Download Leaf beetle feeding patterns on and variable plant quality in

University of Joensuu, PhD Dissertations in Biology
No:10
Leaf beetle feeding patterns on
and variable plant quality in
Betulaceous and Salicaceous hosts
by
Arsi Ikonen
Joensuu
2001
Ikonen, Arsi
Leaf beetle feeding patterns on and variable plant quality in Betulaceous and Salicaceous
hosts. - University of Joensuu, 2001, 154 pp.
University of Joensuu, PhD Dissertations in Biology, n:o 10. ISSN 1457-2486.
ISBN 952-458-074-8
Keywords: Alnus, Betula, Populus, Salix, Agelastica, Chrysomela, Galerucella, Lochmaea,
Phratora, Phytodecta, Plagiodera, chemical defence, chlorogenic acid, condensed tannins,
feeding cue, herbivory, host race, nitrogen, performance trade-off, phenolic glucosides.
Many European leaf beetle species have been recorded both on Betulaceous and Salicaceous host
plants. Accordingly, Agelastica alni L. and Galerucella lineola F. were frequently found on hosts
of both of these plant families, in eastern Finland. However, the host utilization strategies of
these two leaf beetles are very different. For A. alni, alders (Alnus spp.) are the natural primary
hosts, and certain willows (Salix spp.) are used as secondary hosts, especially in high population
densities. A. alni individuals found on different plant families appear to be equally adapted to
individual plant species. In contrast, G. lineola populations associated with Betulaceous and
Salicaceous host plants differ in their behaviour and physiology. In fact, Betulaceae- and
Salicaceae-associated G. lineola beetles may represent distinct host races. Since the hosts of
alternative plant families seem to favour different physiological adaptations in beetles, further
genetic differentation of the host races is likely. Another studied five leaf beetle species were
mainly found on Salicaceous hosts, but in some cases they can obviously have analogous host
races, as demonstrated with G. lineola.
Host utilization patterns of studied leaf beetles are governed by secondary leaf phenolics,
due to the high deterrent activity of many of these substances. Even an association with the
phenolics of a certain structural group does not necessarily pre-adapt leaf beetles to all individual
compounds in a particular group. Thus, willow phenolic glucosides strongly restrict the
utilization of Salicaceous plants by A. alni, even though the leaves of its primary hosts, alders,
also contain certain specific phenolic glucosides. A. alni feeds only on Salicaceous plants with
a low level of phenolic glucosides in their leaves. Similarly, most other studied leaf beetles also
appear to be sensitive to high amounts of willow glucosides. Moreover, leaves of certain phenolic
glucoside-rich willows also contain high amounts of another deterrent phenolic, chlorogenic acid.
The effects of these potent repellents, however, may depend on the background composition of
other plant biochemicals. This indicates that the distribution of stimulants can also affect the food
selection of leaf beetles. A lack of specific stimulants probably explains why A. alni do not even
accept the deterrent-poor willows as well as alders. On the other hand, it is uncertain what those
leaf traits are to which G. lineola beetles associated with the alternative host plant families
respond differently to. However, the phenolic glucosides specific to plant families are probable
candidates for this due to the generally high bioactivity of phenolic glucosides. At the intraspecific level of plants, among conspecific clones and within individual plants, leaf nutritive
traits, such as nitrogen content, may have a decisive role as determinants of leaf quality for leaf
beetles. In addition, the variation in abiotic environmental conditions may sometimes outweigh
the effects of variable food quality on host utilization patterns of leaf beetles. Consequently, leaf
beetles may, in some cases, even aggregate on low-quality host plants.
Arsi Ikonen, Department of Biology, University of Joensuu, P.O. Box 111, FIN-80101 Joensuu,
Finland
CONTENTS
LIST OF ORIGINAL PUBLICATIONS
1. INTRODUCTION
7
2. THE SYSTEM
9
2.1. Plants
9
2.2. Insect herbivores
9
3. GENERAL METHODOLOGY
10
4. PATTERNS IN LEAF CHEMISTRY
11
5. PATTERNS IN LEAF BEETLE HERBIVORY
13
5.1. Utilization of the host plants of two families by leaf beetles
13
5.2. Leaf chemicals as determinants of leaf quality
15
5.3. Plant hybridization and leaf beetle herbivory
17
5.4. The importance of variable food quality in relation to other factors
18
6. CONCLUDING REMARKS
19
ACKNOWLEDGEMENTS
20
REFERENCES
20
LIST OF ORIGINAL PUBLICATIONS
This thesis is based on the following articles, referred to in the text by Roman numerals.
I
Ikonen, A., Sipura, M., Miettinen, S. and Tahvanainen, J.: Preference and
performance patterns of alder- and willow-associated Galerucella lineola beetles.
Submitted (Entomologia Experimentalis et Applicata).
II
Ikonen, A., Tahvanainen, J. and Roininen, H.: Phenolic secondary compounds as
determinants of the host plant preferences of the leaf beetle, Agelastica alni.
Submitted (Chemoecology).
III
Ikonen, A., Tahvanainen, J. and Roininen, H. 2001: Chlorogenic acid as an
antiherbivore defence of willows against leaf beetles. Entomologia Experimentalis
et Applicata 99: 47-54.
IV
Ikonen, A.: Preferences of six leaf beetle species among qualitatively different leaf
age classes of three Salicaceous host species. Accepted (Chemoecology).
V
Sipura, M., Ikonen, A., Tahvanainen, J. and Roininen, H.: Why does the leaf beetle
Galerucella lineola F. attack wetland willows? Submitted (Ecology).
VI
Hallgren, P., Ikonen, A., Hjältén, J. and Roininen, H.: Inheritance patterns of
phenolics in F1, F2 and back-cross hybrids of willows: implications for herbivore
responses to hybrid plants. Submitted (Journal of Chemical Ecology).
Raupp & Sadof 1989; Baur et al. 1991;
Seldal et al. 1994; Mutikainen et al. 1996).
Damaged plant individuals can induce this
kind of change even in their undamaged
neighbours (Dolch & Tscharntke 2000).
Thus, increasing population densities of
insect herbivores are likely to lead to
inhibitory feedback-loops through
decreased resource quality.
For herbivorous insects, the quality
of plant tissues for food depends mainly on
the concentrations of essential nutrients and
defensive secondary compounds
(Tahvanainen et al. 1985; Bryant et al.
1987; Lindroth et al. 1988; Kelly & Curry
1991; Clancy 1992; Rank 1992; Matsuki &
MacLean 1994; Hemming & Lindroth
1995; Van Dam et al. 1995; Stamp & Yang
1996; Orians et al. 1997; Kause et al.
