantly lower than the proportion of male flights that 

occurred outside the mating period in colonies reared at 15, 18 or 35°C (Table 4.3). Data 

collected from colonies reared at 10°C were not included in this analysis. At 15°C, 58% of male 

flights occurred during periods when no mating pairs were observed, and this was statistically 

similar to male flight behavior in colonies at 18°C, 23°C and 35°C, where 35%, 34% 63% and of 

 

87 

flights were observed outside of the mating period, respectively (Figure 4.10, Table 4.3). Few 

mating pairs were observed at 35°C (Figure 4.8), so the high proportion of male flights that 

occurred at this temperature are contributing to this result (Table 4.3).  

 

a 

a 

ab 

b 

a 

Figure 4.10 Proportions of male flights and mated pairs of P. viteana observed each hour in 
colonies held at constant temperatures under 17:7 L:D and 60-75% RH. The shaded 
rectangle covering the period from 2000 to 0300 hours on the x-axis indicates the 
scotophase. The proportion of male flights that occurred when mating was not observed is 
given in the bold numbers on the left hand side of each graph. Proportions with the same 
letter are not statistically different (Q0.05, ∞, 6 > 4.03, P < 0.05, arcsine transformed data, using 
multiple comparison of proportions (Zar 1999)). Data from colonies reared at 10°C (shown 
in red) were not used in this analysis because only one flight was observed in all samples. 

 

88 

Day length. In colonies that were reared in short (12L:12D), moderate (14L:10D) or long 

(17L:7D) day length cycles, the frequency of mating ranged from 0.08 to 0.21 matings per hour 

(mph), and this frequency increased with increasing day length (Table 4.4). Mating frequency in 

the long day length treatment was significantly higher than that in the short or moderate day 

length treatments, but mating in the short and moderate day length treatments was similar (F2,114 

= 21.3; P <0.0001, log transformed data, Figure 4.11a). The number of male flights observed per 

hour (fph) also increased as day length increased, and significant differences were detected 

between day length treatments (F2,72 = 12.1; P <0.0001, log transformed data, Figure 4.11b). 

Male flights per hour ranged from 8.51 fph under a short day length regime to 16.52 fph under 

the long day length treatment. Male flight frequency under this day length treatment was 

significantly higher than male flight frequency in either moderate or short day lengths (Figure 

4.11b).  

(a) 

a

 

M
E
S
±

 

 

M
E
S
±

 

(b)

a 

b 

b 

b 

b 

Day length treatment 

Figure 4.11. Matings per hour (a) and male flights per hour (b) in Paralobesia viteana 
colonies reared under short (12h), moderate (14h), or long (17h) day lengths. Values 
labeled with different letters are significantly different (P < 0.05). 

 

89 

 

 

(a) 

Long 
 

Moderate 

 

 
t
n
e
m
t
a
e
r
t
 
h
t
g
n
e

l
 

y
a
D

 
Short 

 

 

 
Long 

 

Moderate 

 
Short 
 

(c) 

(b)

(d) 

Long

Moderate

Short

Long 

Moderate  

Short

 

 

 

 

 

Time of occurrence

Figure 4.12. Average time of the first observation of mating pairs (a) and male flights (b), of 
Paralobesia viteana and average time of last mating pair (c) and male flight (d) in colonies 
reared under 3 different day length treatments. Times of first and last behaviors in the 24 h 
period from 12:00 on the first day of recording to 11:59 the following day on all days the 
behavior was observed. All colonies were reared at 28°C. Columns with different letters are 
significantly different (P  < 0.05). 

The average time of the first observed mating pair in colonies held under different day 

lengths ranged from 05:22 to 07:03. The first mating pair in the moderate day length treatment 

occurred significantly later than the first mating pair in the long day length treatment, but no 

differences were detected between the short and long day length treatments (F2,96 = 3.35; P = 

0.039, log transformed data, Figure 4.12a). The average time the last mating pair was observed 

ranged from 04:08 to 06:30, but the end of the mating period was not significantly different 

among treatments (F2,96 = 0.34; P =0.47, log transformed data, Figure 4.12c). The average time 

of the first male flight ranged from 08:12 to 10:28, and there were no significant differences 

 

90 

detected between day length treatments (F2,55 = 1.64; P =0.2019, log transformed data, Figure 

4.12b). The average time of the last observed flight across all treatments ranged from 07:38 to 

12:01. The last flight in colonies reared in the long day length treatment was significantly later 

than that in either the short or moderate day length treatments (χ2 = 23.03, P < 0.0001, Figure 

(a) 

(b)

(4.12d).  

 
)
n
m

i

(
 
n
o
i
t
a
r
u
D

Day length treatment

Figure 4.13. Mating period duration (a), and flight period duration (b) of 
Paralobesia viteana, in colonies reared under different day lengths. Averages are 
taken only where a given behavior was observed at least twice during the 24 hour 
period from 12:00 on the first day to 11:59 on the second day of recording. 
Columns labeled with different letters are significantly different (P < 0.0001). 
 

 

 

 

 

 

 

 

91 

Table 4.4. Summary of mating frequency and male flight measurements for colonies of 
Paralobesia viteana held under different day length regimes. Values in a given column with 
different letters are significantly different (P < 0.05). 
Day 
length 

Proportion 
male flights 

Hours 
observed 

Hours 
observed 

mph* 

fph** 

# times 
behavior 
observed 

# times 
behavior 
observed 

outside 
mating 
period 
0.11 
0.06  
0.02  

Short 
8221 
Moderate 
7328 
Long 
  10676 
* mph = Average number of mating pairs per hour averaged across all hours. 
** fph = Average number of male flights per hour  averaged across all hours. 

 9.68 b 
 8.51 b 
16.52a 

0.08 b 
0.08 b 
0.21 a 

763 
584 
737 

  7 
19 
30 

932 
890 
778 

 

The duration of the mating period ranged from 353 minutes (5h, 53m) in the short day 

length treatment to 526 minutes (8h, 46m) for colonies reared under a long day length, but no 

significant effect of day length on the duration of the mating period was detected (χ2 = 3.77, df 

=2,, P = 0.15 Figure 4.13a). There was a significant effect of temperature on the duration of the 

male flight period (χ2 = 23.03, df =2,, P < 0.0001, Figure 4.13b). Male flight period duration 

ranged from 774 to 1406 min (12h 54m to 23h 26m), and the flight period for colonies held at 

short or moderate day length was significantly longer than for colonies reared under the long day 

day length treatment (Figure 4.13b). In colonies reared under the short day length treatment, the 

duration of the flight period was 774 minutes and this was significantly longer than the mating 

period of 353 minutes (χ2 = 36.2, df =2,, P < 0.0001). Similarly, in the moderate day length 

treatment the male flight period was 1406 minutes, and this was significantly longer than the 

mating period of 552 minutes (χ2 = 34.8, df =2,, P < 0.0001). In the long day length treatment, 

the lengths of the flight period (774 minutes) and the mating period (526 minutes) were not 

different (χ2 = 2.88, df =2,, P = 0.09). This indicates that in the short and moderate day length 

 

92 

treatments, males were flying when females were not receptive to mating, but this is not true in 

colonies reared in the long day length treatment.  

