Spatial ecology of an oak-associated herbivore community : A ...

Spatial ecology of an oak-associated herbivore community

Ayco TACK

Department of Biosciences Faculty of Biological and Environmental Sciences University of Helsinki Finland Academic dissertation

To be presented for public examination with the permission of the Faculty of Biological and Environmental Sciences of the University of Helsinki in the Auditorium 1401 in Biocentre 2 (Viikinkaari 5) on May 28th 2010 at 12 o´clock noon.

Supervised by:

Dr. Tomas Roslin Department of Biosciences and Department of Agricultural Sciences University of Helsinki, Finland

Reviewed by:

Dr. Tero Klemola Department of Biology University of Turku, Finland Prof. Peter Hambäck Department of Botany Stockholm University, Sweden

Examined by:

Dr. Marc T. J. Johnson Department of Plant Biology North Carolina State University, USA

Supervised by: Custos:

Dr. Prof.Tomas UlrikaRoslin Candolin Department Department of of Biosciences Biosciences and Department of Agricultural Sciences University of Helsinki, University of Helsinki, Finland Finland

Reviewed by:

Dr. Tero Klemola Department of Biology of Turku, Finland Expert members of the thesisUniversity advisory committee: ISBN 978-952-10-6194-3 (paperback) Prof. Peter Hambäck Prof. Kouki ISBNJari 978-952-10-6195-0 (PDF) Department of Botany http://ethesis.helsinki.fi School of Forest Sciences Stockholm University, Sweden University of Eastern Finland, Finland Examined by: Dr. Marc T. J. Johnson Yliopistopaino Prof. Heikki Roininen Department of Plant Biology Helsinki 2010 Department of Biology North Carolina State University, USA University of Eastern Finland, Finland Custos: Prof. Ulrika Candolin Department of Biosciences Prof. Pekka Niemela University of Helsinki, Finland Department of Biology University of Turku, Finland

ISBN 978-952-10-6194-3 (paperback) ISBN 978-952-10-6195-0 (PDF) http://ethesis.helsinki.fi Yliopistopaino Helsinki 2010

Contents CONTRIBUTIONS

5

ABSTRACT

6

SUMMARY

7

1. Introduction ................................................................................................7 2. Oak-based metacommunities as a model system ....................................... 9

2.1 Oaks 2.2 Gallers, leaf miners and leaf folders 2.3 Natural enemies

9 9 9

3. Material and Methods ................................................................................ 9

3.1 Observational data 3.2 Experiments

10 11

4. Insights ...................................................................................................... 11

4.1 Direct competition among herbivores is of secondary importance (I) 4.2 Indirect competition mediated by the host plant plays a minor role (I) 4.3 Indirect interactions mediated by shared parasitoids can be positive (II) 4.4 Spatial location is more important than host plant genotype in structuring the insect community (III) 4.5 Gene flow among local insect populations affects local adaptation (IV)

11 13 14 15 16

5. Conclusion ................................................................................................. 16 6. Future perspectives ................................................................................... 17 7. Acknowledgements ...................................................................................18 8. References ................................................................................................. 19 I Competition as a structuring force in leaf miner communities II

23

Can we predict indirect interactions from quantitative food webs? – An experimental approach

35

III Spatial location dominates over host plant genotype in structuring an herbivore community

49

IV Overrun by the neighbors: landscape context affects strength and sign of local adaptation

69

The thesis is based on the following articles, which are referred to in the text by their Roman numerals: I

Tack, A. J. M., Ovaskainen, O., Harrison, P. J., and T. Roslin. 2009. Competition as a structuring force in leaf miner communities. Oikos 118: 809-818

II

Tack, A. J. M., Gripenberg, S., and T. Roslin. Can we predict indirect interactions from quantitative food webs? – An experimental approach. Manuscript.

III

Tack, A. J. M., Ovaskainen, O., Pulkkinen, P., and T. Roslin. 2010. Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology, in press.

IV

Tack, A. J. M. and T. Roslin. 2010. Overrun by the neighbors: landscape context affects strength and sign of local adaptation. Ecology, in press.

CONTRIBUTIONS Contribution table: I

II

III

IV

Original idea

TR, AT

AT

AT, TR

TR

Study design

AT, TR

AT

AT, TR, PP

TR, AT

AT

AT, SG

AT

AT

AT, OO, TR, PH

AT

AT, OO, TR

AT

AT, TR

AT, TR

AT, TR

AT, TR

Data collection Analyses Manuscript preparation

AT = Ayco Tack PP = Pertti Pulkkinen OO = Otso Ovaskainen SG = Sofia Gripenberg

© Ayco Tack (Summary) © Wiley Interscience (Chapter I) © The Authors (Chapter II) © Ecology / ESA journals (Chapters III & IV) Cover illustration © Jasper Teunissen Layout © Sami Ojanen

TR = Tomas Roslin P H = Phil Harrison

ABSTRACT Habitat fragmentation is currently affecting many species throughout the world. As a consequence, an increasing number of species are structured as metapopulations, i.e. as local populations connected by dispersal. While excellent studies of metapopulations have accumulated over the past 20 years, the focus has recently shifted from single species to studies of multiple species. This has created the concept of metacommunities, where local communities are connected by the dispersal of one or several of their member species. To understand this higher level of organisation, we need to address not only the properties of single species, but also establish the importance of interspecific interactions. However, studies of metacommunities are so far heavily biased towards laboratory-based systems, and empirical data from natural systems are urgently needed. My thesis focuses on a metacommunity of insect herbivores on the pedunculate oak Quercus robur – a tree species known for its high diversity of hostspecific insects. Taking advantage of the amenability of this system to both observational and experimental studies, I quantify and compare the importance of local and regional factors in structuring herbivore communities. Most importantly, I contrast the

