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This is to certify that the

thesis entitled

Phenophase Dependent Tolerance to
Foliar Herbivory in Grape Vines,
Vitis labrusca (L.) var. 'Niagara'

 

presented by

Rodrigo J. Mercader

has been accepted towards fulﬁllment
of the requirements for

O O u E
M S degree in ntomology

 

 

’1 P c...

 

 

 

 

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Major professor

Date 19 August, 2002

 

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6/01 cJCIFICIDateDuepGSpts

Phenophase—Dependent Tolerance to Foliar Herbivory in
Grape Vines, Vitis labrusca var. ‘Niagara’ (L.)

By

Rodrigo J. Mercader

A THESIS
Submitted to
Michigan State University
in partial fulﬁllment of the requirements
for the degree of
Master of Science

Department of Entomology

2002

ABSTRACT

PHENOPHASE-DEPENDENT TOLERANCE TO FOLIAR
HERBIVORY IN GRAPE VINES, VI T IS LABR USCA VAR.
‘NIAGARA’

By
Rodrigo J. Mercader

This study measured the response of ﬁ'uitless Vitis labrusca (L.) var. ‘Niagara’
grapevines to defoliation during bloom and veraison, to determine how carbon source to
sink relations alter tolerance to herbivory. In these studies mechanical damage was
applied with hole punchers and beetle damage using adult Macrodactylus subspinosus
Fabricius (rose chafer) during bloom, and adult Popillz'a japonica Newman (Japanese
beetle) during veraison. The first set of experiments measured the seasonal growth and
single leaf and whole vine photosynthesis of potted vines damaged mechanically or by
beetles during bloom and/or during veraison. Also, the relative impact of mechanical and
beetle damage during bloom or veraison on carbon assimilation was measured. Tolerance
to foliar damage was higher during veraison than during bloom in these studies, and
beetle damage at veréison was found to have a more detrimental impact on carbon
assimilation than mechanical damage. A second set of experiments in a young vineyard
using mechanical defoliation also indicated that damage during bloom had a more
detrimental impact on vine growth than damage at veraison. Mechanical defoliation in
both of these studies was made on a percentage basis, so the results are not a reﬂection of
the higher leaf area present during veraison, but can be attributed to the relative carbon
sink activity in relation to the available source. Comparisons of different levels of

mechanical and beetle damage indicated a high level of tolerance to foliar herbivory.

ACKNOWLEDGEMENTS

I would like to thank my advisor Dr. Ruﬁis Isaacs for allowing me the opportunity
to work on this system, his patience, and help throughout this project. I would also like to
thank the members of my committee Dr. J. M. Scriber, Dr. G. S. Howell, and Dr. J. R.
Miller for their help and instruction during the past two years.

The work presented here would have not been possible without the help of a large
number of people. In particular I would like to thank the following people for their help
with this project, Keith Mason, Jason Keeler, Bruce VandenBosch, Kasey Watts, Ashley
Grieves, Anna Neiss, Elly Maxwell, Zsoﬁa Szendrei, Kelly Bahns, Jeff Eastrnann, Nikhil
Mallarnpalli, Natalia Botero-Garces, and all the members of Small Fruit Entomology. I
would also like to thank all the people not mentioned above that helped me with the
application of mechanical damage treatments in the vineyard at the Trevor Nichols
Research Complex.

I would also like to thank Dr. J. Wise and the staff of the Trevor Nichols Research
Complex for their help and the use of their facilities.

Finally, I would like to thank the members of the Small Fruit Entomology Lab for
being the great people that they are, and making the past two years a great experience for

me.

iii

TABLE OF CONTENTS

 

List of Tables ......................................................................................................................... vi
List of Figures _______________________________________________________________________________________________________________________ vii
Chapter 1
Project Introduction ................................................................................................................. 1
Literature Review _____________________________________________________________________________________________________________________ 2
Brief Overview of Compensation ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 2
Growth and Photosynthesis (Source: Sink Relationship) .......................................... 5
Tolerance to Damage in Grapevines ___________________________________________________________________________ 7
Growth and Phenophase in Grapevines in Terms of Source-Sink Relations ____________ 8
Sources ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 8
Leaves and Shoots ____________________________________________________________________________________________ 8
Roots, Canes, and Trunks ________________________________________________________________________________ 8
Sinks ____________________________________________________________________________________________________________________ 9
Shoots and Leaves ____________________________________________________________________________________________ 9
Roots, Canes, and Trunks ________________________________________________________________________________ 9
Source and Sink Relation During Bloom and Veraison __________________________________ 10
Bloom ________________________________________________________________________________________________________________ 10
Veraison ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 10
Study System ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, ll
Vitis Iabrusca var. ‘Niagara’ (L.) ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 11
Origin of the Niagara variety _____________________________________________________________________________ 12
Cultivation __________________________________________________________________________________________________________ 12
Attributes ____________________________________________________________________________________________________________ 12
Rose chafer, Macrodactylus subspinosus (Fabre) ...................................................... 13
Japanese beetle, Popilliajaponica Newman ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 14
Control Methods for the Rose Chafer and Japanese Beetle ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 18
Chapter 2

Phenophase Dependent Effects of Foliar Damage on the Growth and Photosynthetic
Capacity of Non-Bearing Juice Grape Vines, Vitis labrusca (Linnaeus) var. ‘Niagara’,___19

Introduction ..................................................................................................................... 19
Materials and Methods ................................................................................................... 22
Plant Material ................................................................................................................ 22
Mechanically Damaged Vines ..................................................................................... 23
Whole Vine Carbon Assimilation ...................................................................... 25

Single Leaf Carbon Assimilation _______________________________________________________________________ 26

Vine Growth ........................................................................................................ 2 6

Beetle Damaged Vines _______________________________________________________________________________________________ 28
Measurements Taken ......................................................................................... 29
Comparisons of Mechanical and Beetle Damage on Single Leaves ........................ 29

iv

Results 30

ooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooooo

Mechanically Damaged Vines ..................................................................................... 30
Carbon Assimilation __________________________________________________________________________________________ 30
Vine Growth Parameters ____________________________________________________________________________________ 31
Weights ............................................................................................................... 36
Beetle Damaged Vines ................................................................................................. 36
Carbon Assimilation __________________________________________________________________________________________ 36
Vine Growth Parameters ____________________________________________________________________________________ 41
Weights ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 41
Single Leaf Comparisons of Mechanical and Beetle Damage ................................... 41
Discussion _______________________________________________________________________________________________________________________ 47
Chapter 3
Phenophase-Dependent Effects of Foliar Damage on the Growth of Establishing Juice
Grape Vines, Vitis labrusca (Linnaeus) var. ‘Niagara’ ......................................................... 55
Introduction _____________________________________________________________________________________________________________________ 55
Materials and Methods ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 56
Plant Material ________________________________________________________________________________________________________________ 56
2000 ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 57
Statistical Analysis _____________________________________________________________________________________________ 58
2001 ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 58
Statistical Analysis ............................................................................................. 59
Results ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 59
2000 _______________________________________________________________________________________________________________________________ 59
2001 _______________________________________________________________________________________________________________________________ 62
Discussion _______________________________________________________________________________________________________________________ 63
Chapter 4
Grapevine tolerance to foliar damage by two temporally-separated scarab beetles and
by mechanical damage during bloom or veraison ................................................................. 68
Introduction ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 68
Materials and Methods ___________________________________________________________________________________________________ 70
Plant Material ________________________________________________________________________________________________________________ 70
Beetle Damage ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 7O
Growing Season Measurements ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 71
Post-Growing Season Measurements ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 72
Mechanical Damage ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 72
Growing Season Measurements ,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 74
Post-Growing Season Measurements ________________________________________________________________ 74
Statistical Analysis ________________________________________________________________________________________________________ 75
Results _____________________________________________________________________________________________________________________________ 75
Beetle Damage ______________________________________________________________________________________________________________ 75
Mechanical Damage _____________________________________________________________________________________________________ 7
Discussion 79

Chapter 5

Conclusion _______________________________________________________________________________________________________________________________ 85
Appendix 1 ______________________________________________________________________________________________________________________________ 87
References 90

vi

LIST OF TABLES

Table 2.1. End of season dry weight (g) of tissues on vines subjected to mechanical
damage treatements. Numbers within the same column followed by the same letter are
not signiﬁcantly different (P<0.05) ............................................................... 37

Table 2.2 End of season dry weight (g) of tissues on vines subjected to beetle damage
treatments. Numbers within the same column followed by the same letter are not
signiﬁcantly different (P<0.05) ..................................................................... 43

Table 3.1. Growth parameters taken from leaf loss and dormancy on vines damaged
during the 2000 growing season. Treatments with the same letters are not signiﬁcantly
different from each other at the P<0.05 level. Means separation performed by least
squares difference using the Tukey-Kramer adjustment method to control for
experimentwise error ................................................................................ 61

Table 3.2. Growth parameters taken leaf loss and dormancy on vines damaged during the
2001 growing season. Treatments with the same letters are not signiﬁcantly different
from each other at the P<0.05 level. Means separation performed by least squares
difference using the Tukey-Kramer adj ustrnent method to control for experimentwise
error ................................................................................................... 64

vi

LIST OF FIGURES

Figure 2.1. Representation of leaves damaged mechanically during bloom or veraison
after veraison damage treatment was applied. Black leaves represent undamaged leaves,
striped leaves represent leaves damaged during bloom, and spotted leaves represent
leaves damaged during veraison ................................................................... 24

Figure 2.2. Whole vine carbon assimilation of mechanically damaged vines at different
phenophases. Arrows represent points at which damage was applied. Signiﬁcant effects
(P< 0.05) of bloom damage treatment are denoted as b and of veraison damage treatment
as v .................................................................................................... 32

Figure 2.3. Single leaf CO2 assimilation of vines mechanically damaged at bloom, for the
four week period after vines were damaged ...................................................................... 33

Figure 2.4. Average single leaf C02 assimilation rates of vines mechanically damaged at
bloom and/or veraison, for the four-week period after vines were damaged at veraison.

Signiﬁcant effects (P< 0.05) of bloom damage treatment are denoted as b. No signiﬁcant
effects of veraison damage were found .......................................................... 34

Figure 2.5. Mean leaf area of mechanically damaged vines separated by the phenophase
at which the measurements were taken. Arrows represent points at which damage was
applied. Signiﬁcant effects (P< 0.05) of bloom damage treatment are denoted as b. No
Signiﬁcant effect of veraison damage was found ................................................ 35

Figure 2.6. Whole vine carbon assimilation of vines damaged by beetles at the
phenophases indicated by the arrows, separated by the phenophase at which
measurements were taken. Signiﬁcant effects (P< 0.05) of rose chafer damage treatment
are denoted as re and of Japanese beetle damage treatment as Jb ............................ 38

Figure 2.7. Single leaf C02 assimilation rates of vines mechanically damaged at bloom,
for the four week period after vines were damaged ........................................................... 39

Figure 2.8. Average of single leaf C02 assimilation of beetle damaged vines, for the

four-week period after vines were damaged at veraison with the Japanese beetle. No
signiﬁcant effects (P< 0.05) of rose chafer or Japanese beetle damage treatments were
found .................................................................................................. 40

Figure 2.9. Mean leaf area of beetle damaged vines separated by the phenophase at which
the measurements were taken. Arrows represent points at which damage was applied. No
signiﬁcant effects (P< 0.05) of rose chafer or Japanese beetle damage treatments were
found .................................................................................................. 42

vii

Figure 2.10. Single leaf carbon assimilation rates of leaves damaged mechanically, leaves
damaged with rose chafers, and undamaged leaves. All leaves initiated at the fourth node
and all measurements were taken at bloom. Measurements taken on damaged portions of
leaves include 25% leaf area removed in the cuvette. Means with different letter indicate
signiﬁcance (P<0.05) by day. Means separation was performed using the Student
Newman Keuls Method ............................................................................ 44

Figure 2.11. Single leaf carbon assimilation rates of leaves damaged mechanically, leaves
damaged with Japanese beetle, and undamaged leaves. All leaves initiated at the fourth
node and all measurements were taken at veraison. Measurements taken on damaged
portions of leaves include 25% leaf area removed in the cuvette. Means with different
letter indicate signiﬁcance (P<0.05) by day. Means separation was performed using the
Student Newman Keuls Method .................................................................... 46

Figure 4.]. Leaves of ‘Niagara’ grapevines after using a hole-puncher to apply
mechanical damage treatments of either 10, 20, or 30% interveinal leaf area
removal ............................................................................................... 73

Figure 4.2. Percent defoliation of total vine canopy area caused by two weeks of different
densities of adult rose chafer and Japanese beetle .............................................. 76

Figure 4.3. Cane diameter of vines damaged at bloom to different levels of defoliation,

measured at veraison. Means separation by Student Newman Keuls method. Treatments
with different letters are signiﬁcantly different at P < 0.05 .................................... 78

viii

Chapter 1

Project Introduction

Plant responses to herbivory may be modulated by their physiological state of
development (phenophase) and the demands placed upon them by their deve10ping
tissues at these times. When foliar herbivores remove photosynthetic area, plants can
become source-limited, and in source-limited plants the distribution of resources is
dependent on the strength of sink demands (Trumble et a1. 1993). The relative strength of
sink demands can potentially impact a plant’s response to herbivory, ranging from no
response to overcompensation, depending on the availability of resources at the time of
damage.

This project focused on the relationship between phenologically-based carbon
source to sink ratios and the compensatory responses of grapevines to damage by foliar
herbivores. This phenomenon was addressed using young juice grape vines (Vitis
labrusca var. Niagara), the rose chafer, Macrodactylus subspinosus, and the Japanese
beetle, Popillia japonica. This study tested the effects of source-sink relationships and
damage timing on plant compensatory response. Key attributes of the system studied
included a well-documented phenology and strength of relative sink demands in the vine,
and two economically important foliar herbivores that feed at two signiﬁcantly different
physiological stages; rose chafer adults feed during bloom and Japanese beetle adults

feed during veraison.

A primary goal of the work presented here was to gather information on vine
response to foliar damage, as part of a larger effort aimed at the future development of

damage thresholds for foliar damage in grapevines.

Literature Review

Brief Overview of Compensation to Herbivory

During their annual growth cycle, plants are often subjected to leaf area loss to
herbivores, potentially limiting resources for vegetative and reproductive growth. In the
1960’s and 1970’s the logical notion of a linear relationship between plant growth and
leaf area dominated much of the literature (reviewed by Trumble et a1. 1993). However,
since then the detrimental effects of foliar herbivory have been shown to be attenuated by
plant compensatory responses to foliar damage (reviewed by Trumble et a1. 1993,
Rosenthal and Kotanen 1994, Strauss and Agrawal 1999), and in some cases have been
shown to induce increased growth and productivity (e. g. McNaughton 1979, Owen 1980,
Paige and Witham 1987, Paige 1992, Vail 1992, Hjalten et a1. 1993, Paige 1994; but see
Bergelson and Crawley 1992). There are several potential reasons why plants may have
evolved not to be maximally efﬁcient, where any loss of leaf area could lead to a cost.
These include tradeoffs between selective pressures (e.g. competition, herbivory, soil
interactions) and physiological constraints (e.g. sink limitation, nutrient balance, growth
patterns).

