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TURUN YLIOPISTO
Turku 2008
TURUN YLIOPISTON JULKAISUJA
ANNALES UNIVERSITATIS TURKUENSIS
SARJA - SER. AII OSA - TOM. 234
BIOLOGICA - GEOGRAPHICA - GEOLOGICA
MUTUALISTIC INTERACTIONS
BETWEEN PLANTS AND BIRDS:
BEHAVIOURAL MECHANISMS AND
ECOLOGICAL IMPORTANCE
by
Elina Mäntylä
From the Section of Ecology, Department of Biology, FI-20014 University of Turku,
Finland
Supervised by
Dr. Tero Klemola
Section of Ecology
Department of Biology
FI-20014 University of Turku
Finland
Dr. Toni Laaksonen
Section of Ecology
Department of Biology
FI-20014 University of Turku
Finland
Reviewed by
Docent Leena Lindström
Department of Biology and Environmental Science
P.O. Box 35
FI-40014 University of Jyväskylä
Finland
Docent Seppo Rytkönen
Department of Biology
P.O. Box 3000
FI-90014 University of Oulu
Finland
Examined by
Dr. Christiaan Both
Animal Ecology Group
Center for Ecological and Evolutionary Studies University of Groningen
P.O. Box 14
9750 AA Haren
The Netherlands
ISBN 978-951-29-3790-5 (PRINT)
ISBN 978-951-29-3791-2 (PDF)
ISSN 0082-6979
Painosalama Oy – Turku, Finland 2008
There is nothing like looking, if you want to nd something.
You certainly usually nd something, if you look,
but it is not always quite the something you were after.
Thorin Oakenshield
(J.R.R. Tolkien: The Hobbit)
4 Contents
CONTENTS
LIST OF ORIGINAL PAPERS ....................................................................................5
1. INTRODUCTION ....................................................................................................6
1.1. Plant defences .....................................................................................................7
1.2. Tritrophic interactions ........................................................................................7
1.3. Possible ways for birds to detect herbivore-damaged plants ..............................8
1.3.1. Vision .......................................................................................................8
1.3.2. Olfaction ...................................................................................................9
1.4. Ecological importance of insect-rich plants to birds ..........................................9
1.5. Ecological importance of insectivorous birds to plants ....................................10
2. AIMS OF THE THESIS .........................................................................................11
3. MATERIAL AND METHODS ..............................................................................12
3.1. Experimental study set-ups ...............................................................................12
3.2. Species studied .................................................................................................12
3.2.1. Plants ......................................................................................................13
3.2.2. Herbivores ..............................................................................................13
3.2.3. Birds .......................................................................................................14
3.3. Observation methods ........................................................................................15
3.4. Plant cues studied .............................................................................................15
3.5. Meta-analysis ....................................................................................................16
4. MAIN RESULTS AND DISCUSSION..................................................................17
5. CONCLUSIONS .....................................................................................................20
ACKNOWLEDGEMENTS ........................................................................................21
REFERENCES .............................................................................................................23
ORIGINAL PAPERS I – V..........................................................................................27
List of Original Papers 5
LIST OF ORIGINAL PAPERS
This thesis is based on the following articles and manuscripts, referred to in the text by
their Roman numerals:
I Mäntylä E, Klemola T & Haukioja E. 2004. Attraction of willow warblers to
sawy-damaged mountain birches: novel function of inducible plant defenses?
Ecology Letters 7: 915–918.
II Mäntylä E, Klemola T, Sirkiä P & Laaksonen T. 2008. Low light reectance may
explain the attraction of birds to defoliated trees. Behavioral Ecology 19: 325–
330.
III Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T,
Piirtola P & Klemola T. 2008. From plants to birds: higher avian predation rates in
trees responding to insect herbivory. PLoS ONE 3(7): 2832.
IV Mäntylä E, Sirkiä PM, Klemola T & Laaksonen T. Territory choice of pied
ycatchers is not based on induced cues of herbivore-damaged trees. Submitted
manuscript.
V Mäntylä E, Klemola T & Laaksonen T. Birds help plants – a meta-analysis of top-
down trophic cascades caused by avian predators. Submitted manuscript.
Articles I, II and III are reprinted with permissions from Blackwell Publishing, Oxford
University Press and Public Library of Science, respectively.
6 Introduction
1. INTRODUCTION
Ecosystems consist of trophic levels (e.g. producers, consumers and decomposers) and
interactions among species of the same or different trophic levels (Price et al. 1980). These
interactions are often depicted as food chains (as in Fig. 1). The base of the food chain is
typically a plant, which is eaten by herbivores. Naturally this interaction is negative for
the plant (Nykänen & Koricheva 2004), which tries to defend itself against herbivores in
several ways (see section 1.1.). Herbivores are themselves preyed on by carnivores of the
next trophic level. At the other extreme of the food chain are the top predators, which eat
lower-level carnivores. Even though trophic interactions almost always involve species
from more than two trophic levels (Oksanen & Oksanen 2000), many intensive ecosystem
studies in the past have nevertheless dealt with only two trophic levels at a time. One
example of tritrophic interaction is the trophic cascade, which usually consists of a predator,
an herbivore and a plant, and where the effect of predation on the herbivore has a positive
impact on the plant (Persson 1999; Schmitz et al. 2004). When herbivore-eating predators
remove herbivores from plants, the result can thus be an indirect mutualistic interaction
between plant and predator (both species benet from each other via the herbivore; Fig. 1)
(e.g. Marquis & Whelan 1994; De Moraes et al. 1998; Mols & Visser 2002; Kalka et al.
2008). During the past couple of decades, the mechanisms of multitrophic interactions have
become a popular research subject (e.g. Dicke et al. 1990; Turlings et al. 1990; Holopainen
2004; Kost & Heil 2006; Halitschke et al. 2008).
top predator merlin
predator willow warbler
herbivore autumnal moth
producer mountain birch
Figure 1. Example of a food chain in northern Finland, with merlin (Falco columbarius), willow
warbler (Phylloscopus trochilus), autumnal moth (Epirrita autumnata) and mountain birch (Betula
pubescens ssp. czerepanovii). Red arrows show predatory interactions (benecial for one species,
harmful for the other); blue arrow shows mutualistic interaction (benecial for both species).
Introduction 7
1.1. Plant defences
Direct defences by plants against herbivores may be constitutive defences, e.g. thorns
or spines, but they may also be certain chemicals that are always present in the plant
(Agrawal 2006). However, chemical defences are often activated only following
herbivore attack (e.g. Haukioja 1990; Heil et al. 2004). A wide range of these inducible
chemicals have been identied in plants, including tannins, alkaloids, terpenoids and
avonoids. Some of those are highly species-specic (either to the plant or against a
certain herbivore species), while others are more universal (Peñuelas & Llusià 2004).
The chemicals in plants consumed by herbivores can harm the herbivore directly, for
instance by slowing its growth or even killing it (e.g. Coley & Barone 1996; Kause et
al. 1999; Haukioja 2003; Haviola et al. 2007). Some plant defences can be indirect, such
as the volatile organic compounds (VOCs) of plants that attract the herbivore’s natural
enemies (Karban & Baldwin 1997; Turlings & Wäckers 2004). This phenomenon, known
as “crying-for-help”, has previously been known only in invertebrate predators and in
parasitoids that consume for instance herbivorous larvae (e.g. Turlings et al. 1990; Vet
& Dicke 1992; Takabayashi & Dicke 1996; De Moraes et al. 1998; Hoballah & Turlings
2001).