1999). Nitrogen, in particularly, seems to
be generally scarce and a limiting nutrient
for herbivorous insects, since plant tissues
contain remarkably less nitrogen than
animal tissues (Feeny 1970; McNeill &
Southwood 1978; Mattson 1980). In
concordance, an increase in diet nitrogen
content has been frequently found to result
in improved insect herbivore performance
(Tabashnik 1982; Bryant et al. 1987;
Lindroth et al. 1997; Ritchie 2000).
Consequently, insect herbivores are
expected to evolve behavioural mechanisms to find and utilize plant tissues with
optimal nitrogen content (McNeill &
Southwood 1978). For example,
herbivorous insects can use amino acids as
feeding stimulants (Hsiao & Fraenkel
1968). In contrast, secondary plant
compounds often inhibit growth and the
development of insects and can even cause
mortality (Todd et al. 1971; Isman &
Duffey 1982; Manuwoto & Scriber 1986;
Bryant et al. 1987; Lindroth et al. 1988;
Kelly & Curry 1991; Matsuki & MacLean
1994; Hemming & Lindroth 1995; Ayres et
1. INTRODUCTION
Outbreaks of herbivorous insects (e.g.
Barbosa & Schultz 1987; Mattson & Haack
1987; Tikkanen et al. 1998) indicate that
the greenness of nature is not a self-evident
fact. Due to their high reproductive
potential and diversity, herbivorous insects
could probably exterminate green plants in
the absence of any limiting factors.
Normally, insect herbivore populations,
however, seem to be strongly limited by the
resource-based bottom-up forces (Hunter &
Price 1992; Roininen et al. 1996; Ritchie
2000). Apparently insect herbivores can
only properly adapt to a restricted range of
qualitative variation in plants, since an
increase in adaptation to a certain type of
food entails a decreased adaptation to
alternative resources (Gould 1979; Fry
1990; Jaenike 1990; Via 1991; Joshi &
Thompson 1995). Thus, herbivorous
insects tend to be more or less specific in
their host utilization (Smiley 1978; Bernays
& Graham 1988; Roininen & Tahvanainen
1989; Jaenike 1990; Kolehmainen et al.
1994; Baur & Rank 1996; Roininen et al.
1999). Even a relatively small inter- and
intra-specific qualitative variation in plants
usually has a great effect on the behaviour
and physiology of insect herbivores
(Larsson et al. 1986; Matsuda & Senbo
1986; Bryant et al. 1987; Meyer &
Montgomery 1987; Kelly & Curry 1991;
Bingaman & Hart 1993; Matsuki &
MacLean 1994; Hemming & Lindroth
1995; Van Dam et al. 1995; Orians et al.
1997). Consequently, herbivorous insects
have qualitatively adequate food available
only in limited amounts and for limited
times. Furthermore, insect feeding on the
basically high-quality host plants may
cause the qualitative detorioration of these
plants (Raupp & Denno 1984; Haukioja &
Hanhimäki 1985; Neuvonen et al. 1987;
7
reduce the relative disadvantage gained
from feeding on poor-quality hosts (see
also Feder 1995; Feder et al. 1995; Rossi et
al. 1999). If herbivorous insects obtain an
’enemy-free space’ on low-quality hosts,
these hosts may even be the most heavily
attacked ones (Damman 1987; Thompson
& Pellmyr 1991). On the other hand,
because of the physiological constraints of
insects the variation in abiotic environment,
in microclimatic conditions for example,
can also have a pronounced effect on the
host utilization patterns of herbivorous
insects in the field (Willmer et al. 1996;
Larsson et al. 1997). In some cases,
variation in abiotic factors may outweigh
the effect of food quality and lead to an
even higher insect herbivore load on lowquality hosts (Sipura 2000; Sipura &
Tahvanainen 2000). Overall, top-down
forces by natural enemies and abiotic
factors are likely to interact with the
resource-based bottom-up forces in the
regulation of natural insect herbivore
populations (Williams 1983; Hunter &
Price 1992; Ritchie 2000).
This thesis mainly focuses on the
consequences of variable food quality on
the feeding patterns of several
Scandinavian leaf beetle species
(Coleoptera: Chrysomelidae). Natural host
plants of the studied leaf beetles belong to
the Betulaceae and Salicaceae families.
Firstly, it is asked if plants of these two
families require and favour different
behavioural and metabolic adaptations in
leaf beetles, and if an increase in adaptation
to one host plant family entails a reduction
in adaptation to another host family (I, II).
Results obtained in laboratory experiments
are discussed in relation to natural host
utilization patterns of the studied species of
leaf beetles. Secondly, it is examined which
traits determine leaf quality for the leaf
beetles (II-V). To answer this, both
al. 1997). Secondary plant substances also
frequently act at the behavioural level of
insects as deterrents and feeding inhibitors
(Kraft & Denno 1982; Matsuda & Senbo
1986; Kelly & Curry 1991; Mori et al.
1992; Gross & Hilker 1994/1995; Van
Dam et al. 1995). Overall, many insect
herbivores may continuosly be faced with
an optimization problem of how to make a
compromise with the intake of essential
nutrients and harmful secondary
compounds (see Rhoades & Cates 1976;
Cates 1980; Meyer & Montgomery 1987;
Van Dam et al. 1995). However, there are
also well-adapted and highly specialized
insect herbivores for which the effects of
specific secondary compounds of their
natural main hosts are either neutral or
positive (Kraft & Denno 1982; RowellRahier & Pasteels 1986; Denno et al. 1990;
Rank 1992; Kolehmainen et al. 1994;
Matsuki & MacLean 1994; Rank 1994;
Soetens & Pasteels 1994; Gross & Hilker
1994/1995; Van Dam et al. 1995; Van der
Meijden 1996; Orians et al. 1997; Roininen
et al. 1999).
Apart from plant quality, a
herbivorous insect also encounters abiotic
conditions and natural enemies, parasites
and predators, on its host plant (Hunter &
Price 1992). It is known that natural
enemies can remarkably decrease survival
and population densities of herbivorous
insects and, consequently, herbivoryinduced damages on the host plants
(Häggström & Larsson 1995; Sipura 1999,
2001a). When herbivorous insects
aggregate on high-quality hosts and when
their natural enemies act in a densitydependent manner, enemy-induced
mortality of a herbivore may be higher on
the high-quality hosts (Sipura 2001b). This
means that feedback by natural enemies can
equalize insect herbivore densities on the
qualitatively different host plants and
8
especially economically important source
of raw material for plywood and paper
industry (Lines 1984; Oksanen 1987). As
fast-growing plants, alders and many
Salicaceous species can be grown in shortrotation forestry as a renewable source of
energy (Salmi 1993; Kendall et al. 1996).
preference and performance experiments
with chemically analysed plant material
and preference studies with pure secondary
compounds were conducted in laboratory.
