Diss. ETH
No. 10704
Interactions
between Green
Apple Aphids
{Aphis pomi De Geer)
and
Apple Plants (Malus domestica Borkh.)
Subjected to Water Stress
A dissertation submitted to the
Swiss Federal Institute of
for the
Technology
degree
of
Doctor of Natural Sciences
presented by
Rima Mekdaschi Studer
M.Sc.
(Major: Crop Production)
born
July 18,
citizen of
Accepted
on
1961
Germany
the recommendation of
Prof. Dr. S. Dorn, examiner
Prof. Dr. J.
Dr. J.
Nosberger, co-examiner
Baumgartner, co-examiner
Dr. U. Schmidhalter, co-examiner
Zurich, 1994
Zurich
To
Chrisloph
Contents
Summary
1.
I
Zusammenfassung
V
General Introduction
1
Apple Orchard Ecosystem
1.1
The
1.2
Short Review
1.2.1
on
Water Stress
Plant Growth
3
3
Quality
1.2.2 Plant Nutritional
4
1.2.3 Plant Water Potential
4
1.2.4 Plant Microenvironment
5
1.2.5 Plant Attractiveness
6
1.3
Effects of
6
1.4
Materials and Methods
1.4.1
Aphids
on
Host Plants
7
The Host Plant
1.4.2 The
7
Aphid
10
1.4.3 The Water Stress
2.
1
Effects of Water Stress
of the Green
on
Apple Aphid:
Introduction
2.2
Materials and Methods
Descriptors
for the
20
Development
Aphid Populations
Experimental Conditions
2.2.3 Data Collected
2.2.4 Data
19
19
of
2.2.2
Population Dynamics
Analysis
Life Table
2.1
2.2.1
12
Analysis
20
22
23
26
2.3
Results
2.3.1
27
Development
2.3.2 Effects of Water Stress
on
Plant
2.2.3 Effects of Water Stress
on
Life Table
and
2.4
Population
Parameters of
Development
27
..
Aphids
53
Effects of Water Stress
on
2.4.2 Effects of Water Stress
on
Population
and
31
44
Discussion
2.4.1
3.
of Water Stress in the Soil
Plant
Development
Aphid
Parameters of
..
53
Life Table
57
Aphids
Effects of Water Stress on
Population Dynamics
Apple Aphid:
Population Development and Growth
of the Green
3.1
Introduction
3.2
Materials and Methods
3.2.1
63
Characterization of the
and Growth of
3.2.2
3.3
65
Development
65
Aphid Populations
Experimental Conditions
66
3.2.3 Data Collected
67
3.2.4 Data
69
Analysis
Results
3.3.1
69
Development
of Water Stress in the Soil
3.3.2 Effects of Water Stress
on
3.3.3 Effects of Water Stress
on
Development and Growth
3.4
63
Plant
of
Development
Aphid Populations
69
..
.
Discussion
3.4.1
3.4.2 Effects of
Plant
on
Plant
Development
..
97
Aphid Populations
Development
3.4.3 Effects of Water Stress
the
86
97
Effects of Water Stress
on
72
99
on
Population Development
of
Aphids
102
4.
Effects of Water Stress
on Population Dynamics
Apple Aphid:
Phloem Sap Quality
of the Green
Changes
in
4.1
Introduction
107
4.2
Materials and Methods
109
4.2.1
Collection of Phloem
4.3
4.4
109
110
4.2.3 Exudation
110
Technique
Carbohydrates
4.2.4
Analysis
4.2.5
Analysis of Nitrogenous Substances
of
111
Analysis
113
4.3.1
113
Sugars
4.3.2 Amino Acids
118
Discussion
123
Sugars
123
4.4.2 Amino Acids
127
Conclusions
135
5.1
Effects of Water Stress
5.2
Effects of Water Stressed Plants
the
5.3
111
112
Results
4.4.1
on
the Host Plant
Effects of
an
135
on
Population Dynamics of Aphids
the Green
6.
Sap
4.2.2 Plant Material
4.2.6 Statistical
5.
107
137
Infestation with
Apple Aphid
on
the Host Plant
141
References
145
Appendix
159
Abbreviations and
Symbols
Curriculum Vitae
Acknowledgements
161
I
Summary
Analysis of apple production in Switzerland has shown that studies
dynamics of subsystems
the
on
create the most useful base to
optimize agricultural
production systems. Therefore, the interactions between insect herbivores
and their host, with special attention to stress factors such
nutrient deficiencies,
are
studied
extensively
as water
and
at the Institute of Plant Sciences
at the
ETH, Zurich. The influence of different levels of water supply on the
sub-system of apple plants (Malus domestica Borkh., cv. 'Golden Delicious')
with green
apple aphids (Aphis pomi De Geer)(Hemiptera: Aphididae) was
study. Effects of different water regimes on
examined for the first time in this
plant growth and
on
dynamics,
as on
as
well
Apple plants, which
different
levels
of
physiological plant parameters,
the feedback of
MPa) using
conducted with
potted plants grown
environmental conditions
regime, 55-60% RH,
maximum size of 1.3
phloem
sap
studied.
(22/17°C day/night temperatures, 18:6 light/dark
umol/rrftsec PPFD). Plants reached a
400-450
m.
The effects of water stress
aphid populations
characteristics
parameters such
were
in a soil mix under controlled
was
described
life table and population parameters of aphids
population
aphid population
multiplied by tissue culture, were subjected to
supply OF^: -0.05, -0.70, -1.20, -1.60 and
intermittent drying cycle technique. The experiments
the
of
on
their host
were
-2.15
development
on
water
were
the
aphids
as
shoot
with
as
plant growth
length, total leaf
area,
on
plant growth and
on
by relating age-specific
well
as
density-dependent
physiological
and
plant
plant
water relations and
quality.
Water stress decreased the
plants' carrying capacity for aphid populations.
The characteristics of the phloem sap
factors
influencing
the
were identified as the most important
population development of aphids. The concentration
and composition of the phloem sap changed with water stress, with leaf
position (i.e. leafs stage of maturity), and with infestation by aphids.
II
The size
(per plant) and density (per leaf and per unit of shoot length) of
aphid populations decreased significantly
Although
with
increase in water stress.
an
phloem sap increased with
carbohydrate ratio decreased up to 10-fold,
the concentration of amino acids in the
water stress, the amino acid to
rendering the quality of the phloem sap less favorable for aphid feeding.
Asparagine, the major amino acid detected in the phloem sap of apple plants
(68-77%
apical and growing leaves),
relative content in
pomi.
determining population development
asparagine in the phloem significantly decreased with
of A.
factor
A
higher amino acid
leaves and
a
lower
identified
as a
water stress.
phloem of the apex and young, growing
content in the
carbohydrate
was
The relative content of
to
nitrogen ratio,
as
well as
higher relative
asparagine compared with the phloem of mature leaves, explain
preference of the green apple aphid for young tissue and the faster
contents of
the
development of aphids
on
young leaves. Therefore, young
actively growing plant parts
are
apple
trees and
by green apple aphid
most threatened
infestation.
The
study presented here confirmed that aphids
sink effect
on
that this sink effect is correlated with the size of
demonstrated that the
with
aphids
contained
phloem
sap of
plants
appreciable
feeding sites, and
can exert an
plants by increasing transport of solutes
an
which
to
aphid colony. It could be
were
significantly higher asparagine
previously infested
and much lower sorbitol
compared with phloem collected from uninfested plants, proving that aphids
altered the
composition of the phloem sap
to favor their nutrition.
Plants grown under conditions of water stress were shown to
adjust osmoti-
cally by actively accumulating solutes. The critical moisture level for a signifi¬
cant reduction in
which
were
plant growth developed below Y^,
not infested with
demonstrated to affect the
aphids.
plants' ability
to
-0.69 MPa for
=
An infestation with
plants
aphids, however,
adjust osmotJcally
assimilates and solutes needed for active osmotic
adjustment, shifting
critical moisture level for
to
plants
this critical moisture range
an
infestation with
infested with
plants
were
aphids
water
>
the
-0.69 MPa. In
particularly sensitive
to
supply, plants were able
to
shown to be
aphids. Under unlimited
Y^
was
by the drain of
compensate for the losses in assimilates withdrawn by aphids, possibly due
to a
on photosynthesis caused by an additional sink and/or
degeneration and mobilization of metabolites.
positive feedback
due to
Ill
Population parameters (mean generation time, intrinsic rate of natural
increase, and days for populations to double), the components of the intrinsic
(development and pre-reproductive times, percent immature
fecundity) and population characteristics (size and density) of
mortality,
A. pomi were assessed using two approaches: the age-specific life table and
the density-dependent population approach. Under conditions of water stress,
development and pre-reproductive time of aphids as well as generation and
doubling time of populations were shorter than in the well-watered treatment.
Net reproduction rate (i.e. cumulative fecundity) significantly increased with
rate of increase
and
water
stress, whereas the
intrinsic
significantly affected by drought
rate
of
natural
increase
stress. The size and
density
was
of
not
aphid
populations, however, was significantly reduced on water stressed plants. The
interrelationship of various factors regulating aphid population, therefore, may
not
necessarily
all
apply
at different
population densities.
Leer
-
Vide
-
Empty
V
Ziisammenfassung
der Untersuchung der Apfelproduktionssysteme in der
gezeigt, dass die Analyse der Dynamik von Subsystemen den
Erfahrungen bei
Schweiz haben
erfolgversprechendsten Weg
zur
Optimierung der Bewirtschaftungsformen fur
landwirtschaftliche Kulturen darstellt. Daher warden
am
Institut fur Pflanzen-
wissenschaften der ETH Zurich seit bald 15 Jahren die
zwischen
Wechselwirkungen
Kulturpflanzen und Pflanzenschadlingen untersucht, wobei Stress-
faktoren besonders
Die
Wasserversorgung auf das Subsy¬
Apfelbaum (Malus domestica Borkh., Sorte 'Golden Delicious') und
einer unterschiedlichen
Auswirkungen
stem
beriicksichtigt werden.
griine ApfelblattJaus (Aphis pomi De Geer)(Hemiptera: Aphididae) wurden in
der
voiiiegenden Studie
wie auch Blattlause
zum
spielen
ersten Mai
untersucht; sowohl Wassermangel
im Obstbau eine bedeutende Rolle. Die hier
vorgesteltte Arbeit beschreibt die Effekte verschiedener Bewasserungsregime
auf das Pftanzenwachstum und auf physiologische Pflanzenparameter, auf
die Populationsdynamik der Aphiden sowie auf den Feedback der AphkJen
auf ihren Wirt.
Geklonte, in Gewebekultur vermehrte Apfelbaumchen wurden unter kontrollierten
125
cm
Bedingungen
in
TSpfen
Saugspannung
in Klimakammern bis
einer Grosse
zu
gezogen. Die Pflanzen wurden
von
jeweils bewassert,
im Boden bestimmte Werte erreichte
maximal
wenn
die
C^boW "°05- ~0-70'
-1.20, -1.60 und -2.15 MPa); dadurch konnten mehrere Versuchsvarianten mit
einer unterschiedlichen kontrollierten
Die Auswirkungen der verschiedenen
wachstum und die
Entwicklung
von
Wasserversorgung festgelegt werden.
Bewasserungsregime auf das
Blattlauspopulationen
Pflanzen-
wurden untersucht,
Populationsgrosse
pflanzenphysiologischen Parametern wie Sprosslange und Blattflache beziehungsweise dem Wasserstatus
der Pflanze sowie der Phloemsaftqualitat in Beziehung gebracht wurden.
indem Lebenstafel- und
Populationsparameter
und -dichte mit dem Pflanzenwachstum und
wie auch
VI
Wasserstress bewirkte eine Abnahme der
einer Pflanze fur
wurden als
Tragfahigkeit ("carrying capacity")
des Phloemsaftes
Blattlauspopulationen. Eigenschaften
wichtigste
Faktoren identifiziert, welche die
Populationsentwick-
lung beeinflussen. Die Konzentration und die Zusammensetzung
saftes waren
abhangig
der Wasserversorgung, der
von
einer Pflanze und der Starke des Befalls mit
Die Grosse von
einer
Blattposition innerhalb
Aphiden.
Aphidenpopulationen pro Apfelbaumchen sowie deren Dichte
Pflanzenorganen
auf einzelnen
des Phloem¬
Erhohung
nahmen mit Wasserstress
signifikant ab.
Trotz
der Aminosaurenkonzentration im Phloemsaft wasserge-
stresster Pflanzen wurde das Verhaltnis zwischen Aminosauren und Kohle-
hydraten (d.h. Zuckern) stark erniedrigt. Dies bedeutete eine Verschlechterung der
Nahrungsqualitat des Phloemsaftes
fur die
Aphiden. Asparagin, die
dominante Aminosaure, welche im Phloemsaft der Apfelbaumchen gemessen
wurde, konnte als bestimmender Faktor fur die Populationsentwicklung
identifiziert werden. Der relative Gehalt
signifikant
Asparagin
an
nahm mit Wasserstress
ab.
Hohere relative Gehalte
von
Blattern im
alteren Blattern konnen die Vorliebe von A. pomi fur
Asparagin
Vergleich
junge RIanzenteile wie auch
zu
im Phloemsaft
von
Apex und jungen
die bessere und schnellere
Entwicklung auf
jungen Blattern erklaren. Daher sind junge Apfelbaume (hohes Verhaltnis von
jungem zu altem Gewebe) sowie wachsende Pflanzenteile (gerade im
Fruhjahr) besonders stark Schaden durch Blattlause ausgesetzt.
Die
vorliegende Arbeit bestatigt, dass Blattlause einen erheblichen Sink-Effekt
auf die Pflanzen ausuben konnen, indem sie den
gelosten Stoffen
zu
dieses Sink-Effekts ist
konnte
bestatigt
Transport
von
im Phloem
Orten der Nahrungsaufnahme erhohen; das Ausmass
der Grosse der BlattJauspopulation abhangig. Es
von
werden, dass durch einen Blattlausbefall die Zusammen¬
setzung des Phloemsaftes zugunsten der Aphiden verandert wird. Es konnte
gezeigt werden, dass durch den Blattlausbefall der relative Gehalt
Asparagin
im Phloemsaft erhoht und der
Pflanzen, die
an
unter
Sorbitolgehart verringert
an
wird.
Wassermangel litten, zeigten eine osmotische Anpassung
den Wasserstress, indem sie
geloste Stoffe akkumulierten. Das Wachstum
mit Blattlausen befallener Pflanzen wurde bei einer
Wasserstresses
fallener Pflanzen
CPsoden
(^Boden
>
<
"°-69
"°-69
geringeren Intensitat des
MPa) beeintrachtigt als dasjenige unbeMPa). Ein Blattlausbefall verringerte das
VII
Vermogen
der
Pflanze, sich osmotisch an einen Wassermangel anzupassen,
Aphiden der Pflanze geldste Stoffe, die zur osmotischen Anpassung benotigt werden, entzogen.
indem die
Die
Untersuchung der Auswirkungen
von Wasserstress auf die Populationsentwicklung und -dynamik mit Hilfe von Lebenstafeln beziehungsweise von
dichteabhangigen Populationscharakteristiken ergab, dass die Larven- und
Prareproduktionszeit der Aphiden sowie die Generations- und Verdoppelungs-
zeitder
Populationen
Fekunditat der
unter Wasserstress abnahmen.
Reproduktionsrate und
Aphiden nahmen unter Wassermangel signifikant zu, wahrend
die artspeztfische Wachstumsrate nicht signifikant beeinflusst wurde.
Populationsgrdsse und -dichte nahmen jedoch mit zunehmendem Wasser¬
stress signifikant ab.
1
1
General Introduction
The
1.1
Apple Orchard Ecosystem
Integrated pest management (IPM)
past decade.
Key
factors
in orchards
attributing
for the
scientific knowledge concerning
profound
arthropods and the introduction
1993a).
aphids
The number of IPM
low is, however, limited
rapidly progressed during the
rapid implementation
the
usefulness of
of new selective
compatible methods
were
the
predatory
plant protectants (Dorn,
keep populations
to
of
(Pflanzenschutzmittel-Verzeichnis 1987/1988,
Schweiz; Dorn, 1992). Many relevant interactions in the orchard ecosystem,
between insect
populations and between insects and plants
are
not
yet
(Dom, 1993b). This is reflected by the control parameters
used in the present European Guidelines for Integrated Production (IP) of fruit
(Sessler, 1993). A comprehensive system management requires more
sufficiently
scientific
As
known
knowledge.
suggested by Baumgartner
ecosystems
hierarchal
can
be
and Delucchi
divided into subsystems
(1988), complicated agroand investigated with a
approach. The whole agroecosystem
terms of all the variables involved in this
determined from
a
study
of the
can
then be
analyzed
in
ecosystem, and their interactions
dynamics of the subsystems. Some
more strongly than others, allowing identification of
conveniently be studied in separate research projects
components often interact
subsystems
that can
(Baumgartner et al., 1990). The plant and its organs
subsystems because they
the basic
are
always part of these
units to be considered,
are
production
irrespective of the presence of associated organisms. Plant, plant parts,
2
arthropods,
weeds and diseases
affected
by
such
cultural
as
treated as
are
uncontrollable factors such
as
populations
which are
the climate and controllable factors
practices.
apple ecosystem is one of the main fields of interest in the
Entomology Group at the Institute of Plant Sciences, ETH Zurich, Switzerland.
Since 1980, the
The
long
goal of analyses and basic research of the apple orchard
term
a scientific base for the development of system
management programs. Experience made during the analysis of apple
system
was
to create
production systems
of
subsystems
in Switzerland has shown that the
the
creates
most
useful
base
yield,
apple
dynamics
the
cultural
practices.
tree
al., 1990),
on
the
dynamics
optimize agricultural
subsystems
investigations of the processes forming crop
production systems (Baumgartner et al., 1990).
needs profound knowledge and
study
to
Work with these
limiting environmental factors and various
subsystems addressed were the 'Golden Delicious'
of pests,
The
(Baumgartner
et al.
1984,1990), the apple scab (Baumgartner
et
the mite (Panonvchus ulmi Koch and Tetranvchus urticae Koch;
Baumgartner and Zahner, 1983) and the apple aphids (Rhopalosiohum
insertum Walk., Dvsaohis plantaainea
1984; Graf et al.,
1985).
The
the evaluation of cultural,
the
same
insights
chemical, and
time, important gaps
research work and
Pass., Aphis pomi De Geer; Graf,
obtained have most
were
biological
notably permitted
spider mites. At
control of
knowledge, requiring further
practical pest management and
shown in
hypotheses relevant
to
ecological theory.
The
physiological
practices,
was
Plant Nutrition
state of the host
Group.
plants and the effect
spider
mite
Schnider
plants
on
and Rutz
The
plant, which varies under different cultural
little examined and therefore studied in
of water stress on the
CL urticae)
were
development
the green
apple
potted apple
of the
two-spotted
investigated by Wermelinger (1985) and
The effect of different levels of
(1989).
cooperation with the
The effect of the nutritional state of small,
nitrogen fertilization
aphid A. pomi was studied
of
apple
by Hugentobler (1990)
(1993).
objective of the present study
between the green
was to investigate the interrelationship
apple aphid and its host, the apple plant, as affected by
different water regimes. For this purpose, the effect of differential water
supply on plant growth and on physiological plant parameters, on the
development of aphid populations, as well as the feedback effects of aphids
on
well-watered
and
water
stressed
host
plants
were
examined
3
Based
simultaneously.
development
of
on
these examinations,
aphid populations feeding
different water regimes
were
The aim of this
study is
or
for the differential
apple plants
to describe and
quantify the possible
apple plant and
effects of water
the green
apple aphid.
abiotic factor of the environment that affects
physiology, chemistry, growth,
and/or
development
in a measurable
(Heinrichs, 1988; Louda and Collinge, 1992). Water
way
grown under
Water Stress
on
stress on the interaction between the
Stress is any biotic
causes
evaluated.
Short Review
1.2
on
stress is the
induction of a turgor pressure below the maximal potential pressure.
et
plant
negative
(Osmond
al., 1987 cf. Louda and Collinge, 1992). It may be caused both by
deficiency
of water available to roots,
result of water
excess
indicates
a
essential
resource
deficiency
for
loss of roots due to
by
(flooding). For the purposes
or
in water and not
an excess
of this
study,
rotting
water stress
due to flooding. Water is
plant metabolism. All aspects
of
a
as a
an
growth, development,
reproduction are directly or indirectly dependent on an adequate water
supply. Since such stress often has strong effects on plant physiology it may
and
also affect the interaction between the
plant
and its herbivores. Both
aphid populations have been
(Waring and Cobb, 1992). Unfortunately, the causal
increases and decreases in the size of
attributed to water stress
relationships leading from water stress to the insect response are very difficult
disentangle and frequently remain obscure.
to
The effects of water stress
insect
on
performance, especially
plant traits
of
and their
potential relevance to
phloem sucking insects, will be briefly
reviewed:
1.2.1
Plant Growth
Many processes involved
in
plant growth, including cell enlargement, cell wall
synthesis and protein synthesis
are
reduction in plant size is the most
cell
enlargement
extremely sensitive
common
to water deficit. A
result of water stress, because
is the process most sensitive to water deficit
Significantly
less tissue will be produced and thus made available to insect herbivores if
during the active growth phase of a plant (Hsiao, 1973;
Gershenzon, 1984; Mattson and Haack, 1987; Holtzer et al., 1988). Total leaf
water stress occurs
4
area decreases appreciably with an increase in water deficiency, thereby
decreasing photosynthetically active surfaces (Mattson and Haack, 1987).
Plant Nutritional
1.2.2
Quality
availability of organic nitrogen (amino acids, amides and related
compounds) has been shown to be a critical, if not limiting, factor in the
population growth of many insect herbivores and in particular of phloem
The
feeders such
aphids. Nitrogen metabolism is among the processes most
(Hsiao et al., 1976). In general, water stress disturbs
as
sensitive to water deficit
nitrogen metabolism in such
a
way that
protein
contents decrease while
amino acids increase in concentration. The observed increase in amino acid
content results from
i.e. reduced
protein hydrolysis
protein synthesis
as
well
as
from reduced
plant growth,
and hence utilization of amino acids. This may
to a qualitative improvement of the nutritional base of aphids.
Photosynthesis, translocation of photosynthates, partitioning of photosynthate
between sugars and starch, rate of hydrolysis of starch, and respiration are
all affected by water stress and lead to changes in carbohydrate metabolism
lead
(Kramer,
1983 cf.
Mattson and Haack,
direct role in the
Not
on
a
presence and absolute concentration of a specific nutritional
improve the aphids diet; also the ratios of these nutrients may be
just the
element
1987). There is little evidence,
carbohydrate availability play
growth of insect populations (e.g. Holtzer et al., 1988).
however, that the effects of water stress
can
important (nutritional-balance)(Mattson and Haack, 1987). A wide
plant secondary metabolites, also found in the phloem of plants
variety
just
as
of
(e.g. phenols and flavanoids), have been shown
defenses in
to function as chemical
plants against insect herbivores. Gershenzon (1984) concluded,
significantly alters the amounts of defensive compounds
cyanogenic glycosides, glucosinolates, alkaloids, and terpenoids
that water stress
such as
present in plants.
Plant Water Potential
1.2.3
Osmotic adjustment is
osmotic
a mechanism by which water stressed plants lower the
potential by dehydrating (passive) and/or accumulating solutes in
thereby maintaining turgor. Some of the solutes responsible
are soluble carbohydrates, sugar alcohols, amino
acids, organic acids, and inorganic ions (Morgan, 1984). Many of the solutes
cells
(active)
for osmotic
and
adjustment
5
that increase in concentration in response to water stress
serve as
feeding
stimulants and/or primary nutrients to insects. Water stressed plants may thus
more attractive and/or nutritious to insects than nonstressed plants.
Despite the positive effects of osmotic adjustment, turgor pressures in plants
may decrease to zero under severe stress (Hsiao et al., 1976). The direct
be
effect of
turgor is likely
consequential on sucking insects. For
key variable determining the
obtain food. Feeding has been attributed to
to be most
them, turgor
pressure must be considered a
physical effort necessary to
capillarity, assisted by a decrease in
sap surface tension due to
saliva, turgor
sucking with the ciberial pharyngeal
pump (Pollard, 1973; Klinglauf, 1987). On the host plant, the normal turgor
pressure is adequate but may become inadequate during water stress with
pressure of the
plant
sap and to active
different aphid species reacting in different ways
almost certain that
of
supply
of
It seems
phloem sap (Wearing, 1968).
Plant Microenvironment
1.2.4
The microenvironment
humidity)
feed
(Pollard, 1973).
aphid feeding is assisted by the pressure and persistence
adjacent
to individual
organisms (temperature and
is most relevant for its development. Small insect herbivores that
leaves can expect a microenvironment dominated by the leaf. Water
experienced by a host plant can have considerable impact on the
on
stress
experienced by
plants suffering from
microenvironment
insect herbivores.
increase when
water
order to lower transpiration, which is
stressed leaves are
warmer
a
deficiency
Leaf
temperatures
close their stomata in
cooling process. Because water
feeding on
than well-watered leaves, insects
stressed
plants will probably maintain higher body temperatures.
Temperature-dependent organisms exhibit significantly different metabolic
rates under different temperature regimes. Temperature differences between
well-watered and water stressed plants are commonly 2 to 4°C, but they can
great as 10 to 15°C depending on size, shape and orientation of leaves
be
as
as
well as on
Willmer,
plant species (Bucks
1986). Unfortunately,
herbivores
can
on
al., 1984 cf. Mattson and Haack, 1987;
microenvironment
of
many
insect
be difficult to measure, not least because of the strong
gradients between leaf surface
effects
et
the
and ambient
atmosphere and its variable
growth (P.W. Miles,
insects of different size and hence stage of
University of Adelaide, South Australia,
pers.
comm.).
6
Plant Attractiveness
1.2.5
For insect growth, survival and reproduction, plants need to be nutritionally
adequate and must also meet requirements of smell and taste to which the
are genetically and conditionally prepared to respond (secondary
plant metabolites). Water stress may alter behavioral responses of aphids
such as the attraction to plants. Accumulation of the amino acid proline is a
herbivores
widely observed response of plants exposed
attractiveness of water stressed plants
proline (Miles
levels of
sucrose)
early
at
et
was
to water stress. An increased
reported to
be related to elevated
al., 1982). Increases in soluble sugars (e.g.
of
stages
water
stress
associated
were
with
phagostimulatory
or
cf. Holtzer et al.,
1988). Leaf texture, hairiness, leaf color, leaf thickness
perhaps nutritional effects (Bernays and Chapman, 1978
or
morphological leaf characteristics are also likely to change under water
stress and, therefore, can have an influence on insect behavior.
other
Effects of Aphids
1.3
An
aphid infestation,
virus diseases,
Host Plants
aside from any role it may
negatively
can
on
and/or
in the transmission of
play
positively affect plant development (e.g.
Oatman and Legner, 1961; Hamilton et al., 1986; Kaakeh et al.,
depending
itself. The
damage
negligible,
are
the insect
on
and
density, time
possible yield
of infestation and
losses caused
they impose
a
at
by aphid feeding may be
aphid species
in
an
in such numbers that
occur
plants they attack
apparent reduction of overall plant growth (Miles,
serious nutrient and fluid drain
eventually resulting
plant
densities. Some
relatively high population
important agriculturally only because they
even
1992)
the host
on
on
the
1989b). Aphids may increase the well-being of their host plants by stimulation
plants' nutrient uptake (Miles, 1989a). Further, aphids have the
of the
potential
to affect the
physiological relations
Miles, 1989a). The penetration of aphids
water
uptake
Miles, 1989a)
symptoms.
and
as
transpiration
well
as on
More obvious
deformation of
in the host
was
of their host
plants (Kloft,
photosynthesis, leading
damage
caused
plant (Pollard, 1973;
shown to have
some
by aphids
are
discoloration and
plant organs caused by salivary toxins, the plant's
on
aphid's
on
to leaf senescence-like
reactions, and/or viruses transmitted by the insects (Pollard, 1973),
by the effects of sooty mold growing
effect
1954 and 1960 cf.
excreta.
hormonal
as
well
as
7
The
to
high diversity
predict
of
plant reactions
the reaction of
aphids
to water stress
implies that it is
not easy
Most
to water stress.
probably some
reactions of the plant to stress will support and promote aphid development
and others will impede aphid development. As both population increases and
decreases have been attributed to water stress
factors
deciding the effect
on
(Waring and Cobb, 1992), the
intensity and
herbivores may well be the
duration of the stress.
Materials and Methods
1.4
The components of the apple ecosystem under study
were:
the
apple plant,
the green apple aphid and water stress.
The Host Plant
1.4.1
Apple tree, Malus domestica Borkh.,
cv.
'Golden Delicious'
Production. The bulk
area (71%) of Switzerland's pome and stone fruit
production is attributed to the cultivation of apples (4 943 ha). A high diversity
among apple varieties exists but the variety 'Golden Delicious' is still
dominant. Sixty five percent of the apple production is under intensive
cultivation
systems with planting densities between 300-3500 trees/ha
(Pezzatti. 1992).
Host
micropropagation.
experiments throughout
The
the
apple plants (maximum 1 year old) used in all
study were produced by tissue culture. As in
previous studies that have been part of the overall apple ecosystem project
conducted in vitro by the Entomology and Plant Nutrition Group, a high
number of genetically and physiologically similar plants were needed.
Micropropagation (multiplication and rooting) of the 'Golden Delicious' plants
was carried out according to Wermelinger (1985). Proliferation and rooting
media were modified according to Hugentobler (1990; see Appendix Table 1).
The
explantate
of the 'Golden Delicious' clone was
mother clone and its successors
were
presented here.
After rooting of seedlings multiplied
a
seedling.
The same
micropropagated
and used
throughout
the study
adapted to
place
in
a
a
under sterile
conditions, plants
were
non-sterile and water unsaturated environment. This step took
diluted
Hoagland
nutrient solution
(1/8 N;
see
Appendix Table
8
2)(Hoagland
a
and Arnon,
1938) modified according
a
Hugentobler (1990)
day/night period,
16/8 h
growth cabinet (20°C temperature,
PPFD measured with
to
35
in
umol/m2/sec
LI 185 Quantum/ Radiometer/Photometer, Lambda
Instr. Corp.). The relative humidity inside the growth cabinet was reduced
stepwise from near saturation to about 75% relative humidity over a period of
days depending on the progress in root development and state of the
plants. During this step an average of about 25% of the plants were lost
7-10
mainly due
1/4
N
to
rotting. For further adaptation, the plants
Hoagland
modified
environmental conditions in
adapt
solution
a
walk-in
to lower relative humidities
transferred to
were
a
experimental
grown
growth chamber. The plants had to
and
under
(about 55%) and
to
higher light intensities
(about 400 umol/m2/sec PPFD).
Environmental conditions.
growth chamber
was set to
The ambient maximum day temperature in the
22°C, and the minimum night temperature was
17°C. The temperature followed
set to
minimum temperature between
1230
between
to
2°°pm.
The
200
mean
the
growth
chamber
temperature, and the
mean
a
sinusoid
6°°am
were
was
2.5°C
to
up
daily temperature
temperature and light intensity and
was
with
the
set
calculated to be 19.8°C.
was
was
were
calculated
divided into 15 minutes segments
Temperature settings corresponding
than
warmer
highest at the maximum
during the night. The mean daily
zero
temperature under fluctuating conditions
day
curve
found, however, that temperatures
The deviation of actual from set temperatures
method: the
day/night
and maximum temperature
daily temperature under such fluctuating
conditions should have been 19°C. It
inside
to
to each
segment
using the following
yielding
were
a
total of 96.
added and then
daily temperature was calculated by dividing this sum by 96. This
procedure is based on the assumptions that temperature effects on plants
the mean
and
aphids per day
are
additive and that
aphid population development.
fluctuating temperatures either have
affect
that
temperature fluctuations do
There
are a
no
not
few studies that suggest
effect,
or
have
a
stimulating
aphid development, enhancing fecundity and longevity, compared
with aphids reared at constant temperatures (Kindler and Staples, 1970 cf.
effect
on
Benedict and
A 16:8
Hatfield, 1988; Michels, Jr. and Behle, 1989).
light/dark regime
and off in three
set to
was maintained in all experiments. Lights went on
intensity steps. Relative humidity in the growth chamber was
70%, but the effective RH
constant
during
a
day,
however
was
was
not
55-60%. The
humidity
surveyed constantly.
was
Maximum
kept
light
9
intensity measured at high noon (at the setting of maximum temperature and
light intensity) amounted to 400-450 u.mol/m2/sec PPFD.
Growth substrate. When the
they
were
transferred
environmental
into
plants reached a length of approximately 20 cm
a
soil
mix
and
to
adapt
to
the
mix
used
for
the
allowed
The
conditions described above.
soil
experiments and aphid rearing consisted of mineral soil
:
composted soil
:
mm diameter) : peat moss
5:5:1:1,
respectively. Pot sizes will be described below under "experimental
procedure" (see page 15).
The micropropagated plants expressed a high morphological variability mainly
at a ratio of
quartz sand (1 to 1.5
in
plant heights.
which
was
possible
A
started
micropropagations
uniformity
that the
a
redifferentiation of the
these
explanations,
it
phenomenon was that the clone
(1986), and has undergone multiple
for this
the years, may have mutated. Another
over
of
reason
few years ago
a
possibility is
clone may not be expressed until 3 to 4 years after
plant (cf. Hugentobler, 1990). Whatever the validity
found that over the adaptation period the effect
was
very small differences in the
system resulted in
a
variation of
height
of
of
between
individuals.
After
transplantation and before starting
several times with 1/2 N modified
depending
on
the
length of
an
an experiment, pots were watered
Hoagland solution. During experiments and
experiment, plants were further fertilized
several times with 1/2 N modified
Plant
protection.
To
prevent and
Hoagland
solution.
to control
plant infestations in the growth
such as powdery
by
chemical
several
and
mildew, two-spotted spider mite,
sprays were
thrips,
Karathane
(Dinocap 25%; Maag)
applied. Funginex (Triforine 20%; Maag),
and Sulfur (Thiovit 80% S, Sandoz) were used against powdery mildew.
Ambush (Permethrine 25%; Maag), Apollo SC (Clofentezine 42%; Maag), and
Arafos (Oxamyl 7.5%, Methanol 12%; Maag) were used against two-spotted
spider mites and thrips. Two weeks before the start of an experiment,
spraying was stopped and in case of further mite or thrips infestations,
and/or biological control with
mechanical control
predatory mites
chambers
pests other than the green
(Phvtoseiulus persimilis
thrips)
On
an
was
apple aphid,
against mites and Amblvseius cucumeris against
used.
average, three months passed from
sterile conditions until the
plants
were
seedling multiplication
ready for the experiments.
under
10
The
1.4.2
The green
Damage.
apple aphid, Aphis pomi De Geer
The green
in Switzerland
small
Aphid
apple
apple aphid is of secondary importance
(Ammon
trees
et
leading
al., 1986). It
become
to shoot deformation and
malformation and curling, both
active leaf area.
can
resulting in
a
a
on
serious
stunting
reduction of
as
apple
trees
problem
on
well as leaf
photosynthetjcally
Watersprout meristems and shoot tips often die under severe
aphid population densities. Older
trees can compensate for the loss and are
therefore not considered to be sensitive
(Baker and Turner, 1916; Oatman
andLegner, 1961).
Systematics. Aphis pomi De Geer: Order of Hemiptera, Suborder of
Sternorrhyncha, Superfamily of Aphidoidea, Family of Aphididae and
Subfamily
Life
on
of
Aphidinae (Carver
al., 1991).
et
cycle. A. oomi is monoecious (sexual and parthenogenetic phases occur
the
same
host) and holocyclic in Central Europe (propagates sexually and
parthenogenetically) (Tomiuk and Wohrman, 1982).
egg stage
on one
(stem-mother)
and
are
summer
is
starts to
spring the eggs hatch and the fundatrix
reproduce parthenogenetically. Reproduction in spring
entirely parthenogenetical. These generations of virgins,
mainly apterous, feed
summer.
It passes the winter in the
year old shoots. In
on
the succulent
This aspect of the green
makes it easy to
rear
foliage
which
apple throughout
apple aphid life cycle, beside others,
of
the insect under controlled environmental conditions.
Alatae
produced are merely for dispersal when the population density on the
host plant becomes too high. In fall, males and oviparous females (sexuales)
are
produced by the sexuparae,
deposited preferentially
mate and the
over-wintering eggs
are
watersprouts (Baker
Lathrop,
1923). The life cycle of a parthenogenetically reproduced aphid consists of 4
larval instars and an adult stage. The aphid develops from one stage to
another
instar
and Turner, 1916;
on
by molting (ecdysis). The
can
be
distinguished from
instars among each other
can
particular the fourth larval
aphid by the form of its cauda. The
distinguished by body size and form.
instars and in
the adult
be
Nutrition. The majority of aphids
are
phloem feeders.
In
general, nitrogen
is
the basic nutrient which first becomes limiting for aphid development. The
phloem sap is rich
in
carbohydrates
advantage that nutrients
Dixon, 1987).
are
and poor in amino acids but has the
in soluble and renewable form
As a result, vast
quantities
of soluble
(Risebrow
and
carbohydrates (e.g.
11
sucrose)
ingested
are
high sugar
in
excess
of
dietary requirements, and this explains the
content of the excreted
component found in
and it appears that
aphids' dietary
honeydew. Melezitose is the main sugar
aphid honeydew. It is not found in phloem sap, however,
of the
sucrose
phloem
is transformed to melezitose in the
tract.
question of the degree to which aphids ingest their food passively and/or
actively is still not entirely certain. Phloem sap is under pressure (reported
The
turgor pressures in phloem range from 0.5 to 2.5 MPa depending on the
author)(Wright and Fisher, 1980; Weatherely, 1982 cf. Schulze, 1991) and is
expected
to flow
by capillarity (passively) into the aphid's stylet, whenever
of the sieve tube elements is
one
pierced. Aphids
have
ciberial
pharyngeal
passive uptake but it undoubtedly
suck their food actively (Pollard, 1973; Klinglauf, 1987;
a
pump which could be used to control
enables
aphids
to
Hugentobler, 1990),
since
aphids
can
survive
on
artificial diets which
are
not
under pressure. The fact that aphids do not grow to maximum rates on such
diets, even when they contain much higher concentrations of limiting nutrients
than
phloem
1968)
sap, has been considered
to indicate that
on
by some authors (e.g. Wearing
their normal food plants
aphids
must feed
et
al.,
passively
to some extent at least.