The phenomenon of compensation has been attributed as an evolutionary response

to both herbivore damage and competition. Compensation may have evolved from

selective pressures from competition, because competition for light has led to strong
apical dominance in plants (Aarssen and Irwin 1991, Hjalten et al. 1993, Irwin and
Aarssen 1996). Therefore, when apical dominance is removed due to damage to the
apical meristem, secondary grth occurs leading to higher productivity under conditions
where intense competition for light is not present. An alternate hypothesis that
compensation has evolved due to herbivore selection pressure arises from the idea that
intensive and predictable herbivory could select for plants with restrained growth of
primary shoots (Crawley 1987, van der Meijden 1990, Vail 1992, Tuomi et al. 1994).
There is increasing theoretical and empirical evidence that plant tolerance is an
adaptation to herbivory (e.g. Dyer et al 1991, Jaremo et al. 1996, Nilsson et al. 1996,
Naber and Aarssen 1998, Sirnons and Johnston 1999, Strauss and Agrawal 1999).
However, as pointed out by Rosenthal and Kotanen (1994) other selective pressures that
damage plants (such as drought and ﬁre) can lead to the evolution of compensatory
mechanisms, and can be misconstrued as adaptations to herbivory.

Whatever the selective pressures leading to compensatory mechanisms, their
existence has been clearly documented (reviewed by Trumble et al. 1993, Rosenthal and
Kotanen 1994, Strauss and Agrawal 1999). Maschinski and Whitham (1989)
demonstrated how extrinsic factors (plant association, water, nutrients, and timing of
damage) interact to affect compensation in Ipomopsis arizonica. That study indicated that
depending on conditions affecting the physiological state of the plant, a continuum of
compensatory responses to damage existed. Other studies corroborate the importance of
extrinisic factors in determining a plants ability to compensate (reviewed by Trumble et

al. 1993; Hjalten et al. 1993, Shabel and Peart 1994, Weltzin et al. 1998), although the

effect of the extrinsic factor may be debated, such as the negative relationship reported
between nutrients and compensatory capacity (e.g. Ovaska et al. 1992, Gertz and Bach
1994, Mutikainen and Walls 1995, Irwin and Aarssen 1996).

In addition to extrinsic factors, several intrinsic factors affecting compensatory
mechanisms have been identiﬁed such as regrowth patterns, photosynthetic activity,
senescence, leaf morphology, and canopy architecture (reviewed by Trumble et al. 1993).
These intrinsic factors have been classiﬁed by Strauss and Agrawal (1999) into ﬁve
primary mechanisms involved in increased tolerance to herbivory: 1) increased net
photosynthetic rate after damage, 2) high relative growth rates, 3) increased branching or
tillering after release of apical dominance, 4) pre—existing high levels of carbon storage in
roots for allocation to above ground reproduction, and 5) ability to shunt carbon stores
from roots to shoots after damage. The ability to utilize these mechanisms is potentially
tied to carbon source: sink relations, since the relationship between sink and source
strength have been shown to be important in the regulation of photosynthesis (reviewed
by Flore and Lakso 1989, Wardlaw 1990) and growth (reviewed by Wardlaw 1990).
Under conditions in which extrinsic factors are not limiting, such as many agricultural
situations, carbon source: sink ratios are potentially a major factor inﬂuencing plant
tolerance to foliar damage.

This study was designed to understand the impact of phenological shifts in carbon
source: sink ratios on tolerance to foliar damage in grapevines. Timing of damage is often
considered an extrinsic factor (e.g. Maschinski and Whitham 1989, Trumble et al. 1993,
Strauss and Agrawal 1999), as the external environment (the herbivores) regulates it.

However, in this study I consider timing of damage to be an intrinsic factor, due to its

relation to source: sink ratios in plants. Source: sink ratios in plants change through time
depending on the strength of sinks (e. g. meristems, fruits, actively growing tissue, storage
tissues) and available sources (e.g. leaves, storage tissues), particularly in perennial plants

where the changes are seasonal as well as on a year-to-year basis.

Growth and Photosynthesis (Source: Sink relationships)

“partitioning is clearly inﬂuenced by both the supply and demand for
photosynthate and is moderated by vascular connections and the storage capacity of the
leaves and pathway tissues” (Wardlaw 1990).

The preceding quote summarizes the importance of carbon source: sink relations
to plant growth, but for a current review of sink regulation of photosynthesis see Paul and
Foyer (2001). As carbon is the major source of energy and dry weight, carbon
assimilation and partitioning have a central position in a plants ability to compensate for
foliar damage. For example, carbon balance was identiﬁed by Francesconi et al. (1996b)
as the primary force explaining the high tolerance to damage by European red mite,
Panonychus ulmi (Koch), in lightly cropped apples compared to normally cropped
apples. Furthermore, in the same study, whole canopy net C02 exchange rates (which
were negatively affected by mite damage) had a higher explanatory power for ﬁnal fruit
weight, return bloom, and return fruiting than cumulative mite days.

Upregulation of photosynthesis is considered to be a potential compensatory
mechanism (reviewed by Trumble et al. 1993, Strauss and Agrawal 1999) and several
studies have reported increased carbon assimilation on leaves of damaged plants (e.g.

Kliewer 1982, Chapman et al. 1991, Anten and Ackerly 2001). The ability to upregulate

photosynthetic rates has been suggested to be due to a reduction in the source: sink ratio
causing a release of feedback inhibition (Neales and Incoll 1968, Flore and Lakso 1989,
Layne and Flore 1995) or due to alleviated competition between leaves (Wareing et al.
1968, Aarssen and Irwin 1991, Ovaska et al. 1992, Iwin and Aarsen 1996). The reduction
in interleaf competition is mainly in the form of more available root produced cytokinins,
light, water, and nutrients (Waering 1968, Ovaska et al. 1992, Irwin and Aarssen 1996).
In addition to differences in photosynthetic rates, altered source: sink ratios can
drastically affect carbon allocation patterns. Various studies have indicated defoliation
can cause a shift in carbon allocation and translocation away from storage tissues and
towards shoot growth, leaf growth, and reproductive structures (e. g. Evans 1991,
Candolﬁ-Vasconcelos and Koblet 1990, Koblet et al. 1992, Candolﬁ-Vasconcelos et al.
1994, Tschaplinski and Blake 1995). These shifts in carbon allocation are in accordance
with studies on sink hierarchy, which generally indicate storage tissues are a lower
priority than vegetative and reproductive tissues (reviewed by Wardlaw 1990). Dry
matter partitioning in grapevines in relation to sink strength has been particularly well
studied for vines with varying crop loads. In a series of studies, Edson et al. (1993, 1995
a,b) documented the dry matter partitioning of ‘Seyval’ grapevines, Vitis vinifera (L.),
with a range of crop loads. Those studies found no differences in whole vine carbon
assimilation rates on vines with different crop loads. However, a marked difference was
observed in allocation of dry matter away from vegetative growth and towards
reproductive structures. Furthermore, Candolﬁ-Vasconcelos et al. (1994a) reported a
strong retranslocation of carbon reserves to support ﬁ'uit maturation in defoliated vines,

while no retranslocation was observed in non-defoliated vines. These studies further

illustrate the importance of source: sink relations in determining carbon allocation

patterns in grapevines.

Tolerance to Damage in Grapevines

High levels of tolerance to defoliation by removal of whole leaves in grapevines
have been well documented (Boucher and Pfeiffer 1989, Candolﬁ-Vasconcelos and
Koblet 1990, 1991, Candolﬁ-Vasconcelos et al. 1994b). Tolerance to high levels of
arthropod foliar damage has also been documented in grapevines (Laing et a1. 1972, J ubb
et a1. 1983, Boucher and Pfeiffer 1989, Welter et al. 1991, Candolﬁ et al. 1993; but see
Flaherty and Huffaker 1970, Welter et al. 1989a). One important consideration is that,
unlike annual plants, woody perennials rely upon their stored reserves for growth the
following season. Early in the season a relatively small number of leaves are present, and
most carbohydrates used for shoot growth are derived from storage tissues. Indeed, until
the 6-leaf stage in grapevines, shoot development is dependent upon re-translocation
from storage tissues, and not until bloom is the vine able to rely upon assimilates
produced during the current year (Yang and Hori 1979). This is an important
consideration when evaluating the degree of tolerance to foliar damage, as impacts may
only be seen in storage tissues or growth the following season or seasons. For example,
Welter et a1. (1991) found that the complete recovery of ‘Zinfandel’ grapevines to
Williamette spider mite, Eotetranychus williametti (Mcgreggor), required two damage-

free years.

Growth and Phenophases in Grapevines in Terms of Source-Sink

Relations

After centuries of grape production, a sizeable amount of information on vine
growth and development has been gathered. Not surprisingly, several books and reviews
have been written detailing the annual growth cycle of grapevines (e.g. Bush et al. 1895,
Winkler et al. 1974, Mullins et al. 1992). Here I will limit my discussion of the growth
cycle to the identiﬁcation of the primary sinks and sources in non-bearing vines at

different points in the season.

Sources

Lgvesﬁand shoots: Leaves are the primary source of photosynthate in grapevines.
However, several studies have indicated that single leaf measurements do not adequately
represent whole vine photosynthetic capacity (Edson et al. 1993, Edson et al. 1995 b,
Miller 1996, Miller et al. 1997). This is because single leaf measurements can be
inﬂuenced by leaf age (Kriedmann et al. 1970, Poni et al. 1994), source: sink interaction
(Hofacker 1978, Edson et al. 1995b, Petrie et al. 2000a), and the contribution of other
photosynthetic organs such as shoots (Kriedmann and Buttrose 1971).

Roots, Canes, and Trunks: As described above the initial ﬂush of growth in grapevines is
derived from the photosynthate accumulated the previous season. In Delaware
grapevines, Yang et al. (1980a) reported that early shoot development prior to the six-leaf
stage is entirely dependent upon retranslocated assimilates, and after this point the
retranslocation of assimilates gradually decreased until it stopped by the ﬂowering stage.

In addition to providing the necessary assimilates during the initial growth period,

retranslocation can take place during times of sink limitation. Candolﬁ-Vasconcelos et al.
(1994a) demonstrated that defoliation stress can alter natural translocation patterns,

directing carbon stored in storage tissues towards the fruit.

Sinks
Shoots and leales: Three to four weeks aﬁer buds break dormancy the season’s period of
most rapid growth begins and continues until approximately bloom when rapid shoot
elongation slows, initially at a rapid rate and then trailing at a continuously slower rate
(Winkler et al. 1974). After shoot elongation has slowed, carbohydrates begin to
accumulate in the shoots, the accumulation being slow at ﬁrst and then rapidly
accelerating, except for a possible slow down in fruiting vines during the ripening period
(Winkler et a1. 1974). Newly developing leaves in Delaware grapevines act as sinks until
reaching approximately 80% of their full size (Yang et al 1980b).
Roots. CanesLJand Trunks: Yang et al. ( 1980a) recorded the translocation of 14C fed to
leaves at different times of the season to shoots, cane and trunks, and roots. Prior to fruit
set, most of the labeled carbon recovered 24 hours after feeding was recovered from the
shoots (100% and 86% on the two days measured prior to ﬂower set). However, by the
ﬂowering stage the majority of the recovered labeled carbon was in the canes, trunks, and
particularly the roots. By midseason when xylem tissue began to become ligniﬁed, the
accumulation of labeled carbon became more pronounced in the roots than the canes and
trunks.

Data from ﬁeld studies on vine root growth appear to indicate that root growth

occurs only when other sinks in the vine are not using large amounts of photosynthate

(Williams and Matthews 1990). In addition, Miller et al. (1996b) reported an increase in
root weight in the period between veraison and harvest in uncropped vines and no

increase in root growth in cropped vines.

Source and Sink Relations During Bloom and Veraison

B_lggn_; As mentioned above, bloom is the point at which the vine shifts from reliance on
retranslocation of assimilates from storage tissues and becomes reliant upon
photosynthate produced during the current season. Bloom is also the point at which the
rapid rate of shoot production begins to decline. This situation leads to the presence of a
strong vegetative sink, a lowered quantity of stored assimilates, and relatively small
number of leaves present. For these reasons, at this point in the season the vine is liable to
have a lower source to sink ratio than during the remainder of the season in non-fruiting
vines.

Circumstantial evidence for the potential source limitation at this time of the
season exists from viticultural practices used during bloom to increase or reduce fruit set.
For example, reducing vegetative sinks by shoot tipping at bloom (removing competition
between vegetative growth and the relatively weak sink of grape inﬂorescences)
increases fruit set (Coombe 1959, Coombe 1962, Skene 1969), while leaf removal during
bloom (Candolﬁ-Vasconcelos and Koblet 1990) reduces fruit cluster set. The effects of
these practices indicate that vines at bloom are potentially source limited at bloom.
Veraison: During veraison, non-bearing vines lack the strong sink typically present at this
time of the season. Several studies found lowered photosynthetic rate per leaf area in

cropped vines during veraison compared to uncropped vines. Downton et al. (1987)

10

reported that the onset of the diurnal decline of photosynthesis occurred earlier in the day
for vines without ﬁ'uit. Studies on potted ‘Seyval’ vines reported lower carbon
assimilation rate per leaf area in uncropped vines when compared to cropped vines
(Edson et al. 1993, Edson et al. 1995a). In addition, higher dry matter accumulation has
been reported per leaf area in cropped vines compared to uncropped vines (Miller et al.
1996b, Petrie et al. 2000a). The results of these studies indicate that sink limitations can

occur during veraison in uncropped vines.

Study System

The rose chafer, Macrodaclylus subspinosus, and the Japanese beetle, Popillia
japonica, are two foliar pests considered to be of economic importance in juice grape
growing regions of Eastern North America. These insects are both highly polyphagous
scarab beetles, which as adults are leaf skeletonizers (Mcleod and Williams 1990, Potter
and Held 2002). Adult emergence is temporally separated, the rose chafer emerging
during bloom and the Japanese beetle during veraison. Both of these insects aggregate
while feeding and, depending on population size and vine susceptibility, can entirely

defoliate grapevines.

Vitis labrusca var. ‘Niagara’ (L.)

Vitis labrusca (L.) is native to North America, growing from New England to
Illinois, Ohio, and Indiana to the west and south to Georgia (Vines 1960). In it’s natural
habitat it is found in a variety of microenvironments including dry and moist areas, and

sun and shade areas (Van Dersal 1938). However, it is most commonly found in well-

11

drained alluvial soils (Van Dersal 1938). The vine is reported to grow slowly in its ﬁrst
year and quite vigorously once established (Van Dersal 1938), often found climbing or

trailing up to 40 ft (Vines 1960).