1.2. Tritrophic interactions
The mutualistic relationships observed between plants and the predators of herbivores
have opened up new insights into trophic level interactions. Inter-specic communication
between plants and invertebrate predators and parasitoids is based on inducible VOCs
that are emitted by plants and that act as chemical attractants (Price et al. 1980; Vet and
Dicke 1992; Takabayashi & Dicke 1996; De Moraes et al. 1998; Kessler & Baldwin
2001, Tentelier et al. 2005; Kost and Heil 2006). The feeding of herbivore larvae on a
single tree branch has been found to cause rapid systemic inducible responses (i.e. leaf
quality alters in intact leaves close to the damaged ones as well as in the whole tree)
within a few hours or days (e.g. Haukioja & Niemelä 1979; Haukioja & Hanhimäki
1985; Hanhimäki & Senn 1992; Kaitaniemi & Ruohomäki 2001). Thus predators and
parasitoids are able to sense herbivore-damaged trees from a distance, before they
actually see or smell the herbivores themselves (Farag & Paré 2002; Heil & Silva Bueno
2007; Staudt & Lhoutellier 2007).
There have been some studies on the competence of avian predators in nding
insect herbivores on plant individuals of varying quality (Heinrich & Collins 1983;
Marquis & Whelan 1994; Mols & Visser 2002; Boege & Marquis 2006; Müller et
al. 2006). Avian predation can considerably reduce the herbivore load or damage
to plants (e.g. Marquis & Whelan 1994; Van Bael et al. 2003); thus it may give
plants an adaptive advantage to attract avian predators that reduce their herbivore
8 Introduction
load. However, predators or parasitoids may have adapted to recognise cues from
herbivore-damaged plants without the plants specically adapting for this purpose
(Janssen et al. 2002; Niinemets et al. 2004; Rosenstiel et al. 2004). Such cues may
include for example the products or by-products of induced chemical defence, or
other structural, physiological or chemical changes in the plant that are sensed
by the natural enemies of the herbivores. It is therefore crucial to understand the
mechanisms behind the attraction, before arriving at conclusions as to potential co-
evolution between plants and the avian predators or the parasitoids of their herbivores
(Peñuelas & Llusià 2004; Halitschke et al. 2008). Birds may also compete with
invertebrate predators and parasitoids for the same prey or host (e.g. caterpillars).
Additionally, it has been suggested that predators are more protable to plants than
parasitoids because they remove the herbivore immediately from the plant (Dicke &
van Loon 2000; van der Meijden & Klinkhamer 2000).
1.3. Possible ways for birds to detect herbivore-damaged plants
The two primary sensory mechanisms that birds may use to detect plants carrying
herbivores are vision and olfaction. One hypothesis is that vision can be important in
detecting herbivores at both long and short distances, while olfaction may be useful
mainly closer to the damaged plants, especially under windy conditions.
1.3.1. Vision
Birds can naturally use visible feeding marks in leaves or qualitative structural differences
among plant individuals as cues to nd insect herbivores (Heinrich & Collins 1983;
Mols & Visser 2002; Boege & Marquis 2006; Müller et al. 2006; but see Bergelson &
Lawton 1988). In addition to their broad range of vision (315–700 nm), diurnal birds
can distinguish a large scale of chromatic variation; thus they see colours differently
and with more shades than humans (Cuthill 2006). This is because birds have four
cone cell types and colour-vision-enhancing oil droplets in their eyes, giving rise to a
tetrachromatic form of vision in which every perceived colour consists of red, green,
blue and ultraviolet (UV, 315–400 nm) components. In comparison, humans have only
three cone cell types and trichromatic vision, lacking the UV part visible to birds (Cuthill
2006; Jones et al. 2007).
The UV vision of birds may be a good candidate for the mechanism behind the attraction
of birds to plants suffering from herbivore defoliation, as several bird species are known
to use it for instance during foraging (e.g. Church et al. 1998; Honkavaara et al. 2002;
Viitala et al. 1995). Additionally, in the case of the birch (Betula sp.), insect herbivory
induces the production of defence chemicals (Haukioja 2003), such as avonoids, which
are visible in UV wavelengths (Valkama et al. 2003).
Introduction 9
1.3.2. Olfaction
In contrast to vision, the olfactory ability of most birds, including passerines, was
long thought to be negligible (Roper 1999). Recent studies, however, have shown that
passerines can make use of olfaction in many situations, such as in aromatising nests
(Petit et al. 2002; Mennerat et al. 2005; Gwinner & Berger 2008; Mennerat 2008)
and in predator recognition (Amo et al. 2008; Roth et al. 2008). Many invertebrate
predators in tritrophic systems use VOCs produced by plants to detect and locate their
prey (Turlings et al. 1990; Dudareva et al. 2006). Novel VOCs emitted by herbivore-
damaged plants may be the rst indicators of herbivore presence to predators. It is
therefore possible that olfaction may also be utilised by birds in receiving signals from
plants.
Now there is also physiological and genetic evidence of the olfaction ability of birds.
Steiger et al. (2008) studied nine bird species [blue tit (Cyanistes caeruleus), black
coucal (Centropus grillii), brown kiwi (Apteryx australis), canary (Serinus canaria),
galah (Eolophus roseicapillus), red jungle fowl (Gallus gallus), kakapo (Strigops
habroptilus), mallard (Anas platyrhynchos), and snow petrel (Pagodroma nivea)] and
found that they all had more active olfactory receptor (OR) genes than had previously
been assumed. In vertebrates (especially in mammals and sh, which have been
studied the most) the number of active OR genes generally correlates positively with
the size of the olfactory bulb (i.e. the physiological capability to smell) (Niimura &
Nei 2006). It thus seems that birds can detect smells much better than has previously
been thought.
1.4. Ecological importance of insect-rich plants to birds
One question remains: how important is it to birds to know which plants have many
herbivores? This can be especially benecial for bird tness if only some plants have
large numbers of herbivores. Can birds, for example, choose their nesting sites close
to herbivore-rich places? Quick choice of a breeding ground is especially important
for migratory birds, which are time-limited and need to quickly select good-quality
territories to ensure successful reproduction (Lundberg & Alatalo 1992; Siikamäki 1998;
Sanz 1999). During the breeding season birds need to nd food for both themselves
and their offspring, so ample food resources close by should improve their breeding
success (von Haartman 1982; Lundberg & Alatalo 1992). At least diurnal birds of prey
can use their UV vision to assess the size of vole populations, since vole urine reects
UV light (Viitala et al. 1995; Koivula & Viitala 1999). Thus, assessing the size of prey
populations, especially close the nesting sites may also be useful for other birds, such as
insectivorous passerines.
10 Introduction
1.5. Ecological importance of insectivorous birds to plants
Carnivorous birds are common in ecosystems throughout the world, and numerous
studies have shown that they can affect the population sizes of insects and other small
herbivores (e.g. Holmes 1979; Fowler et al. 1991; Williams-Guillén et al. 2008). An
increasing number of studies have also examined the effect of bird predation cascading
down to plants. A recent review has assessed the importance of birds in reducing plant
damage mainly in forests and agricultural environments in the tropics (Van Bael et al.
2008). One question is to what extent this phenomenon varies among climatic areas, or
between natural and agricultural environments. Recent studies (Sekercioglu 2006; Van
Bael et al. 2008; Whelan et al. 2008) have shown that birds are benecial to plants and
constitute an important part of ecosystems, and that the removal of herbivores from
harvested plants is certainly a potential ecosystem service of economic value (Sekercioglu
2006; Whelan et al. 2008).
Aims of the Thesis 11
2. AIMS OF THE THESIS
In this thesis I studied whether passerine birds are attracted to herbivore-damaged trees
even if they do not see the larvae or damaged leaves (I, II, III, IV). The purpose of study
I was to nd out whether this occurs; studies II and III repeated the rst study with
different species and examined the possible mechanisms birds might use to nd insect-
rich plants. I approached these questions both in controlled laboratory aviaries (I, II) and
in nature (III, IV), carrying out experiments in the northern subarctic (Kevo Research
Station, Finland) (I, III) and in hemiboreal conditions (Turku, Finland) (II, IV) (Fig.
