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Plant-seed predator interactions –
ecological and evolutionary aspects
Hannah Östergård
Stockholm University
©Hannah Östergård, Stockholm 2008
Cover: Flowering Lathyrus vernus and mating pair of the predispersal seed predator Bruchus atomarius.
Photo: Hannah Östergård
ISBN (978-91-7155-643-1)
Printed in Sweden by Universitetsservice, US-AB, Stockholm 2008
Distributor: Department of Botany, Stockholm University
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Doctoral dissertation
Hannah Östergård
Department of Botany
Stockholm University
SE-106 91 Stockholm
Sweden
Plant-seed predator interactions – ecological and
evolutionary aspects
Abstract - Plant-animal interactions are affected by both abundance and distribution of interacting species and the community context in which they
occur. However, the relative importance of these factors is poorly known. I
examined the effects of predator host range, environmental factors, host
plant populations, plant traits and fruit abortion on the intensity of predispersal seed predation in 46 host populations of the perennial herb Lathyrus vernus. I recorded damage by beetle pre-dispersal seed predators, mainly
Apion opeticum and Bruchus atomarius with different host ranges on L. vernus as well as on two additional host plants. Local seed predator population
size was mainly influenced by plant population size, current seed production
and beetle population size in the previous year, but was not strongly affected
by connectivity. The monophagous seed predator was less abundant and had
lower densities than the oligophagous. Both predator species had a strong
ability to track fluctuations in seed production; intensity of predation increased with relative increases in seed production. Oligophagous predation
on L. vernus increased with the abundance of alternative hosts, but presence
of L. vernus did not affect predation on alternative hosts. Abundances and
trait preferences differed among three co-occurring seed predators, but were
also associated with the abundance of the other species. Overall, seed predation influenced selection on flower number. I found clear indications of seed
predator offence but no obvious plant defence. The pattern of fruit abortion
was associated with reduced plant fitness since the seed predator had an advanced ability to locate fruits with high probability of retention. Taken together, different factors influencing abundance of the seed predator species,
different preferences, and context dependent trait selection are likely to result in complex spatio-temporal variation in overall seed losses and trait
selection in the common host plant.
Keywords – apparent competition, community context, fruit abortion, defence, host range, monophagous, offence, oligophagous, plant-animal interactions, pre-dispersal seed predation, selection, spatio-temporal variation
List of papers
The thesis is comprised by a summary and four papers, which are referred to
by their Roman numerals:
I
Östergård, H., and J. Ehrlén. 2005. Among population variation
in specialist and generalist seed predation - the importance of
host plant distribution, alternative hosts and environmental variation. Oikos 111:39-46.
II
Östergård, H., P. A. Hambäck, and J. Ehrlén. Regional dynamics
and host plant utilization by two pre-dispersal seed predators.
Manuscript.
III
Östergård, H., and J. Ehrlén. Phenotypic selection pressures on
Lathyrus vernus by a monophagous, an oligophagous and an occasional seed predator. Manuscript.
IV
Östergård, H., P. A. Hambäck, and J. Ehrlén. 2007. Pre-dispersal
seed predation: The role of fruit abortion and selective oviposition. Ecology 88:2959-2965.
Previously printed and accepted papers are reprinted in this thesis by the
kind permission of the copyright holders.
Contents
Introduction .....................................................................................................7
Ecological aspects ........................................................................................................8
Evolutionary aspects .....................................................................................................9
Aim of the thesis............................................................................................11
Methods ........................................................................................................12
Study system ..............................................................................................................12
Data collection ............................................................................................................13
Data analysis ..............................................................................................................15
Results ..........................................................................................................18
Discussion .....................................................................................................20
Concluding remarks ....................................................................................................22
Acknowledgements .......................................................................................23
References ....................................................................................................24
Svensk sammanfattning................................................................................28
Tack...............................................................................................................32
Introduction
Plants are generally involved in multiple mutualistic and antagonistic interactions, which may occur simultaneously or be separated in time, and may
affect one or several plant organs or different stages of the lifecycle, i.e. reproductive organs, seeds or seedlings. Both mutualistic and antagonistic
interactions between plants and animals have important and sometimes reciprocal effects. Herbivory is an antagonistic interaction displaying a wide
variety of forms. Pre-dispersal seed predation deviates from other kinds of
herbivory in several important aspects, such as the discrete packaging of the
resource, time-limited access to the seeds and the higher variation in resource production as compared to other plant resources. Another aspect is
that the interaction between plant and pre-dispersal seed predator generally
takes place during or in close proximity to the flowering period. Thus, predispersal seed predators are often active during the same period and attracted
to the same features as pollinators, causing conflicting selection pressures in
the plant.
Different species utilizing the same resource may vary in host range. In
spite of the obvious advantages of utilizing multiple hosts, herbivorous insects are often specialized on one or a few host plants. The evolution of specialization in herbivorous insects is suggested to be a trade-off between adaptations to a particular host trait and the ability to utilize multiple hosts
(Jaenike 1990, Thompson 1994, Agrawal 2000). The commonness of specialization has been explained by the information-processing hypothesis,
stating that the limited neural capacity in an insect should gain in efficiency
on a narrow host range since they only need to respond to a few cues in
searching for host plant (Levins 1969, Janz and Nylin 1997, Bernays 1998,
Egan and Funk 2006). In addition, specialists that have overcome a plant
chemical defence may also improve the search accuracy by utilizing the
defensive chemicals as an attractant in host finding (Van Zandt and Agrawal
2004, Lankau 2007). A generalist, on the other hand, would suffer in effectiveness by having to screen multiple stimuli from their various hosts, but
also have a reduced need of increasing efficiency.