The proportions of male flights that occurred outside of the mating period were similar 

among day length regimes. This proportion was lowest in colonies under the long day length 

treatment: under these conditions only 2% of male flights occurred when mated pairs were not 

visible. In colonies reared under a moderate day length, 6% of male flights occurred during 

periods when no mating pairs were observed. The highest proportion of male flights occurring 

outside of the mating period (11%) was recorded in colonies reared under a short day length 

treatment (Figure 4.14, Table 4.4). 

 

93 

 

Hour 

Figure 4.14. Proportion of mated pairs and male flights of P. viteana observed each 
hour in colonies reared under different day length treatments at 28°C and 60 - 75% RH. 
Numbers in the plot area of each graph indicate the proportion of male flights that 
occurred when no mating pairs were detected. The shaded rectangles in each graph 
indicate the scotophase of the light: dark cycle. No significant differences in the 
proportion of male flights that occurred when mating was not observed were detected 
among day length treatments (Q 0.05, ∞, 3 < 3.31, P > 0.05, Multiple comparison of 
proportions, Zar 1999).  

94 

 

 

Diurnal temperature cycles. In the third experiment, mating frequency and male flight  activity 

in colonies reared in diurnal temperature regimes, the frequency of mating in the cool weather 

treatment (20°C during the day to 10°C at night) was 0.038 matings per hour (mph). Mating 

frequency in the warm weather treatment (28°C day to 10°C night) was 0.043 mph, and in the 

hot weather treatment (28°Cday to 18°C night) mating frequency was 0.082 mph (Figure 4.15a). 

Despite a nearly two-fold difference in average matings per hour, no significant differences were 

detected in mating frequency between treatments (F2,34 = 1.32, P = 0.28, log-transformed data, 

Figure 4.15a). The number of male flights per hour ranged from 4.0 fph in colonies that received 

the cool weather diurnal treatment to 5.7 fph in the hot weather treatment. No significant 

differences in male flight frequency were detected between diurnal temperature treatments (F2,34 

= 0.24, P = 0.78, log transformed data, Figure 4.15b).  

(a) 

(b) 

Diurnal temperature treatment 

Figure 4.15 Mating frequency (a) and male flight frequency (b) of Paralobesia viteana 
recorded in colonies reared under three diurnal temperature regimes. Cool treatment colonies 
were reared in a temperature scheme that changed from 20°C during the day to 10°C at night. 
Day:night temperature cycles in the Warm and Hot treatment were 28°C:10°C and 28°C:18°C 
respectively. All treatments incorporated a 17:7 light: dark (day:night) cycle. “ns” denotes no 
significant differences were detected between treatments (P < 0.05).                            

 

95 

(a) 

(c) 

 
t
n
e
m
t
a
e
r
t
 
e
r
u
t
a
r
e
p
m
e
t
 
l

a
n
r
u
D

i

(b) 

(d) 

Time of occurrence 

Figure 4.16. Average time of the first observation of mating pairs (a) and male flights (b), and     
average time of last mating pair (c) and male flight (d) in colonies reared under 3 different 
diurnal temperature regimes. Treatments are the same as described in Figure 4.15. “ns” denotes 
no significant differences were detected between treatments (P >0.05). 

The average time of first mating ranged from 23:02 in the hot temperature regime to 

04:07 in the warm temperature treatment, and there were no statistically significant differences 

among the diurnal temperature regimes in the time of first mating (F2,20 = 0.32, P = 0.73, log 

transformed data, Figure 4.16a). The average time the last mating occurred was also not 

significantly different between treatments (χ2 = 2.97, df =2,, P = 0.23, Figure 4.16c), and ranged 

from 20:43 in the warm treatment, to 01:36 in the cool weather treatment, and the last mating in 

the hot weather treatment occurred at 22:53 (Figure 4.16c). The average time of the first male 

flight in the cool weather treatment was 09:11, while in the hot weather treatment, the average 

time the first flight was observed was 11:40, and the average start time for male flight was 10:18 

in the warm weather treatment. These times were not significantly different among treatments 

 

96 

(F2,31 = 2.88, P = 0.07, log transformed data, Figure 4.16b), but there was a significant difference 

in the average time of the last flight among diurnal temperature treatments. This ranged from 

from 05:22 in the cool weather treatment to 07:14 in the warm treatment. The last male flight 

occurred significantly later in the hot and warm treated colonies than in the cool weather treated 

colonies (χ2 = 6.27, df =2, P = 0.046, Figure 4.16d).   

The average duration of the mating period ranged from 36 minutes in the warm weather 

treatment to 158 minutes in the hot weather regime, and mating period duration in the cool 

weather treatment was 112 minutes (Figure 4.17a). There were no significant differences in 

mating period duration between diurnal temperature treatments (F2,20 = 1.72, P = 0.21, log trans-

formed data, Fig 4.17a). The average duration of the male flight period ranged from 1169 

minutes to 1255 minutes, indicating males were active for most of the 24 hour cycle. There were 

no significant differences in the duration of the male flight period, which shows that the male  

(a)  

(b)  

ns 

 
)
n
m

i

(
 
n
o
i
t
a
r
u
D

ns 

Diurnal temperature regime 

Figure 4.17. Mating period duration (a) and flight period duration (b), in colonies of P. 
viteana reared under different diurnal temperature regimes. Treatments are the same as 
described in Figure 4.16. “ns” denotes no significant differences were detected between 
treatments (P > 0.05). 

 

 

97 

flight period is not strongly influenced by these different temperature regimes (F2,31 = 0.33, P = 

0.72, log trans-formed data, Fig 4.17b). In colonies reared in the cool weather treatment, the 

duration of the flight period was 1211 minutes and this was significantly longer than the mating 

period of 112 minutes (χ2 = 13.8, df =1, P = 0.0002). Similarly, in the warm weather treatment 

the male flight period was 1255 minutes, and this was significantly longer than the length of the 

mating period of 526 minutes (χ2 = 14.2, df =1, P = 0.0002). This indicates regime, in that all of 

the diurnal temperature treatments, males were flying when females were longer than the mating 

period of 36 minutes (χ2 = 10.7, df =1, P = 0.0011). In the hot weather not receptive   

The proportion of male flights that occurred outside of the mating period was highest in 

colonies that experienced the cool weather treatment (20°C:10°C day:night cycle). Under these 

conditions almost three quarters (73%) of male flights occurred when mated pairs were not 

observed, and this was significantly higher than colonies held under the Hot weather treatment 

(28°C:18°C day:night cycle, Figure 4.18). In colonies reared under the Warm weather treatment 

(28°C:10°C day:night cycle), two thirds (67%) of male flights occurred during periods when no 

mating pairs were observed, and this was similar to the proportion of male flights in colonies 

held in the cool weather treatment. The lowest proportion of male flights that occurred outside of 

the mating period (22%) was recorded in colonies that were reared in the hot weather treatment, 

and this value was significantly lower than that for the cool or warm weather treatments. Thus, 

under cooler conditions, higher proportions of male flights occurred when mating pairs were not 

observed compared to colonies under warmer conditions (Table 4.5). 