2). In addition to bird attraction, I also used measures from herbivore-damaged and
undamaged birch leaves: light reectance (II), net photosynthesis rate (III) and VOC
emissions (III). In addition, I investigated whether passerine birds were able to use cues
from herbivore-damaged plants in their territory choice (IV). Finally, in order to obtain
a broader view of mutualistic interactions between birds and plants, I conducted meta-
analyses of published articles on this topic (V).
Figure 2. Map showing the experimental study sites: Turku (60°27’ N, 22°16’ E) and Kevo
(69°45’ N, 27°01’ E). Original map is from Wikimedia Commons (commons.wikimedia.org).
12 Material and Methods
3. MATERIAL AND METHODS
In this chapter I briey introduce the species and methods used in the experimental
studies (studies I – IV). More detailed accounts of the methods can be found in the
original articles. Studies I and III were carried out in the subarctic birch zone at the
Kevo Research Station at Utsjoki, Finland (69°45’ N, 27°01’ E). Study II was carried out
at the Botanical Gardens of the University of Turku on the island of Ruissalo, close to the
city of Turku (60°27’ N, 22°16’ E). Study IV was carried out in three forests close to the
city of Turku. They are typical Finnish mixed forests, with Scots pine (Pinus sylvestris
L.) and Norway spruce (Picea abies (L.) H. Karst.) as the main tree species. Both study
sites in Turku (II, IV) belong to the hemiboreal zone.
3.1. Experimental study set-ups
Studies I, II, III and IV were experimental studies, with varying species and methods
(Table 1). In all four of these studies, half of the birches (Betula sp.) had larvae in mesh
bags (herbivore trees); the other half (control trees) had empty mesh bags, with no
herbivores. For the aviary studies (I, II), I always had another person cut a branch from
both an herbivore tree and a control tree. The branches were from outside the mesh bags,
and contained no larvae, damaged leaves or larval faeces. Thus I did not know which
branch was from which tree (i.e. a double blind experiment). The birds were released in
the aviary individually; I observed their behaviour and recorded which branch the bird
rst visited after calming down. The birds could not see the larvae in any of the studies.
The plant, herbivore and bird species used in the experimental studies, the methods used
to monitor birds’ attraction to plants, and the plant variables measured in addition to bird
attraction are shown in Table 1.
3.2. Species studied
In this section I introduce the species shown in Table 1. In all experimental studies I
used common species of deciduous trees, herbivore larvae and passerine birds, in either
the south (II, IV) or the north (I, III) of Finland. Thus these species have had a long
period of coevolution and may already have been interacting mutualistically prior to
the experiments. The species were chosen mainly for practical reasons. In study I, for
instance, willow warblers were not accessible before the end of their breeding season in
late July; I therefore had to use sawy larvae as herbivores, as they feed on mature birch
leaves at that time.
Material and Methods 13
Table 1. Species used in the experimental studies, methods used to monitor birds’ attraction to
plants, and plant variables measured in addition to bird attraction.
Study I Study II Study III Study IV
Plant species
- mountain birch X X
- silver birch X X
- downy birch X
Herbivore species
- autumnal moth X X X
- sawy X
Bird species
- willow warbler X
- great tit X
- blue tit X
- pied ycatcher X
- passerine birds X
Response variable
- choice in aviary X X
- predation of plasticine larvae X
- territory choice X
Plant cues measured
- light reectance X
- photosynthesis rate X
- VOC emissions X
3.2.1. Plants
Mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hämet-Ahti) is the
tree-line species in northern Fennoscandia (Hämet-Ahti 1963). All mountain birches
represent some level of hybridisation of downy birch (B. pubescens Ehrh.) and dwarf
birch (B. nana L.). In northern Finnish Lapland they are typically poly-cormic, i.e. bush-
like formations with multiple stems (ramets) (Kallio & Mäkinen 1978). Silver birch (B.
pendula Roth) and downy birch are common tree species in Europe and Asia (Atkinson
1992). Silver birches mainly grow on dry and sandy soils, while downy birch can also
grow in wetter ground. Downy birch is usually smaller than silver birch. There are no
major genetic differences between these three birch species, all of which can hybridise
with each other (Elkington 1968; Wilsey et al. 1998).
3.2.2. Herbivores
The autumnal moth (Epirrita autumnata Borkhausen; Lepidoptera, Geometridae) is the
main herbivore of mountain birch in northern Finnish Lapland (Tenow 1972) but is also
relatively common in southern Finland (Ruohomäki et al. 2000). Its population cycle is
ca. 9–11 years, and at its peak phase it can cause large-scale forest defoliation in northern
Fennoscandia (Haukioja et al. 1988). It overwinters in the form of eggs; the larvae hatch
at the time of birch budbreak (Kevo, late May – early June; Turku, early May). The larvae
14 Material and Methods
can feed on several woody plants, but are usually found on birch leaves since birch is
often the most common deciduous tree. The autumnal moth has ve larval instars, after
which it pupates in the soil (Kevo, late June – early July; Turku, early June). Adult
moths emerge and y from August to October. Autumnal moth larvae, pupae and adults
are common prey for e.g. insectivorous birds (Tanhuanpää et al. 2001), small mammals
(Tanhuanpää et al. 1999) and invertebrate predators (Karhu & Neuvonen 1998), and
eggs, larvae and pupae common hosts for several parasitoids (Ruohomäki et al. 2000;
Klemola et al. 2008).
The sawy used in study I (Arge fuscinervis Lindqvist; Hymenoptera, Symphyta) is
one of many sawy species found in Finnish Lapland (Kouki et al. 1994). A. fuscinervis
overwinters as a prepupa; the adults emerge in spring. Females oviposit their eggs on
birch leaves. The larvae hatch in June – July and eat mature birch leaves before pupating
in late July – early August. The predators of A. fuscinervis are mainly ants (Punttila et
al. 2004; Petre et al. 2007) and birds, which eat also adult sawies (Wilson et al. 1999).
The sawies also have parasitoids (K. Ruohomäki et al., unpublished data) but there has
been no detailed research of those.
3.2.3. Birds
The willow warbler (Phylloscopus trochilus L.) is the most common bird species in
Finland (especially in Lapland), and breeds throughout northern and temperate Europe
and Asia (Väisänen et al. 1998). It is a migratory bird, wintering mainly in sub-Saharan
Africa. Willow warblers forage in the canopies of trees and eat various insects, such as
lepidopteran and sawy larvae (Nyström 1991). They build their nests of grasses on the
ground; the edglings leave the nest between mid-July and early August.
The pied ycatcher (Ficedula hypoleuca Pallas) is also a migratory bird, wintering in
western Africa. It is a common insectivorous bird species in many parts of Europe,
including Finland. It breeds in natural holes and in nest-boxes. Although pied ycatchers
are often thought to catch insects mainly in the air, they actually also forage to a
considerable extent on the ground and on tree branches (Lundberg & Alatalo 1992).
They arrive in Finland in May and leave in late summer – early autumn.
In contrast to the above two bird species, tits are mainly residents in Finland; after
successful breeding years, however, there may be short-distance partial migrations
(Väisänen et al. 1998). The great tit (Parus major L.) is one of the most common bird
species in Eurasia. It breeds in holes, nowadays often in nest-boxes. The great tit is
omnivorous, but during the summer its diet consists mainly of insects (Eeva et al. 2005).