Developmental biology. The developmental threshold (T0) of A. pomi was
reported by Lathrop (1923) to be 5°C. Experiments by Graf et al. (1985) to
determine A. pomi life table statistics showed that T0 was 5.9°C. Furthermore,
the authors specified the highest developmental rate of A. pomi to be at
25.8°C, and the maximum mean fecundity to be at 19.7 20°C. The average
daily temperature (19.8°C) approximated over a day in the present study was
optimal for maximum fecundity per female.
In the study presented here, the temperature of 19.8°C was the weighted
-
mean over the whole
the
growth chamber
growth chamber.
varied
depending
In
fact, ambient temperatures inside
on
the distance from the source of
fight, the ventilation, the distance from chamber
walls etc. These variations
could amount to 5°C. Leaf surface temperatures further increase with water
stress and in
Generally,
growth chambers
the temperature of
can even
an
temperature of the microenvironment.
aphids
are
highly affected by
Aphid rearing. Aphids
under
cages
in
the
were
exceed the ambient temperature.
insect is close to air temperature
Hence,
leaf surface
reared
on
greenhouse.
the
or
to the
body temperatures of
temperatures.
apple plants grown in soil
Reproduction was exclusively
young
parthenogenetic. Temperatures in the greenhouse ranged
between 23°C
12
was 17 h. Every two to
aphid population densities on the plants became too high
during the day and 18°C during the night. Daylength
three weeks, when
and alatae
adults
were
were
produced, uninfested plants were placed in the cages. A few
plants and the damaged plants were
transferred to the uninfested
removed and discarded.
Exp.
For
1 and
greenhouse
The insects
(referred
Exp.
2 fourth larval instars
and transferred to the
were
released
to as leaf
on
(L4)
were
carefully collected
experimental plants
in the
growth
the tenth leaf counted from the
A). These larvae
were
reproduction. After four to six L1 were bom the mother
Subsequent handling of L1 depended on the objectives
experiment
greenhouse
was
to the
induce water stress
marked
removed.
set for each
respective section. The beginning of
by the birth of the L1. Aphid transfer from
growth chamber and the
were
start of
counted backwards from
day
withholding
0. In
Exp.
water to
3 and
Exp.
allowed
respective sections)
aphids (specified
up a population. Aphid transfer in these experiments
signified by day 0.
in the
4, the transferred
to
was
and will be discussed in the
experiment (day 1)
the
plant apex
allowed to reach adulthood and
start
an
in the
chamber.
were
reproduce and build
was
The Water Stress
1.4.3
Preliminary experiments. Three preliminary experiments were conducted to
find the most
on
appropriate
method to induce water stress and to test the effect
aphid development (e.g. Sumner
et
al., 1983 and 1986; Krizek, 1985;
were: (1) water stress induced
Tingey, 1985).
in soil culture by controlled watering and (2) water stress induced in a nutrient
solution using polyethylene glycol (PEG) as an osmoticum. In summary, soil
culture had the advantage of approaching field patterns of water stress
development and had the disadvantage of not maintaining the stress at a
constant level. The nutrient solution culture had the advantage of allowing a
constant and reproducible water stress as well as nutrient supply and the
disadvantage of PEG being a potential toxicant for plants and aphids and of
not reflecting patterns of water stress in the field. Results of the preliminary
Snow and
The methods tested
experiments also showed that water stress in the soil and the nutrient solution
cultures
produced different effects. Most striking
were
the visual differences.
Plants, cultivated in nutrient solution expressed very little decrease in plant
growth and development: there was no reduction in number of leaves per
plant and in total leaf area, a slight reduction in shoot length and increased
13
leaf succulence with water stress. None of the expected
(decreased
water stress
potentials,
leaf water
typical reactions
increased stomatal
to
resistance)
observed.
were
Theory.
Water in soil and
the presence of the solid
pressure
plants is subject
to several force fields caused
phase, dissolved substances, hydrostatic
or
by
tension
(external gas pressure), and the gravitational field. These effects are
quantitatively expressed
common
in terms of the potential energy of water. The
potential is the megapascal (MPa). A commonly used
unit of water
alternative unit is bar (1 MPa
plant)
or
be
can
expressed
«F
4*
?„
Yp
=
as
=
10
bars). Water potential
(Begg
V0
+
and Turner,
¥P
+
Vm
potential or total potential
potential due to the presence
=
water
=
osmotic
system (soil
¥g
of dissolved substances.
pressure potential. In soils it is related to the hydrostatic pressure
=
found under saturated conditions. In
acting
Ym
+
in any
1976):
=
outward
on
potential due
matric
plants it is the turgor pressure
cell walls and membranes.
to
the
forces
of
capillarity
molecular
and
imbibitional forces.
Yg
gravitational potential
=
The
*Fg
in soils
can
be of
due to the
be
in
as
low
-2 MPa
as
comparison
In the
plant
plant,
negligible (Nobel, 1991).
¥g is considered insignificant
Water deficit in soils is
are
forces of water.
importance for drainage in very
otherwise, it is considered to be
situations, the
gravitational
(Begg
and
wet soils but
In most crop
Turner, 1976).
usually dominated by the Ym component, which
or even
lower. The other two components
(¥„
and
can
Yp)
frequently negligible.
*F had
gained wide acceptance
as a
fundamental
measure
of
(indicator of physiological water stress). Leaf water
the plant OF) is the algebraic sum of ¥„, Yp and ¥„,. However, in
water status
potential in
potential components of concern are the *¥P and Y0, unless
badly dehydrated (Hsiao, 1973; Begg and Turner, 1976; Holtzer
most cases the
the tissue is
et
al., 1988; Schnider, 1989). On the other hand,
and Corlett
(1992),
rather than Y
plants
to
was
drought
the notion of Hsiao
as was
reviewed
and Oertli
by Jones
(1976),
that
«FP
controlling physiological responses of
been supported by later investigations (Turner and
the crucial factor
has
(1973)
14
Jones, 1980; Sinclair and Ludlow, 1985). Furthermore, Sinclair and Ludlow
(1985) suggested that changes
cellular volume
in cell volume act
Turgor
pressure, i.e. of water deficit.
as
the transducer of turgor
(Yp)
is thought to influence
through elastic and plastic dimensional changes of cell walls
pressure
(cf. Sinclair and Ludlow, 1985; Turner, 1986). Cell elasticity and extensibility
by environmental conditions such as
availability (Studer, 1993). In addition, several
vary with species and may be affected
and/or water
nutrient
investigations suggested that
roots act as a sensor of water deficit via root-
produced plant growth regulators (e.g. ABA and cytokinins)(Davies, 1987;
Tardieu and Davies, 1993). According to Turner (1986), the identification of
the root
the site of
as
of turgor pressure
"sensing" soil water deficits does not eliminate the role
as
the transducer of water deficits,
but
moves
the
from leaves to roots.
emphasis
plant water deficit that develops in any particular situation is the result of
complex combination of soil, plant, and atmospheric factors (Begg and
Turner, 1976; Schnider, 1989), all of which interact to control the rate of water
The
a
absorption and
water loss. It is the result of both reduction in soil matric
potential (Y^,) which occurs, usually progressively, over a period of time, and
evaporation rate which occur with daily changes in net radiation
and humidity. Typically, plants experience diurnal cycles in which water
fluctuations in
deficits
the
develop in the late morning and afternoon and may be relieved during
evening when transpirational loss decreases and at night when transpi¬
ration may become
zero.
during
recovers to
Characteristically Y in the leaves is lower than Y^
Ysoi| at night (Holtzer et al., 1988; Schulze,
1991). Components of plant water potential in phloem and xylem cells can be
the
day but
much different from bulk tissue. In
xylem, Y0 is very small and Yp is mostly
negative. On the other hand, Y0 for phloem can be very strongly negative,
and Yp is positive (Holtzer et al., 1988; Nobel, 1991).
Adaptation. Many plants developed morphological and physiological
adaptations to water stress. They range from drought escape to dehydration
tolerance
on a
cellular basis. The mechanisms of
maintaining turgor
or
in
adaptation act either in
maintaining volume by increased elasticity. Some
examples of ways to maintain turgor are the maintenance of water uptake
(increased root density and depth), reduction of water loss (increase in
stomatal
as
osmotic
adjustment.
adaptations
well
as
cuticular resistance and reduction of leaf
For
a
to water stress in
review of
apple
morphological
trees see Lakso
and
(1983).
area), and
physiological
15
Osmotic
adjustment
ability of higher plants to accumulate solutes in
(active osmotic adjustment), thereby maintaining
is the
response to water deficit
turgor, cell enlargement and growth (probably at
opening
a
photosynthesis,
and
consequence of
adjustment)(Turner
rather than the
decreasing
and
mere
reduced rate), stomatal
a
accumulation of solutes
water contents in
cells
as
(passive osmotic
Jones, 1980; Morgan, 1984; Turner, 1986). Some of
responsible for osmotic adjustment
the solutes
are soluble carbohydrates
(fructose, glucose), sugar alcohols (sorbitol), amino acids (proline), organic
acids, and inorganic ions (Morgan, 1984). Osmotic adjustment of leaves and
other organs varies with
plant species and even among cultivars. The degree
adjustment is affected by both the rate of stress and stress
of osmotic
preconditioning of the plant (Turner and Jones, 1980; Morgan, 1984).
Apple leaves are very drought tolerant (Davies and Lakso, 1979a; Sritharan
and Lenz,
1989) and
drought (Lakso,
et al.
in the cell sap of
woody
et
was
adjust osmotically
found to be
species and
changes,
contribute to
elasticity
the tissue
of
number of
a
drought
soil matrlc
tolerance in
apple
potential (Y^) by
Moisture
apple changes but
are too
means
Equipment Corp., CA).
in the soil was measured
Tensiometers
are
suitable
soil
placed in
for
(i.e. high Ysoil). Below Y^ of
on
-
the other
insensitive when there is little water stress
(Y^ > -0.10 MPa).
(well-watered) treatments
means
One tensiometer was
cm
a
of tensiometers and gypsum blocks
Throughout this study, therefore, Y^ of control
measured by means of tensiometers and that of the
by
Y0
trees.
were
treatments
not
It seems that
MPa, tensiometers give incorrect readings. Gypsum blocks,
hand,
10
adjustment (cf.
morphological and physiological adaptations
measurement of low levels of soil water stress
0.08
well as of many
as
deficiency.
Experimental procedure. The level of water stress
(Soil
in response to
primary carbohydrate
to contribute to total osmotic
the season in response to water
combination of
as
a
al., 1991). Davies and Lakso (1979a) proposed that, apart from
any diurnal
throughout
observed to
1984). Sorbitol
apple leaves (Wang and Stutte, 1992)
rosaceous
Ranney
were
depth).
water stressed
of gypsum blocks.
placed approximately in
the center of the control pot
In the water stressed pots, 1 to 2 gypsum blocks
(at
were
1 to 2 gypsum blocks in 7 cm soil
depth
diagonally opposite. Measuring Y^ by gypsum blocks or/and tensiometers
does not give an exact measure of the water status in the rhizosphere of the
plants
14
cm
soil
depth and
roots. Soil matric
than at the
point
potential
of measurement,
at the root surface is
especially when
expected
to be lower
the soil dries out and soil
16
water conductance decreases. Measurements of soil matric potentials
measurements in time and space.
point
are
extrapolated from them had
measured and the water stress intensities
considered to represent
potential
an
to be
absolute value. Soil matric
measured daily and in the afternoon (after the period of
temperature and light intensities). The readings of the gypsum
was
maximum
placed
blocks
range rather than
a
(Y^)
Therefore, the Y^-values
in
14
depth indicated
soil
cm
watering
when
became
necessary.
Water stress
time and
induced
allowing
by withholding
the soil to
reached; the
stress was
several
was
drying cycles,
a
dry
plants
were
desired
intensity of
plants experienced
pattern called Intermittent drying cycles. Since the
at least one
To allow the soil to
gradually and uniformly
dry
care
a
then rewatered. All
length of an experiment was
technique was inevitable.
given conditions,
plants for a period of
water from the
gradually until
out
as
month, the intermittent drying cycle
had to be taken in
as
possible
under the
choosing the soil mix and the pot
size. To reduce
(2
-
3.5
mm
in the soil is
in
a
evaporation from the soil surface, a 1 cm layer of quartz sand
diameter) was spread to cover the soil surface. Water stress
dynamic process
and cannot be held uniform in a pot. The
soil and the soil around the roots will
dry
more
bottom of the pot. The quartz sand cover was
at which
the top soil dried out due to
quickly
an
attempt
to reduce the rate
environmental conditions
irradiation, temperature and ventilation). The pot sizes used
pots (30*30*26 cm) for
(light
20 L square
cm in
diameter)
plant.
for
one
To
quantify the effect
the
plant to water stress had to
or
were
plants and 10 L round pots (30
two
top
than the soil at the
of water stress on
indirectly could affect
or
plants, physiological reactions of
be measurable. Those
changes which directly
were of special
aphid development
influence
interest:
Leaf water
potentials (Y)
Scholander bomb method
al., 1965).
and
A leaf
directly
was cut
were
measured in
general
(PMS
Instrument Co. Model
with
sharp
measured. The
a
same
leaf
predawn using the
1002) (Scholander
et
petiole
immediately frozen to -70°C
membranes), its sap squeezed out,
razor
was
(to interrupt metabolism and destroy cell
at
blade at the base of its
then
and osmotic
potential Y0 measured by a vapor pressure osmometer
(Wescor 5100 C). The readings in milliosmol/kg water (mOs/kg) were
transformed to pressure units
mOs/kg
=
-2.43 MPa at 20°C
(MPa) according
(based
on
the
to the conversion factor: 1000
equation of van't Hoff, refer
to
17
Schnider, 1989; Wermelinger et al., 1990). Turgor pressure
calculated according to the
Water content of
calculated
on a
equation: Yp
plant can
a
fresh
=
Y
(Yp)
was
Y0.
-
also indicate water stress. Water content
weight basis. Fresh (FW) and dry weight (DW)
was
were
determined for the harvested shoots
used to measure water
(leaves and stem) as well as for leaves
potentials during the experiments. Plant tissues were
dried for 48 h at 65°C.
Individual leaf (also
were
measured
by
during
the
experiment)
means of a
and total leaf area at harvest
portable leaf
area meter
(LI
3000
(LA)
A). The
parameters described above that were used to quantify water stress in plants,
all destructive in nature.
were
In addition,
non
destructive parameters such
as
the increase in shoot
length
and number of leaves, rate of shoot extension and leaf appearance per
and leaf surface
temperatures
number of leaves
throughout
using
assessed. Shoot
day,
and total
measured and counted at constant time intervals
experiments. Leaf surface temperatures were measured
techniques and will be discussed in the relevant section. This
also to other parameters which
experiment.
length
the
different
applies
were
were
were
assessed
only
in
a
certain
Leer
-
Vide
-
Empty
19
2
Effects of Water Stress
on
Population Dynamics
of the Green Apple Aphid:
Life Table
Analysis
Introduction
2.1
The range of effects of water stress
aphids, is
broad. Literature
on
plant sucking insects,
in
particular
the action of water stressed host
on
plants
aphid species has accumulated since the nineteen fifties and continues
report diversely
on
the effects
on
the insects. For
on
on
to
example, Kennedy and
(1959 cf. Sumner et al., 1983) reported that drought reduced survival
fecundity of Aphis fabae (Soopoli) on spindle and on sugarbeet. Wearing
Booth
and
and van Emden
(1967)
stressed Vicia faba
found A. fabae
(F.)
and
Harris) fecundity increased
Tauber, 1954 cf. Sumner
reproductive
(Wearing
on
et
Pea aphid (Acvrthosiphon oisum
drought stressed garden peas (Baker and
al., 1983). Brevicorvne brassicae (Linnaeus)
rates declined with
and Van
reproduction unaffected by drought
marigolds.
Emden, 1967),
increasing
water stress in brussel
sprouts
whereas Mvzus persicae (Sulzer) exhibited
reduced
reproduction only at high stress levels on brussels sprouts and
highest reproduction at intermediate stress levels. For additional literature on
this aspect see Waring and Cobb (1992).
Despite the wealth of literature, however, the development of the green apple
aphid (Aphis pomi De Geer) on hosts suffering from water stress does not
seem to
have been studied
previously.
20
The
objective of the present section
apple plants and
the
was
to
study the effect of water stress on
population dynamics
of resident green
apple aphid.
plant itself had to be
characterized and quantified first in order to delineate adequate descriptors
for the effect of water stressed hosts on population dynamics of aphids.
on
For this purpose the effect of water stress
The best
single
measure
defined conditions is
of the
regarded
(Southwood, 1978; Hurting
et
on
the host
population growth of
species under
rm
al., 1990; Kaakeh and Dutcher, 1992). The
intrinsic rate of natural increase can be calculated
by parameters derived from
cohort life tables.
age-specific
or
2.2
Materials and Methods
2.2.1
Descriptors
of
for the
Development
Aphid Populations
The rate of increase in
unlimited environment is
population
a
minus death rate, and thus
If the number of
with
a
stable age distribution in
an
given by:
where N indicates the number of
at time t is
insect
to be the intrinsic rate of natural increase
organisms
organisms,
a measure
at time
t<,
is
t is time and
for the
rm is the birth rate
populations' growth potential.
N0 then, by integration, the population
given by:
N,
-
N0ermt
Under constant conditions,
age-specific fecundity (mx), survival rate (lx) and
development time (x) has often been estimated (Dixon, 1987; Chi, 1988). The
data of these life table parameters
using
the
can
be used to
equation:
£e(^x)lxmx-1
X
iteratively approximate rm
21
Since rm is
estimate, it is important to recognize the uncertainty associated
an
with this value.
Meyer
variance of rm which
(1986) introduced
et al.
a
Jacknife estimate of the
uncertainty. Some programs
to perform the required computations were made available lately (Abou-Setta
et al., 1986 (in Basic); Chi, 1988 (in Basic); Hurting, et al., 1990 (in Pascal);
Wermelinger et al., 1991 (in Fortran)).
Other useful
be used to
assess
this
(descriptors) are the net reproductive rate (R0), the
generation
(G) and the doubling time (DT). The net reproductive
is the multiplication rate per generation and is obtained by multiplying lx
measures
time
mean
rate
can
and mx:
Ro
E 'x
"
mx
X
Mean
generation time is defined
as
the
mean
development
time of
from birth until half of its progeny had been bom and is calculated
a
female
by:
Q_lnRo
and
mean
doubling
time is defined as the
until half of the progeny in
a
population
mean
was
development
time needed
born and is calculated
by:
DT-iHl
For
a
detailed description of these parameters and their
studies the reader is referred to
Southwood
Messenger (1964),
stress,
concurrent increase in the
Since aphids
are
increase in the
poikilotherm and
body temperature
The temperature effect
development in
et
in
ecological
(1972), and
(1978).
Since leaf surface temperatures, may increase
a
use
Krebs
terms of
can
significantly under
aphid's body
react rather
sensitively
may affect the rate of
be considered
physiological
water
temperature is assumed.
to
temperature this
aphid development.
by expressing
rather than
the aphid's
chronological time (Gilbert
al., 1976 cf. Asante et al., 1991).
Chronological time expressed
the
in
days is converted
equation:
t'
-
t
(T-T0)
to
physiological time using
22
where: t'
t
-
T
=
T0
=
time
estimate of aphid body temperature (°C)
developmental temperature threshold (°C)
Conditions
Experimental
2.2.2
Two
(day-degrees)
chronological time (days)
physiological
=
experiments, Exp. 1 and Exp. 2, were conducted to study plant and life
apple plants (cv. 'Golden Delicious') and the green apple
table parameters of
aphid under conditions
In both
experiments,
square
containers.
preparations,
as
of water stress.
two
apple plants were grown diagonally opposite in 20 L
mix, environmental conditions, experimental
Soil
well
as
induction and measurement of water stress
gypsum blocks per container in water stressed
on
treatments)
pages 8, 9, 15, 16 and 17. The treatments
(i.e.
water
(four
described
were as
regimes) applied
were:
1.
2.
3.
(C):
moderately stressed (M):
severely stressed (S):
control
If not otherwise
container
not.
8
one
of the two
or
experiments,
>
-1.80 MPa
10th
In
used to
to as leaf
newly
aphids
were
treatment in
40 and 55
were
In
kept
measure
plant
A) and
Exp.
per
removed, resulting in
Exp.
1 and 96
1 and
plant
a
or
stress treatment.
(L4)
were
transferred to the 8th,
apex at the
were
allowed to
beginning of the
develop
into adults
had died due to the transfer were
Exp. 2,
four and six
respectively of
in all treatments, and the
theoretical cohort size of 32
aphids in Exp.
days, respectively.
was
leaf water
potentials
Exp. 2, both plants of a container were infested
reproduce. Any L4 that were missing
born L1
1
per water stress treatment. In each
infested with aphids and the other
was
was
leaf counted from the
(referred
(well-watered plants)
water stressed treatments was
two fourth larval instars
replaced the following day.
the
Y^
aphids resulting in 16 replicates per water
experiments
and
-0.60 MPa
reading of all four gypsum blocks. Experiment
plants
The uninfested plant
In both
9th
-0.05 MPa
>
replicates (8 containers)
throughout the experiment.
with
>
Y^
mentioned, Ysog of the
calculated from the average
comprised
Y^
2.
Experiments
remaining
aphids per
1 and 2 lasted for
23
2.2.3
Data Collected
Plant Parameters
Plant growth. In both experiments,
number of leaves)
increase in
day
plant
measured
was
size
(final
initial
-
plant size (i.e. shoot length and total
weekly. Mean total plant size, mean
measurement),
and mean rate of leaf appearance per
day
mean
were
extension rate per
weighted
over
the whole
made it possible to
disregard fluctuations
experimental period.
procedure
in plant growth due to intermittent drying, particularly in water stressed
treatments. Plant growth was observed to decrease with the build up of water
stress in the soil and to increase again after watering. Mean internodal length
of the growth which took place during the experimental period was calculated.
This
Plant water relations.
first
fully expanded
plants
were
directly
During Exp. 1, leaf water and osmotic potentials of the
leaf (the 10th leaf from the apex) of aphid uninfested
measured predawn at the peak of
a
drying cycle
a
days after watering (start
repeated several times during Exp. 1 (maximum
consecutive leaf 1 to 2
cycle). This
was
of
and
new
4
on
the
drying
times). At
harvest, leaf water and osmotic potentials of the first fully expanded leaf of
plants as well as of plants infested with aphids were measured at
predawn. During Exp. 2, predawn leaf water and osmotic potentials of the first
uninfested
fully expanded
leaf at the
peak of a drying cycle were measured only once,
aphids feeding on the plants. In Exp. 2 at harvest,
osmotic potentials of two apical leaves, of two just
in order not to disturb the
predawn leaf water and
fully expanded leaves and
plant)
were
were
assessed.
of two mature leaves
Turgor
(in the lower parts
of the
pressures and water contents of these leaves
calculated.
In addition, one
water
plant of each
potential components
treatment in
on
Exp.
2
was
chosen to
measure
leaf
every second leaf from top to bottom of the
plant.
Area of Individual leaves. In
harvest to measure leaf water
was
assessed.
Exp. 2,
the
area
of each leaf
potentials (see plant
sampled
water relations
at
above)
24
Leaf surface temperature. Leaf surface temperatures were measured in the
growth chamber
23°C).
at maximum light intensities and ambient temperature (ca
Exp. 1, temperatures were measured on the lower leaf surface of
In
the seventh leaf from the apex
by
of
means
infrared thermometer
an
(Telatemp Corp., Fullerton, CA). The disadvantage, however, was that leaves
had to be turned
to measure lower leaf
over
operating distance,
which
was
required
often not be held free of other
surfaces, and that the 30
cm
for accurate measurements, could
objects. Leaf surface temperatures
were
measured at the beginning (day 5), in the middle (day 27) and at the end
Exp. 2, lower leaf surface temperatures were
portable thermocouple device (chromel/alumel, 0.02
(day 40) of the experiment,
assessed
in
mm
Exp.
by
means
diameter).
of
a
in
Leaf surface temperatures
and leaf A, which
was
defined at the
measured. The temperature
distance from the leaf
sensor was
measured 9 times
were
2. The tenth leaf from the apex, counted
on
the
day
during
of measurement,
beginning of the experiment
held next to the midrib
one
were
third the
petiole.
Plant biomass production. A "harvest" time was defined in Exp. 1 as
directly after all aphids of a cohort had terminated their reproduction,
irrespective of the level of water supply in the containers at that point. In Exp.
2, harvest
the
peak
after all aphids of
was
of the current
a
cohort had died and water stress reached
drying cycle.
leaves, fresh and dry weight
as
At harvest shoot
well
as water
length, total number
content of the shoots
of
were
assessed.
Life Table Parameters
The duration of each larval stage, the
until birth of first
offspring)
recorded
as
pre-reproductive time (time from birth
offspring), reproductive time (time from birth of first to last
well
daily.
as
adult
longevity, survival rates and fecundity
Larvae and adults that had died
recorded and larval
as
well
as
adult
mortality
was
during
the
study
were
were
Exp. 1, the
length of their
calculated. In
different instar
stages were recorded to determine the
development time. This was done on the basis of relative body size, ecdysis,
cauda form and color.
removed with
During adulthood offspring
small brush.
were
counted daily and
Age-specific fecundity (mx) and mortality (lx) as
well as development time (x) of adult aphids within cohorts feeding on
differentially water stressed plants were assigned to a life table and summary
statistics
were
a
then calculated.
25
For the conversion of the
aphids' body
chronological time (t)
to
temperatures under the different water
physiological
regimes
were
time
For this purpose leaf surface temperatures measured in each plant in
and
Exp.
2
page 8. In
were averaged over a day according
Exp. 1, mean daily body temperature of aphids
respectively.
stressed treatment,
aphids feeding
Exp. 2,
In
mean
the tenth leaf from the apex
on
the well-watered,
On leaf A in
Exp.
to the method described
be 20.9, 21.4 and 21.7°C in the well-watered,
moderately
Exp.
2
and
(f),
estimated.
1
on
calculated to
was
moderately and severely
daily body temperature of
was
21.2,21.4 and 21.3°C in
severely stressed treatment, respectively.
(see page 23), mean daily temperature was 19.5,19.6
moderately and severely stressed treatment,
and 19.8°C in the well-watered,
respectively.
This
approach
Temperature
effects
temperatures)
on
assumed that:
(fluctuating daily temperatures, e.g. day/night
development of aphids were additive.
The body temperatures of aphids in the three water supply treatments
remained constant throughout the experiments (no effect of intermittent
watering
leaf
on
temperatures).
All leaves within
(beside
the
the
a
plant and
rough separation
a
treatment had the same
temperature
between the tenth leaf from the apex
on
the day of measurement, and the tenth leaf from the apex at the
beginning
It
was
of
Exp. 2, i.e. leaf A).
observed that leaves which
were nearer
to the
growth chamber had higher surface temperatures than
irrespective of
leaves at
water stress treatment. Surface
source
more
of
light
in the
distant leaves,
temperatures of uppermost
higher than the ambient temperature. The distance
of light was an artefact encountered throughout the
noon were even
of leaves to the source
experiments which influenced aphid development.
During Exp. 2 it was noticed that aphids which settled
on
the upper part of
plant (growing leaves) behaved and developed quite differently from
aphids that had settled on the lower part of the plant (mature leaves). After
termination of the experiment, therefore, the plants were divided into upper
and lower parts and data analysis was done on the parts separately. The
apex and the upper 15 leaves were assigned to the upper and the rest to the
lower part of the plant.
the
Plants of
Exp.
surface. These
1
were
cut down at harvest to the fourth node above soil
to regrow to be used in Exp. 2. Only one
develop. This technique was applied to obtain a high
which was expected to induce a more gradual and uniform
plants were allowed
shoot was allowed to
root to shoot ratio
26
water stress on the
each container
was
Data
a
soil
sample of
taken to determine soil water content at the time of
peak of the
harvest when water stress was at the
2.2.4
Exp. 2 plants
After the harvest of
plant.
current
drying cycle.
Analysis
approximate rm, R0, G, and DT a computer program kindly made available
by B. Wermelinger (WSL/FNP, CH-8903 Birmensdorf) and described in
To
Wermelinger
et al.
(1991)
was
used. To test the effect of water stress
plant, life table and population parameters, differences among
on
means were
by standard analysis of variance (ANOVA) followed by a test of
significance difference (LSD) at a 5% level of significance if not
otherwise mentioned (Statgraphics 5.0, STSC Inc., Rockville, MA, USA).
compared
least
Simple linear regression
Ysou
and Y,
plant.
Y0
and
Yp
was
as
Correlation coefficients
applied
well
as
were
to describe the
among
relationship
between
potential components within
computed.
a
27
2.3
Results
2.3.1
Development of Water Stress
in the Soil
The water stress that developed in the well-watered,
moderately and severely
stressed treatments and among the 8 replicates of any
one
treatment
proved
highly variable. Figures 1 and 2 show the development of water stress
in one well-watered, one moderately and two severely stressed examples of
to be
Exp.
1 and
Exp. 2, respectively.
single pots.
At the beginning of
because
plants
examples shown
are
of
experiment, particularly in Exp. 1, Y^,
an
were
The
still
relatively
small in size and
were
representative
was
very
high
very well watered.
Watering frequency decreased with an increase in intensities of water stress.
Until plant harvest in Exp. 1, well-watered plants experienced 5 to 8,
moderately stressed 3 to 5 and severely water stressed plants 2 to 3 drying
In
cycles.
Exp. 2,
well-watered
plants experienced
stressed 6 to 9 and severely stressed plants 5 to 7
harvest. As
for
the
expected,
the chosen
well-watered,
Y^,
moderately
9 to 12, moderately
drying cycles until plant
values of -0.05, -0.60 and -1.80 MPa
and
severely stressed treatments,
exactly. The Y^, ranges measured at
the peak of the drying cycles in both experiments are given in Table 1.
respectively, could
not be maintained
Table 1.
of soil matric
Range
potentials (Y^,) in replicates of a treatment at
(control), moderate and severe
stress in experiments 1 and 2 a.
maximum stress under well-watered
conditions of water
Treatment
Range
of soil matric
Experiment
potentials (MPa)
Experiment
1
2
Control
-0.02 to -0.05
-0.03 to -0.06
Moderate
-0.42 to -1.56
-0.63 to -421
Severe
-1.21 to -2.44
|
Y^i was calculated from the average reading
placed at 14 cm soil depth.
-1.56 to -8.22
of the two gypsum blocks
28
0.00
~<X*oCr
-0.01
-0.02
-0.03
-0.04
well-watered
Pot 19
i
-0.05
-10
20
10
0
0.5
\
1.0
40
30
Vw
\i
V
\i
1.5
'
moderately stressed
0
i
i
i
i
0
10
20
30
i
i
20
30
Pot 17
40
0
'
-1
Vh
-2
-3
-4
-severely
10
0
Pot 18
stressed
10
0
-1
*J
\
Qr ¥^*
-2
40
"^r
-3
-4
-severely stressed
-10
i
0
10
20
Time
o
v
•
o
1.
Soil matric
Pot 23
i
i
40
30
(days)
gypsum blocks at 7 cm soil depth
gypsum blocks at 14 cm soil depth
tensiometer at 10
potentials (Y^,)
in
cm
soil
depth
representative, single pots of well-
watered, moderately and severely water stressed treatments during
experiment
1.
29
0.00
0vnry<*
0.01
o.
0.02
o
*
-
0.03
0.04
well-watered
Pot 19
i
i
L
0
10
20
o
a
0
30
40
50
60
0
-1
o
o.
-2
i
-3
-4
i
Pot
stressed
severely
.
i
i
13
4
i
o
2
1
j
-10
severely
i
i
10
20
30
Time
o
v
•
o
Soil matric
Pot 24
stressed
i
i_
40
j
50
(days)
gypsum blocks at 7
cm
soil
potentials (Y^)
2.
depth
gypsum blocks at 1 4 cm soil depth
tensiometer at 10 cm soil depth
in
representative, single pots
watered, moderately and severely water stressed
experiment
i_
60
of well-
treatments
during
30
The
variability
in
Ysoi,
peak of drying cycles
at the
high within and
rather
was
between the different treatments.
treatment did not develop
Additionally, the drying cycles within a
synchronically; therefore, it was not always possible
consider pooled data for comparisons of certain parameters (e.g.
components of leaf water potentials) at a specific sampling date. The two last
to
plots in Figs. 1 and
in
procedure:
other had just
when
In
2 visualize this
problem
of data
pooling. The differences
timing between the drying cycles in each comparison
taken
Exp. 1, soil
compared with
within
a
drying
place
in
and
was
measured at 14 cm. In
smaller. A
higher
beginning of the experiment, and
container resulted in
root to shoot
of the
a more
Exp.
were
2, the
lower
gradient
ratio, particularly at the
uniform root distribution
uniform moisture distribution in
a more
due to
was
peak, watering
its
had been initiated.
a new
potentials
water
was at
drying cycle
potentials measured at 7 cm soil depth
water
container
container
one
a
over
the
container.
In Exp. 1, the first drying cycle was initiated at day 0 of the experiment. The
peak of the first drying cycle was reached ca 15 days after the experiment
had started. At the
beginning plants
were
rather small and had
enough soil
volume to buffer water loss and to postpone the onset of stress. In
the first
drying cycle
reached its
In
Fig. 3,
study
is
a
was
initiated before the
peak between day
5 and
soil water retention
presented. Soil
day
curve
experiment had
10 of the
Exp. 2,
started and
experiment.
specific for the soil
water retention was determined
mix used in this
using a pressure
by measuring soil
plate apparatus (for pressures down to -1.0 MPa) and
potentials in Exp. 2 at harvest.
water content and soil matric
The soil mix used
(25 g
was
characterized
by
an
average water
water per 100 g soil at field
portion
of coarse soil pores,
capacity). There
probably due to the sand
soil also contained considerable amounts of
made up
quite
a
large
holding capacity
was a
relatively large
mixed in. Because the
clay, plant unavailable
amount of the soil water fraction
(ca 8.5%,
see
water
Fig. 3).
31
o
a.
2
c
o
a.
a
"5
en
0 05
0 10
0.15
0 20
Grovimetric Soil Water Content
°
I—I
Fig.
3.
Plant
curve
curve
Soil water retention
(mean
Exp.
(mean
on
Plant
Development
experiments
=
42.2
cm)
and 21
1 and between 35.5
=
36.0
leaves)
in
over
the
experimental
is shown.
length and number
Initial shoot
in
of the soil mix used in all experiments of
growth. In Table 2, the weighted plant growth
period
cm
curve
study.
Effects of Water Stress
of both
(g g~1)
(pressure plate)
(gypsum blocks)
Measurement points (gypsum blocks)
SD of measurement points (pressure plate)
Soil water retention
Soil water retention
the present
2.3.2
0 25
-
-
of leaves
(at day -6) ranged between 20
38 leaves
(mean
87.5
Exp. 2.
cm
(mean
In both
=
=
28.3
71
leaves), respectively
67.0 cm) and 27
experiments,
-
mean
-
42 leaves
initial plant size
among the three treatments
was similar. Final growth was measured at day
Exp. 1 and day 50 for Exp. 2.
In Exp. 1, plant growth was significantly reduced with increasing intensities of
water stress. During Exp 2, shoot length and extension rate per day were
40 for
significantly
reduced with
increasing
rate of leaf appearance per
moderately
and
severely
day
water stress, whereas leaf number and
decreased
stressed treatment.
significantly only between the
32
length and total leaf number at harvest as well as the
length, increase in number of leaves, extension rate
per day and rate of leaf appearance per day averaged over the
experimental period, of well-watered (control), moderately and
severely water stressed apple plants in Exp. 1 and Exp. 2 (Exp.1,
measured at day 40; Exp. 2, measured at day 50). Means ±SE (in
Table 2.
Total shoot
increase in shoot
parenthesis)
are
shown
a'b;
l.=
length,
app.= appearance.
total
increase
increase
extension
leafapp.
leaf
shoot I.
in leaf
rate
rate
[
number
(cm)
number
(cm/d)
(leaves/d)
\
(cm)
1
Experiment
Control
Moderate
Severe
1
total
shoot 1.
Treatment
0.73
120.3 a
63.5 a
74.9
a
34.5 a
1.59 a
(±2.2)
(±1.2)
(±2.1)
(±0.5)
(±0.03)
101.4 b
57.5 b
61.8 b
30.8 b
1.32 b
0.65 b
(±2.6)
(± 1.3)
(±1.9)
(±0.5)
(± 0.04)
(± 0.01)
a
(±0.01)
86.1 C
52.0
c
44.3 c
24.4 c
0.94 c
0.52 c
(±2.0)
(± 1.0)
(±2.3)
(±0.8)
(±0.05)
(±0.02)
—
Experiment
Control
Moderate
Severe
125.0 x
70.3
(±2.8)
(±1.3)
68.0
x
56.9 y
31.4
(±2.2)
(±1.4)
(±2.4)
(±1.5)
1.26 y
x
(± 0.05)
0.77
x
(± 0.03)
0.70
X
(± 0.03)
61.9 y
49.4
z
26.5 y
1.10Z
0.59 y
(±2.4)
(±1.7)
(±2.0)
(± 0.04)
(± 0.05)
of 16
in
a
replicates (aphid infested
and uninfested
plants showed
no
growth).
column followed
by
the same letter
are
not
significantly different
0.05).
Mean rate of extension per
moderately stressed plants
Exp.
x
(±0.07)
1 (±3.4)
means
with
1.43
x
(±1.4)
1 108.9 y
mean
s
34.8
x
(± 2.9)
115.8 y
difference in
(P
64.3
x
2
day
and
was
lower in
1. Mean rate of leaf appearance per
1
compared
a
longer time
with
Exp.
2. Plants of
compared
Exp.
with those in
about 25 cm; A time about 10
Exp.
2 for well-watered and
higher for severely stressed plants compared
2
Exp.
day
1
was
slightly lower in Exp.
day 0 and grew for
(difference A in shoot length was
were
larger
at
days). Thus, plants in Exp.
