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Thermal adaptation along a
latitudinal gradient in damselflies
Viktor Nilsson
Akademisk avhandling
som med vederbörligt tillstånd av Rektor vid Umeå universitet för
avläggande av filosofie doktorsexamen framläggs till offentligt försvar i
sal N450, Naturvetarhuset.
Fredagen den 18 januari, kl. 13:00.
Avhandlingen kommer att försvaras på engelska.
Fakultetsopponent: Docent Karl Gotthard,
Zoologiska institutionen: Ekologi, Stockholms Universitet, Sverige.
Ecology and Environmental Science
Umeå University
Umeå 2012
Organization
Document type
Umeå University
Doctoral thesis
Ecology and Environmental Science
Date of publication
14 December 2012
Author
Viktor Nilsson
Title
Thermal adaptation along a latitudinal gradient in damselflies
Abstract
Understanding how temperature affects biological systems is a central question in
ecology and evolutionary biology. Anthropogenic climate change adds urgency to this
topic, as the demise or success of species under climate change is expected to depend on
how temperature affects important aspects of organismal performance, such as growth,
development, survival and reproduction. Rates of biological processes generally increase
with increasing temperature up to some maximal temperature. Variation in the slope of
the initial, rising phase has attracted considerable interest and forms the focus of this
thesis. I explore variation in growth rate-temperature relationships over several levels of
biological organization, both between and within species, over individuals’ lifetime,
depending on the ecological context and in relation to important life history
characteristics such as generation length and winter dormancy.
Specifically, I examine how a clade of temperate damselflies have adapted to their
thermal environment along a 3,600 km long latitudinal transect spanning from Southern
Spain to Northern Sweden. For each of six species, I sampled populations from close to
the northern and southern range margin, as well from the center of the latitudinal range.
I reared larvae in the laboratory at several temperatures in order to measure individual
growth rates. Very few studies of thermal adaptation have employed such an extensive
sampling approach, and my finding reveal variation in temperature responses at several
levels of organization.
Keywords
Growth rate, metabolic theory of ecology, universal temperature dependence, environmental
gradients, thermal performance, thermal sensitivity, environmental variability, optimality theory,
life history, acclimation, size structure, competition, cannibalism, intraguild predation
Language
English
ISBN
978-91-7459-529-1
Number of pages
35 + 5 papers
Thermal adaptation along a
latitudinal gradient in damselflies
Viktor Nilsson
Department of Ecology and Environmental Science
Umeå 2012
Copyright © Viktor Nilsson
ISBN: 978-91-7459-529-1
Cover image: Coenagrion puella from August Johann Rösel von Rosenhof’s Der
Insecten Belustigung, Zweiter Theil (1749). Distributed under a CC-BY 2.0 licence
by Pecay @ Bibliodyssey.
Elektronisk version tillgänglig på http://umu.diva-portal.org/
Printed by: VMC, Umeå University
Umeå, Sweden 2012
“You behold there a considerable number of a remarkable species of
beautiful insects, the elegance of whose appearance, and their attire,
have procured for them the name of damsels”
Sonnini de Manoncourt, Travels to Upper and Lower Egypt (1799)
LIST OF PAPERS
This thesis is a summary and discussion of the following papers, referred to
in the text by the roman numerals.
I.
Nilsson-Örtman, V., R. Stoks, M. De Block and F. Johansson. 2012.
Generalists and specialists along a latitudinal transect: patterns of thermal
adaptation in six species of damselflies. Ecology 93: 1340-1352.
II.
Nilsson-Örtman, V., R. Stoks, M. De Block, H. Johansson and F.
Johansson. In press. Latitudinally structured variation in the temperature
dependence
of
damselfly
growth
rates.
Ecology
Letters
III.
Johansson, H., R. Stoks; V. Nilsson-Örtman, P. Ingvarsson and F.
Johansson. In press. Large-scale patterns in genetic variation, gene flow and
differentiation in five species of European Coenagrionid damselfly provide
mixed support for the central-marginal hypothesis. Ecography.
IV.
Nilsson-Örtman, V., R. Stoks, M. De Block and F. Johansson. Latitudinal
patterns of phenology and age-specific thermal performance across six
Coenagrion damselfly species (Odonata). Submitted manuscript
V.
Nilsson-Örtman, V., R. Stoks and F. Johansson. Competition modifies the
temperature dependence of damselfly growth rates. Manuscript
Papers I, II and III are reproduced with kind permission from the respective
publishers.