A study with parental willow species and
their four hybrid categories tries to reveal
the inheritance patterns of main leaf
secondary compounds of these plants (VI).
Patterns in leaf chemistry are compared to
plant susceptibility for a natural community
of several leaf beetle species. In addition,
one of the articles explores the importance
of variable plant quality in relation to topdown and abiotic factors as determinants of
the field distribution pattern of Galerucella
lineola F. (V).
2.2. Insect herbivores
Betulaceous and Salicaceous plants in
northern Europe harbour a diverse
community of leaf-eating insects
(Kreslavsky et al. 1981; Shaw 1984; Dodge
et al. 1990; Soetens et al. 1991; Koch 1992;
Hanhimäki et al. 1994; Chinery 1997;
Rousi et al. 1997; Tikkanen et al. 1998;
Kause et al. 1999; Nyman 2000; Sipura
2000). One of the most prominent groups
among them are leaf beetles. Many
European leaf beetle species have been
found to feed both on Betulaceous and
Salicaceous plants (Tischler 1977;
Kreslavsky et al. 1981; Dodge et al. 1990;
Koch 1992; Palokangas & Neuvonen 1992;
Seldal et al. 1994; Gross & Hilker
1994/1995; Baur & Rank 1996). In some of
these species conspecific beetles associated
with different host plant families seem to
be separate host races (Kreslavsky et al.
1981; see also Gross & Hilker 1994/1995).
However, there are also species of leaf
beetles that only utilize the hosts of one of
these two plant families (Koch 1992).
All these leaf beetles are univoltine
insects which overwinter as adults (see
Baur & Rank 1996; Kendall et al. 1996;
Häggström 1997; Kendall & Wiltshire
1998; Sipura 2000). The overwintered
adults colonize their host plants in the
spring at budbreak, after which they mate
and feed on host plant leaves for a few
weeks before oviposition. The eggs laid on
the leaves hatch within a few weeks.
Larvae also feed on the leaves of the same
2. THE SYSTEM
2.1. Plants
In northern Europe, Betulaceous plants,
alders (Alnus spp.) and birches (Betula
spp.), and Salicaceous plants, aspen
(Populus tremula L.) and willows (Salix
spp.), often naturally grow together,
especially in early successional habitats.
All these plants are deciduous trees or
shrubs. The taxonomy of these plants is
complicated by the fact that in both plant
families con-generic pure species may form
inter-specific hybrids (e.g. Hanhimäki et al.
1994; Hjältén 1997). In both families, plant
leaves contain phenolic secondary
substances such as cinnamic acid
derivatives, condensed tannins, flavonoids
and phenolic glucosides, but only few
individual compounds are recorded both in
Betulaceous and Salicaceous plants
(Matsuda & Matsuo 1985; Julkunen-Tiitto
1986, 1989; Daniere et al. 1991; Mori et al.
1992; Suomela et al. 1995; Ossipov et al.
1996; Keinänen & Julkunen-Tiitto 1998;
Rank et al. 1998; Kause et al. 1999).
Among Betulaceous plants, birches are an
9
young G. lineola adults from separate
laboratory cultures and naturally
overwintered adults of several populations
both on Betulaceous and Salicaceous
species, it is examined to see if behavioural
differences of conspecific beetles result
from differences in genetics, earlier host
experience or both (I). The performance of
naive larvae of four G. lineola populations
both on Betulaceous and Salicaceous hosts
was studied in order to find out if
conspecific beetles associated with the
different host plant families are differently
physiologically adapted.
Laboratory experiments were also
conducted to study what leaf traits are
crucial in determining plant quality for leaf
beetles (II-V). In order to see if plant
secondary phenolics govern the host
utilization of A. alni, the effects of five
pure phenolic secondary compounds on its
behaviour were tested in 2-choice bioassays
with naturally overwintered adults (II). For
the bioassays, all A. alni adults were
collected from A. incana, and the beetles
were also kept on their original hosts in
laboratory prior to experiments. Test
compounds and the used concentrations
were selected on the basis of secondary
chemical analyses of the potential host
plants (see below). Test solutions were
applied onto natural substrates, host plant
leaves. Leaves treated with the solvent
were used as controls. The effects of
chlorogenic acid were also tested for G.
lineola, L. capreae, Ph. polaris and P.
versicolora (III). In addition, the preference
tests among the chemically screened plant
species (II, III), conspecific leaf age classes
(IV) and willow clones (V) were done with
naturally overwintered adult beetles of
several species. In article V, the larval
performance of G. lineola on chemically
analysed Salix phylicifolia L. clones was
also measured. The plant material for all
plants. As they are rather poor dispersers,
adult host choice largely determines larval
food plant. After the larval period, fullygrown larvae move to the soil beneath the
host plant in order to pupate, but some
species may pupate on the shoots or stems
of the host (see Tischler 1977; Baur &
Rank 1996; Häggström 1997; Sipura 2000).
Adults of the new generation emerge in
early autumn after a short pupal stage.
Under certain circumstances, leaf beetles
can cause severe defoliation that entails
stunted plant growth and the death of
young shoots (Kendall et al. 1996).
3. GENERAL METHODOLOGY
This thesis is based both on experimental
and observational data (I-VI). Since the
main interest was the effect of variable
food quality on leaf beetles, the majority of
the experiments were done in a laboratory
where it is possible to standardize all other
factors that may affect leaf beetle behaviour
and performance. In the laboratory
experiments, adults and larvae belonging to
seven species of leaf beetles were used:
Agelastica alni L., Chrysomela populi L.,
Galerucella lineola F., Lochmaea capreae
L., Phratora polaris Schneid., Phytodecta
rufipes Geer and Plagiodera versicolora
Laich. Plant species used in the laboratory
experiments were: Alnus incana (L.)
Moench, A. glutinosa (L.) Gaertner, B.
pendula Ehrh,, P. tremula L., Salix caprea
L., S. cinerea L., S. lapponum L., S.
myrsinifolia Salisb., S. pentandra L. and S.
phylicifolia L. As A. alni and G. lineola
were rather frequently found both on
Betulaceous and Salicaceous host plants
even in sympatry, it was examined if adults
of conspecific populations naturally
associated with different host plant families
behave differently in standardized host
selection experiments (I, II). By rearing
10
comparing their retention times and UV-vis
spectra to those of authentic compounds.