The blue tit (P. caeruleus L.; also Cyanistes caeruleus) likewise occurs in many parts of
Eurasia; the Finnish population is found in the southern half of the country (Väisänen et
al. 1998). Breeding and foraging habits are similar to those of the great tit.
Material and Methods 15
In study III, the birds used belonged to the local passerine bird fauna. Species observed
in the study area were the pied ycatcher, the willow warbler, the brambling (Fringilla
montifringilla L.), the great tit, the Siberian tit (Parus cinctus Boddaert; also Poecile
cinctus), the common redpoll (Carduelis ammea L.), the yellow wagtail (Motacilla
ava L.), the bohemian waxwing (Bombycilla garrulus L.), the bluethroat (Luscinia
svecica L.) and the eldfare (Turdus pilaris L.).
3.3. Observation methods
The aviary (or booth) used in study I was 118 cm deep, 97 cm high and 75 cm wide. I
observed bird behaviour through a window (10 × 10 cm) in the door. The light in the
booth was made as natural as possible, covering a wide spectrum (with UV wavelengths),
and non-ickering. The aviary used in study II was slightly larger (height 176 cm, depth
116 cm, width 116 cm) than in the rst study. It too had a small window in the door;
the main form of observation, however, was with a video camera lming through a hole
in the ceiling. This aviary had two different light conditions: UV light (non-ickering
uorescent light with a wide spectrum) and non-UV (normal uorescent light with a UV
lter).
In study III, articial larvae were used to measure the bird predation rate in the
experimental trees. The larvae were made of light green plasticine (close to the colour of
for instance the autumnal moth larva) and were attached to the branches with thin metal
wire. As the plasticine remained soft for several days (despite rain or cold weather), it
was easy to check the articial larvae daily and record whether they had been pecked at
by birds (see also Brodie 1993).
Study IV dealt with the territorial choices of pied ycatchers. All territories had two
nest-boxes, with two small birches growing close to the boxes. Half of the territories
contained autumnal moth larvae on birch branches inside mesh bags, while the other
half contained only empty mesh bags. The arrival date of both male and female pied
ycatchers in the territories in spring was recorded daily. I also observed whether the
birds preferred territories with hidden larvae over control territories.
3.4. Plant cues studied
Birds most likely receive cues from herbivore-damaged plants through sight and/
or olfaction. To study these cues I used several methods. In study II half of the birds
were tested in UV light, the other half in non-UV light. If the birds were interested in
herbivore-damaged branches only in UV light, they were probably using their UV vision
to nd these trees. In study II, the light reectance of the leaves of the experimental
silver birches was measured with a spectrophotometer to obtain more information as
16 Material and Methods
to whether birds were able to use their vision to recognise herbivore-damaged birches.
In study III the plant cues of mountain birches measured were VOC emissions and net
photosynthesis rate. A total of 15 different VOCs (mono-, homo- and sesquiterpenes and
green leaf volatiles) were measured. The differences between the herbivore and control
trees in the composition and quantities of these VOCs, and the correlations between
VOC emissions and avian predation on the birches, would indicate whether birds could
use olfaction in detecting herbivores. The net photosynthesis rate is generally correlated
with the light reectance of the leaves; undamaged plants can photosynthesise more
than damaged ones and are therefore greener (Zangerl et al. 2002; Peñuelas et al. 2004;
Louis et al. 2005). This is another way to determine whether birds are able to use vision
to search for insect-rich trees.
3.5. Meta-analysis
To obtain the studies for the meta-analyses in my study V, I searched online databases
with different combinations of keywords, as well as references in already found articles,
to nd all studies of tritrophic interactions among birds, herbivores and plants. To qualify
for use in the meta-analysis, an article had to fulll the following requirements: 1) at least
one of the predators in the system studied had to be a bird species; 2) the experiment had
to include a group with either no birds at all or signicantly fewer of them than in the
second group, in which bird predation was allowed; 3) there had to be at least one plant
response measured, such as the extent of leaf damage or changes in biomass, growth, or
mortality; 4) sample sizes and means, with their deviation terms, had to be stated in the
article text or in a table or gure, for both experimental and control groups. I calculated
an effect size [log response ratio, lnR = ln(control mean) - ln(experimental mean)] and
its condence interval for all experiments in the articles found. I used those values to
compare studies performed in different environments and climatic areas, and different
plant responses in plants of different ages.
Main Results and Discussion 17
4. MAIN RESULTS AND DISCUSSION
The rst experiment (I) showed that willow warblers were more attracted to the intact
branches of herbivore-damaged trees than to those of the control trees. The experiment
was designed to reveal the possible attraction of herbivore-induced trees, not the
mechanism behind the hypothetical phenomenon. In the subsequent experiments I
tested how the birds were able to nd the herbivore-damaged trees. I therefore used
in study II two different light conditions in the aviary, with half of the birds tested in
light with UV wavelengths and half in non-UV light, but this did not affect the birds’
attraction. I also measured the light reectance of the trees with a spectrophotometer.
The control trees reected signicantly more light throughout the visible spectrum
than the herbivore-damaged trees. Thus we could rule out the possibility of UV cues
alone being important in attracting birds. It seems more likely that light reectance
across the whole spectrum visible to birds (315–700 nm) is relevant. Another nding
in study II was that birds were attracted to herbivore-damaged birches only if the
branches were from trees growing in the sunnier forest patch. Likewise in the case
of the light reectance of the leaves, a difference was found between treatment and
control trees only in the sunnier forest patch but not in the shadier one. This was an
unexpected nding; I can only speculate as to why the birds could not distinguish
between the branches or why the difference in light reectance is absent in the shadier
forest patch. Shaded plants photosynthesise less than plants in sunshine, and their
chemistry is thus different (Henriksson et al. 2003); possibly they cannot invest as
much in defence chemicals as plants in sunnier places.
In study III signicantly more pecked articial plasticine larvae were found
in herbivore-damaged birches than in undamaged control trees; thus the same
phenomenon as observed in studies I and II in aviaries was also observed in nature.
To nd potential cues the birds might use, we measured emissions of several VOCs
and the net photosynthesis rate in the same experimental trees. There were signicant
differences in VOC emissions between herbivore-damaged and control birches, and a
correlation was found between the emission of three VOCs [(E)-DMNT, β-ocimene
and linalool] and avian predation on the birches. The same three VOCs are also
among the key compounds in the attraction of insect parasitoids and predatory mites
to herbivore-damaged plants (Dicke et al. 1990; De Moraes et al. 1998; Kappers et
al. 2005; Shimoda et al. 2005). This suggests that birds, invertebrate predators and
parasitoids may be taking the same cues from foliage, and plants may thus possess a
more universal signalling system, functioning for all predators and parasitoids. The net
photosynthesis rate was also signicantly higher in control than in herbivore-damaged
trees, suggesting that birds may use olfaction, vision or both as cues for nding insect-
rich trees.
18 Main Results and Discussion
My studies (I, II, III) are the rst to suggest that insectivorous birds may react to
induced changes in herbivore-damaged plants, as the birds were more attracted to the
intact branches of herbivore-damaged birches than to the intact branches of the controls.
Because of the systemic nature of inducible responses (e.g. Haukioja & Niemelä 1979;
Haukioja & Hanhimäki 1985; Hanhimäki & Senn 1992; Kaitaniemi & Ruohomäki 2001;
Farag & Paré 2002), the test branches from herbivore trees probably differed in chemical
composition from those of the control trees. The birds were somehow able to sense this
difference and adjust their behaviour accordingly. Studies in behavioural ecology are
rarely replicated nowadays, which can make it difcult to generalise over other taxa
and ecosystems (Owens 2006). Thus these three separate studies on the attraction of
passerine birds to herbivore-damaged trees, using different combinations of species and
different methods, provide strong support for the existence of this phenomenon (I, II,
III).