6

impact of direct and indirect competition, host plant genotype and local adaptation (i.e. local factors) to that of regional processes (as reflected by the spatial context of the local community). As a key approach, I use general theory to generate testable hypotheses, controlled experiments to establish causal relations, and observational data to validate the role played by the pinpointed processes in nature. As the central outcome of my thesis, I am able to relegate local forces to a secondary role in structuring oak-based insect communities. While controlled experiments show that direct competition does occur among both conspecifics and heterospecifics, that indirect interactions can be mediated by both the host plant and the parasitoids, and that host plant genotype may affect local adaptation, the size of these effects is much smaller than that of spatial context. Hence, I conclude that dispersal between habitat patches plays a prime role in structuring the insect community, and that the distribution and abundance of the target species can only be understood in a spatial framework. By extension, I suggest that the majority of herbivore communities are dependent on the spatial structure of their landscape – and urge fellow ecologists working on other herbivore systems to either support or refute my generalization.

A metacommunity of herbivores

SUMMARY Ayco Tack Metapopulation Research Group, Department of Biosciences, PO Box 65, FI00014, University of Helsinki, Finland

1. Introduction

Throughout the world, natural habitats are becoming increasingly fragmented (Hanski 2005). As a result, more and more species are split into metapopulations (Fig. 1A; Hanski 1999, Hanski and Gaggiotti 2004). During the last few decades, research has revealed how spatially structured dispersal within such metapopulations may critically affect what species occur where and at what abundances (Thomas and Kunin 1999). More recently, ecologists have extended the focus from metapopulations to metacommunities, i.e. to metapopulations of multiple, potentially interacting species (Fig. 1B; Leibold et al. 2004, Holyoak et al. 2005). In such metacommunities, the abundance and distribution of species is explained jointly by the interplay between direct and indirect interactions within a local community, and by the dispersal of its component species between communities (Amarasekare 2008). Yet, the extent to which the structure of local communities is mainly affected by random forces (Bell 2001, Hubbell 2001), by interactions among species (Holt 1977, Denno et al. 1995, Kaplan and Denno 2007), by niche differentiation (Urban 2004, Freestone and Inouye 2006) or by differences in dispersal abilities (Leibold and Miller 2004) remains the topic of an ongoing debate (Cottenie 2005, Driscoll and Lindenmayer 2009, Pandit et al. 2009, Driscoll et al. 2010). In the context of this debate, theory roams wild but empirical data are scarce. Due to the complexity of natural communities, many studies have been conducted on laboratory systems ranging from two species to a whole suite of species (Huffaker 1958, Kendi et al. 2009). But laboratory studies cannot necessarily be extrapolated to the natural world, and recently researchers have gone back to the field to study metacommunities in a range of natural study systems, like invertebrates in rock pools (Kolasa and Romanuk 2005, Vanschoenwinkel et al. 2007), zooplankton in fresh water (Cottenie and De Meester 2005), invertebrates in moss patches (Gonzalez 2005) and birds in forest patches (Driscoll and Lindenmayer 2009). Strikingly, very few studies have been conducted on plant-feeding insects (but see van Nouhuys and

Hanski 2005, Cronin 2007). Nonetheless, a focus on this group would be justified for several reasons. As plants, plant-feeding insects and parasitoids make up approximately half of the world’s eukaryotic species (Strong et al. 1984, Godfray 1994), they have an enormous impact on ecological systems. Here, an understanding of the natural dynamics of plants, herbivores and their parasitoids may then also pay off in economic terms, e.g. by yielding an improved understanding of pest control in agroecosystems (Losey and Vaughan 2006). Moreover, many insect taxa are currently in a state of decline, and thus conservation efforts require an increasing knowledge of insect population dynamics (Samways 2005, Stewart et al. 2007). Finally, due to their short generation times and amenability to experimental manipulation, insects can serve as model systems for other species groups (Ehrlich and Hanski 2004). This thesis uses herbivorous insects to offer a new grip on factors structuring the abundance and distribution of species, and how these result in patterns in emergent community descriptors like species richness. Drawing on a combination of observations and experiments, I quantify both local and regional influences on insect community structure, and compare their relative contribution. Of local factors, I explore direct interactions among herbivores, induced defences by the host plant, impacts of hostplant genotype, and indirect interactions mediated by the host plant and parasitoids (see Fig. 2). Of regional factors, I analyze the effect of spatial context on the distribution of species. I achieve this through a determined research programme, with each chapter of my thesis addressing one key factor that may structure an herbivore metacommunity, and, where possible, placing this factor in an explicitly spatial context. When combined, my work covers the following series of questions: • What is the importance of direct interactions among herbivores? (I) • What is the importance of indirect interactions among herbivores, mediated by the host plant? (I) 7

Summary

Box A. Populations and communities in space Populations and communities

Individuals of a single species often live together in a distinct area, which is referred to as the habitat. Such a group of conspecific individuals, called a population, has for decades, if not for centuries, been the prime research focus for ecologists interested in ‘population dynamics’. However, in many cases it has proven impossible to understand the dynamics of a single species without considering other species, for example its predator or competitor. Hence, classical models of population dynamics were developed in the early decades of the twentieth century by e.g. Alfred Lotka and Vito Volterra to show how prey species, and prey and predator, interact (Lotka 1925, Volterra 1926, Lotka 1932). Later, ecologists incorporated multiple interacting species in their studies, establishing the field of community ecology (e.g. Elton 1927). Metapopulations and metacommunities