Polymeric phenolics, condensed tannins,
were analysed with a colourimetric
Butanol-HCl assay (II-VI). The total
nitrogen concentrations of leaves were
measured from subsamples of powdered
leaves with an automatic CHN-analyzer
(IV, V). Water content (V) was calculated
based on the weight difference between
fresh and dried leaves.
laboratory experiments was collected from
naturally growing plants. Because of the
possibility of intra-specific hybridization
(e.g. Hanhimäki et al. 1994; Hjältén 1997),
only characteristic individuals of each plant
species were used.
In article VI, the seeds of two
parental willow species, S. caprea and S.
repens L., as well as their four hybrid
categories were produced by handpollination. Subsequently, potted clones
were exposed to the feeding of the natural
communities of several leaf beetle species
and other leaf-eating insects in the
experimental field. After the experiment, it
was possible to separately determine leaf
damages caused by the leaf beetles and
other herbivores. As leaf samples of all the
193 study plants were individually
screened, it was possible to relate the
patterns in herbivore feeding to the patterns
in the leaf chemistry. In order to examine
how well plant quality measured in
laboratory predicts insect distribution in the
field, field surveys were conducted in
articles II and V. Field observations and
experiments were also used to evaluate the
importance of abiotic factors and natural
enemies, along with variable food quality,
as determinants of the field distribution of
G. lineola (V). Most studies were done in
eastern Finland in the city of Joensuu or
nearby (I-V), but the field experiment of a
hybrid study was conducted in Umeå in
north-eastern Sweden (VI).
The leaf samples used in the
chemical analyses were firstly dried and
ground to a fine powder in a plant mill (IIVI). Extraction of phenolics from the
powdered leaf samples was done as
described below (III). High performance
liquid chromatography (HPLC) was used to
analyze low-molecular weight phenolics in
leaf extracts (II-VI). Individual compounds
in chromatograms were identified by
4. PATTERNS IN LEAF CHEMISTRY
Both Betulaceous A. incana and several
Salicaceous plant species studied contained
low-molecular weight phenolics such as
cinnamic acid derivatives, flavonoids,
phenolic glucosides and phenolic polymers
such as condensed tannins in their leaves
(II-VI). In relation to the generally rather
restricted distribution of phenolic
glucosides in the plant kingdom, it is
remarkable that both Betulaceous and
Salicaceous plants contain phenolic
glucosides in their leaves. Earlier studies
corroborate this observation (JulkunenTiitto 1986, 1989; Kelly & Curry 1991;
Mori et al. 1992; Bingaman & Hart 1993;
Keinänen & Julkunen-Tiitto 1998; Rank et
al. 1998; Mutikainen et al. 2000). Apart
from A. incana, phenolic glucosides can
also be found in the leaves of the following
Scandinavian Betulaceous plant species: A.
glutinosa, B. pendula and Betula pubescens
Ehrh. (Keinänen & Julkunen-Tiitto 1998;
Mutikainen et al. 2000; Ikonen unpubl.
data). Structurally, phenolic glucosides can
be divided into two main categories (e.g.
Julkunen-Tiitto 1989). Salicylates are
derivatives of salicin in which a variable
number of structural groups is linked to the
salicin core of molecules. In contrast, nonsalicylic phenolic glucosides are a
structurally more heterogenous group. The
11
and condensed tannins are produced in a
shikimate pathway, but in different
branches of the pathway (e.g. Lavola 1998;
Keinänen et al. 1999). The common
precursor of condensed tannins and
phenolic glucosides is cinnamate. Thus, if
a plant allocates a lot of cinnamate for the
production of phenolic glucosides, only a
small amount of this precursor is available
for production of condensed tannins in
another branch of the pathway and vice
versa. The trade-off between the content of
condensed tannins and phenolic glucosides
is also obvious among the different leaf age
classes of those Salicaceous plants that
produce glucosides in detectable amounts
(IV). The highest phenolic glucoside
content and the lowest level of condensed
tannins are found in young leaves. Young
leaves also contain more nitrogen.
Leaves of a tea-leafed willow, S.
phylicifolia, are characterized by the
presence of a low-molecular weight
flavoinoid, ampelopsin, in very high
amounts, whereas other simple phenolics
can be found only in small amounts (II, V).
In addition, leaves of S. phylicifolia contain
high-molecular weight condensed tannins.
In article V, S. phylicifolia clones grown in
three habitats along a soil moisture gradient
(wetland, flood zone and dry zone) differed
significantly in their leaf chemistry.
Namely, leaves of wetland willows
contained less nitrogen and water but more
secondary phenolics than leaves of clones
growing in drier habitats. In general, clonespecific variation in leaf chemistry may be
due to variable plant genetics,
environmental conditions, or both (Larsson
et al. 1986; Bryant et al. 1987; Rousi et al.
1997; Hakulinen 1998; Mutikainen et al.
2000). As the studied S. phylicifolia clones
(V) were naturally growing plants, it is
impossible to surely say whether their
variable susceptibility results from some of
common character for all of them is that a
molecule contains one phenolic ring which
is, in various ways, linked to the glucose
moiety. Both types of glucosides can be
found in leaves of Salicaceous plants, but
Betulaceous plants appear to contain only
certain non-salicylic phenolic glucosides
(Julkunen-Tiitto 1986, 1989; Mori et al.
1992; Keinänen & Julkunen-Tiitto 1998;
Mutikainen et al. 2000; II; Ikonen unpubl.
data). Most individual glucosides seem to
be restricted either to the leaves of
Betulaceous or then Salicaceous plants.
Data from leaf chemistry of
different willow hybrid categories and
parental species indicate that the levels of
the main secondary compounds, condensed
tannins and salicylic phenolic glucosides,
are additively inherited (VI). The F1 and F2
hybrid forms were intermediate to pure
parental species and back-crosses were
intermediate to the respective parental
species and F1 and F2 hybrid forms.
Earlier, Orians et al. (2000) have reported
that in another complex of two pure willow
species and their F1 hybrids condensed
tannin content of hybrid leaves is also
intermediate to parental species. However,
phenolic glucosides were in this case below
the midpoint of parental species in hybrid
leaves indicating their dominant
inheritance. Moreover, our data from
hybrid willows show that leaf
concentrations of phenolic glucosides and
condensed tannins correlate negatively
among the plant individuals of all
categories in which a considerable fraction
of individual plants contain detectable
amounts of glucosides in their leaves (VI).