 

 

98 

 

 

 

                0.67a  
 

               0.73a  

                0.22b 

Hour 

Figure 4.18 Proportion of mated pairs and male flights of P. viteana observed 
each hour in colonies reared under diurnal temperature treatments and constant 
day length 17:7 and 60 % RH. The shaded rectangle surrounding the time from 
20:00 to 03:00 shows the scotophase. Proportions of male flights that occurred 
when mating was not observed are given in bold on the left hand side of the 
graphs. Proportions with the same letter are not statistically different 
(Q0.05, ∞, 3 > 3.31, P < 0.05, Multiple comparison of proportions, Zar 1999). 

Table 4.5. Summary of mating frequency and male flight measurements for colonies held 
under diurnal temperature regimes. Values in a column values with different letters are 
significantly different (P < 0.05). 
Diurnal 
mph*
Treat-
ment 

# times 
behavior 
observed 

# times 
behavior 
observed

Proportion 
male flights 

Hours 
observed

Hours 
observed

fph**

outside 
mating 
period 
0.67 a 
0.73 a 
0.22 b 

Cool 
4.0 
5.5 
Warm 
5.7 
Hot 
* mph = Average number of mating pairs per hour averaged across all hours. 
** fph = Average number of male flights per hour  averaged across all hours.

0.04 
0.04 
0.08 

635 
470 
493 

26 
21 
45 

2444 
2454 
3351 

635 
470 
493 

99 

Response to pheromone lures at different times of the season 

Traps baited with lures that contained pheromone caught more males than the control traps that 

were baited with a blank lure (Figure 4.19). Captures of male moths declined as the pheromone 

quantity increased when data were summed over all sampling periods (F5,30 = 92.2; P < 0.0001, 

log transformed data, Figure 4.19). Traps loaded with a 15 µg lure caught significantly more 

males than traps baited with a lure containing the standard amount of pheromone in commercial 

lures (100 µg). Male captures in traps containing the 15 µg lure were significantly higher than  

captures in traps with the 125 µg lure. The number of males captured in traps loaded with either 

the 60 µg lure or the 75 µg lure were not statistically different than captures in any of the other 

 
a 

c 

ab 

ab 

b

 
b 

Pheromone per lure (µg)

Figure 4.19 Total male moth captures of P. viteana for the entire season in traps loaded with 
different amounts of pheromone per lure. Data are averages from seven replicate vineyards 
in southwest Michigan. Columns labeled with different letters are significantly different     
(P  < 0.05). 

 

 

100 

Figure 4.20. Captures of male P. viteana in traps baited with lures containing different 
amounts of pheromone in different sampling periods. The legend gives the amount of 
pheromone per lure in µg. In any sampling period, columns with different letters are 
significantly different (P < 0.05).  

 

pheromone loaded traps (Figure 4.19). Male captures varied significantly among lure treatments  

for the five sampling periods (May: F5,30 = 56.8, P < 0.0001; June: F5,30 = 38.4, P < 0.0001; July: 

F5,30 = 12.2, P < 0.0001; Aug: F5,30 = 22.0, P < 0.0001; Sep-Oct: F5,30 = 18.5, P <0.0001, all data 

log transformed, Figure 4.20). The lowest average daily temperature (16.8°C) and the lowest 

average temperature during the scotophase from 20:00 to 5:00 when males are likely to fly 

(12.3°C) occurred during the May sampling period. During this period, the captures in all traps 

with pheromone lures were significantly higher than in the blank lure control traps, and captures 

in the traps containing 15µg lures were significantly higher than in traps baited with 100 µg 

lures. In the June sampling period, average daily temperature was 21.8°C and average night time 

temperature was 18.2°C. The highest average male captures occurred during June and ranged 

 

101 

from 10.7 ± 3.1 in the blank lure traps to 257 ± 62.5 males in the 15µg traps. Significantly more 

males were captured in the 15µg traps than in the 100µg or 125µg traps (128.6 ± 28.9 and 145.4 

± 41.0 males, respectively). In July, average daily temperature increased to 22.7°C and 

scotophase temperatures averaged 19.6ºC, and male captures dropped off considerably. Male 

captures ranged from 3.1 ± 1.0 males in the blank lure traps to 56.1 ± 22.6 males in the 15µg 

traps, and this was the only significant difference in captures detected during this period. In 

August the average daily temperature cooled to 19.9°C, and during the scotophase temperature 

averaged 17.1°C. Male captures ranged from 2.0 ± 1.0 males in the blank lure traps to 53.7 ± 

10.7 males in the 15µg traps. In August, captures in the 15µg traps were significantly higher than 

captures in all other traps except for traps with the 60 µg lure. In the final trapping period that 

ran from September through October, average daily temperature fell to 17.8°C and during the 

scotophase average temperature was 13.8°C. All traps with lures containing pheromone were 

significantly higher than the traps baited with blank lures. Captures in the 15µg traps were 

similar to captures in the 60µg traps, and these were both significantly higher than the traps with 

the 100µg lures. 

To illustrate the relationship between male captures and pheromone release at different 

times of the season, moth capture was regressed on pheromone release for each sampling period. 

There was a consistent negative relationship between moth captures and pheromone release with 

the strongest effect of increasing pheromone release in May and August (Figure 4.21).  

Analysis of covariance was used to determine if the relationship between moth capture 

and pheromone release is consistent at different times of the season (Table 4.6), revealing 

significant effects of sampling period (P = 0.00001) and pheromone release/day (P = 0.00009)  

on captures, and we also detected a significant interactive effect of sampling period and 

pheromone release on male captures (P = 0.043). 

 

102 

Table 4.6. Analysis of covariance to determine if the relationship between 
male captures of P. viteana and pheromone release differs between 
samping periods. 
Source 
DF 

Mean Square  F  Ratio  Prob > F 

17.44 

6.78
0.39

<0.0001 
 
 

 
 

 

Model 
Error 
Total 

9 
15 
24 

Sum of 
Squares
61.01
5.83
66.84

            Comparison of the least square means from this analysis showed that the relationship 

between captures and pheromone loss was similar in the May and August sampling periods, but 

different than the effect of pheromone release on captures in the June, July and September-

October sampling periods (Table 4.7). That is, increasing pheromone release caused a larger 

reduction in captures in May and August than in the other sampling periods.  

 

 

 

 

 

 

  

 

Table 4.7. Comparison of least squares means for captures 
of P. viteana in different sample periods (Tukey’s HSD). 
Means with the same letter are not significantly different. 
Sample period        

Least square means 

for captures 

4.61 a 
3.41 a 
1.59 b 
1.58 b 
0.91 b 

May 
August 
June 
Sep-Oct 
July 

103 

  

 

(a) 

(c) 

(e) 

 

y
a
d
/
p
a
r
t
/
s
e
r
u
t
p
a
c
 
e
a
M

l

(b)

(d) 

Pheromone release µg/lure/day 

Figure 4.21 Relationship between captures of Paralobesia viteana and pheromone 
release for different sampling periods in 2017. Each point represents the average male 
capture and pheromone release for each lure load (15, 60, 75, 100, 125 µg/lure) at 7 
southwest Michigan vineyards. Blank lures were not included in this analysis because 
they did not contain pheromone. 