2 suffered
more
Exp. 1,
plants
compared
particularly the fast growing well-watered and moderately stressed plants.
from limited soil volume and space
with the
in
33
Internodal
with
length.
In
Exp. 1, the internodal length decreased significantly
increasing intensity of water stress (control: 2.17 cm; moderate: 2.01 cm;
1.80 cm; P
severe:
<
0.05). Hence, leaf production
stress to the same extent as shoot
did not
a
change significantly with
trend towards
elongation.
water stress,
In
was not
Exp. 2, the internodal length
although
longer internodes (2.31 cm)
affected by water
in
there
severely
appeared
stressed
to be
plants
compared with well-watered and moderately stressed plants (1.85 cm). Here,
also, leaf production
was
Individual leaf area. In
watered plants was
stressed plants
(P
impaired by
Exp. 2,
the area of
water stress.
fully expanded leaves
significantly larger compared
0.05). The difference in single
with those of
£
watered and severely stressed plants
reduction in leaf
severe
area
growing leaves which
was
leaf
cm2.
about 10
due to water stress was not
area
of well-
severely water
between well-
The extent of the
yet apparent in immature
had not reached their maximum size.
Visual differences. Clear visual differences among
different water regimes
were
observed
particularly
intense the water stress became, the smaller
plants
in
plants grown under
Exp. 1. The more
and leaves
were.
The
shape of the plant differed under the three water regimes: well-watered plants
shape of a triangle pointing downwards, moderately stressed plants
rectangle and severely stressed plants that of a triangle pointing
took the
that of
a
Leaf color became
upwards.
lighter and leaf toughness as well as hairiness
increasing intensities of water stress. Throughout the
experiments, wilting was not observed in any treatment.
increased
with
Leaf surface temperature. Leaf surface temperatures at maximum light and
temperature intensities in the growth chamber did not differ significantly
among treatments. The
problem
of
example
pooling data
of leaf surface
temperatures illustrated the
of treatments measured at the same time
(while
development
variable).
Exp. 2,
however, significant differences in leaf surface temperature between the tenth
water stress
among containers was
In
uppermost leaf on measuring day and leaf A (tenth leaf from the apex on day
0) of the plant were apparent (P £ 0.05). Figure 4 shows mean leaf surface
temperatures measured
at several dates
during Exp. 1 and Exp. 2. In Exp. 2,
surface temperatures of the tenth uppermost leaf
of leaf A
(tenth leaf
from the apex at
day 0)
are
on
measuring day and
plotted separately.
that
34
Experiment
1
5
27
Time
Control
Severe
Moderate
Experiment
30
40
(days)
2
TSE
28
26
24
22
J
20
5
10
15
l_
20
Time
v
—
—
Control
o
J
30
25
35
L.
40
(days)
Moderate
10th leaf from the apex at
10th leaf from the apex
on
o
Severe
day 0
measuring day
Leaf surface temperatures measured in apple plants grown under
different water regimes and at maximum intensities of light and
temperature
1:8
same
letter
during Exp. 1 and Exp. 2. Means (Exp.
Exp. 2:16 replicates) ol one date labelled by the
not significantly different (P £ 0.05).
at several dates
replicates
and
are
35
At the
Exp.
beginning of the experiment, leaf surface temperatures, particularly
1, did not differ among treatments.
and plants
a
temperature could be observed which
in leaf surface
plants growing towards the
in leaf surface temperature
whereas in the lower
was
in
just started
yet suffering from water stress. Later in the experiments,
were not
general increase
due to the
Withholding
water had
parts
of
was
light. In Exp. 2, this increase
restricted to the upper parts of the plant,
was
a
source
general decrease
in leaf surface
temperatures
explained by the shading of the lower
observed. This decrease can be
parts of the plant by the increasing number of leaves in the upper parts. The
differences in leaf surface temperatures between the tenth uppermost leaf
measuring day and leaf
A
(tenth
leaf from the apex at
on
day 0) reached 5°C.
Exp. 1 and that of leaf A in Exp. 2, tended to
increasing intensities of water stress. In Exp. 2, surface
Leaf surface temperature in
increase with
temperatures of leaves positioned in the upper parts of the plant
affected, in addition
to the water stress,
of
by
light (effect also observed by Schnider, 1989).
leaves from the
source
Plant biomass
production. Table
3 shows fresh and
water contents of shoots of individual
shoots in both
dry weight
as
well
as
plants.
weight
plant
experiments decreased with an increase in the intnesity of
Fresh and dry
water stress. This decrease was
significant between
both water stressed treatments in
Exp.
the
were
the distance of the measured
severely stressed
treatment in
Exp.
of
the well-watered and
1 and between the well-watered and
2.
dry weight as well as water content of shoots of well(control), moderately and severely water stressed apple
plants in Exps. 1 and 2. Means ±SE (in parenthesis) are shown *".
Fresh and
Table 3.
watered
Fresh
Treatment
Control
70.80
Dry weight (g)
Exp. 1
Exp. 2
weight (g)
Exp. 1
a
Exp.
99.84
2
25.56
x
(±6.68) (±4.93)
46.78 b
Moderate
Severe
90.82 xy
Exp.
1:8
(P
4
x
64.06
1
a
61.80
x
(±2.61) (±2.32)
(±0.48) (±0.54)
17.62 b
62.50 b
37.57 xy
58.75 y
(±1.98) (±2.07)
(±0.32) (±0.46)
33.37 b
13.23 b
60.42
76.34 y
replicates; Exp.
0.05).
38.45
Exp.
(±4.88) (±4.64)
31.45y
(±1.25) (±2.47)
(±2.95) (±5.70)
means in a
a
(%)
Exp. 2
Water content
58.71 y
replicates (except moderate: 14 replicates)
by the same letter are not significantly different
2:16
column followed
c
(±0.61) (±0.96)
36
The reduction in fresh
water stressed
plants
mentioned above
growing
Exp.
2
was
page
peak of the
higher
between well-watered and both
Exp.
in
1
compared with Exp.
2. As
water stress additional stresses
31), beside
plant growth
plants
water stress
dry weight
Exp. 2, particularly that of the
plants. Another difference between Exp. 1 and
overall
that the
as
much
well-watered
(irrespective of
at the
well
was
(see
eventually impaired
faster
as
in
in Exp. 1 were harvested on the same day
level), whereas plants in Exp. 2 were harvested
current
drying cycle: well-watered plants first, then
moderately stressed, then severely stressed plants.
Exp. 1, plant water content decreased significantly with an increase in
stress intensity. In Exp. 2, the decrease in water content was only significant
In
between well-watered and stressed
water content of
plants
in
Exp.
plants, irrespective of stress intensity. The
1
was
the
Exp.
2. As
presented in Fig. 5, leaves and
were
affected
assumption that
differently by
an
Exp. 2,
plants in
single plants in Exp. 2
generally higher
than in
additional stress had acted
supporting
stems of
on
water stress.
Fig.
5.
Fresh and
dry weight
well as water content
FW
CONTROL
Fresh
MODERATE
weight
SEVERE
H Dry weight
K88 Woter content
as
(on
basis) of leaves and
single apple plants
stem of
grown under well-watered
(control), moderately and
severely
water
conditions in
stressed
Exp. 2.
Means (16 replicates, ex¬
cept moderate: 14 repli¬
cates) between treatments
labelled by the same letter
are not significantly diffe¬
rent (P < 0.05).
CONTROL
Fresh
MODERATE
weight
gggg
SEVERE
^M Dr> weight
Water content
37
In
Exp. 2, fresh and dry weight
of stems
gradually
decreased with
increasing
intensities of water stress. The decrease between well-watered and severely
stressed plants
significant. Fresh and dry weight of leaves decreased
significantly only between moderately and severely stressed plants. The water
was
content of stems decreased
stressed
significantly between well-watered and water
significant difference among treatments was
No
treatments.
observed in water contents of leaves.
In
Exp. 2,
leaf loss due to
senescence (bottom leaves) at harvest
significantly different and reached 27.1, 23.6 and
22.7% of the total leaf number for well-watered, moderately and severely
mean
among treatments
water stressed
was
not
plants, respectively.
Plant water relations. As demonstrated in
in
soil.
Examples shown
are
of
potentials
was
to a lesser extent
when the stress
fluctuated
In
Y0
was
a
the
course
in
plant
of water stress
of
Exp.
predawn Y,
1
over
development
the
in the
representative single plants.
A consistent trend between the
matric
Fig. 6,
leaves of
apple
Yp development
Y0
experimental period reflected the course
and
components of plant
observed. In severely stressed
water
potential and soil
plants, predawn
Y and
decreased with
decreasing Y^ and increased again
relieved by watering (increase in Y^). Hence, Yp
experiment (e.g. between 0.50 and 1.50 MPa; Fig. 6).
during
Y
Exp. 1,
ranged between -0.40 and -1.40 MPa in well-watered plants,
the
between -0.40 and -1.78 MPa in
-2.85 MPa in
moderately stressed and between -0.50 and
severely stressed plants. The osmotic potential in leaves (YJ
-1.33 and 2.10 MPa in well-watered plants, between -1.55
ranged between
and -2.22 MPa in
-
moderately stressed and
between -1.71 and -3.20 MPa in
severely stressed plants. Turgor (Yp) in the leaves of well-watered plants
ranged between 0.38 and 1.40 MPa, in moderately stressed plants between
severely stressed plants between 0.21 and 1.85
Exp. 2, Yp ranged between 0.53 and 2.35 MPa in well-watered
plants, between 0.00 and 1.73 MPa in moderately stressed plants and
0.33 and 1.50 MPa and in
MPa. In
between 0.00 and 2.00 MPa in
The effect of water stress
severely stressed plants (see
also Table
4).
(position within the plant)
is briefly discussed. Leaves at different stages of development in well-watered
and
not
on
leaves of different age
moderately stressed plants were similarly
shown). Apical
leaves
affected
(5 youngest leaves) tended
by
water stress
(data
to maintain the lowest
Yp (particularly in moderately stressed plants) within a plant.
in leaf age, Yp increased until leaves were fully expanded.
With
an
increase
38
C
Fig.
0-
6.
(Y), osmotic
potential (Yp) in
Predawn leaf water
(Y„)
g
relation
g
15
0.01
r=
c
O
V
20
30
25
r\n
-
l
0.02
E .0
35
0.04
\
V
Ji
«
•5
E
1
Pot 19
1
1
1
1
1
r
15
20
25
30
35
40
0
0-0
-oO-
-3
15
0
-1
E .2
20
25
moderately stressed
20
^
0.
o
w
30
25
Time
c
35
40
L/VW^
15
0
30
-2
-3
Pot 17
35
40
30
35
40
30
35
40
(days)
/^V
t—
S
•
*
2.
S
§
_i
o
i
15
20
15
20
i_
25
_
E .9
=
c
O
V
of
potential
one
25
Time
(days)
well-
one
cate
periods
Dotted lines indi¬
with
no
measure¬
ments.
a
leaf water
o
osmotic
O
turgor pressure
potential
potential
soil matric
-1
-2
matric
(days)
-*•—
«-c
soil
moderately and one
severely stressed apple plant in
Exp. 1. Points indicate one leaf
watered,
2
3
to
(Y^) development
measurement.
1
well-watered
-
40
rAT
0.03
Time
iJ
and turgor
potential
39
Thereafter, Yp remained almost constant until leaves started senescence,
which point leaf Yp decreased again. Leaf water potentials (Y) tended
respond similarly
as
Yp.
Osmotic
apex. Similar trends
al.
reported a "gradation"
(1989).
These authors
mature leaves;
mature and
In Table 4,
apex
>
Y0
in Y,
Y0
and
Yp
that reflects
1-year old branches of peach (Y
mature and
apex
growing leaves; Yp apex
<
<
Y, Y0 and Yp and their corresponding Y^y at the peak
Exp. 1. (assessed predawn during the experiment) and
(assessed predawn at harvest) are shown.
mean
Table 4.
in
of
in
Predawn leaf water
(Y), osmotic (YJ and turgor potentials (YP) of
as their corresponding soil matric potentials
(Y^i) measured at the peak of drying cycles under well-watered
(control), moderately and severely water stressed conditions in Exp.
1 (during the experiment) and in Exp. 2 (at harvest); n indicates
number of observations. Means ±SE (in parenthesis) are shown a.
apple plants
Treatment
<F
n
as
well
(MPa)
Y0(MPa)
Yp (MPa)
Experiment
I
Control
1
Moderate
46
26
Severe
Control
114
1
Moderate
1
Severe
78
I
means
£
in
a
0.05).
1
-1.70
(± 0.02)
(± 0.04)
(± 0.00)
-0.88 b
0.98
a
a
-0.01
a
b
-1.96 b
0.93
(± 0.05)
(±0.03)
(± 0.05)
(±0.04)
-1.69 c
-2.50
0.81
-2.19
(±0.10)
(± 0.06)
-0.66
c
x
-1.82
(± 0.03)
-1.20 y
(±0.05)
1
-1.74
1
ab
b
(± 0.08)
c
(± 0.15)
2
1.17
x
(± 0.01)
77
Y^fMPa)
(± 0.04)
-1.03
25
|
-0.72 a
Experiment
(P
Y
Yp
growing leaves).
drying cycles
Exp. 2
Y0
to
potentials, however, were highest (least
were reported by Steinberg et
negative) in leaves of the
the maturity of the leaves along
at
x
-0.01
x
(± 0.03)
(±0.001)
-2.17 y
0.97 y
-0.98 y
(± 0.03)
(± 0.06)
(±0.07)
z
-2.13 y
0.39
-1.84
(± °-07)
(± 0.04)
(± 0.06)
column followed by the same letter
are
not
z
z
(±0.17)
significantly different
40
experiments, Ysoil was distinctly different at the peak of drying cycles
three treatments (well-watered, moderate and severe water stress). In
In both
in the
Exp. 1, Y, Y0 and to a lesser extent Yp decreased significantly with
increasing intensities of water stress. In Exp. 2, Y and Yp decreased
significantly with increasing water stress, whereas Y0 significantly decreased
between the well-watered and both water stressed treatments.
severely
Leaf turgor pressures in the
much lower than in
The data
Exp.
presented
water stressed
plants of Exp.
2 were
1.
in Table 4 show
a
relationship
supply in
between water
readings
plant. Thus, when all
Y0 and
Yp in Exp. 1 as well as in Exp. 2 were plotted against corresponding Y^,
regression lines could be fitted for each component of plant water potential
and Revalues calculated (Fig. 7).
the soil and water relations in the
In both
experiments, Y, Y0
decrease in
2: r=0.83;
was
Ysoi|.
see
and
YP decreased
Y^, (Exp.
The extent of decrease in Y due to
Fig. 7).
similar to that
expressed by
degrees with
to various
Predawn Y correlated best with
a
of Y,
1:
decrease in
slope of the regression lines (b
the
a
n*0.75; Exp.
Y^
ot the
equation). In Exp. 1, Ys decreased with an increase in the intensity of water
stress, whereas in Exp. 2 almost no change in Y0 was observed. This
indicated that osmotic
adjustment had occurred in Exp.
addition, the correlation between
compared with Exp.
in
Exp.
increasing
Exp.
1 to
Ysoil
(r=0.34), again indicating
2
but not in
1
Y0
and
Exp.
2.
was
certain
In conclusion,
Yp
degree with
an
in leaves tended to decrease with
on
i.e. to accumulate solutes.
Relating Y0
and
In
Yp
Exp.
osmotic
(r=0.75)
adjustment
dropped
2
2. In
with
could be maintained in
an
increase in soil water
the capability of the
plant to adjust
Yp with their corresponding Y also indicated
plants grown under different water regimes
the extent to
could adjust
Yp were plotted against Y, regression lines
and Revalues calculated.
Fig. 8, Y0
each treatment fitted
Exp.
1
increase in water stress.
osmotically,
osmotically.
in
Consequently, Yp in Exp.
stress, the extent of which depended
which leaves of
higher
a trend to
intensities of water stress, whereas,
a
1 but not in
and
for
41
Experiment
o
1
y=-1.79+0.29x
-3
-4
R =0.57
-2
Soil Matric Potential
Experiment
CO
»
-w
P<0.001
-1
0
(MPa)
2
y=1.16+0.33x
R =0.53
P<0.001
c
CD
c
o
a-
^
o
E^
o
O
—
D
s
w
CO
CD
a
y=5.0.76+0.43x R2=0.68
P<0.001
-*-»
*
I
o
-4
o
y-1.92-t-0.10x
-3
R=0.11
-2
Osmotic Potential
Turgor
1
Fig.
7.
P<0.001
-1
Soil Matric Potential
0
-_..
•
2
D
_
l*i-^i*"^^
a
0
(MPa)
Leaf Water Potentfal
Pressure
SD of values with soil matric
potential
>
-0.1
MPa
Predawn leaf water (Y), osmotic (Y0) and turgor potentials (YP) of
apple plants in relation to soil matric potentials (Y^) in Exp. 1 and
Exp. 2. Regression equations, R2- and P-values are shown.
42
90
85
-1. y=75.52-3.49x
R2=0.11
"..".. y=73.46-1.66x
R =0.03
P<0.05
ns
-as!
80
?
'
1"
„"»
75
0_
^_
70
65
°
°
I
R =0.03
i
-2.5
-3.0
-2.0
-1.5
R2=0.68
R2=0.83
_°_ y=1.69+0.55x
1.0
..".. y=1.72+0.80x
0
1
1
-0.5
0
°0o
P<0.001
^.4
"
-2.5
o
°
°D
XOrno
v
8^
y
»
i
P<0.001
i
i
-1.0
-1.5
-2.0
v
R2=0.73
y=1.7Q+1.00x
V
7~
1
-3.0
".'''
0
.-
0.0
0.0
q^
oo
jf
*'
0*
P<0.001
o
-
0
*
-1.0
0
0.5
o
°
8
ns
1
2.0
1.5
D
°°
a
y= 74.03+1.07x
o
„°
S
„
o
8
.'
60
"a
°
°
0
-0.5
0.0
-1.0
R =0.00
_!_ y=-1.70+0.004x
ns
V
V
-1.5 -.."..
y=-1.72+0.20x
R2=0.23
P<0.001
-2.0
"
0
-2.5
-3.0
.
-°--8-<r
°J5«
$9*
o
°
o
0
-
o''
°
-
-3.0
y- 1.69+0.45X
,
t
-2.5
-2.0
-3.5
Leaf water
_o_
8
Severe
Comparison
_°_
R2=0.58
P<0.001
i
I
I
-1.5
-1.0
-0.5
0.0
potential (MPa)
Moderate
of
_»_
Control
predawn leaf osmotic (Y0) and turgor (Yp) potentials
predawn leaf water potentials (Y) of
well-watered (control), moderately and severely stressed apple plants
in Exp. 1. Regression equations for each treatment and the corre¬
sponding R2- and P-values are shown.
as
well as leaf water content with
43
In
Exp. 1, Y0 of moderately and particularly of severely
decreased with
a
decrease in Y, whereas
Y0
plants
plants did not
stressed
of well-watered
change with decreasing Y. Since leaf water contents did not decrease
significantly with decreasing Y, the decrease in Y0 in moderately and
severely stressed plants could primarily be attributed
to active osmotic
Exp. 2, Y0 of well-watered and severely
stressed plants also decreased with an increase in Y (data not shown). The
adjustment
to water stress. In
relationship between the two components was, however, not very close (low
R2- and high P-values). Leaf turgor pressure of well-watered and water
stressed plants in both experiments decreased to various degrees with
decrease in Y. The relationship between
was
indicated by high
between Y and
Yp,
R2- values;
since
Yp
was
Yp
this was
calculated
and Y was
certainly
as
Y0
+
relatively close
due to a
a
as
collinearity
Y.
regression lines indicated a disparate ability of
plants grown under different water regimes to adjust osmotically: whereas
moderately and particularly severely stressed plants of Exp. 1 showed distinct
The comparison between the
adjustment, well-watered plants could not adjust Y0 when Y
-1.0 MPa, Y0 in severely water stressed plants was lower
than in moderately water stressed plants (difference A in Y0
0.21 MPa), and
Y0 in moderately water stressed plants was lower than in well-watered plants
(A in Y0 0.25 MPa). With respect to Yp the opposite was true: at Y= -1.0
osmotic
decreased. At Y
=
=
=
MPa, YP in severely stressed plants
was
higher compared
with
moderately
YP 0.20 MPa), which in turn was higher than in well0.24 MPa; see Fig. 8).
watered plants (A in Yp
In Exp. 2, Y0 and Yp at a given Y did not differ significantly in plants grown
stressed plants (A in
=
=
under the three water
regimes. This indicated that plants under conditions of
water stress did not show any
significant osmotic adjustment.
44
Effects of Water Stress on
2.3.3
Life Table and
Population
Parameters of
Aphids
Mortality
was
of immatures. In aphid cohorts of Exp. 1, mortality of immatures
3.7, 8 and 8% in the well-watered, moderately and severely water
stressed treatments,
16.1 and 10%
on
In Exp. 2 on the other hand, it was 19.6,
parts and 17,25 and 6.5% on the lower parts of
respectively.
the upper
plants grown under well-watered, moderately and severely
conditions, respectively.
The upper
parts
of the
water stressed
plant consisted of the apex
and the upper 15 leaves counted from the apex and the lower
comprised
the rest of the
25% in both
experiments.
Figures 9 and
cohorts
parts
plant. Accidental aphid losses ranged between 20-
10 show the
feeding
on
and cumulative
survivorship
apple plants
grown in different water
fecundity
o
60
80
«fifiOOOOOpOfloOOOO a
{%
Survial
o
c
3
c_
i
50
i
40
i
30
(?
i
20
c
3
a.
o
a
<
a
o
20
_
0
pomi
70
100
^
of A.
regimes.
»eeaeae»<ff
10
'
'
i
i
i
i
15
20
25
30
35
40
10
45
Age (days)
a
Fig.
9.
control
D
moderate
o
severe
Survival rates and mean cumulative fecundity in cohorts of K pomi
feeding on apple plants grown under well-watered (control),
moderately and severely water stressed conditions in experiment 1.
Development
Exp. 1, the development time of
aphids (from
adulthood) in the three water supply
treatments was not significantly different and lasted on an average 8.6 days
immature
time of Immatures. in
birth
to
45
60
c
3
50
40
rvae ulati
\
a>
20
ma ecu
a
10
20
30
CD
M)
*^
-i
Q.
40
Age (days)
a
Fig.
control
moderate
°
o
mean cumulative fecundity in cohorts of A. pomi
feeding on upper (apex and upper 15 leaves counted from the apex)
and lower parts (rest of the plant) of apple plants grown under well-
watered
in
as can
severe
Survival rates and
10.
be
(control), moderately and severely
experiment 2.
seen
in Table 5. In
Exp. 2, the time of development of immature
the lower parts of the plant
aphids feeding on
in Exp. 1 but about
Fig. 10).
However in Exp. 1,
instars within
significantly
a
one
a
day longer than
difference in the
on
shorter than for the
21.5 % of the total
(Table 5).
was
about the
the upper parts
development
treatment was observed. The
which were similar
water stressed conditions
previous
same
length
as
(estimated from
time between the larval
development
time for L4
was
three larval instars, the durations of
The fourth larval instar
premature development
comprised
time in all treatments.
a mean
of
46
(L1, L2, L3, L4) and total immature time of
development of A^ pomi reared on apple plants growing under wellwatered, moderately and severely water stressed conditions in Exp.
1. Ranges, means and ± SE (in parenthesis) are given a.
Observed larval instar
Table 5.
tim«> of
larval
instar
mean
range
L1
development (days)
moderately stressed
well -watered
1-3
2.17
a
a
1-4
2.30
a
2.35 ab
1-3
2.09 ab
1-3
1.91
C
1-3
1.78
7-11
8.65
x
7-10
2.31
a
1-3
L2
1-4
2.35 a
1-4
2.39
L3
2-4
2.31
a
2-4
L4
1-3
1.81
b
7-10
8.77
x
£
in
s
column followed
was
in this row followed
(see Fig. 9).
Exp.
different
the same letter are not
significantly
different
letter
same
are
by
Exp. 1, the mortality of adults until reproduction had
In
Exp. 2, adult mortality
In
on
water stressed
1 and
on
plants grown
moderately and severely stressed conditions, respectively
and 10, 12 and 0 %
In
significantly
the
23, 30.4 and 13 % for aphid cohorts feeding
under well-watered,
severely
not
by
0.05).
Mortality of adults.
ended,
8.35 x
0.05).
means
(P
a
b
(± 0.35)
(± 0.23)
(± 0.20)
(P
mean
be
2.00
1-3
means
range
mean
range
L1
-L4b
severely stressed
the lower
was
parts
22, 4 and 8 %
on
of well-watered,
the upper parts
moderately
and
plants, respectively (see Fig. 10).
particularly
on
the lower
parts of plants in Exp. 2, age-specific
survivorship (lx) of aphid cohorts feeding on moderately water stressed
plants decreased faster compared with the other two water supply treatments
(Figs.
were
age
9 and
10). On the lower parts
dead between
(Fig. 10).
were
day
53
of
(severe stress)
On the upper parts of
dead between
day
42
plants in Exp. 2, all adults of a cohort
and 55
plants
in
(moderate stress)
(moderate stress) of aphid
Exp. 2, all adults of a cohort
day 55 (severe stress; see
and
Fig. 10).
In Exp. 1, pre-reproductive time of aphids
offspring) decreased significantly between well-
Development time of aphids.
(time from birth
to birth of first
47
watered and severely water stressed plants (Table 6). About
virginoparae
on
one
third of the
well-watered and
moderately stressed plants and nearly 90%
severely stressed plants began to reproduce on the first day after molting.
on
The bulk of the offspring
was
bom
during the first 20 days of aphid lifespan
(see Figs. 9 and 11).
On the upper parts of
leaves),
was
no
plants in Exp. 2 (i.e. apex and the uppermost 15
significant difference in pre-reproductive time among treatments
found and pre-reproductive time
parts (i.e.
the rest of the
pre-reproductive
was
in
general shorter than
on
the lower
plant). On the lower parts of the plants, however, the
time of
aphids decreased significantly between the well-
watered and water stressed treatments.
Table 6.
Pre-reproductive
and
reproductive time (days) of & pomi feeding on
moderately and severely water stressed apple
plants in Exp. 1 as well as on the upper (apex and upper 15 leaves
counted from the apex) and lower parts (rest of the plant) of plants in
Exp. 2; n indicates cohort size. Ranges and means ± SE (in
parenthesis) are shown a.
well-watered (control),
Experiment
Treatment
pre-ref>roductive time
Control
26
Moderate
Severe
I
(d)
mean
range
8-11
9.15
23
7-11
23
7-11
rep reductive time (d)
mean
range
(±0.23)
6-27
19.16 ab
(±1.23)
9.04 ab
(±0.24)
4-26
15.59
a
(± 1.31)
8.48 b
(±0.20)
2-31
20.13 b
(±1.74)
a
Experiment
2 upper
parts of the plant
Control
37
6-11
8.14
a
(±0.21)
4-27
15.16
a
(±0.73)
Moderate
26
6-11
8.19 a
(±0.27)
11-27
17.31
a
(± 0.74)
Severe
36
6-11
8.03
(±0.21)
5-42
17.31
a
(±1.11)
a
Experiment
a
1
n
Control
40
7-11
9.38
Moderate
33
6-13
Severe
43
6-10
means
(P
£
parts of the plant
(±0.18)
8-33
21.03
x
(± 0.89)
8.85 y
(±0.24)
2-37
18.85
x
(±1.25)
8.67 y
(±0.14)
11-42
24.81
y
(±1.16)
in a column followed
0.05).
2 lower
by
x
the same letter
are
not
|
significantly different
48
In
Exp.
1 and
on
(time between
parts of plants in Exp. 2,
the lower
first born and last born
severely stressed plants compared
the upper parts, however,
no
larvae)
mean
was
reproductive
time
significantly longest
on
with that in the other two treatments. On
difference in the
among treatments was observed. In both
reproductive time of aphids
experiments, the actual reproductive
some individual aphids in a cohort was longest on severely stressed
plants. The reproductive time of aphids feeding on the lower parts of the plant
time of
was
significantly longer (P
Age-specific fecundity.
fecundity (mx)
<
0.05) compared with the upper parts.
As is shown in
fluctuated in both
Figs.
11 and 12, mean
age-specific
experiments.
Age (days)
Fig.
Age-specific fecundity of A^ pomi feeding on well-watered (control),
moderately and severely water stressed apple plants in Exp. 1.
11.
Means of
In
a
cohort
are
Exp. 1, age-specific fecundity
between
was
day
plants (Fig. 12).
uppermost
in cohorts of all three treatments
12 and 20 after birth
highest between day
Mean
15 leaves
two larvae per
11 and
(Fig. 11).
In
was highest
Exp. 2, age-specific fecundity
day 15 in both upper and lower parts of the
age-specific fecundity
compared
female).
shown.
in a cohort was
with lower parts in
a
plant (by
higher
an
on
the
average of
49
upper
part
of the
plants
*
control
o
severe
moderate
20
30
40
Age (days)
Fig.
12.
Age-specific fecundity
A^. pomi feeding on upper (apex and upper
apex) and lower parts (rest of the plant)
of well-watered (control), moderately and severely water stressed
apple plants in Exp. 2. Means of a cohort are shown.
of
15 leaves counted from the
In
Exp. 1 and in Exp. 2, maximum fecundity per day in
virginopara
was not
significantly
affected
However, this maximum fecundity within
(P
<,
0.05)
in the lower parts
compared
by
a
water stress
treatment
was
a
lifespan of
a
(data
not shown).
significantly lower
with that in the upper parts of the
plants.
Total fecundity. Figure 9 (see page 43) shows that the differences in
cumulative
fecundity between aphids feeding
on
well-watered and
on
mean
water
50
plants in Exp.
stressed
On the upper parts of
on
water stressed
1 were not
plants
in
plants (ca
significant (48.5 to 53.5 larvae per female).
Exp. 2,
fecundity was higher
female) than on well-watered
cumulative
mean
50 larvae per
plants (38.5 larvae per female; see Fig. 10, page 44). This difference in
fecundity was significant between the well-watered and the moderately
stressed treatments. On the lower parts, mean cumulative
highest
stressed
was
severely (35.7
plants (23.5 larvae
on
significantly higher
per
fecundity
was
female)
moderately
female). The cumulative fecundity of aphids
on
the upper parts of the plants (i.e. apex and the
apex) compared with the lower parts (i.e. the rest
on
upper 15 leaves from the
of the
and lowest
larvae per
plant; PS 0.05).
Total fecundities observed in this
reported by Graf (1984;
study
larvae/female at 20/16°C fluctuating
in
were
75 larvae/female at
general lower than those
20°C)
(1990;
and Rutz et al.
75
day/night temperatures).
Population parameters (summary statistics). In both experiments, the
experimentally determined life table parameters (x, mx and lx) were tabulated
to calculate net reproduction rate R0, intrinsic rate of natural increase rm,
mean generation time G and doubling time DT. These results are
presented
were
In
in Table 7 for
Exp.
1 and
Exp.
2. In
Exp. 2, summary
statistics
calculated separately for the upper and the lower parts of the plants.
Exp.
1 and
on
natural increase
the upper parts of
not
was
plants
in
Exp. 2,
the intrinsic rate of
significantly affected by water stress. On the lower
parts of plants in Exp. 2, rm increased significantly for cohorts feeding
severely
plants compared
experiments, however, rm tended to increase with
stressed
with
well-watered
an
plants.
on
significantly higher (P
0.05) compared with rm of the lower parts.
<,
parts of plants in Exp. 2, rm
Intrinsic rates of natural increase presented in this
range of rm estimates reported for A. pomi and
(Graf
et
a
on
both
increase in stress
intensity. Furthermore,
tiie upper
In
study
were
range of other
was
within the
aphid species
al., 1985; Sumner et al., 1986; Kaakeh and Dutcher, 1992; Zhou and
Carter, 1992). Gaston (1988) stated that
most
aphid species have maximum
rm values in the range of 0.11-0.50 surviving offspring per female per day.
Intrinsic rates of natural increase for the green apple aphid reported by Rutz
et al.
(1990) and by Graf
reported
female.
in the present
(1985)
general higher than rm-values
study probably because of higher fecundity rates per
et al.
were
in
51
reproduction rate (R0), mean
doubling time (DT, days) of A.
apple plants grown under well-watered
Intrinsic rate of natural increase
Table 7.
generation
(G, days),
time
pomi cohorts reared
on
and
(rm),
net
mean
(control), moderately and severely water stressed conditions in Exp.1
as well as on the upper (apex and the uppermost 15 leaves) and the
lower (the rest of the plant) parts of plants in Exp. 2. ±SD are shown;
indicates cohort size a.
n
Experiment
Treatment
1
n
±SD
R0
'«
±SD
G
±SD
±SD
DT
Control
26
48.52
a
±17.58
0.2644
±0.0436
14.7
a
±2.1
2.6 a ±0.4
Moderate
23
45.00
a
±22.96
0.2707 a ±0.0505
14.1
a
±1.7
2.6 a ±0.5
Severe
23
53.48
a
±21.82
0.2813
14.2
a
±1.7
2.5
a
±0.0421
a
Experiment 2 upper parts
of the
a
±0.4
plant
Control
37
38.50
±13.01
0.2943
a
±0.0448
12.4 a ±1.6
2.4 a ±0.4
Moderate
26
51.06 b ±12.48
0.3051
a
±0.0443
12.9
a
±1.5
2.3 a ±0.3
Severe
36
48.90 b ±17.24
0.3087
a
±0.0509
12.6
a
±1.8
2.2
a
±0.4
3.0
x
±0.6
a
2 lower
Experiment
±9.66
0.2287
parts of the plant
±0.0478
14.7
±2.0
Control
39
28.81 y
Moderate
33
23.48
x
±11.59
0.2335 xy ±0.0552
13.5 y ±1.6
2.9 xy ±0.7
Severe
43
35.70
z
±11.47
05527 y ±0.0367
14.2 xy ±15
2.7 y ±0.4
means in a
(P
In both
£
experiments, the
generation
reared
by
on
net
to the cumulative
previously (see
stressed
by
the
same
letter
are not
x
significantly
different
0.05).
corresponded
affected
column followed
x
page
time
(G)
49).
In
reproduction rate of aphid cohorts (Rq)
fecundity of cohorts which was discussed
Exp.
and cohort
doubling
water stress. On the lower
well-watered
plants
plants
and upper
1
was
plant parts of Exp. 2,
(DT)
parts of plants
were not
in
significantly longer
and DT decreased with
difference between DT of cohorts
time
an
feeding
than
moderately
intensity. The
on
increase in stress
on
significantly
Exp. 2, G of aphids
well-watered and severely
significant. Generation and doubling time correlated
negatively with rm (G in Exp. 1: r= -0.75, P<0.001; G in Exp. 2: r= -0.84;
P<0.001; DT in Exp. 1: r= -0.999, P<0.001; DT in Exp. 2: r= -0.978; P<0.001).
stressed
plants
was
52
The intrinsic rate of natural increase
aphid
Calculating fm using physiological
summary statistic to
some
negatively
also found to relate
Exp.
1 and
Exp.
2
instead of
to
chronological time altered the
extent and also resulted in no
presented
between treatments. The values
in
was
pre-reproductive time.
significant difference
in Table 8 refer to the case
study
(see page 24).
Exp. 1, rJm did not differ significantly among treatments. Moreover, the
increasing trend of rm with increasing intensities of water stress (see Table 7)
In
was
In
not confirmed
Exp.
significant
the
by
2, for cohorts
the
feeding
difference in
r'm
(Table 8).
values
fm
on
was
the upper and lower
detected. However,
parts of the plants
r*m
no
parts of
in the lower
compared with the well-
severely
increasing trend of rm with increasing intensities of
(see Table 7) was not as clear with the observed r'm (Table 8).
rate of natural increase, however, was significantly higher for
plant tended to be
higher
stressed
in the
watered treatment. The
water stress
The intrinsic
cohorts
feeding
the plants
(P
<
on
the upper
parts compared with those
on
the lower parts of
0.05).
Intrinsic rate of natural increase (rm) of A. pomi cohorts reared on
apple plants grown under well-watered (control), moderately and
severely water stressed conditions in Exp.1 and on the upper (apex
and the uppermost 15 leaves) as well as the lower (the rest of the
plant) parts of plants in Exp. 2. ±SD are shown; n indicates cohort
Table 8.
size a.
Treatment
J
Experiment
Experiment 2
plants
1
Treatment
n
upper parts of
±SD
r'm
±SD
r"m
Control
26
0.0170 a
± 0.0027
Control
37
0.0184 a
±0.0027
Moderate
23
0.0168 a
± 0.0031
Moderate
26
0.0189 a
±0.0027
Severe
23
0.0171 a
± 0.0025
Severe
36
0.0192 a
±0.0031
^ShN
Experiment 2
plants
^ti!i/3L
means in a column
(P
<
0.05).
followed
lower parts of
by
Control
39
0.0162
x
±0.0033
Moderate
33
0.0164
x
±0.0038
Severe
43
0.0181
X
±0.0048
the same letter are not
significantly
different
53
2.4
Discussion
2.4.1
Effects of Water Stress
Development
Plant
on
present study, apple plants were clearly affected by water stress:
were smaller in size, had lower growth rates, had lower shoot
In the
stressed plants
fresh and
dry weight, and lower individual leaf
area
(Tables
2 and 3,
Fig. 5).