A metapopulation consists of a group of spatially separated populations of the same species, which interact by dispersal, and can hence be seen as a ‘population of populations’ (Fig. 1A; Levins 1970, Hanski and Simberloff 1997). This spatial view adds reality to previous models focusing on single locations, by explicitly incorporating the fact that local populations may sometimes go extinct, and empty habitats be colonized. Many species will naturally occur as metapopulations - like beetles that live in tree hollows (Ranius 2000, 2001), or plants adapted to light conditions in forest gaps (Valverde and Silvertown 1997). Other species have for a long time been continuously distributed in space, but their current distribution has now become scattered with the disappearance and fragmentation of their habitat, and the species now occur as metapopulations (Levins 1970, Hanski 1999). Where the metapopulation framework deals with single species, the metacommunity framework focuses on multiple, potentially interacting species (Fig. 1B). Here, the distribution and abundance of species can be explained by both local interactions and by regional processes. Compared to studies of metapopulations, in studies of metacommunities the focus often moves to emergent properties like species richness and to community composition, where the latter refers to a shift in relative abundances among species.

A)

Metapopulation ´local populations linked by dispersal`

B)

Metacommunity ´local communities linked by dispersal`

Fig. 1. Where studies of metapopulations (left) focus on single species in fragmented habitats, studies of metacommunities (right) focus on multiple species. In both cases, the habitat patch (circle) can be occupied or unoccupied by a local population (as depicted by a moth of a given species).

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• Do indirect interactions mediated by shared parasitoids link the dynamics of herbivores? (II) • Does host plant genotype play a major role in structuring the insect community? (III) • Do local insect populations adapt to individual host plants? (IV) 2. Oak-based metacommunities as a model system

My thesis is based on a specific model system: the oak Quercus robur and its herbivores. Oak trees are relatively long-lived, large entities, and in Finland oak trees are often patchily distributed. As a result, they form long-lasting, spatially structured habitats. Many of the herbivores feeding on oak in my study area (Finland) are specialists on Quercus robur. Thus, for these specialist insects, the landscape will form a mosaic, where each oak tree crown offers suitable habitat, and is surrounded by a matrix of unsuitable

C

E

C

A

B

D

B

Fig. 2. Interactions within a local herbivore community. Interactions may be direct or indirect, and take place within or between trophic levels. (A) Direct competition among herbivores. (B) Direct interactions among the host plant and the herbivore, including the effect of host plant genotype and of induced plant responses on the herbivores. (C) Direct interactions among the herbivore and parasitoid. (D) Indirect interaction among herbivores, mediated by induced responses in a shared host plant. (E) Indirect interactions among herbivores, mediated by a shared parasitoid.

habitat ( Janzen 1968). Hence, the oak–herbivore system forms an ideal study target for ecologists interested in plant-insect interactions in a spatial context. 2.1 Oaks

After the last ice age, Finland has been re-colonized by a single oak species, the pedunculate oak Quercus robur (Ferris et al. 1998). Most likely, other oak species are not able to withstand the cold Finnish winter with its short growing season, and even the pedunculate oak is limited in its distribution to the south-western part of Finland (Fig. 4A). 2.2 Gallers, leaf miners and leaf folders

Most insect herbivores on oak are hard to find – both larvae and adults can be difficult to spot due to their tiny body size and concealed habits. Further, as most species are only observed during a small part of the year, a community ecologist would have to search through the oaks multiple times during the season to record the abundance of several species, significantly increasing the amount of work. Luckily, there are exceptions to this rule: the larval stages of the leaf miners, gallers and leaf folders are often very conspicuous, and remain visible during a large part of the season. As a result, one can greatly reduce the number of times one has to search for the different insect species. Another advantage is that for some species, the fate of the individual larva can be inferred from the larval structure, even when the larva has already died or left the leaf mine or gall (see Box B for more information on the natural history of gallers, leaf miners and leaf folders). 2.3 Natural enemies

A wide variety of natural enemies are known to attack leaf miners and gallers, including birds (Itämies and Ojanen 1975, Owen 1975, Burstein and Wool 1992), ants (Sato and Higashi 1987) and vertebrates (Yamazaki and Sugiura 2008). However, the single most dominant natural enemies are parasitoids (Hawkins et al. 1997; see Box B for details on the life-history of parasitoids). 3. Material and Methods

In this thesis, I combine experimental and observational data. Importantly, this allows me to establish the mechanisms behind the patterns, and quantify the importance of different factors in structuring metacommunity dynamics. 9

Summary

Box B. Herbivore guilds and their natural enemies Leaf miners

Leaf mining is an intriguing adaptation, which has evolved several times during the last 300 million years (Labandeira 1998). It is currently found in the orders Lepidoptera (butterflies and moths), Hymenoptera (wasps), Coleoptera (beetles) and Diptera (flies) (Connor and Taverner 1997). In the typical life cycle of a leaf miner, the adult insect oviposits an egg on (or in) a leaf. The larva will then hatch from the egg, and start eating the tissue between the upper and lower leaf epidermis. Many species specialize in different layers of the leaf, like the photosynthetic cells in the upper layer or the cells used for transport of nutrients and photosynthates in the lower layer. In addition, different species make mines of completely different shapes, ranging from blotch-like to linear structures (Fig 3AB). These different mine patterns – besides being examples of a high degree of specialization - make it relatively easy to identify the leaf miner species (or genus). Gallers

Galling insects are highly diverse on the oak trees. Galling insects evolved 300 MY ago, around the same time as leaf miners (Labandeira 1998), and are intricate examples of how insects may manipulate host plant development. The most striking examples are those where the host larva is concealed by plant tissue (‘the gall’), and feeds upon a nutritious tissue layer lining the inner surface of the gall. Oak trees are especially famous for the large number of cynipid galls (Hymenoptera) that can be found on them (Askew 1961), and which are well-known for their fascinating morphologies (Fig. 3CD). Leaf folder