 

104 

 

y
a
d
/
s
e
r
u
t
p
a
C

 

 

 

 

 

 

 

 

 

 

 

y
a
d
/
e
r
u
l
/
g
µ
e
n
o
m
o
r
e
h
P

 

 Growing degree days base (8.41˚C)

Figure 4.22 Regression of P. viteana captures (a) and pheromone release (b) on 
accumulated heat units (GDD8.41). Residuals from (a) were regressed on the residuals 
in (b) to test the effect of pheromone release on captures with the effect of temperature 
removed (Table 4.8). 

Captures and pheromone release both decline with the heat units accumulated during the 

sampling period (GDD8.41) (Figure 4.22). Regression analysis using the residuals from the linear 

regressions of captures and pheromone release on GDD8.41°C showed the reduction in captures 

due to pheromone release with the effect of temperature removed (Table 4.8). This shows that 

lures that release larger quantities of pheromone have lower captures of male P. viteana. 

Table 4.8. Analysis of variance and parameter estimates from linear 
regression of residuals from the analyses in Figure 4.22 to evaluate the 
effect of pheromone release on captures of male P. viteana after removing 
the effect of temperature 
Source 

Mean Square

F Ratio

Prob > F 

 

 
 
 
 
 
 

 

DF 

Model 
Error 
Total 

1 
23 
24 

Sum of 
Squares
22.15
24.53
46.68

22.15
1.07

20.77

0.0001 

105 

DISCUSSION 

This research highlights temperature as a critical factor affecting many behaviors and 

physiological processes associated with mating by P. viteana, and how these effects determine 

the observed phenology of this pest in Michigan vineyards. With increasing temperature, 

longevity decreases, but mating, male flight frequency and oviposition, all increase. The 

proportion of males that fly outside of the mating period (i.e., when females are not receptive to 

mating) is highest during cool temperatures and decreases with increasing temperature. This 

provides support for the model outlined in Figure 4.1 that predicts cool temperatures reduce the 

duration of the female calling period relative to the duration of the period when males respond to 

pheromone. While, during periods of high temperatures, like those that occur during the mid-

summer P. viteana generation, the duration of the mating period is similar in length to the flight 

period. This results in fewer male flights that occur when females are not receptive to mating, 

compared to the first generation. These relationships are likely to contribute to higher male 

captures in traps in cool conditions because males are flying (receptive to pheromone) and 

searching for females, but no calling behavior is occurring. In this situation, pheromone-baited 

traps would not be in competition with calling females, and males would be more likely to be 

attracted to and captured in pheromone-baited traps.  

High temperature reduced adult male and female P. viteana longevity, and this decrease 

was similar between the sexes. There was a six-fold decrease in longevity between 10 and 28°C 

and a two-fold decrease between 18 and 28°C. This is consistent with other studies that show 

decreased longevity in response to constant experimental temperatures in several insect orders 

including; Lepidoptera, Hymenoptera, Coleoptera, and Hemiptera (Graham et al. 1967, Emana 

2007, Gómez et al. 2009, Régnière et al. 2012). Several studies have reported longevity for 

tortricid moths held at different constant temperatures, and these results are similar to my results 

 

106 

for P. viteana. Semi-field bioassays using caged wild moths showed that longevity in successive 

generations of the Nantucket pine tip moth decreased significantly as temperature increased 

through the season (Asaro and Berisford 2001). In constant temperature experiments in the same 

study, male longevity was reduced by 8 to 10-fold over the range from 5 to 40°C. Although the 

authors did not compare longevity between sexes, it appears females live almost twice as long as 

males (Asaro and Berisford 2001), and decreased male longevity caused by high ambient 

temperatures in the second and third generations was a contributing factor to low captures of 

males in the later generations when ambient temperatures were high (30-35°C). Codling moth 

adults held in constant temperatures survived approximately 4 times longer at 14°C than those 

held at 33°C (Aghdam et al. 2009). The increased longevity of male moths at low temperatures 

may contribute to high first generation P. viteana male captures. If males live longer in low 

nonlethal temperatures, they may have an increased probability of being caught in traps, 

assuming that for a portion of their lives temperatures are high enough for flight. It is also likely 

that decreased male longevity at high temperatures contributes to the reduction in P. viteana 

male captures in the second and third generation during high temperatures. Increased female 

longevity at low temperatures may allow first generation females to wait until warm conditions 

to begin laying eggs.  

The temperature required for flight in male and female P. viteana was found to be 15°C 

and this is similar to the lower temperature thresholds for flight in other tortricids. Among the 

Tortricidae, the minimum temperature for flight is typically in the range of 12-15°C. Reported 

temperatures include 14°C for the eastern spruce bud worm, Choristoneura fumiferana 

(Greenbank et al. 1980); 15°C for oriental fruit moth, Grapholita molesta (Rothschild and Minks 

1974) and 12.7°C for codling moth, Cydia pomonella (Batiste et al. 1973). The minimum 

temperature for flight in the light brown apple moth, Epiphysis postvittana was considerably 

 

107 

lower than other tortricids and ranged from 8 to 11°C (Danthanarayana 1976). However, this 

study used suction traps to collect moths during natural temperature variation, and it is possible 

this trapping method may have underestimated the minimum threshold by collecting moths that 

were near the trap, but not flying. My finding of this lower threshold for P. viteana could be 

integrated into the degree-day model that is currently used for this pest to better predict when 

egglaying will start in the spring and through the rest of the growing season. 

Oviposition in P. viteana is highly dependent on temperature, and I found more eggs on 

grapes that were attached to the oviposition cage floor than on grapes suspended in the cages. 

This likely reflects that walking and flying females could reach the grapes more easily in these 

cages compared to when the grapes were suspended, and only climbing or flying moths could 

reach the grapes. These results agree with egg laying rates in previous research with some 

overlap in the range of temperatures that were used. In pink bollworm, oviposition increases 10-

fold between females held at 15.5°C and those reared at temperatures ranging from 18.3 to 

26.7°C (Graham et al. 1967). Særthre and Hofsvang (2002) showed codling moth were able to 

lay eggs at temperatures as low as 12.3°C, and the amount of oviposition doubled when 

temperatures increased to 17°C and reached a maximum at 25°C, which was the highest 

temperature tested. In tests of Oriental fruit moth oviposition temperature preference, egg laying 

was highest in the range 22 to 30°C, and drops off rapidly at 33°C with no egg laying at 35°C 

(Notter-Hausmann and Dorn 2010). This study did not measure oviposition at temperatures 

below 22°C, so I cannot directly compare the lower temperature limits of P. viteana to that for 

Oriental fruit moth. However, these studies show that, in P. viteana and other species, 

oviposition is positively related to temperature, and oviposition over the range of temperatures 

that insects are active can increase 10 to 100-fold from the lowest to highest temperatures. This 

 

108 

provides strong support for temperature being a major factor determining oviposition rates and 

for the phenology of egg laying in P. viteana (Chapter 1, Figure 1.3). 