In concordance, Julkunen-Tiitto (1989) and
Orians et al. (2000) have earlier reported
negative correlations of leaf condensed
tannin and phenolic glucoside contents in
willows. This kind of trade-off may result
from the fact that both phenolic glucosides
12
Koch 1992; Palokangas & Neuvonen 1992;
Seldal et al. 1994; Gross & Hilker
1994/1995; Baur & Rank 1996). In
concordance, A. alni and G. lineola were
found on hosts of both of these plant
families in the main study area in eastern
Finland (I; II). The most frequently used
hosts for both beetles appear to be A.
incana, A. glutinosa and S. phylicifolia, but
birches (Betula spp.) are also occassionally
utilized by them. Host utilization strategies
of A. alni and G. lineola in a BetulaceaeSalicaceae host plant complex seem to be,
however, totally different. In standardized
laboratory feeding trials, both Betulaceaeand Salicaceae-associated sympatric A. alni
beetles preferred grey alder, A. incana, over
tea-leafed willow, S. phylicifolia (II). Thus,
in A. alni no indication of intra-specific
host-associative differentation or
conditioning on alternative hosts was
found. For A. alni, birches and willows
appear to be secondary hosts which are
especially used in times of high population
densities (II; see also Tischler 1977; Baur
& Rank 1996). This may be linked to the
fact that A. alni is sensitive to herbivoryinduced detorioration of alder leaves (Baur
et al. 1991; Baur & Rank 1996; Dolch &
Tscharntke 2000; see also Seldal et al.
1994).
If a host race of a herbivorous insect
species is defined as a population that is
partially reproductively isolated from other
conspecific populations because of its hostspecific adaptations (see Jaenike 1981;
Diehl & Bush 1984; Prokopy et al. 1988;
Craig et al. 1993), Betulaceae- and
Salicaceae-associated G. lineola beetles
seem to represent separate host races (I).
Firstly, Salicaceae-associated G. lineola
populations accept only willows as their
hosts in standardized laboratory feeding
trials, whereas conspecific Betulaceaeassociated populations also accept
the above factors or from all of them.
However, since S. phylicifolia as a
terrestrial plant species has no clear
adaptations to grow subemerged, it is likely
that differences between the clones of three
moisture zones are largely due to the floodstress of willows in wet habitats. Moreover,
as both ampelopsin and condensed tannins
were at the highest level in the leaves of the
same clones (V), in S. phylicifolia there did
not appear to be a similar trade-off between
the production of low- and high-molecular
weight phenolics as found in other,
phenolic glucoside-producing willow
species (VI). Accordingly, data from
different leaf age classes suggest that young
leaves of S. phylicifolia contain both higher
concentrations of ampelopsin (unpubl.
data) and condensed tannins (IV). Young
S. phylicifolia leaves also contain more
nitrogen than conspecific older leaves
suggesting that decreasing concentrations
of nitrogen with increasing leaf age is a
rather universal pattern in higher plants
(Feeny 1970; Raupp & Denno 1983;
Langenheim et al. 1986; Julkunen-Tiitto
1989; Denno et al. 1990; Van Dam et al.
1995; IV).
5. PATTERNS IN LEAF BEETLE
HERBIVORY
5.1. Utilization of the host plants of two
families by leaf beetles
Herbivorous insects generally tend to be
more or less host-specific (Smiley 1978;
Bernays & Graham 1988; Roininen &
Tahvanainen 1989; Jaenike 1990;
Kolehmainen et al. 1994; Baur & Rank
1996; Roininen et al. 1999). Nevertheless,
many European species of leaf beetles
feeding on deciduous woody plants utilize
both Betulaceous and Salicaceous hosts
(Tischler 1977; Kreslavsky et al. 1981;
13
but successfully demonstrated in only a few
cases (Gould 1979; Hare & Kennedy 1986;
Fry 1990; Jaenike 1990; Via 1991; Fox
1993; Joshi & Thompson 1995; Lazarevic
et al. 1998). Thus, the evidence for
performance trade-offs found in G. lineola
(I) is remarkable. In general, performance
trade-offs would be a potentially powerful
mechanistic explanation for the
specialization of insect herbivores, since in
order to maximize their performance
insects should specialize. However,
Salicaceous plants appear to be superior
hosts for even the most Betulaceae-adapted
G. lineola beetles (I). This result is in line
with the increasing evidence that in many
cases modifications in insect host plant
utilization may take place primarily at the
behavioral level, whereas specific
metabolic adaptations of insects are
consequences rather than causes of the host
shifts (Smiley 1978; Futuyama 1984;
Prokopy et al. 1988; Roininen &
Tahvanainen 1989). Consequently, even
shifts onto poor-quality host plants appear
to be possible if there exists some factor
that balances the negative effect of lowquality food on an insect’s overall fitness
(see Feder 1995; Feder et al. 1995; Rossi et
al. 1999). In G. lineola, the fundamental
factor driving host-race formation may be
the patchy distribution of the original main
host, S. phylicifolia. Since G. lineola is,
because of its phylogenetic constraints (see
below), restricted to the microclimate of
shoreline habitats, it has to utilize those
plants it can find in its preferred habitat. If
S. phylicifolia is locally rare or absent, it
may be possible for G. lineola to gain the
highest overall fitness by readily accepting
alternative host species irrespective of their
poor quality. Accordingly, Betulaceaeassociated G. lineola populations seem to
be most frequently found at sites where
willows are rare or absent (I).
Betulaceous plants or prefer them (I). Even
the sympatric G. lineola populations
associated with the hosts of different plant
families differ significantly in their feeding
behaviour. Moreover, these behavioural
differences of G. lineola populations seem
to have an underlying genetic basis. In the
field, behavioural differences of
conspecific insects are likely to lead to
reproductive isolation even in sympatry,
since matings in nature are most probable
between insect individuals sharing equal
host preferences (Craig et al. 1993; see also
Kreslavsky et al. 1981). However, in G.
lineola this behaviour-based pre-zygotic
reproductive isolation appears to be
incomplete since Betulaceae-associated
populations usually also accept Salicaceous
host plants (I). Moreover, G. lineola beetles
can be conditioned to ’wrong’ hosts if
forced to feed on them. This is in line with
other findings which indicate that the
association of an individual insect with a
certain plant species may increase its
probability to be attacked in future
encounters (e.g. Prokopy et al. 1982). On
the other hand, G. lineola beetles were
found to be physiologically better adapted
to their respective hosts than their
conspecifics from other host species, and
increasing adaptation to a certain host
appears to entail a decreased adaptation to
other hosts (I). This means that Betulaceous
and Salicaceous host plants seem to favour
and require different adaptations in G.
lineola. Thus, natural selection may largely
eliminate those G. lineola genotypes from
a certain host species which are successful
and abundant on alternative hosts possibly
producing a post-zygotic reproductively
isolating mechanism.