The larvae of leaf folders fold the leaf to create a concealed habitat for feeding and living in (Fig 3E). Only a single leaf folder species, Ancylis mitterbacheriana, was observed on oak in our study area. Powdery mildew

In addition to insect herbivores, one can often spot white, powder-like blotches on the oak leaf. These are colonies of the powdery mildew Erysiphe alphitoides (syn. Microsphaera alphitoides) (Fig. 3F). Parasitoids

The insect herbivores are attacked by a range of parasitoid species with a fascinating – but arguably abhorrent - lifestyle. The female adult parasitoid (often a wasp or tachinid fly) uses her ovipositor to lay an egg inside (or on top) of the egg, larva or pupa of the insect herbivore (Godfray 1994). The parasitoid larva then hatches from the egg and starts consuming the living body of its host. In contrast to parasites, a parasitoid will always kill the host larva during its own development. This life style made Darwin write “I cannot persuade myself that a beneficent and omnipotent God would have designedly created the Ichneumonidae (=group of parasitoid wasps).” Parasitoids fulfil an important ecological and economic role by causing a large fraction of the mortality in herbivore populations - especially in leaf miners and gallers (Hawkins et al. 1997) - and are often used in the biological control of herbivore pests (Van Driesche et al. 2008).

3.1 Observational data

A fundamental understanding of a metacommunity requires detailed knowledge of the distribution and abundance of its component species throughout the landscape. When such data is available for multiple years, insight is gained into the persistence of local communities, the frequency of local extinctions and colonizations, and the level of synchronization among local populations. 10

For this thesis, much of the observational data was collected on the island Wattkast (Fig. 4). As searching the approximately 100 million oak leaves on the island was (far) beyond our reach, we resorted to sampling a subset of trees. At the start of my PhD, I continued two long-term surveys initiated by Sofia Gripenberg and Tomas Roslin in 2003 (and hopefully continued long in the future). In the first survey, we search through the leaves of 89 trees distributed across the island Wattkast (Fig. 4B),


Box B continued

Fig. 3. Examples of herbivore species on oak. A) blotch-mine of Tischeria ekebladella, B) linear leaf mine of Stigmella, C) spherical gall of the sexual generation of Neuroterus quercusbaccarum, D) doughnut-shaped gall of the asexual generation of Neuroterus numismalis, E) leaf folded by Ancylis mitterbacheriana, and F) colonies (white spots) of the powdery mildew Erysiphe alphitoides. Photos by Ayco Tack, Sofia Gripenberg and Riikka Kaartinen.

and record the species richness and abundance of each herbivore species (I, III). These data illustrate both spatial patterns in species richness (Fig. 5A) and, when compared among years, colonizationextinction dynamics (Fig. 5B). We further sample a set of twenty trees growing in a relatively small area (ca. 5 hectares; Chapter II). On each of these trees, we annually look for herbivores on the same five branches. This hierarchical sampling design gives additional insight into the level of variation in herbivore densities both within and among trees, and whether variation observable at one point in time persists through time. Interestingly, it seems that some insect species have consistently higher densities on the same trees during multiple years, while others show more or less random abundance patterns across trees and years (Fig. 6). 3.2 Experiments

While describing spatial patterns in herbivore dynamics is fascinating, only experimental work can establish the mechanisms behind such patterns. For this, a series of experiments was conducted, ranging from the manipulation of insect densities in the laboratory to the use of grafted oak trees. More specifically, I explored direct and indirect host-mediated competition by manipulating host

densities on trees in a laboratory setting (Fig. 7A); pinpointed parasitoid-mediated indirect interactions among herbivores by manipulating host densities in the field (Fig. 7BC); used common gardens at two spatial scales to detect the relative importance of host plant genotype and spatial location (Fig. 7D); and used grafted trees in reciprocal common gardens to detect local adaptation of insects to individual host trees (Fig. 7E). Together, these experiments provide a versatile view of factors affecting community structure, and offer stringent tests of hypotheses generated by field observations. 4. Insights 4.1 Direct competition among herbivores is of secondary importance (I)

In the fifties and sixties, resource competition was shown to be a key process in structuring animal communities (MacArthur 1958, Connell 1961). However, Hairston and colleagues (1960) argued that since the world is demonstrably green, some other factor is keeping herbivore densities far below levels required to fully exploit the plant resources. Consequently, Hairston and colleagues denounced resource competition as a structuring force in herbivore communities. Since then the popularity 11

Summary

A)

Southwest Finland Läyliäinen

Wattkast 50 km

B)

Wattkast

500 m

Fig. 4. Distribution of oak trees. Panel A shows the natural distribution of oak in Finland. The lower-left arrow marks the location of the island Wattkast, which is shown in more detail in panel B. The upper right arrow shows the location of the tree breeding station in Läyliäinen (Metla), where the experiment on indirect, plant-mediated competition was conducted (I; Fig. 7A). To analyze the importance of host plant genotype (III), we collected host plant genotypes form six locations (circles) and planted them in two common gardens (stars; Fig. 7D). Panel B shows the island Wattkast, where each black dot represents one oak tree (n=1868). Grey dots represent a subset of small trees (1-3 m) which we annually search for the presence/absence of herbivores (since 2003; see Fig. 5 for some of the emerging patterns). The white triangles show 20 medium-sized trees, on which we each year search through the same five branches (see Fig. 6 for herbivore dynamics on these trees). 12


A)

Species richness 2008

B)