In P. viteana colonies reared at different constant temperatures, I observed strong positive 

relationships between temperature and the frequency of mating (mph) and the frequency of male 

flights (fph). Mating frequency increased exponentially with temperature over the range of 10 to 

28°C (from 0.01 to 0.52 mph), but mating was reduced at 35°C indicating that between 28 and 

35°C there is a critical maximum for this behavior. The frequency of P. viteana male flights was 

also strongly linked to experimental temperature in a positive exponential relationship. Both 

mating and flight frequency show characteristic thermal performance curves (Huey and 

Kingsolver 1989) that increase through a range temperatures above a critical low value, but 

decline rapidly at or above a critical high temperature (Lachenicht et al. 2010).  

The time of first mating was not significantly different between colonies reared at 

different constant temperatures, in contrast to other work that shows female calling begins earlier 

at lower temperatures (Cardé et al. 1975b, Cardé and Minks 1995). In my experiments, all of the 

average start times for mating were within the scotophase of the photoperiod, and this is similar 

to reports of many other tortricids that mate during the dark phase (Cardé, et al. 1975a, Baker 

and Cardé 1979a, Delisle and McNeil 1987, Webster 1988). The time of last mating was 

significantly later in colonies held at 28°C compared to colonies reared at 15 or 23°C. There were 

significant differences in the duration of the mating period, and this period was longer at 28°C 

than at either 15 or 18°C indicating the period females are receptive to mating is longer at higher 

temperatures. This is similar to previous studies that show female calling period starts and ends 

later at higher temperatures, and results in a longer period where females are calling and 

receptive to mating (Cardé et al. 1975b, Baker and Cardé 1979a, Webster 1988). 

 

109 

The time of the first male flight differed significantly between colonies reared at 18°C 

and those reared at 23°C and 35°C, but more importantly all first flights were observed during 

the photophase of the photoperiod. This shows that male flights occur before the scotophase, 

when females are not yet receptive to mating. There were no significant differences in the 

average time of the last male flight, but these times were all outside of the scotophase showing 

that male flight activity starts and ends beyond the period when females are receptive to mating. 

For all constant temperature treatments except 15°C, the male flight period was also 

significantly longer than the mating period (Figure 4.9a and b). This is strong evidence that 

males are actively seeking mates or mating sites when females are not receptive to mating, and 

this has been shown in other Lepidoptera such as Antherea polyphemus (L.) (Kochansky et al. 

1977). This is expected to contribute to higher male captures in traps if flying males are receptive 

to pheromone and searching for females, but few receptive (calling) females are present. This 

decreased competition between traps and calling females at different times of the season has 

been noted in other moth species (Palanisawamy and Seabrook 1978, Noguchi and Tamaki 1985, 

Sanders 1987). This increases the likelihood that males will find pheromone-baited monitoring 

traps, because the traps release pheromone throughout the day and night, and thus would be the 

only sources of pheromone during the day as females only call at night. 

 

My analysis of the proportion of male flights that occur outside of the mating period 

clearly demonstrated that more male activity occurs outside of the mating period in colonies held 

in low temperatures compared to colonies reared at high temperatures. A significantly higher 

proportion of male flights occurred outside of the mating period in colonies held at 15, 18 or 

35°C than in colonies reared at 28°C. This supports the hypothesis that there would be higher 

male captures in traps during cool temperature conditions, such as in the spring in Michigan 

 

110 

when the first generation of P. viteana is active, than during the hot part of the growing season 

(mid-summer) when the second and third generations are active. It also fits the observed pattern 

of moth capture in Chapter 1, Figure 1.3. 

 

The role of day length in determining the timing and intensity of mating behaviors is less 

clear than for temperature. However, I observed some significant effects of day length on some 

mating parameters that align with observed phenology patterns. Mating frequency and male 

flight frequency were significantly higher in colonies held under the longest day length (17h) 

compared to colonies reared under either the moderate (14h) or short (12h) day length treatment. 

In the field, the longest day lengths occur during midsummer during Generation 2, and this is 

when there are substantial increases in egg laying and fruit damage in vineyards (Chapter 1, 

Figure 1.3) (Hoffman et al. 1992, Teixeira et al. 2009). In addition, the duration of the mating 

period was longer in the moderate and long day length treatments, and this agrees with 

observations in the field, because periods of highest egg laying are seen when day lengths are 

moderate or long. This shows that increasing day length could also play a role in the high levels 

of oviposition in the second and third grape berry moth generations. For all day length treatments 

tested, some male flights always occur outside of the time when females are receptive to mating. 

Even though the flight period is longer than the mating period for all treatments, day length did 

not significantly affect the proportion of male flights that occurred outside of the mating period. 

In addition, the proportions of male flights that occurred outside of the mating period in the day 

length treatments were much lower than observed in the constant temperature treatment (Figures 

4.10 and 4.14). Overall, these results suggest that the effect of day length on mating behaviors is 

much less important than the effect of temperature, and seasonal changes in day length are not 

likely to be primary factors responsible for the lower captures of male P. viteana in the middle 

and late parts of the season.  

 

111 

 

Diurnal temperature fluctuations in colonies had little effect on mating or male flight 

frequency or timing, except that the time of the last male flight was significantly earlier in the 

Cool season treatment. This contrasts with previous research in different species that showed 

female calling and male responsiveness to pheromone start and end earlier in cool weather 

(Cardé et al. 1975a, b, Webster 1988). This may reflect the different methods that were used in 

the current study compared to the previous experiments. Previous studies directly measured 

female calling, male antennal responses and/or male precopulatory and mating behaviors in 

response to changes in temperature (Cardé et al. 1975a, b, Webster 1988). I measured the 

frequency of mating as a proxy for female receptivity, and male responsiveness was inferred 

from the frequency of  flights. Although these are vastly different methodologies, the past and 

present research show that temperature is a key factor in determining the patterns of mating 

behaviors.  

The frequency of mating in colonies under a diurnal temperature regime was generally 

lower than in the constant temperature and day length experiments, but the frequency of male 

flights was more similar in all three data sets (Figures 4.10, 4.14 and 4.18). Overall, the mating 

period in the diurnal temperature experiment was shorter than in the constant temperature or day 

length experiments. It is likely that the decreased temperatures in these treatments during the 

scotophase reduced the frequency of mating. The proportion of male flights that occurred outside 

of the mating period was significantly lower for the hot weather treatment than in the cool or 

warm weather treatments. This result also supports my interpretation of how temperature affects 

mating and observed phenology. That is, if flying males are receptive to pheromone, and they are 

searching for females, but no females are calling, males will be more likely to be attracted to the 

pheromone lures in monitoring traps. If this is occurring in the field, then I would expect to catch 

more males in the cooler part of the growing season, as observed across the temperate, northern 

 

112 

portion of eastern North America. Additional studies that compare pheromone trap and 

temperature data across the latitudinal range of P. viteana from Ontario to Texas would certainly 

help to test this prediction, especially if there is not geographic variation in male response to 

pheromone (see Chapter 2).   