Origin of the Niagara Variety. The ‘Niagara’ variety was ﬁrst produced by C. L. Hoag
and B. W. Clark in Lockport New York in 1868, by fertilizing Vitis labrusca (L.) var.
‘Concord’ ﬂowers with V. labrusca (L.) var. ‘Cassady’(Hedrick 1919). The Concord
variety originated from plantings of seeds of a wild grape in 1843 by E. W. Bull in
Concord, Massachusetts one of the seedlings was named Concord (Hedrick 1919). The
Cassady variety originated in the yard of H. P. Cassady in Philadelphia as a chance
seedling (Bush 1895). Bush (1895) reported that the proprietors of the Niagara variety
kept a close guard on it’s planting in hopes of increasing its reputation in order to sell it a
higher price. Bush (1895) also reported that it had acquired an assured position as the

leading white market grape and that he had tasted a very ﬁne white wine made from it.

Cultivation. The Niagara variety is primarily used as a juice grape, and in Michigan is
the most actively planted variety, with 1145 acres planted between 1996 and 2000
(Kleweno and Matthews 2001). In 2000, 19,100 tons of ‘Niagara’ grapes were processed

(Kleweno and Matthews 2001).

Attributes. The Niagara grape variety is considered to be hardy (Edson and Howell
1989). However, it is not as hardy as V. Labrusca var. ‘Concord’, which may tolerate

temperatures of —20 degrees F arenheit (Howell and Wolpert 1978).

12

Rose chafer, Macrodactylus subspinosus (Fabre)

The adult rose chafer Macrodactylus subspinosus (Fabre) is a tan scarab beetle
approximately 13 mm long with long, spiny, reddish-brown legs that gradually become
darker near the tip (McLeod and Williams 1990). The eggs are oval, white, shiny and are
laid in sandy soils at approximately four to six inches in depth. The C-shaped grubs feed
on roots of grasses, weeds, grains, and other plants (McLeod and Williams 1990). This
beetle is distributed across much of North America east of The Rockies (Chittenden
1916, McLeod and Williams 1990). In areas where it occurs, regions with light sandy
soils are preferred as breeding grounds, and crops grown in clay soils are seldom affected
by rose chafer damage unless they are near sandy soils (Chittenden 1916). Chittenden
(1916) reports that after the rose chafer was ﬁrst noticed it “conﬁned its ravages to the
blossoms of the rose”, but also reports a record indicating it had been destructive to
grapes as early as 1810. By at least the late 1800’s the rose chafer was considered a major
pest of grapes in areas where it occurred (Bush et al. 1895, Chittenden 1916).

Rose chafers emerge in late May to early June in Michigan, approximately
coinciding with bloom in grapevines. The larvae feed on the roots of grasses, having a
particularly preference foxtail, timothy, and bluegrass (Hendrick 1919). Adults live for
about 4 to 6 weeks, and during this time eggs are laid about 15 cm deep in sandy or
grassland soil in groups of 6 to 40 (but each egg is deposited in a separate cavity). Eggs
hatch in 1 to 3 weeks, and the larvae feed on the roots of their hosts. Larvae overwinter
deep in the soil, and in early spring the grubs migrate upward and pupate in early May in

earthen cells (Anonymous 1997).

13

The rose chafer adult is highly polyphagous, feeding on a variety of omamentals,
cultivated trees and shrubs, along with a variety of fruit crops including grapes (reviewed
by Potter and Held 2002). The major economic damage caused by the rose chafer to
grapevines is from feeding upon developing ﬂowers and newly set berries. If not
controlled, heavy infestation can result in little or no grape production (McLeod and
Williams 1990). In addition to feeding on developing clusters these beetles feed on the
foliage, in some cases almost defoliating thin-leaved cultivars (Williams 1979, McLeod
and Williams 1990). The foliar damage caused by the rose chafer can be visually
alarming due to the gregarious nature of the beetle skeletonizing individual leaves. This

can create the perception of a signiﬁcant problem even under low infestation levels.

Japanese beetle, Papilliajaponica Newman

The Japanese beetle, Popillia japonica Newman, is a scarab beetle native to Japan
where it is considered a pest of minor importance. Prior to its introduction into the United
States, P. japonica’s range was limited to the main islands of the Japanese archipelago,
where it is common in Kyushu, Shikoku, Honshu, and Hokkaido (Fleming 1972). Within
this distribution it is most abundant in Northern Honshu and all of Hokkaido where
grasslands occur (Fleming 1972). The beetle was ﬁrst observed in the United States in
southern New Jersey in 1916 (Fleming 1972). Since then the population has expanded
over much of the Northeastern United States, where it has become a pest on turf grass
and a multitude of ornamental and horticultural crops. P. japonica has infested all states
east of the 85th meridian and north of the 35th parallel as well as Illinois and Indiana, and

has partially infested Michigan, Wisconsin, Minnesota, Nebraska, Iowa, Missouri,

14

Alabama, Georgia, and South Carolina (Allsopp 1996, Anonymous 2000). In Canada the
beetle has become established in the Niagara peninsula of Ontario, and in Belleview and
Ganonoque on the northern edge of Lake Ontario (Waithe 1991). In addition, P. japonica
was found on the Terceira island of Azores in 1974, and has since become established in
half of the island (Martins et al. 1988).

In the majority of its range, P. japonica has a one-year life cycle. The egg, three
larval instars, and pupal stages all occur underground and comprise approximately 80%
of the beetles lifespan. The beetle has a dormancy period, in which the larva forms an
earthen cell and remains in a state of arrested development throughout the winter, where
it can survive temperatures as low as —9.4°C (Fleming 1972). The cycle from egg to adult
is generally completed within one year; although in the coldest limits of its range the
larval stage is extended and the life cycle is completed in two years (Clausen et al. 1927).
The adult stage lasts for approximately 1 to 3 months, depending upon local conditions.
The availability of grassland or prairies is considered to be one of the main indicators of
the suitability of habitat for P. japonica. This notion is supported from the observation
that in its native Japan it occurs in areas where grasslands are abundant (Clausen et al.
1927, Fleming 1972), and that in the United States the same pattern is observed. The
larvae are able to feed on decaying organic matter, but their growth is signiﬁcantly
affected by the absence of living roots (Smith and Hadley 1926). The larvae feed on the
roots of a wide variety of grasses, and occasionally feed on the roots of fruit, vegetable,
or ornamental plants. Fleming (1972) reports that larvae do not thrive in plantings of
certain clover species (T rifolium spp. and Meliotus indica), soybeans (Glycine max),

buckwheat (F agopyrum esculentum), and orchardgrass (Dactylis glomerata).

15

 

Soil moisture appears to be the most important limiting factor affecting
oviposition and survival of all the immature stages. The eggs have no mechanisms to
retain water, and the absorption of water is necessary as a prelude to and during
embryonic development (Ludwig 1932). Ludwig and Landsman (1937) also found fairly
high water requirements for the developing larvae, pre-pupa and pupa. In general, P.
japonica is found in areas where the annual rainfall is uniformly distributed and averages
at least 250 mm during the summer (Fleming 1972). Oviposition usually occurs in the
closest suitable site to the plant on which the female was feeding, with a strong
preference for pasture lands (Fleming 1972). However, during droughts when soils are
fairly dry the female beetle will search for a more suitable site, usually selecting low
poorly drained ground, ﬁelds and turf under irrigation, and cultivated and fallow ﬁelds
where the soil is loose and moist (Fleming 1972).

Topography has a very strong effect on dispersal, particularly on dispersal
through appetitive ﬂight. The spread of P. japonica is facilitated by the presence of
nearly level or gently rolling country (Fleming 1972), as found in the areas of infestation
in the United States. Mountainous regions and large forests signiﬁcantly reduce the
spread of P. japonica, by providing ill suited habitat for development of the immature
stages (Fleming 1972). In the absence of strong winds adults can sustain ﬂight for
approximately 5 miles (Fleming 1972), enough to infest vineyards located within ﬁve
miles of grasslands or pastures as is the case in the majority of commercial vineyards in
Michigan.

P. japonica is a highly polyphagous species, feeding on the roots of a wide variety

of plants during its immature stages, and on the foliage and fruit of a wide variety of

16

plants as adults. The adults feed on approximately 300 plant species in 139 plant families
(Fleming 1972). Resistance to P. japonica adult feeding has been found in several plants
closely related to favored hosts (e.g. Fulcher et al. 1998). Even plants that are generally
considered to be non-hosts for the adults can induce feeding and subsequent growth
(Ladd 1989). In addition, adult Japanese beetles appear to be able to detoxify a large
number of plant toxins, as shown by feeding assays on plants known to cause paralysis in
the Japanese beetle. Adult P. japonica that previously fed on geranium, Pelargonium
domesticum, consumed seven times more geranium and had lower incidence of paralysis
than naive beetles (Potter & Held 1999). This study in a plant known to be toxic to P.
japonica indicates the strength and inducibility of detoxiﬁcation systems within this
species.

Loughrin et al. (1996, 1997) have demonstrated that P. japonica utilizes feeding-
induced plant volatiles to locate appropriate host plants within a mosaic of host and non-
host plants. This ability to utilize feeding-induced plant volatiles is not restricted to
feeding by other P. japonica, but includes feeding by other herbivores such as the fall
webworrn, Hyphantria cunea (Loughrin et al. 1997). This mechanism of host location
potentially allows P. japonica to locate suitable host plants that it has never encountered
before. In addition, this host-location mechanism also serves to create aggregations of P.
japonica on host plants. This results in the ability to rapidly locate mates, and high levels

of damage on individual plants.

17

Control Methods for the Rose Chafer and Japanese Beetle

Methods of controlling the rose chafer have evolved through time, beginning with
hand removal or shaking the beetles onto sheets as the sole recommended forms of
control (Bush et al. 1895). Later control methods, included cultivation to kill the pupae
and sweetened arsenical sprays to kill the adults (Hedrick 1919). The methods of
cultivation described by Hedrick (1919) were cultivating crops to disrupt the grasses on
which the larvae feed on and cultivating during the pupating stage to break the cells and
crush the pupae. Currently several insecticides are recommended for use against the rose
chafer in Michigan vineyards; Guthion, hnidan, Lannate, Sevin, Danitol, and Surround
(Gut et al. 2002). Control of the Japanese beetle is primarily accomplished through
chemicals. Chemicals recommended for its control are almost identical to those registered

for the rose chafer (Gut et al. 2002).

18

CHAPTER 2

Phenophase-Dependent Effects of Foliar Damage on the Growth and Photosynthetic
Capacity of N on-Bearing Juice Grape Vines, Vitis labrusca (Linnaeus) var.
‘Niagara’

Introduction

Leaf area loss due to damage by phytophagous insects presents an instantaneous
source of plant stress. The rapid loss of photosynthetic machinery can have a drastic
impact on the carbon economy of the plant, and can cause a direct shift in the carbon
source to sink ratio. A source-limited plant can incur signiﬁcant loss in terms of growth
and reproductive potential, as shown by the abundant examples of yield loss due to
arthropod foliar damage in crop plants (e.g. Welter et al. 1989a, Graf et al. 1992,
Francesconi et al. 1996a,b, Martinson et al. 1997, Norris 1997, Burkness and Hutchison
1998, Muro et al. 2001). However, the loss of photosynthetic machinery may not have
signiﬁcant effects at the whole plant level due to compensatory mechanisms that have
been found in various plants (reviewed by Trumble et al. 1993, Strauss and Agrawal
1999). The degree to which plants can tolerate foliar damage can depend on the
environmental conditions (Maschinski and Whitham 1989, Trumble et al. 1993, Hjalten
et al. 1993, Shabel and Peart 1994, Weltzin et al. 1998, Strauss and Agrawal 1999), and
on the physiological state of the plant (Trumble et a1. 1993, Rosenthal and Kotanen 1994,
Strauss and Agrawal 1999). Strauss and Agrawal (1999) identiﬁed the ﬁve primary
mechanisms reported to increase tolerance: 1) increased net photosynthetic rate after
damage, 2) high relative grth rates, 3) increased branching or tillering after release of

apical dominance, 4) pre-existing high levels of carbon storage in roots for allocation to

19

aboveground reproduction, and 5) the ability to shunt carbon stores ﬁom roots to shoots
after damage. A common thread amongst these mechanisms is that, as with most major
factors affecting plant growth and differentiation, they can be heavily affected by carbon
source to sink ratios.

The importance of source to sink ratios in determining a plant’s ability to
compensate for foliar damage can be seen in the various studies that have demonstrated
altered carbon assimilation rates and allocation patterns due to shifts in the source to sink
ratios (e.g. Flore and Lakso 1989, Layne and Flore 1995, Miller et al. 1996a,b Cruz-
Aguado et al. 1999). Edson et a1. (1993, 1995a,b) illustrated the impact of increased sink
strength on grapevine carbon allocation patterns by manipulating the number of clusters
per vine. Those studies indicated that total vine carbon may remain identical for vines
over a range of cluster numbers, but the allocation of resources drastically shifts
according to the size of the fruit sink. In addition, Candolﬁ-Vasconcelos et al. (1994a)
demonstrated that defoliation during the ripening period alters carbon translocation
patterns, moving carbon from lower tissues (storage sites) to the ﬁ'uits.

Varying source to sink ratios can also signiﬁcantly affect a vine’s ability to
tolerate foliar damage by directly affecting the size and the likelihood of causing a source
limitation due to herbivory. For example, carbon balance has been identiﬁed as the
primary force explaining the high tolerance of ‘Starkimson Delicious’ apples, Malus
domestica Borkh to damage by European red mite, Panonychus ulmi (Koch), in lightly
cropped trees compared to normally cropped trees (Lakso et al. 1996, Francesconi et al.

1996a,b).

20

An important aspect of carbon source to sink ratios in plants is that they are
highly dynamic and change throughout the season as sink strengths and available sources
shift. In apples, based on carbon assimilation rates and growth curves, Lakso et al. (1998)
were able to estimate that source limitations in apples could take place at two points in
the season, 2-3 weeks after bloom and at the end of the season. In grapevines, the relative
sink strength of various tissues in grapevines changes drastically throughout the growing
season, in accordance to their phenophase (Williams and Mathews 1990). This shift in
tissue activity during the growing season presents two important considerations to the
understanding of the impacts of foliar damage; 1) tissues will be affected differently
depending on the timing of damage, and 2) the impact of damage on a plant may shift
depending on the overall sink strength and the available source at the time of damage.
This emphasizes the need to consider the impact of source-sink interactions at the time of
damage, rather than simply focusing on whole season sink intensity.