Number of years occupied by T. ekebladella

# Years 0 1 2 3

4 5 6

Fig. 5. Spatial patterns in herbivore species richness and population turnover. Panel A shows the species richness on each of 88 trees in 2008, where the colour of the circles ranges from white (zero species) to red (16 species). The spatial pattern suggests that species richness is higher in dense oak stands as compared to isolated oak individuals. The small black dots each represent one of 1868 oak trees on the island. Panel B shows the number of years that each of these trees was occupied by the leaf mining moth T. ekebladella during the period 2003-2008. The fact that a large fraction of trees was occupied for a few years only indicates the importance of colonization-extinction dynamics. of resource competition has been fluctuating among ecologists. In 1966, it was revived when Murdoch (1966, Janzen 1977) stated that while the earth may appear green and tasty in our eyes, the herbivores will see it as “colored lectin, tannin, cyanide, caffeine, aflatoxin, and canavanine”, and experience plants as “prickly and tasting bad”. In a world like that, one might posit that herbivores aggregate onto the few high-quality resources, and compete fiercely for those. In Chapter I, I assess the occurrence of direct competition among herbivores sharing the same leaf. Drawing on patterns of co-occurrence in nature, I show that conspecific and heterospecific leaf miners (i.e. individuals of the same or different species) often aggregate on the same trees (I). Within trees, conspecific individuals show further aggregation on the same branches, and on the same leaves within branches. However, I also show direct competition, defined as the mortality due to sharing the leaf with conspecifics, to be relatively weak – and as a result, intraspecific competition will only be important when densities are unnaturally high. While some competition among heterospecifics may take place, it will be even rarer than intraspecific competition, as heterospecifics co-occur less often on the same leaf than do conspecifics. Overall, my results then support the generalization that direct competition is rarely important in natural herbivore communities, as densities are far below carrying capacity. Only at extreme and rare densities may competition then

play a role. At the same time, I show that in the absence of parasitoids leaf miner survival is very high – and far higher than observed in the field. Hence, I conclude that leaf miners are not like “the ancient Mariner surrounded by undrinkable water” (Morris et al. 2005), but rather live within a juicy and nutritious leaf. Hence, as hypothesized by Hairston and colleagues, parasitoids are more likely to play a key role in suppressing leaf miner densities. 4.2 Indirect competition mediated by the host plant plays a minor role (I)

In the eighties, ecologists realized that competition can also be indirect, with one herbivore inducing a response by the host plant, which in turn affects the survival or growth of another herbivore species (reviewed in Karban and Baldwin 1997). The induced response often consists of an increase in secondary chemicals - but it can, among other things, also involve a change in the physical structure of the leaves or the concentration of nutrients (Karban and Baldwin 1997). In the mid-nineties, Denno, Ott and McClure declared the “resurrection of competition”, at least partly based on a rising number of studies showing indirect competition (Denno et al, 1995). Over the years, this view has gained added support, as shown by a recent meta-analysis by Kaplan & Denno (2007). This summary of the status quo shows convincingly that many interactions among herbivores are indirect and asymmetric. Much 13

Summary

0.30 0.15

0.20

0.25

Tree 901 Tree 902 Tree 903 Tree 904 Tree 905 Tree 906 Tree 907 Tree 908 Tree 909 Tree 910 Tree 911 Tree912 Tree 913 Tree 916 Tree 920 Tree 1096 Tree 1163 Tree 1341 Tree 1371 Tree 1467

0.10

Density T. ekebladella / leaf

T. ekebladella

0.00

0.2

0.4

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Tree 901 Tree 902 Tree 903 Tree 904 Tree 905 Tree 906 Tree 907 Tree 908 Tree 909 Tree 910 Tree 911 Tree912 Tree 913 Tree 916 Tree 920 Tree 1096 Tree 1163 Tree 1341 Tree 1371 Tree 1467

0.0

Density Phyllopnorycter / leaf

B)

Phyllonorycter

0.05

A)

2003

2004

2005

2006

2007

2008

Year

2003

2004

2005

2006

2007

2008

Year

Fig. 6. Variation in herbivore abundance across trees (n=20) and years (n=6). Each line connects annual tree-specific densities of A) Phyllonorycter and B) T. ekebladella during the period 2003-2008. Note that Phyllonorycter shows higher abundances on given trees across years, whereas the abundances of T. ekebladella show no consistency across either years or trees. See Fig. 4B for the location of the 20 trees.

competition thus takes place among herbivores that are spatially and temporally isolated, where the latter refers to early-season herbivores affecting the survival of herbivores occurring later in the season on the same plant. In my work, I examined plant-mediated competition among leaf miner individuals by conducting a controlled experiment (Fig. 7A). More specifically, I assessed whether leaf miners had a higher mortality when conspecific or heterospecific individuals were present on the same tree, but on different leaves (hence, excluding direct interactions). In this experiment, I detected signs of negative indirect interactions among both spatially segregated conspecific and heterospecific herbivores. However, instead of simply increasing the list of studies that have shown indirect interactions mediated by the host plant, I refined this observation by quantifying the importance of plant-mediated indirect interactions using data on field densities. As a result, I was able to conclude that the effect size of indirect competition was very small, even at densities higher than those encountered in the field. Hence, my work shows that induced responses are unlikely to be a key structuring force in the leaf miner community on oak. Based on the insight gained by combining effect sizes quantified in the lab with field observations on insect abundances, I urge other researchers to take their lab results back into the field, and quantify the impact of induced responses in a natural setting.