Although plant growth decreased significantly with water stress, overall growth
did not stop
even
in the
severely stressed treatments, which reached very low
leaf water potentials (Y
Fig. 7).
for
only
The
a
plants
-2.85 MPa measured predawn; see Table 4 and
period, however, before they
intermittent drying cycles).
short
result of the
Apple
<
continued to suffer from severe intensities of water stress
were
relieved by
watering (as
a
drought tolerant, having the capability to grow and carry on
at low water potentials (Davies and Lakso, 1979a;
Lenz, 1989). Reductions in plant growth rate, particularly in
trees are
photosynthesis
Sritharan and
even
terms of leaf area
expansion are commonly observed
trees and are considered
expansion
of
an
important
apple was strongly influenced by turgor pressure in potted
(Lakso, 1979; Lakso et al., 1984):
as
linearly until growth finally ceased
The
of
stress
development,
experienced by the plants
apple
trees
turgor decreased, leaf expansion also
decreased
rate
in water stressed
water stress response. Leaf area
stress
as
turgor fell below 0.25 MPa.
intensity
and
stress
duration
determines, among other factors, the extent of
plant suffering (Lakso et al., 1984; Wang and Stutte, 1992). Rapid stress
development may not give sufficient time for adaptation mechanisms such as
osmotic adjustment. Hence, methods used to induce water stress can greatly
affect the above mentioned factors, and should therefore be taken into
consideration when different studies
compared. For example
plant
on
in studies with
responses to water stress
aphids,
are
water stress was induced
by
drying cycle technique (Wearing, 1972), by just letting the soil
et
al.,
1982), or hydroponically using an osmoticum (Sumner et al.,
dry (Miles
1983 and 1986). The rate of water stress development also strongly depends
the intermittent
on
the ratio between
available.
more
plant size and/or plant growth
Wang and Stutte (1992) mention that
rate and the soil volume
water stress
develops much
rapidly in potted plants grown under controlled environmental conditions
(growth chambers, greenhouse) than
potted plants,
soil volume.
water stress can
According
in
field-grown trees:
develop even within
to Miles
1 to 2
in
experiments with
days, due
to limited
(P.W. Miles, University of Adelaide, South
54
Australia, pers. comm.) and Louda and Collinge (1992), ail plants in pots may
with the levels measured in the field.
moderately stressed compared
be
An effect of limited soil volume
the
on
plant growth could clearly be observed
beginning
of the
experiment about
soil volume became limited
a
rapid development of
This
was
reflected in
20
development of water
stress and on
in
already
cm
2. Plants
Exp.
larger than
in
were
Exp.
Very
1.
(small pots) and the plants began
at the
soon
the
to suffer from
probably of nutrient deficiencies.
plant growth in Exp. 2, particularly of
water stress and
generally
slower
moderately stressed plants, compared with Exp. 1 (see
probably was the cause for the inability of the plants to adjust
the well-watered and
Table 2) and
osmotically (to be discussed below).
In
very few studies, reactions of
a
plant sucking insects
to water stress have
been determined in relation to actual
changes in plant water relations (e.g.
Schnider, 1989 and English-Loeb, 1990 for mites; Dorschner et al., 1986 for
aphids).
Predawn measurements of leaf water
reflected to
certain extent the three water
a
potentials (Y) in Exp. 1 and 2
supply levels in the soil (well-
see Table 4 and Fig. 6). Hsiao
(1973) proposed for general purposes three functional levels for water stress
watered, moderately and severely stressed;
in
mild stress entails
leaves:
lowering of
a
plants;
values in well-watered
corresponding
lowering of Y by
MPa); and
more
severe
a
few bars but less than 12
stress refers to
MPa). The level of
the
than
by several bars below
Y
moderate stress refers to
lowering of Y by
a
water stress in the soil
applied
or
15 bars
more
(1.2
or
a
1.5
than 15 bars
in the present
(1.5
study and
Y in
resulting
plants (at the peak of drying cycles) corresponded quite
proposed by Hsiao (1973) (see Table 4).
well to the levels
Measurements of predawn Y may be indicative of the range of water supply
in the soil
on
physiological
state of
is
the
plant level but does
not
necessarily describe the
adaptation
plant
Turgor pressure
generally thought to be more relevant for many plant processes than Y per
se.
or
a
its
to water stress.
Hsiao et al. (1976) explained that
0.3 MPa
crop
species.
In contrast,
a
similar
lowering
a
through dehydration normally
reduces
drop
in
increase
in
solute
concentration
measured. Nevertheless, Studer
(1993)
measurements of
can
of the
degree
Y0
of tissue sap
of "active" osmotic
as
distinguish
when
Y0 by
to
Y0 through
may maintain cell turgor and cell volume
processes. It is, however, difficult to
of
Yp
Y0
well
more
nearly
than 0.2
solute accumulation
as
turgor mediated
between active and
of extracted
tissue
has demonstrated that
provide
adjustment
a
or
in many
zero
passive
sap
is
predawn
good basis for comparison
in water stressed
plante.
55
In
Exp. 1, osmotic adjustment
7). Stressed plants
in response to water stress occurred
(see Fig.
higher Yp than control plants at any Y and were
capable of maintaining positive Yp at lower Y (see Fig. 8). Furthermore,
severely stressed plants could maintain turgor better than moderately
stressed plants at low Y: under moderate stress conditions, zero turgor was
reached at Y
8). Since Y
=
had
-2.0 MPa and under severe stress, at Y
measured
was
significantly with
predawn
<
-3.0 MPa
(see Fig.
and leaf water content did not vary
Y within a treatment, the observed decreases in
attributed to active solute accumulation. In addition,
Y0 can be
Y0-values corresponded
well to ranges reported in other studies
on apples and other woody plants
(compare below). The higher YP observed in rewatered, stressed compared
with always well-watered plants (see Fig. 8) can be explained by the
accumulation of solutes
adjustment
(lower YJ during the water stress period. Osmotic
plants (even if it is not sufficient to maintain
in water stressed
turgor during stress)
well watered
higher turgor values after rewatering
plants (Studer, 1993).
can
lead to
In Exp. 2, Y0 did not decrease enough to maintain turgor at low
7). Turgor reached zero at Y^ about -3.5 MPa (corresponding
Y about -2.3
MPa). The capacity
probably limited by
a
(limited soil volume)
and
too
for osmotic
Y
than in
(see Fig.
predawn
adjustment in Exp. 2 was
rapid development of high levels
to
of water stress
by additional stresses (nutrient deficiencies, mite and
powdery mildew infestation). This lack of osmotic adjustment was reflected in
generally slower plant growth in Exp.
2
compared
with
1
Exp.
(see Table 2).
Wang and Stutte (1992) cited studies in which decreases in Y0 in apple
varying from 0.5 to 3.0 MPa have been found. Only 0.2 to 0.5 MPa of these
decreases, however, could be attributed to active adjustment; the remainder
passive dehydration. Goode and Higgs (1973) observed osmotic
adjustment in apple trees of as much as 0.7 MPa during the day (diurnal) and
was
due to
of up to 2.0 MPa over a
Y0
to decrease
which is
a
by
as
growing
much
as
season.
1.65 MPa
far greater decrease than
Results from
Davies and Lakso
diurnally
(1979a) noticed
in field grown
apple trees,
generally observed in other mesophytes.
Fanjul and Rosher (1984) showed that osmotic adjustment
occurred in both field and pot grown trees and that the extent of
was
similar
(0.3 MPa) for both potted and orchard
in the rate and intensities of stress
Stutte
(1992) noticed that Yp
adjustment when
Y
trees.
adjustment
despite differences
imposed. On the other hand, Wang and
could not be maintained
dropped below
potted Jonathan apple
trees
-1.6 MPa in
through osmotic
greenhouse grown 2-year old
56
adjustment does not represent the only
maintaining YP in apple trees under water stress. High tissue
It has been noted that osmotic
mechanism for
elasticity allows apple leaves
levels that would
cause
to decrease relative water content
irreparable damage
thereby buffering turgor against changes in
addition, particularly
in
big
trees
from leaf and trunk tissues
growing
(capacitors)
Y
(Davies
and Lakso, 1979a and
results of the study
presented
can
1979a).
In
transpiration
be released to the
high transpirational demand
1979b). This
was
also confirmed
by the
significant changes in
decreasing supply of water (see Figs
here: whereas
contents of leaves occurred with
and Lakso,
to
plants,
under field conditions, stored water
stream, which buffers Y under conditions of
(Davies
(RWC)
to most herbaceous
no
water
5 and
8), water content of stems significantly decreased with increasing water stress
The
(Fig. 5).
ability of apple
pressure range is in itself
an
trees to continue
The distance of leaves from the
main artefact in
were
to the
measuring
of
source
over a
light in the growth chamber
temperatures. The
leaf surface
wide turgor
to water stress.
nearer the
was a
leaves
light, the higher their temperatures. This artefact
of
source
growth
important adaptation
confounded differences in leaf surface temperature between treatments due
particularly on the upper parts of the plants. Leaf surface
temperatures of the upper parts of well-watered plants were higher than the
to water stress,
ambient air temperature which
was
approximately 23°C (see Fig. 4) and,
despite the transpirational cooling effects, higher than temperatures measured
on the
In
upper leaves of
plants which have
can
severely stressed plants.
access to unlimited water
transpire freely (Burrage,
1976 cf.
supplies (well-watered),
leaves
Willmer, 1986), and may be cooler
than ambient temperature when air temperatures
are
high (e.g. 30°C).
These
differences between foliage temperatures and ambient air temperature
dependent on both
water stress
net radiation and soil water
by closing their stomata to
are
availability. Plants respond
reduce water loss
by transpiration, i.e.
leaf temperatures increase. Under field conditions, net radiation received
a
leaf is
a
function of the leaf size, leaf
to
by
shape, reflectance of the leaf surface,
leaf, the site of the leaf (height above ground and orientation;
Willmer, 1986). In growth chambers, the distance from the source of light,
texture of the
however,
can
temperature,
In
both
become
as was
the
dominating factor influencing
observed in the present
experiments,
temperature
measurements in time and space
leaf
surface
study.
measurements
were
(location). Temperatures
of
only
only
point
one
leaf
57
measured, and at maximum light intensities and growth chamber
were
temperatures. Willmer (1986) cited that temperature variation over a single
large leaf (upper leaf surface) could be up to 7°C with the higher temperature
being
in the center of the leaf. It follows that the leaf surface
measured in Exp. 1 and
Exp. 2, only crudely described
temperatures
the situation under
growth chamber. Nevertheless, leaf surface temperature
study tended to increase with an increase in stress intensity (see Fig.
water stress in the
in this
4). The average difference in temperature between well-watered and
stressed
plants
disappeared during
the
difference
This
2°C.
among
water
treatments
night and when plants were rewatered, rendering data
difficult.
pooling
plant growtii, fresh and dry weights, leaf
In conclusion,
decreased
components
temperatures tended
Osmotic
Clear
about
was
degrees,
various
to
to increase with an increase in
adjustment was observed in Exp.
differences
between
treatments
water
potential
leaf
surface
whereas
1 and to
intensity of water stress.
a
lesser extent in
Exp.
2.
probably underestimated,
were
however, by several unfavorable "conditions" in these experiments, such
as
intermittent drying, limited pot size and growth under artificial light. Water
stress caused
changes
in
temperatures, which in
plant growth, plant water relations and leaf surface
one
way
or
another could have affected
aphid
population development and will be discussed in the following.
Effects of Water Stress
2.4.2
Life Table and
The
on
Population Parameters of Aphids
development time of immature aphids is variable and dependent on
as temperature and food quality (Baker and Turner,
extrinsic factors such
1916; Dixon, 1987). In Exp.
1 of the
present study, the overall development
supply treatments did not decrease
(see Table 5). At the beginning of the
time of immatures in the three water
significantly with
experiment
water stress
water stress
was
just beginning
to build up, hence the
by
increase in leaf surface temperatures mediated
occurred in the
in larval
appropriately treated plants.
development time of
expected
water stress had not
yet
(1984) reported a decrease
days at 20°C to 5.3 days at
Graf
A. pomi from 7.2
25.8°C.
an average larval development time for h.
days, the time being equally divided between the four stages.
Baker and Turner (1916) reported
pomi of 7 to 8
58
The present
mean total development time of
unevenly distributed among the instars, L4 being
study, however, showed that the
larvae of 8.6
days
approximately
was
20% shorter than the
(1976 cf. Asante
et
periods of many aphid species
that the
reported
previous larval instars. Gilbert
et al.
al., 1991) also considered that the first three instar
development
are
similar in duration. Graf
(1984)
in his
study
time for the first and the last larval instar of
pomi tended to be longer than the other two immature stages. Graf
A.
(1984)
experiments under constant temperatures, whereas in this
study temperatures fluctuated rhythmically between 22°C and 17°C.
conducted his
Another parameter
the
on
contributing to the generation time of aphid populations is
pre-reproductive time. This period is of variable duration and dependent
food
more
quality
(Dixon, 1987). High food quality
and temperature
rapid aphid development,
developmental rate. In Exp.
while
overall
2,
a
significant
decrease in the
an
will favor
a
increase in temperature increases
1 and on the lower
pre-reproductive
time
parts of plants in Exp.
was
observed with an
increase in intensities of water stress. This decrease could well have been
induced
stress
by
a
slight increase
(see Fig. 4). On the
in leaf surface
upper
uppermost 15 leaves), however,
temperatures mediated by water
in Exp. 2 (i.e. apex and the
parts of plants
no
change in the pre-reproductive time
measured. The shorter distances of the upper leaves of well-watered
to the
light source
the slower
fecundity
In
on
stressed
on
the uppermost
parts of the plants.
plants
as
well
as on
leaves
of
aphids feeding
to a much
Table
6). The
greater
extent
rate of
by
on
severely water
positioned in the lower parte of tiie plant
longer compared with well-watered plants
plants (see
than the upper leaves of
significant effect of water stress on leaf surface temperature
the aphids' pre-reproductive time as well as longevity and
Exp. 2, the reproductive time period
was
more
growing, severely stressed plants (see Fig. 4). This probably
"masked" any
and hence
heated the leaf surfaces up
was
plants
and the uppermost parts of the
population growth, however, is determined
the rate of
total number of larvae born in the entire
reproduction
in
early life than by the
lifespan (Dixon, 1987).
The lower surface temperatures as well as the less favorable nutritional
quality of leaves in the lower parts of the plants probably accounted
significantly longer development times and the significantly
fecundities observed in aphid cohorts
with leaves of the upper parts
feeding
on
those leaves
(see Table 6 and Fig. 10).
for the
lower
compared
59
Graf (1984) reported
a
maximum
fecundity per virginopara of A, pomi of
larvae/female when reared at constant 20°C. At 25.8°C
75
fecundity decreased
Aphids usually achieve their highest reproductive
life. The size and timing of the peak in reproductive
to 68.5 larvae/female.
rates in
early adult
activity is important
in determining revalues (Dixon, 1987). Aphids in this
study reached their reproductive peaks between 12 and 20 days after birth in
Exp. 1 and between 11 and 15 days in Exp. 2 (see Figs. 11 and 12). Beside
genetic variability, intermittent drying of the soil and its effect
probably resulted
these
ing
in the fluctuations in
experiments. For example,
for 1
Aphids
or
2
days
which
some
then resumed
develop
when host
on the plants
age-specific fecundity observed in
aphids completely stopped reproduc¬
reproduction
in lower numbers.
quality is poor devoted less
resources
to
reproduction and thus had larger fat
that
develop
when host
reserves and lived longer than aphids
quality is high (Dixon, 1975; Dixon and Wellings,
1982; Leather et al., 1983 cf. Dixon, 1987). In the present study, it was found
that
aphids feeding on the lower parte of plante (probably of inferior food
quality), beside having a longer development time, were smaller in body size,
darker in color and had lower body water content than aphids reared on the
upper parte. The
when conditions
harsh,
was not
opposite trend
report that several aphid species give birth to small offspring
are
favorable and to
large offspring
confirmed in the study presented here;
was
when conditions
on
are
the contrary, the
observed.
In the present study, the intrinsic rate of natural Increase (rm) increased in
tendency (Exp.1 and on the upper parts of plante in Exp. 2) or significantly
(on the lower parts of plants in Exp. 2) with an increase in intensities of water
stress
(Table 7). This increase in rm may well be due to the increase in leaf
by water stress. Graf (1984) reported an
surface temperatures mediated
increase in rm from 0.117
(1/day)
at 10.8°C to 0.427
Furthermore, the significantly higher rm
on
(1/day)
at 25.8°C.
leaves of the upper parts of the
plant (i.e. apex and the uppermost 15 leaves) compared with those of the
lower parts (i.e. the rest of the plant) was due partly to differences in leaf
surface temperatures (see Fig. 4) but mainly to the poorer food quality
(reflected in Rq) of leaves in the lower parts of the plants.
When this
on a
was
temperature effect was taken into consideration by expressing rm
physiological time basis (r"m, Table 8) no effect of water stress on fm
revealed, although the relativity of the r'm-values between
tended to be different from the relativities of the
revalues.
treatments
When Graf
(1984)
60
and Graf et al.
A.
(1985) expressed rm per day-degree, then a decrease in rm of
0.0245
pomi between 14.8°C and 25.8°C was observed (at 14.8°C rm
=
and at 25.8°C rm
0.0.214). It follows that any changes in the aphids' habitat
=
temperatures could be expected
Since the
rm-value
rm.
combines information
on
the
development time, survival
age-specific fecundity (Lewontin, 1965)
rates and the
same
to affect
factors,
or a
combination of factors,
intrinsic rate of natural increase
as
well
as
as
it is affected
by the
its component variables. The
G and DT under conditions of
water stress and the
experimental conditions in Exp. 1 and Exp. 2 were
probably defined by the mortalitity of immatures and early adults, by the prereproductive time and/or by fecundity, particularly in early stages of
adulthood.
Changes
in rm, due to water stress were
reported to result mainly from
mortality (Birch and Wratten, 1984), pre-reproductive and
early reproductive time (Lewontin, 1965; Reed et al., 1992; Wennergren and
Landin, 1993) and generation time (Gaston, 1988).
changes
in larval
Several circumstances may be responsible for the results obtained. The
importance of the high variability in leaf surface temperatures (other than
changes
due
temperatures
leaf size,
to
of
a
water
stress)
leaf may
even
shape, architecture
etc.
were
depending on
(Willmer, 1986). In this study, temperature
differences in the growth chamber at the
already
and
fluctuated
uneven
treatments,
by
1 -3°C
(data
probably underestimated. Surface
vary up to several degrees
not
same
distance from the
shown) due
to
light source
irregular light intensities
ventilation. Differences in leaf surface temperatures between the
on
the other hand,
were
small (<
3°C). Therefore, differences in
habitat temperatures of
treatments
probably
aphids (i.e. body temperatures) between
and their effects on the development of aphids
overshadowed
by
the much
other factors than water stress. It
changes
in the habitat
can
higher variability
in
the different
were
most
temperature due to
further be noted that the effect of small
on aphid development can be
(1988) mention that even subtle temperature
changes (less than 3°C) can be expected to have an impact on insect
population dynamics. On the other hand, Hoffmann and Hogg (1991)
concluded in their study that the higher temperatures found in water stressed
temperature of aphids
variable. Benedict and Hatfield
fields
were
insufficient to compensate for the change in rm of the potato leaf
Another important factor to be considered is the
hopper
high variability
in their treatments.
among data within
a
treatment.
Aphids although originating
61
parthenogenetically from the same "mother" are not necessarily biologically
similar (Chi, 1988). In addition, under unfavorable conditions the genetic
heterogeneity of a population in terms of individual fitness of the females
become
to
seems
(Wermelinger
reared
on
pooled
so
et
evident
more
than
in
an
optimum
al., 1991). In the present study, aphids in
environment
a
cohort
were
plants. Samples for life table construction were then
that the effect of plant variation could be disregarded. Although the
different
apple plante
development
same clone, their growth and
and
conditions,
particularly under intermittent
given
originated from the
used
under the
drying, nevertheless
varied to a great extent.
apple aphids had a wide choice of microclimates
(temperature and humidity) and feeding sites within their host plant, simply by
Last but not least, the green
moving short distances around the host plant. Therefore they could be subject
temperatures, levels of relative humidity and nutrition through their
to different
behavioral actions, to
some
relative
Although
intention.
independent of experimental design and
humidity was held constant (55-60% RH) in the
extent
growth chambers, and was therefore
the
near
proximity
not
of the leaf surface.
due to the distance from the
source
surveyed, it was expected
Changes
of
light,
to vary in
in leaf surface
to
temperatures
day and night fluctuations
humidity considerably. In addition
provide disparate environments for the
insect. The mobility of aphids may be an additional factor in the explanation
why rm did not differ significantly among the treatments in the present study.
and/or water stress may affect relative
upper and lower leaf surfaces can
The influence of water stress
on
the method
stress) used
(soil
vs
the population dynamics of aphids depends
solution) and patterns (intermittent vs constant
on
nutrient
to induce water stress.
intermittent water stress was
although
stress largely detrimental
to the
Wearing's (1972) results showed that
largely beneficial and continuous water
reproduction
and survival of M. persicae and
brussels sprouts, there were differences
potted
feeding
species on different leaf ages. Sumner et al. (1986) found that hosts
constantly stressed by drought (water stress induced hydroponically by the
addition of the osmolyte PEG) decreased the rm of Schizaphis araminum
EL brassicae
on
between
(Rondani).
watering)
Miles et al.
water stress (complete stop of
development of JL. brassicae born on rape
(1982) reported that
increases the rate of
plants, but as stress becomes pronounced insects became restless and when
plants became severely wilted they were rejected by the insects. Thus, aphid
behavior
was
markedly
affected
by
water stress
causing
an
increase in the
62
aphids which
movement of
present study
in turn can influence
the different parts of the
on
Different hosts (woody
vs
herbaceous)
plants
and
revalues
as
determined in the
outlined above.
aphid species can react differently
slowly in trees versus
to water stress. Stress effect will be manifested more
herbaceous plants
(Waring and Cobb, 1992). Herbaceous plants may be less
tolerant of water stress than other
plant types, rendering poorer hosts
when
water stressed.
The results of experiments under controlled environmental conditions do not
always correspond well to results obtained under field conditions (e.g. Price
et
al., 1989; Waring and Cobb, 1992). Nevertheless, there do exist reports
which prove that experiments conducted in
greenhouses
are
comparable
and
Hogg, 1991).
An
important
to field trials
growth chambers and/or
(Fanjul
and
in
Rosher, 1984; Hoffman
consideration in
population dynamics
studying the effect of water stress on the
aphids is which approach was used: a density-
of
independent life table approach
or a
density-dependent population approach.
The average rate of increase assigned to
a given aphid species existing at
density may not be representative of the rate of increase of the same
aphid existing at a moderate to high density level (Kaakeh and Dutcher,
low
1992). Since
in this section the method of
tables did not
provide
a
constructing
satisfactory understanding
and
analyzing
life
of the effect of water
stressed hosts
section the
on the development of the green apple aphid, in the following
density-dependent population approach is applied with the
objective to shed more light
dynamics of aphids.
In conclusion, counter to
aphid
on
population
expectations, the combined effects of changes in
habitat temperatures encountered in this
stress could not be shown to
population
rate
of
study and imposition of water
significantly affect aphid development and
growth. The
nevertheless, appeared
a
the effect of water stress on the
water
to have had
some
stress
applied
to
"beneficial" effects
on
the
plants,
the insects:
slight decrease in the pre-reproductive time, especially on leaves positioned
in the lower parts of the
were
observed.
plant, and
a
slight
increase in
fecundity (Rq)
and rm
63
3
Effects of Water Stress
Population Dynamics
of the Green Apple Aphid:
Population Development
on
and Growth
Introduction
3.1
In the previous section, the effect of water stress on aphid population
development was described by relating life table parameters and summary
statistics of aphid cohorts with plant growth and the physiological parameters
of plants. The intrinsic rate of natural increase, an adequate descriptor for
population development
cohorts
feeding
contrast to much
on
under unlimited conditions, was calculated for aphid
plante grown under various levels of water supply. In
published work the
of natural increase
(rm)
was
results have shown that the intrinsic rate
little affected
by
water stress,
although
water
biomass accumulation and
growth,
plant. This result is, from a theoretical and pest
management point of view, important enough to be interpreted in detail. The
stress had a
significant
effect
on
shoot
water relations of the
experimental method used in the previous section did
explanation for the
statements
on
results obtained.
the life of
a
typical
not
Age-specific life tables
individual of
a
cohort
(Price
provide
are
et
an
summary
al., 1989),
and rm is regarded as the best available single description of the population
growth of insect species under defined conditions (Southwood, 1978; Hurting
et
al., 1990; Kaakeh and Dutcher, 1992). Price
et al.
(1989) pointed
out that
64
many researchers
analysis
was
led into
were
sufficient to
analysis, often applied
as
thinking that life table construction and
explain insect population dynamics. Life table
a purely correlative approach, does not reveal
causation and the need for further studies to
explain
causes
and effects is
recognized.
In the
on
following,
an
plant growth
attempt is made
and
to understand the effects of water stress
development of aphid populations from
the
on
biophysical and biochemical relationships. The aim is to create a base for
better understanding of the results obtained using the method of the previous
section.
Already
in 1923,
Lathrop
factor limiting the rate of
stated that plant growth frequently constituted a
development of Aphis pomi De Geer feeding on
slowly growing foliage. The positive correlation of long shoots and vigorously
growing plants and insect herbivore development has often been emphasized
(Price
et
al., 1989; Waring and Cobb, 1992; P.W. Miles, University of
Adelaide, South Australia, pers.
Resources, however,
are
densities become very
nutrient stress
(Price
and/or the
high
et
comm.).
often abundant and not
limiting until insect herbivore
is modified by water and
resource
al., 1989) and/or by the capacity of the plant
to
quantity
age-specific life
master allelochemical responses (Miles and Oertli, 1993). Resource
and
quality
often not considered in the construction of
are
By removing the progeny of the individuals used for constructing life
tables, the carrying capacity of a plant, its ability to defend against mass
tables.
attack
and
the
abundance
of
an
insect
are
neglected.
The
rate
of
aphid populations is probably determined by the balance
between assimilate demand of the aphids and the carrying capacity of the
development
plant in
of
terms of assimilates
chemicals under
Individual
their host
are
aphids, which do
not transmit
feed on the
to
synthesize defensive
viruses, have few if any effects
plant (Pollard, 1973; references
important agriculturally only
Aphids are considered
can
produced and its ability
given environmental conditions.
because
1990)
high numbers.
cf. Miles, 1989b; Miles
they
can occur in
on
and
damage than other insects because they
photosynthesis without destroying the photo-
to cause less
products
of
synthetic machinery (Llewellyn, 1972 cf. Meyer, 1993; cf. Pollard, 1973; cf.
Miles, 1989a). Even mass feeding by aphids may only damage the plante by
an overall reduction of growth due to a massive drain of plants' assimilates
towards the insects
(sink-effect) (Pollard, 1973; Mallot
and
Davy,
1978 cf.
65
Wellings
et
Wellings
et
al., 1989; tor other references
see
Miles, 1989a and 1989b;
al., 1989). An apparent reduction of overall growth results when
the drain of assimilates exceeds the
capacities of the plant for compensatory
growtii (aphid density threshold for significant reduction in yield)(Miles,
1989a).
explain causal relationships between modified host
To
resources (quantity
quality) and aphid population development and, conversely, between high
aphid population densities and host development, aphid populations were
and
allowed to build up
Population
and
on
apple
characteristics
trees grown under different water
were
assessed and were related to
regimes.
plant growth
plant physiological parameters.
Materials and Methods
3.2
Two experiments (Exp. 3 and Exp. 4) were conducted to study the
development and growth of aphid populations on apple plants grown under
different water
3.2.1
regimes.
Characterization of the
of
The size and
Development
and Growth
Aphid Populations
density of aphid populations (according
to
Krebs, 1972 primary
populations) as well as age distribution and alatae
production (secondary characteristics) were assessed for populations feeding
characteristics of
on
apple plants grown under different water regimes. Measurements were
a specific time of development in Exp. 3 and after host plants had
taken after
stopped growing and
densities in
Exp.
4.
were
apparently suffering
from
high aphid population
Further, this approach weighted the "oscillating" effects of
corresponding changes in plant growth and in
physiological plant parameters on aphid development, since population size
is a longer term effect.
intermittent drying and of the
66
Experimental Conditions
3.2.2
In both
experiments,
apple plant
one
Soil mix, environmental conditions,
grown per 10 L round
was
experimental preparations
water stress induction and measurement
plastic pot.
well
as
(2 gypsum blocks per pot
as
in water
treatments) were as described on pages 8, 9,15, 16 and 17. The
regimes, i.e. treatments imposed in Exp. 3 were similar to Exp. 1 and
stressed
water
Exp.
=
2
(control: Y^, -0.05 MPa, moderate: Y^, -0.60 MPa,
MPa). In Exp. 4, the treatments applied were:
=
(C):
1. control
2.
mildly
stressed
3.
moderately
1 stressed
moderately
2 stressed
Treatments in
Y^,
Y^
Y^,,
Y^,
(MD):
4.
Exp.
(Mod. 1):
(Mod. 2):
>-0.05 MPa
>
>
-0.40 MPa
>
-0.60 MPa
moderately
Exp. 3. If not otherwise mentioned, Ysoil of the
In both
half of the
experiments,
while the other half
aphids (+A)
replicates
of +A and -A
plants
plants
water stressed treatments was
not
was
a
readings.
treatment were infested with
(-A). In Exp. 3, the number of
was 6 and 5, respectively.
+A and -A
plants
in each treatment
3.
Similarly
Exp. 1, plants
to
soil surface. These
one
of
intensity
in each treatment
Exp. 4, the number of replicates of
was
(well-watered)
water stressed treatments in
calculated from the average of both gypsum block
In
Y^,
-0.20 MPa
4 were chosen to be intermediate in stress
between the well-watered and the
In
severe:
-1.80
branch
Exp. 3,
upper
as
cardboard
was
plants
of
Exp.
were
3
cut down to the fourth node above
allowed to regrow to be used in
Exp.
4.
Only
kept.
two fourth larval instars
well
were
(L4)
of A pomi
barrier.
The
barrier
was
plant and
expanded leaf (tenth leaf counted from plant apex)
experiment (referred
to as leaf
were
transferred to the
separated by a
placed below the first completely
the lower parts of the
as
A). Aphids
were
were
at the
beginning of the
collected after 22
days
of
on the host. This period was enough to have a rather dense aphid
population on the upper part of the plants, particularly on well-watered plante.
Based on the age distribution of a population after 22 days in the different
feeding
treatments in
Exp. 3,
transferred to the
17 L1-L2;
a
certain number of aphids of each age category
plants of Exp.
mildly, Mod.
4
(well-watered: 3 apterous adults,
1 and Mod. 2 water stressed: 3
4
was
L3-L4,
apterous adults, 6 L3-
67
L4,15 L1-L2). The objective was
population;
specific under a certain
structure in a
and
quickly
as
possible
set
of
stable age
a
to be rather constant
expected
growth conditions. According
to
variation in environmental conditions
and Landin
(1993),
change
only population growth but also the structure of the population which after
Wennergren
not
to reach as
age structures were
initial oscillations, will then become almost fixed.
Plants in
Exp.
4 were not divided into upper and lower
transferred to the first
parts. Aphids were
completely expanded leaf (10th leaf counted from the
apex; referred to as leaf
growing, suffering from
A). When
a
a
plant infested with aphids stopped
high density pressure, aphid populations
were
collected.
Data Collected
3.2.3
Plant Parameters
Plant water relations. In
Exp. 3, predawn and midday leaf
turgor (Yp) potentials
11th leaf from the apex) in +A and -A plants
osmotic
(Yg)
and
were
(Y),
(10th and
water
of two consecutive leaves
determined at harvest In
Exp. 4, predawn Y, Y0 and Yp were assessed for every tenth leaf from the
plants only. Leaves of +A plants were covered with honeydew
apex of -A
which affected measurements. Washing the honeydew off the leaves
found to falsify measurements of
weight, and
Plant
In
were
(final
experiments,
fresh
Exp.
3 and
Exp. 4, shoot length and number
was
weight, dry
of leaves
measured and counted every second to fourth
trees were harvested. Mean total
-
In both
water content of these leaves were assessed.
growth.
plant size)
Y0.
initial measurement),
leaf appearance per day
mean
were
Comparisons in growth among
plant size,
mean
extension rate per
weighted
over
(i.e.
day until the
increase in
day
the whole
treatments were made at
and
plant size
mean rate
of
experimental period.
day 27 in Exp.
3 and
24 in Exp. 4. Mean internodal length of the growth which took place
during the experimental period was calculated.
day
Plant biomass
productiom.
shoot, of leaf and stem
as
In
Exp. 3, the fresh and dry weight of total
well as the total leaf area of +A and -A
determined at harvest. After all aphid
populations
were
plante were
collected, +A and -A
peak of the current drying cycle; the date of
harvest varied among plants depending on treatment. In Exp. 4, the fresh and
dry weight of shoot, leaf and stem of the additional growth of +A and -A
plants
were
harvested at the
68
plants were assessed
at harvest. Plants infested with
aphids
were
harvested
of the current
collected and when the
after aphid populations were
peak
drying cycle was reached. Corresponding -A plants were harvested parallel to
+A plants when the peak of the current drying cycle was reached. Leaf area
was measured in -A plants only. For both experiments, tissue water content
was
determined.
Characteristics of
In
Aphid Populations
Exp. 3 after 22 days of rearing, aphid populations which had developed on
the upper and lower parts of the
purpose,
a
suction device
was
plants
were
collected
constructed with which
separately. For this
a
large number of
and alive. After collection, the different
efficiently
aphids
developmental stages in an aphid population (L1+L2, apterous L3+L4,
could be collected
apterous adults, winged L3+L4, alatae)
were
separated, counted (the whole
as dry weight determined
(Sartorius S4 supermicro balance, Sartorius GmbH, Gbttingen, Germany).
population
In
Exp.
were
was
counted)
and their fresh
4 when +A infested
as
well
plant had stopped growing, aphids of a population
populations in
efficiency at work, a
collected with the self-made suction device. Since aphid
4 were rather
large, and
in order to maximize
Exp.
technique for taking representative samples
developed
and
applied. Collected aphids
ethanol solution in
poured
into
a
a
500 ml
out of a collected
were
plastic bottle, agitated and
100 ml bottle. The
population was
mixed with 300 ml of 70%
an
aliquot of 50 ml
then filtered out of the solution,
aphids were
dry for a short time before being counted.
washed with water and allowed to
Aphids
were
still alive after
sampling which facilitated the distinction among
stages. Two samples of each population were taken. The
aphid developmental stages (L1, L2, apterous L3 and L4, apterous
adults, winged L3+L4, alatae) of a sample were separated, counted and their
the different
different
well as
dry weight determined. The standard
samples ranged
from 0.01% to 5.10% for the different
The rest of the
population
fresh
as
was
well as the age structure of the
the
samples.
error
between the two
developmental stages.
weighed and the total number of aphids as
population
were
approximated according
to
69
3.2.4
Data
To test the
between
significance
means
regimes by
Analysis
of water stress
of uninfested
standard
analysis
plante
on
were
of variance
plant parameters, differences
compared
(ANOVA)
under different water
followed
by a test of
least
(LSD) at a
significance
(Statgraphics 5.0, STSC Inc., Rockville, MA, USA). Similarly the
significance of an infestation with aphids on plant parameters was tested by
comparing aphid infested and uninfested plants. To test the significance of
water stress on population characteristics, differences between means, upper
and lower parte of plante in Exp. 3 taken separately, were compared using
ANOVA followed by LSD test at a 5% level of significance. Similarly the
significance of feeding site (i.e. leaf position within plant) on the development
of aphid populations was tested. Simple linear regression was applied to
describe the relationship between Y^, and Y, Y0 and Yp as well as among
significance difference
5% level of
if not otherwise
mentioned
potential components within
a
plant.
Predawn
and
midday potential
measurements were correlated.
3.3
Results
3.3.1
Development
Figures 13 and
and
Exp.
of Water Stress in the Soil
14 describe the
4 induced
development of soil water stress in Exp. 3
by the intermittent drying cycle technique. An example of
each treatment in both
experiments is plotted. The examples shown
are
of
representative, single pots.
Watering frequency decreased with an increase in intensities of water stress.
In Exp. 3, the well-watered treatment experienced 4 to 6, the moderately
stressed 2 to 4 and the
day
severely stressed treatment 1 to 3 drying cycles (to
In Exp. 4, the well-watered treatment experienced
mildly stressed 5 to 7, the moderately 1 stressed 4 to 6 and the
40 of the
6 to 8, the
moderately
experiment).
2 stressed treatments 3 to 5
drying cycles (to day
40 of the
experiment).
As in
Exp.
1 and
Exp. 2, the chosen intensities of
treatments could not be
Exp. 3, the
severe
soil water stress of the
consistentiy maintained, particularly in Exp. 4. In
stress treatment, which
was
supposed
to reach a
Y^,
of
70
0.00
D
-0.01
0_
-0.02
-0.03
-0.04
well—watered
Pot
12
O
Q-
O
Q_
^
10
20
Time
o
•
o
Fig.
13.
30
(days)
gypsum block at 7 cm soil depth
gypsum block at 14 cm soil depth
tensiometer at 10
cm
soil
depth
Soil matric potentials (Y^,) in representative, single pots of wellwatered, moderately and severely water stressed treatments during
experiment
MPa, reached
3.
Ysoi, of -2.4 MPa instead (see Table 13 below). In
Exp. 4, the chosen difference in Y^, from one treatment to the other was 0.2
MPa. Since already at the beginning of the experiment the plants were rather
big (mean size of 85 cm), it was impossible to maintain these Y^ under the
given experimental conditions (see Table 14 below).
-1.8
a mean
71
0.00
0.01
o
0_
0.02
0.03
,
m
0.04
_,
•0.05
-10
0
10
20
30
40
i
i
50
0.0
o
-0.2
-0.4
o
-0.6
-0.8
-1.0
-
mildly
i
stressed
i
Pot 7
i
i
0.0
-0.2
a
a.
-0.4
-0.6
-0.8
-1.0
0.0
o
a.
O
10
20
Time
o
•
o
14.
Soil matric
(days)
gypsum block at 7 cm soil depth
gypsum block at 14 cm soil depth
tensiometer at 10
potentials (Y^,)
in
watered, mildly, moderately
1
treatments
30
during experiment 4.
cm
soil
depth
representative, single pots of welland moderately 2 water stressed
72
Y^ measured at maximum stress
Exp. 3 and Exp. 4 are presented.
In Table 9, the ranges of
of
experimental period
over
the entire
potentials (Y^ in replicates of a treatment at
(control), moderate and severe
conditions of water stress in experiment 3 and under well-watered, mild,
moderate 1 and moderate 2 conditions of water stress in experiment 4 ".