In the field experiment to determine the response of male P. viteana to different rates of 

pheromone release, traps loaded with lures that contained (and released) higher amounts of 

pheromone caught significantly fewer moths. Pheromone release is dependent on temperature 

and the quantity of pheromone in a lure (McDonough et al. 1989). High pheromone release rates 

in high temperatures may be inhibitory to male P. viteana and contribute to lower captures in 

pheromone traps as has been shown in other species (Baker et al. 1980, Allen et al. 1986, 

McDonough et al. 1989, Charlton et al. 1993). In the present study, analysis of covariance 

showed that in two of the cooler sampling periods, May and August, pheromone release from 

high load lures had a stronger effect on reducing male captures than was observed in the June, 

July or September-October sampling periods. These results suggest that during the warmer 

periods in June and July the evaporative release of pheromone from any lure was high enough to 

suppress male captures in a trap. Surprisingly there was not a strong effect of pheromone loss on 

captures in the September-October sampling period, because these were cool periods compared 

to June and July. It is likely that the effect of pheromone release on capture was diminished 

because the sampling period was twice as long as the other periods in this experiment. Still, these 

data do suggest high rates of pheromone release from lures is a contributing factor that helps 

explain low male moth captures in mid- and late-summer when temperatures are high. 

My field experiment shows that temperature and pheromone release contribute to the 

observed P. viteana phenology that is evident from monitoring traps. The consistent high 

captures in the traps baited with 15µg lures and the consistent low captures in traps baited with 

 

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the standard quantity of pheromone (100µg) suggests seasonal temperature changes affect male 

captures and higher load lures can suppress male captures in the hottest parts of the season. 

However, even in traps baited with 15µg lures, male captures declined through successive 

sampling periods. Whether this is a suppressive effect resulting from high pheromone release or 

is caused by pheromone loss resulting in low pheromone quantity and reduced attraction to traps 

during high temperature is not clear. Overall, low load lures appear to release an appropriate 

pheromone dose and could result in improved capture of male P. viteana, not only in the hottest 

part of the season, but also during the first generation that occurs in the spring. This highlights 

the need for future testing of lures with pheromone loads of 15µg and lower. 

 

The relationships between temperature, mating and male flight activity in P. viteana 

described in my research provide new insights to explain the pattern of moth activity and 

oviposition phenology observed in Michigan vineyards. In the spring, cool temperatures prevail 

which increases the longevity of male P. viteana, and because they are living longer, there is a 

higher probability that males will encounter and be caught in traps. At these low temperatures, a 

higher proportion of male flights occur when females are not calling and therefore not receptive 

to mating. This could also lead to high male captures because lures in traps constantly release 

pheromone, and this would attract flying males.  Furthermore during the spring, daytime 

temperatures are above the threshold for flight, but often temperatures are below this threshold 

during the night. My data show that less mating occurs in the daytime and during low 

temperatures, so females are presumably not calling during cool spring nights. So it is probable 

that males flying in the spring are more likely to encounter pheromone from a trap than from a 

calling female. Low temperatures also reduce oviposition, and this combined with the lower 

flight and mating activity of the pest is why there are few eggs and larvae seen on clusters in the 

first generation. In the second generation that occurs in mid-summer, temperatures are usually at 

 

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their seasonal maximum. Mating increases with temperature, so more females are calling and 

receptive to mating. This leads to a lower proportion of male flights that occur when mating is 

not occurring, so fewer males are caught in traps because they are attracted to the calling 

females. More eggs are also observed during this time because the high mid-summer 

temperatures increase mating and increase the rate of the physiological processes associated with 

oviposition.  

During the latter part of summer, P. viteana damage is at the highest levels of the season 

even though temperatures are generally not as high as in the mid-summer. Mating and egg laying 

occur at a rapid pace during this period, and the resulting high levels of damage observed at this 

time of year are likely due in part to increased moth longevity. In the typical range of 

temperatures that occur during this time of the year, the proportion of male flights when mating 

is not occurring is higher than in mid-summer, but lower than in the spring, so there is a slight 

increase in the number of males in traps compared to the previous generation, but fewer males 

are trapped than in the first generation.  

Temperature also affects the main monitoring tool for tracking P. viteana phenology, the 

pheromone-baited trap. The rate of release of pheromone from a lure increases with temperature, 

and P. viteana male response is influenced by the amount of pheromone released (Roelofs et al. 

1971, Witzgall et al. 2000). High rates of pheromone release from lures can reduce the 

attractiveness of traps, and result in reduced captures. This is most likely to occur during the 

middle and late summer generations of P. viteana, contributing to the reduced captures that occur 

in the middle and late summer. If males in summer generations could be trapped consistently this 

could refine predictions of when egg laying will begin in the middle and late summer 

generations. This would potentially improve timing of insecticide applications and provide better 

control of this key vineyard pest. 

 

115 

 

Currently P. viteana management involves using a degree-day model to time insecticide 

applications that target the eggs and newly emerged larvae of the second (middle summer) and 

third (late summer) generations (Teixeira et al. 2009, 2011). The MSU Enviroweather model 

predicts when egg laying is likely to begin based solely on temperature accruals using wild grape 

(Vitis riparia L) bloom as a biofix. This, along with the addition of new insecticide chemistries, 

has improved P. viteana management over calendar-based conventional insecticide approaches 

(Teixeira 2009). However, there is still room for improvement as many Michigan vineyards can 

have 75 to 100% of clusters infested with P. viteana in areas of high pest pressure. In Michigan, 

wild grape bloom occurs in late May or early June and this is typically over a month before 

second generation oviposition begins. Testing whether traps baited with pheromone lures that 

contain lower pheromone quantities than the standard 100µg/lure load can be used to detect the 

start of the second flight, and then using this as a mid-season biofix would be a useful first step 

to try and improve control of the summer generations. In addition, the results of my research 

could be used to refine the current model and inform future predictive models, by incorporating 

factors that take into account the effect temperature has on moth longevity, oviposition and 

mating activity. This would potentially allow for the formulation of action thresholds based on 

male captures, and better control. 

An additional point that my research brings to light is that increasing global temperature 

is likely to increase the risk of P. viteana infestation for Michigan grape growers. Average daily 

temperatures during the growing season are generally in the range of 15 to 23°C. If those 

averages are increased by 5°C, an increase in mating and oviposition during the middle and late 

summer would lead to higher levels of damage in vineyards. In addition, higher temperatures 

would lead to increases in the rate of P. viteana larval development and the number of P. viteana 

 

116 

generations per season could potentially increase (Tobin et al. 2008, Lamichhane et al. 2015). All 

of these factors could make P. viteana management even more challenging than it is today. 