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4.3 Indirect interactions mediated by shared parasitoids can be positive (II)

Since the early twentieth century, researchers have shown both empirically and theoretically that density-dependent parasitism may regulate herbivore populations (Howard and Fiske 1911, Nicholson 1933, Hassell 1978, 2000). In contrast, the importance of indirect interactions mediated by shared predators was realized only decades later (Williamson 1957), and it took till the late 1970’s before the idea of apparent competition permeated into the ecological literature – as stimulated by the seminal paper by Holt (1977). In my work, I took a novel approach to apparent competition by manipulating leaf miner densities in a large-scale field experiment. To investigate the role of parasitoids in keeping herbivore densities low, and to assess the impact of parasitoids shared among herbivores, I first constructed a quantitative food web – that is, a description of who eats who, and in what numbers (Memmott and Godfray 1993). Based on this web, I made explicit predictions on the strength of density-dependent parasitism and of indirect interactions among herbivores that share parasitoids. I then tested these predictions in a largescale field experiment, and compared the results with herbivore survival and population dynamics in the observational data. Based on the joint evidence, I concluded that delayed density-dependent parasitism may affect the densities of herbivores, where the parasitism rate in year t+1 is positively correlated with the density of conspecifics in year t.


In addition, I detected indirect interactions among herbivores sharing parasitoids – however, contrary to what has often been assumed, the interactions were mainly positive. Hence, this study shows that indirect interactions among herbivores with overlapping parasitoid communities may range from apparent competition to apparent mutualism. I then caution that hypotheses derived from quantitative food webs – e.g. predictions about the strength and sign of indirect interactions among herbivores – should be rigorously tested in the field. 4.4 Spatial location is more important than host plant genotype in structuring the insect community (III)

In the field of agriculture and forestry, it is wellknown that some crop varieties suffer less damage from herbivores than others. However, only recently have researchers suggested a potential role for

intraspecific genetic variation in structuring natural communities (Price 1983, Antonovics 1992, Fritz 1992). Empirical research in this field took off for real after a stimulating paper by Whitham and colleagues in a special issue of Ecology (Whitham et al. 2003). Already after a few years, common garden trials conducted in multiple study systems had convincingly demonstrated that host-plant genotype can affect the associated insect community (Whitham et al. 2006). However, as pointed out by Johnson and Stinchcombe (2007), the next step still remained: go out into the field and test the importance of intraspecific genotypic variation as compared to other ecological factors. In my thesis work, I am one of the first to meet this challenge. In Chapter III, I compare the relative importance of host-plant genotype to that of spatial location at two different spatial scales: the island Wattkast (ca. 5 km2) and the range of oak in Finland (ca. 10,000 km2). I show that the variation

Fig. 7. Photos of the key experiments. Panel A shows the experiment designed to detect host-mediated competition as conducted at the tree breeding station in Läyliäinen (I). To exclude parasitoids, the experiment was conducted in a large cage covered with fabric. The small bags around tree branches are used to introduce adult moths to specific branches on the tree. Panel B shows a tree on which I increased herbivore densities, in order to detect parasitoid-mediated indirect interactions (II). The close-up in panel C reveals that each colored tag in panel B marks a branch with an elevated leaf mine density. Panel D shows the common garden in Parainen, part of the experiment aimed at estimating the relative importance of host plant genotype and spatial location (III). Panel E shows the transport of trees used in a reciprocal common garden experiment to detect local adaptation (IV). Photos by Ayco Tack and Tomas Roslin. 15

Summary

in herbivore communities among common gardens is much larger than among host-plant genotypes – thereby providing the first evidence that hostplant genotype may be of secondary importance in structuring the insect community in nature. In addition, I show that host plant traits are mainly affected by host plant genotype, and differ little among locations – a pattern precluding a strong causal link between host plant traits and insect distribution. A more likely explanation for variation in insect community structure among locations is the spatial context, where species richness increases with increasing spatial connectivity of the host tree. Hence, the dispersal ability of the herbivores is likely to play an important role, where species are more likely to colonize well-connected trees and may be absent from isolated trees. 4.5 Gene flow among local insect populations affects local adaptation (IV)

The idea that insect populations may adapt to individual host trees was first proposed by Edmunds (1973), who studied a non-dispersive scale insect. In later studies, the hypothesis has been referred to as adaptive deme formation (Edmunds and Alstad 1978, Van Zandt and Mopper 1998). Interestingly, when van Zandt and Mopper (1998) reviewed the literature accumulated in this field by the late nineties, as much as half of the studies actually refuted the adaptive deme formation hypothesis. Due to these mixed results, many reviews have tried (and failed) to pinpoint what makes local adaptation more likely in some study systems than in others, as based on traits of either the host plant or the insect (e.g. Boecklen and Mopper 1998, Van Zandt and Mopper 1998, Lajeunesse and Forbes 2002, Greischar and Koskella 2007). In chapter IV, I propose that the adaptive deme formation hypothesis should be placed in a spatial framework. More specifically, I predict that local adaptation is more likely in insect populations that receive few immigrants, and that lack of adaptation – or even maladaptation – may occur when a large fraction of immigrants enters the local population. To estimate the fraction of immigrants on each tree, I use predictions from a spatially explicit, empirically-parameterized metapopulation model of the leaf miner Tischeria ekebladella, as developed by Gripenberg et al (2008). Using a reciprocal common garden design, I am then able to show a relationship between the strength of local adaptation and the fraction of immigrants into the population. Hence, local adaptation may depend on the dispersal ability of the herbivore as compared to the spatial 16

distribution of its host plant – and variation in the strength of local adaptation may take place at a relatively small spatial scale (among individual trees within a landscape). 5. Conclusion