Pre-dispersal seed predators with different host ranges, from monophagous to polyphagous, and the intermediate oligophagous species, may
have differential effects on the plant due to differences in abundance or preference. To understand population dynamics and plant trait evolution it is
therefore necessary to identify the factors that determine the strength of these
7
interactions. This thesis examines the antagonistic interaction between a
perennial herb and its beetle pre-dispersal seed predators in a spatial, temporal and evolutionary context.
Ecological aspects
The spatial distribution of species is generally patchy and patchiness is found
over both small and large scales in the global distribution of a species. On
the landscape level, the incidence and abundance of herbivores have often
been studied within the theoretical framework of metapopulation theory.
Metapopulation theory predicts that animal populations will more often go
extinct in small host plant populations and will colonize more isolated host
patches less frequently (Levins 1969, Hanski 1998, 1999). Such effects of
spatial and temporal variation in resources will most likely have different
impacts on different herbivores because resource-tracking in time and space
will be the result of species specific behavioural and population processes
(Hambäck and Englund 2005).
From the plant perspective, variation in the abundance and species composition of seed predators will result in variable effects on local population
dynamics. Reductions in plant reproductive output and subsequent fitness
losses by pre-dispersal seed predation has been observed in several systems
(Louda and Potvin 1995, Traveset 1995, Ehrlén 1996). The impact of seed
predation on plant population dynamics may depend on whether recruitment
is seed- or microsite limited. When seed densities are low, seed predation
may reduce recruitment but as seed densities increase, recruitment will be
limited by microsites or density dependent regulation of seedling survival
and impacts of seed predation may therefore be lower (Crawley 1992).
However, persistent reductions of seeds may, via reduced accumulation of
seeds in the seed bank, have considerable effects on mean abundance even if
recruitment is microsite limited (Maron and Kauffman 2006). The long-term
intensity of seed predation can in some plant species be reduced by synchronized irregular variation of seed production, i.e. mast seeding (Kelly 1994,
Silvertown and Charlesworth 2001).
From the animal perspective, the spatio-temporal variation of resources
will affect the distribution and abundance of herbivores (Bach 1988a, b,
Turchin 1991). In some systems also higher trophic levels have effects on
herbivore density (Elzinga et al. 2005, von Zeipel et al. 2006). Search behaviour and the relevant scales in resource tracking may vary due to what cues
herbivores use and their efficiency in using those cues (Kunin 1999). Host
plant clustering will cause different responses depending on whether an animal uses visual or olfactory cues. The relative probability of an individual
host being targeted by visual cues may decrease with aggregation of hosts
because single individuals will be less conspicuous within a cluster. When
8
olfactory cues are used the effects of clustering may be the reversed because
increased aggregation increases detection distances (Cain 1985, Kunin
1999). Herbivores will also respond differently to host patch size and density
depending on whether they are active or passive dispersers and whether they
are poor or effective dispersers. Active dispersers may respond more to
patch edges whereas passive dispersers will be most affected by patch area.
Poor dispersers are more affected by distances among resource patches than
good dispersers. Interactions between plants and consumers are also likely to
be influenced by host range of the consumer since specialist species are
completely dependent on their one food source whereas more general feeders have the possibility to alter between hosts. This will have consequences
both for regional and local population dynamics since specialist feeders are
more prone to go extinct as their single resources decrease, as well as being
more severely affected by fragmentation of host populations than generalists
(Zabel and Tscharntke 1998, Östergård and Ehrlén 2005). Host range will
thus affect the spatio-temporal variation of coexistence of multiple interactors causing local variation in predation intensity.
Evolutionary aspects
The fitness and population dynamics of herbivores will largely depend on
the ability of insects to track the resource and select suitable oviposition sites
(Ehrlich and Raven 1964, Thompson and Pellmyr 1991). Search behaviour
will have consequences both for seed predator dynamics and for the smallscale choice of oviposition sites. The negative effects experienced by the
plant of an antagonistic interaction have resulted in the evolution of various
defensive strategies of plants. Plants may reduce attack rates in several ways,
i.e. by producing poisonous or deterring chemicals, avoidance traits, abscising damaged parts or by hiding in time or space (Augner et al. 1991, Augner
1994, Eriksson 1995, Wilson and Addicott 1998, Tiffin 2000). The evolution
of flower and fruit abscission patterns may depend on whether they are the
result of selection to decrease losses from predation or a result of that the
resources available for fruit development are partly unknown at the flowering and fruit initiation stages (Lloyd 1980). Not uncommonly, antagonist
insects outwit plant defences since their shorter generation time results in a
higher evolutionary potential (Toju and Sota 2006). Antagonists are likely to
exert selective pressures not only on plant defences but also on nondefensive plant traits as a result of their choices and preferences among different plant individuals (Brody 1992, Herrera et al. 2002, Leimu et al. 2002,
Cariveau et al. 2004). Many of the floral traits in plants that are attributed to
attracting pollinators (Thompson and Pellmyr 1989, Eckhart 1992, Herrera
1993, Brody and Mitchell 1997) will also attract antagonists. Thus, the optimal trait values are often the result of a trade-off between benefits by in9
creased pollination and costs by increased herbivory (Brody 1992, Brody
and Mitchell 1997, Ehrlén 1997, Strauss 1997, Vanhoenacker et al. 2006).
Coevolution is the reciprocal evolutionary change in interacting species
and spatial variation in these interactions forms the basis for geographic
mosaics of coevolution (Thompson 1994, Gomulkiewicz et al. 2000). In
natural systems interactions between plants and insects are rarely a simple
affair within a single pair of species, but will mostly occur within the context
of other interactions experienced by the plant as well as by the insect. An
interaction will depend on context because it is influenced, directly or indirectly, by both the number and intensity of other interactions (Johnson and
Stinchcombe 2007). Indirect selection on plant traits, caused by contextdependent intensity of interactions, is suggested to result in a diffuse rather
than pairwise coevolution (Janzen 1980, Thompson 1994, Strauss et al.