 

117 

CHAPTER 5 

 

 

SYNTHESIS AND FUTURE RESEARCH NEEDS 

We are taught early on in school that science is an intellectual journey designed to help explain 

phenomena that we see in the natural world. We make observations and formulate hypotheses, 

and then test them by asking questions that we can answer through inductive reasoning and 

experimentation1. Typically these questions are designed to be answered using whatever 

experimental means are necessary, appropriate or available. However, the dynamic nature of 

science, the logistical challenges of our experiments, or in some cases human limitations dictate 

that the path of the investigation is altered along the way. This highlights one of the hidden 

benefits of scientific research; that most questions are actually open-ended, and because of this 

answering them is bound to uncover other ideas, and in turn other questions are revealed whether 

or not the original query is satisfactorily explained. I would argue that while the original question 

is important, and every reasonable effort should be made to fully answer it, the other questions 

that occur to us along the way are just as critical to scientific progress as the initial query. As Sir 

Francis Bacon wrote in Of the Advancement of Learning in 1605, “Every act of discovery 

advances the art of discovery,” (Bacon 1857). So in fact, we leave two important things for those 

who follow us down this path of science; we leave what we do know, and what we do not. With 

that I pass on this collection of ideas and questions that have been unearthed, but that remain 

largely unanswered. 

The main objective of my research reported in Chapter 2 was to determine if the regional 

variation in P. viteana male captures in Michigan vineyards is due to differences in the male 

response to pheromone. Regional variation of male response and pheromone composition has 

                                                 
1 For these ideas we all are indebted to Sir Francis Bacon, who laid the groundwork for modern science in Novum 
Organum (Bacon 1904).  

 

118 

been described for some Lepidoptera including the Tortricidae (Foster et al. 1986, El-Sayed et al. 

2003, Stelinski et al. 2007b), Noctuidae (Hansson et al. 1986, Löfstedt et al. 1986, Tòth et al. 

1992) and Crambidae (Kawazu et al. 2009).  My results from laboratory and field studies suggest 

that male response does not vary between populations in different regions in Michigan. I have 

reached this conclusion based in part on the results of choice tests using the Y-tube olfactometer, 

a methodology that has not been used to a large extent to study moth behavior. Although male 

moths did walk or fly through the apparatus and some fanned their wings, I did not observe the 

other pre-copulatory behaviors such as abdominal curling or attempted copulation with the top of 

the sample chamber adjacent to the pheromone source. This suggests that the methods used were 

adequate for movement behaviors, but did not provide an opportunity to observe behaviors later 

in the sequence before mating as observed in other related species (Cardé et al. 1975a, Baker and 

Cardé 1979b, Curkovic et al. 2006).  

A wind tunnel may be more suitable for choice tests between pheromone sources, and my 

conclusions certainly would be strengthened if comparable results were obtained in wind tunnel 

tests and Y-tube assessments. Wind tunnels have been used to determine the response of P. 

viteana response to leaf, shoot and cluster volatiles for lure development (Cha et al. 2008 a,b)  

and my original research plan did include testing male responses in the wind tunnel. However, 

previous researchers have found it difficult to get P. viteana to fly reliably in a wind tunnel (Greg 

Loeb, pers. comm.), and my efforts were hampered by logistical constraints including limited 

moth availability and insufficient time to work out wind tunnel methods. Thus I will leave this 

additional work for a future researcher. 

My original research plan also included collecting, analyzing and comparing sex 

pheromone composition in female P. viteana from different regions. This was attempted by 

excising the terminal abdominal segments that contain the pheromone gland and associated 

 

119 

structures, and placing groups of 10-20 glands in hexane to extract the pheromone. Despite 

combining moth samples this way from over 600 glands, analysis with GC-MS did not show 

distinct peaks that would allow me to determine whether pheromone composition varies between 

regions. I suspect that too many other compounds were present in the excised abdominal tips and 

these obscured the presence of pheromone. This also reduced the number of moths that were 

available for other experiments, and development of new extraction or analysis methods were 

beyond the scope of my research. Furthermore, the preliminary results from Y-tube bioassays 

and field trials with pheromone lures and captive females showed that males did not respond 

preferentially to females from the same region. These facts, along with the advice of my research 

committee, led me to invoke my researcher’s prerogative and leave the analysis of pheromone 

composition for future investigations. 

 My results do provide sufficient evidence to postulate that the low captures in the 

northwest grape growing region are due to lower population size than that in the southwest of 

Michigan. Investigating how P. viteana population size and native host plant abundance affects 

the number of males captured in pheromone traps in vineyards and natural areas across Michigan 

grape production regions would be an excellent graduate student research project. I encourage 

future students to consider comparing the captures in woodland in grape growing areas of 

Southwest and Northwest Michigan to captures in vineyards in those regions (see Chapter 2 

discussion). It would also be important to characterize habitat surrounding those vineyards, as 

the amount of wild grape present in this habitat is an important factor in determining risk of P. 

viteana infestation (Hoffman et al. 1992, Fergusson-Kolmes and Dennehy 1993, Botero-Garcés 

and Isaacs 2003, 2004a, Isaacs et al. 2012b).  

Coincidentally, there are new vineyard plantings in ‘The Tip of the Mitt’, Michigan’s 

newest AVA (American Viticultural Area) in the northcentral portion of Michigan’s lower 

 

120 

peninsula. This provides a unique opportunity to monitor the population of this major grape pest 

as the grape and wine industry expands into a heavily wooded area. This is appealing from an 

agro-ecosystem perspective, because early efforts to monitor the expansion of this native insect 

could be used to help prevent populations from reaching economically damaging levels. 

Additionally,  because P. viteana populations are presumably at low levels in these areas, IPM 

tactics such as mating disruption (Dennehy et al. 1989, Dennehy 1991, Jenkins and Isaacs 2008, 

Crowder et al. 2010, Isaacs et al. 2012a), biocontrol (Nagarkatti et al. 2002a, Jenkins and Isaacs 

2007b)  or cultural controls such as native host removal (Prokopy 2003, Jenkins and Isaacs 

2007a) or tilling ( Johnson and Hammar 1912, Isley 1917, Pettit 1932, Matlock et al. 2016) may 

be more effective than they have proved to be in areas with high P. viteana populations. If these 

tactics could be incorporated into an area-wide system of deployment, and if reduced-risk 

insecticides were used for insect management, the industry would likely benefit from better 

control, and allow the buildup of natural enemies through conservation biological control. This 

could reduce the need for chemical controls and increase vineyard sustainability. This presents 

an interesting opportunity for a research/extension project that would involve trapping and 

monitoring experiments, integrated pest management trials and building relationships with 

growers and other grape industry members (Kroma 2006, Ohmart 2008, Shaw et al. 2011). 

One important point to take from the results of Chapter 2 is that there is an immediate 

need to educate grape growers and vineyard managers in Northwest Michigan about the potential 

for rapid increases in P. viteana populations in this region. This could involve setting up a 

network of cooperating growers that will use sex pheromone monitoring traps to get baseline 

data to characterize the current size of local P. viteana populations. It would also be important to 

monitor traps from year to year to determine if populations are growing. Given that currently few 

moths are caught in pheromone traps in this region, scouting programs should be developed that 

 

121 

help grape producers recognize the characteristic signs of infestation on the clusters. These 

programs should also include training workshops that focus on using the MSU Enviroweather 

model (Isaacs 2017) to predict when egg laying is likely to occur and when treatments should be 

applied.  