My thesis reveals a multitude of interactions with a potential impact on local community structure. Overall, it suggests that in my study system, direct interactions among herbivores are relatively unimportant at insect densities typically encountered in the field (I). Moreover, bottom-up processes like induced responses by the host plant (I) and effects of host plant genotype (III) only weakly affect the mortality and distribution of the herbivores. In contrast, parasitoids – a top-down effect – cause a major fraction of the mortality, either through hostfeeding or through parasitism (I, II). When present, indirect interactions mediated by the host plant are negative but weak (I), whereas indirect interactions mediated by shared parasitoids are absent or positive (II). Both in terms of evolutionary responses (IV) and local community structure (I-III), the imprint of spatial context seems to far override that of local forces. This consistent imprint of spatial location leads me to conclude that a metacommunity view will significantly improve our understanding of local community structure in the focal system. As little comparative data exists on plant-herbivore metacommunities, the current study may offer a new baseline for studies to come. While ecologists never tire of pointing out exceptions to generalizations, I would expect that the patterns found in this thesis may be successfully extrapolated to a large set of herbivorous insects inhabiting fragmented, terrestrial habitats. Overall, I predict that direct and indirect interactions are relatively unimportant in understanding the distribution of herbivores, whereas spatial processes will play a key role. I hope that this straightforward prediction will be taken up as a challenge by fellow ecologists. While my impression is then that many herbivore communities are structured by similar processes as described for my study system, I still expect large differences in the strength of forces structuring herbivore communities and other terrestrial and aquatic communities. For example, in marine communities, direct competition seems to play a much larger role in structuring the local community (Connell 1983). However, recent work suggests the importance of spatial processes to be paramount even in aquatic study systems ( Jackson et al. 2001, Cottenie and De Meester 2005). Unfortunately, many difficulties exist in comparing the factors


structuring metacommunities, and attempts so far have been impaired by a lack of data on speciesspecific dispersal abilities (Cadotte and Fukami 2005, Jacobson and Peres-Neto 2010). In addition, spatial scale may affect metacommunity patterns (II, III, IV), and has to be taken into account when comparing the factors structuring different study systems. The appropriate choice of spatial scale will then depend on both the dispersal ability of the species and the structure of the landscape (Thomas and Kunin 1999). 6. Future perspectives

While the chapters in this thesis shed light on some key ecological and evolutionary questions, many new questions and ideas for follow-up studies emerged during the writing-up phase. Part of them can be answered by analyzing data already available on the shelf, whereas others will require additional fieldwork. I am particularly keen on following the next four avenues: First, a combination of modelling and experimental work could reveal how species-specific dispersal abilities affect the distribution and abundance of species in the landscape. To estimate dispersal abilities, I have already conducted two experiments: in the first experiment, I placed potted oak trees at different distances from an oak stand and scored colonization as the presence of leaf mines and galls by the end of the season; in the second experiment I artificially removed focal herbivore species from ca. 80 trees, and scored herbivore colonization in the next year. These experimental data are currently used to fit a spatially-explicit, empiricallyparameterized metacommunity model to our longterm observational data (Tack, Zheng, Ovaskainen, Gripenberg and Roslin, in preparation). Hopefully, the results will elucidate how species-specific dispersal abilities, in combination with landscape configuration, shape local community structure. Second, in the context of the ‘world is green hypothesis’, I have so far partly failed to explain why the natural densities of herbivores on oak are below the carrying capacity set by the plant resources. While I have shown parasitism rate to be densitydependent, it does not appear strong enough to counter-balance herbivore population growth rates. Hence, other density-dependent factors must be evoked to explain the continuously low, but sometimes heavily fluctuating, densities of the herbivores (Fig. 6). Interestingly, a comparable study system of leaf miners on oak in Japan, involving the same leaf miner genera (but different species) shows very similar population dynamics (Nakamura et

al. 2008). Currently, I hypothesize that densitydependent mortality takes place in the leaf litter by parasitoids and generalist predators, which aggregate in areas of high host density. It would be relatively easy, and fascinating, to look for this often ignored life in the undergrowth. Third, the abundance and mortality of herbivore species may vary in different ways across hierarchical scales (e.g. branches and trees), with both ecological and evolutionary implications for herbivore communities (Denno and McClure 1983). As an ecological example, female moths of some species may show a strong oviposition preference for specific branches within a single tree, whereas in other species the female moths may show a preference for individual trees (and are largely insensitive to heterogeneity within trees). As a result, in the former species the larval abundance will vary mostly among branches within individual trees, whereas in the latter species the larval abundance will vary mainly among trees. From an evolutionary viewpoint, large differences in larval mortality among branches may lead to the absence of adaptation, or local adaptation to individual branches. In contrast, species that experience large differences in mortality among trees are more likely to adapt to individual host trees. That species within a single community indeed respond differently to variation between trees is suggested by Figure 6: while the abundance of T. ekebladella seems to vary randomly across trees and years, the density of Phyllonorycter is consistently higher on some trees than on others. The same notion is also supported by the pattern detected in chapter IV, where I found lower levels of local adaptation in T. ekebladella than in other species. Finally, the reader of this thesis may get the impression that leaf miners and gallers are the only herbivores living on oak leaves. However, in real life the leaf miners and gallers share the oak leaves with a wide variety (but low density) of free-feeding insects, and with a specialist powdery mildew (Erysiphe alphitoides; see Roslin et al 2007). While I did not focus on these additional taxa in this thesis (except III), I did not ignore them completely. During the years 2006-2008, I conducted many (relatively) small experiments on the interactions among powdery mildew, free-feeding insects, and the leaf miner Tischeria ekebladella. In this context, my preliminary analyses show a complex network of interactions. For example, the larvae of T. ekebladella grow faster on mildew-infected leaves, but at the same time suffer from increased parasitism. In striking contrast with the increased growth rate of T. ekebladella, free-feeding insects grow slower on mildew-infected leaves. Revealing the exact 17