The impact of insect foliar damage on plant growth is difﬁcult to assess directly
through the use of insects due to the high level of variation in feeding intensity that they
may produce, and the difﬁculty of controlling the quantity of damage produced.
However, the importance of understanding the speciﬁc effects of insect damage on
growth and photosynthetic capacity cannot be ignored. Insect damage simulations,
although useﬁil, have been shown to not accurately reﬂect insect damage (reviewed by
Baldwin 1990). In Michigan, the polyphagous leaf skeletonizing scarab beetles, the rose
chafer, Macrodactlus subspinosus (F.), and the Japanese beetle, Popillia japonica

(Newman) are considered to be pests of economic importance in vineyards. The

21

emergence of adults of these two beetles is temporally separated, with the rose chafer
emerging during bloom and the Japanese beetle during veraison.

This study examines how source-sink relations at the time of damage impact a
grapevine’s ability to tolerate foliar damage, using mechanically-simulated damage to
achieve accurate damage levels and using beetles to observe the response of leaves to
actual herbivory. We predicted that vines would be better able to tolerate foliar damage
during periods in the growing season when there is a relatively high source to sink ratio.
To test this, the growth and photosynthetic rates of non-bearing 1 yr old Vitis labrusca
(L.) var. ‘Niagara’ vines were measured before and after mechanical or beetle damage
during bloom and/or veraison. The use of non-bearing plants reduced the variability
introduced by crop load and ensured that time for compensatory growth was not a factor
explaining our results. Canopy size at bloom is small and the relative activity of
vegetative sinks is high early in the season. By veraison, leaf area is relatively high and
vegetative sinks are low (Williams and Mathews 1990).

In addition, we compared the impact of mechanical and beetle damage on the
photosynthetic rates of damaged and undamaged portions of leaves during bloom and

veraison, using the rose chafer during bloom and the Japanese beetle during veraison.

Materials and Methods
Plant Material. Eighty 1 yr old, own-rooted Vitis labrusca var. ‘Niagara’ grapevines
were weighed and planted in 8 liter pots in loamy soil on 23-24 April 2001. Vines were
trained on two 1.5 m stakes per pot and grown in the Michigan State University

greenhouse facilities under natural light conditions. Vines were fertilized with an all-

22

purpose fertilizer (15-30-15, N-P-K) on June 13, July 15, and August 20 2001.
Experimental vines did not bear clusters, but six cluster—bearing vines were grown

simultaneously under identical conditions to determine the appropriate phenophases.

Mechanically Damaged Vines. Vines of similar weights were assigned to two blocks of
12 plants each according to position along a greenhouse bench. Bloom damage or
veraison damage treatments were imposed on these vines in a 2 x 2 factorial design.
Vines were either damaged at bloom, at veraison, at bloom and veraison, or not damaged.
Damage consisted of removing 20% of the interveinal leaf area of each fully expanded
leaf using a hole puncher (size of holes = 38.5 mmz) to avoid damaging major veins. To
allow time for measurements to be taken, damage was applied to each block on
consecutive days; bloom damage was applied on 1 June 2001 for block 1 and on 2 June
2001 for block 2, and veraison damage treatments were applied on 13 or 14 August 2001
for block 1 and 2, respectively. Leaves were damaged only once, therefore vines
damaged only during veraison had the same level of damage after veraison damage

treatments were imposed as vines damaged during bloom and veraison (Figure 2.1).

23

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Whole Vine Carbon Assimilation: Whole vine carbon assimilation was measured using
the open gas exchange system outlined by Miller et al. (1996 c), using a CIRAS I infrared
gas analyzer (PP-Systems, Hertfordshire, UK.) to measure C02 concentrations. Early in
the season, weather conditions made ideal light conditions difﬁcult to obtain, and
therefore measurements used were taken at a minimum of 800 umol rn'2 s' l photon ﬂux
density. By midseason light conditions had signiﬁcantly improved and measurements
were taken at an excess of 1000 umol m'2 s'1 photon ﬂux density. Vines were allowed to
adjust to the chambers for 10 minutes and three measurements were taken per vine with
at least 5 minutes between recordings. The average of the three measurements were used
in the analysis. Temperature inside the chambers was generally within 0.2 °C of the
ambient temperature and never exceeding a 1.5 °C difference, mean ambient temperature
when measurements were taken was 30.33 at 0.16 °C, and ranged between 26.05 i 0.34
°C on September 29, 2001, and 34.9 2+: 0.95 °C on 12 June, 2001.

Whole vine carbon assimilation was recorded on alternate days for vines in blocks
1 and 2 on the following dates: at bloom (29, 30 May 2001), post bloom damage (9, 11
June 2001), midseason (10, 11 July 2001), veraison (12, 13 August 2001), post veraison
damage (28, 29 August 2001), and post full berry ripening (28, 29 September 2001).
Measurements taken prior to veraison were analyzed as a blocked one-way ANOVA,
with bloom damage as the sole treatment and initial vine weight as a covariate.
Measurements taken after veraison were analyzed by date as a blocked 2 x 2 factorial
analysis with initial vine weight as a covariate, using the SAS System Version 8

statistical package (SAS Institute 1999).

25

mle leaf carbon assimilation: Single leaf carbon assimilation was recorded using a
CIRAS I unit with a PL6U broad leaf cuvette (PP-Systems, Hertfordshire UK) with a 2.5
cm2 chamber and a light unit attached to the cuvette set at 1500 umol m’2 s'1 photon ﬂux
density. Carbon assimilation values were adjusted for damaged leaves by subtracting the
leaf area missing (holes were 38.5 m2), and using adjusted leaf area in the calculations.
Carbon assimilation calculations were made using a Microsoft Excel spreadsheet
developed by Parsons et al. (1998).

Single leaf carbon assimilation was recorded on leaves from a single shoot on
each vine. Data were taken from the basal leaf, a leaf at the third or fourth node position,
the most recently fully expanded (MRFE) leaf at bloom, the MRFE leaf 10 days after
bloom damage, the MRFE leaf at veraison, and the most recently fully expanded leaf 10
days after veraison damage. Recordings were taken on the leaves present 1 day prior to
damage treatments and once a week for 4 wks after damage treatments were imposed. In
addition, leaves were measured once a week for 3 wks during midseason (7-8,]4-15, 21-
22 July, 2001).

Measurements taken prior to veraison were analyzed as a blocked repeated
measure analysis of variance with bloom damage as the sole treatment, and initial vine
weight as a covariate. Measurements taken after veréison were analyzed as a blocked
two-factor factorial repeated measures analysis of variance, using SAS System Version 8
statistical package (SAS Institute 1999).

Vine Growth: Trunk diameter was measured directly below the main branching point

using Vernier calipers on 11 May, 14 June, 17 July, 16 August, and 13 September, 2001.

26

Total shoot length was measured keeping individual shoots and their laterals separate on
25 May, 13 June, 13 July, 16 August, and 13 September, 2001.

Leaf area was measured non-destructively using a linear correlation between the
length of the midvein (measured from the tip of the petiolar vein to the tip of the
midvein) and leaf area, as used by Edson et al. (1993) and Smithyman et al. (1998). To
determine this relationship all fully expanded leaves were removed from six vines grown
under the same conditions, and for each leaf the midvein length was recorded. The leaf
area of each leaf was determined using a HP ScanJet 6300c scanner and Scion Image-
Release Beta 4.0.2 software (Scioncorp). There was a strong relationship between midrib
and leaf area (r2=0.86, P<0.001) using the equation [Leaf Area=l.7243 X Midvein
lengthl'm‘]. The midvein length of every ﬁrlly expanded leaf on each vine was then
recorded throughout the season, and the total leaf area estimated using this relationship.

At the end of the growing season (once basal leaves had senesced), the vines
were destructively partitioned into leaves, shoots, trunks, and roots (5 and 10 October
2001) and maintained in a freezer (below 0 °C) until they could be dried. The individual
components were then oven dried at 80 °C until no further weight loss was observed. On
3 September, 2001 the senescent leaves were counted and collected as they fell and kept
frozen to dry along with all other leaves from the same vine.

Measurements taken prior to veraison were analyzed as a blocked one-way
ANOVA, with bloom damage as the sole treatment and initial vine weight as a covariate.
Where F-values for the blocking factor and initial weight were below 1, the analysis was
performed without using the block and initial weight as factors. Measurements taken

after veraison were analyzed by date as a blocked 2 x 2 factorial analysis with initial vine

27

weight as a covariate, using the SAS System V8 statistical package (SAS Institute 1999).
The effect of treatments on senescent leaves per vine was analyzed for bloom damage
within veraison damage and veraison damage within bloom damage with the non-
parametric Median test (reviewed by Zar 1999). This was due to data not being normally

distributed.

Beetle-Damaged Vines. Twenty vines of sirrrilar weights were assigned to two blocks as
described for the mechanically damaged vines, with eight plants in block 1 and 12 plants
in block 2. As with mechanically damaged vines, two treatments were imposed on these
vines, early season damage (2 wks post bloom) and late season damage (at veraison), in a
2 x 2 factorial design. Early season damage was induced with adult rose chafer,
Macrodactylus subspinosus, and late season damage with adult Japanese beetles,
Popillia japonica. Rose chafer beetles used in this study were collected with traps (Great
Lakes IPM, Vestaburg, Michigan) from ﬁelds with sandy soils surrounding peach
orchards in Oceana County Michigan on 20 June 2001. Japanese beetles were collected
with traps (Trécé Inc., Salinas, California) at the Trevor Nichols Research Complex in
Allegan County Michigan on 10 August 2001. In both of these cases, traps were emptied
the night before beetles were collected in order to ensure beetles used in this study had
spent no more than 1 d in traps. Vines were damaged by exposing each vine to 36 hours
of feeding by 120 beetles.

Damage levels on these vines were estimated by scoring the approximate percent
damage of each leaf, using the visual system used by Boucher and Pfeiffer (1989), and

estimating the leaf area of the damaged leaves in relation to the leaf area of the whole

28

vine, using the previously mentioned relationship between midrib length and leaf area.
During both of these damage periods, all vines were caged. in highly porous Bridal
illusion ﬁne mesh (Fabric Gallery, Williamston, MI) draped over supporting stakes and
fastened to the pot. These cages did not restrict plant gowth and cages were only placed
twice for no more than 40 hours.

Measurements taken: Vine gowth parameters, whole vine carbon assimilation, and
single-leaf carbon assimilation were recorded using the same protocol and analyzed in
the same manner as for the mechanical damaged vines. Single leaf carbon assimilation

measurements were all taken on undamaged portions of leaves.

Comparisons of Mechanical and Beetle Damage on Single Leaves. To compare the
impact of simulated and insect herbivory on carbon assimilation, twenty-four vines were
divided into two goups of 12 vines each. One of these goups was desigrated for
damage during bloom and the other for damage during veraison. Within the two goups
one leaf at the third or fourth node was selected ﬁom each vine and randomly assigred to
one of the following treatments: beetle feeding, mechanical damage, or no damage. The
three treatments were blocked into one goup, whereby the mechanically damaged leaves
received approximately the same percentage of leaf area loss as the beetle damaged
leaves in the same goup. Beetle feeding was applied by placing 10 beetles on each leaf
enclosed in a single cage made of white plastic mesh (mechanically damaged leaves and
no damage leaves were also caged for the same period of time). Treatments were applied
during bloom using rose chafers and during veraison using Japanese beetles. Mechanical

damage was applied using a hole-puncher (size of holes = 38.5 m2) at the same time.

29

C02 assimilation rates were measured on damaged and undamaged sections of the leaves
and on the leaf apical to the damaged leaf using the same CIRAS unit and cuvette system
described above. Measurements on these leaves were taken 1, 3, 8, and 16 d after damage
for the goup damaged at bloom and 1, 3, 10, and 17 d after damage for the goup
damaged during veraison.

The effect of damage on carbon assimilation rates were analyzed by date as a
blocked one-way AN OVA. Means separation was performed using the Student Newman

Keuls method, using the SAS System Version 8 (SAS Institute 1999) statistical package.

Results

Mechanically Damaged Vines.

QaLrboLassimilation: There were no signiﬁcant interactions in whole-vine carbon
assimilation between bloom damage and veraison damage treatments, so main effects
were analyzed separately. Ten days after bloom damage was imposed there was a
signiﬁcant reduction in whole vine carbon assimilation (F 1,13=5.95, P=0.03). This
difference was not signiﬁcant by midseason, and by veraison, no effect of damage was
apparent (Figure 2.2). Ten days after veraison damage treatments were imposed there was
a sigriﬁcant reduction induced by both bloom and veraison damage on whole vine
carbon assimilation (131,159.19, P=0.008 and F1,16=12.01, P=0.003, respectively).
However, by the post-harvest samples only bloom damage had a sigriﬁcant negative
effect on whole vine carbon assimilation rate (F 1,20=6.36, P=0.02 and F1,20=1.91,

P=O. 1 82, respectively).

30

Prior to veraison there were no signiﬁcant effects of bloom damage on single leaf

carbon assimilation rate (Figure 2.3). However, there was a sigriﬁcant negative effect of
bloom damage on carbon assimilation rates of basal and third to fourth node leaves
during veraison (F1,19=4.52, P=0.046 and F1,19=6.62, P=0.018 respectively). These
negative effects of bloom damage on photosynthesis later in the season (Figure 2.4)
appear to indicate an early senescence of vines damaged at bloom.
Vine growth pgameters: Mechanical damage had no sigriﬁcant effect on trunk diameters
or shoot length were found throughout the season. However, there was a sigriﬁcant effect
on leaf area gowth early in the season after bloom damage was imposed (Figure 2.5).
This effect was present 10 days, 1 month, and 2 months after bloom damage had been
imposed (F 1,22=14.66 P=0.001, F 1 32=10.11 P=0.005 and F132=4.89, P=0.039
respectively). Post-harvest, no effect of either bloom damage or veraison damage on leaf
area was observed.

Veraison and bloom damage both had sigriﬁcant impact on the number of
senescent leaves. Within vines damaged at veraison, bloom damage had no sigriﬁcant
impact (x2=0.41, P=0.52), but within vines not damaged at veraison, bloom damage
signiﬁcantly increased the number of senescent leaves (x2=4.9, P=0.027). In contrast
veraison damage sigiiﬁcantly decreased the number of senescent leaves on vines
damaged at bloom (x2=4.9, P=0.027), and no impact on vines not damaged at bloom

(x‘=1.37, P=0.24).

31

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33

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period after vines were damaged at veraison. Signiﬁcant effects (P< 0.05) of bloom damage treatment are denoted as b. No signiﬁcant

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Weights: There was no sigriﬁcant effect of mechanical damage at either bloom or
veraison on dry weights of leaves, shoots, or two-year old wood. However, there was a
signiﬁcant negative effect of both bloom damage (F 1,13 =23.7, P<0.001) and veraison
damage treatments (F1,lg= 6.25, P=0.022) on dry root weight. Bloom damage had a
sigriﬁcant negative effect on whole vine dry weight (F 1,1s=22.19, P=0.0087) whereas

veraison damage did not (Fug =3.12, P=0.0945)( Table 2.1).