Table 9.
of soil matric
Range
maximum stress under well-watered
Ex seriment 3
Experiment
q^, (MPa)
Treatment
Treatment
4
Control
-0.00 to -0.08
Control
-0.00 to -0.05
Moderate
-0.46 to -1.43
Mild
-0.18 to -1.56
Severe
-1.07 to -4.96
Moderate 1
-0.28 to -2.48
Moderate 2
-0.58 to -2.18
Y^ readings taken
As in
Exp.
1 and
at 14 cm soil
depth.
Exp. 2, the variability among replicates of
high. The gradient in Ysoil between the
Exp. 4 was smaller than in Exp. 3 (Figs.
section 2, the
7 and 14
13 and
cm
soil
a
treatment was
depths
in a pot in
14). As already mentioned in
practice of allowing plants of the previous experiment to regrow
after cutting them down
permitted a
uniform soil water distribution within
more
the pot.
In both
experiments, water
was
first withheld at
beginning
drying cycle
was
3.3.2
Effects of Water Stress
of
Plant
experiment (day
an
already
=
aphid
day -10. Therefore,
transfer to
(mean
leaves
(mean
44.0
cm)
=
at
25.7
between 50.0 -113.5
growth chamber),
leaves
(mean
treatments
=
was
43.1
a
on
Plant
Development
day
22.0
-
61.0
cm
-5 and total number of leaves between 16-35
leaves)
cm
at the
in progress.
growth. In Exp. 3, initial shoot length ranged between
=
at
(mean
leaves)
at
similar. Since
day
=
Exp. 4, initial shoot length ranged
cm) and leaf number between 26 57
1. In
84.8
day -3. The
-
mean
initial size of
plant growth expressed
plante among
in number of leaves
plant growth expressed in shoot length, only data of
development of the shoot under water stress are presented in Table 10.
showed results similar to
the
0
73
Table 10.
length
well as inaease in shoot
length and
experimental period, of
apple plants grown under different water regimes in Exp. 3 and Exp.
measured at day 24).
4 (Exp. 3 a, measured at day 27; Exp. 4
Means ±SE (in parenthesis) are of aphid infested (+A) and uninfested
Total shoot
at harvest
extension rate per
as
day averaged
over
the
,
(-A) plants0.
Treatment
length
(cm)
total shoot
+A
increase in shoot
extension rate
length (cm)
(cm/day)
|
+A
-A
Experiment
Control
Moderate
Severe
80.4
Mild
Mod. 1
Mod. 2
3
a
76.8 a
32.1a
33.1a
1.19a
1.23a
(±4.8)
(±5.7)
(±2.2)
(±3.8)
(±0.10)
(±0.14)
50.3 b
49.7 b
3.5 b
5.6 b
0.13 b
0.21 b
(±5.8)
(±8.6)
(±1.4)
(±3.5)
(±0.05)
(±0.13)
49.8 b
55.3 ab
I
1.7 b
2.5 b
0.06 b
0.09 b
(±5.3)
(±3.1)
|
(±0.7)
(±0.6)
(± 0.02)
(± 0.02)
Experiment
Control
-A
+A
-A
120.7
x
123.3
x
31.2
x
4
32.7
x
(±7.4)
(±10.6)
(± 1-9)
(±0.9)
113.0x
110.0
23.3
31.5
(±3.5)
(±8.0)
106.8
X
x
(±0.8)
x
(±1.8)
1.02
x
(±0.07)
0.83
X
(±0.03)
1.17x
(± 0.03)
1.13
X
(±0.06)
114.8 X
22.8 X
24.3 y
0.81 x
0.87 y
(±5.3)
(± 1.8)
(±4.8)
(± 1-8)
(±0.17)
(± 0.06)
114.0
111.8
x
x
(± 12.5)
x
(±8.2)
x
26.3 y
(±2.0)
(±1.7)
25.5
0.91
x
(± 0.07)
0.94 y
(±0.06)
plants: mean of 6 replicates (except moderately stressed: 5 replicates)
plants: mean of 5 replicates (except severely stressed: 3 replicates)
+A plants: mean of 2 replicates (except well-watered: 3 replicates)
A plants: mean of 3 replicates
means in a column followed by the same letter are not significantly different
(P £ 0.05).
+A
-
-
A
74
In
Exp. 3,
mean
total and
mean
increase in shoot
day
aphid
significantly decreased with water
extension rate per
was
-A
not
of
significantly affected by
plants, however,
mean
stress. In
length
well as mean
as
and uninfested
(-A) plants
Exp. 4, the growth of +A plants
the different water stress treatments, in the
increase in shoot
significantly between
per day decreased
(+A)
infested
the
length and
mean
extension rate
mildly and moderately
1 stressed
treatments.
Although plant size
that of
Exp.
1
at the beginning of Exp. 3 (mean of 45 cm) was similar to
(mean of 42 cm) and Y^, within treatments were more or less
similar, growth parameters of the plants
(see Table 10)
3
in
was
general
were
different. Plant
smaller than in
Exp.
1
growth
in
Exp.
Table
(see
2).
Uninfested well-watered
plants grew on an average 20 cm or 0.25 cm/day
less in Exp. 3 compared with Exp. 1 (comparisons were made at day 40, data
shown). The average difference in plant growth between Exp.
not
3 for the moderate and severe stress treatments
and 40
cm or
In both
0.85
(+A) plants were
not
significantly different (P
was
growth of individual plants
Exp.
cm/day
the
growth
The effects of soil
drying cycle
Exp.
<
0.05), except for those growing
growth of -A plants under
4. The
decreased with the build up of water stress in
of shoots to intermittent
presenting
A
1.00
higher than that of +A plants (see Table 10).
the soil and increased again after
day
cm or
cm/day, respectively.
conditions of mild stress
per
50
experiments, the growth of uninfested (-A) and with aphid infested
under conditions of mild water stress in
The
was
1 and
watering.
The reaction of the extension rate
of the soil is
drying
pattern of two Mod. 2 stressed
drying and rewatering
on
pictured
in
Fig.
15
by
plante.
plant growth
were
very obvious.
in the Mod. 2 stressed treatment decreased the extension rate
of shoots
on
by at least 0.5 cm/day depending on the level of water stress and
plant size. More severely stressed plants showed higher reductions than
less severely stressed plants (not all data shown). As time progressed,
growth rates generally decreased. Plants increased in size and the limited soil
volume became
an
additional constraint to plant growth. In Exp. 4,
infested plants stopped
growing
at the end of the
high aphid densities rather than from
uninfested and with
aphids
infested
aphid
experiment suffering from
water stress
(comparison
single plants; Fig. 15).
between
75
moderately 2 stressed
+ Aphids
CD
c
°
X
UJ
o
0_
w
10
20
P^
o\
"5 {-
moderately 2 stressed
Aphids
4
—
3
2
C
O
(U-w
1
X
0
LU
30
(days)
Time
0.0
o
-O.h
0.
2
—
-1.0
o
^OT
-1.5
-2.0
10
20
Time
o
Fig.
15.
(days)
gypsum block at 14
cm
soil depth
Extension rate per day of shoots in relation to the development of
water stress in the soil
(- Aphids) and
conditions of
one
(Y^).
with
Shown
are
examples
of
one
uninfested
aphid infested plant (+ Aphids) grown
moderately
2 water stress in
Exp.
4.
under
76
Internodal length. In Exp. 3,
plants
(1.87
P
<
was
significantly
±SE
cm
=
0.08)
(0.98
±SE
cm
=
0.17) than in well-watered
severely stressed plants (1.21
and in
0.05). A similar trend
internodal length of moderately stressed
mean
smaller
also observed in
was
Exp.
±SE
cm
4: with
increasing
intensities of stress, internodal lengths first decreased, but increased
plants (data
from Mod. 1 to Mod. 2 stressed
at low intensities of water stress stem
suggest that
to a
greater
production
In
At
production.
high
shown). These
elongation
restricted
was
however, leaf
water stress,
decreased and was reflected in an increase in
strongly
length.
no
difference in internodal
(-A) plants
was
measured
well-watered and under conditions of mild water stress
(difference
became
cm). With
of 0.37
an
insignificant (difference
increase in stress
of 0.06
Leaf area. Means of the total leaf
the leaf
area
Exp. 3,
was
observed. Plants
aphids had significantly shorter intemodes than
infested with
In
again
results
length between aphid infested (+A) and
(data not shown). In Exp. 4, however,
significant difference in internodal length between +A and -A plants under
Exp. 3,
uninfested
a
extent than leaf
was
internodal
not
0.16;
=
of the additional
mean
significantly higher
total leaf
area
growth
in
of
plants
4
Exp.
treatments, although
a
was
Exp. 3 and of
at harvest in
are
presented
in Table 11.
of well-watered, +A and -A
area
plants
cm).
than that of water stressed
difference in leaf area
intensity
-A
this difference
plants.
In
Exp. 4,
plants
no
was
significant
plante of the different
from well-watered/mildly
observed among -A
decrease
in
leaf
area
plante was observed. The
probably partly due to the variable harvest
stressed to Mod. 1 and further to Mod. 2 stressed
high variability observed
was
also
area between the two moderately stressed
registered, although plant growth (increase in shoot length;
dates. A difference in leaf
treatments
see
Table
was
10)
was
slightly lower for the Mod.
treatment. This
suggested
expansion than
leaf
1
that water stress had
production
and stem
compared with the Mod.
a
greater effect
elongation.
on
leaf
2
area
77
Table 11.
Leaf area of plants grown under well-watered (control) and water
stressed conditions at harvest in Exp. 3 and Exp. 4. In Exp. 3, total
aphid infested (+A)
separately *. In Exp. 4,
of uninfested (-A) plants was
parenthesis) are shown °.
leaf
area
of
determined
Experiment
3
Total leaf
s
Treatment
Moderate
Severe
(-A) plants
of the increase in
area
measured
.
Means
±
were
growth
SE (in
Experiment 4
reafcm2)
+A
Control
and uninfested
leaf
Leaf area
Treatment
-A
880.8 a
1135.9 a
(±91.3)
(± 108.9)
544.4 b
620.7 b
(± 59.4)
(± 105.1)
527.6 b
664.0 b
(± 62.2)
(± 82.0)
(cm2)
-A
Control
494.2
x
(±78.1)
Mild
499.1
x
(± 70.5)
Moderate 1
421.5
X
(± 66.2)
Moderate 2
312.1
x
(±60.7)
+A
A
-
plants:
plants:
mean
of 3
means
(P
S
of 6
mean
of 5
replicates (except moderately stressed: 5 replicates)
replicates (except severely stressed: 4 replicates)
replicates (except moderately 1 stressed: 2 replicates)
by the same letter are not significantly different
in a column followed
0.05).
Plant biomass
decreased
mean
production. In Exp. 3, fresh and dry weight of plants
significantiy with
water stress
well-watered plants (+A and -A
water stressed
plants)
(Table 12). Fresh and dry weight of
was
almost twice
as
high
as
that of
plants. Water stressed plants had on average 6% lower tissue
plants. Reductions in water content between
water content than well-watered
well-watered and water stressed
(data
not
shown).
In
general,
plants were greater
12.5%) than of leaves, irrespective of
Although in Exp.
3 the fresh and
lower than in uninfested
plants
plants, but the
infested
with -A
in stems than in leaves
the water content of stems
was
lower
(4.5-
treatment.
dry weight of aphid infested (+A) plants was
(-A) plants, differences were not significant. Aphid
slightly higher tissue water content compared
overall difference was again insignificant.
tended to have
78
In
Exp. 4,
the decrease in mean fresh and
dry weight between plants grown
under well-watered and water stressed conditions was
significant for +A
plante. Well-watered plants had twice as high fresh and dry weights
compared with water stressed plants. Fresh and dry weights of -A, Mod. 2
stressed plants were significantly lower than that of well-watered plante. Plant
yield parameters of aphid infested and uninfested plants in Exp. 4 were not
compared due
to considerable differences in the harvest date.
Shoot fresh and
Table 12.
dry weights as well as shoot water content of aphid
(+A) and uninfested (-A) plants under well-watered (control)
a
and water stressed conditions in Exp. 3 and Exp. 4 b. Means ±SE (in
shown.
In
are
values
are of total shoot, whereas
parenthesis)
Exp. 3,
in Exp. 4 values are of the additional increase in shootc.
infested
"
fresh
Treatment
weight (g)
|
+A
dry weight (g)
-A
|
+A
-A
Experiment
Control
Moderate
Severe
41.85
a
64.25 a
63.78 a
(± 1.37)
(± 1.83)
(± 0.69)
(± 0.35)
18.93 b
21.94 b
7.745 b
8.99 b
59.24 b
58.02 b
(± 2.54)
(± 4.58)
(± 1.09)
(± 1.73)
(± 0.84)
(± 1.49)
18.91 b
21.40 b
7.88 b
9.44 ab
57.95 b
55.97 b
(± 2.76)
(± 3.74)
(± 1.80)
(± 1.69)
(± 1.59)
(±0.19)
x
8.26 y
Mod. 2
a
19.15
x
(± 2.24)
17.80
x
(± 2.39)
(± 2.66)
12.50
a
15.09
8.55
x
(± 0.57)
4
6.97
x
(± 0.74)
58.22
X
(± 0.65)
63.47
x
(± 0.62)
3.18 y
6.39 xy
61.48 y
64.27
(± 0.92)
(± 1.06)
(± 0.14)
(± 0.80)
x
6.59 y
15.13 xy
2.53 y
5.62 xy
(± 0.97)
(±2.15)
(± 0.43)
(± 0.92)
61.87y
(± 0.97)
(± 0.80)
7.59 y
11.04y
(± 0.78)
2.99 y
4.14 y
60.65 y
62.46
(± 0.72)
(± 0.30)
(±0.19)
(± 0.43)
(±1.83)
+A
3
(± 5.32)
(±1.32)
Mod. 1
-A
(± 3.59)
20.46
| Mild
|
+A
(%)
34.86 a
Experiment
Control
water content
plants:
plants:
mean
of 6
mean
of 5
62.97
x
x
replicates (except moderately stressed: 5 replicates)
replicates (except severely stressed: 4 replicates)
mean of 3 replicates (except Mod. 1 stressed -A plants: 2 replicates)
means in a column followed by the same letter are not significantly different
(P £ 0.05).
-
A
79
In contrast to
Exp. 3, the
in +A than in -A
water content of
plants. Higher
plante
content in well-watered, +A
caused by
an
fresh and
as
dry weights
compared
artefact: well-watered, +A
aphid honeydew,
plant tissue
plants
not all of which could be
was
to -A
were
significantly lower
and lower tissue water
plants
were
probably
completely covered with
wiped off before plants
were
weighed.
Plant water relations. Soil matric
potentials (Y^)
were
positively correlated
components of leaf water potential (Y, Y0, Yp). In Figs. 16 and 17,
all readings of Y, Y0 and Yp assessed at harvest in Exp. 3 and Exp. 4 were
with the
plotted against corresponding Y^ and regression lines
As in
Exp.
1 and
Exp. 2,
Y
(measured predawn and
were
at
fitted.
midday) correlated
midday; Exp. 4: r-0.45
extent of decrease in Y0 with decreasing Y^ was
more or less similar to that measured in Exp. 1, although the decrease in Y
was more steep in Exp. 1 than in Exp. 3 (comparison of slopes (b) in both
experiments; see Figs. 7 and 16). In Exp. 4, the decrease in Y0 was not as
distinct as in Exp. 3: a steep decrease in Y0 to maintain Yp above a critical
Y^, (Exp.
predawn). In Exp. 3, the
3: r=0.82
best with
value was not necessary, since
as
In
in the other
Exp. 3,
and at
Y^, did
not reach as severe stress intensities
experiments.
the componente of
midday.
predawn,
r=0.83
The
slopes
plant water potential
of decrease
(b)
were
determined predawn
in the components of leaf water
water potential were very similar, whether
midday (see Fig. 16). However, the intercepts
potentials with decreasing soil
measured predawn
or
at
of the regression lines were different Leaf water potentials (Y)
midday were on average 0.78 MPa lower than Y measured
predawn (Fig. 16 and Table 13). Average Y0-values at midday, however,
were only 0.16 MPa lower than at predawn. Therefore, Yp at midday was on
average 0.62 MPa lower than at predawn. Predawn Y and Y0 correlated well
with midday Y (r=0.79, P<0.001) and Y0 (r=0.93, P<0.001), respectively,
whereas Yp did not (r=0.34, P<0.01).
("heights*)
measured
80
3
CO
o
c
CD
c
2
Q.
o
E %
O
O
Predawn
1
-$-
%
2
w
D
<D
CD
'+*
£
—
a
cd
c
a>
P<0.05
R =0.08
y=1.05+0.07x
J-4
o
*
H
0
a
y=-0.68+0.33x
R =0.68
P<0.
-1
-2
(D
-3
o
-4
-4
y=-1.73+0.26x
R =0.54
i
i
i
-3
-2
-1
0
Soil Matric Potential
3
co
»
c
2
CD
a
E i
o
o
y==0.45+0.09x
1
D
CO
QJ
c
<D
o
a>
—
-i-*
0
A
y==-1.43+0.35x
R2=0.70
P<0.001
-1
i
o
o-
P<0.01
t*—0-42—-*^H*-i
<F*
2
w
R2=0.12
-2
l^-^BSS
o
1_
CD
-3
0
o
o
-4
-4
R2=0.59
y=-1.88+0.27x
i
i
-3
-2
Soil Matric Potential
Fig. 16.
(MPa)
Midday
C
Q-
P<0.001
i
o
Osmotic Potential
0
Turgor
1
SD of values with soil matric
a
P<0.001
i
i
-1
0
(MPa)
Leaf Water Potential
Pressure
potential
>
—0.1
MPa
Predawn and midday leaf water (Y), osmotic (Y„) and turgor
potentials (Yp) of apple plants in relation to soil water potentials (Y^,)
in Exp. 3. Regression equations, R2- and P-values are given.
81
3
co
<•
+j
c
cu
c
O
a
predawn
^-N
o
o
O
co
CD
'-^
£
CD
-M
ns
0
2
w
—
C
R =0.07
1
E %
o
y=1.26+0.13x
2
O
CD
_J
O
°-
0
a
-1
R
y=-0.79+0.23x
P<0.01
.
£
=0.2^0
_A_
_
i
A*
A
A
o
-2
o
1_
<D
-3
O
o
y=-2.05+0.11x
-3
R =0.09
I
I
-2
-1
0
(MPa)
Soil Matric Potential
Fig.
17.
ns
I
-4
o
Osmotic Potential
o
Turgor
a
Leaf Water Potential
Pressure
Predawn leaf water (Y), osmotic (Y0) and turgor potentials (Yp)
apple plants in relation to soil water potentials (Y^i) in Exp.
Regression equations, R2- and P-values are given.
Relating Y0
and
Yp
of uninfested and with
aphid infested plants
of
4.
measured at
harvest in the three treatments with respective Y also demonstrated the
ability
of plants to adjust osmotically. In Figs. 18 and 19, Y0 and Yp were
plotted against Y, and regression lines for each treatment fitted and R2-
values calculated. In Fig. 18, +A and -A plante
were
examined
separately.
In both experimente, Yp of water stressed plants could be maintained at
higher values at decreased Y than Yp of well-watered plante. This was due
to a
steeper decrease in Y0 with decreasing
generally
lower
Y0 (lower intercept)
Y
(steeper slope)
and/or to
in water stressed than in well-watered
plants. Measurements of the componente of plant
water
potential
in both
experimente suggested that in uninfested plante grown under low levels of
(i.e. mildly stressed in Exp. 4 and moderately stressed in Exp.
3), Yp maintenance was not only due to generally decreased Y0 (due to
active osmotic adjustment) but also due to a steeper decrease of Y0 with
water stress
declining Y, indicating
an
inaease in tissue elasticity.
82
1.6
D
C
CU
-H
1.2
*~^
O D
Q.Q.
,_
0.8
2
Ow
0.4
?
3
h-
0.0
-1.0
o
-1.5
-M
c
cu
-?.o
o P
Q.0O
s
w
-2.b
-*j
o
F
-3.0
CO
O
-3.5
Leaf matric potential
Control +A
Severe +A
Moderate +A
Moderate —A
Control —A
Fig. 18.
(MP)
Predawn leaf osmotic
Severe —A
(Y0) and turgor (Yp) potentials in
relation to leaf
(+A) and uninfested (-A) apple
plants grown under well-watered (control), moderately and severely
water stressed conditions in Exp. 3. For illustration purposes symbols
have been removed. The regression equation for each treatment and
corresponding Ft2- and P-values are shown below.
water
potentials (Y)
Treatment
Leaf osmotic
of
aphid
infested
Equation
potential (y) as related
Revalue
to leaf water
P-value
potential (x)
Control +A
y
=
-1.23
0.47
x
0.17
ns
Control-A
y
=
-157 +0.06
x
0.12
ns
Moderate +A
y
=
-1.38
0.62
x
0.14
ns
Moderate -A
y =-1.40 +0.82
x
0.58
<0.01
Severe +A
y =-1.43 +0.61
-1.99+ 0.25
y
x
0.85
x
0.44
Severe -A
+
+
=
<
0.001
ns
Leaf turgor pressure (y) as related to leaf water potential (x)
<0.1
051
1.23 +0.53 x
Control +A
y
=
Control -A
y =1.72 +0.94
x
0.73
Moderate+A
y
=
1.38+ 0.38
x
0.06
ns
Moderate -A
y
=
1.40 +0.18
x
0.06
ns
Severe +A
y =1.43 +0.39
x
0.71
Severe -A
y
1.99 +0.75
x
0.87
=
<
<
0.001
0.001
<0.01
83
2.0
-v
«
c
+J
1.5
-•>
1.0
.
y=2.10+1.12x
y=1.79+0.67x
y=1.56+0.51x
R =0.48
P<0.05
R_=0.49
P<0.05
R =0.50
P<0.05
o
° p
Q.Q-
o
-
°
«
o
R2=0.65
y==1.84+0.60x
-2.5
-2.0
^^"^
„
V
'
i
V
"
-»
0.5
I
y°°
,J^t^^^ "v
a
0.0
V
*
i
i
-1.5
-1.0
P<0.01
I
-0.5
-1.0
v
-1.5
c
^
o
»
„°
-2.0
y=-2.10-0.12x
y=-1.79+0.33x
y=-1.56+0.49x
R2=0.01
ns
R,=0.19
ns
R =0.48
P<0.05
r
Q.Q-
-2.5
o
E
-3.0
O
y=-1.84+0.40x
o
CO
\1
-3.5
-2.5
-2.0
Leaf motric
Control
Fig. 19.
Mild
o
R =0.45
P<0.05
I
I
L_
-1.5
-1.0
0.5
potential (MP)
°
Mod. 1
o
Mod. 2
Predawn leaf osmotic
(Y0) and turgor (YP) potentials in relation to leaf
potentials (Y) of uninfested apple plants grown under wellwatered (control), mildly, moderately 1 and moderately 2 water
stressed conditions in Exp. 4. The regression equation for each
treatment and the corresponding R2- and P-values are shown.
water
Since, at harvest, the components of plant water potential in Exp. 3 and Exp.
4 were measured at the
peak
of
a
drying cycle, mean Y, Y0 and Yp at
regimes could be calculated
maximum water stress in the different water
(Tables 13 and 14). In both experimente, Y^-values at harvest were
significantly different between the different water regimes (treatments),
although variability within each category
was
high.
84
Table 13.
Predawn and midday leaf water
(Y), osmotic (Y0) and turgor
potentials (YP) as well as their corresponding soil matric potentials
(Y^) of aphid infested (+A) and uninfested (-A) apple plants grown
under well-watered (control), moderately and severely water stressed
conditions measured at the peak of drying cycles at harvest in
Exp. 3 *. Means ±SE (in parenthesis) are shown b.
I Treatment
|
<P(MPa)
I
*0(MPa)
9V (MPa)
predawn
+A
Control
Moderate
Severe
-A
+A
I
*«*
(MPa)
+A
-A
-0.64 a
-0.79 a
-1.53 a
-1.77 a
(± 0.06)
(± 0.05)
(± 0.07)
(± 0.03)
0.89
-A
a
(± 0.07)
0.98 b
(± 0.05)
-0.01
a
(±0.00)
-0.71 a
-0.88 a
-1.82 b
-2.09 b
1.11 b
154 8
-0.69 b
(± 0.03)
(±0.06)
(± 0.05)
(±0.05)
(±0.05)
(± 0.03)
(±0.04)
-1.51 b
-1.60 b
-2.35 C
-2.39 C
0.84 a
0.79C
-2.43C
(±0.10)
(±0.10)
(±0.06)
(±0.04)
(±0.04)
(±0.08)
(±0.15)
midday
Control
-156x
(± 0.05)
Moderate
-1.73 y
(± 0.07)
Severe
-2.24
z
(±0.08)
A
means
(P
In
-1.69 X
•1.93
(±0.05) 1 (±0.05)
-1.77 y
I
-2.04 y
-2.40 z
1
-2.53
S
Exp. 3,
in
a
column followed
0.30
(±0.06)
-2.52
Z
I (±0.07)
same
x
(± 0.09)
0.29
Z
(±0.06)
by the
x
(± 0.05)
-255 y
(±0.07) 1 (±0.06)
(±0.05)
0.43
x
(± 0.03)
plants, number of replicates: control=15,
plants, number of replicates: control=19,
+A
-
-1.46 X
1
X
(±0.06)
0.46 X
(± 0.06)
-0.01
x
(± 0.00)
0.49 X
-0.69 y
(± 0.07)
(±0.04)
0.13 y
(±0.03)
-2.43
Z
(±0.15)
moderated 2, severe=12
moderated 3, severe=6
letter
are not
significantly different
0.05).
a
significant reduction
in
predawn
Y was measured between well-
watered/moderatefy stressed and severely stressed plants. Predawn Y0
decreased significantly with each increase in intensity of water stress. This
resulted in significantly higher Yp in moderately stressed plants compared
with the other two treatments. Both Y and
Y0, when measured at midday
significantly with increasing intensities of water stress and were
significantly lower than at predawn (P <, 0.05). Leaf turgor pressure of water
decreased
stressed
plante measured
of well-watered
at
midday
was
plants (exception: severely
not
significantly
water
different from that
stressed, uninfested plante).
85
The components of
plant water potential of aphid infested (+A) and uninfested
(-A) plante in Exp. 3 were affected differently by soil water stress. Uninfested
plante under well-watered and moderately stressed conditions had
significantly lower Y and Y0 than +A plante (mean difference in Y=0.14 MPa
and in Yo-0.20 MPa, P s 0.05; see Table 13). Turgor pressures, particularly
under moderately water stressed conditions, were higher in -A than +A plante
(mean difference in Yp=0.10 MPa). in severely stressed plante, significant
differences in Y, Y0 and Yp between +A and -A plants were not observed.
Predawn leaf water
Table 14.
well
(-A)
as
their
apple
(Y), osmotic (Y„) and turgor potentials (Yp) as
corresponding soil matric potentials (Y^) of uninfested
plants grown
under
well-watered
(control),
mildly,
moderately 1 and moderately 2 water stressed conditions measured
at the peak of drying cycles at harvest in Exp. 4; n indicates number
of replicates. Means ±SE (in parenthesis) are shown *.
Treatment
n
Control
12
Mild
12
Moderate 1
9
Moderate 2
means
(P
In
£
Exp. 4,
9
in
a
Y
(MPa)
-0.64
-2.03
a
(± 0.08)
1.39 a
-O.ooa
(±0.12)
(± 0.00)
-1.02 b
-2.13 ab
1.11b
-0.69 b
(± 0.07)
(± 0.06)
(± 0.07)
(± 0.072)
-1.15 b
-2.12 ab
0.97 b
-1.20C
(±0.11)
(± 0.08)
(± 0.08)
(± 0.10)
-1.17 b
-2.31 b
1.14 ab
-1.60d
(±0.11)
(± 0.07)
(± 0.09)
(± 0.20)
column followed
by
the same letter
are not
significantly different
plants was significantly higher than in
plants (Table 14). Significant reductions in Y0 were observed
Y of leaves of well-watered
between well-watered and Mod. 2 stressed
significantly
aphid infestation
experiment.
the effect of
plants only. Leaf turgor pressure
reduced between well-watered and water stressed
Since components of plant water potentials
in this
a
(± 0.07)
Ysoil(MPa)
0.05).
water stressed
was
YD(MPa)
Y„ (MPa)
on
were
plante.
measured only in -A plants,
plant water relations could
not be examined
86
Effects of Water Stress
3.3.3
on
Development and Growth
In
Fig. 20, the size of aphid populations
weights,
after 22
regimes in Exp.
days
3.
of
development,
of
well
their total fresh and
dry
plotted against the different water
as
are
Aphid Populations
as
Populations which had developed on the upper parts of the
A (10th leaf counted from the apex at the beginning of
plants, i.e. above leaf
the
experiment),
are
shown
separately from those which had developed
on
the lower parts, i.e. below leaf A.
Aphid populations which developed
Further,
the
on
well-watered plante, whether
on
the
significantly larger
plants.
aphid populations with an increase in
intensity of water stress was observed. The decline in an aphid population
upper
lower parts,
or
a
decline from
moderately stressed plants
moderately
in soil matric
severe
in the size of
slight decrease
from well-watered to
potential
treatment
than on water stressed
were
to
was
much steeper than the
severely stressed plante, although the bigger drop
between the moderate
was
(Ysoi,= -2.4 MPa).
-0.7 MPa) and the
suggested that a critical
(Y^p
This observation
moisture level for aphid development existed between the well-watered and
the
As in
the
stressed treatment, below which the
moderately
populations
Exp.
plant
1
severely impaired.
and Exp. 2, aphid development
development
differed. The size of
the upper parte,
an
particularly
on
the upper and lower
aphid population
of well-watered
was
aphid
Hence population size
was
by the feeding position
to dominate at
plante, compared
with the lower
size between treatments and/or between
water stress.
affected both by the water supply level
in a
high levels of
Aphid densities of
parte of
significantly larger on
population
position in the plant, decreased with increasing intensities of
parte. The difference in
and
of
was
(treatment)
plant (leaf age), but the former effect tended
water stress.
upper and lower
parts of plants grown under different
length (cm) or per leaf. On the
plants, aphid density amounted to 52.5 aphids/cm
shoot length (or 104 aphids/leaf), of moderately stressed plants to 21.5
aphids/cm shoot length (or 42 aphids/leaf) and of severely water stressed
water
regimes
were
calculated per unit shoot
upper parte of well-watered
to 13.0 aphids/cm shoot length (or 28 aphids/leaf). These differences
aphid densities on the upper parte of the plante were significant between
well-watered and water stressed plants (P < 0.05). On the lower parte of the
plants
in
plante, aphid densities amounted
aphids/leaf)
on
well-watered
plante,
to 30
aphids/cm shoot length (or
to 14.5
to 47
aphids/cm shoot length (or to 22
87
CO
Q.
O
3500
Y//A upper
3000
m
2500
J
lower
parts
parts
standard
error
2000
CU
E
c
"5
1500
1000
500
ML\
*->
o
0
600
E
500
400
gi
"co
$
-C
CO
CO
300
200
100
0
CONTROL
MODERATE
I
Y//A upper
Hi
T
lower
SEVERE
parts
parts
standard
error
i
fc_jfc.
CONTROL
MODERATE
r*n;
I
SEVERE
300
C7I
E
Y//A upper
250
|^|
T
200
lower
ports
parts
standard
error
150
'cu
s
100
a
50
0
.
i
JlS.
CONTROL
MODERATE
If7f hlMIH—
SEVERE
Treatment
Fig. 20.
Size
dry weights of aphid populations feeding on
(control), moderately and
severely water stressed apple plants collected after 22 days. Upper
parts of the plant refers to plant parts above leaf A (10th leaf counted
from the apex at the beginning of the experiment); lower parts refers
to parts below leaf A. Means (6 replicates) labelled by the same letter
are not significantly different (P £ 0.05).
as
well
as
fresh and
the upper and lower parts of well-watered
88
aphids/leaf)
8
on
aphids/leaf)
moderately stressed
and to 5.0 aphids/cm shoot length (or to
severely stressed plante. The differences in aphid density
on
per leaf on the lower parts of the
and water stressed
lower
parts
of the
plante (P
plant,
<
plant were significant between well-watered
0.05). Aphid density, whether
tended to decrease with
the upper
on
or
intensity of
increase in
an
water stress.
Aphid density
number (r=0.81,
density
plant correlated positively
the upper parte of the
on
P<0.001)
as
well
as
shoot
with leaf
length (r=0.82, P<0.001). Aphid
the lower parts did not correlate with shoot
on
On the upper
as
well
as on
the lower
length or leaf number.
parts of the plant in Exp. 3, individual
body weights of aphids correlated positively (and highly) with aphid density
(r=0.75, P<0.001): the higher the observed aphid density, the heavier tiie
aphids, probably indicating that both effects
nutritional
the result of the same
were
cause.
By dividing fresh and dry weight of the different aphid stages of development
by
the
weight
of individuals, mean body fresh and dry
aphid Individuals under well-watered and water stressed
were calculated (Table 15). In Table 15, body weights of aphids
corresponding number
of
conditions
collected from the upper parte of the
counted from the apex at the
plants,
beginning
(10th leaf
i.e. above leaf A
of the
experiment),
shown
are
separately from those collected from the lower parts, i.e. below leaf A.
Under water stress conditions,
stages
were
mean
significantiy lower, both
plant, compared with well-watered
conditions,
mean
aphid body
Aphid body weights
on
significantly higher
weights decreased with
than
Carroll and
body weights of the apterous aphid
on
the upper and lower parte of the
conditions. Under
increasing
water stress
weight tended to decrease further.
the
upper
parts of well-watered plants
(P
0.05). This difference in body
on
the lower parts
an
increase in intensities of water stress.
£
were
Hoyt (1986) reported medium birth weights of 20-28 ug for A.
pomi progeny of apterae reared at 20°C. The authors also
apterae weight
of 0.712 mg
on
growing
reported
leaves and of 0.580 mg
on
an
mature
leaves. In
Exp. 3 of this study, the weights of apterae feeding on well-watered
plante (upper and lower parts) were lower than reported by Carroll and Hoyt
(1986). This reduction is probably explained by the higher ambient air
temperatures of 23-24°C reached in the present study (at midday) compared
with 20°C utilized
by Carroll and Hoyt. Fresh weights of A. pomi reported by
89
Body fresh and dry weights of aphid individuals in the different stages
of development feeding on the upper and lower parts of well-watered
(control), moderately and severely water stressed apple plants in Exp.
3. Upper parts of the plant refers to plant parts above leaf A (1 Oth leaf
counted from the apex at the beginning of the experiment); lower
parts refers to parts below leaf A. Means ±SE On parenthesis) are
shown a,b.
Table 15.
Fresh
Stage
weight (mg)
lower parts
upper parts
control
alatae
moderate
0.439 a
0592 8
(±0.045)
(±0.000)
severe
control
-
--
L3+L4
0.333 a
0584 8
0559 a
0.312
winged
(±0.015)
(±0.032)
(±0.018)
(±0.029)
x
moderate
severe
-
-
-
-
adults
0.642 a
0.357 b
0587 b
0.518
x
0574 y
0565 y
apterous
(±0.034)
(±0.039)
(±0.019)
(±0.036)
(±0.015)
(±0.017)
L3+L4
0.397
a
0.154 b
0.135 b
0.174 x
0.132 y
0.116 y
apterous
(±0.011)
(±0.020)
(±0.016)
(±0.016)
(±0.005)
(±0.005)
L1+L2
0.076 a
0.050 b
0.035C
0.048
(±0.005)
(±0.004)
(±0.002)
(±0.004)
X
0.040 xy
0.036 y
(±0.002)
(±0.003)
Dry weight (mg)
alatae
0.106 a
0.0818
(±0.012)
(±0.000)
-
-
L3+L4
0.092 a
0.079 a
0.083 8
0.096
winged
(±0.005)
(±0.007)
(±0.003)
(±0.008)
x
-
-
-
-
adults
0.176 a
0.115 b
0.101 b
0.153
x
0.098 y
0.092 y
apterous
(±0.011)
(±0.007)
(±0.009)
(±0.009)
(±0.005)
(±0.004)
L3+L4
0.104 a
0.049 b
0.043 b
0.055
X
0.040 y
0.038 y
apterous
(±0.004)
(±0.005)
(±0.005)
(±0.005)
(±0.004)
(±0.003)
L1+L2
mean
0.023 a
0.016 b
0.011 C
0.015
(±0.002)
(±0.001)
(±0.011)
(±0.002)
of 6
replicates
means in a row
(P
£
at 20°C/16°C
environmental conditions
0.50
-
0.014 xy
0.011 y
(±0.001)
(±0.001)
apterous steges only
by
the same letter
are not
significantly different
0.05).
(1993)
Rutz
for
followed
x
0.58 mg and 28
-
(sinuous day/night temperature curve, similar
in the study presented here) ranged between
ug for apterous adults and L1, respectively.
as
35
90
Aphids
significantly higher water contents (%) when feeding on the upper
had
plante compared with the lower parte, particularly
parts of
plants (P
0.05; data not shown).
<
on
well-watered
increasing
severely stressed
This difference diminished with
intensities of water stress and became insignificant
plants. The body size of aphids seemed
to be affected
on
by water stress and by
aphid feeding position in the plant.
Therefore, aphids appeared to react to
attaining
lower
upper parte of
water stress by reproducing less and
body weight. A range of body weights was observed on the
the plant, particularly on well-watered plante. It was noticed,
however, that the
positioned
of
an
on a
more severe
the water stress, the lower the
plant and the smaller the size and
aphid became. This
As demonstrated in
was
most
more
clearly observable
aphids
uniform the
on
adult
were
weight
aphids.
Fig. 21, analyzing aphid populations into their various
stages of development (L1+L2, apterous L3+L4, apterous adults, winged
days of development
after 22
A
(10th leaf counted from
on
an aphid population
parts of the plants, i.e. above leaf
alatae), showed the age distribution of
L3+L4 and
on
the upper
the apex at the
beginning of the experiment), and
the lower parts, i.e. below leaf A.
populations
The most obvious difference between
parte of the
plant was
in the number of
number of alatae and
winged
winged L3+L4
was
on
the upper and lower
forms. On the upper parte, the
higher and decreased with an
were only
increase in intensities of water stress. On the lower parte alatae
just starting
to
develop
on
plante.
aphid population
the well-watered
On the upper parte, the trend within
an
proportion of apterous L3+L4 and adults and
(and winged L3+L4)
L1+L2
parte,
with water stress
to increase the
(data
not
proportion of
shown). On the lower
significant increase in percentage apterous L3+L4 and
a
decrease in percentage L1+L2 with
was
was
to decrease the
observed. Aphids feeding
generation
time and/or
were
on
an
increase in
stressed
intensity of
plants had
most
a
significant
water stress
probably
a
longer
less fecund.