Performance trade-offs, the
negative genetic correlations of insect
performance on the alternative host species,
have been recently frequently sought out
14
and S. pentandra, with high leaf phenolic
glucoside content. Clearly, association with
non-salicylic alder phenolic glucosides
have not entailed in A. alni a general
behavioural tolerance for willow phenolic
glucosides. These results support earlier
findings that willows with high phenolic
glucoside content are usually avoided by
the insect herbivores which are not well
adapted to willows (Rowell-Rahier 1984;
Orians et al. 1997). Moreover, the fact that
three other leaf beetle species, L. capreae,
Ph. polaris and P. versicolora, avoided
high-glucoside S. myrsinifolia (III)
indicates that they are also sensitive to
phenolic glucosides in high amounts (see
also Tahvanainen et al. 1985; Palokangas &
Neuvonen 1992; Kendall et al. 1996). On
the other hand, some willow species with a
high leaf phenolic glucoside level also
contain chlorogenic acid in high amounts in
their leaves (Rank et al. 1998; II; III). In
bioassays, chlorogenic acid particularly
deterred the feeding of A. alni and L.
capreae (II; III). Earlier, Matsuda & Senbo
(1986) have demonstrated a deterrent effect
of chlorogenic acid on several Japanese leaf
beetles. Overall, the high resistance of S.
myrsinifolia and S. pentandra against
certain leaf beetles seems not to result
solely from their high leaf salicylate
content (II; III). Apart from their inhibitory
effects on behaviour, both chlorogenic acid
and phenolic glucosides may negatively
affect the performance of non-adapted
insects (Todd et al. 1971; Isman & Duffey
1982; Lindroth et al. 1988; Kelly & Curry
1991; Hemming & Lindroth 1995; Stamp
& Yang 1996). In contrast, condensed
tannins may generally be rather ineffective
at the behavioural level of leaf beetles,
since even A. alni primarily associated with
low-tannin hosts, alders, was not deterred
by low-molecular weight basic structural
unit of condensed tannis, (+)-catechin (II).
In my study area, Ch. populi, L.
capreae and Ph. polaris seem to be
restricted to Salicaceous plants, even
though they have been recorded elsewhere
in Europe to live also on Betulaceous host
plants (Kreslavsky et al. 1981; Koch 1992;
Palokangas & Neuvonen 1992). It is likely,
that these three leaf beetle species also have
Betulaceae-associated races (Kreslavsky et
al. 1981; see also Gross & Hilker
1994/1995) as found here in G. lineola (I).
However, the conditions favouring the
formation of Betulaceae-associated races in
Ch. populi, L. capreae and Ph. polaris may
be rather specific and rarely occur, since
the majority of their populations obviously
lives on Salicaceous plants (see Matsuda &
Senbo 1986; Dodge et al. 1990; Augustin et
al. 1993; Köpf et al. 1996; Chinery 1997;
III; IV). Among the leaf beetles studied in
this thesis, only Ph. rufipes and P.
versicolora seem to be completely
restricted to Salicaceous plants (see Raupp
1985; Jones & Coleman 1988; Raupp &
Sadof 1989; Dodge et al. 1990; Soetens et
al. 1991; Koch, 1992; Orians et al. 1997;
III; IV).
5.2. Leaf chemicals as determinants of
leaf quality
In concordance with earlier studies
(Tahvanainen et al. 1985; Kelly & Curry
1991), present results suggest that leaf
beetle herbivory on Salicaceous plants is
strongly limited by their characteristic lowmolecular weight secondary compounds,
phenolic glucosides. Even though leaves of
the natural primary hosts of A. alni, alders,
contain their specific non-salicylic phenolic
glucosides, both salicylic and non-salicylic
willow phenolic glucosides deterred this
leaf beetle from feeding (II). In feeding
preference experiments, A. alni also
avoided two willow species, S. myrsinifolia
15
living on salicylate-rich Salicaceous plants
(Rank 1992; Soetens & Pasteels 1994;
Kolehmainen et al. 1995; see also Smiley et
al. 1985). Consequently, the preference of
Ch. populi and Ph. rufipes for young leaves
of their host plants (IV) may be partially
due to the higher content of salicylates in
younger rather than in conspecific old
leaves.
Experiments with chlorogenic acid
and A. alni (II) lend support to earlier
studies which suggest that effects of
individual secondary substances on insect
herbivores may depend on the background
variation of other plant chemicals (Renvick
& Radke 1987; Soetens & Pasteels 1994).
Namely, for A. alni chlorogenic acid was a
deterrent only on the leaves of the
secondary host, S. phylicifolia, while the
effect on the leaves of the primary host, A.
incana, was neglible (II). Moreover, current
data show that A. alni prefers grey alder, A.
incana, even over the willow species that
contain little feeding deterrents in their
leaves (II). Overall, leaves of A. incana
seem to contain some very specific and
strong stimulants for A. alni. These
stimulants may obviously outweigh even
the effects of potent deterrents. However,
these stimulants have not yet been
identified.
It is not known which leaf traits
Betulaceae- and Salicaceae-associated G.
lineola beetles respond differently to (I).
For another leaf beetle, Chrysomela
lapponica L., a salicylic phenolic
glucoside, salicin, is a deterrent for beetles
associated with Betulaceous plants,
whereas for Salicaceae-associated
conspecifics salicin acts as a stimulant
(Gross & Hilker 1994/1995). Salicin is
present only in the host plants of the
Salicaceae-associated Ch. lapponica
beetles. Analogously, it is possible that G.
lineola populations associated with
Whether or not condensed tannins have
effects on performance of the studied leaf
beetles remains an unsolved question. In
general, condensed tannins are known as
potential inhibitors of insect herbivore
performance (Manuwoto & Scriber 1986;
Bryant et al. 1987; Ayres et al. 1997).
Extremely abundant flavonoid ampelopsin
in S. phylicifolia leaves probably has no
strong antiherbivore activity even against
A. alni, since S. phylicifolia is rather
palatable for A. alni (II) and is also suitable
for complete larval development (Baur &
Rank 1996). A. alni also prefers young S.
phylicifolia with higher ampelopsin content
than in conspecific older leaves (IV).