Beetle-Damaged Vines

Defoliation levels induced by beetle damage were lower than those caused by mechanical
damage and therefore comparisons between beetle damage and mechanical damage need
to be made with caution. The mean defoliation caused by rose chafers was 8.0i1 .1%, and
the mean defoliation caused by Japanese beetles was 17.1:1: 2.4% of the total leaf area.
Carbon assimilation: As with mechanically damaged vines, there were no sigriﬁcant
interactions between bloom damage and veraison damage treatments in whole carbon
assimilation measurements, so main effects were analyzed separately (Figure 2.6).
Feeding by rose chafers or Japanese beetles did not impact carbon assimilation from the
beginning of the season through veraison. How‘EVer, measurements taken post-harvest
indicated a sigriﬁcant negative impact of Japanese beetle damage (F1,15=10.12, P=0.006).

No sigiiﬁcant effects of rose chafer or Japanese beetle damage on single leaf

carbon assimilation rates were found (Figures 2.7 and 2.8).

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Vine growth Dmters: There was no signiﬁcant impact of damage two weeks after
bloom or at veraison on trunk diameters and shoot length. In contrast to the effect of
mechanical damage during bloom, there was no signiﬁcant effect of beetle feeding on
leaf area throughout the season (Figure 2.9).

Weights: There was no signiﬁcant effect of feeding by either rose chafers or Japanese
beetles on the weight of leaf, shoot, or two-year old wood (Table 2.2). As with
mechanically damaged vines, foliar damage by rose chafers and Japanese beetles had a
signiﬁcant negative impact on dry root weights (F 1,14 = 26.78, P <0.001 and F1,” = 16.26,
P=0.001 respectively). However, unlike mechanically damaged vines, there was a
signiﬁcant negative impact of damage by rose chafers and Japanese beetles on total vine

dry weights (F1,14 = 9.86, P= 0.007 and F1,” = 8.75, P: 0.01 respectively) (Table 2.2).

Single Leaf Comparisons of Mechanical and Beetle Damage

Carbon assimilation rates of leaves damaged mechanically and with the rose
chafer during bloom exhibited a consistent pattern of response to damage (Figure 2.10).
There were signiﬁcant differences in carbon assimilation between damaged portions of
leaves and undamaged portions of leaves between 1 and 8 days after damage treatments
were applied. Measurements taken 16 days after damage treatments were imposed
indicated no signiﬁcant differences between undamaged vines and vines damaged at
bloom. However, measurements taken during this period were highly variable (Figure
2.10) and should not be considered a sign that damaged portions of leaves had
compensated photosynthetically at the tissue level. Measurements of undamaged portions
of rose chafer and mechanically damaged leaves did not detect a signiﬁcant difference

from the undamaged controls.

41

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Measurements taken from leaves damaged during veraison indicated a signiﬁcant
reduction in carbon assimilation rate 1 day aﬁer damage treatments were imposed in
damaged portions of leaves compared to undamaged portions. There was no signiﬁcant
difference in assimilation rates between undamaged portions of leaves (Figure 2.11).
However, by the third day after damage treatments were imposed, the earlier differences
could not be detected. Ten days after damage treatments were imposed, the undamaged
control had a signiﬁcantly higher carbon assimilation rate than damaged and undamaged
portions of leaves damaged mechanically or by the Japanese beetle (Figure 2.11).
Seventeen days after damage treatments were applied, undamaged portions of
mechanically damaged leaves had higher carbon assimilation rates than all other
treatments. In addition, no signiﬁcant differences between the undamaged control and the
damaged portion of mechanically damaged leaves were found. In contrast, a signiﬁcant
reduction in carbon assimilation rate between the undamaged control and both the

undamaged and damaged portion of Japanese beetle damaged leaves was found.

45

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46

Discussion

This study indicated that the ability of vines to tolerate foliar damage is dependent
upon the relative strengths of carbon sources and sinks at the time of damage, and that the
relative impacts of different modes of damage are dependent upon the timing of damage.
The effect of sink strength, as crop load, on tolerance to foliar damage the European red
mite, Panonychus ulmi (Koch), has been demonstrated previously in apples by Lakso et
a1. (1996) and Francesconi et al. (1996a,b). In grapevines, the importance of carbon
source to sink relations has been stressed by researchers working on the effects of crop
load on carbon assimilation and dry matter partitioning (e.g. Edson et a1. 1993, 1995a,b
Miller et al. 1996a,b, Petrie et al. 2000). This study builds on the knowledge gathered
from research on crop load, by using the principal of source-sink dynamics and applying
it to timing of damage. This study illustrates that the relation between carbon sources and
sinks at the time of damage has a stronger impact on grth than the level of damage
experienced by the vine.

Immediately after mechanical damage treatments at bloom and veraison, whole
vine carbon assimilation rates were reduced by both damage, indicating that foliar
damage at both of phenophases induced a source limitation. However, the negative
impacts of damage at bloom persisted throughout the season, but were not consistent
throughout the season. At midseason and early veraison there was no signiﬁcant effect of
bloom damage on whole vine carbon assimilation, but at veraison and post-harvest,
bloom damage had a signiﬁcant negative impact upon whole vine carbon assimilation.
The impact of bloom damage on whole vine carbon assimilation late in the season may

have been due to increased senescence of leaf tissue at this time, see below, or due to a

47

smaller root system caused by damage at bloom creating a smaller sink size. We did not
look directly at carbohydrate movement or root growth throughout the season and it is
therefore difﬁcult to speculate as to the causes of this reduction in whole vine
photosynthesis late in the season in terms of the source to sink relation in the vines.
Although no impact of bloom damage on whole vine carbon assimilation was
observed by midseason (Figure 2.2), impact upon growth was evident in the leaf area
present up to 2 months after damage was imposed (Figure 2.5). This lasting impact on
leaf area, but not on whole vine carbon assimilation could be explained by an increased
photosynthetic efﬁciency of the vines on a per leaf basis. Several studies have indicated
increased levels of photosynthesis in the remaining leaves of grapevines after partial
defoliation through whole leaf removal (Hofacker 1978, Kliewer 1982, Candolﬁ-
Vasconcelos and Koblet 1991). However, we failed to detect any signiﬁcant differences
in single leaf carbon assimilation rates prior to veraison at any leaf position (Figure 2.4).
Our single leaf results agree with studies in which damage was caused without removing
the whole leaf by either herbivores or mechanical simulations (Boucher et al. 1987,
Welter et al. 1989b, Candolﬁ et al. 1993). In these studies no increase or decrease in
carbon assimilation rates was observed on damaged leaves. The lack of any differences
detected upon whole vine carbon assimilation may be due either to the presence of a
small difference in carbon assimilation rate undetected by our set up, or within-canopy
interactions such as lower self-shading, greater air movement, and leaf angle. Other
studies comparing whole vine and single leaf assimilation rates in grapevines have also
indicated large discrepancies between whole vine and single leaf carbon assimilation

measurements (e. g. Edson et al. 1993, Edson et al. 1995b, Miller et al. 1997).

48

The signiﬁcantly lower exact leaf area carbon assimilation measurements on the
basal and 3-4 node leaves on vines damaged at bloom (Figure 2.2), are indicative of early
senescence. These two leaves were the oldest leaves measured and a lower carbon
assimilation rate is associated with leaf age and senescence (Kriedmann 1968, Flore and
Lakso 1989). In addition, leaves on vines damaged at bloom were observed to senesce
earlier. Accelerated leaf senescence has been observed as a plant compensatory response

to various stresses including drought, excess water, minerals, temperature, pathogens
(reviewed by Smart 1994), and O3 (reviewed by Pell et al. 1994). Edson (1993) observed

increased senescence on the basal leaves of vines with high crop loads compared to those
with medium, low, or no crop present. This indicates that carbohydrate-induced stresses
may also be a factor inﬂuencing leaf senescence. In addition, in a study comparing shoot
number and dry matter accumulation and partitioning in non-bearing grape vines, Miller
et al. (1996a) found no differences in whole vine dry weight or dry weight partitioning
between budburst and veraison, but a signiﬁcant reduction in dry weight accumulation
between veraison and harvest. The similarity between these results appears to indicate a
potential for reduced dry matter accumulation late in the season caused by high stress
levels early in the season. However, a mechanism for such a relationship is unknown, and
further investigation of early season stress levels on late season dry matter assimilation is
needed.

Despite the difference in leaf area observed early in the season, by post-harvest
there was no signiﬁcant difference in leaf area detected between any of the damage
treatments and undamaged control vines (Figure 2.5). The similar leaf and shoot dry

weights indicate that this was not due to thinner leaves or shoots being produced. No

49

increase in carbon assimilation was detected at any point throughout the season. Rather,
only reductions in whole vine carbon assimilation were detected, indicating that the
absence of differences between any of the damage treatments was not due to a
compensatory photosynthetic response.

The lack of difference in above ground grth despite the absence of higher
carbon assimilation rates can be understood in terms of carbon allocation patterns. During
the period between bloom and veraison, shoot and leaf growth are the primary sinks and
therefore a source limitation is most likely to be observed in the storage tissues. In
addition, Candolﬁ-Vasconcelos et al. (1994) demonstrated that stress levels induced by
defoliation can induce re-translocation of assimilates from the roots. Through a shift in
allocation patterns, the difference in leaf area produced before veraison could have been
mitigated by the time of harvest. Miller et al. (1996b) found an increase in leaf dry weight
in the period between veraison and harvest in non-bearing vines, but at a rate much
slower than between bud-burst and veraison, suggesting that the relative sink strengths of
leaves and storage tissues had changed. They found that in non-bearing vines, roots
accumulated dry weight faster than any other organ in the period between veraison and
harvest. In this study damage at bloom had a signiﬁcant negative impact on root weight,
and bloom-damaged vines exhibited a greater allocation towards the current seasons
growth and away from the roots (Table 2.1). However, we also found that damage at
bloom caused a reduction in whole vine carbon assimilation rates during veraison and
post harvest, which may have caused signiﬁcant reductions in root weight at this time.

Because damage was applied on a percentage basis and only on previously

undamaged leaves, vines damaged only during veraison and those damaged during bloom

50

and veraison had the same level of damage imposed upon them (Figure 1). The ﬁnding
that vines damaged during bloom and veraison had lower dry root weights than vines
damaged only during bloom or only during veraison (Table 2.1), indicates that bloom
damage compromised the vines ability to compensate for damage during veraison.
Veraison damage also led to a reduction in root weight. However, unlike bloom damage
there was no signiﬁcant difference observed in total vine weight when compared to the
undamaged control. This indicates that damage at veraison may have induced a source
limitation, but it did not affect vines as severely as bloom damage did. During veraison
non-bearing vines lack the strong sink typically present at this time of the season.
Previous studies have indicated lowered photosynthetic rate per leaf area in cropped vines
during veraison compared to uncropped vines. For example, Downton et al. (1987)
reported that the onset of the diurnal decline of photosynthesis occurred earlier in the day
for vines without fruit. As a result those vines ﬁxed 22% less carbon than ﬁ'uiting vines,
an indication that fruitless vines at veraison are sink limited. In addition, using potted
‘Seyval’ vines Edson et a1. (1993, 1995a) showed a lower carbon assimilation rate per
leaf area in uncropped vines when compared to cropped vines. Further evidence comes
from reports of higher dry matter accumulation per leaf area in cropped than in
uncropped vines (Edson et al. 1993, Miller et a1. 1996, Petrie et al. 2000).

Prior to qualitative comparisons between mechanically damaged vines and beetle
damaged vines, two major differences in treatment application need to be recognized;
early season rose chafer herbivory was applied two weeks after bloom and only removed
an average 8% of the leaf area compared to 20% in mechanical damage treatments. The

difference in timing of damage is highly important, as Candolﬁ-Vasconcelos et al.

51

(1994b) found no effect of whole leaf removal treatments starting at pea size berry on
single leaf photosynthesis, while Candolﬁ-Vasconcelos and Koblet (1991) found a
signiﬁcant increase in single leaf photosynthesis in vines defoliated by whole leaf
removal starting around bloom. Damage induced by the Japanese beetle during veraison
was more similar to mechanical damage treatments at 17% mean defoliation, applied
within 3 days of mechanical damage. The small level of defoliation caused by the rose
chafer probably explains the lack of major effects upon season long growth parameters
and photosynthetic efﬁciency. However, as with mechanical damage at bloom, there was
a signiﬁcant negative impact upon root and whole vine dry weight (Table 2.2),
illustrating that despite the low level of damage, herbivory early in the season can still
have a strong impact upon vine growth and allocation patterns.

The response of vines to Japanese beetle herbivory suggests a greater impact of
beetle damage than mechanical damage at veraison. Whole vine carbon assimilation at
post-harvest was signiﬁcantly reduced by Japanese beetle damage (Figure 2.6). In
addition, unlike in mechanically damaged vines, a negative effect on whole vine dry
weight was observed (Table 2.2). Mechanical simulations of herbivore damage rarely
reﬂect feeding damage accurately, because factors such as the time required to perform
damage, the tissues damaged, the amount of cellular shearing, and/ or the presence of
frass and saliva (Baldwin 1990) may be required for the full response. In apples, Hall and
F erree (1976) found that the amount of cut surface had a higher impact on photosynthetic
rate than the amount of leaf area removed. Damage by these leaf-skeletonizing beetles
can create a larger proportional level of cut surface to leaf area removed than can

mechanical damage induced with hole punchers. In addition, the instantaneous removal

52

of leaf tissue by hole-punchers is markedly different from the slower tissue removal
caused by insect mandibles.

The comparisons of carbon assimilation rates between similar levels of damage
to single leaves by mechanical and beetle damage during bloom and veraison illustrate
some of these differences. In these experiments only a single leaf was damaged and
therefore the source to sink relation at the whole vine level is unlikely to have been
affected. Although the rose chafer and Japanese beetles are both polyphagous leaf
skeletonizers producing visually similar types of damage, the results indicate a
differential response of vines to these two beetles as compared to undamaged and
mechanically damaged leaves (Figures 2.10 and 2.11). The differences found between
these two damage timings are most likely a reﬂection of responses to damage inﬂuenced
by leaf age and activity at the time of damage. Leaves damaged mechanically or by rose
chafers during bloom maintained a similar pattern of response, whereby undamaged
portions of leaves had similar carbon assimilation rates as the undamaged controls while
damaged portions had a reduced assimilation rate. In contrast, in leaves damaged during
veraison mechanical damage had a lesser negative effect than beetle damage 17 days
aﬁer damage (Figure 2.11). The difference was found on both damaged and undamaged
portions of the leaf indicating that the difference in assimilation rates was not simply due
to the amount of damaged area, but likely a systemic reaction at the leaf level.