Study IV showed that induced cues from herbivore-damaged birches did not affect
the order in which pied ycatchers occupied the territories. There are several potential
explanations for this. One is that the birches did not raise induced defences or production
of VOCs that would have been detectable by the birds. We did not measure tree responses
in this experiment, but it has been shown repeatedly that birches have induced responses
to herbivory (e.g. Kause et al. 1999, Haukioja 2005, Vuorinen et al. 2007), and that these
are detectable by birds (I, II, III). Another explanation could be that the pied ycatchers
have not evolved to use such cues in their choice of territory. The autumnal moth larvae
reach their nal instar during the time of pied ycatcher egg-laying which is energetically
demanding and food availability affects the tness of the birds (e.g. Visser & Lessells
2001; Moreno et al. 2008). Thus, an ability to choose a larval rich territory should be
benecial for the birds. Yet another reason may be that the scale of our treatment (two
small defoliated or control birches per territory) was too small to inuence the birds’
decisions. But still the amount of larvae in our treatment (60–80 larvae in two small trees
per territory) was at least tenfold higher than natural larval densities in the area (0.27
larvae per 100 birch short shoots, Kai Ruohomäki, pers. comm.). It is still not known
what pied ycatchers’ main criteria are in choosing a territory (Alatalo et al. 1986;
Slagsvold 1986). So far it is known that pied ycatchers prefer to nest in deciduous over
coniferous forest (Lundberg et al. 1981), probably since the former tend to have more
caterpillars (Gibb & Betts 1963; Royama 1970), and that they rst choose territories in
larger forest patches (Huhta et al. 1998). Pied ycatchers also avoid nesting too close to
their avian predators, sparrowhawks (Accipiter nisus) (Thomson et al. 2006) or pygmy
owls (Glaucidium passerinum) (C. Morosinotto et al., unpublished data). They are also
attracted to the presence of resident species (e.g. tits) close to the territories (Forsman et
al. 2002, 2007). Nonetheless, these aspects were not examined in study IV, as the main
interest was the role of herbivore larvae which evidently needs more research.
Main Results and Discussion 19
The set of meta-analyses in study V (a review study) revealed that plants in all
environments (natural and agricultural) and climates (boreal, temperate and tropical)
benet from the presence of birds that remove herbivorous insects and other arthropods
feeding on the plants. There is thus a trophic cascade, from birds via herbivores to plants.
The results do not support the general notion that trophic cascades can only occur in
simple ecosystems, such as agricultural environments, or in colder climatic areas (Polis
& Strong 1996). The strongest effects were usually found in measuring plant leaf
damage, biomass or mortality. Leaf damage is the rst sign of herbivory and is usually
rather easy to measure, but it does not always reveal the degree of damage to the tness
of the plant over time. Thus the study by Mols & Visser (2002) is a notable exception;
they found that the presence of birds increased the amount of fruit produced by apple
trees (Malus domestica). Studies with mature plants showed stronger effects than studies
with saplings. This result may derive from higher bird abundances in mature forests (e.g.
Rice & Greenberg 2000), or from the tendency of saplings to be controlled more by
bottom-up effects (e.g. inorganic resources) than top-down ones (e.g. predation). Study
V, along with some other recent studies (Sekercioglu 2006; Van Bael et al. 2008; Whelan
et al. 2008) have shown that birds are benecial to plants and form an integral part of
ecosystems.
20 Conclusions
5. CONCLUSIONS
What general conclusions can be drawn from the studies presented in this PhD thesis?
First of all, I can say that birds recognise herbivore-damaged trees and are attracted to
them (I, II, III). I succeeded in showing this preference under both aviary (I, II) and
natural conditions (III). I examined the possible cues emitted by herbivore-damaged
birches that birds could sense either visually, i.e. differences in light reection (II)
and net photosynthesis rate (III), or by olfaction, i.e. differences in VOC emissions
(III). To study the importance of herbivore-damaged plants for birds, I examined the
territory choices made by pied ycatchers between territories with herbivore-damaged
and undamaged birches (IV). I found no differences, even though plants with abundant
herbivores are most likely important to birds. My review of trophic cascades from birds
to plants showed that plants do better in the presence of birds (V). It thus seems that the
interaction is mutually benecial to both birds and plants. These ve studies have opened
up opportunities for future research on the role for instance of vision and olfaction in this
mutualistic interaction between birds and plants. The next steps in this eld should focus
on the details of birds’ sensory mechanisms (vision and olfaction), and on the ecological
importance of the tritrophic interaction to both birds and plants on a broader scale (e.g.
more species in an experiment or a longer study time).
Acknowledgements 21
ACKNOWLEDGEMENTS
When in early spring 2003 professor Erkki Haukioja asked if I would be interested in a bit
risky MSc thesis topic, I would have never thought that it would be a topic I would work
with the next ve years. We were both sceptical if birds could sense herbivore-damaged
birches without seeing the herbivores or damaged leaves. But as my MSc thesis and this
PhD thesis show, birds are attracted to herbivore-damaged trees. I am very grateful for
professor Haukioja for giving the idea for me to study.
My supervisors Tero Klemola and Toni Laaksonen have helped me with planning the
experiments, eld work, analysing the data, writing the papers and in several other ways.
I am very pleased that I had them as supervisors because they are both persons I can
always ask questions (even stupid ones) and get understandable answers.
Docents Leena Lindström and Seppo Rytkönen reviewed the thesis and gave helpful
comments. Tea Ammunét, Fiia Haavisto, Anne Muola, Päivi Sirkiä, Outi Vesakoski and
Sonja Yletyinen did an excellent job as the opponents of my practice defence. Ellen Valle
kindly checked the language of the introduction. My co-authors from the University of
Kuopio have taught me a lot about chemistry of plants, so thank you to Jarmo Holopainen,
James Blande, Giorgio Alessio, Juha Heijari and Panu Piirtola.
I would not have done any research without funding. Therefore I am very thankful for
the Jenny and Antti Wihuri foundation for funding basically my whole PhD project.
Several people have helped me with the eld work and otherwise in both Turku and
Kevo. Special thanks I want to give to Päivi Sirkiä who was rst my assistant in 2004
and 2006 (I think she has been the best research assistant I have had) and then a very
good colleague and co-author. I want to thank also Tea Ammunét, Tommi Andersson,
Tapio Eeva, Annette Heisswolf, Marjo Helander, Lasse Iso-Iivari, Aino Kalske, Lauri
Kapari, Netta Klemola, Riitta Koivikko, Julia Koricheva, Saara Koutaniemi, Kukka
Kyrö, Esa Lehikoinen, Jorma Nurmi, Kirsi Reponen, Kai Ruohomäki, Suvi Ruuskanen,
Pälvi Salo, Robert Thomson, Elina Vainio, Emilia Vainio and Outi Vesakoski. There
were also several other people helping at the Kevo Subarctic Research Institute, at the
Ruissalo Botanical Gardens and forests around Turku. The city of Turku allowed me to
use their forests in my studies. Tuija Koivisto and Jorma Nurmi have helped with all
kinds of practical things at the university and Niina Kukko is an irreplaceable ofce
secretary. Matti Ketola has always helped with all computer-related problems.