The results of the cluster removal experiments in Chapter 3 provide a strong case for 

refuting my hypothesis that the presence of grape clusters reduces male moth captures in 

pheromone traps in the middle and late parts of the growing season. Similarly the canopy 

manipulation experiment in the same chapter shows that the dense juice grape canopy does not 

reduce male captures. In fact there were more males caught in traps in plots with unaltered 

canopies than in traps with an open canopy. My interpretation of the results of these two 

experiments is that grape shoots and leaves and the volatiles they produce are more important for 

mate (and trap) finding behaviors than the fruit. This agrees with the results of previous research 

that shows the relative importance of shoot and leaf volatiles compared with volatiles from fruit 

(Cha et al. 2008a,b).  

Male moths may first orient to the grapevine using leaf volatile cues, and then find 

females (or traps) by short hopping flights on grape shoots or walking along the shoot until a 

pheromone source is detected. Exploration of these topics could be accomplished by video 

recording male behavior around tethered or captive P. viteana females either in small 

observation chambers as described in Chapter 4, or in larger field cages set up over a single vine 

and seeded with male moths. Traps could also be modified by attaching natural or artificial 

shoots that provide walkways into the traps to determine if males use shoots to locate females or 

traps. The importance of shoot and leaf volatiles in trap finding could be explored further by 

comparing male captures in modified traps with artificial shoots that contain leaf volatiles, and 

traps with untreated artificial shoots. These experiments could provide some insight into how 

 

122 

males orient to traps and this could be used to improve male trapping consistency, and improved 

efficacy for better prediction of the activity and abundance of this pest. It is possible that new 

trap designs with artificial shoots could be used for future mass trapping or lure and kill 

experiments.  

It is widely known that temperature is an important factor in many aspects of insect 

physiology. Hence temperature influences the reproductive biology and mating behaviors in 

most insects. In Chapter 4, I measured the effects of temperature on several aspects of the 

reproductive biology of P. viteana. The positive relationships between temperature and 

longevity, flight ability, oviposition, mating frequency, male flight frequency, and the duration of 

mating period and male flight period, as well as the duration of the period of male activity 

relative to the period that females are receptive to mating were used to explain the observed 

phenology of male captures in pheromone traps and the large increases in oviposition that occur 

from the middle of the summer through the period of harvest in the autumn.  

 

My data reveal a strong link between temperature, mating and phenology. A logical next 

step for improving P. viteana management would be to incorporate some of these findings into 

the MSU Enviroweather model (Isaacs 2017) that predicts when grape berry moth oviposition is 

likely to occur. For example, given that mating and oviposition decrease with temperature and 

neither sex can fly below 14.5ºC, mathematical modeling could be used to estimate the expected 

level of infestation based on cumulative weather conditions using the data I have collected. This 

could inform grower management decisions for each P. viteana generation.  

 

A potential caveat lies in the limitations of using laboratory colonies to make inferences 

about what is happening in the vineyard. It is possible that this may have influenced some of 

myexperiments, and I think this is most evident in testing the effect of day length. For all of my 

experiments moths were reared in set conditions (28°C, 17:7 light:dark, 60% RH), and we cannot 

 

123 

rule out that immatures or adults were not irreversibly entrained to behave in specific ways that 

were molded by rearing conditions. This may have occurred despite adding new P. viteana stock 

to the colonies each year and allowing experimental colonies to acclimate to new treatment 

conditions for 3 to 5 days before taking data. For example, the length of the observed mating 

periods in the day length experiments were longer than we found in the constant temperature or 

diurnal temperature experiments (Figures  4.9, 4.13 and 4.17). Previous research with other 

tortricids has shown that moth mating periodicity can be entrained to a new temperature or day 

length regime in 24-48 hours (Cardé et al. 1975b, Castrovillo and Cardé 1979, Schal and Cardé 

1986). In addition, and related to the length of the mating period, the proportion of male flights 

outside of the mating period was considerably lower in the day length experiments compared to 

the constant temperature or diurnal temperature tests. This is particularly surprising given that 

the same conditions (28°C, 17L:7D, 60% RH) were included in the constant temperature and day 

length experiments. Why this occurred is not evident from my data, but a factorial experiment 

that varies day length and temperature conditions may help to explain these inconsistencies.  

Another important avenue of further research is found in the results of my field study to 

test male response to different quantities of pheromone, and different rates of pheromone release. 

I found in 4 out of 5 sampling periods that traps baited with lures containing 15µg of the 

standard pheromone blend caught significantly more male moths than traps baited with a 100µg 

lure that is similar to most commercial and experimental lures (Roelofs et al. 1971, Taschenberg 

et al. 1974, Jordan et al. 2013). The sampling periods encompassed the entire growing season 

and included a range of average daily temperatures from 16.8 to 22.7ºC.  The response to the 

15µg lure suggests that a reduced rate lure may provide more consistent male captures and allow 

for more precise monitoring during the entire season. It is likely that if male captures could be 

used as the biofix for the MSU Enviroweather model in the middle and late season, then the start 

 

124 

of the corresponding P. viteana egg laying periods could be more precisely estimated, allowing 

for improved insecticide application timing. 

 

My data show there is decreased attraction of lures with large quantities of pheromone 

during the middle and late season, and this effect appears to be linked to the high temperatures 

that occur during this part of the season. My data also suggest there is a rate effect and the 

reduction in captures is greater for lures with higher quantities of pheromone. Because 

pheromone release increases  and lure attraction decrease with increasing temperature, this likely 

contributes to reduced male captures in the middle and late summer when conditions are hot or 

warm (Sanders 1981, McDonough et al. 1989, Charlton et al. 1993, Cork et al. 2003, Cork 2016, 

Cardé et al. 2018). This could be tested empirically using a wind tunnel set up in a walk-in 

environmental chamber with adjustable temperature settings. The proportion of moths that fly, 

approach or contact different load lures at different temperatures could be compared across the 

lure loads and temperatures. This may also be possible in the field using temperature monitors 

and surveillance cameras set up to observe lures of different loads throughout the season and 

across a range of temperatures. 

 

My research has answered several questions, and I have pointed to how this new 

knowledge will inform P. viteana management. However, I have at the same time, created a 

number of additional lines of potential research into important facets of P. viteana mating 

biology and phenology, and these remain open for additional exploration.  

 

 

 

125 

 
 
 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 
 

APPENDIX 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

126 

RECORD OF DEPOSITION OF VOUCHER SPECIMENS 

 

 

 

 
The specimens listed below have been deposited in the named museum as samples of those 
species or other taxa, which were used in this research. Voucher recognition labels bearing the 
voucher number have been attached or included in fluid preserved specimens. 
 
 
Voucher Number: 2018-04 
 
 
Author and Title of thesis:  
Keith Scott Mason. 
FACTORS AFFECTING MATING, MONITORING AND PHENOLOGY OF GRAPE BERRY 
MOTH, PARALOBESIA VITEANA, IN MICHIGAN VINEYARDS. 
 
 
Museum(s) where deposited: 
Albert J. Cook Arthropod Research Collection, Michigan State University (MSU) 
 
 
Specimens:  
Family  
 
Tortricidae 
 
 
 
 
 
 

Paralobesia viteana  adult 

Life Stage   Quantity 

Genus-Species  

Preservation 

 

 

 

10 

 

pinned 

 

 

127 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

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128 

 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

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