In a study measuring the effect of different densities of hole punches on carbon
assimilation, Boucher et al. (1987) found that on leaves with low levels of damage there
was a greater depression of assimilation rate 12 days after damage was inﬂicted. That

result is similar to our results for 10 day after damage (Figure 2.11). However, in this

53

study 17 days after damage treatments were imposed undamaged portions of
mechanically damaged leaves had a signiﬁcantly higher carbon assimilation rate than the
undamaged control, and no signiﬁcant differences were found between damaged portions
of mechanically damaged leaves and the undamaged control. The release of feedback
inhibition or the creation of a new sink due to the mechanical damage is unlikely due to
the delay in response. In addition, an induction of higher root produced cytokinin levels
reducing leaf senescence is unlikely, as there was no reduction in competition between
leaves. This increase in photosynthetic rate in mechanically damaged leaves, and
reduction in photosynthetic rate of Japanese beetle damaged leaves, illustrates that leaf
age and type of damage have a potentially strong interaction.

In conclusion, the results presented in this study demonstrate the importance of
vine phenology when considering response to damage. Source-sink interactions are a
critical component of plant physiology that has been used to understand the effects of
crop load on vine growth (e.g. Edson et a1. 1993, 1995a,b). The results in this study
demonstrate the importance of source-sink interactions at the time of damage on vine
tolerance to foliar damage. The application of mechanical damage treatments on a
percentage basis in this study removed intensity of damage and whole season sink size as
factors explaining the increased tolerance to damage at veraison when the source to sink
ratio was highest. In addition, the results from this study illustrate the importance of
timing of damage and plant physiology on the adequacy of mechanical simulations of
herbivory. This study stresses the importance of studying herbivory within the

physiological context of the plant.

54

CHAPTER 3

Phenophase-Dependent Growth Responses to Foliar Damage in Establishing Juice
Grape Vines, Vitis labrusca (Linnaeus) var. ‘Niagara’

Introduction

In Michigan, Vitis labrusca var. ‘Niagara’ grapevines have been planted at a
faster rate than any other grape variety in the past 20 years (Kleweno and Matthews
2001). The establishment period of grapevines is a highly important period as a poor start
can hinder vineyard productivity for several years (Zabadal 1997). The smaller size and
lower levels of carbohydrates generally found in the storage organs of young vines can
signiﬁcantly reduce the compensatory abilities of young vines to foliar damage compared
to those of mature vines. However, in their ﬁrst years of establishment, vines bear very
little or no fruit, and the fruit that is produced are generally removed. The lack of fruits as
carbohydrate and nitrogen sinks in young vines may create a signiﬁcantly greater relative
source to sink ratio during veraison compared to that of mature vines. Several studies
have found that sink demand strongly inﬂuences carbohydrate production (Wardlaw
1990), and studies using potted grapevines have indicated sink limitations in ﬁ'uitless
vines during veraison (Miller et al. 1996b, Petrie et al. 2000a). The potential for a sink
limitation during veraison indicates that in non-bearing vines a high level of tolerance to
foliar damage may be present at this time.

The lack of fruits in young vines changes the plant protection strategies
employed, as there is no need to control fruit damaging pests (such as the grape berry
moth, Endopiza viteana). Insecticides used are generally broad spectrum in nature, and
therefore also control foliar pests such as the rose chafer, Macrodactylus subspinosus,

and the Japanese beetle, Popillia japonica. For this reason it is important to understand

55

how young vines react to damage, as they may be vulnerable to foliar damage at this time
and control methods would be targeted mainly at these indirect pests. In addition, the
potential for high levels of tolerance to foliar damage late in the season may allow for a
reduction in the use of insecticides even under high infestations in young V. labrusca
vines.

This study examines the relative ability of young V. labrusca (L.) var. ‘Niagara’
vines to tolerate foliar damage during bloom and veraison. In particular this study tested
whether non-bearing grapevines are capable of higher tolerance to damage during
veraison than bloom, as would be expected by the higher source to sink ratio at this time.
This was tested by a study in 2000 where similar absolute levels of damage were
performed during bloom and/or veraison, and in the 2001 by damaging vines on a

percentage of their total leaf area at bloom and/or veraison.

Materials and Methods
Plant material. This study was undertaken in a V. labrusca (L.) var. ‘Niagara’ vineyard
established in 1999, at the Trevor Nichols Research Complex in Fennville, Michigan.
Two shoots from two canes (total of four shoots) of each vine were trained onto a 1.37
meter high bilateral cordon Hudson River Umbrella trellis system. There were seven
vines per row, with 1.8 meters in between vines and 3 meters between rows. Vines were
maintained using 45.5 kg of Urea fertilizer (46% Nitrogen) per acre, applied on 16 March
2000 and 102.3 kg of Urea on 25 March 2001, and standard plant protection program
(Gut et al. 2002), except on rows where vines were caged with beetles. On these rows, no

insecticides were applied at least one month prior to beetles being caged on vines and

56

insecticide and ﬁmgicide applications were postponed until cages were removed.

Treatments were initiated in spring 2000.

2000 Experiment. Sixteen vines with cane height between 0.5m and 1.0m were selected
to receive mechanical damage treatments during bloom and/or during veraison.
Treatments were imposed in a 2 x 2 factorial design; vines were either damaged at bloom,
at veraison, at bloom and veraison, or not damaged. Leaf area was removed using hole
punchers (size of holes = 38.5 ml). This was done to avoid all major veins in order to
imitate beetle feeding and to avoid the differential impacts on photosynthetic capacity
caused by interveinal damage when compared to whole leaf removal or treatments
including midrib and main lateral vein damage (Hall and Ferree 1976, Boucher et al.
1987). Damage at bloom consisted of removing 30% of the total leaf area of every fully
expanded leaf during bloom between the 19-21 June 2000. Damage during veraison (15-
16 August 2000) consisted of removing 30% of the leaf area of every fully expanded leaf
on 1.5 m of each shoot, starting at the point where the shoot ﬁrst reached the trellis. To
ensure appropriate damage levels were applied, visual aids were made for use while
damaging leaves.

During the 2000 growing season, vegetative growth parameters were measured at
trace bloom (13-14 June), at veraison (6 August), and after leaf senescence (21 October)
on vines damaged at bloom and veraison. In addition, the number of mature nodes and
the total shoot length were measured after leaf loss (10-11 November).

On 26 January, 2001, all vines were pruned to 15 nodes per shoot and the weight

of wood pruned off (pruning weights) was determined by immediately tying all the

57

cuttings, and weighing them with a Stren digital scale (Stren, Madison, NC.) in the ﬁeld.
Prior to bloom the following season (2001) the diameter of canes (9 May), and the
number of nodes remaining dormant after the 16 inch shoot grth stage had been
reached (22 May) were recorded on all vines.

StatisticaLAnalvsis. Measurements taken prior to veraison damage were analyzed as a
one-way ANOVA, with bloom damage as the sole treatment and cane diameter at trace
bloom as a covariate. Measurements taken after veraison damage were analyzed by date
as a 2 x 2 factorial analysis with cane diameter at trace bloom as a covariate, using the
SAS statistical package (Version 8, SAS Institute 1999). The analysis of pruning weight
data indicated a signiﬁcant bloom damage by veraison damage interaction, therefore
bloom damage was analyzed within veraison damage and veraison damage within bloom
damage. This was performed using the “LSmeans Slice” function of ProcGLM (Version

8, SAS Institute 1999).

2001 Experiment. On 20 February, 200,1 40 vines were pruned to 15 nodes on each of
two canes and the pruning weights recorded as described above. The number of shoots on
these vines were adjusted to four per cane on 8 May, 2001. Due to strong winds between
5 June 2001 and 11 June 2001, vines lost shoots and only 28 vines were retained for the
experiment. Vines were assigned to three blocks according to shoot number; there were
12 vines with 5 shoots, 12 vines with 6 shoots, and 4 vines with 7 shoots. These vines
were mechanically damaged during bloom and/or veraison as a 2 x 2 factorial design
within each block. Bloom damage consisted of removing 20% of the total leaf area of all

fully expanded leaves between 18 June and 19 June 2001, and veraison damage consisted

58

of removing 20% of the total leaf area of all fully expanded leaves between 21 August
2001 and 24 August 2001. Because leaves were damaged only once, vines damaged only
during veraison had the same level of damage as vines damaged during bloom and
veraison.

Vegetative growth parameters were measured during the 2001 growing season at
node burst, bloom, midseason, veraison, and post harvest. On each vine, the length of
main shoots (ll-14 June, 9-13 July, 8-14 August, 9-14 October), the node number of
main shoots (ll-l4 June, 9-13 July, 8-14 August, 9-14 October), the node number of
lateral shoots per main shoot (18 July, 20 August, 23 October), and cane diameters (14
May, 13 June, 11-13 July, 6 August, 25 September) were measured. On 17, 24 February,
and 4, 5 March 2002, the number of mature nodes was recorded on all experimental
vines, and these vines were pruned to 15 nodes per shoot and the pruning weights
measured as above.
mtg Analysis. Measurements taken prior to veraison damage were analyzed as a
blocked one-way ANOVA with bloom damage as the sole treatment and the pruning
weights as covariates. Measurements taken after veraison damage were analyzed by date
as a blocked 2 x 2 factorial analysis with pruning weights as covariates, using the SAS
System V8 statistical package (SAS Institute 1999). Where F -values for the blocking
factor were below 1 they were considered to be ineffective (Kuehl 2000), and the analysis

was performed without the blocking factor.

Results

2000 Experiment. Damage at bloom did not cause any reduction cane diameter, or node

59

number when vines were measured at veraison (F1,12=l.7l, P=O.30 or F1,12=0.25, P=0.63
respectively). No signiﬁcant interactions between bloom and veraison damage were
observed in the growth parameters measured after leaf senescence. These measurements
indicated that damage at bloom had no signiﬁcant effect of damage on cane diameters
(F1,1o=0.02, P=0.88), total node number (F1,1o=2.66, P=0.13), and mature node number
(F 1.10:1-99, P=0.19). Damage at veraison also had no signiﬁcant impact on the above
ground grth parameters (cane diameters: F1,10=0.19, P=0.67; total node number:
F1,10=0.24, P=0.64; mature node number: Fug: 0.66, P=0.44). However, damage at
bloom did have a signiﬁcant negative impact upon shoot length (F1,1o=6.64, P=0.03),
while damage at veraison did not (F1,10=0.45, P=0.52). This difference in shoot length
due to bloom damage was not found in our means comparisons (Table 3.1).

Damage at both bloom and veraison signiﬁcantly affected pruning weights. In this
case there was a signiﬁcant interaction between the damage timings. Within vines that
were not damaged at bloom, veraison damage caused a signiﬁcant increase in pruning
weights (F 1,10=10.77, P=0.01). However, among vines damaged during bloom, damage at
veraison caused a signiﬁcant reduction in pruning weights (F 1.10:5-79, P=0.04). Within
vines damaged at veraison, bloom damage had a signiﬁcant negative impact on pruning
weights (F 1,10=41.2, P<0.01), and within vines not damaged at veraison bloom damage

had no signiﬁcant impact on pruning weights (F 1,10: 0.61, P=0.45) (Table 3.1).

60

 

 

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61

Cane diameters measured prior to bloom in the 2001 growing season were
signiﬁcantly impacted by damage at bloom during the previous season (F1,1o=6.5,
P=0.03), but no signiﬁcant difference in cane diameters was found in vines damaged at
veraison (F1,1o=0.51, P=0.49). No signiﬁcant effects of either bloom (F 1,10=0.37, P=0.56)
or veraison (F1,1o=0.05, P=0.82) damage were observed in the number of nodes remaining

dormant after the 16 inch shoot grth stage.

2001 Experiment. At midseason no signiﬁcant impact of bloom damage was observed
on shoot length (F133 =0.29, P=0.60), total node number (F1,23=0.04, P=0.85), main shoot
node number (F1,23=1.67, P=0.21), lateral shoot node number (F133=0.35, P=0.56), or
cane diameters (F 1,23=0.12, P=0.73). However, by veraison, bloom damage had a
signiﬁcant negative impact upon the total number of nodes (F133=6.59, P=0.02), number
of nodes on lateral shoots (F 1,23= 6.32, P=0.02), and shoot length (F 1 ,23=5.59, P=0.03). No
signiﬁcant impact of bloom damage was found on main shoot node number (F 1,23=1.35,
P=0.26), or cane diameter (F1,2=0.61, P=0.44) at veraison.

Measurements taken at post-harvest still indicated a signiﬁcant negative impact of
bloom damage on the total number of nodes (F 1 32:10.56, P=0.004) and number of nodes
on lateral shoots (F 1,22=11.18, P=0.003), but not on shoot length (F 1 ,23=2.84, P=0.11). As
found during veraison, no signiﬁcant impact of bloom damage was found on the number
of nodes on the main shoots (F 1,250.59, P=0.45), or cane diameter (F 1,2=2.10, P=0.16).
No signiﬁcant effect of damage at veraison damage was observed on total node number
(F132=O.10, P=0.75), lateral shoot node number (F132: 0.39, P=0.54), shoot length

(F1,23=1.21, P=0.28), main shoot node number (F1,22=0.66, P=0.43), or cane diameter

62

(F1,21=O.02, P=0.89).

Bloom damage had a signiﬁcant negative effect on mature node number
(F1,21=13.68, P=0.001) and pruning weights (F1g1=11.26, P=0.003). In contrast, veraison
damage treatments did not have a signiﬁcant impact on either one (F 1,21=0.05, P=0.82

and F1,21=1.0, P=0.33 respectively) (Table 3.2).

Discussion
The results presented here indicate that non-bearing young V. labrusca vines are better
able to tolerate foliar damage during veraison than during bloom. In both 2000 and 2001,
bloom damage had signiﬁcant negative impacts upon several of the growth parameters
measured, while veraison damage did not affect any of the growth parameters measured.
The negative impact of bloom damage during the 2000 growing season was observed the
following season in reduced cane diameters. However, in other research performing
similar damage treatments in the same vineyard in the same year, we did not ﬁnd a
negative impact of bloom damage on cane diameters the following season (see Chapter

4).