Exp. 3 was used in Exp. 4. In Fig. 22, the size as
weights of aphid populations were plotted against
the different soil water regimes. In contrast to Exp. 3, where aphid
populations remained for 22 days on the host, aphid populations in Exp. 4
had different lengths of developmental period. Aphids were collected when
A similar
well
as
approach
as
in
total fresh and dry
the host
plant stopped growing due
to a
high population density.
91
2500
parts
upper
of the
plants
2000
1500
1000
500
ADULTS
L3 + L4
ADULTS
winged
II
parts
of the
L3+L4
L1+L2
I
apterous
1000
lower
a
plants
800
600
HH
Control
P^|
Moderate
ES3
Severe
T
SE
400
lab
1
200
i^ £s
:°°
ADULTS
|
ADULTS
L3 + L4
winged
||
Aphid Stage
Age distribution
b
L3+L4
L1+L2
I
apterous
of
Development
aphid populations feeding for 22 days on the upper
(control), moderately and severely
water stressed apple plants in Exp 3 Upper parts of the plant refers
to plant parts above leaf A (10th leaf counted from the apex at the
in
and lower parts of well-watered
beginning of
the
experiment),
lower parts refers to parts below leaf A
(6 replicates) labelled by
different (P < 0 05)
Means
the
same
letter
are not
significantly
92
aphids
10000
of
mber
8000
6000
4000
nu
Total
2000
0
CONTROL MILD
MOD.1
M0D.2
CONTROL MILD
MOD.1
M0D.2
CONTROL MILD
MOD.1
M0D.2
1000
en
E
800
weight
600
Fresh
400
200
0
500
[mg)
weight
Dry
400
300
200
100
0
Treatment
Development
time
22.
(days)
37
25
20
25.3
a
b
b
b
as well as development time of aphid
populations feeding on well-watered (control), mildly, moderately 1
and moderately 2 water stressed apple plants (until host had stopped
growing). Means (3 replicates) labelled by the same letter are not
significantly different (P £ 0.05).
Size, fresh and dry weight
93
The
period of population development ranged between 20
depending
23
treatment
on
(well-watered: 35, 37,
days; mild
39
to 39
stress:
days
31, 21,
days; Mod.1 stress: 21,19,20; Mod.2 stress: 27,22,27 days). The
mean
plante was significantly higher than on
water stressed plante (P <. 0.05). Most notable was that the plante in
treatment Mod. 1 stopped growing first (20 days).
developmental period
well-watered
aphid populations feeding
The size of
significantly
on
smaller
on
well-watered
on
plante
water stressed
were
compared with stressed plante. The
significantly, were collected from Mod. 1
stopped growing first. Mean fresh and dry
plante
decreased
of
significantly between the well-watered
weights aphid populations
and Mod. 1/Mod. 2 water stressed treatmente. From both plant and aphid
smallest
populations, although
not
which also had
stressed
growth parameters, the Mod. 1 plante appeared
growth restraints than the Mod. 2 plante.
Aphid density (per
an
unit of shoot
increase in water stress. A
length
or
per
to be under more
leaf) tended
significant decrease
in
to decrease with
density
was
between the well-watered and the Mod. 1 stressed treatment
Aphid densities measured in the four treatments
were:
severe
(P
Control: 134
observed
£
0.05).
aphids/cm
(235.5 aphids/leaf); Mild: 97.5 aphids/cm (168 aphids/leaf); Mod.
aphids/cm (126 cm/leaf); Mod. 2:81 aphids/cm (141 aphids/leaf).
1: 69
Aphid density correlated positively with number of leaves (r=0.76, P<0.01)
and shoot length (r=0.62, P<0.05). However, these correlations were lower
compared with those in Exp. 3 indicating, that another factor beside plant size
was affecting aphid population development under the conditions of Exp. 4.
Body weights of aphid individuates correlated highly with population densities
(r= -0.84, P<0.01; exception: L2). In contrast to Exp. 3, this correlation was
negative. The higher the density of aphids in a population, the smaller the
body weight of individuals became, probably indicating that weight here was
being adversely affected by population size.
body fresh and dry weight of aphid individuals under
well-watered and water stressed conditions were calculated (Table 16). In
As in
Exp. 3,
contrast to
mean
Exp. 3, fresh and dry weight of the different stages of aphid
not decrease with increasing water stress. The body weight
development did
of
aphids tended
to increase with an increase in stress, were lowest on well-
watered plante and highest
significant, except
became
more
for L2,
distinct when
on
Mod. 1 stressed
Table
plants (differences
were
These differences among treatmente
16).
dry instead of fresh weights
see
were
compared.
94
Body fresh and dry weights of aphid individuals in the different stages
development feeding on well-watered (control), mildly, moderately
1 and moderately 2 water stressed apple plants in Exp. 4. Means ±SE
(in parenthesis) are shown a,b.
Table 16.
of
Fresh we ight
Stage
control
mild
(mg)
moderate 1
moderate 2
0.198 b
0.225 ab
0.252 a
0224 ab
(±0.006)
(± 0.020)
(±0.014)
(±0.019)
L3+L4
0.220 b
0250 ab
0.304 a
0.263 ab
winged
(±0.017)
(±0.027)
(± 0.012)
(±0.005)
alatae
I
adult
0.257 b
0.384 ab
0.441a
0.387 ab
|
apterous
(±0.017)
(±0.056)
(±0.036)
(±0.044)
L4
0.165 b
0.221 ab
0257 a
0270 a
apterous
(±0.011)
(±0.016)
(± 0.008)
(± 0.029)
L3
0.113C
0.120 be
0.153 a
0.149 ab
apterous
(±0.003)
(±0.010)
(±0.007)
(±0.015)
L2
L1
0.055 a
0.068 a
0.078 a
0.080 a
(± 0.004)
(± 0.007)
(± 0.003)
(±0.016)
0.021 b
0.028 ab
0.033 a
0.029 ab
(± 0.002)
(± 0.004)
(± 0.004)
(±0.003)
Dry weight (mg)
alatae
0.073 c
0.079 be
0.096 a
0.091 ab
(± 0.004)
(± 0.003)
(± 0.008)
(± 0.005)
L3+L4
0.073 b
0.076 b
0.093 a
0.086 a
winged
(± 0.004)
(± 0.004)
(± 0.002)
(± 0.002)
adult
0.091 b
0.119 ab
0.138 a
0.125 ab
apterous
(± 0.004)
(±0.013)
(±0.014)
(± 0.014)
L4
0.055 b
0.068 b
0.082 a
0.086 a
apterous
(±0.003)
(± 0.003)
(±0.003)
(±0.007)
L3
0.041 b
0.040 b
0.050 a
0.050 a
apterous
(±0.001)
(±0.002)
(±0.003)
(±0.003)
L2
L1
mean
of 3
means
In
0.020 a
0.023 a
0.025 a
0.028 a
(±0.001)
(±0.001)
(± 0.002)
(± 0.004)
0.008 b
0.009 ab
0.011 a
0.010 ab
(±0.00)
(±0.001)
(±0.002)
(±0.001)
replications
a row
followed
by
the
same
letter are not
significantly different (P
5
0.05).
95
The
body
treatments
or
well-watered than
on
began
to reach their
plants,
whereas
reached
stressed
favorable
in
size,
In
factor
main
in
particularly
on
those
on
population
water stressed
had
already
been
Population density
collapsing
determining body weight of aphid individuals
nutrition)
plants had stopped
into their various
Exp
populations
growing
which
3,
in
in
Exp
ADULTS
probably
as a
stages of development
populations
L3+L4
ADULTS
an
result of
as
aphid population
high aphid
densities
started off with two to three L4
4 started off with
a
predefined
L3
L4
winged
age structure
L2
L1
apterous
Aphid Stage
23.
a
Fig 23, showed the age distribution of
In contrast to
not
Exp 3, aphid populations only just
showed signs of
populations
and
presented
Fig.
among
development (data
of
aphid stages
4 the maximum size of
Analyzing aphid populations
instars,
significantly
not differ
did
aphids
plants
maximum
Exp
in
seemed to be the
after
of
among the different
The larval instars, however, tended to have lower water contents
shown)
(under
(%)
water content
of
Development
in aphid populations feeding on well-watered (control),
mildly, moderately 1 and moderately 2 water stressed apple plants
Age distribution
(until plants stopped growing)
by the same letter are
labelled
in
not
Exp
4
Means
significantly
(of 3 replications)
< 0
05)
different (P
96
Larval instars significantly decreased in number from well-watered to stressed
plants. The number of apterous adults significantly decreased only between
the well-watered and the Mod. 1 stressed treatmente. Alatae and winged
L3+L4 tended to decrease in number with an increase in water stress.
Except for L1 and apterous L3, the differences in the proportion of aphid
stages among treatments
tion of L3 in
higher
than
proportion
on
were not
populations feeding
on
of L1
Mod. 1 stressed
feeding
on
plante (16.1%
vs
plante
35.9%, P
shown). The propor¬
plante was significantly
not
well-watered
well-watered
plante (27.3%
Mod. 1 stressed
significant (data
on
vs
11.5%; P
was
£
0.05).
£
significantiy
The
lower than
0.05).
The trend in age distribution under water stress described for
Exp.
4 was
opposite to that observed in Exp. 3. Compared with the upper parts of the
plante in Exp. 3, populations in Exp. 4 had a lower proportion of L1 and L2
higher proportion of alatae, winged L3+L4, apterous L3 and L4 (data
shown). An explanation is almost certainly that aphid populations in Exp.
had not reached their maximum size, particularly those on well-watered
and
a
not
3
plante, whereas in Exp.
4 the
populations showed signs
of
main factor in
among
a
reached and
collapsing. Population density seemed
determining population age
Age distribution in
variable. One
maximum size had been
to be
a
structures.
population among replicates of a treatment were highly
for this variability is the observed variation in density
reason
replicates. Wennergren and Landin (1993) mention that variations
the local environment of insect herbivores, such as
crowding,
can
in
also
structure of populations. Moreover, towards the end of Exp. 4, a
of the large size apterous adults into the pot was
large
dispersion
very
observed (particularly in the well-watered treatment). This dispersion changed
change the
aphid populations on the plante: the proportion of adults and
newly born progeny (L1) decreased within a population. Comparably, Vehrs
et al. (1992) observed that most of the decrease in the Mvzus persfcae
(Sulzer) population was due to the high numbers of dispersing apterous
the structure of
aphids found in the
water bath below the
dispersal behavior by crowding
effects.
plante. The authors explained this
97
3.4
Discussion
3.4.1
Effects of Water Stress
In both
on
Plant
Development
experiments, growth (stem elongation and production of new leaves),
accumulation of fresh and
plante decreased with
dry weight as well as total leaf area of uninfested
(see Tables 10,11 and 12). In Exp. 3, a
water stress
critical moisture stress level for the
growth of uninfested plante was observed
(mean Y^ at harvest 0.00 MPa, range: -0.00 to
MPa)
moderately stressed treatment (mean xPsoi at harvest
-0.69 MPa, range: -0.46 to -1.43 MPa; see Table 13). In Exp. 4, the critical
moisture stress level for the growth of plante was observed between the
mildly (mean ¥„, -0.69 MPa, range: -0.18 to -1.60 MPa) and the Mod. 1
-1.20 MPa, range: -0.28 to -2.48 MPa; see
stressed treatment (mean Y^,
Table 14). Hence, the critical moisture stress level, below which the growth of
apple plante in pots under artificial environmental conditions was significantly
affected, developed below ¥- -0.65 MPa. Under conditions of intermittent
drying, i.e. those imposed in this series of experimente, however, it was
between the well-watered
-
and the
-0.07
=
-
-
difficult to define
growth
an
among other
exact critical moisture stress level. For
plant
parameters decreased with
stress within a treatment and increased
start a new
In the
study presented here,
In both
greater extent than
internodes
again when plante were rewatered
was
pF^
also
leaf production was not affected at
impaired with a further increase in stress
3 and 4, internodal
indicating that
stem
greatly
is a
to a
restricted to
a
production. Beyond this moisture level, leaf
strongly affected which was expressed by longer
for Exp. 3
<
-0.69 MPa and
^ for Exp.
was
4
<
-1.20
MPa).
A
Exp.
2.
observed in
to be associated with water stress
reported
significant reduction of the above ground biomass. Water stress
alters the biomass distribution of trees,
increasing
was
leaf
One of the traditional responses
plants
length decreased
elongation
similar reaction of internodal lengths to water stress
in
to
new
was
experimente
certain moisture level
production
example, plant
increase in water
drying cycle (see Fig. 15).
moderate stress levels but
intensity.
an
the root to shoot ratio
(Dorschner
decreasing
shoot
growth and
et al., 1986; Schnider, 1989;
Sritharan and Lenz, 1989; Steinberg et al., 1989; Honek, 1991; Buwalda and
Lenz, 1992). Under conditions of water stress, the production of new leaf area
is reduced
or
completely halted, thereby reducing
the
transpiring surface,
98
production
whereas root
is maintained
et al., 1989; Buwalda and Lenz,
(Sritharan and Lenz 1989; Steinberg
1992), favoring the search for
water. In
addition, direct effects of water stress
cause
on leaf area expansion may be the
photosynthesis and hence growth (Buwalda and Lenz,
for restricted
1992).
Different water
plant
water
regimes clearly affected the reaction of the componente of
potential to soil drying. At a certain stress intensity (e.g. Y= -1.00
MPa), Y0 in uninfested plants
watered plante (difference A in
turgor pressure of
lower in water stressed than in well-
were
Y0
water stressed
ca
0.45 MPa;
plante
was
values at decreased Y than in well-watered
decrease in
with
Y0
stressed than
decreasing
see
Figs. 18 and 19). Leaf
therefore maintained at
plants. This was due
Y and/or to a
generally
lower
well-watered plants. A steeper decrease
in
to
a
higher
steeper
Y0
in water
in
Y0
with
decreasing Y may indicate an increase in tissue (cell wall) elasticity, whereas
generally lower Y0 with declining Y are consistent with an active
accumulation of solutes, i.e. to osmotic adjustment to conditions of water
stress. Predawn measurement of the
experimente
indicated that,
namely
maintenance of turgor pressure
componente of
was
regimes,
a
potential
in both
due not only to
certain Y, but also to increases in tissue
water stress
water
in treatments with low stress intensities,
generally lower Y0 at a
(cell wall) elasticity. Under severe
distinct (active) osmotic adjustment seemed to take
place. These results support and clarify the conclusions of Davies and Lakso
(1979a) who suggested a combination of active osmotic adjustment and
increases in tissue
elasticity to
account for the
high drought tolerance of apple
trees.
Exp. 3, predawn Yp in moderately stressed plants was higher than in wellFig. 18 and Table 13), although average Y^, reached
levels
lower
significantly
(see Table 13). This was probably due to the fact
that at night, plant roots which had grown into still wet areas of the soil could
provide a temporary relief of the water stress for the plant, which was
reflected in only insignificant lower Y-values in moderately stressed compared
with well-watered plante (see Table 13). Since the moderately stressed plante
In
watered plante (see
had
adjusted osmotically, turgor
pressures were significantly higher in these
plante. Similar effects of temporary stress relief were
Exp. 4, where predawn plant Y and Yp of the three stressed
than in well-watered
also observed in
treatmente
were
predawn Yp
was
(see Fig. 19), although average Y^ of the
significantly different (see Table 14). Even though
very similar
different treatmente
were
maintained, the growth of plante in both moderately water
99
was reduced. This might be due to significantiy lower
midday Y of moderately stressed plante compared with well-watered plante.
In addition, changes in cell wall extensibility and the minimum turgor threshold
stressed treatments
growth may further decrease growth
for
Mathews et al., 1984 cf.
Steinberg
rates of water stressed
plants (e.g.
al., 1989).
et
In
Exp. 3, components of plant water potential measured at predawn gave
higher values than at midday (mean difference for Y= 0.78, Y0* 0.16, Yp=
0.62
MPa). Steinberg
et al.
(1989) reported that,
midday, Y0 of peach
by 0.5 to 0.8 MPa from
at
leaves under well-watered conditions had decreased
predawn values. Because this decrease was accompanied by a relatively high
the authors suggested that both active solute build-up as well as water
Yp,
loss from the leaf tissue had taken
place. Davies and Lakso (1979a) even
apple by as much as 1.65 MPa during
Y0
the day which they attributed to a combination of (active) osmotic adjustment
and tissue dehydration. In the present study, the decreases in Y0 determined
at midday, compared with predawn, were not very distinct and probably
mostly due to a concentration of solutes in plant sap by dehydration, i.e.
passive osmotic adjustment, rather than to an active accumulation of more
reported
a
decrease in
in leaves of
solutes, since leaf water contents
predawn (data
not
keep up
not
with the loss of water,
reduced leaf turgor pressures that
3.4.2
were
generally lower
at
shown). The decrease in osmotic potential
however, and this
were
was
midday than
at
at
midday could
reflected in the
observed.
Effects of Aphid Populations
Plant
on
Development
Growth (as measured by the increases in shoot length and number of leaves
as
well as fresh and
aphid infested (+A)
dry weighte, leaf
and uninfested
area, and the
plante (-A) did
length
of
intemodes)
not differ
of
significantly.
Growth parameters
were always smaller in infested than in uninfested plante,
however, and significantly so in the mildly water stressed treatment in Exp. 4.
Adding the production of aphid
biomass to the
did not alter these
since
relationships,
6.5% of the total biomass
control
production
production of plant biomass
aphid biomass accounted for less than
in the
system (even in heavily infested
plants).
These results show that under conditions of mild water stress
MPa)
an
besides
infestation with
water
stress.
aphids exerted
Whereas
an
additive stress
well-watered
plante
(Y^,
-0.65
>
the
plants
probably
could
on
100
compensate
feeding)
feedback of
great extent the "damage" (loss
to a
due to
even
high
densities of
in assimilates
aphids (stimulation by
by aphid
positive
a
additional
sink), plante under even mild water stress suffered
significantly reduced growth even when attacked by much smaller densities
of
an
aphids. Aphids drained from the plant assimilates which
osmotic
lower
adjustment to maintain growth
Y0
were
at low stress intensities.
in leaves of uninfested than infested
plante
needed for
Significantly
confirmed these
observations. This drain of assimilates needed by the plants
can also explain
higher critical moisture stress level, below which plant growth is
significantly reduced, in plants which were infested with aphids (Y^, > -0.69
the
MPa) compared with uninfested plante (-0.69 > Y^, > -1.2 MPa) in Exp. 4. At
high intensities of water stress, the differences in plant growth between aphid
infested and uninfested
plants decreased and became insignificant. This
be due to two "reasons" or
stress
with
a
combination of both:
(1)
With
an
can
increase in
intensity, the dominant limiting factor became
an
water stress and/or (2)
aphid population density
have affected plant development.
increase in intensities of water stress,
remained below the critical level that would
In addition, the loss in productive leaf area (photosynthetically active leaf
surfaces) due to leaf curling and honeydew production of +A plante could well
have affected plant growth. Since water stressed plants had lower aphid
densities, leaf curling and honeydew would have affected leaf area less.
The
aphids, depending
seemed to be
on
density
length
damaging on
as a feeding site and depends
of the infestation
period,
young tissue. Aphis pomi definitely
more
growing tissues
and
on
tissues to increase populations to great numbers
Lathrop, 1923; Cutright, 1930;
food from actively
(Baker
prefers
growing
and Turner, 1916;
Oatman and Legner, 1961;
Specht, 1972).
In
young trees, the ratio between growing and mature tissues is much higher
than in older trees; it follows that young trees should therefore suffer
more
than older trees.
Results of previous work concerning effects of A. pomi
trees
green
are scarce
on
the
growth of apple
and contradictory. Oatman and
apple aphid
reduced shoot
growth
of
Legner (1961) found that the
7-year-old "Red Delicious" and
"Cortland" apple trees. Hamilton et al. (1986) found that A. pomi did not affect
growth of terminal shoots
effect
on
A. pomi decreased the
slightly (due
al.
of mature "Red Delicious" trees, but had
mature "Golden Delicious" trees.
a
limited
Hugentobler (1990) reported that
growth of 1-year old "Golden Delicious" plants only
to reductions in leaf
(1992, 1993) reported
area) after 10 days of infestation. Kaakeh
that the accumulation of fresh and dry
et
weight in
101
leaves, lateral shoote, rootetock and roote of
Delicious"
months)
trees grown in
apple
were
negatively
year old "Redchief
one
pots during the first growing
(Patch.)
contrast, Vam and Pfeiffer (1989) reported that dry matter accumulation
by A+
not affected
(infestation period
spiraecola
materials and methods
40
-
(3-
season
affected bv A. pomi and Aphis spiraecola
days). Differences
(cuitivars, plant age, experimental
generalized conclusions difficult.
conditions
In
was
in
etc.)
among these studies make
In
Exp. 3, the componente of
potential
water
measured at
predawn and
at
as tissue water content) were lower in -A plants compared
plante (see Table 13). This difference became insignificant, however,
under severely water stressed conditions. Leaves of +A plante under well-
midday (as well
with +A
watered
and
populations
moderately stressed conditions maintained larger aphid
and densities, the leaves
were
therefore also covered with
more
This may well
plante.
viscosity
severely
large aphid populations with high honeydew production may
actually affect gas exchange between leaves and environment causing less
honeydew
than
of lesser
stressed
indicate that
and decreased photosynthesis. Many authors have
reported detrimental effects of honeydew on plant functioning (e.g. Cammed,
1981; Wood et al., 1988; Rossing and Van de Wiel, 1990; all cf. Hurej and
transpiration (higher Y)
1993), whereas experimente of Hurej and Van der Werf (1993)
on growth and yield when artificial honeydew was sprayed
on sugar beet. Decreased transpiration might also explain higher percentage
water contents of leaves in +A compared with -A plante in Exp. 3.
Van der Werf,
showed
In
no
Exp. 3,
effect
leaf turgor pressures
well-watered and
due to
generally
moderately
lower
which indicated that
to
adjust osmotically
Y0
an
(Yp) were higher in -A than
stressed treatments
at a
given
(see
in +A
Table
Y in -A than in +A
plants
in the
13). This
was
plante (see Fig. 18),
infestation with aphids may reduce the plants' ability
to water stress. In
addition,
a
steeper decrease of Y0
declining Y in water stressed compared with well watered plants was
only observed in leaves of -A trees. This probably indicates that tissue
with
elasticity in -A plants increased with increasing stress intensity, whereas in +A
plante, no changes in tissue elasticity occurred. The differences in Y0 and Yp
between +A and -A
plante decreased within
increasing intensity
of water stress.
Dorschner et al.
araminum
as
well as among treatments with
(1986) reported that in wheat plants subjected
(Rondani) and drought stress, the aphids
with plante subjected to drought
negative) Y0 compared
to Schizaohis
caused increased
(less
stress alone, i.e.
an
102
aphids reduced osmotic adjustment
infestation with
to
drought
stress.
and Van der Werf,
by aphids can be quite significant (Hurej
1993), and Riedell (1989) demonstrated that +A plants accumulate less
proline and glycinebetaine during a drought stress period than -A plante and
therefore an infestation with aphids limits the capacity of plants to adjust
Assimilate drain
successfully to drought
study
the present
stress
show that
(will
be discussed in section
aphids might impair
4). The results
of
turgor maintenance in water
stressed plants: (a) by decreasing the plants' ability to adjust osmotically,
and/or
(b) by possibly impairing
increases in tissue
elasticity under
water
stress.
In Exp. 4, aphid populations were allowed to develop until host plants stopped
growing. This density threshold for plant growth decreased with water stress,
and water stressed plants, therefore, had stopped growth earlier (after 20 25
-
plants (after 37 days), although aphid populations
developed more slowly under conditions of water stress. According to
Kieckhefer and Gellner (1992), aphid density thresholds for significant yield
days) than
in well-watered
loss differ with environmental conditions, plant and aphid genotype.
Effects of Water Stress
3.4.3
the
In both
experiments, plant growth (see Table 10)
and 22)
and densities of
intensities of water stress.
was
In
on
Population Developement
affected
Exp.
as
Aphids
well as the size
(Figs.
20
aphid populations decreased with increasing
Obviously, the development of aphid populations
by plant growth.
4 and on the upper
populations
of
parts of plants in Exp. 3, the size of aphid
length and
in leaf
r=0.95 between number of
aphids
and shoot
length;
between number of
aphids
and leaf
correlated well with the increase in shoot
number: e.g. in
Exp. 3,
P<0.001 and in
Exp. 4, r=0.88
Exp. 3, such
number;
correlation
was not
plante
of
found. This could be explained
young
growth rate, i.e. the production
tissue, is more important to the growth of aphid populations than the total size
P<0.001). On the lower parte of
in
a
if the
of the
plant The fact that the proportion of growing to mature tissue is higher
compared with large plants may be the reason that young plante are
in small
more
susceptible
to
an
infestation with
aphids than old plante.
103
Water stress generally affects plant growth by decreasing plant water
potentials, i.e. by reducing turgor pressure. It could be speculated that it is not
plant growth per se, but changes in turgor pressure that decreased the size
and density of aphid populations under water stress. Nevertheless, analysis
of the data revealed that
explain
the
changes
no
specific component of plant water potential could
in size
or
density of aphid populations.
Since on the lower parte of the plante in Exp. 3, neither plant growth nor
turgor pressure correlated with the decrease in the size and density of aphid
populations, probably the nutritional quality of leaves for aphids was
negatively affected by water stress. Even on the upper parts of plante some
leaf quality characteristics changed with water stress, since even here aphid
densities decreased with
an
increase in stress, in contrast, Dorschner et al.
(1986) showed that although the total number of aphids declined with
an
increase in water stress, the density of the infestation could increase on water
stressed wheat Most
with the type and
probably the
response of
intensity of water stress
aphids
and with
to water stress differs
aphid and plant genotype.
quality (assimilate production and transport) beside food quantity (plant
an important role in the development of aphid populations
(Atkinson, 1979; Honek, 1991) and becomes especially obvious when alatae
production and aphid size are considered. Leather (1989) reported that
Food
size) plays
suboptimal conditions manifested themselves by constraints in size and the
reproductive potential
In
of
apterae and by the production of alatae.
Exp. 3, the body size of aphids (fresh and dry weight) decreased with
water stress
(see Table 15) whereas in Exp. 4, aphid size increased with
water stress
(see Table 16). The difference between the two experiments was
that
aphid
densities in
probably had reached
plant). Variation
environment
Exp.
4 were much
their maximum size
in adult size is seen
(Cockburn,
1991
higher than in Exp. 3 and most
(past the carrying capacity of the
as a measure
of
coping
cf. Kindlmann and Dixon,
with
a
1992)
variable
or
as a
maximizing population growth (Kindlmann and Dixon, 1992)
under a particular combination of temperature and food quality (Atkinson,
1979; Dixon, 1985; Kindlmann and Dixon, 1992; Thomas, 1993). This is true
consequence of
Exp.
probably changed leaf nutritional quality and leaf
changes affected aphid body size negatively.
Further, food quality and availability were strongly influenced by aphid feeding
and could be related to the level of competition among the members of the
population on the host (density, crowding)(Baugh and Phillips Jr., 1991;
for
surface
3: water stress had
temperatures and these
104
Honek, 1991; Kaakeh et al., 1992; Kindlmann and Dixon, 1992; Thomas,
1993). This
was
tiie
case
in
4. One way in which
Exp.
aphids respond
to
Table
body weighte (see
quality
quantity
16) and decreased fecundity (see Fig. 23). Thus fecundity is positively
correlated with adult size and/or weight (Calow, 1978 cf. Dixon, 1985;
lower food
and
is to maintain lower
Kouame and Mackauer,
constraint
1992). It follows that in the present study, the first
plants
well-watered
on
which affected
aphid body
size
was
crowding, whereas under water stress conditions it was water stress via the
change in food quality. On mature leaves the main constraint for aphid size
quality of their food. The ability of aphids to respond to changes in
quantity of phloem sap and thereby to anticipate the onset of adverse
nutritional conditions is of great adaptive significance (Dixon, 1985).
was
the
the
Another way to
is to
population
aphids
as
adapt to lower food quantity and quality for an aphid
produce winged morphs. Alatae are produced by many
deteriorating conditions in their local environment such
quality (Lees, 1966 cf. Baugh and Phillips
in response to
crowding
or
reduction in food
Jr., 1991; Watt and Dixon, 1981 cf. Wiktelius, 1992; Dixon, 1985; Leather,
1989; De Barro, 1992). In Exp. 3, formation of alatae could be primarily
aphid density (r=0.72
related to
larvae; P
<
0.001); and not to
an
between
density and number of winged
assumed reduction in the
In
in food
quality arising
from both
crowding and
quality of plants
4).
be discussed in Section
increase in water stress
(to
Exp. 4, alatae production was also related
between density and number of alatae; P < 0.05)
consequent upon
an
to
aphid density (r=0.59
as
well as to the reduction
water
deficiency.
A decrease
in the
carrying capacity of the plant under water stressed conditions (indicated
by
decrease in maximum
a
aphid density in a population) decreased the
production is initiated. Baugh and
(1991) found a positive correlation between alatae production and
potential of wheat with maximum alatae production between Y=
density threshold below
Phillips Jr.
leaf water
which alatae
-0.76 and Y= -1.03 MPa. The authors conclude that the host itself is involved
in alatae
production and
A further
point
of interest
not
population density
was
to consider when
an aphid population starts to
(1983) mentioned that a critical
suffer from water stress. Sumner et al.
moisture level (Y- -0.75
longevity of S.
araminum
alone.
MPa) existed, below which the fecundity and
sharply decreased. In the present study, the
were
size and density of aphid populations decreased significantly between wellwatered and
moderately stressed plante
well-watered and
mildly
stressed
plants
in
in
Exp. 3 (see Fig. 20) and between
Exp.
4
(Ysoi|
>
-0.69 MPa;
Fig. 22).
105
If the
assumption is
true that water stress
changes plant quality
then
a
relationship between specific aphid load (aphid abundance, density) and plant
quality (carrying capacity of the plant) should exist The carrying capacity of
a
plant decreased significantly with
water stress. The critical moisture stress
level for the
development of aphid populations and the threshold of population
density for
a
however,
15 and
as
significant reduction in biomass of hosts did not coincide,
by aphid size, particularly on well-watered plante (Tables
shown
16). Thus,
in
Exp. 4, well-watered plants which
aphids stopped growing
had
long
since
begun
at an
aphid density
to suffer decreased
at which the
were
infested with
aphids
body weighte (of
all
themselves
morphs)
as
fecundity,
dispersion
production of
apterae
in
alatae. According to references cited
Price et al. (1989), the carrying
capacity of a plant will be well below the level where damage to the plant
approaches a lethal threshold or even becomes very conspicuous.
well
as
lower
In conclusion,
development
the
of
and the
3 and 4 clearly showed that the rate of aphid population
negatively affected by water stress. In contrast to the
Exps.
was
slightly higher rm found under water stress as compared with well-watered
Exps. 1 and 2, the size and density of aphid populations
conditions in
plant growth and, thus,
new plant tissue, changes in leaf surface temperature
production
as well as supposed changes in phloem characteristics, particularly in sap
quality, affected population development by decreasing the carrying capacity
of the plant The next section (section 4) will examine in detail the quality of
decreased
significantiy
reduced
the
aphids'
with water stress. Reduced
of
source
of nutrition
(phloem sap)
under different water
regimes.
Leer
-
Vide
-
Empty
107
4
Effects of Water Stress
Population Dynamics
of the Green Apple Aphid:
Changes in
Phloem Sap Quality
on
Introduction
4.1
As also
factor
implied from the results presented in the previous section, a major
controlling the population dynamics of aphids, and thus their attack and
damage
potential
of crops, is the
host
quantity and quality of the food offered by the
plant. Aphids feed primarily on the phloem sap of plante and
presumably get all their essential starting materials for the metabolites they
need for growth and reproduction from the phloem sap of their hosts
(carbohydrates, amino acids, minerals, vitamins, water, etc.)(Dadd, 1985 cf.
Slansky
Jr. and
Scriber, 1985; Srivastava, 1987). Although phloem sap is
nitrogen (1-2.3 %) compared
(e.g. xylem)(Pollard, 1973), N is nevertheless limiting
in the nutrition of insects (Auclair, 1965 cf. Prosser and Douglas, 1992;
SenGupta and Miles, 1975; Mattson, 1980 cf. Klinglauf, 1987, Hugentobler,
considered to contain
with other
relatively high
amounte of
plant tissues
1990). The phloem sap of plants is often described as a very dilute, nutrientnutritionally incomplete and unbalanced food source, the most important
poor,
limiting factor being nitrogen present in the form of amino acids (Raven, 1983
Douglas, 1993; Slansky Jr. and Scriber, 1985; Klinglauf,
the
1987). Although
phloem sap is rich in carbohydrate and poor in amino
cf. Prosser and
108
acids and minerals essential for insect nutrition
Prosser and
Douglas, 1992),
one
all nutrients are in soluble and renewable form
Risebrow and Dixon,
(Byrne
advantage of feeding
on
(Slansky Jr.
and Miller, 1990;
this source is that
and Scriber, 1985;
1987). In order to obtain and accumulate sufficient
components, however, aphids must process large
amounte of the scarce
amounts of
liquid (Llewellyn, 1977 cf. Dorschner 1993; Mullin, 1986; Risebrow
Slansky Jr.
and Dixon, 1987;
excess
and Scriber, 1985;
is excreted
(e.g. carbohydrates)
by
Byrne and Miller, 1990). The
aphids in the form of
the
honeydew.
of food available to
aphids fluctuates and may
supply. Typical plant responses to water
stress are probably highly relevant for the feeding success of aphids. Nitrogen
The
quantity and quality
depend
on
factors such
as
water
metabolism is among the processes most sensitive to water stress
al., 1976).
In
water stress disturbs
general,
protein decreases
(increased protein hydrolysis
amount of
nitrogen
metabolism
(Hsiao
so
et
that the
while amino acids increase in concentration
and reduced
plant growth)(Kramer, 1983 cf.
Klinglauf, 1987; Srivastava,
carbohydrate metabolism so that starch
Mattson and Haack, 1987; cf. Louda, 1986;
1987). Further,
water stress disturbs
generally decrease while sugar levels increase (cf. Mattson and Haack,
1987). Other plant responses to water stress which may be relevant for the
levels
feeding
success
water stress
in
of
aphids
are
changes in the distribution of assimilates
as
increases, reduction of carbohydrate translocation and changes
secondary metabolite concentrations (cf. Louda, 1986).
Not all
feeders
plants
or
(Slansky
are equally nutritionally suitable for phloem
Scriber, 1985; Risebrow and Dixon, 1987;
plant parts
Jr.
and
Srivastava, 1987; Douglas, 1993). Many aphids showed preferences for
or early senescent leaves (Dixon, 1985; Klinglauf, 1987; cf. Srivastava,
1987). It is widely accepted that for most deciduous trees the amino acid
young
content of
phloem sap is relatively high when the foliage is growing
then
being actively
senescing (nutrients
leaves) but low in mature leaves (e.g. Douglas, 1993). Further, aphids
are
capable
of
altering
in ways which
the
can
nitrogen
translocated into
balance of their host
be beneficial to themselves
or out
or
of the
are
to a certain extent
plants
("additional sink effect")
(Klinglauf, 1987; Risebrow and Dixon, 1987; Miles, 1989a; Dorschner, 1990).
Few studies exist
cf.
on
phloem sap composition of apple
Wermelinger, 1985; Kluge,
Hugentobler, 1990). The
most
1967
thorough
cf.
trees
Kollar and
and extensive
(Bieleski,
Seemuller,
study
was
1969
1990;
conducted
109
by Kollar and Seemuller (1990). Next
to
carbohydrates and amino acids, the
organic
acid), inorganic constituents (K+,
Mg", Na\ S04~, etc.), proteins, lipids, and RNA nucleotide. It is not entirely
authors found
acids
(citric and malic
certain, however, that all these componente (e.g. proteins)
in the bulk flow of
of
are freely available
phloem sap available to the aphids (P.W. Miles, University
Adelaide, South Australia, pars. comm.). The effect of water
concentration and
relevance to the
composition of nutrients
performance
in the
stress on the
phloem sap of apple and its
of Aphis pomi De Geer has not been studied
yet.
In this
study, changes
and amino acids in
were
in the concentration and
phloem
sap of
composition of carbohydrates
plante grown under different water regimes
examined, in order to speculate
on
how they relate to the development
aphid populations
growth. Further, since aphids developed
significantly differently on growing leaves compared with mature leaves
(sections 2 and 3), it was of interest to examine differences in nutritional
quality within the plant. Last but not least changes in phloem sap composition
due to aphid infestation were investigated.
and their
of
4.2
Materials and Methods
4.2.1
Collection of Phloem
Precise
Sap
quantitative and qualitative data on pure phloem sap composition can
be obtained
by severing
frequency microcautery
the
or a
stylets of feeding aphids by
laser
technique (e.g.
means
of
a
high
Fisher and Frame, 1984;
Weibuil et al., 1986; Kuo-Sell, 1989; Girousse et al.
1991). However,
as a
preliminary experiment to this study had shown, this approach (using
radiofrequency microcautery) was unsuitable for the relatively small A. oomi
water stressed
feeding
on
phloem
sap seemed
sieve tubes
more
plante.