Summary

interaction network among these guilds, and the consequences for colonization-extinction dynamics of the insect herbivores, will be part of my postdoctoral studies. 7. Acknowledgements

Following scientific tradition, I am writing the acknowledgments in the very last moment – a strategic mistake given the knowledge that this section will, without any doubt, be the heaviest-read part of the thesis. Many of you may even have gone straight to this piece of text, ignoring the summary itself. Then, by keeping it short, I will give the reader some extra time to actually browse through (or even read!) some of the chapters. *This thesis would not have been possible without the help of numerous collaborators, colleagues and friends* \Tomas Roslin: a superb, superior supervisor; strikingly, even after four years I do not grasp how you always find the time to provide such lightning-speed, highquality, stimulating, encouraging, optimistic, and realistic comments on my work - I must be blessed with such a guidance \Oak-group: many people are blinded by fluffy animals and shiny butterflies. It then is a great delight to have colleagues who perceive the true beauty of nature: those tiny critters that rule the earth \Sofia: the one who bravely (or naively?) labelled the very first oak tree on Wattkast – it is great to see how many papers have come about, and will still be published, as a result. Thanks for guiding me during my first steps in the oak-world, and being a friend on the continuing journey through the wondrous world of plants and insects \Riikka: your enthusiasm of higher trophic levels like birds, parasitoids (and good beer?) is unrivalled – and highly infectious. Thanks for sharing the rustic life in Böhle, the PhD-journey and those cool conference trips \Böhle: this lovely village in the middle of Korpo, with its charming wooden house, Finland’s best wood-heated sauna, its friendly neighbours, and its water supply that runs out during the most critical and hectic end-of-the-season \Fieldworkers: over the years about fifteen excellent, cheerful and hardship-enduring fieldworkers joined for the autumn survey – and made it such a pleasant time; in particular Bess, Janne and Elina greatly helped me out with a zillion other jobs \Wattkast: this idyllic island full of tagged oaks, insects, mushrooms and friendly inhabitants: the Roslin-family with its chats, plums and drinking water; the ‘greenhouse-people’ with their fresh vegetables; Henry & Thomas for driving around hundreds of oaks and thousands of litres of water around the island in the name of science \Haapastensyrjä tree breeding station: the great leader Pertti and his fondness of oaks – and his willingness to support any experiment I ever

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proposed; Tommi, Raimo, Piritta and Hiski for all those lovely days in the field and greenhouse, driving the mönkijä, chilling out at rantasauna, your great care of our beloved oak trees (which should have been your lowest priority), and always borrowing fieldworkers when my experiments ran out of control; tens (?) of forestry students who volunteered (or were forced) to help with insect research: hope you enjoyed this glimpse into ecology! \Students: Liselotte, my great help during those uncertain early days of experimentation – you were a great companion with so many projects; Elena, while you must sometimes have felt lost in the deep quietness reigning the archipelago, I am sure you miss it! \opponent: I am deeply grateful that you accepted the invitation to act as an opponent - on such a short time notice - within a split-second \5310: here I was located in (probably) the best-hidden corner of the fifth floor; with Chris, his great stories and unique ability to show up and disappear without any regularity; with Kristjan and haphazard daily chats, admirable knowledge of Statistix, and ability to hit the right light switch – be assured your garden will flourish when you return back to Finland; Eva with her lovely daily life stories; I am only worried that when I leave, the office will suddenly turn clean and organized \ football table: there is no better way to relax than beat a few fellows in fusball \Ilkka: for being one of those bright lights in ecology – and thereby providing one of the best places one could imagine to do its PhD; \coffee breaks: where would science be without the joyful moments during early & late coffee? And will science improve with the new coffee machine? \Funding: Academy of Finland (grant to Tomas) and Societas Entomologica Helsingforsiensis\co-authors: Otso and his magic data-handling, Phil who so kindly wrote my R-code, and hey, I mentioned the others already above \MRG: this wonderful, fun and friendly group of dedicated scientists creates an amazing scientific and non-scientific atmosphere; idem for the department; \Luova for the courses, and Anni for recent help with bureaucracy and the mini-symposium \Veijo for his quick and cool handling of dissertationformalities and last-minute changes \MRG secretaries: this most-gifted, patient and oh-so-friendly buffer zone in between me and university bureaucracy – without you I’d probably still be busy finding the right form in alma; Sami for fine-tuning my computer, and the splendid layout of the current thesis \Jasper: for spending so many hours of his ‘non-working’-career on my cover design\pre-examiners: Tero and Peter, for so graciously scrutinizing my thesis, insightful comments and encouraging words; \external supervisors: Heikki, Jari & Pekka: I am very thankful that you voluntarily, and with dedication, followed the development of my thesis\friends: obvious \sports: playing ice-hockey in Brahe, throwing frisbees along the bay, and skiing to work are the best ways to keep the mind fresh and the body in condition. \Family: my parents for their unconditional and ever-lasting support (and bringing


the booze for the karonkka); Sanna, my shining light for so many years; I am deeply grateful for your ability to run our family affairs, where I may often bring more chaos than order (but one day I’ll make up for that!), your delicious food and heavenly cakes, and the secret behind those cute trees in my presentation; (do you already know what’s a leaf miner?); Helmi, for making me feel such a proud father, clearing my head from scientific thoughts with a single smile, and for playing together with all those cool kids toys; and my cats, one soft and affectionate, taking the important role of paper-weight (preventing any homestudy), while the other gives this lovely anarchist touch to the house.

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