Among the experimentally studied
leaf beetle species (I-V), Ch. populi and
Ph. rufipes are species which live on
Salicaceous plants with high contents of
salicylate-type phenolic glucosides (IV). In
general, many leaf beetle species living on
salicylate-rich willows and poplars are
known to use host plant salicylates as
precursors to their own defensive larval
secretion (Rowell-Rahier & Pasteels 1982;
Pasteels et al. 1983; Smiley et al. 1985;
Rank 1994). In contrast, non-salicylic
phenolic glucosides are inappropriate
precursors for the production of
salicylaldehyde-containing defensive larval
secretion. The secretion of Ch. populi
larvae also contains salicylaldehyde
(Pasteels et al. 1983), but larval defenses of
Ph. rufipes appear to be unknown. In any
case, in salicylate-using leaf beetles the
amount of larval secretion and, therefore,
the effectiviness of larval defense
positively correlates with the amount of its
precursors in the food (Rowell-Rahier &
Pasteels 1982; Pasteels et al. 1983; Smiley
et al. 1985; Denno et al. 1990; Rank 1994).
Following evolutionary logic, it should not
be surprising that salicylates are found to
stimulate the feeding of many leaf beetles
16
Moreover, experiments with differently
aged leaves of three Salicaceous hosts
indicate that young leaves with high
nitrogen content and low toughness tend to
be generally preferred over less nitrogenous
and tougher older leaves (IV). The
preference for young leaves is true
irrespective of whether these young leaves
contain more or less condensed tannins
than conspecific older leaves. Moreover,
both salicylate-using leaf beetle species and
those generally sensitive to high amounts of
phenolic glucosides preferred young leaves
of glucoside-rich S. pentandra, even though
young leaves contain more glucosides than
older leaves. This result contradicts the
observations made of several other leafeating insects. Many herbivorous insects
minimize the intake of harmful lowmolecular weight secondary compounds
rich in young leaves by selecting the older
rather than younger leaves of their hosts
(Rhoades & Cates 1976; Cates 1980;
Meyer & Montgomery 1987; Van Dam et
al. 1995). Obviously, even some of the
studied leaf beetle species living on
glucoside-poor willows (IV) have,
however, to some degree adapted to these
typical secondary substances of willow
leaves. This view is supported by
observations that in small concentrations
willow phenolic glucosides act as feeding
stimulants even for certain leaf beetles
associated with low-glucoside willows
(Kolehmainen et al. 1995).
different host plant families in the study
area (I) are differently adapted to those
non-salicylic phenolic glucosides which are
specific to plant families (see above).
Basically, phenolic glucosides are potent
regulators of host selection behaviour in G.
lineola (Tahvanainen et al. 1985;
Kolehmainen et al. 1995), and Betulaceaespecific non-salicylic phenolic glucosides
are known to be potent deterrents for insect
herbivores (Mori et al. 1992). Furthermore,
Lindroth & Weisbrod (1991) have in a
gypsy moth, Lymantria dispar L.,
demonstrated intra-specific genetic
variation in insect ability to metabolize
aspen phenolic glucosides. Similarly, it is
also possible that G. lineola populations
associated with Betulaceous and
Salicaceous host species are differently
adapted in their physiology to Betulaceaespecific non-salicylic phenolic glucosides
(I). This could partially explain the tradeoff found in the survival of naive larvae of
four G. lineola populations on two host
species, A. incana and S. phylicifolia.
At the intra-specific level of plants,
among conspecific clones and within
individual plants, leaf quality variation for
leaf beetles may be more closely related to
the variation in leaf nutritive traits than to
secondary chemistry (IV; V). This is not
surprising since the leaf secondary
chemical variation at intra-specific level of
plants is less dramatic than among the
different plant species. In article V, leaf
nitrogen content seems to explain host
preferences for adult G. lineola beetles
among 60 S. phylicifolia clones growing in
three habitats along a soil moisture
gradient. Larval performance was most
clearly related to leaf water content,
whereas the concentrations of main
secondary compounds, ampelopsin, (+)catechin and condensed tannins, were not
related to any performance parameter.
5.3. Plant hybridization and leaf beetle
herbivory
Because of the potentially large role of
inter-specific plant hybridization both in
the evolution of plants and associated
insect herbivores, there has recently been
increased scientific interest in insect
responses to hybrid plants (Soetens et al.
17
caprea), a high-glucoside species (S.
repens) and their inter-specific F1 hybrids
with intermediate leaf glucoside content did
not differ in their total leaf beetle damage
or total leaf herbivory. On the study site
there were both non-adapted (L. capreae,
Ph. polaris and Phratora vulgatissima L.)
and glucoside-adapted (Phratora vitellinae
L.) leaf beetle species (see Rowell-Rahier
& Pasteels 1982; Tahvanainen et al. 1985;
Kelly & Curry 1991; Palokangas &
Neuvonen 1992; Kendall et al. 1996).
Possibly, decreased feeding by non-adapted
insect species on plants with high leaf
glucoside content was balanced by
increased feeding of well-adapted
specialists (V). On the other hand, the
complex willow hybrids, F2 and back-cross
types, were, in the field, more heavily
attacked by leaf beetles and other leafeating herbivores than F1 hybrids and two
pure parental species. As the susceptibility
of F1 hybrids for herbivores did not differ
from that of the parental species, the high
susceptibility of complex hybrids is
difficult to explain mechanistically. Maybe
the inheritance patterns of other leaf traits
than phenolic glucosides and condensed
tannins should also be known. Regardless
of this, current results indicate a natural
selection against complex willow hybrids
provided that leaf herbivory is a significant
determinant of plant overall fitness. Thus,
leaf-eating herbivores such as leaf beetles
may be partially responsible for
maintaining a high richness of species in
the plant kingdom.
1991; Hanhimäki et al. 1994; Häggström &
Larsson 1995; Fritz et al. 1996; Kendall et
al. 1996; Hjältén 1997; Häggström 1997;
Orians & Floyd 1997; Orians et al. 1997).
These studies have formulated many
alternative hypotheses to herbivore
responses to hybrid plants: 1) the hybrid
susceptibility hypothesis predicts that
hybrids are attacked more intensively than
either of the parental species, 2) the hybrid
resistance hypothesis suggests that hybrids
have lower herbivore load than the parental
species, 3) the additive hypothesis predicts
that hybrid susceptility is intermediate of
parental species, 4) the dominance
hypothesis states that herbivory loads on
hybrids and one of the parental species are
equal and 5) the no-difference hypothesis
states that all plant categories are equally
attacked (see Fritz et al. 1996; Hjälten
1997). Responses of individual herbivore
species to hybrid plants, however, do not
answer the question regarding what is the
overall herbivory susceptibility of different
plant categories in a certain system of
parental species and their intra-specific
hybrids. In nature, plants are usually
attacked by a multitude of insect herbivore
species, each of which may select totally
differently among the plant categories of a
particular complex of parental species and
hybrids (Fritz et al. 1996; Orians & Floyd
1997; Orians et al. 1997).