I want to thank all the people of the Section of Ecology for a pleasant working
environment. The PhD seminar has been very helpful for the PhD students with all the
teaching, comments and discussions. I have learned e.g. how to write manuscripts, have
presentations and review papers. I thank also the fellow SEBDEM 2008 organisers
22 Acknowledgements
Fiia Haavisto, Paula Lehtonen, Meri Lindqvist, Anne Muola, Marie Nordström, Suvi
Ruuskanen and Päivi Sirkiä. At least I thought that the symposium organising was fun,
educating and it looks good in my CV. The almost weekly coffee break with the Peggy
group has been a meeting I have not wanted to miss. It is very relaxing to chat about other
things than your own research problems and hear what is happening in other sections. I
am also thankful of the infrequent coffee and lunch breaks with lively discussions of all
aspects of life for Annette, Anniina, Chiara, Elina K., Fiia, Karen, Katrine, Liisa, Marja,
Miia, Nanne, Netta, Päivi, Pälvi, Salla-Riikka, Sari, Sonja, Suvi and all the people who
I forgot to mention.
I have been fortunate to have friends to take my thoughts away from work every now
and then. Pauliina Wäli always managed to nd something fun to do during the long
evenings at Kevo. Anna Swanljung was rst a friend from the world of tennis but
later also a fellow biologist. I will never forget all those visits we had to the Kungliga
Tennishallen in Stockholm. Following the happenings in the world of pro tennis has
been my dear hobby for over 12 years. All the people I have met in online tennis forums,
and at tournaments in Stockholm, Rosmalen, Paris, Wimbledon, Barcelona etc deserve
big thanks for sharing the tennis fandom with me. I will always be a tennis fanatic with
you! During the past couple of years I have been also a “hang-around” member in an
aikido group of Turku. So thanks for all the cheerful evenings to Paavo, Hanne, Petteri,
Anni, Tuomas, Piia, Asko and several others.
I guess I have been a bird watcher more or less all my life thanks to my father. There
is no better place to watch birds than in Pori. And it never has been a problem that
often I was the only female taking part in the bird station course in Säppi or freezing in
Tahkoluoto watching bird migration on the sea. So I want to thank Matti, Matti, Matti,
Martti, Petteri, Kalle, Kimmo, Asko, Leo and many, many others.
I think I have the best family in the world. My parents Kari and Anna, sister Inkeri and
brother Risto are very important to me. I knew already in very young age that I am
interested in nature, and they have always supported and understood me. The last person
to be thanked deserves the dearest thanks. Toni N. has been in my life almost as long as
I have worked with this book and these years with him have been the best of my life.
He is (almost) always willing to listen about the new things I have learned about birds,
larvae and birches. He is also very helpful with anything involving computers, cameras
or other technical gadgets. Besides, he brought to my life Tiikeli and Pantteli. A giant
hug & kiss to you!
References 23
REFERENCES
Agrawal A. 2006. Macroevolution of plant defense
strategies. Trends in Ecology and Evolution 22:
103–109.
Alatalo RV, Lundberg A & Glynn C. 1986. Female
pied ycatchers choose territory quality and not
male characteristics. Nature 323: 152–153.
Amo L, Galván I, Tomás G & Sanz JJ. 2008.
Predator odour recognition and avoidance in a
songbird. Functional Ecology 22: 289–293.
Atkinson MD. 1992. Betula pendula Roth (B.
verrucosa Ehrh.) and B. pubescens Ehrh. Journal
of Ecology 80: 837–870.
Bergelson JM & Lawton JH. 1988. Does foliage
damage inuence predation on the insect
herbivores of birch? Ecology 69: 434–445.
Boege K & Marquis RJ. 2006. Plant quality and
predation risk mediated by plant ontogeny:
consequences for herbivores and plants. Oikos
115: 559–572.
Brodie ED III. 1993. Differential avoidance of coral
snake banded patterns by free-ranging avian
predators in Costa Rica. Evolution 47: 227–235.
Church SC, Bennett ATD, Cuthill IC & Partridge
JC. 1998. Ultraviolet cues affect the foraging
behaviour of blue tits. Proceedings of the Royal
Society B 265: 1509–1514.
Coley PD & Barone JA. 1996. Herbivory and plant
defenses in tropical forests. Annual Review of
Ecology and Systematics. 27: 305–335.
Cuthill IC. 2006. Color perception. In: Hill GE,
McGraw KJ, editors. Bird Coloration, Mechanisms
and Measurements. Cambridge, Massachusetts:
Harvard University Press. p. 3–40.
De Moraes CM, Lewis WJ, Pare PW, Alborn HT &
Tumlinson JH. 1998. Herbivore-infested plants
selectively attract parasitoids. Nature 393: 570–
573.
Dicke M, van Beek TA, Posthumus MA, ben Dom
N, van Bokhoven H & de Groot AE. 1990.
Isolation and identication of volatile kairomone
that affects acarine predator–prey interactions.
Involvement of host plant in its production.
Journal of Chemical Ecology 16: 381–396.
Dicke M & van Loon JJA. 2000. Multitrophic
effects of herbivore-induced plant volatiles
in an evolutionary context. Entomologia
Experimentalis et Applicata 97: 237–249.
Dudareva N, Negre F, Nagegowda DA & Orlova I.
2006. Plant volatiles: Recent advances and future
perspectives. Critical Reviews in Plant Sciences
25: 417–440.
Eeva T, Ryömä M & Riihimäki J. 2005. Pollution-
related changes in diets of two insectivorous
passerines. Oecologia. 145: 629–639.
Elkington TT. 1968. Introgressive hybridization
between Betula nana L. and B. pubescens Ehrh.
in north-west Iceland. New Phytologist 67: 109–
118.
Farag MA & Paré PW. 2002. C6-Green leaf volatiles
trigger local and systemic VOC emissions in
tomato. Phytochemistry 61: 545–554.
Fowler AC, Knight RL, Luke George T &
McEwen LC. 1991. Effects of avian predation
on grasshopper populations in North Dakota
grasslands. Ecology 72: 1775–1781.
Gibb JA & Betts MM. 1963. Food and food supply
of nestling tits (Paridae) in Breckland pine.
Journal of Animal Ecology 32: 489–533.
Gwinner H & Berger S. 2008. Starling males select
green nest material by olfaction using experience-
independent and experience-dependent cues.
Animal Behaviour 75: 971–976.
von Haartman L. 1982. The biological signicance
of the nuptial plumage of the male pied ycatcher.
In: Proceedings of the XVIII International
Ornithological Congress (eds. Ilyichev VD &
Gavrilov VM), pp. 1–22. Nauka Publishers.
Halitschke R, Stenberg JA, Kessler D, Kessler A &
Baldwin IT. 2008. Shared signals – ‘alarm calls’
from plants increase apparency to herbivores
and their enemies in nature. Ecology Letters 11:
24–34.
Hämet-Ahti L. 1963. Zonation of the mountain birch
forests in northernmost Fennoscandia. Annales
Botanici Societatis ‘Vanamo’ 34: 1–127.
Hanhimäki S & Senn J. 1992. Sources of variation
in rapidly inducible responses to leaf damage
in the mountain birch-insect herbivore system.
Oecologia 91: 318–331.
Haukioja E. 1990. Induction of defenses in trees.
Annual Review of Entomology 36: 25–42.
Haukioja E. 2003. Putting the insect into the birch-
insect interaction. Oecologia 136: 161–168.
Haukioja E & Hanhimäki S. 1985. Rapid wound-
induced resistance in white birch (Betula
pubescens) foliage to the geometrid Epirrita
autumnata: a comparison of trees and moths
within and outside the outbreak range of the
moth. Oecologia 65: 223–228.
Haukioja E, Neuvonen S, Hanhimäki S & Niemelä
P. 1988. The autumnal moth in Fennoscandia. In:
Berryman AA, editor. Dynamics of forest insect
24 References
populations: patterns, causes, implications. New
York: Plenum Press. p. 163–178.
Haukioja E & Niemelä P. 1979. Birch leaves as a
resource for herbivores: seasonal occurrence of
increased resistance in foliage after mechanical
damage to adjacent leaves. Oecologia 39: 151–
159.