TABLE OF CONTENTS
INTRODUCTION
1
Background
1
Adapting to thermally heterogeneous environments
1
Studying thermal adaptation
2
The Universal Temperature Dependence hypothesis
4
Context-dependent thermal performance
4
Thermal performance and life history theory
5
The evolutionary ecology of thermal adaptation
6
Aims
7
Research questions
STUDY SYSTEM
METHODS
Experiment 1: Thermal sensitivity of growth rates across latitudes
Experiment 2: Effects of competition and temperature on growth rates
PAPER I: THERMAL BREADTH DECREASE WITH LATITUDE
7
8
11
11
11
12
Model 1: lake temperature across latitudes
13
Model 2: larval life cycles and temperature variation
13
Results and discussion
PAPER II & III: GROWTH RATES DO NOT SCALE WITH METABOLISM
Results and discussion
PAPER IV: THERMAL PERFORMANCE SHIFTS DURING ONTOGENY
Results and discussion
14
15
16
17
18
PAPER V: COMPETITION AND TEMPERATURE MODIFIES GROWTH RATES 19
Results and discussion
20
CONCLUDING REMARKS
20
ACKNOWLEDGEMENTS
22
AUTHOR CONTRIBUTIONS
23
Paper I
23
Paper II
23
Paper III
23
Paper IV
23
Paper V
23
REFERENCES
24
THANKS
31
TACK
32
ABSTRACT
Understanding how temperature affects biological systems is a central question in
ecology and evolutionary biology. Anthropogenic climate change adds urgency to this
topic, as the demise or success of species under climate change is expected to depend
on how temperature affects important aspects of organismal performance, such as
growth, development, survival and reproduction. Rates of biological processes
generally increase with increasing temperature up to some maximal temperature.
Variation in the slope of the initial, rising phase has attracted considerable interest
and forms the focus of this thesis. I explore variation in growth rate-temperature
relationships over several levels of biological organization, both between and within
species, over individuals’ lifetime, depending on the ecological context and in relation
to important life history characteristics such as generation length and winter
dormancy.
Specifically, I examine how a clade of temperate damselflies have adapted to their
thermal environment along a 3,600 km long latitudinal transect spanning from
Southern Spain to Northern Sweden. For each of six species, I sampled populations
from close to the northern and southern range margin, as well from the center of the
latitudinal range. I reared larvae in the laboratory at several temperatures in order to
measure indiviudal growth rates. Very few studies of thermal adaptation have
employed such an extensive sampling approach, and my finding reveal variation in
temperature responses at several levels of organization.
My main finding was that temperature responses became steeper with increasing
latitude, both between species but also between latitudinal populations of the same
species. Additional genetic studies revealed that this trend was maintained despite
strong gene flow. I highlight the need to use more refined characterizations of
latitudinal temperature clines in order to explain these findings. I also show that
species differ in their ability to acclimate to novel conditions during ontogeny, and
propose that this may reflect a cost-benefit trade-off driven by whether seasonal
transitions occur rapidly or gradually during ontogeny.
I also carried out a microcosm experiment, where two of the six species were
reared either separately or together, to determine the interacting effects of
temperature and competition on larval growth rates and population size structure.
The results revealed that the effects of competition can be strong enough to
completely overcome the rate-depressing effects of low temperatures. I also found
that competition had stronger effects on the amount of variation in growth rates than
on the average value.
In summary, my thesis offers several novel insights into how temperature affects
biological systems, from individuals to populations and across species’ ranges. I also
show how it is possible to refine our hypotheses about thermal adaptation by
considering the interacting effects of ecology, life history and environmental
variation.
INTRODUCTION
Background
Temperature not only dictates the limits for life, it sets the pace. For most
organisms, the biochemical processes that are necessary for their existence
can only occur within a narrow range of temperatures, roughly between 0°C
and 45°C (Pörtner 2002). Within this temperature range, the rates of
virtually all biological processes, from enzyme kinetics to species interactions
and populations growth rates, depend strongly on temperature (Angilletta
2009; Daniel & Danson 2010).
With the exception of a small number of model organisms kept in
laboratories, very few organisms live in a world of constant temperatures.
Rather, temperature varies considerably between geographic regions, over
the seasons, throughout the course of the day and between sun and shade
(Bradshaw et al. 2004). Unlike processes like predation and competition,
that only exist when individuals interact with other individuals, temperature
is an inescapable physiological reality that acts directly on each molecule,
enzyme and cell within an organism (Hochachka & Somero 2002; Angilletta
2009). But temperature does not affect all organisms in the same way.