Under conditions of water stress, the
viscous and
probably
also less
the turgor pressure in the
the flow
positive, rendering
through the severed
stylet more tedious (also found by U. Hugentobler, Institute of Plant Sciences,
ETH Zurich). Stylectomy has been successful mainly if at all on herbaceous
plants (Gruppe, 1989; P.W. Miles, University of Adelaide, South Australia,
pers.
was
comm.). Therefore, the technically
exudation method
was
used
in
this
simple and convenient EDTAstudy (King and Zeevart, 1974).
more
Diethylene diamine tetraacetic acid (EDTA)
is known to inhibit callose
sealing
110
by complexing the calcium ions which
of the sieve tubes
process
(Costello
are
essential for this
al., 1982; Bolsinger and Fluckiger, 1986), allowing
et
exuding phloem sap. The drawbacks of this method
possible contamination from surrounding cells (Girousse
therefore to collect the
sap dilution and
are
al., 1990; Weibull et al., 1990). In
et
exudation
technique
given conditions based
Girousse et al. (1990),
preliminary experiment,
a
optimized for
was
the EDTA-
apple plante grown under the
method descriptions by Groussol et al. (1986),
on
the
Hugentobler (1990),
Miles
(1990, technical report) and
(1990).
Weibull et al.
4.2.2
Plant Material
Phloem sap
was
collected from the upper and lower parte of
plante grown
under well-watered and water stressed conditions in experiment 3. The
were taken from uninfested plants as well as from plante, that were
previously infested with aphids. For a detailed description of the experimental
conditions and layout see pages 65 and 66. The leaf samples for the phloem
samples
phloem sap were taken at midday (around 1°°pm) on the day of
plant harvest and at the peak of the current drying cycle. Aphid populations
collection of
had
already been collected
on
the
day
Samples
of harvest.
from the upper
parts of the plant consisted of tiie decapitated apex with 5 apical leaves
(referred
to as
apex), and that from the lower parte consisted of
consecutive leaves from leaf A
(referred
to as basal
leaf 10 for stressed and leaf 30 for well-watered
apex;
see
page
Exudation
Immediately
after excision of the
petioles,
plante, counted from the
65).
4.2.3
their
the first 3
leaves; ranged between
Technique
the samples
were
apices and the basal leaves
at the base of
dipped into vials containing 0.750 ml of
EDTA-buffer solution. About 0.5-1.0
cm
of the basal part of the
petiole
an
was
immersed in the solution. The EDTA-buffer solution consisted of 3.5 mM
disodium EDTA
pH
of 6.7.
(Titriplex) and
During
5 mM di- and monosodium
the time of exudation, the
were
phosphate with a
kept in darkness,
at 23 °C and in
high relative humidity
sealed into the
top of tiie vials below the level of the leaf blades with
Parafilm. Exudation time
were
heated in
a
was
in
samples
a
4 hrs. After
growth cabinet.
The stems
were
exudation, the collected solutions
water bath to 90 °C for two minutes
(to stop enzyme
111
activity) and then frozen
Leaf area, fresh and
Analysis
4.2.4
at -30 °C until tiie assay of sugars and amino acids.
dry weight of the tissue samples
of
were
measured.
Carbohydrates
aliquot of 200 pi from the exudate solution was microfirtered and directly
analyzed by HPLC (Series 3B, Perkin Elmer Corp., USA) with a Rl detector
An
(ERC 7510, Erma Optical Works Ltd., Japan). The separation of the sugars
sucrose,
glucose and fructose and the sugar alcohols arabitol and sorbitol (all
referred to below
as
HPX-87C column
(300
in
a
sugars or
column heater. A
USA)
analytical column.
Bio Rad, Ca,
7.8
*
carbohydrates) was achieved with an Aminex
i.d., Bio Rad, CA, USA) maintained at 85 °C
mm
guard column (Micro Guard
at room
was
used between tiie
was
water and
temperature
The mobile
phase
DeAsh Cat. 1 and An. 2,
injector and
sample flow rate
Sugars were identified by comparing retention times
samples and standards. Arabitol at a concentration of 2.5 mM served as an
internal standard, since arabitol is unlikely to be found in phloem sap
amounted to 0.6 ml/min.
of
(Tarczynski
et al., 1992); F. Machler, Institute of Plant Sciences, ETH Zurich,
comm.). The internal standard was added to the EDTA-buffer solution
pers.
before exudation had started. This allowed correction for changes in the
volume of the EDTA-solution
well
as
components which
solution and do not enter
(Byrne
and
the time of exudation, since arabitol as
exuded into the solution remain in the
through xylem tissue
as a
result of
transpiration
Miller, 1990).
Analysis
4.2.4
during
were
of
Nitrogenous Substances
Amino acids and amides
automated
(referred to below as amino acids) were analyzed by
gradient HPLC (Waters 600 E, MA, USA) using the Pico Tag
analysis system (Waters, Division of Millipore Corpor., MA, USA).
amino acid quantification, samples were dried and derivatized. An
amino acid
Prior to
aliquot of
Tag
100
pi from
the exudate solution
was
dried under
vacuum
in
a
Pico
Redrying was accomplished by adding 15 pi of 2:2:1
methanols M Na-acetate:triethylamine (TEA) and drying under vacuum.
work station.
Twenty pi
of 7:1:1:1 methanol :H20:TEA:
added to each redried
sample
phenylisothiocyanate (PITC)
were
and allowed to react for 20 min at room
temperature. Samples were then dried and reconstituted in 100 pi sample
solution (phosphate buffer: 5 mM sodium phosphate with 6% acetonitrile).
112
Amino acid standards
similar
manner.
concentration of 30
pM
derivatized in
a
methionine sulfone at
a
(Fiuka, Buchs SG Switzerland)
The internal standard used
and
was
was
were
added to the sample just prior to drying and
derivatisation. Standards and samples
microfiltered before
were
analyzed. The separation of the amino acids
was
achieved with
they
a
were
Pico Tag
analysis (reversed phase, 3.9*30 cm, Waters,
Millipore Corpor., MA) maintained at 46 °C column temperature. Peak
detection occurred at the wavelength of 254 nm in a UV detector maintained
column for free amino acid
at 64 °C
(Waters 486, MA, USA). The mobile phases
acetate buffer and
a
gradient
and the
TEA)
sample
flow rate
Eluent A
was
(sodium
USA)
run
at
1.0 ml/min.
aspartic acid (ASP), glutamic acid (GLU),
(SER), asparagine (ASN), glycine (GLY), histidine (HIS), threonine
The amino acids measured
serine
were
and Eluent B (acetonitrile; Waters; MA,
were
(THR), alanine (ALA), arginine (ARG), proline (PRO), tyrosine (TYR), valine
(VAL), methionine (MET), cysteine (CYS), isoleucine (ILE), leucine (LEU),
phenylalanine (PHE), tryptophan (TRP), ornithine (ORN) and lysine (LYS).
Glutamine (GLN), although an amino acid commonly found in the phloem sap
of several
study,
plants
was not
and also
quantified
initially detected
in the exudate solutions in this
due to the fact that it was
missing in the standard
mix.
4.2.5
Statistical
Analysis
using analysis of variance
significant difference range
Differences among the treatmente were evaluated
(ANOVA), and
test
(LSD)
the means were tested
at a 5 % level of
software used
was
by
a
significance
least
if not otherwise mentioned. The
SAS (SAS release 6.04, Institute Inc. Cary, NC, USA).
113
4.3
The
Results
phloem exudation technique using EDTA allowed the
assessment of the
concenbation of total sugars and amino acids in the exudate and the
measurement of the
exudation
relative content of the different componente. The
technique
phloem sap
does not allow the determination of the absolute amount
of collected
4.3.1
nor
the flow rate.
Sugars
Figure
24
presents the concentration of total sugars (mM) measured in the
phloem of uninfested (-A) plante and of plants
previously infested with aphids (+A) that were grown under different water
regimes. Concentrations for the apices and basal leaves are shown
exudate solution of the
separately, since
the size of the leaf
samples differed.
20
E
15
&
10
Apices
-
3
o
a
5
a
o
mmw-y
CONTROL
a
-T-,
a
x
b
rx_l
fffi»-x
MODERATE
X
b
fxl
CONTROL
SEVERE
Treatment
I
Fig. 24.
MODERATE
SEVERE
Treatment
I +A plants
-A
plants
T
SE
Total sugar concentration in the exudates of phloem sap collected
from apices and basal leaves of apple plants previously infested with
aphids (+A) and without aphids (-A) grown under well-watered
(control), moderately and severely water stressed conditions. Means
(5 replicates) with the same letter are not significantly different
(PS 0.05); letters on top of bars indicate differences among
treatments (+A and -A separately) and letters within bars between +A
and -A plants within
a
treatment.
114
Mean
leaves
area
(ca
of apex
74
cm2).
sugars found in the
samples
was
This may
phloem
smaller
cm2)
(ca 35
than that of basal
the concentration of total
partly explain why
exudate collected from
apices
was
significantly
lower than in the exudate collected from basal leaves. Even so,
manipulation of
the data, the
basal leaves of
aphid infested plante appeared
discussed below. The size of the
as
was
In
higher sugar
highly variable
even
within
a
by any
content of the exudates from the
to be disproportionately large
samples from apices and basal leaves
water stress treatment.
apical phloem exudates, the concentration of total sugars increased with
water stress, which was
significant only
in uninfested
exudate collected from basal leaves of
phloem
aphids, the concentration of total sugars did
water stress treatmente
probably because of
plante (Fig. 24). In the
plante
not differ
the
not infested with
significantly
among
variability in the size of
samples mentioned above. The high concentration of sugars measured in the
exudate solutions of the basal leaves of well-watered, with aphid infested
plants was probably due to contamination with honeydew which also covered
the
petioles of leaves (honeydew
immersion into the exudation
was not
washed off the
solution). Despite
petioles
before
the effort to exclude any
surface contamination from exudates, this conclusion seemed inevitable from
quantitative analyses (see below). A higher aphid density (see page 85) and
a less viscous honeydew on well-watered plants led to a large amount of
honeydew production
contamination
with
and its uniform distribution onto the lower leaves. This
honeydew could be inferred from relevant HPLC
chromatogram: before the sucrose peak an extra
detected. According to the retention time it was
and
large peak
identified
as
was
due to
an oligosaccharide typical of and exclusive in honeydew.
Honeydew of A^ pomi feeding on similar apple plante grown under different
melezitose,
levels of
nitrogen fertilization
fructose,
sucrose
was
reported
to contain
sorbitol, melezitose,
and glucose in decreasing order (Hugentobler, 1990).
Therefore, the high sugar concentrations measured in the exudates of these
basal leaves
can be attributed to the contamination of the exudate solution by
honeydew.
The phloem exudate collected from plante which were previously infested with
aphids contained higher concentrations of total sugars than uninfested plants,
although this difference reached significance only in the well-watered
treatment.
115
An attempt was made to allow for tiie size of apex and basal leaf
show in the
expression
phloem exudate.
divided by
samples to
of the concentration of total sugars found in the
For this purpose, the concentration of total sugars
the respective leaf
area
(cm2)
of the
sample (data
not
(mM) was
shown). In
plante uninfested with aphids, apices still gave lower concentrations of total
sugar than basal leaves, particularly under well-watered conditions. Further,
significantly with water stress.
Moderately water stressed plants tended to give the highest concentrations
per cm2, indicating either a higher concenbation of the pure phloem sap or a
the concentration of total sugars increased
faster flow rate. Even when allowance
previously
infested with
sugar than
plante
made for sample size, plants
was
aphids generally gave higher concentrations of total
aphids, particularly in the well-watered
not infested with
treatment
The main
samples
sugar).
carbohydrate component found in the phloem exudates of all
was
the sugar alcohol sorbitol
The other
componente
(ranged between 47
glucose and
were sucrose,
to 82 % of total
fructose. Since
phloem sap is considered to contain only non-reducing sugars and sugar
alcohols, the amount of glucose and fructose recovered indicates
contamination of the exudate solution with either invertase,
reducing
sugars
themselves,
from
extra-phloem tissue sap,
as
or
with the
discussed in
detail on page 122. The dominance among these three sugars in the exudate
solution
the
depended on the water stress treatment, the presence of aphids and
position within the plant. Table 17 presents the relative content (%) of
each sugar component in the exudate of
phloem
purposes, the percentage sugar composition of the
sap.
For illustration
phloem exudates is also
presented graphically (Fig. 25).
The relative content of sucrose,
glucose and fructose in the phloem sap
apices and basal leaves (whether infested or not); the
differences, however, were significant in the well-watered treatment only
varied between
significantly
glucose significantly higher in the apex. The relative content of
sorbitol was not significantiy affected by the position of the sample within a
(Table 17). The relative
content of sucrose and fructose was
lower and
plant.
In
aphids, the relative content of
significantly higher than in
the exudate of aphid uninfested plante. Further, previously infested plante
showed significantly lower proportions of sorbitol in their phloem exudate
plante which
sucrose
were
previously infested
with
and fructose in the exudate solution
was
collected both from the apex and basal leaves
compared with that of
116
Table 17.
(%) of sugar components in the phloem exudate of
and basal leaves of apple plants previously infested with
Relative content
apices
aphids (+A)
moderately
and without
and
severely
aphids (-A)
under well-watered
(control),
water stressed conditions; means ±SE are
shown *.
Carbo¬
hydrate
-A
Control
|
+A
Moderate
Severe
Control
|
Moderate
|
Severe
Apex
Sorbitol
65.90
a
±1.75
Sucrose
4.59
26.30
a
±2.27
Fructose
3.20
77.88 b
±4.03
±2.11
6.26
a
±0.90
Glucose
74.94 ab
a
±1.02
4.54
a
a
±2.60
±0.68
13.25 b
12.35 b
±2.27
±0.67
5.55 a
5.23
±1.38
±0.37
a
49.79
x
±3.09
10.74
x
55.69 xy
±8.69
11.38
x
±2.33
14.96
10.11
x
±2.46
±1.65
18.06 xy
±3.73
11.00y
±1.24
24.51
x
69.81 y
±2.74
14.86
x
±1.10
x
±3.42
±0.49
9.08
x
±0.92
Basal Leaves
Sorbitol
71.70
73.98
a
±2.26
Sucrose
7.46
a
±1.21
Glucose
11.40 a
9.43
5.80 a
4.41
±1.14
8.93
a
±1.32
±0.82
(5 replicates) in
a row
a
a
±1.66
8.03 ab
a
±1.22
means
±2.50
±0.81
12.19
±0.84
Fructose
81.76 b
a
±1.67
4.91b
i
±0.66
followed
by the
49.90
x
47.03
±2.60
15.11
x
22.10
15.83
x
x
±6.66
19.22
x
±4.47
13.53
x
±1.88
15.04 y
±1.80
12.89 y
±1.60
x
±0.60
same
x
54.37
±2.92
±2.06
20.30
x
±4.30
±0.91
14.69
x
±5.74
letter
are not
significantly
different (P s 0.05).
uninfested plants, irrespective of the water stress treatment (Fig. 25).
Although the interpretation of these data is complicated by the evidence of
contamination of the
can
phloem sap as discussed above, one conclusion
aphid infestation had considerably increased
be drawn is that
leakiness" of the tissue
(surrounding cells).
that
the
117
Apex
100
o
nur F
80
en
Basal
Leaves
100
CO
60
"o
40
-
20
-
Treatment
CMS
Infestation
I
Fig.
CMS
A
+
HHH
| sorbitol
25.
Relative content
CMS
A
-
+
A
A
-
^H
glucose
sucrose
(%)
CMS
fructose
of sugar
components in the phloem exudate of
apple plants previously infested with
aphids (+A) and without aphids (-A) under well-watered (C),
moderately (M) and severely (S) water stressed conditions
apices and basal leaves of
To
study
the
component
aphids
in
were
effect of water stress
the
phloem
considered
content of sorbitol
the
on
exudate alone,
(Table 17)
A
only
percentage of each sugar
the
significant
plants
not infested with
increase
the relative
in
the exudate collected from apices and basal leaves with
in
water stress was observed
glucose
contents from
stress
Therefore
Fructose content of basal leaf exudates and
apical exudates decreased significantly
the
most
carbohydrate composition
of
important
phloem
effect
of
exudates
water
was
the
with water
stress
on
increase
in
the
the
proportion of sorbitol
In
plants
sorbitol
which
were
significantly
previously
increased
infested with
only
in
Similar to the results from uninfested
in
exudates
decreased
contents
collected
significantly
from
with
basal
plants,
leaves
water stress,
impeded the leakiness of
tissues
Another difference with respect to the
exudates
collected from
aphid
aphids, the
relative content of
the exudates collected from the apex.
infested
the relative content of fructose
and of glucose
possibly because
from
apices
lower water
suggested above
carbohydrate composition
and
uninfested
plants
in
the
was
the
118
presence
or
absence of the
oligosaccharides stachyose and raffinose. In the
particulariy of phloem exudates collected from plante
previously infested with aphids, two extra peaks were detected
HPLC chromatograms,
which
were
and identified as stachyose and
larger than the stachyose peak.
peak
was
in
general
Amino Acids
4.3.2
Figure
raffinose. The raffinose
26 demonstrates the total concentration of amino acids measured in
phloem exudate of plante which were previously infested with aphids (+A)
and of uninfested plante (-A) grown under different water regimes. Data of the
the
samples from apices and basal leaves
are
again shown separately due
to
differences in their size.
Basal Leaves
Sl
CONTROL
MODERATE
SEVERE
CONTROL
I
Fig.
26.
I +A plants
MODERATE
SEVERE
Treatment
Treatment
-A
plants
T
The concentration of total amino acids in the exudates of
SE
phloem sap
apices and basal leaves of apple plants previously infested with
aphids (+A) and without aphids (-A) grown under well-watered
(control), moderately and severely water stressed conditions. Means
with the same letter are not significantly different (P £ 0.05); letters on
top of bars indicate differences among treatments (+A and -A
separately) and letters within bars between +A and -A plants within a
from
treatment.
119
In contrast to total sugars, the concentration of amino acids in exudates from
apices and basal leaves of water stressed plante did not differ significantly. In
phloem exudates collected from the apex, the concentration of total amino
significantly with an increase in water stress, whether
previously infested with aphids or not. In the exudate of basal leaves, total
acids decreased
amino acids concentrations did not change
significantly with water stress.
The
high concenbation measured in the exudate solution of the basal leaves of
well-watered, aphid
plante was probably again due to the
honeydew. Hugentobler (1990) stated that total amino acid
concentration in honeydew was about one third compared with the phloem.
An attempt was made to include the size of the sample used for exudation in
the expression of total amino acid concenbation found in the corresponding
exudate solutions. For this purpose, total amino acid concentrations (pM)
were divided by the respective leaf area (cm2, data not shown). The exudate
solutions collected from apex samples still gave higher concentrations of
amino acids/cm2 than from basal leaves. The samples taken from plante
which were previously infested with aphids also contained higher
infested
contamination with
concentrations of total
amino acids than from
uninfested
plants. The
concentration of total amino acids in the exudates decreased with
intensity of
water
of uninfested
plants. In the latter, the concentration of total amino acids /cm2
increased with water stress, the
watered and
increasing
stress, except in exudates collected from the basal leaves
moderately
stressed
highest difference being between well-
plante. Whether these changes
concentrations of amino acids in the
concentrations in the
phloem exudate
phloem itself or due
to
changing
were
in the
due to variable
flow rates could not be
determined.
major components of amino acids found in the phloem exudates of all
samples were ASN (12 80% of the total content), THR (2 30%), CYS (1.4
The
-
28%),
GLU
(4% -19.4%)
-
and ASP
(1.4
-
8.1%).
-
These made up 70 to 90 %
high proportions of ASN might
together with ASN
proportions (Hugentobler, 1990), was not measured.
acids measured, only arginine was not detected in the
of the concentration of total amino acids. The
be overestimated since
although
at lower
Of the 20 amino
GLN, which often appears
phloem exudate and will be excluded from further discussions. Table 18
presents the relative
in the exudates of
content
(%)
phloem sap
of each amino acid detected and measured
of
apple plants. Since phloem exudates from
significantly in
presented separately.
the apex and the basal leaves differed
composition,
these results will be
their amino acid
120
In the exudate collected from the apex, the relative content of ASN
of THR, ALA,
significantly higher, whereas that
significantly
from
collected
significantly
In the
with
in
different
the
relative
plants.
uninfested
from the apex of
was
significantly
lower
(VAL,
significantly)
the relative content of ASN
study
lower than in uninfested
phloem exudate, only samples
(Table 18).
amino acids found in
on
of
plants
not
0
'
'—'
'
'
''
exudates is also
aphids
were
of the
major
proportion
presented graphically (Fig. 27).
I—i
0 I—I
CMS
ASN
I
ii
I
1
II
THR
§
Relative content (%) of the
(22
SER
I
r^
CMS
-A
+A
^
ASP
'I
CMS
-A
+A
I
27.
'I
'ii
EEI
Fig.
was
Basal Leaves
CMS
Infestation
infested with
For illustration purposes, the
phloem
LYS
composition of the
the amino acid
Apex
Treatment
plants
plants.
the effect of water stress
considered
than in
significantly
was
PHE,
higher, whereas that of ASP, GLU, SER, HIS, LEU,
significantly
were
that of
higher, whereas
not
In the exudate collected from the basal leaves of
previously infested with aphids,
To
acids
plants previously infested
the relative content of ASN tended to be
ASP, CYS and PHE
amino
remaining
the
not
exudate
exudate.
apical
phloem exudate collected
aphids,
All
was
were
in
those found
from
amounts
leaves.
basal
lower in the
ILE, LEU and PHE
CYS
HI
HH
others
GLU
major amino acids in the phloem exudate
apple plants previously infested with
and without aphids (-A) under well-watered (C),
moderately (M) and severely (S) water stressed conditions.
apices and
aphids (+A)
of
basal leaves of
121
Table 18.
Relative content
(%) of amino acid components in the phloem
apices and basal leaves of apple plante previously infested
with aphids (+A) and without aphids (-A) under well-watered (control),
moderately and severely water stressed conditions; means and ±SE
exudate of
are
Amino
acid
shown.
-A
A
Control
Moderate
Severe
ASN
68.06±1.67
5527115.68
27.94112.72
THR
8.95±1.86
12.1818.16
27.91 ±6.60
CYS
5.06±1.11
9.19±2.57
GLU
5.04 ±0.56
7.3212.12
ASP
2.49±0.25
32810.58
ALA
2.17±0.60
4.4212.94
ILE
3.1010.90
2.0411.68
SER
0.68±0.66
0.5510.50
GLY
1.04 ±0.08
PRO
Control
Moderate
77.1612.92
643619.78
4926111.18
5.5312.38
9.6214.71
20.93111.88
16.7514.96
3.67±1.6B
6.7912.79
43311.39
8.8511.48
4.0310.61
5.5511.20
72710.55
5.1711.25
1.4310.18
1.74±0.34
33810.84
1.4910.09
3.3811.41
3.3810.99
32811.36
3.4812.97
021 ±0.03
1.3611.10
4.5412.72
1.1711.08
0.4310.42
0.9210.84
0.77±0.74
1.17±0.34
1.5610.25
0.8410.12
12210.30
1.4810.35
0.67±0.15
0.5410.09
0.9510.24
037±0.12
03510.22
1.1410.34
VAL
0.45±0.07
0.77±0.17
1.5810.52
0.4610.07
0.8910.15
0.61 ±0.19
Severe
Apex
LYS
0.38±0.06
0.5310.06
0.6310.23
0.41 ±0.06
0.5910.09
0.4010.05
PHE
0.79±0.09
1.0710.28
0.4210.06
0.4510.06
05110.14
0.5010.10
HIS
02010.06
0.3310.07
0.5910.19
02210.04
0.3910.07
03610.12
TYR
0.32±0.06
0.41 ±0.09
027±0.05
0.3910.10
0.5210.13
0.3010.09
LEU
0.36±0.09
0.6210.21
0.6810.08
0.3110.08
0.3910.20
05110.07
ORN
0.0910.03
0.1510.03
02710.05
0.0910.01
02210.07
0.1610.06
TRP
0.1210.0S
0.1410.06
0.1210.01
0.0710.02
0.1510.03
0.0510.01
MET
0.03±0.01
0.0310.01
0.1710.15
0.0510.02
0.0710.03
0.0210.00
ASN
19.5416.43
22.77±6.41
12.4413.84
79.78±1.27
33.5919.44
223018.33
THR
9.9014.08
20.4419.14
30.3011.62
2.0310.18
18.6716.28
292014.95
CYS
28.0317.89
14.97±3.50
21.9812.65
1.37±0.25
19.76±6.72
26.4513.91
GLU
19.3610.58
12.9312.33
9.5111.75
63310.45
10.501228
5.1510.62
ASP
8.0710.86
4.5611.29
42210.44
22210.11
4.4210.93
3.0910.38
ALA
2.6610.88
5.5013.27
1.4410.22
1.4910.25
1.9110.74
1.31 ±0.45
ILE
0.6010.19
0.5610.05
4.951427
0.4110.08
0.3610.12
12810.91
SER
2.61 ±2.57
6.3511.34
4.3111.46
0.3510.35
0.77±0.72
2.4410.99
Basal Leaves
GLY
2.0410.69
2.97±0.70
2.1810.53
15310.15
2.3210.88
1.8810.31
PRO
0.6410.28
2.3210.58
2.0811.31
1.4010.37
2.37±0.83
2.0210.54
VAL
0.90±0.37
132±0.37
2.0710.82
1.0710.30
15110.55
12610.69
LYS
157±0.72
0.9710.17
0.9510.14
02610.04
0.4910.11
0.4810.07
PHE
1.1010.55
0.79±0.11
0.6210.07
02910.03
0.4210.08
0.3710.05
HIS
0.8910.48
1.0610.06
1.031024
02210.04
0.6010.14
0.6310.06
TYR
0.6910.25
1.0010.36
0.4910.05
02310.05
1.0810.31
0.3710.10
LEU
0.6310.15
0.7310.09
0.6410.14
0.1510.05
0.5110.16
0.71 ±0.08
ORN
0.31 ±0.20
0.3610.13
0.3410.10
0.1310.01
0.3410.22
02510.10
TRP
0.2810.14
02710.08
02310.05
0.0610.01
021 ±0.05
02210.14
MET
020±0.09
0.13±0.04
02210.13
0.1910.05
0.1510.06
0.0910.06
122
In the apical exudate, the proportion of ASN was observed to decrease
significantly with increasing intensity of water stress, whereas that of THR,
CYS, ASP, HIS (VAL, LEU, ORN) increased significantly. In the phloem
exudate collected from the basal leaves, GLU and ASP decreased with water
stress, whereas THR tended to increase. In these samples, therefore, the
exudates collected from the apex and from the basal leaves, besides
a
completely different
amino acid
totally different reactions
also
having
to indicate
appeared
to water stress.
plants which
With respect to
composition,
previously infested with aphids, phloem
significantly decreasing relative contents of
significantly increasing contents of GLU and ASP (THR and LEU)
were
exudates from the apex contained
ASN and
with
increasing intensity of
and ASP
(GLU)
increased
phloem exudates collected from
significantly, whereas THR, CYS, LEU, HIS
water stress. In
the basal leaves, ASN decreased
significantiy
between the well-watered and water
stressed treatments.These results must be treated with
some
caution, in
new
samples from aphid infested plants with
general contamination of the samples with the
of the evidence of contamination of
honeydew
as
well
as
with the
leaked contents of extra-phloem tissue sap,
as
noted above in relation to
sugar concentrations. Nevertheless, in conclusion, water stress seemed to
decrease the relative content of ASN in the exudate solution, whereas HIS
and THR
(to
a
lesser extent LEU and
VAL) increased. For the
amino acids the change with water stress
the
plant and
on
whether the
other
major
depended on sample position within
plant was previously infested with aphids
Proline, often mentioned in context with water
stress and the
or
not.
ability of plante
adjust osmotically,
proportion
degrees depending on the specific comparisons. In exudates from
apices, the relative content of proline increased between the moderately and
tended to increase in
to
with water stress, but
to different
severely stressed treatmente, whereas
in the exudates from basal
leaves, the
relative content of
watered and the
a
proline already increased significantly between the wellmoderately stressed treatment. The proline data overall had
particular high variance, however, which
variable water stress
development
was
probably due
to the
highly
even within a treatment. The relative
content of
proline was in general higher in the exudates from basal leaves
compared with apical exudates (exception: well-watered, -A plants) as well as
in
plante which
plants.
were
previously infested with aphids compared with uninfested
123
4.4
Discussion
4.4.1
Sugars
The sugar alcohol sorbitol
was
clearly the major carbohydrate component
found in the phloem of the apple plante in the study presented here. Most
other
plant species, however, have predominantly sucrose in their phloem sap
of the sap)(Pollard, 1973; Klinglauf 1987); sucrose is therefore
commonly regarded as the main transport sugar in plants (cf. Kuo-Sell, 1989;
cf. Byrne and Miller, 1990). For species such as com (Ohshima et al., 1990),
(5-25%
wheat
(Hayashi
and Chino, 1986 cf. Girousse et al.
1978 cf. Girousse et al.,
1991), rice (Kawabe et al.
(Kuo-Sell, 1989), cotton (Tarcynzki, et
al., 1992),
al., 1991), peas (Rochat and Boutin, 1991),
(Girousse
and most leguminous species (Girousse et al. 1991) sucrose was reported to
constitute the predominant or exclusive carbohydrate. On the other hand,
Wang and Stutte (1992) reported that sorbitol constitutes 60 to 80 % of the
translocated carbohydrate in most woody Rosaceae species. Hugentobler
(1990) found almost exclusively sorbitol (70% of total sugar) and sucrose in
the pure phloem sap of apple plante collected by stylectomy. Also Bieleski
(1969 cf. Wermelinger, 1985) reported that sorbitol comprised 80 % of total
sugars found in the phloem of apple. Besides sucrose and sorbitol, oligo¬
saccharides of the raffinose type (raffinose, stachyose, ribose) have been
identified in the stylet sap of different plant species (Ziegler, 1975; Klinglauf,
1991),
alfalfa
oats
et
1987; Tarczynski et al., 1992). For example, evergreen ash (Costello et al.,
1982) and pumpkin (Byrne and Miller, 1990)
predominantly raffinose and stachyose
As mentioned in the
study
on
the
The authors
here, fructose
to contain
introduction, the most comprehensive and complete
sap of
was
stachyose, raffinose and fruc¬
completely missing. Also in the study presented
low concentrations of
was
measured and
phloem extract, particularly
But also
reported
apple was done by Kollar and Seemiiller (1989).
reported that beside the main sugars sorbitol and sucrose, the
phloem
phloem sap contained
tose, whereas glucose
the
were
in addition to some sucrose.
glucose
was
found in
of
stachyose and raffinose
were
identified in
samples taken from aphid infested plants.
extracts of apple plante, although it
phloem
suggested that, generally, glucose was unlikely to be found in the
phloem sap of any plant species (e.g. Tracynzki et al., 1992).
has been
The
relatively high
amounte of
glucose (ranging between 9 and 26
% of total
124
to a lesser extent, of fructose (3-20 %) in relation to sucrose (4.5%) found in the exudate solutions indicated that the solution contained
sugar) and,
22
recovered hexoses in the EDTA-exudate
cutting
surrounding the phloem
from the
resulting
cells
et al.
(1991) reported that
than just pure phloem sap. Girousse et al.
more
are
to be considered
petioles: Leakage
of the
may contaminate the
of
as
artefacts
compounds
from the
phloem
extract. Groussol
(1986), showed that leakage from surrounding cells under the employed
conditions was negligible in comparison with the amount of
experimental
sugars
from
collected
contamination is the
the
phloem sap. Another important
enzymatic
inversion of
sucrose to
source
of
glucose and fructose
by invertase during the time of exudation. Since the main carbohydrate
component found in the phloem of apple was sorbitol, however, and since it
is not
susceptible
hydrolyzed by
study. It has
exudates
to
invertase in the
to be
was on an
probably
sampling procedure employed in the present
hydrolysis,
a
great proportion of
sucrose was
noted, though, that the glucose fraction in phloem
average two-fold
higher
than the fructose fraction
(data
Hugentobler, 1990 show similar resulte). Sucrose hydrolysis should
produce equimolar amounte of glucose and fructose; if leakage from
surrounding cells can indeed be considered negligible, the question arises,
from where originates this surplus in glucose? The resulte of the present
from
experiment
do not,
unfortunately, suggest
an answer.
study presented here, the concentration of total sugar in the phloem
particularly when the
water
collected
from
of
stressed
the
plants (Fig. 24). This
apex
phloem was
In the
sap exudate tended to increase with water stress,
is in
agreement with
most of the literature
carbohydrates induced by
Irigoyen
et
water stress
reporting changes
in the content of
(e.g. cf. Mattson and Haack, 1987;
a major carbohydrate
al., 1992). Because sorbitol constitutes
component in apple trees (cell sap and phloem) Wang and Stutte (1992),
hypothesized that it has an important role in the osmotic adjustment during
stress. They demonstrated that in mature apple trees, sorbitol
accounted tor over 50% of total osmotic adjustment. In potted young cherry
trees, Ranney et al. (1991) found that the change in sorbitol concentration
alone accounted for the total solute accumulation. Wang and Stutte (1992)
water
give several possible explanations for the effect
accumulation. Water stress may
of water stress
on
sorbitol
(1) increase the partitioning of newly fixed
carbon into sorbitol (2) induce the enzymatic pathways that break down
starch and sucrose which increases sorbitol
synthesis (3)
of transport of sorbitol, relative to sucrose from the leaf.
decrease the rate
125
The present
the
study
revealed that the relative content of sorbitol increased in
phloem exudate when apple
Normally,
however, osmotic
plante
were
subjected
to water stress.
adjustment refers to solute accumulation
on a
cellular basis; solutes and assimilates needed for this accumulation have to
be
transported
to the
respective
changes
carbohydrate
changes in the phloem sap
composition are to be expected, since osmotic adjustment, namely of growing
tissues, depends to a great extent on the import of recent photosynthates
(e.g. Boyer, 1988 cf. Studer, 1993). An increase in the sorbitol fraction in the
composition
occur
phloem sap of
cells. If
due to water stress, similar
water stressed
role of sorbitol in osmotic
apple plants, therefore confirms the important
adjustment to
water stress.
Leaves of different stage of development
sensitivity (ability
to
in leaf/cell
adjust osmotically)
cf. Premachandra and
to
are
considered to exhibit differential
plant water stress (e.g. O'Neil, 1983
al., 1984; Steinberg et al., 1989;
1992, Lakso et
Joly,
1992). In section 2 of the study presented here, it was
suggested that growing tissues (the five apical leaves) may show a reduced
Wang
and Stutte,
ability to adjust osmotically to water stress (lower turgor pressure)
compared with mature leaves of the same plant
Depending on plant species and plant organ under consideration,
hydrate componente other than sorbitol such as sucrose and glucose
as
carbo¬
can
be
considerably involved in the process of osmotic adjustment. Therefore, the
proportions of the compounds involved in osmotic adjustment may be of
importance. In this study, no significant differences in phloem exudate
composition between samples from the apex and from basal leaves of water
stressed plants could be observed. Also, the relative content of sorbitol,
probably
the most
important carbohydrate for osmotic adjustment
in
apple,
was not different in exudates from the apex and basal leaves in any
treatment. These results indicate that the
carbohydrate composition of
the
phloem sap can not explain the different ability of apex and basal leaves,
respectively, to adjust osmotically to water stress. Additionally, it has to be
noted that carbohydrate composition within other than sieve cells might have
been different between apex and basal
transported
in sink and
leaves: the nature of sugars
may be different from the carbohydrate composition
phloem
particularly source tissues (Ziegler, 1975).
in the
126
The total concentration of
carbohydrates
was
significantiy higher
from basal leaves than from the apex. Mature basal leaves
in exudates
produce great
great part of which is exported to other plant parte,
growing tissues (apex) depend to a great extent on the import of
assimilates. In this study, it was not possible to determine whether the higher
amounte of assimilates, a
whereas
amounte of
were
in the
carbohydrates
due to
a
higher
phloem exudate solutions from basal leaves
concentration in
phloem sap
or
to a
higher flow
rate of
the sap.
Coleman (1986) and Milburn (1974 cf. Girousse et al., 1991) mention that
there are concentration
along
sap
gradients in the various components of the phloem
gradients depend on the proximity of a source or
stems. These
sink organ. In castor bean, sucrose
was
found to be highest in the phloem
sap of the shoot apex and to decrease towards the base of the stem
(Vreugdenlid and Kool-Grousveld, 1989). Klinglauf (1987) reports
that
leaves age, their carbohydrate concentration decreases. Hugentobler
on
the other hand, found
higher
no
sucrose
to sink leaves.
(1990)
difference in total sugar concentration but
relative content of sorbitol in exudates collected from
compared
as
source
Similarly, Kuo-Sell (1989) reported
no
leaves
a
as
difference in
phloem sap in the different parte of oats.
carbohydrates in the phloem sap of apex and
similar (according to Kuo-Sell, 1989 and Hugentobler, 1990)
concentration in the
Whether the concentration of
basal leaves
or
higher
are
in the sieve cells of the apex
(according
Grousveld, 1989, and Klinglauf, 1987), it would
carbohydrates
to a
higher
in exudates of basal leaves
flow rate of the
As mentioned in the
to
seem
compared
Vreugdenlid and Koolthat
higher
amounts of
with the apex
are
due
phloem sap from basal leaves.
introduction, aphids may change the food quantity and
quality of their host. The concentration of total sugars was in general
significantly higher in exudates collected from previously aphid infested than
uninfested plants (see Fig. 24). Although it was not possible to determine
whether this was due to a higher concentration in the phloem sap or a higher
flow rate, this higher sugar concentration in exudates was probably due to the
"sink" effect the aphids exerted on their host. As cited in Dorschner (1990),
aphids act as powerful sinks which can direct assimilates and nutrients from
distant parte of the plant towards the aphid colony. Dorschner (1990)
proposed that salivary enzymes may increase the flow of nutrients and
assimilates to the aphid colony because salivary secretions can be
translocated within the host and thus affect long distance transport of
nutrients within
a
plant. In addition, the larger the colony, the
more
powerful
127
the sink
produced until the carrying capacity
1990). This
1989a; Dorschner
of the
plant is reached (Miles,
study: the
confirmed in the present
was
difference in total sugar concentration in the exudate collected from
previously
significant only in well-watered
the
where
plante,
greatest aphid population size and density had developed
In
moderately and severely stressed treatmente, with smaller
(see Fig. 20).
aphid infested and uninfested plants
aphid populations, the differences
and not significant.
was
in total sugar concentrations
were
smaller
only the quantity of sugars, but also the carbohydrate composition of the
phloem exudate was affected by aphid infestation. The nonphagostimulant
sorbitol (Pollard, 1973) was significantiy lower in the exudate of previously
infested plants in favor of the phagostimulant sucrose (Srivastava, 1987)
Not
and/or in favor of raffinose and
detected almost
discussed
on
exclusively
stachyose. These oligosaccharides
in exudates of
pages 100 and 101, a
aphid
infested
were
plante. As
previous aphid infestation reduced the
apple plants to adjust osmotically under conditions of water stress.