63

 

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64

Vines damaged solely at veraison in 2000 had signiﬁcantly higher pruning
weights than all other vines. This indicates that a certain level of foliar damage can
potentially induce an increase in above ground growth late in the season. This increase in
above ground growth may have been caused by a reallocation of resources or an increase
in sink activity induced by damage. Candolﬁ-Vasconcelos et al. (1994 a) have
demonstrated that defoliation-stressed vines can re-translocate carbohydrates stored in
storage tissues to fruit. In addition, studies on potted V. labrusca var. ‘Niagara’ vines
have shown that root weight is signiﬁcantly impacted by damage at veraison while no
differences in above ground damage were observed (see Chapter 2). Increases in
individual leaf carbon assimilation rates have been reported in vines where defoliation
has been induced by whole leaf removal (Hofacker 1978, Candolﬁ-Vasconcelos and
Koblet 1991). In addition, several studies have reported cases of overcompensation
induced by herbivory or mechanically simulated herbivory (e.g. McNaughton 1979,
Owen 1980, Paige and Witham 1987, Paige 1992, Vail 1992, Hjéilten et al. 1993, Paige
1994; but see Bergelson and Crawley 1992). However, in these cases the damage
released apical dominance increasing branching patterns, and reduced competition for
cytokinins and other root-produced resources between leaves. These changes have been
associated with observed increases in single leaf photosynthetic rates (Wareing et al.
1968, Aarssen and Irwin 1991, Ovaska et al. 1992, Iwin and Aarsen 1996). The type of
mechanical damage in this study is unlikely to have caused a release of apical dominance
or reduced competition between leaves. Whether the difference observed here is due to an
increase in sink activity or a reallocation of resources is an important consideration, as a

reallocation of resources towards above ground grth may cause a reduction in

65

carbohydrates stored in roots and other tissues, potentially compromising future growth
and yield.

When vines that had been damaged during bloom were damaged at veraison in
2000, they did not exhibit an increase in above ground growth. Indeed, these vines had
signiﬁcantly lower pruning weights than did the control vines. The reversal in vine
response to veraison damage indicates that bloom damage compromised the vines ability
to respond to damage at veraison. Various types of stresses, from pollution to plant
association, have been shown to reduce plant compensatory abilities (e. g. Maschinski and
Whitham 1989, Hjalten et a1. 1993, Shabel and Peart 1994, Irwin and Aarssen 1996,
Weltzin et a1. 1998, Zvereva and Kozlov 2001; but see Coughenour et al. 1990). In
addition, various studies have found plants unable to tolerate several episodes of damage
(e. g. Hare 1980, Crawley 1983, Cartwright and Kok 1990). This response to damage
suggests that the increase in pruning weights exhibited in vines damaged solely at
veraison is probably due to a reallocation of resources towards above ground growth.

Damage at bloom in 2001 had a signiﬁcant negative effect on total node number,
lateral shoot node number, and shoot length at veraison. This contrast to vines damaged
at bloom in 2000 is most likely due to the higher replication and the use of pruning
weights as covariates in 2001, and not to a difference between two-year-old and three-
year-old vines. Measurements taken at veraison and post harvest indicated no signiﬁcant
difference in main shoot node number between bloom damaged vines and controls. This
indicates that bloom damage treatments primarily affected the production of lateral
shoots in these vines. A similar response has been reported in V. vinifera var. ‘Pinot Noir’

and var. ‘Riesling’ vines subjected to water stress, in which lateral shoot growth was

66

signiﬁcantly reduced by water stress (Reynolds and Naylor 1994).

In contrast to results from vines damaged in 2000, vines damaged solely at
veraison in 2001 did not have a signiﬁcant increase in pruning weights compared to
undamaged controls. This difference between 2000 and 2001 indicates that the level of
damage can potentially affect the vines response to damage. Damage applied at veraison
in 2001 was applied on all fully expanded leaves while veraison damage in 2000 was
only applied on 1.5 m of the shoot (average shoot length in 2000 = 3.62 m). The
application of damage at veraison in 2001 reduced 20% of the available source at the
time of damage at both bloom and veraison. Because of the vine growth between bloom
and veraison, the total amount of damaged leaves at veraison was approximately three
times more than what was damaged at bloom. This enabled a direct comparison of bloom
damage and veraison damage in terms of the vine source to sink ratio at the time of
damage. The comparison between bloom and veraison damage in 2001 suggests that the
stronger effect of bloom damage is not due to the presence of a higher source (leaves) at
veraison, but due to a lower relative sink at veraison in these fruitless vines.

In conclusion, these results are consistent with the notion that source to sink ratios
at the time of damage have a strong impact on a vines ability to tolerate damage. This
effect translates to a higher risk of injury due to foliar damage early in the growing

season than late in the growing season in non-bearing V. labrusca vines.

67

CHAPTER 4

Grapevine tolerance to foliar damage by two temporally-separated scarab beetles
and by mechanical damage during bloom or veraison
Introduction

The rose chafer, Macrodactylus subspinosus (F abricius) (Scarabaeidae:
Macrodactylini), and the Japanese beetle, Popillia japonica Newman (Scarabaeidae:
Anomalini), are two leaf skeletonizing scarab beetles considered to be pests of economic
importance in vineyards in eastern North America. Emergence of adult rose chafers
coincides with grape bloom in most of the beetle’s geographic range, while Japanese
beetle adults coincide with veraison (berry ripening). Grapevines have been shown to
tolerate signiﬁcant levels of foliar damage (Petrie et al. 2000a,b, Candolﬁ-Vasconcelos
et al. 1994, Boucher & Pfeiffer 1989), and insecticide applications may not be necessary
if foliar damage by these insects is below levels that impact vine growth and productivity.
The relationship between the level of herbivory and the impact on Vitis labrusca
(Linnaeus) grth and production is not well understood, particularly in young
establishing vineyards that typically do not have a crop. However, in bearing vines,
Boucher and Pfeiffer (1989) found that natural infestations of Japanese beetle in Virginia
failed to have any signiﬁcant impacts upon fruit quality, quantity, or growth of Vitis
vimfera (Linnaeus) var. ‘Seyval Blanc’. This indicates a high level of tolerance in
grapevines to foliar damage by leaf skeletonizers.

The detrimental effects of foliar herbivory are oﬁen attenuated by plant
compensatory responses to foliar damage (Trumble et al. 1993). Reduction in leaf area by

beetle feeding can alter the carbon source to sink balance, potentially causing a source

68

limitation. This in turn may drastically affect the distribution of carbon resources,
because their allocation is dependent on the strength of sink demands in resource-limited
plants (Wardlaw 1990, Trumble et al. 1993).

The relative sink strength of various tissues in grapevines changes signiﬁcantly
throughout the growing season, in accordance to their physiological stage of development
(phenophase) (Williams & Matthews 1990). Plant responses to foliar damage may be
affected by the seasonal change in demands placed upon the available sources by
developing tissues and reproductive sinks. Studies of tolerance and compensation in
perennial crops have focused on mature plants, in which vegetative growth tends to be
the major carbon sink early in the season, while ﬁ'uit production dominates carbohydrate
distribution late in the season (Williams & Mathews 1990). In contrast, young woody
plants, including grapes, produce relatively few fruits. Indeed, viticultural
recommendations include cluster removal in the ﬁrst years of growth to ensure that
energy is directed toward vine establishment (Zabadal 1997). The lack of fruits as
carbohydrate sinks may create a differential response to foliar herbivory late in the season
in young plants when compared to mature, fruiting plants. While vineyards are being
established, the photosynthetic and storage tissues act as the main sources of carbon,
while actively growing tissues and damaged tissues act as the main sinks. During and
prior to bloom, vegetative grth in grapevines is highly active, but by veraison shoot
and leaf growth slows considerably (van Zyl 1984, Williams 1987). This translates into a
situation with a low carbon source and high carbon sink during bloom and a high source
and low sink during veraison. This difference in source to sink ratio is expected to pose a

greater risk of source limitation during bloom than veraison, potentially affecting the

69

vines ability to tolerate damage early in the year.

This study examined the tolerance of young (1 yr after planting) grape vines, Vitis
labrusca L. var. ‘Niagara’, to beetle and mechanical defoliation during bloom and
veraison. The goals were to quantify the level of feeding by M. subspinosus and P.
japonica on young V. labrusca vines, and to determine the response of young grapevines

to different levels of mechanical and beetle damage during the different phenophases.

Materials and methods
Plant material This study was undertaken in a V. labrusca (L.) var. ‘Niagara’ vineyard
established in 1999, at the Trevor Nichols Research Complex in Fennville, Michigan.
Two shoots from two canes (total of four shoots) of each vine were trained onto a 1.37
meter high bilateral cordon Hudson River Umbrella trellis system. There were seven
vines per row, with 1.8 meters in between vines and 3 meters between rows. Vines were
maintained using 45.5 Kg of Urea fertilizer (46% Nitrogen) per acre applied on 16 March
2000 and 102.3 Kg of Urea per acre on 25 March 2001, and standard plant protection
program (Gut et al. 2002), except on rows where vines were caged with beetles. On these
rows, no insecticides were applied at least one month prior to beetles being caged on
vines and insecticide and ﬁmgicide applications were postponed until cages were

removed. Treatments were initiated in spring 2000.

Beetle Damage. Four densities of rose chafer or Japanese beetles were maintained inside

caged vines during bloom or veraison respectively. Four vines in a row of seven vines

were selected with a cane size between 0.5 m and l m. Selected vines within a row had 0,

70

10, 20, or 40 beetles caged onto them for two weeks during bloom or veraison, arranged
as two randomized complete block designs (one for bloom and one for veraison) with ten
replicates each. During bloom, vines were infested using adult rose chafers collected
from traps (Great Lakes IPM, Vestaburg, Michigan) in Oceana County, Michigan.
During veraison, Japanese beetles were collected from traps (Trécé Inc., Salinas,
California) in Allegan County, Michigan. For both beetles, traps were emptied the day
before beetles were collected, so that recently caught beetles were used. To ensure beetle
densities remained constant in cages, beetles were counted every other day and any dead
beetles replaced with live ones. Cages consisted of a highly porous bridal illusion plastic
mesh (Fabric Gallery, Williamston, Michigan) draped over the trellis and suspended ﬁom
a 0.3 m radius wire ring taped onto the trellis. Mesh was fastened to the base of the vine
with garden wire and the side of the cage was sealed with binder clips. This created a
cone-shaped cage that encased all of the above-ground vine tissues, and allowed for plant
growth and beetle movement.
Growing Season Measurements. Adult rose chafers were placed on vines on 20 June,
2000 and removed on 4 July, 2000. The level of defoliation was determined using visual
aids adapted from Boucher & Pfeiffer (1989). Cane and trunk diameters were measured
using Vernier calipers at bloom (19 June), veraison (30 August), and leaf senescence (29
October), and prior to bloom the following season (9 May, 2001). The number of mature
nodes was determined after leaf loss (11 November).

Adult Japanese beetles were placed on separate vines on 3 August, 2000 and
removed 17 August, 2000, and the level of defoliation determined. On these vines, cane

diameters were measured just prior to veraison (26 July) and at leaf senescence (29

71

October). The number of mature nodes was determined after leaf loss (11 November).

Post-Growing Season Measurements. Vines damaged by beetles in 2000 were pruned to
15 nodes per cane (30 total) between 26 January and 6 February 2001. For each vine, the
weight of mature cane prunings (pruning weights) was determined by bundling and
weighing them with a digital scale in the ﬁeld. To determine the possible impacts of
beetle feeding on vine storage, growth parameters were measured prior to bloom the
season after caging. We recorded the diameters of canes and trunks (9 and 14 May, 2001,
respectively), and the number of nodes remaining dormant after the 16-inch shoot growth

stage had been reached (22 May, 2001).

Mechanical Damage Treatments. To determine the effect of leaf area loss during bloom
and veraison on vine development, vines were subjected to mechanical damage during
each of these phenophases. Either O, 10, 20, or 30% of the total leaf area was removed
from every fully expanded leaf during bloom or veraison (Figure 4.1). Leaf area was
removed using hole punchers, avoiding all major veins in order to imitate beetle feeding
and to avoid the differential impacts on photosynthetic capacity caused by interveinal
damage when compared to whole leaf removal or treatments including midrib and main
lateral vein damage (Hall and Ferree 1976, Boucher et al. 1987). To ensure appropriate

damage levels were applied, visual aids were made for use while damaging leaves.

72

 

Figure 4.]. Leaves of ‘Niagara’ grapevines after using a hole-puncher to apply

mechanical damage treatments of either 10, 20, or 30% interveinal leaf area removal.

73

For vine defoliation applications during bloom, thirty-two vines with cane height
between 0.5 m and l m were separated into two blocks of 16 plants each. Within each
block, selected vines were randomly assigned to one of the four damage levels, creating
eight replicates of each treatment. These vines were damaged at bloom to the appropriate
level between the 15 and 23 June 2000.

Larger canopy size during veraison restricted the number of vines that could be
treated, and therefore only four replicates were possible. For these treatments four vines
from a row of seven were selected (vines with cane height between 0.5m and 1m) and
assigned to one of the four damage levels (0, 10, 20, or 30% defoliation), and replicated
four times. These vines were damaged on the14 and 15 August, 2000 in an identical
fashion to bloom damaged vines.

Growing Season Measurements. During the 2000 growing season vegetative grth
parameters were measured at trace bloom (13-14 June), at veraison (6 -11 August), and at
leaf senescence (21 October) on vines damaged at bloom and veraison. On each vine, the
node number of every shoot and cane diameters were measured. In addition, the number
of mature nodes and the total shoot length were measured after leaf loss (10-11
November).

Post-Growing Sea_son Measurements. On 16 and 26 January, 2001, all vines were pruned
to 15 nodes per shoot and the pruning weights recorded as above. Prior to bloom the
following season (2001) the diameter of canes and trunks (9 May) and the number of
nodes remaining dormant after the 16 inch shoot growth stage had been reached (22 May)

were recorded on all vines.

74

Statistical Analysis. Data were analyzed by one way ANOVA using cane diameters
measured prior to applying treatments as covariates and blocking where appropriate
(PROC GLM, SAS Institute, 1999). Cane diameters were used as covariates in order to
reduce variance introduced by differences in vine size. Means separation was performed

where appropriate using the Student Newman-Keuls method.

Results
Beetle Damage. Defoliation by the rose chafer was minimal even at the highest beetle
density, with less than one percent of the leaf area removed. Defoliation by the Japanese
beetle was much greater, approaching 7% at the highest beetle density (Figure 4.2). This
difference in defoliation intensity was even greater when the relative canopy size present
during veraison is considered (approximately 2-3 times larger during veraison than
during bloom). However, even at the highest beetle density, neither beetle species had
any signiﬁcant effect upon any of the growth parameters measured. The diameter of
canes on rose chafer damaged vines was not signiﬁcantly affected by beetle foliar
damage, when measurements were taken at the end of veraison or at leaf senescence
(F336=0.75, P=0.53, and F3,26=0.52, P=0.67, respectively). In addition, there was no
signiﬁcant effect of foliar herbivory on above-ground growth in the year of damage,
whether measured as the number of mature nodes after leaf loss (F3,26=0.31, P=0.82) or
pruning weights (F3,26=l.09, P=0.37). Growth parameters taken prior to bloom the
following season (2001) also indicated no impact of rose chafer damage; cane diameters

and number of shootless nodes were not impacted by the treatments imposed (F 3,26=O.64,

75

=0.60 and F 3,250.42, P=0.74 respectively).