2005, Agrawal et al. 2006, Morris et al. 2007). However, the complexity of
interactions is more than diffuse evolutionary responses. On the contrary, it
offers an exciting challenge to detect and understand an interaction within its
relevant context. The abundance and composition of the interacting insect
community is often highly variable in time and space. The spatio-temporal
variation in the context of a plant-animal interaction will thus translate into a
mosaic variation of selection among different plant populations.
10
Aim of the thesis
The overall aim of this thesis was to investigate how variation in the intensity of plant-animal interactions is affected by the spatio-temporal variation
of resources and environmental conditions within the framework of host
range, community context and plant trait variation. I used a system with one
focal host plant the perennial understory herb, Lathyrus vernus, two alternative host plants, Lathyrus linifolius and Vicia sepium, and three pre-dispersal
seed predators, the monophagous Apion opeticum, the oligophagous Bruchus
atomarius and the more polyphagous Tychius quinqepunctatus only occasionally attacking L. vernus. The interactions were studied both within and
among plant populations. Specifically I asked the following questions: (1) Is
the intensity of pre-dispersal seed predation affected by spatio-temporal
variance in host plant population size, seed production, connectivity and
local environmental factors and does the relative importance of those factors
differ with host range (Paper I & II)? (2) Do seed predators, species by species and in combination, change trait selection gradients in their host plant,
and what are the underlying mechanisms of such changes (Paper III)? (3)
How is the relationship between seed predator offence and plant defence
related to the production of flowers, young fruits and the pattern of fruit
abortion in individual plants (Paper IV)?
11
Methods
Study system
The long-lived perennial understory herb Lathyrus vernus has a Eurasian
distribution (Hultén 1971). In the study area it mainly occurs in deciduous or
mixed forests (Fig. 1). Individuals are well defined and have no special features for vegetative spread. The subterranean rhizome produces one to several shoots annually and the average life-span of an individual reaching maturity is estimated to 44.1 years (Ehrlén and Lehtilä 2002). Flowering usually
takes place in early May, and each shoot carries 1-5 racemes with 1-9 purple-red flowers per raceme (Fig.2). Number of flowers is determined in the
previous
summer
when flower buds
differentiate. Flowering is sequential, starting with the proximal
(closest to the stem)
flowers on the basal
(closest to the ground)
raceme. All flower
buds are visible at the
onset of flowering.
The plant is selfcompatible but lacks
mechanisms for selfpollination. Pollination is mostly carried
Figure 1. Deciduous forest islands surrounded by
out by Bombus spp.
moved meadows representing the typical Lathyrus
Recruitment is seed
vernus habitats in the study area.
limited (Ehrlen 2003).
Lathyrus vernus seeds have an average mass of 12.0 ± 3.5 mg (Ehrlén and
van Groenendael 2001).
Apion opeticum (Coleoptera: Aphidae) is monophagous on L. vernus in the
study area. It has a restricted distribution in Sweden but occurs scattered
across Europe, East Palearctic and Near East (Alonso-Zarazaga 2004a). Females insert eggs in young fruits through the closure of a pod, and pods are
glued together to avoid dehiscence before development is completed. Larvae
12
develop inside the pod, discretely
consuming one or rarely two seeds.
Pods are glued to avoid dehiscence
before development is completed.
Adults exit the pod by cutting a hole
through the exocarp.
Bruchus atomarius (Coleoptera:
Bruchidae) utilizes a few species of
the closely related genera Vicia and
Lathyrus but shows a preference for
L. vernus in the study area, attacking a relatively large proportion of
seeds every year. It is common in
the study area and is distributed
widely across Europe (Audisio
2004). Eggs are laid on the exterior
of young pods and larvae enter
through the exocarp. Larvae develop inside a single seed and disperse with the seeds as pods dehisce
at maturity.
Figure 2. Flowering individual of the
Tychius quinqepunctatus (Colperennial understory herb Lathyrus
eoptera:
Curculionidae) attacks L.
vernus
vernus only in some years. Its host
range is not fully known but it is reported to attack species of Vicia and
Lathyrus (Bullock 1992) and has been reported as a plague on cultivated
Lens esculenta (Monreal et al. 1990). It has a wide distribution across
Europe, East Palearctic, Near East and North Africa (Alonso-Zarazaga
2004b). The oviposition procedure is not known. Larvae develop and move
around inside a pod, consuming one to several seeds, and adults are found in
mature pods.
Data collection
The study was performed in a 5 x 5 km area in the province of Uppland,
central eastern Sweden (Fig. 3). The area is dominated by coniferous forest
but a large fraction consists of a mixture of meadows, pastures, cultivated
fields and broad-leaved deciduous or mixed forests. This mosaic landscape is
partly protected and managed to preserve the pre-industrial agricultural landscape structure. Studies were performed during six consecutive years (2000–
2005) and within the study area, I localized 46 Lathyrus vernus patches and
recorded their size and degree of isolation.