Haviola S, Kapari L, Ossipov V, Rantala MJ,
Ruuhola T & Haukioja E. 2007. Foliar phenolics
are differently associated with Epirrita autumnata
growth and immunocompetence. Journal of
Chemical Ecology 33: 1013–1023.
Heil M, Greiner S, Meimberg H, Krüger R, Noyer
J-L, Heubl G, Linsenmair KE & Boland W. 2004.
Evolutionary change from induced to constitutive
expression of an indirect plant resistance. Nature
430: 205–208.
Heil M & Silva Bueno JC. 2007. Within-plant
signaling by volatiles leads to induction and
priming of an indirect plant defense in nature.
Proceedings of the National Academy of Sciences
of the U.S.A. 104: 5467–5472.
Heinrich B & Collins SL. 1983. Caterpillar leaf
damage, and the game of hide-and-seek with
birds. Ecology 64: 592–602.
Henriksson J, Haukioja E, Ossipov V, Ossipova S,
Sillanpää S, Kapari L & Pihlaja K. 2003. Effects
of host shading on consumption and growth of the
geometrid Epirrita autumnata: interactive roles
of water, primary and secondary compounds.
Oikos 103: 3–16.
Hoballah MEF & Turlings TCJ. 2001. Experimental
evidence that plants under caterpillar attack may
benet from attracting parasitoids. Evolutionary
Ecology Research 3: 553–565.
Holmes RT, Schultz JC & Nothnagle P. 1979.
Bird predation on forest insects: an exclosure
experiment. Science 206: 462–463.
Holopainen JK. 2004. Multiple functions of
inducible plant volatiles. Trends in Plant Science
9: 529–533.
Honkavaara J, Koivula M, Korpimäki E, Siitari H
& Viitala J. 2002. Ultraviolet vision and foraging
in terrestrial vertebrates. Oikos 98: 505–511.
Huhta E, Jokimäki J & Rahko P. 1998. Distribution
and reproductive success of pied ycatcher
Ficedula hypoleuca in relation to forest patch
size and vegetation characteristics; the effect of
scale. Ibis 140: 214–222.
Janssen A, Sabelis MW & Bruin J. 2002. Evolution
of herbivore-induced plant volatiles. Oikos 97:
134–138.
Jones MP, Pierce KE & Ward D. 2007. Avian vision:
A review of form and function with special
consideration to birds of prey. Journal of Exotic
Pet Medicine 16: 69–87.
Kaitaniemi P & Ruohomäki K. 2001. Sources of
variability in plant resistance against insects: free
caterpillars show strongest effects. Oikos 95:
461–470.
Kalka MB, Smith AR & Kalko EKV. 2008. Bats
limit arthropods and herbivory in a tropical
forest. Science 320: 71.
Kallio P & Mäkinen Y. 1978. Vascular ora of Inari
Lapland. 4. Betulaceae. Reports from the Kevo
Subarctic Research Station 14: 38–63.
Kappers IF, Aharoni A, Van Herpen TW, Luckerhoff
LL, Dicke M & Bouwmeester HJ. 2005. Genetic
engineering of terpenoid metabolism attracts
bodyguards to Arabidopsis. Science 309: 2070–
2072.
Karban R & Baldwin IT. 1997. Induced Responses
to Herbivory. University of Chicago Press,
Chicago, IL, USA.
Karhu KJ & Neuvonen S. 1998. Wood ants and
a geometrid defoliator of birch: predation
outweighs benecial effects through the host
plant. Oecologia 113: 509–516.
Kause A, Ossipov V, Haukioja E, Lempa K,
Hanhimäki S & Ossipova S. 1999. Multiplicity
of biochemical factors determining quality of
growing birch leaves. Oecologia 120: 102–112.
Kessler A & Baldwin IT. 2001. Defensive function
of herbivore-induced plant volatile emissions in
nature. Science 291: 2141–2144.
Klemola N, Kapari L & Klemola T. 2008. Host
plant quality and defence against parasitoids: no
relationship between levels of parasitism and a
geometrid defoliator immunoassay. Oikos 117:
926–934.
Koivula M & Viitala J. 1999. Rough-legged
buzzards use vole scent marks to assess hunting
areas. Journal of Avian Biology 30: 329–332.
Kost C & Heil M. 2006. Herbivore-induced plant
volatiles induce an indirect defense in neighboring
plants. Journal of Ecology 94: 619–628.
Kouki J, Niemelä P & Viitasaari M. 1994. Reversed
latitudinal gradient in species richness of sawies
(Hymenoptera, Symphyta). Annales Zoologici
Fennici 31: 83–88.
Louis J, Ounis A, Ducruet J-M, Evain S, Laurila
T, Thum T, Aurela M, Wingsle G, Alonso L,
Pedros R & Moya I. 2005. Remote sensing of
sunlight-induced chlorophyll uorescence and
reectance of Scots pine in boreal forest during
spring recovery. Remote Sensing of Environment
96: 37–48.
References 25
Lundberg A & Alatalo RV. 1992. The pied ycatcher.
London: T & A D Poyser Ltd.
Lundberg A, Alatalo RV, Carlson A & Ulfstrand S.
1981. Biometry, habitat distribution and breeding
success in the pied ycatcher Ficedula hypoleuca.
Ornis Scandinavica 12: 68–79.
Marquis RJ & Whelan CJ. 1994. Insectivorous
birds increase growth of white oak through
consumption of leaf-chewing insects. Ecology
75: 2007–2014.
van der Meijden E & Klinkhamer PGL. 2000.
Conicting interests of plants and the natural
enemies of herbivores. Oikos 89: 202–208.
Mennerat A. 2008. Blue tits (Cyanistes caeruleus)
respond to an experimental change in the
aromatic plant odour composition of their nest.
Behavioural Processes 79: 189–191.
Mennerat A, Bonadonna F, Perret P & Lambrechts
MM. 2005. Olfactory conditioning experiments
in a food-searching passerine bird in semi-natural
conditions. Behavioural Processes 70: 264–270.
Mols CMM & Visser ME. 2002. Great tits can
reduce caterpillar damage in apple orchards.
Journal of Applied Ecology 39: 888–899.
Müller MS, McWilliams SR, Podlesac D,
Donaldson JR, Bothwell HM & Lindroth RL.
2006. Tri-trophic effects of plant defenses:
chickadees consume caterpillars based on host
leaf chemistry. Oikos 114: 507–517.
Niimura Y & Nei M. 2006. Evolutionary dynamics
of olfactory and other chemosensory receptor
genes in vertebrates. Journal of Human Genetics
51: 505–517.
Niinemets Ü, Loreto F & Reichstein M. 2004.
Physiological and physicochemical controls
on foliar volatile organic compound emissions.
Trends in Plant Science 9: 180–186.
Nykänen H & Koricheva J. 2004. Damage-induced
changes in woody plants and their effects on
insect herbivore performance: a meta-analysis.
Oikos 104: 247–268.
Nyström, KGK. 1991. On sex-specic foraging
behaviour in the Willow Warbler, Phylloscopus
trochilus. Canadian Journal of Zoology 69: 462–
470.
Oksanen L & Oksanen T. 2000. The logic and realism
of the hypothesis of exploitation ecosystems. The
American Naturalist 155: 703–723.
Owens IPF. 2006. Where is behavioral ecology
going? Trends in Ecology & Evolution 21: 356–
361.
Peñuelas J & Llusià J. 2004. Plant VOC emissions:
making use of the unavoidable. Trends in Ecology
& Evolution 19: 402–404.
Peñuelas J, Munné-Bosch S, Llusià J & Filella
I. 2004. Leaf reectance and photo- and
antioxidant protection in eld-grown summer-
stressed Phillyrea angustifolia. Optical signals of
oxidative stress? New Phytologist 162: 115-124.