 

 

 

 

   

 

 

 

 

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e .
mi
0) 5 -
+I
:
'2 4
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.2
3 ,,
.\°
5 2 .
0
E
1 ..
0 T . —'|
0 1O 20 40 0 10 20 40
Rose Chafer Japanese Beetle
Beetle Density On Vines

Figure 4.2. Percent defoliation of total vine canopy area caused by two weeks of

different densities of adult rose chafer and Japanese beetle.

On vines subjected to Japanese beetle feeding, a similar result was found; cane
diameters measured at leaf senescence (F 3 36:1.06, P=0.38), mature node numbers
measured at leaf loss (F 3 36:1.26, P=0.31), and pruning weights (F3 ,26=O.55, P=0.65) were
not affected by Japanese beetle damage. Growth parameters taken prior to bloom the
following season (2001) also indicated no impact of Japanese beetle damage; cane

diameters and number of shootless nodes for Japanese beetle damaged vines were not

76

impacted by the treatments imposed (F3, 26:08], P = 0.50 and F3, 26:0.87, P=0.85

respectively).

Mechanical Damage. Mechanical damage during bloom did not affect vegetative growth
of the vines measured as the number of nodes at veraison (F 3 35:1.12, P=0.67). However,
a reduction in cane diameter (F3,25=5.3, P=0.006) was observed on bloom damaged
plants, when measured at veraison (Figure 4.3). Although the 20 % leaf area removal
treatment was not signiﬁcantly different from the control, the overall pattern indicates
that early season foliar damage induced a source limitation, reducing the amount of
resources allocated to cane growth. When these vines were measured at leaf senescence,
there were no signiﬁcant differences between treatments in the number of nodes
(F335=O.21, P=0.89) or cane diameters (F3,25=2.22, P=0.11). In addition, total shoot
length (F3,25=0.39, P=0.76) and mature node number at leaf loss (F 3,25=0.86, P=0.48) was
not impacted by early season defoliation. The total weight of new shoots produced,
measured as pruning weights, was not affected by defoliation at bloom (F3,25=1.19,
P=0.33). Finally, the diameter of canes (F3,25=1.39, P=0.27) and number of shootless
nodes (F 3 ,25=1.33, P=0.29) recorded the following season (2001) were not impacted by

bloom damage treatments (F3, 25:0.71, P=0.56).

77

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Mean cane diameter size :I: S. E. (mm)
0

...........
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------

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V U V U

0 10 20 30
% Leaf Area Removed

 

 

 

 

 

 

 

 

Figure 4.3. Cane diameter of vines damaged at bloom to different levels of defoliation,
measured at veraison. Means separation by Student Newman Keuls method. Treatments

with different letters are signiﬁcantly different at P < 0.05.

78

Mechanical damage during veraison had no signiﬁcant effect upon any of the vine
growth parameters measured after leaf senescence. Cane diameters (F3,3=0.73, P=0.56),
number of nodes (F3,g=0.97, P=0.45), shoot length (F3,3=1.49, P=0.29), and mature node
numbers (F3,3=0.97, P=0.45) were not signiﬁcantly different between the different
damage levels. In addition, pruning weights were not signiﬁcantly impacted by the
defoliation treatments during veraison (F3,3=0.24, P=0.86). Growth measurements taken
early the following season also indicated no signiﬁcant impacts of damage at veraison on
subsequent vine grth (cane diameters F3,g=0.5, P=0.69 and shootless nodes F3, 3:0.97,

P=0.45).

Discussion

This study demonstrated that two of the primary scarab beetle pests of vineyards in
eastern North America remove a very small proportion of the leaf area on V. labrusca
vines. This small level of herbivory caused no signiﬁcant impact on the above ground
vegetative grth of young vines, even when 40 beetles were allowed to feed for two
weeks. In addition, mechanical removal of leaf area at levels much higher than seen in
our caging study showed that vines were negatively impacted by damage early in the
season, but no signiﬁcant impacts were found in above-ground tissues by the season’s
end and at the beginning of the following season.

Vine grth between bloom and veraison resulted in approximately two to three
times the leaf area being present at veraison, compared to that at bloom. Due to

mechanical damage treatments being applied on a percentage basis, the total amount of

79

leaf area removed during veraison far exceeded that removed during bloom. Despite the
greater leaf area removed during veraison, no impact of this damage was observed in
above ground tissues. The relative ratio of carbon source to sink during bloom and
veraison provides a framework for understanding this result. Early in the season a
relatively small number of leaves are present, and most carbohydrates used for shoot
growth are derived from storage tissues. Indeed, until the 6-leaf stage, shoot development
is dependent upon re-translocation from storage tissues, and not until bloom is the vine
able to rely upon assimilates produced during the current year (Yang et al. 1980a). At
bloom and prior to bloom there is also a relatively high activity of growth in all
vegetative tissues (van Zyl 1984, Williams 1987). In contrast, during veraison a full
canopy is present and vegetative sinks have been shown to be relatively inactive in
irrigated V. vinifera vines (van Zyl 1984, Williams 1987). In non-irrigated V. labrusca
vines grown under rainy conditions root activity is considered to remain active (G. S.
Howell, personal communication), making roots a potentially strong sink during
veraison. However, increased root activity is unlikely to cause a source limitation at this
period, as potted vine studies (Miller et al. 1996b, Petrie et al. 2000a) have indicated sink
limitations at veraison in uncropped vines when compared to cropped vines.

Mechanical damage at bloom had a signiﬁcant impact on storage tissues,
measured as cane diameters, but no impact upon shoot growth, measured as node
number, when measured at veraison. This preferential allocation to growth over storage is
in accordance with studies on sink hierarchy (Wardlaw 1990), indicating that defoliation
during bloom in young vines can induce a source limitation. However, no impact upon

above ground storage tissues was detected by the time of leaf loss in the study reported

80

here, and vegetative growth parameters measured the following season did not differ
between damage treatments. These ﬁndings indicate that young V. labrusca vines were
able to compensate for high levels of defoliation during bloom by the end of the season,
despite the initial source limitation experienced after damage was applied at bloom.
However, results from a study performed in the same vineyard in the same year using
similar damage treatments did indicate a signiﬁcant reduction in growth parameters
measured the following year (see Chapter 3). The main difference between the two
studies lies in the experimental design; the study reported in chapter 3 used a factorial
design comparing damage during bloom and veraison with only one level of damage. The
design of that study may have added more power to the statistical test. These contrasting
results indicate the limitation of using cane diameter as an estimate of impacts on storage.
Root growth has been shown to be the lowest sink priority and impacts on storage tissues
would most likely be detected here.

Whether foliar herbivory leads to changes in allocation to below-ground tissues
was not studied here, and is experimentally challenging in vineyard studies. However,
given the low level of defoliation caused ﬁ'om these scarab beetles and the lack of
signiﬁcant impacts on aboveground vegetative growth during the year following damage,
the potential for high levels of tolerance is likely. This is may be particularly true during
veraison when the source to sink ratio is particularly high. During bloom the higher sink
activity is a potential source of concern, but the low level of defoliation caused by the
rose chafer (Figure 4.2) leads one to believe that unless exceptionally high numbers of
beetles are present the impact on the vine should be minimal.

The lack of effect of mechanical damage during veraison on cane diameter or

81

shoot growth indicates that at this point of the season, when sink demands are low in non-
fruiting vines, the creation of a source limitation is extremely difﬁcult. Although
replication was low due to vine canopy size, the highest damage treatments were extreme
(Figure 3.1). Despite the severe intensity of damage applied during this period, vines with
30% leaf area removed were able to produce enough photosynthate to mature the same
number of nodes as the undamaged vines. Furthermore, no impacts on initial growth
parameters were observed the following season, suggesting a high level of tolerance.

We propose that mechanical damage during veraison did not affect vine growth
because non—bearing vines have relatively few sinks and a full vegetative canopy, making
them sink-limited. Other authors working on grapevines have found similar results. For
example, using potted vines with and without fruit, Petrie et al. (2000) found that despite
a higher leaf area in non-bearing vines compared to bearing vines, no signiﬁcant
differences in total dry weight were found. Furthermore, Layne & Flore (1995) have
demonstrated the impact of end-product inhibition in sour cherry, Prunus cerasus (L.), as
a mechanism for sink limitations at a whole plant level. These studies illustrate the
importance of source to sink ratios in understanding a plant’s ability to assimilate carbon,
and therefore their ability to respond to leaf area loss.

In light of the high levels of mechanical defoliation and the lack of signiﬁcant
differences in above ground growth by the end of the season, it is not surprising that the
level of herbivory caused by beetles did not impact their growth. This study illustrates the
low level of defoliation that M. subspinosus and P. japonica are capable of causing on V.
labrusca var. ‘Niagara’ vines. Based on these ﬁndings we expect defoliation in

establishing ‘Niagara’ vineyards with less than 40 beetles per vine to be below levels

82

likely to affect vine establishment, particularly after the initial vegetative growth has
taken place.

Due to the large canopies present at veraison, the proportion of leaf area damaged
by Japanese beetle in established V. labrusca vineyards ought to be minimal, but further
studies are required to test this prediction. Boucher & Pfeiffer (1989) found no effect of
natural infestations of Japanese beetle (6.5% defoliation) on fruit quality and quantity or
vine growth in V. vinifera ‘Seyval blanc’ vines, even though these vines had fruit as an
active sink for carbon. Due to the relatively small level of defoliation by 40 adult
Japanese beetle in our study (6.4% mean defoliation, and mean leaf number at veraison
=187), we expect lower defoliation levels in established V. labrusca vineyards than were
found by Boucher & Pfeiffer (1989) on V. vinifera. However, viticulture in cool climates
such as Michigan requires consideration of climatic conditions that are near the limits of
commercial grape production (Howell 2001). Shorter growing seasons reduce the post-
harvest carbon assimilation period, limiting the available time to recover and sequester
enough carbohydrates to tolerate cold temperatures. Cropping level is expected to be an
important factor that will impact tolerance to grapevine foliar herbivory. Further studies
should include various cropping levels in order to develop economic injury thresholds for
these or any other foliar pests on fruiting grapevines.

While the impact of foliar herbivory by rose chafers has been shown here to be
negligible, future studies should concentrate on their impacts upon ﬂower clusters. This
insect is still likely to be a potential source of concern in fruiting vineyards due to feeding
on ﬂower clusters during bloom (Chittenden 1916, R.J. Mercader unpublished data).

It is apparent from these studies that young V. labrusca vines have a signiﬁcant

83

ability to tolerate foliar damage, in particular after the initial vegetative growth has
occurred. This tolerance was seen in above ground growth at levels of leaf area loss far
beyond the defoliation potential of 40 rose chafers or Japanese beetles per vine. This
indicates that even under intense infestations of these two pests, the damage caused may
not warrant chemical control unless other forms of stress such as disease or drought have
critically stressed the vines. Sustainable grape production, as deﬁned by Howell (2001),
refers to maintaining the highest yields of ripe fruit per unit area without reducing
vegetative grth and doing so over a period of years at costs which return a net proﬁt.
Within this framework, it is important to consider the unique characteristics of the initial
years of vineyard establishment in which no crop is produced, and vines therefore have

fewer carbohydrate sinks.

84

CHAPTER 5

Conclusion

This study has yielded three primary results 1) agreement with the notion that
source to sink ratios at the time of damage are a major factor in grape vines ability to
tolerate damage, 2) vine photosynthetic response to damage is dependent upon the timing
of damage and the type of damage, and 3) two of the primary foliar herbivores in Eastern
US. vineyards consume relatively small amounts of foliage compared to the size of the
vine canopy.

In young Vitis labrusca (L.) vines, foliar damage early in the season presents a
greater risk to young vines than damage late in the season. The application of mechanical
damage treatments on a percentage basis removed intensity of damage and whole season
sink size as factors explaining the increased tolerance to damage at veraison when the
source to sink ratio was highest. Despite the apparent compensation to damage at bloom,
there was a signiﬁcant impact of bloom damage on photosynthetic rate late in the season.
This effect appeared to be due to an early senescence in bloom damaged vines, a ﬁrrther
indication that stress induced by defoliation can have similar impacts as stress induced by
high crop loads (Edson et a1. 1993).

The work presented in Chapter 2 illustrates the importance of timing of damage
and plant physiology on the adequacy of mechanical simulations of herbivory. The
differences in carbon assimilation found between Japanese beetle and mechanical damage
at veraison illustrated that the physiological stage of the plant needs to be taken into

account when considering the accuracy of simulations of herbivore damage. This

85

research stresses the importance of studying herbivory within the physiological context of
the plant.

Finally, these studies also indicated that young V. labrusca vines have a
signiﬁcant ability to compensate for foliar damage, in particular after the initial
vegetative growth has occurred. Compensation in above ground grth was seen at
levels of leaf area loss far beyond the defoliation potential of forty rose chafers or
Japanese beetles per vine. This indicates that even under high infestations of these two
pests, the damage caused may not warrant chemical control in V. labrusca vineyards
unless other forms of stress such as disease or drought have compromised the vines

ability to tolerate defoliation.

86

APPENDIX I

87

Appendix 1
Record of Deposition of Voucher Specimens*
The specimens listed on the following sheet(s) have been deposited in the named museum(s) as
samples of those species or other taxa, which were used in this research. Voucher recognition
labels bearing the Voucher No. have been attached or included in ﬂuid-preserved specimens.
Voucher No.: 2002-04

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

Phenophase dependent tolerance to foliar herbivory in grape vines, Vitis labrusca (L.) var.

‘Niagara’

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

Entomology Museum, Michigan State University (MSU)

Other Museums:

lnvestigator’s Name(s) (typed)
Rodrigo J. Mercader

 

 

 

Date 16/08/2002

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

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

Copies: Include as Appendix 1 in copies of thesis or dissertation.
Museum(s) ﬁles.
Research project ﬁles.

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

88

Appendix 1.1

Voucher Specimen Data

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89

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90

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Anonymous. 1997. Identifying and Understanding the Major Insects and Mites on
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Anonymous. 2000. “Cooperative Agriculture Pest Survey and NAPIS’s page on
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Candolfi-Vasconcelos, M.C., and W. Koblet. 1990. Yield, fruit quality, bud fertility,
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Candolfi-Vasconcelos, M.C. and W. Koblet. 1991. Inﬂuences of partial defoliation on
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Candolﬁ-Vasconcelos, M.C., M.P. Candolfi, and W. Koblet. 1994 a. Retranslocation
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Candolfi—Vasconcelos, M.C., W. Koblet, G.S. Howell, and W. Zweifel. 1994 b.
Inﬂuence of defoliation, rootstock, training system, and leaf position on gas exchange of
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