13
Population studies
To study the effects of spatio-temporal variation of plant resources on the
intensity of seed predation (paper I and II) I recorded several characteristics
of the 46 plant
patches. A Lathyrus vernus patch
was defined as a
group of individuals separated from
conspecifics by at
least 20 m. I used a
geographical
information system to
map the spatial
location of each
patch. I calculated
the area of each
patch by making
polygons
within
field
monitored
GPS-positions on a
digital map. To
examine effects of
Figure 3. The location of 46 Lathyrus vernus populathe adjacent landtions in a 5 x 5 km area in the province of Uppland,
scape, I calculated
central eastern Sweden (black dots). Yellow areas reprethe proportion of
sent open areas, e.g. meadows, arable fields or pastures.
the patch perimeter
Green areas represent forested landscape. Blue-ruled
areas represent watercourse.
adjoining to open
areas. All spatial
variables were calculated in ArcView GIS 3.2. The intensity of predation
from the two beetles as well as variables describing host plant population
seed production and patch characteristics was recorded in all patches that
were not to heavily grazed by cattle. I measured environmental variables in
each patch, such as the height of the field layer, litter layer and canopy
cover. Each year the number of flowering L. vernus individuals was counted
in all patches at peak flowering and at fruit maturity I estimated the proportion of flowering individuals producing fruit. The abundance of the alternative host plants utilized by B. atomarius was estimated both within patches
and in the matrix landscape surrounding L. vernus patches. The number of
seeds per plant was estimated within each L. vernus patch by collecting pods
from up to 20 randomly chosen individuals with mature fruits. In these individuals I also recorded the number of flowers and fruits. The damage rate of
B. atomarius and A. opeticum was estimated from the collected fruits. The
14
number of seeds per patch was calculated as the mean number of seeds per
individual in fruiting individuals multiplied by the number of individuals
that produced fruits. Apion opeticum and B. atomarius population sizes were
calculated as the proportion of seeds damaged multiplied by the number of
seeds in the patch.
Selection studies
To study phenotypic selection pressures through seed predation (paper III), I
followed 107 L. vernus individuals from initiation of flowering to fruit maturation and recorded flowering phenology in terms of the first flowering date
(FFD). At maturity all fruits were collected, and the number of non-fruiting
flowers, in terms of pedicel scars, counted. Seeds and adult beetles of all
three seed predators remained in the collected fruits, making it easy to quantify the number of undamaged seeds and assign damaged seeds to each respective seed predator. I estimated gross seed production, the total number of
intact and damaged fully developed seeds as well as net seed production, the
number of fully developed seeds that escaped damage. I also calculated the
number of seeds that escaped damage from each of the three predators, by
subtracting number of seeds damaged by each predator from gross seed production. Gross seed production was considered an accurate estimate of plant
seed production and fitness in the absence of seed predators.
To study the relationship between seed predator offence and plant defence
(paper IV), I followed fruit initiation and early fruit abortion (before seedexpansion) on fifty randomly selected Lathyrus vernus individuals. Individual fruits were surveyed from the initiation of the first fruit until oviposition
activity ended, which occurred as flowering in the latest flowering individuals ended. The total number of flowers on an individual was recorded and
sorted in each individual raceme and each flower was followed individually
throughout the study by recording its position within the raceme. Fruit initiation and the subsequent state of fruits (retained or aborted) were recorded on
each flower position on four occasions. I used the date of the first observation of an initiated fruit at a flower position as a measure of fruit phenology.
On all visits each fruit (both newly-initiated and previously present) was
carefully surveyed for Bruchus atomarius eggs and the number of eggs present was recorded. At fruit maturation all fruits on each plant were collected
and the number of larval entrance holes in the endocarp, adult beetles and
damaged seeds were counted. I counted each egg that developed into an
adult beetle as a successful larva.
Data analysis
Connectivity between patches was estimated separately for each species and
year as Si = Σexp(αdij)Ntj (Hanski 1999), where α is a constant describing
15
how the number of migrants decline with increasing distance, dij is the distance between patch i and j, and Ntj is the population size of A. opeticum, B.
atomarius or L. vernus respectively in patch j, year t. I examined several
values of α and I then selected the best fit (α = 0.02), corresponding to an
average migration distance of 50 m (Hanski 1999).
To examine effects of spatial patterns and local environment on seed predation intensity (Paper I), I used generalized linear models that were built in
three steps. First I examined all candidate predictor variables for each response variable by univariate tests. Response variables were incidence of
predation by A. opeticum, proportion of individuals preyed, proportion of
seeds damaged and population size of A. opeticum and B. atomarius respectively, and total seed loss. Second, multiple models were constructed with
population size and isolation, number of flowering L. vernus and connectivity included in all models. Other predictor variables were included if P <
0.10 in the respective univariate tests. Third, I used AIC (Akaike information
criterion) to rank models. I calculated AIC as –2(log-likelihood of fitted
model) + 2(number of predictors in the fitted model) (Venables and Ripley
1999), and selected models with the lowest AIC that included population
size and connectivity. A log-linear model was used to test if A. opeticum and
B. atomarius utilized L. vernus individuals independently of each other in
nine patches where they co-occurred.
To examine how temporal variation in seed predation intensity was affected by resource- abundance and variation (paper II), I used logistic regressions to test how colonization and extinction events were related to seed
predator population size and connectivity. I used linear mixed-effects models
nested within patch to examine how changes in seed production between two
adjacent years affected the proportion of seeds preyed, and how previous
year population size, current seed production and patch openness affected
abundance of A. opeticum and B. atomarius in a given year. Models were
simplified by removing variables that did not significantly improve fit.
To examine phenotypic selection pressures by seed predation (paper III), I
first performed selection analysis, using the relative number of seeds as a
measure of individual fitness. I quantified phenotypic selection on number of
flowers and first flowering day using regression methods with standardized
trait values according to Lande and Arnold (1983). To estimate how predispersal seed predation changed selection on flower number and first flowering day, I compared the partial regression coefficients in absence and presence of the seed predators. Since residuals were not normally distributed I
assessed 95 % confidence intervals of selection differentials and selection
gradients by bootstrapping. Data were resampled 10000 times, and the confidence intervals were constructed using bias-corrected and accelerated
methods based on saved coefficients from each bootstrapping in package
“boot” in R. Preference by each of the seed predators was measured by the
proportion of seeds of a Lathyrus vernus individual that were attacked by a
16
focal seed predator. Preference patterns were examined with models containing number of flowers, first flowering day and seeds per flower. I used AIC
to rank models and selected the model having the lowest AIC.