Soetens et al. (1991) have suggested
that leaf phenolic glucoside content may
largely predict the field distribution of leafeating insects on clones of parental willow
species and their hybrids (see also Kendall
et al. 1996). In general, glucoside-adapted
insect herbivore species can be expected to
prefer high-glucoside willow categories,
whereas non-adapted insects tend to feed
on low-glucoside clones (Orians et al.
1997). Article V shows that a lowglucoside parental willow species (S.
5.4. The importance of variable food
quality in relation to other factors
Leaves of S. phylicifolia clones growing in
three habitats along a soil moisture gradient
(wetland, flood zone and dry zone) were
very differently palatable and suitable for
18
behavioural differences of conspecific
adults of this beetle indicate that
Betulaceous and Salicaceous plants favour
and require different adaptations in leaf
beetles. This probably results from the fact
that individual leaf secondary compounds
in plants of these two families are different,
even though structurally related.
Experiments with A. alni show that an
association with phenolics of a certain
structural group do not necessarily entail a
general pre-adaption to all members of a
particular group of compounds.
Consequently, individual leaf beetles can
be properly adapted only to a limited set of
secondary chemicals and host plants.
Current results show that several lowmolecular weight willow phenolics deter
the feeding of non-adapted leaf beetles,
making many willow species poorly
palatable for these insects. As shown in the
field with A. alni, these poorly palatable
willow species are avoided even during leaf
beetle outbreaks. On the other hand, the
distribution of specific stimulants seems to
also have an influence on the host plant
preferences of leaf beetles. The presence of
specific stimulants probably explains why
A. alni even prefer grey alder, A. incana,
over the deterrent-poor willows. Moreover,
intra-specific variation in leaf nutritive
traits may cause a remarkable variation in
leaf acceptability and suitability for leaf
beetles. Overall, only a small fraction of
available plant biomass appears to be
adequate food for leaf beetles, which sets
fundamental limits for leaf beetle
populations. This means that resourcebased bottom-up forces are basically
important for leaf beetles. Nevertheless, in
some cases, variation in abiotic conditions
may overcome the effect of variable food
quality on leaf beetle host utilization
patterns in the field.
G. lineola, since in laboratory experiments
G. lineola performed best on and preferred
clones growing in the dry zone (V). In this
case, host plant quality is clearly linked to
the highest leaf nitrogen and water content
and the lowest content of secondary
phenolics in dry zone clones. In nature, G.
lineola, however, is not distributed as
expected on the basis of food quality. In the
field, both adult G. lineola beetles, larvae
and eggs were aggregated in wetland
habitats. Variation in enemy pressure
obviously does not explain this unexpected
result. Instead, a wetland habitat appears to
provide for G. lineola more favourable
abiotic conditions than the flood or dry
zones. Probably, high air humidity in the
wetlands is an especially important factor
for G. lineola, since its larvae perform
better in moist rather than in dry conditions
(see also Larsson et al. 1997). The
dependency of G. lineola on air humidity
may result from ancient phylogenetic
constraints, as the majority of the species in
the genus Galerucella appear to be rather
restricted to aquatic or semi-aquatic plants
or terrestrial plants growing in moist
habitats (Nokkala & Nokkala 1989a, b;
Kouki 1991; Koch 1992). Overall, G.
lineola adults in the field probably firstly
find a favourable abiotic habitat, and host
selection behaviour appears to take place
secondarily. These results strongly support
recent suggestions that field variation in
abiotic environmental conditions may
sometimes mask the resource-based
bottom-up effects placed upon on
herbivorous insects (Williams 1983;
Willmer et al. 1996; Ritchie 2000; Sipura
& Tahvanainen 2000).
6. CONCLUDING REMARKS
A performance trade-off found in naive
larvae of four G. lineola populations and
19
activity in condensed tannins. Ecology
78: 1696-1712
Barbosa P, Schultz JC (eds) (1987) Insect
outbreaks. Academic Press, San Diego
Baur R, Binder S, Benz G (1991)
Nonglandular leaf trichomes as shortterm inducible defense of the grey alder,
Alnus incana (L.), against the
chrysomelid beetle, Agelastica alni.
Oecologia 87: 219-226
Baur R, Rank NE (1996) Influence of host
quality and natural enemies on the life
history of the alder leaf beetles
Agelastica alni and Linaeidea aenea. Pp
173-194 in Jolivet PHA, Cox ML (eds)
Chrysomelidae Biology. Vol 2:
Ecological studies. SPB Academic
Publishing, Amsterdam
Bernays E, Graham M (1988) On the
evolution of host specificity in
phytophagous arthropods. Ecology 69:
886-892
Bingaman BR, Hart ER (1993) Clonal and
leaf age variation in Populus phenolic
glycosides: Implications for host
selection by Chrysomela scripta
(Coleoptera: Chrysomelidae). Environ
Entomol 22: 397-403
Bryant JP, Clausen TP, Reichardt PB,
McCarthy MC, Werner RA (1987)
Effect of nitrogen fertilization upon the
secondary chemistry and nutritional
value of quaking aspen (Populus
tremuloides Michx.) leaves for the large
aspen tortrix (Choristoneura conflictana
(Walker)). Oecologia 73: 513-517
Cates RG (1980) Feeding patterns of
monophagous, oligophagous and
polyphagous insect herbivores: The
effect of resource abundance and plant
chemistry. Oecologia 46: 22-31
Chinery M (1997) Euroopan hyönteisopas.
Otava, Helsinki
Clancy KM (1992) Response of western
spruce budworm (Lepidoptera:
ACKNOWLEDGEMENTS
First of all, I wish to express my deepest
gratitude to Anne and to our dogs Punkku
and Roosa who have shared their life with
me. Without your endless love I would
never have the strength to complete this
thesis. I am grateful to my supervisors Prof.
Jorma Tahvanainen and PhD Heikki
Roininen for their advice and support,
provided in many forms, during this work.
Sari Miettinen, Mika Sipura, Per Hallgren
and Joakim Hjältén deserve my sincerest
thanks because of their inspiring
collaboration. I would like also thank Riitta
Julkunen-Tiitto for her advice regarding
chemical analyses, and Outi Nousiainen as
well as Sinikka Sorsa for their technical
assistance. Greg Watson revised the
English of my manuscripts. I would like
also thank entire personnel of the
Department of Biology and members of our
herbivory research group. I am grateful to
my relatives and to my friends Esko,
Hannu, Markku and Timo. Because of you,
I have had a lot of other things besides of
leaf beetles in my life. My work was
financed by the Finnish Ministry of
Education (Graduate School for Biology
and Biotechnology of Forest Trees) and the
Academy of Finland (Finnish Centre of
Excellence Program, Project no. 51997).
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