Persson L. 1999. Trophic cascades: Abiding
heterogeneity and the trophic level concept at the
end of the road. Oikos 85: 385–397.
Petit C, Hossaert-McKey M, Perret P, Blondel J
& Lambrechts MM. 2002. Blue tits use selected
plants and olfaction to maintain an aromatic
environment for nestlings. Ecology Letters 5:
585–589.
Petre C-A, Detrain C & Boevé J-L. 2007. Anti-
predator defence mechanisms in sawy larvae of
Arge (Hymenoptera, Argidae). Journal of Insect
Physiology 53: 668–675.
Polis GA & Strong DR 1996. Food web complexity
and community dynamics. The American
Naturalist 147: 813–846.
Price PW, Bouton CE, Gross P, McPheron BA,
Thompson JN & Weis AE. 1980. Interactions
among three trophic levels: inuence of plants
on interactions between insect herbivores and
natural enemies. Annual Review of Ecology and
Systematics 11: 41–65.
Punttila P, Niemilä P & Karhu K. 2004. The impact
of wood ants (Hymenoptera: Formicidae) on the
structure of invertebrate community on mountain
birch (Betula pubescens ssp. czerepanovii).
Annales Zoologici Fennici 41: 429–446.
Rice RA & Greenberg R. 2000. Cacao cultivation
and the conservation of biological diversity.
Ambio 29: 167–173.
Roper TJ. 1999. Olfaction in birds. Advances in the
Study of Behavior 28: 247–332.
Rosenstiel TN, Ebbets AL, Khatri WC, Fall R &
Monson RK 2004. Induction of poplar leaf nitrate
reductase: A test of extrachloroplastic control of
isoprene emission rate. Plant Biology 6: 12–21.
Roth TC, Cox JG & Lima SL. 2008. Can foraging
birds assess predation risk by scent? Animal
Behaviour 76: 2021–2027.
Royama T. 1970. Factors governing the hunting
behaviour and selection if food by the great tit
(Parus major L.). Journal of Animal Ecology 39:
619–668.
Ruohomäki K, Tanhuanpää M, Ayres MP,
Kaitaniemi P, Tammaru T & Haukioja E. 2000.
Causes of cyclicity of Epirrita autumnata
(Lepidoptera, Geometridae): grandiose theory
and tedious practice. Population Ecology 42:
211–223.
26 References
Sanz JJ. 1999. Seasonal variation in reproductive
success and post-nuptial moult of blue tits
in southern Europe: an experimental study.
Oecologia 121: 377-382.
Schmitz OJ, Krivan V & Ovadia O. 2004. Trophic
cascades: the primacy of trait-mediated indirect
interactions. Ecology Letters 7: 153–163.
Sekercioglu CH. 2006. Increasing awareness of
avian ecological function. Trends in Ecology and
Evolution 21: 464–471.
Shimoda T, Ozawa R, Sano K, Yano E &
Takabayashi J 2005. The involvement of volatile
infochemicals from spider mites and from food-
plants in prey location of the generalist predatory
mite Neoseiulus californicus. Journal of Chemical
Ecology 31: 2019–2032.
Siikamäki P. 1998. Limitation of reproductive
success by food availability and breeding time in
pied ycatchers. Ecology 79: 1789–1796.
Slagsvold T. 1986. Nest site settlement by the
Pied Flycatcher: does the female choose her
mate for quality of his house or himself? Ornis
Scandinavica 17: 210–220.
Staudt M & Lhoutellier L. 2007. Volatile organic
compound emission from holm oak infested
by gypsy moth larvae: evidence for distinct
responses in damaged and undamaged leaves.
Tree Physiology 27: 1433–1440.
Steiger SS, Fidler AE, Valcu M & Kempenaers B.
2008. Avian olfactory receptor gene repertoires:
evidence for a well-developed sense of smell in
birds? Proceedings of the Royal Society B 275:
2309–2317.
Takabayashi J & Dicke M. 1996. Plant–carnivore
mutualism through herbivore-induced carnivore
attractants. Trends in Plant Science 1: 109–113.
Tanhuanpää M, Ruohomäki K, Kaitaniemi P &
Klemola T. 1999. Different impact of pupal
predation on populations of Epirrita autumnata
(Lepidoptera; Geometridae) within and outside
the outbreak range. Journal of Animal Ecology
68: 562–570.
Tanhuanpää M, Ruohomäki K & Uusipaikka
E. 2001. High larval predation rate in non-
outbreaking populations of a geometrid moth.
Ecology 82: 281–289.
Tenow, O. 1972. The outbreaks of Oporinia
autumnata Bkh. and Operopthera spp. (Lep.,
Geometridae) in the Scandinavian mountain chain
and northern Finland 1862–1968. Zoologiska
Bidrag från Uppsala, Supplement 2: 1–107.
Tentelier C, Wajnberg E & Fauvergue X. 2005.
Parasitoids use herbivore-induced information
to adapt patch exploitation behavior. Ecological
Entomology 30: 739–744.
Turlings TCJ, Tumlinson JH & Lewis WJ. 1990.
Exploitation of herbivore-induced plant odors
by host-seeking parasitic wasps. Science 250:
1251–1253.
Turlings TCJ & Wäckers F. 2004. Recruitment of
predators and parasitoids by herbivore-injured
plants. In: Gardé RT & Millar JG, eds. Advances
in Insect Chemical Ecology. Cambridge
University Press, pp. 21–75.
Väisänen RA, Lammi E & Koskimies P. 1998.
Muuttuva pesimälinnusto. Otava, Helsinki,
Finland.
Valkama E, Salminen J-P, Koricheva J & Pihlaja
K. 2003. Comparative analysis of leaf trichome
structure and composition of epicuticular
avonoids in Finnish birch species. Annals of
Botany 91: 643–655.
Van Bael SA, Brawn JD & Robinson SK. 2003.
Birds defend trees from herbivores in a
Neotropical forest canopy. Proceedings of the
National Academy of Sciences of the U.S.A.
100: 8304–8307.
Van Bael SA, Philpott SM, Greenberg R, Bichier
P, Barber NA, Mooney KA & Gruner DS.
2008. Birds as predators in tropical agroforestry
systems. Ecology 89: 928–934.
Vet LEM & Dicke M. 1992. Ecology of infochemical
use by natural enemies in a tritrophic context.
Annual Reviews of Entomology 37: 141–172.
Viitala J, Korpimäki E, Palokangas P & Koivula M.
1995. Attraction of kestrels to vole scent marks
visible in ultraviolet light. Nature 373: 425–427.
Whelan CJ, Wenny DG & Marquis RJ. 2008.
Ecosystem services provided by birds. Annals
of the New York Academy of Sciences 1134:
25–60.
Williams-Guillén K, Perfecto I & Vandermeer
J. 2008. Bats limit insects in a Neotropical
agroforestry system. Science 320: 70.
Wilsey BJ, Haukioja E, Koricheva J & Sulkinoja M.
1998. Leaf uctuating asymmetry increases with
hybridization and elevation in tree-line birches.
Ecology 79: 2092–2099.
Wilson JD, Morris AJ, Arroyo BE, Clark SC &
Bradbury RB. 1999. A review of the abundance
and diversity of invertebrate and plant foods of
granivorous birds in northern Europe in relation
to agricultural change. Agriculture, Ecosystems
and Environment 75: 13–30.
Zangerl AR, Hamilton JG, Miller TJ, Crofts AR,
Oxborough K, Berenbaum MR & de Lucia EH.
2002. Impact of folivory on photosynthesis is
greater than the sum of its holes. Proceedings of
the National Academy of Sciences of the U.S.A.
99: 1088–1091.