To evaluate how the oviposition pattern affected B. atomarius fitness (Paper IV) in terms of egg survival, I first assessed the relationship between the
number of eggs per fruit and the number of developed beetles per fruit. I
then fitted the function y = a + bx + cx 2 , where x is number of eggs on
retained fruits; y is number of developed beetles and the quadratic term
models density dependent egg survival. To calculate the number of beetles
for a random oviposition scenario, I used the mean number of eggs per fruit
on all initiated fruits (retained + aborted) as the value of x in this fitted function. The effects on reproductive output of the oviposition pattern for the
plant was estimated as the difference between the actual number of intact
seeds produced and the number of seeds that would have been the result of
random oviposition. To investigate the effects of beetle oviposition pattern
on average beetle fitness I used a t-test. Individual plant traits, i.e. number of
flowers, fruit phenology, and fruit abortion patterns among and within individuals, versus egg laying patterns were tested with linear regressions models. In cases where the causal relation between variables was uncertain I used
a model II regression (Bartlett's three-group method, Sokal and Rohlf 2001).
I tested for effects of individual fruit position and phenology on the number
of Bruchus atomarius eggs on a Lathyrus vernus fruit with a generalized
linear model.
17
Results
Spatio-temporal variance in host plant population size, seed production, connectivity and local environmental factors had partly different and partly
similar effects on the intensity of pre-dispersal seed predation in two seed
predators with different host range. Different host ranges resulted in varying
local abundances and disparate distributions in time and space. Pre-dispersal
seed predators had potential to change trait selection gradients in their host
plant and this depended on the context in terms of co-occurrence of species.
The underlying mechanisms of the trait changes were differing trait preferences in species with differing host range and trait preferences also changed
with differing abundances of the co-occurring species. The predictive pattern
of fruit abortion in a long-lived perennial plant resulted in an advantage for
seed predator offence over plant defence.
Paper I – effects of plant patches and environment on seed predation
intensity
The intensity of pre-dispersal specialist and generalist seed predation was
affected by both host plant population size and local environmental factors.
Effects of plant population size were relatively more important in the specialist than in the generalist seed predator, and the specialist seed predator
occurred in less than half of the patches whereas the generalist was present
in nearly all patches. Generalist seed predation was affected by environmental factors, such as the height of the field layer. Intensity of generalist
seed predation on Lathyrus vernus increased with the abundance of the alternative hosts but there were no effects in the reversed direction; presence or
absence of L. vernus did not affect the predation rate on alternative hosts.
My results suggest that the relative importance of different factors influencing the intensity of interactions depend on the degree of specialization.
Paper II – dynamics of two pre-dispersal seed predators over six years
The temporal variation in the intensity of seed predation was affected mainly
by seed production but also by environmental conditions. Relative increases
in seed production from one year to the next resulted in an increased intensity of predation by the monophagous Apion opeticum. The trend was similar
in the oligophagous Bruchus atomarius. I found relatively weak effects of
connectivity and relatively strong effects of previous years population size
and the current years seed production within patches, indicating that popula18
tion dynamics were relatively more affected by local factors than by migration. Although, the monophagous A. opeticum was less abundant and had
lower population densities, abundance of the oligophagous B. atomarius was
more correlated to seed production. Openness of patch edges when seed
production was high had positive effects on the abundance of A. opeticum.
Extinction events were related to local population size of B. atomarius but
not for A. opeticum. Connectivity did not affect population size of A. opeticum and for B. atomarius it was only important in closed forests.
Paper III – plant trait selection, effects of seed predation and seed predator
preferences
Selection on flower number was influenced by pre-dispersal seed predation.
My results show that the patterns of preference differed among the three
investigated seed predators with differing host plant range but also show that
trait-preferences were associated with the abundance of the other seed predators. Thus, the impact on phenotypic selection of seed predation was the
result of relatively complicated relationships between co-occurrence and
preference patterns in the seed predators. The increase in fitness with increasing number of flowers in presence, but not in the absence, of seed predation was disproportional, indicating satiation of seed predators at the level
of plant individuals.
Paper IV – the role of fruit abortion and selective oviposition
The relative effects by the observed oviposition and fruit abortion patterns
on seed predator and plant fitness indicated a clear seed predator offence but
no obvious plant defence. Lathyrus vernus individuals had a predictable
abortion pattern, late fruits and fruits in distal positions had a higher probability of abortion. Bruchus atomarius females preferentially laid their eggs
on fruits with a lower than average probability of abortion and appeared to
use fruit position and phenology as well as some additional unidentified cue.
From the plant perspective, the average reproductive output was reduced by
the observed oviposition as compared to a random oviposition pattern indicating that the abortion pattern has evolved to optimize allocation of resources rather than as a response to seed predation.
19
Discussion
Ecological aspects
Varying host range was associated with differences in abundance and predation intensity by the three seed predators. The most polyphagous species
Tychius quinqepunctatus only occasionally attacked Lathyrus vernus, the
oligophagous Bruchus atomarius was most abundant and was positively
affected by the abundance of the alternative hosts, and the monophagous
Apion opeticum had lower abundance and was most closely related to host
plant population size. The consumer dynamics in this system with moderate
temporal variation in the resource were relatively stable and responses to
relative variation in resources differed in both magnitude and direction from
those reported from systems with high fluctuations (cf. Kelly 1994). Shortterm responses to resource fluctuations were qualitatively the same in monophagous and oligophagous seed predators. However, a narrower host range
resulted in lower densities and fewer patches colonized. Thus, the effect of
differential resource availability may result in long-term effects of host
range. Predation by the oligophagous seed predator on L. vernus increased
with increasing abundance of alternative hosts indicating apparent competition. There was no reverse effect by presence or absence of L. vernus on
seed predation rate on alternative hosts. Effects of the local environment on
the two species were partly different, but both seed predators seemed to
benefit from the same conditions that were favourable for seed production,
thus experiencing dynamics well synchronized with the temporal resource
variation. The seed predator species differed in attack rates and seed loss in
L. vernus was relatively high (mean: 34 %, range 0-100%) and varied considerably in time and space.
Evolutionary aspects
Given that seed predator species exert at least partly different selection pressures, the net selection pressure will vary spatially as a consequence of all
factors affecting any of the involved predators. Interactions will take different expressions at varying scales and this will partly depend on the search
behaviour in the insect. The predation rates on plant individuals may be affected by distance among neighbouring plants or by preference for individual fruits within plant individuals, hence variation host density on the patch
20
level are not necessarily mirrored by processes acting at lower hierarchical
levels.