The significantly lower relative content of sorbitol in leaves which were
ability
of
previously infested with aphids compared
with uninfested leaves
might thus
confirm the important role of sorbitol in osmotic adjustment The mechanism
change the composition of the phloem sap, their source
(1985) stated that aphids
secrete substances into plants that rapidly affect the metabolism of their host
plant leading to an improvement of the quality of the phloem sap. Miles (1968
by which aphids
can
of nutrition, is still not well understood. Dixon
"aphids produce their own specific
well as unspecific plant hormones,
organizer
Later Miles retracted the suggestion
into
host.
their
which are then introduced
that aphids significantly add to the amounte of auxin present in plant tissues,
cf.
Dixon, 1975)
even
but
suggested
that
of plant growth"
chemical
as
suggested (Miles, 1990) that general redox reactions induced by their
oxidases would tend to produce reactions simulating those in
salivary
senescent tissues,
presumably including the increase in mobilization of
(P.W. Miles, University of Adelaide, South
nutrients referred to above
Australia, pers. comm.).
4.4.2
In the
Amino Acids
study presented here, all
common
amino acids with the exception of
detected in the phloem exudate of apple plante. The major
arginine
amino acids found in the exudate solution were ASN, THR, CYS, GLU and
were
128
ASP which accounted for 70
90 % of the total amino acids found in the
-
phloem exudates (see Table 18).
depended
treatment and whether the
Comparable
other crops
The dominance among these componente
sample position within the plant,
the
on
amino acid
(Weibull
plant
previously
was
compositions
et al.
were
on
the water stress
aphids
infested with
or
not.
reported for apple and several
1986, Weibull et al., 1990; Ohshima et al., 1990;
Girousse et al., 1991). Kollar and Seemuller (1990) found that ASP and GLU
together
with their amides
of different
apple curtivars,
(ASN
and
whereas
GLN)
were
predominant
in the
arginine and cysteine were
major amino acids found by Hugentobler (1990) in
apple plante (originating from the same clone as plants
The
ASN, GLN, HIS, ASP, GLU and SER. In contrast to
phloem
not detected.
phloem sap of
study) were
this study, arginine was
the
in this
also detected in considerable amounts.
The ten essential amino acids for animal and insect nutrition
are
ARG, HIS,
ILE, LEU, LYS, MET, PHE, THR, TYR and VAL (Fried and Dadd, 1982 cf.
Hugentobler,
1990;
Prosser
Douglas,
and
1992). However,
often
as
mentioned in the literature, non-essential amino acids dominate in the
phloem
only THR was detected at appreciable
completely missing. The ability of aphids to
sap. Of the essential amino acids
amounte, whereas arginine
grow well
rather limited amino acid mixture in their diet is attributed to
on a
the presence of
dietary
a
large numbers of symbionts in their gut which upgrade the
non-essential amino acids
essential
et
was
ones
and thus
supply
the
(e.g. ASP, GLU and their amides) to
missing amino acids (Houk, 1987; Sasaki
al., 1991 cf. Dorschner, 1993; Prosser and Douglas, 1992).
As
one
example: methionine,
appreciable
important
amounts in the
source
of the sulfur
essential amino acid often found in
an
phloem sap (e.g. Hugentobler, 1990) is
in very low relative amounte in the
phloem (present study; Kollar
may
occur
and
Seemuller, 1990). In such situations, there
aphids
to
cysteine,
study,
was
are
alternative ways for
get the essential methionine and/or sulfur: It may be
a
non-essential sulfur amino acid,
and/or in the form of
probably
inorganic
the case in the
possibility is that
methionine
inorganic sulfur and
an
required by aphids. Nevertheless, methionine
as was
provided by
probably the
case
in this
sulfur which is also found in
phloem, as
study of Kollar and Seemuller (1990). Another
can
be
synthesized by
non-sulfur amino acids
as was
the
symbionts
from
shown for Mvzus persteae
(Sulzer)(Douglas 1990cf. Prosser and Douglas, 1992).
Prosser and Douglas
specific aphid species may be
(1992) suggested that
the
specifically adapted
complement the amino acids in the phloem sap of
to
symbionts
of
a
129
aphid's host plant Therefore, whether the presence of
phloem should be considered
the
essential
an
amino acid in the
on plant species,
aphid, its symbionts and other circumstances, so that generalization is not
as
or
not
depends
possible.
quality of
composition of the phloem is of great
Since amino acids rather than sugars determine the nutritional
aphids,
importance for aphid population development. As
the amino acid
sap for
phloem
can
the different treatmente affected phloem composition
be
seen
from
Fig. 27,
significantiy in this study.
Asparagine constituted with 68-77 % relative content the most important
amino acid fraction in phloem exudate collected from apices of well-watered
plants. As the brief literature overview of Girousse et al. (1991) shows and
other studies report (Kuo-Sell, 1989; Douglas, 1993), asparagine is the major
component in the phloem sap of several crops and is considered the chief
nitrogen transport compound. This is probably linked to ASN's specific
properties and to ite position in nitrogen metabolism (high N/C ratio as
mentioned by Milfin and Lea, 1977 cf. Girousse et al., 1991). The relative
content of ASN in phloem exudates from basal leaves of uninfested, wellplante, however, amounted to only 20 %, i.e. the composition of the
phloem exudates from the basal leaves was totally different from apical
watered
exudates. In exudates from the basal leaves, the relative contents of
practically all other amino acids
well
as
were
higher, particulariy of CYS and GLU
as
ASP and SER.
Water stress induced
phloem exudate
amino acids
a
striking reduction in the relative
TYR, CYS, GLU, ASP
In exudates from basal
in amino acid
were
well
as
major
of HIS, ORN, VAL increased.
leaves, water stress exerted less significant changes
aphids also
previously
tiie relative content of ASN. A
affected the amino acid
phloem exudates. The relative
plante that
as
composition, namely on
infestation with
content of ASN in
from the apex, whereas the fractions of the other
content of ASN
infested with
aphids
whereas the relative content of ASP and PHE
was
previous
composition of the
significantly higher
than in uninfested
were
in
plante,
lower.
presented here may be of particular importance in explaining the
development of aphid populations under different levels of water supply as
well as for the understanding of the preference for young (growing) tissues by
A. oomi. Asparagine has been reported to support faster development of M.
The results
oersicae. Brevicorvne brassicae
(L) and Sitobion avenae (F.)(van Emden and
Bashford, 1977 cf. Kuo-Sell, 1989; Weibull et al., 1986). In addition, ASN has
130
highest N/C ratio (2/4) of all the protein amino acids (cf. Girousse et al.,
1991). This again is of advantage to the aphids, because N is arguably the
the
limiting chemical element in their nutrition. Since, additionally, symbionts
aphids' gut may upgrade ASN to essential amino acids, ASN is
probably an "optimal" compound in the aphids' diet. The relative content of
ASN in the phloem might therefore be a determining factor influencing aphid
most
in the
performance and population development.
The resulte of this
study support
(1) A- pomi generally prefers young
hypothesis
growing tissues as feeding sites. The relative content of ASN was significantly
in a number of ways:
this
higher in phloem
exudates from the apex than from basal leaves. Not
only the
relative content, but also ASN concentration (per unit sample tissue)
was
in exudates from the apex than from basal leaves.
significantly higher
Hugentobler (1990) similarly reported higher concentrations of all amino acids
(except TYR) in the exudate collected from sink leaves as compared to
population
density. The relative content of ASN in the phloem exudates
decreased significantiy with increasing water stress. (3) An aphid infestation
leads to higher relative content of ASN in the phloem exudates compared
with uninfested plants. The greater the population size and density, the bigger
source
leaves. (2) Water stress of the host clearly reduces aphid
size and
were
the differences in the ASN fraction. The ASN export from basal leaves
seemed to be significantiy increased
which
aphids
can
(whether by their "sink" effect
their
by aphid infestation. The mechanisms by
influence their hosfs
or
phloem composition are not clear
actively by injecting salivary secretions into
host).
The relative content of
other,
even
LEU, VAL and CYS, GLU, ASP
tion size and
or
density. Regarding
essential amino acids such
as
ORN seemed not to affect
aphid popula¬
THR, HIS,
the effects of water stress as well
as
of
aphid
proportion
population size decreased. On the other hand, it would be of interest to study
the development of glutamine in this context. Glutamine, which could not be
measured in this study, can occur in similar proportions as ASN in the phloem
sap (Kollar and Seemuller, 1990) and was reported to support faster develop¬
ment of M. persicae (van Emden and Bashford, 1977 cf. Kuo-Sell, 1989).
while
sample position, these amino acids actually increase in
Many plante respond
tissue
as
well in the
to water stress
by
a
marked increase in
proline in their
phloem (Hsiao, 1973; Miles et al., 1982; cf. Mattson and
Haack, 1987; cf. Holtzer et al., 1988). Miles et al. (1982)
even
stated that in
absolute quantity proline overshadowed all other amino acids in
stressed
plante. In the present study,
the relative content of
proline
some
increased
131
however,
with water stress. This increase,
was not
sugars to water stress
(Irigoyen
is known to affect amino acid
water stress,
et
significant, probably
due
organic
respond
al., 1992) and the nature of water stress
to several reasons: Proline seems to
later than
acids and
composition. For example, under progressive
proline (and glycinebetaine)
were the
dominant accumulated
compounds measured in wheat extracts, whereas rapid stress resulted in the
accumulation of a number of other amino acids, particularly amides (NakJu et
al., 1990). Towards the end of the experimente of this study, plante became
relatively big
resulting
and their soil volume rather limited
in
a
fast water
stress build up and shorter
watering intervals, which could therefore have
affected proline accumulation. Further, most amino acids including proline are
completely metabolized
upon
present study demonstrated
proline
actually
in the
rewatering (Naidu
et
al., 1990). Although the
significant changes
phloem exudates, the absolute amounts of proline might
have increased
(see Fig.
It should be noted that
in the relative content of
no
28
according
below).
to
some
authors, proline correlates
negatively with the growth of M. persicae (Van Emden and Bashford, 1977 cf.
Kuo-Sell, 1989). Therefore, negative effecte of proline on aphids can not be
excluded. In addition, whether
an amino acid acts as a phagostimulant or not
probably depends on the aphid species, morph, physiological state of the host
plant and other circumstances.
In
general, levels of soluble nitrogen
tissues under water stress
Miles et al.
are
reported
to increase in organs and
and Haack, 1987; Naidu et al.,
(Mattson
(1982) reported that water
content of all amino acids in rape leaf extracts as well
In tiie
study presented here, the
exudate (as well
as
1990).
stress caused an increase in the
as
in pure
phloem sap.
amino acid concentration in the
the concentrations calculated per unit of
phloem
plant tissue) of
apple plante decreased with increasing intensity of water stress (Fig. 26). The
reason
for the
divergence
in results of this
study from those quoted above will
be discussed below.
Using the EDTA-exudation technique allowed the
tration of total sugar and total amino acids
the exudate solution. To
or
assessment of the concen¬
any of their
componente only in
assume that the concentration found in the exudates
reflect absolute concentrations present in the phloem is probably wrong,
particulariy under conditions of water stress. Under conditions of water stress
it can be
decreases
expected that the flow rate
(higher phloem viscosity and
out of the
phloem into the solution
High phloem
lower turgor pressures).
132
viscosity
possible
probably
was
the
reason
why
phloem
plante. Furthermore,
water stressed
in
a
preliminary experiment it was
not
feeding
on
sap from severed stylets of aphids
to collect
the
significant decrease
potential with water stress (see page 83)
pressure relations in the
in
plant
impact
must have an
water
on
the
phloem sap.
Figure 28 presents a hypothetical scheme relating the effect of varying
phloem sap concentration and flow rate on the concentrations recovered in
the
phloem exudates (considering sample size). The
flow
rate
and
development
concentration
are
assumed
based
patterns of
theoretical
on
considerations and reports in the literature. Flow rate and concentration will
mainly determine
how much will flow out of the
phloem sap into the
solution
and thus determine the solute concentrations measured in the exudates. In
the
hypothetical scheme presented in Fig. 28, the concentration of total amino
acids in the phloem exudate decreases with increasing water stress. Total
sugar,
increases
however,
decreases
again
as
initially until moderately stressed and then
stress becomes more severe.
1
1
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Rate trati
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o
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100
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80
S
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60
D
or
fl>
rn
100
-
8U
-
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-
40
-
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-
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-
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£•
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xtra ntra
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t-t-
o
-
20
3
a?
oL
MODERATE
CONTROL
SEVERE
Treatment
Flow Rote:
Phloem Sap Concentration:
Extract Concentration:
Fig. 28.
Hypothetical
and the
the
scheme
on
and Amino Acids
the concentration of
resulting concentration
phloem
Sugars
Sugars
Sugars
Amino Acids
Amino Acids
phloem sap,
flow rate
in the exudate solutions collected from
of plants grown under different water
regimes.
133
The concentration patterns observed in the
sample size)
in this
study
conform to those
therefore not unreasonable to
patterns actually developed
It
can
be concluded that
the overall
composition
assume
were
phloem exudates (considering
presented
that the flow rates and concentration
much
as
presented in Fig. 28.
changes in the composition
of the
in the model. It is
of amino acids and in
aphids' diet may be of greater importance for
aphid population growth (size and density) than general changes in total
(and/or carbohydrate) contents. Besides the fraction of specific
particulariy amino acids, also the ratio of total sugars to total
amino acids in the phloem sap may be of great importance: this ratio
increased up to 10-fold due to water stress in the phloem exudates, and was
up to 10-fokj higher in exudates from basal leaves than from the apex. These
relativities are particularly important, since even if the phloem analysis were
amino acid
sugars and
to contamination, the relative increase in amino acid content seems
beyond doubt. Moreover, the much greater increase from the basal leaves
subject
particular significance to the insects, since mature leaves are of
quality to the insects before infestation. The aphids'
response to changes in the phloem sap quality of the plant was probably
conditioned by both physiological (nutritional) and behavioral (phagostimulant
factors). Since the effect of water stress on aphid population size and density
would be of
inferior nutritional
was
it
less
can
phenols
istics)
severe
than the effect of leaf age
be assumed that other
or
other defensive
compounds
not assessed in this
population development.
(apex vs basal leaves), however,
important leaf characteristics (e.g. content of
study,
well as physical leaf character¬
additionally have affected aphid
as
must
Leer
-
Vide
-
Empty
135
5
Conclusions
An
analysis of biophysical and biochemical changes
in
under well-watered and water stressed conditions may be
apple plants grown
expected to
lead to
better understanding of the interrelationship between host (Malus domestica
Borkh.) and aphid (Aphis pomi De Geer) under different levels of water
supply. Nevertheless, the changes induced in the plant by ongoing water
stress are not uniform within the plant and present a continuum of effecte in
time, some stages of which may be advantageous to the insects, whereas
a
others
are
not
Effects of Water Stress
5.1
on
the Host Plant
Water stress reduced plant growth and biomass production
in all the
same
experimente of this
in all four
study.
(FW, DW, LA)
The extent of these effects
was
not the
experimente. Factors which may have influenced the degree
of reduction included among others the
pattern of
water stress
(the rate,
intensity and duration), experimental conditions (e.g. pot size and shape,
plant size), and environmental conditions (e.g. soil fertility, light intensity). In
experiments 1 and 2, plant growth decreased gradually with increasing
intensity of water stress, whereas in experiments 3 and 4, a critical moisture
stress level pF^ ca -0.69 MPa) developed, below which plant growth was
significantly reduced.
potential of leaves decreased with a decrease in leaf water
potential maintaining turgor pressure or at least delaying a decrease in turgor
The osmotic
pressure in leaves,
a
process known
as
osmotic
adjustment.
In all four
136
experiments, plante
were
adjust osmotically
able to
to water stress, with the
exception of plante in experiment 2 which showed very low osmotic
adjustment. A greater part of the osmotic adjustment could be attributed to
active accumulation of solutes. Osmotic adjustment was accompanied by an
increase in the concentration and relative contents of stress substances in the
phloem such
as
sorbitol, the major carbohydrate detected in the phloem of
apple plants. Proline, although a minor contributor
phloem sap also increased with water stress.
The total concentration of
sap
was
carbohydrates
shown to increase with
solution,
and amino acids in the
increasing intensity of water
concentration of amino acids detected in
EDTA-buffer
to the amino acids of the
phloem exudate collected
decreased
however,
and
that
of
increased with water stress. Concentrations measured in the
do not
necessarily reflect the concentrations
rate out of the
size
or
in the
phloem probably decreases with
diameter of the sieve tube,
phloem
stress. The total
sap
in an
carbohydrates
phloem exudate
phloem sap, since the flow
(depending on
pressure). The
water stress
viscosity
and
composition of phloem sap
was shown to change under conditions
compared with well-watered conditions.
concentration of carbohydrates and amino acids as well
of water
stress
The
composition also varied with leaf position within plants, i.e. with
stage of maturity. Generally, the concentration of amino acids
the
their
as
leaf age
or
higher
in
was
phloem sap of the apex compared with mature, basal leaves, whereas the
concentration of
higher and that
carbohydrates
was
lower. The relative content of ASN
of CYS and GLU lower in the
that of the basal leaves. Further, the
of the
phloem
due to water stress
phloem
changes in the amino
were not
was
sap of the apex than in
the
same
acid
composition
in the apex and the
mature, basal leaves (e.g. GLU, ASP, CYS).
Leaf surface temperature tended to increase with
increasing intensity of
3°C, and
water stress. The differences due to water stress did not exceed
after
rewatering,
as
well as at
night,
the differences
disappeared. Leaves
situated in the lower parts of the plant had lower leaf surface temperatures
than leaves in the upper parts. Beside color, size, orientation of leaves, the
distance to the
source
of artificial
light
in the
growth chamber to
determined leaf surface temperatures. This
because
was a
changes in surface temperatures due
situated in the upper parts of the
plant
were
a
large extent
drawback in this
study
to water stress in leaves
overshadowed
by
this artefact.
137
As in most
Plants
in pots and under controlled environ¬
extrapolation of resulte to the field is problematic.
experiments conducted
mental conditions, direct
growing
stress than
in pots
are
in
general subject to
in the field which
plants
rapid
more
and intense water
may reduce their
ability
to
adjust
phloem quality differentially
gradual and uniform water stress development as generally encountered in
the field. This certainly may affect not only overall plant growth, but
osmotically
and also affects
than under
particulariy the development of aphids
on
these
plante. Relating
a more
measure¬
potentials at the peak of drying cycles to plant growth
and characteristics can, therefore, be misleading, since the actual nature of
ments of soil matric
sufficiently by these measurements alone.
Many plant characteristics such as plant growth, leaf surface temperatures,
the componente of plant water potential and probably also phloem sap
the water stress is not described
characteristics
(flow rate, pressure, quality) oscillate with the pattern of water
point measurements in time and space
stress. A more sensitive method than
would be needed to characterize water stress, if stress
rate of
development
are to
be
intensity, duration and
successfully integrated into a comprehensive
plant and insects. This
characterization of water stress as it affects both
particularly important for the extrapolation of resulte from studies in
pots under controlled environmental conditions to field conditions.
would be
study, it can be concluded that water stress resulted in
biophysical and biochemical characteristics of the plant which
affected aphid population development and growth, although the kind and
As for the present
changes
in
extent of such effects were not
to measure
or
Effects of Water Stressed Plants
5.2
the
The effect of
interpret.
on
Population Dynamics of Aphids
plant
water stress
rate of K pomi was studied
and the
always easy
on
using
the
two
population development and growth
approaches: the life table approach
density-dependent population approach.
Life table approach. The intrinsic rate of natural increase rm,
of population growth which combines information
survival rates and the
age-specific fecundity,
was
on
the
a
descriptor
development time,
generally
not
significantly
affected by water stress in this study. Nevertheless, the development and pre-
138
reproductive time
time of aphid
higher
of larvae and
populations
aphids
as
the
generation and doubling
aphid fecundity
with well-watered
plante compared
in water stressed
in leaf surface temperature which
induced the
well
as
tended to be shorter, whereas
slight changes
in the
mediated
were
by
plants.
water stress
population parameters
of
was
Increases
probably
aphids.
for only insignificant changes in rm under the severe water
applied in this study were: Differences in leaf surface
temperatures due to water stress were not high enough to affect aphid
development significantly and/or the variability in temperature because of
Possible
stress
reasons
levels
factors other than water stress, such
differences due to water stress
effect of
changes
important
reason
leading
in leaf surface
is that
the distance to the
as
source
of
light
growth chamber, overshadowed temperature
and ventilation within the
to
an
underestimation of the
temperature due
aphids had
a
potential
to water stress. Another
wide choice of microclimates and
feeding sites within their host plant, which they could easily reach simply by
moving
A
short distances
significantly
lower rm
the host plant.
on
measured for
was
leaves situated in the lower parts of the
growing leaves situated
on
aphid cohorts feeding
plants compared
on
mature
with those
feeding
in the upper parts. Differences in leaf surface
temperature alone, however, could
not
Life table construction and
are
analysis
sufficiently explain
the difference in rm.
useful for comparing the
of increase of individuals or cohorts of
a
species
potential
rate
under defined conditions.
However, extrapolation of the intrinsic rate of natural increase of individuals
or
cohorts to
because
populations
with
population density
The nutritional
quality of
a
mobility
of individuals
restricted at
high densities.
the
Population approach.
high densities has
to be done with
caution,
may affect factors which in turn may influence rm:
host
plant is affected by population density, and
(choice of optimal feeding and birth sites) is
The rate of
aphid population development
was
affected by water stress induced by intermittent drying. In contrast
negatively
slightly higher rm under
to the
water stress
compared with well-watered
experiments 1 and 2, the size and density of aphid
populations decreased significantly with water stress in experimente 3 and 4.
conditions found in
aphid development, below which the size
significantly reduced, seemed at "F^n < -0.69 MPa
peak of a drying cycle). The effect of fluctuating
The critical moisture stress level for
of
aphid populations
(measured
at
experimental
the
was
conditions
on
aphid population
size
represents
a
longer
term
139
effect and
therefore
summarizes the
corresponding changes in plant
drying. Plant growth and
factors
had
which
under
water stress and which
physiological
changed
had
an
on
possibly
aphid population development were: the rate of
impact
and
plant growth
production of new tissue, leaf surface temperatures, plant
characteristics which change under intermittent
water relations and
phloem feeding quality.
The reduction in
the rata of
aphid population size was closely related with a decrease in
plant growth, i.e. the production of young tissue, which are
aphid species. A decrease in
length with water stress indicated
that the magnitude of this response changed under water stress and that
other factors beside shoot length affected the development of aphid
greatly preferred sites for the nutrition of
aphid density per leaf
or
most
per unit of shoot
populations.
Significantly smaller populations
leaves of the lower parte of the
aphids and lower densities on mature
plant further confirmed the importance of
of
newly produced young tissue for aphid development. The preference of the
apple aphid for young tissue resulte in the higher susceptibility of apple
green
trees to
aphid infestation
in
spring compared with
ceased and most leaves are mature.
rather than older,
bigger
trees are more
The differences found in the
summer
when
growth has
Further, it explains why young
susceptible
to
aphid
trees
infestation.
population characteristics of aphids (size and
density) under well-watered and water stressed conditions and/or within the
plant could not be sufficiently explained by differences in leaf surface
temperature due to water stress. Several phloem sap characteristics such
as
phloem sap viscosity, pressure, carbohydrate and amino acid concenbation
as
well
and
as
composition
intermittent
are expected
drying and exert
to vary under water stress conditions
a
more
significant effect
on
aphid
development than leaf surface temperatures.
phloem sap viscosity and pressure were expected to become
limiting only under very severe water stress. The increase in the
concenbation of carbohydrates as was observed under conditions of water
stress, increases the viscosity of phloem sap (Ziegler, 1975) and may thereby
decrease sap flow. In addition the significant decreases in the componente of
plant water potentials with water stress measured in this study, may indicate
a decrease in phloem sap pressure. Although turgor pressure of the sieveChanges
in
tubes and
capillarity
may have
a
considerable impact
on
aphid feeding,
140
aphids
are
able to suck
actively with the ciberial pharyngeal pump when
necessary.
Although amino acid concentrations in the phloem sap increased with an
increase in water stress, the carbohydrate to amino acid ratio increased up
proving that carbohydrate concentrations increased
to 10-fold
extent than amino acid concentrations. A
ratio renders the
have to invest
quality
more
The most apparent
which
were
of
high carbohydrate
greater
phloem sap less favorable for aphids which then
energy in
disposing
of the excessive sugars consumed.
changes in phloem sap composition with
closely related
to a
to amino acid
to the size and
water stress,
density of aphid populations,
were
the increase in the relative content of sorbitol and the decrease in the fraction
of ASN. The relative content of other amino acids
stress. The fraction of amino acids such as
even
of essential amino acids such
water stress.
THR, HIS, LEU
as
also affected
CYS, GLU, ASP
This, however, seemed to have
development, probably
was
or
effect
no
quantities or because they
inhabiting the aphids' gut.
may be
by
water
ORN and
VAL increased with
aphid population
already found in
on
because these amino acids were
sufficient
or
supplemented by symbionts
In this study, the relative content of ASN in the phloem was found to be a
determining factor influencing the development of A^ pomi populations.
Asparagine (ASN) is present in high
amounte in the
transport of N because of its high N/C ratio and is
acid
a
phloem, is efficient in the
good
precursor for amino
upgrading by symbionts.
The size and
individuals
density
were
of
aphid populations
significantly higher
mature leaves situated in the lower
watered
plante. The carbohydrate
in mature
on
as
well
growing leaves compared with
parte of the plant, particularly in well-
to amino acid ratio was up to 10-fold
leaves, and the relative content of ASN
confirms that the
apple plant
body weighte of aphid
as
is not
a
higher
significantiy lower. This
was
homogeneous
source
of nutrition for
insects.
The content of phenols and other defensive
well as
physical
thickness
were
leaf characteristics
not determined in this
compounds (allelochemicals) as
as
leaf hairiness,
study.
toughness and
These factors may also be
important limiting factors for aphid population growth and may be subject
changes under conditions of
water stress and/or due to
position within
to
a
141
plant Newly expanding leaves are reported to contain relatively low amounts
of
allelochemicals, whereas the
mature leaves have
relatively high levels of
defensive allelochemicals. Water stress may exert differential effects
on
the
production of allelochemicals, which may depend on the plant species, the
compound under consideration, and environmental/experimental conditions.
It
can
be concluded that among the factors assessed in this
production of
new
and young
study, the
plant tissue under well-watered conditions and
changes in phloem sap quality under water stressed conditions were the main
factors
influencing aphid population development.
Effects of
an
the Green
Apple Aphid
5.3
The effect of
aphids
water stress and
on
the Host Plant
plant growth and development, the interaction of
aphid infestation
feedback effecte of
to understand the
on
Infestation with
on
the
aphid infestation and
plant,
as
well
as
the
water stress may be of
potential of aphid population growth
and
possible
importance
development.
aphid densities (as in experiment 3), overall plant growth was
significantly affected by an aphid infestation. At "high" aphid densities (as
experiment 4), however, mildly water stressed plante pF^ £ -0.69 MPa)
At "moderate"
not
in
aphid infestation. In the well-watered and the two
Exp. 4, plant growth was only reduced by
moderately
before
few
aphids a
days
plant growth had completely stopped due to high
aphid densities, whereas the growth of mildly stressed plante was clearly
suffered the most from
an
stressed treatmente in
decreased
by aphid infestation during the experiment and even at low aphid
growth of aphid infested plante
densities. The critical moisture level for
(Y^g >
{4^ <
-0.69
MPa) developed below that of aphid uninfested plante
Fig. 29). Thus, a critical moisture range was identified
-0.69 MPa;
within which assimilate drain
adjust osmotically
decrease
a
by feeding aphids reduced the plants' ability to
large enough to significantly
to water stress to an extent
plant growth: although
negative
effect
on
osmotic
infestation with
adjustment
translated into reduced plant
stress.
an
aphids generally exerted
plants, this was
of water stressed
growth only
under conditions of mild water
142
9000
1.5
ra
8000
1.4
'-g_
7000
1.2
-
3
O
CD
U)
<
a
^-v
a
6000
h-
1 n
o
0.8
.o
E
J
3
\c/>
Q.
5000
fe
—
4000
3"
D
*<
O
O
**s
r-*-
0.6
3
[—
CD
2
3
3000
0.4
3"
0.0
-1.0
-0.5
-1.5
Soil Matric Potential
Mild
Treatment: Control
Fig.
(MPa)
Mod. I
Mod. II
interdependence of plant growth (increase in shoot length per
day) and aphid population size under different water supply levels.
Bars:
Aphid population size per plant
The
29.
Squares
/ solid line:
Growth of
Diamonds / dotted line:
Error bars:
Under field conditions, plants
are
aphid uninfested plants
Growth of aphid infested plants
Standard error
most
likely growing in the range of critical
moisture defined above most of the time. Under "unlimited" water
plante
were
supply,
able to compensate for the losses in assimilates withdrawn
aphids possibly
due to
positive
feed back
on
photosynthesis
caused
by
by
an
degradation and mobilisation of metabolites. In
the range of critical water supply, however, even relatively low aphid densities
significantly restricted plant growth by the consumption of assimilates and
additional sink and/or due to
adjustment to maintain
plante). Under more severe
solutes needed for active osmotic
growth (as
in uninfested
growth
dominated
was
damage that
an
It follows that
effects of water stress,
aphid infestation could
an
when the drain
by the
exert became
less normal
water stress,
so
plant
that the extent of
insignificant.
apparent reduction of overall growth of the plant resulte
of assimilates exceeds the capacities of the plant for
compensatory growth, i.e. when the carrying capacity of
aphid density
production decreased with
Thus, the
more or
a
plant is surpassed.
threshold for significant loss in biomass
water stress due to a reduction in the
carrying
143
capacity of
plant under
a
slower on water stressed
development time (a difference
experiment 4) compared with well-watered plante.
plante stopped after
stressed
of 12
Although aphids developed much
plante (see experiment 3), plant growth of water
water stress.
days
in
The results of the study
a
much shorter
presented here confirm
affect both the concentration as well
as
the
that an aphid infestation may
composition of phloem sap.
Higher concentrations and significantly greater proportions of ASN, the major
transport amino acid identified in this study, in phloem exudates of previously
aphids exerted
effect, hereby increasing transport
feeding sites.
Additionally, the larger the colony, tiie more powerful the sink effect. Aphid
infestation also significantly altered the composition of the phloem sap. The
fraction of the nonphagostimulant sorbitol was significantiy lower, whereas the
fraction of ASN, apparently an important amino acid for A. oomi nutrition, was
significantly higher in phloem exudates collected from plant previously
infested with aphids compared with uninfested plante. The mechanisms by
infested compared with uninfested apices confirmed that the
a
of solutes to
sink
aphids
which
can
alter their nutritional basis in this way are not well
understood. Possibly the
induce
changes
plant due to
aphids.
an
in
injection of salivary secretions
into the
plant
may
plant metabolism and/or degenerative changes within the
additional sink effect, i.e. in
direction that favors nutrition for
a
the
An
aphid infestation that is increasing presumably stimulates allelochemical
defenses of the
plant making
it less attractive and nutritious.
defenses
are
overwhelmed
Eventually,
a
size where allelochemical
cooperatively by the
insects. Under conditions of
however, the aphid population may reach
water stress, either the concentration of allelochemicals increases in the
making
it
more
difficult to overwhelm the
plant defenses
or
plant
water stress
decreases allelochemical concentrations but also reduces plant feeding
quality to such
were
a
level that
allelochemicals
a
can
population
of
aphids cannot build up to the point
(P.W. Miles, University of
be overwhelmed
Adelaide, South Australia, pers. comm.).
Numerous biotic and abiotic factors which influence the development of aphid
populations under increasing levels of water stress could be identified in this
study. Due to the high complexity of the system, however, the complete
elucidation of certain
(e.g.
metabolic
system.
cause
pool model)
require additional work
complete understanding of the whole
and effect relations would
to allow a
Leer
-
Vide
-
Empty
145
6
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159
Appendix
Table 1.
Propagation and rooting media modified according to Hugentobler
(1990) used for the micropropagation of apple (cv. Golden Delicious)
according to Wermelinger (1985).
Propagation
Rooting
medium
medium
Macronutrients
mM
mM
CaCI,*2H20
MgS04*7H20
3.0
1.5
1.5
0.75
KNO3
18.8
9.4
NH4N03
KH,P04
FeS04*7H2O
Na^-EDTA
20.6
10.3
1.3
0.63
0.1
0.05
0.1
0.1
Micronutrients
pM
jiM
MnSC-4*H20
ZnS04*7H20
H3BO3
100
50
30
15
100
50
2.5
Kl
5
Na2M04*2H20
00012*6^0
CuS04*5H20
1
0.5
0.1
0.05
0.1
0.05
Vitamins
pM
pM
myo-inositol
560.0
thiamin-HCI
\2
Hormones
mg/L
mg/L
IBA
0.2
0.2
6BA
1.0
g/L
Sucrose
Bacto-Agar
pH without agar
g/L
30
10
8
7.5
5.5
5.7
160
Table 2.
of the Hoagland solution (1N) modified
according to Hugentobler (1990) and used in the
present study.
Composition
Concentration
Macronutrients
|
2
Ca(N03)2*4H20
MgS04*7HzO
0.025
KCI
3
KN03
NH4H2P04
0.5
Micronutrients
uM
Fe-EDTA
50
MnS04*4H20
ZnS04»7H20
H3BO3
0.5
5
25
Na2Mo4*2H20
CoS04*7H20
0.25
CuS04*5HzO
0.5
0.1
Concentration of nutrients (in
Ca 80, N 105,
Fe 2.8,
(mM)
Mg 24,
ppm):
S 32, K 118.5, CI 0.9, P 15.5,
Mn 0.275, Zn 0.033,
Co 0.06, Cu 0.032.
B 0.27,
Mo 0.024,
161
Abbreviations and
*g
*m
¥
^0
*p
*soil
Symbols
gravitational potential (MPa)
matric potential (MPa)
ALA
alanine
ASP
asparticacid
potential (MPa)
leaf osmotic potential (MPa)
leaf turgor potential (MPa)
ASN
asparagine
ARG
arginine
CYS
cysteine
soil matric potential (MPa)
GLN
GLU
glutamine
glutamic acid
glycine
leaf water
X
development time (days)
GLY
"x
survival rate
HIS
fiistidine
mx
age-specific fecundity (larvae/female)
ILE
isoleucine
rm
intrinsic rate of natural increase
LEU
leucine
"o
net
LYS
lysine
G
generation time (days)
DT
population doubling
(%)
reproduction rate
time
(days)
L1-L4 first to fourth larval instar
+A
plante which
-A
plants
DW
were infested
which were not infested
FW
dry weight (g)
experiment
fresh weight (g)
LA
leaf
Exp.
by aphids
area
MET
methionine
ORN
ornithine
PHE
PRO
phenylalanine
proline
SER
serine
THR
threonine
TRP
tryptophan
TYR
tyrosine
VAL
valine
ABA
abscisicacid
(cm2)
Mod.
moderately
PPFD
photosynthetic photon flux density
6BA
benzyladenine
(umol/nr/sec)
IBA
indole
ETH
WSL/FNP
water stressed
Eidgenossische Technische Hochschule, Zurich.
Eidgenossische Forschungsanstalt fOr Wald,
Schnee und Landschaft, Birmensdorf.
butyric acid
Curriculum Vitae
Name:
Rima Mekdaschi Studer
Birthday:
July 18,1961
Place of Birth:
Beirut, Lebanon
Parents:
Gudrun and Badreddin El-Adou Mekdaschi
Nationality:
German
Status:
married to C. Studer
Education:
1967 -1980:
German School of Beirut, Lebanon.
Baccalaureat 2eme Partie
1980-1986:
American University of Beirut, Lebanon.
Bachelor of Science in Agriculture
Master of Science,
1989-1994:
Federal
Major: Crop Production
Technology (ETH) Zurich,
Institute of
Switzerland.
Experience:
1983 -1986:
Graduate and research assistant at the American
University
1986-1988:
Research
of Beirut, Lebanon.
assistant
at
the
Institute
Nutrition, University of Hohenheim,
1988-1989:
Research
assistant
Sciences of the
at
the
of
Plant
Germany.
institute
of
Plant
Federal Institute of Technology
(ETH), Zurich, Switzerland.
1989-1994:
Ph.D. thesis at the Institute of Plant Sciences of
the Federal Institute of
Switzerland.
Technology (ETH), Zurich,
Acknowledgments
I wish to express my
support and
profound gratitude
understanding during
I am very thankful to Prof. J.
the
I thank Prof. J.J. Oertii for the
plant
guidance,
writing phase of the thesis.
Nfisberger,
Schmidhalter for their critique and advice
the
to Prof. S. Dorn for her
Dr. J.
as
Baumgartner,
and Dr. U.
co-examiners.
opportunity given to work on a Ph.D. thesis
cooperation with the Entomology group.
in
nutrition group and in
My heartful thanks go to Prof. P.W. Miles (University of Adelaide, South
Australia) and to Dr. C. Studer (Federal Institute of Technology Zurich,
Switzerland) for many valuable comments and suggestions on both the
experimente and the manuscript
Most
sincerely
I thank my
colleagues
and friends at Eschikon for their
help,
technical support, advice, discussions, encouragement and the many nice
moments
we
had. I like to mention
whom I may have overlooked:
Urs
a
few
names
and
apologize
to those
Sera, Michel, Peter, Fritz, Christoph, Urs H.,
Sch., Charlotte, Yuncai, Felix, Hans D., Richi, Michael, Jeannette,
Theres, Emil,
etc.
Last but not least I wish to thank my
family and
husband
love, moral support and patience in all situations.
Christoph for their