The number of flowers in individual plants is an important character, determining the number of seeds and the fitness potential. The number of flowers also has the dual role of simultaneously attracting pollinators and seed
predators. The difference in selection on flower number in absence or presence of pre-dispersal seed predation was the combined effect of the three
seed predators different preference patterns. Relative fitness in the presence
of seed predation increased disproportionately with higher flower numbers.
Thus, even though seed predators preferred plants with many flowers, a larger proportion of seeds escaped damage in these plants with higher number
of flowers. This suggests that high numbers of flowers may result in predator
satiation and that it may be beneficial, in the presence but not in the absence
of seed predators, to concentrate reproductive efforts to only some seasons,
i.e. not to flower every year. The negative relationship between seed predator abundances and differing preferences with varying abundances of the
other species suggests that occurrence patterns are a ghost of competition
past. The complex pattern of trait preferences of all three seed predators for
flower number suggest that plant trait selection mediated by a seed predator
will vary with varying abundances of co-occurring species.
The production of surplus flowers is a common phenomena (Burd 1998).
The subsequent excess of young fruits enables high rates of fruit abortion
potentially reducing seed loss through pre-dispersal seed predation
(Stephenson 1981, Ehrlén 1993, Holland et al. 2004). Initial herbivore damage could be a potential cue to future damage and would thereby enable suitable plant responses, such as induced fruit abortion, similar to the induction
of chemical defences (Dicke and Hilker 2003). However, I found no evidence that L. vernus reduced seed loss due to pre-dispersal seed predation
through an increased mean abortion rate of fruits at high levels of infestation.
On the contrary B. atomarius was highly capable of locating viable fruits.
The patterns observed in my study suggest that Lathyrus vernus is constrained by the predictive fruit abortion that has evolved independently of the
seed predation, i.e. due to sequential resource allocation (cf Lloyd 1980).
Nevertheless, some fruits with eggs were aborted which may suggest an
evolutionary potential in L. vernus to reduce seed loss caused by predispersal seed predation. Poor defensive strategies in plants in combination
with highly offensive strategies of consumers are likely the result of differential evolutionary capacities due to the large discrepancy in generation time
(Gandon and Michalakis 2002).
21
Concluding remarks
All is a matter of scale and context. This thesis has shown that interactions
between plants and antagonists vary in time, that processes differ at varying
scales, that differing host range results in different damage intensity as well
as in differing trait preferences. Moreover, pairwise interactions are affected
by the abundance of co-occurring plants and animals. Taken together, this
will result in complex selection mosaics and coevolutionary trajectories.
Such complex interactions among co-occurring antagonists in combination
with spatial and temporal variation in abundances will result in diffuse selection on plant traits as well as in the reciprocal selection on antagonists. The
fact that coevolutionary processes are diffuse gives further emphasis to the
importance of studying coevolutionary relationships in their full context (cf.
Thompson 1994). A step towards dissecting diffuse coevolutionary relationships would be the examination of variation of interaction processes on a
geographical scale by comparing trait selection in populations that vary in
the seed predator guild. Further studies should also benefit of examining the
mechanisms involved in search behaviour and host choice, such as the degree of competition within a consumer guild and the relative role of defensive, visual and olfactory cues.
22
Acknowledgements
I am grateful to Johan Dahlgren, Johan Ehrlén and Peter Hambäck for valuable comments on this text.
23
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Svensk sammanfattning
I den här avhandlingen har jag studerat interaktionen (samspelet) mellan
vårärt, Lathyrus vernus, och tre fröätande skalbaggar (fröpredatorer), Apion
opeticum (gruppen spetsvivlar), Bruchus atomarius (ärtsmyg eller bönbagge)
och Tychius quinqepunctatus (gruppen vivlar), med olika grad av
värdväxtspecialisering. De vuxna skalbaggarna lägger sina ägg på eller i
vårärtens frukter (baljor) och därefter utvecklas larverna inuti baljan, eller
inuti enskilda frön, tills de är fullvuxna skalbaggar. Apion angriper endast
vårärt och har en begränsad utbredning i Sverige, Bruchus föredrar vårärt
men angriper också bland annat gökärt, Lathyrus linifolius, och häckvicker,
Vicia sepium och Tychius förekommer bara vissa år på vårärt och använder
flera arter inom släktena Lathyrus och Vicia och även andra ärtväxter. Syftet
med studierna var att undersöka hur intensiteten i växt-djurinteraktioner
påverkas av födoresursens variation i tid och rum med särskilt avseende på
effekter av värdväxtspecialisering, artsammansättning och växtegenskaper.
Interaktioner mellan växter och djur påverkas på många sätt av såväl
miljöfaktorer som förekomst, utbredning och egenskaper hos de berörda
arterna. Växter är ofta fläckvis utbredda i landskapet, i både små och stora
växtpopulationer på varierande avstånd från varandra, och detta påverkar de
interagerande djurens möjligheter till spridning och lokal överlevnad. En
växt är ofta involverad i åtskilliga, både mutualistiska och antagonistiska,
interaktioner och styrkan av en interaktion är oftast beroende av övriga
interaktörer. Mutualistiska interaktioner (t ex pollinering) är gynnsamma för
båda parter medan det i antagonistiska interaktioner är en part som gynnas
på bekostnad av den andra. Fröpredation (fröätande) delas in två kategorier,
beroende på om angreppet sker före eller efter fröspridningen, på grund av
att de ekologiska och evolutionära konsekvenserna skiljer sig åt mellan de
två typerna. Jag har studerat fröpredation före fröspridning som förekommer
inom många djurgrupper men främst bland insekter. Eftersom interaktioner
sällan sker oberoende av varandra är det viktigt att ta hänsyn till olika
interaktioners effekter på varandra, till exempel kan närvaron av en art
påverka beteendet hos en annan.
Värdväxtspecialisering förekommer i olika grad hos djur som angriper
växter, en del är helt specialiserade på en enda art (monofaga), andra arter
använder ett fåtal närbesläktade eller likartade växter (oligofaga) och de arter
som är generalister använder ett stort antal växtarter (polyfaga).
Interaktionen mellan växt och insekt påverkas av graden av
28
värdväxtspecialisering, bland annat genom att specialister är helt beroende
av sin enda värdart och därmed får en mer begränsad spridningsförmåga och
löper en större risk för ett lokalt utdöende vid de tillfällen då växtresursen
minskar. Generalister har oftast ytterligare resurser att tillgå, i form av
alternativa värdväxter. Trots fördelarna med att ha ett stort antal värdväxter
är det vanligt att insekter är specialister och detta tror man bland annat beror
på att specialister blir effektivare på att både finna och nyttja sin födoresurs.
Fröpredatorer med olika grad av specialisering kan ha skilda effekter på
den gemensamma värdväxten, både på grund av skillnader i förekomst och
antal, men också för att deras val (preferens) mellan växtindivider med olika
egenskaper (t ex blomantal) kan skilja sig åt. Preferensen för olika
växtegenskaper skiljer sig sannolikt åt hos insekter med olika
värdväxtspecialisering och påverkas förmodligen också av förekomsten av
andra arter som konkurrerar om samma resurs. Preferens för specifika
växtegenskaper leder till varierande reproduktionsframgång (fitness) för
olika växtindivider (selektionstryck) och om egenskaperna är ärftliga
kommer variationen av egenskaper inom arten att förändras. Individer med
många blommor är attraktiva för pollinatörer men lockar samtidigt till sig
fler fröpredatorer, vilket kan leda till motstående selektionstryck från
pollinatörer och fröpredatorer eftersom de förra gynnar reproduktionen och
de senare reducerar den.
Coevolution (samevolution), är ömsesidiga evolutionära anpassningar hos
växt och insekt, som uppstår då växtegenskaper resulterar i anpassningar hos
insekterna vilka i sin tur kan ge upphov till nya anpassningar hos växten osv.
Eftersom interaktioner sällan är en enskild företeelse mellan två parter är
sådana anpassningar (adaptationer) oftast svåra att härleda, vilket gör det
ännu viktigare att ta hänsyn till hela nätverket av interaktioner som en art
ingår i. Möjligheterna till anpassning påverkas också av hur långlivade
arterna är. Eftersom insekter oftast har väsentligt mycket kortare
generationstid än värdväxterna så har de en större kapacitet till evolutionär
respons (anpassning) än vad långlivade växter har. I många fall har man
funnit att insekter övervunnit, och ibland till och med kunnat dra nytta av,
försvarskaraktärer hos växten.
Under evolutionen har olika försvarsstrategier mot antagonister uppstått
hos växter såsom produktion av gifter, taggar och tornar. Även andra
strategier kan minska angreppsgraden, till exempel kan en växt minska
skadan av ett angrepp genom att avlägsna angripna delar och därmed strypa
resursen för angriparen. Det omgivande växtsamhället påverkar också
intensiteten av en interaktion, eller angreppsgraden, beroende på hur mycket
alternativa värdväxter det finns tillgång till, och ibland kan växter indirekt
konkurrera med varandra genom att förekomst av en art ökar
angreppsgraden på en annan.
Vårärt blommar som namnet antyder i maj och förekommer i Sverige
oftast i lövskog eller örtrika blandskogar. Jag lokaliserade 46
29
vårärtspopulationer inom ett 5 km x 5 km stort område några mil norr om
Uppsala. Mitt i detta område finns ett naturreservat, Andersby ängsbackar,
där ett jordbrukslandskap med förindustriell karaktär har bevarats. Under sex
år följdes dessa populationer från blomning till frömognad då baljprover
samlades in från samtliga populationer för att beräkna fröproduktion och
angrepp av respektive skalbagge. På varje undersökt växtindivid noterades
antalet blommor och frukter. I varje population räknades antalet blommande
individer, och yta och avstånd till övriga populationer mättes. Jag mätte
också ett antal miljöfaktorer, till exempel trädkronornas täckningsgrad, som
påverkar ljusförhållandena, och markvegetationens sammansättning.
Förekomsten av alternativa värdarter (gökärt och häckvicker) noterades
också, både i och mellan vårärtspopulationerna.
I den första och andra studien (Paper I & II) fann jag att
vårärtspopulationernas storlek samt de lokala miljöförhållandena påverkade
angreppsgraden av både Apion (specialist) och Bruchus (generalist). Apion
förekom bara i hälften av populationerna medan Bruchus förekom i alla
utom en. Båda skalbaggarna populationsstorlekar ökade med ökande storlek
på vårärtspopulationen och effekten var störst för Apion. Miljöfaktorer och
tillgången till alternativa värdväxter ökade graden av Bruchus-angrepp på
vårärt. Förekomst av vårärt hade däremot ingen effekt på angreppsgraden på
de alternativa värdväxterna utan de blev lika hårt angripna där vårärt fanns
som där den inte fanns. Skalbaggarnas populationsdynamik (variation i
populationsstorlek mellan år) varierade under de sex åren och
populationsstorleken var starkt knuten både till årlig fröproduktion och till
föregående års skalbaggsantal hos båda arterna.
I den tredje studien (Paper III) fann jag att selektionstrycket på blomantal
skiljde sig åt i närvaro eller frånvaro av fröpredation. Vårärtsindivider med
många blommor hade högre reproduktionsframgång (fitness) både med och
utan fröpredation, men i närvaro av fröpredation hade individer med stort
blomantal en oproportionerligt högre fitness än de med färre blommor. Den
här skillnaden verkade bero på att de tre skalbaggsarterna delvis föredrog
olika växtindivider och att deras preferens (förkärlek) för individer med
många blommor påverkades av närvaron av de andra arterna. Det var
skillnader i skalbaggarnas preferens och deras påverkan på varandra, som
sammantaget förändrade selektionstrycket på blomantal hos vårärt. Det är
alltså troligt att selektionstrycket av fröpredation kommer variera beroende
på hur många arter som samexisterar.
I den fjärde studien (Paper IV) fann jag att växten aborterade unga baljor i
ett förutsägbart mönster, och att skalbaggen (Bruchus atomarius) lade sina
ägg på de baljor som hade lägst sannolikhet att bli aborterade. Resultatet av
växtens aborteringsmönster och skalbaggens äggläggningsmönster visade att
skalbaggen ökade sin fitness (antalet fullutvecklade skalbaggar) jämfört med
om den lagt sina ägg slumpmässigt. Däremot minskade vårärtens
reproduktionsframgång (antalet oskadda frön) jämfört med ett slumpmässigt
30
scenario, alltså hade växten ingen förmåga att minska skadorna av
fröpredationen genom att abortera angripna frukter.
Sammantaget visar de fyra studierna att växtpopulationens
storleksvariation i tid och rum, fröproduktion, avstånd till övriga
populationer, lokala miljöfaktorer delvis hade olika och delvis likartade
effekter på två fröätande skalbaggar med olika grad av
värdväxtspecialisering. Fröpredation påverkade selektionstrycket på
värdväxten och detta var beroende av hur varje art påverkades av
samexistensen med de övriga. Ett förutsägbart utvecklingsmönster hos
växten var fördelaktigt för angripande insekter. Allt som allt kommer detta
att leda till en brokig blandning av olika selektionstryck på olika
växtpopulationer. Resultatet blir en stor variation av diffusa anpassningar
hos både växter och djur vilket understryker vikten av att studera hela
nätverket av interaktioner som en art är involverad i för att få ökade
kunskaper om hur interaktioner påverkar populationsdynamik och
evolutionära anpassningar.
Tack Karin, Kim och Peter för värdefulla synpunkter på den här
sammanfattningen.
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Tack
Jag vill tacka mina handledare för allt tålamod. Johan för allt du har lärt mig
om vridande och vändande på idéer och uppslag. Peter för inspiration, alla
barngrejer och för att du hjälpte mig att hålla näsan över vattenytan under en
särskilt jobbig vecka. Jag vill tacka Gisela för att du alltid hälsat lika glatt,
och för goda råd. Tack till Peter och Ingela för goda råd och trevligt jobb
nere i växthuset. Tack alla som har jobbat i fält och räknat baljor Ade, Ana,
Anna, Camilla, Jessica, John, Karin, Liv, Mia, Samira, Suzanne och Tove.
Sofia för trevliga promenader. Åsa och Anna, mina alltid saknade
rumskompisar. Åsa du lärde mig som kom utifrån lite om Botan. Anna du
lärde mig att allt inte är mitt fel. Maria, tack för hela vår botaniska resa
tillsammans men framförallt för att du höll kontakten när du hade valt en
annan väg. Micke för diskussioner om livet, arbetet och makten.
Tack för att jag slapp fika vid twin-peaksdjurparken någonstans i
Dalslands djupaste avkrokar. Kristina för mammakläder, alla trevliga samtal
och goda råd. Mathias, för alla tips och mycket uppmuntran inför det
avslutande avhandlingsarbetet. Didrik för gemensam avhandlingsstress och
för att du gav mig en knuff upp på vägen när jag var utan opplösning.
Tack alla som var med på Mallis för en trevlig resa. Johan D, för att du
lyssnade på trötthet och frustration. Kajsa för alla trevliga samtal om
spindlar och musik. Leena för all uppmuntran. Hugo och Karin för trevligt
sällskap på kurser. Sonja för allt trevligt ventilerande om barn och annat.
Camilla och Jessica, utan er hjälteinsats med baljorna hade jag aldrig hunnit.
Alla trevliga människor som jag har mött under min tid på Botan.
Jag vill tacka alla mina vänner och släktingar för att ni finns kvar trots att
jag ofta varit distraherad. Karin, tack för sällskap i fält, för tak över huvudet,
för alla resor och för allt stöd när tillvaron inte kändes så hanterbar. Åsa för
att du alltid är en vän var du än är. Lotta för all bio och alla fikasamtal, kom
hem snart. Ana, because you once told me I had to try science. Elize for
company when I was starting my project. John för dina tappra försök i fält
och för att du alltid varit intresserad, Towe för att du alltid trott på min
förmåga, Bengt för alla filosofiska diskussioner och mamma för att du älskar
blommor. Karin F, Mona och Bengt för att ni passade Märta när dagiset
kapsejsat.
Märta och Kim, utan er hade det aldrig gått. Tack för att ni har väntat på
mig. Nu kommer jag tillbaka!
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