Temperatures that would cause the sudden death of an Antarctic brachiopod
(Peck 2002) can represent the optimum temperature for activity in a Sahara
ant (Gehring & Wehner 1995). Thus, temperature not only affects organisms
– organisms adapt to temperature.
Adapting to thermally heterogeneous environments
Organisms have evolved a multitude of strategies that allows them to cope
with temperature heterogeneity. A striking example is thermoregulation, the
ability of an organism to maintain a constant body temperature over a range
of environmental temperatures. Famous examples include the basking
behavior of lizards and snakes and the tightly controlled internal body
temperature of mammals and birds. Thermoregulatory strategies, however,
are available to a small number of organisms. These mainly include large,
terrestrial vertebrates (Huey & Slatkin 1976; Chappell 1983). For the vast
majority of species on earth, body temperature is highly or completely
dependent on ambient temperatures. This is especially true for small-bodied
(Unwin & Corbet 2008) and aquatic organisms, due to the high specific heat
and thermal conductivity of water (Feder & Hofmann 1999).
It is therefore not surprising that ectotherms display a range of
adaptations that allows them to move, feed, grow and develop over a wide
1
range of body temperatures. Adaptation to thermal heterogeneity frequently
involves changes in the degree to which an organism’s performance depends
on changes in body temperature. This is referred to as the thermal sensitivity
or dependence of performance. Important performance traits include
growth, development and locomotion. Thus, some organisms are able to
maintain relatively constant levels of performance over a wide range of
temperatures. These are referred to as thermal generalists. Others can only
tolerate a very narrow range of temperatures, with even small changes in
temperature causing major changes in performance. These are referred to as
thermal specialists (Angilletta 2009).
Studying thermal adaptation
Thermal performance curves (TPCs) forms an unifying, conceptual
framework for studying differences in the thermal sensitivity of performance
among organisms (Fig 1). TPCs describe the relationship between a
temperature and a continuous phenotypic character (e.g. growth,
development, or activity). These curves represent a special type of
continuous reaction norms, and the slope of TPCs represents a measure of
plasticity. TPCs of many traits have a distinct shape: a more or less steeply
increasing “rise” phase, a single optimum, and a sharply declining “fall”
phase (Figure 1; a,b,c). Six characteristics of performance curves has
attracted considerable interest: 1) the optimal temperature (Topt) – the body
temperature at which performance is maximized; 2) the maximum
performance (Pmax) – the height of the curve at the optimal temperature; 3)
the thermal breadth –the temperature range over which an individual can
maintain an arbitrary level of performance, for example 80% of Pmax; 4) the
amount of thermal plasticity of performance – the slope of the rising and
falling parts of TPCs (a and c in Figure 1); 5) critical thermal thresholds – the
lower (CTmin) and upper (CTmax) body temperatures at which performance is
zero; and 6) the tolerance range – the difference between CTmin and CTmax.
The complex shape of TPCs reflects the contribution of several underlying
mechanisms. There is, however, little consensus about what mechanisms
give rise to these different aspects of thermal performance curves. In fact,
different processes may be important for TPCs at different hierarchical
levels, in different organisms and for different aspects of organism
performance (Pörtner 2002). For example, lower critical thresholds may
reflect temperature-induced changes in the structure of cellular membranes
(Hochachka & Somero 2002) or the ability of mitochondria to generate ATP
(Pörtner et al. 2006). Upper critical limits have been suggested to reflect the
denaturation of important proteins (Hochachka & Somero 2002), or limits
2
Figure 1. Thermal Performance Curve (TPC) showing
important characteristics, including the lower (CTmin) and
upper (CTmax) critical thermal thresholds, a single thermal
optimum (Topt), maximal performance (Pmax) and performance
breadth (defned as the range of temperatures over which a
given fraction. e.g. 80% of Pmax, is maintained. In the text I also
refer to the rising (a), plateau (b) and falling (c) phases. Note
that the amount of plasticity (i.e. the slope of the curve) is great
during the rising and falling phases, but zero during the plateau
phase.
to the ability to supply mitochondria with oxygen (Pörtner 2010). The slope
of the rising phase is thought to reflect the effect of temperature on ratelimiting enzymes and/or metabolism (Brown et al. 2004). While the falling
phase has attracted less interest than the rising phase, it has been suggested
to reflect the rate of degradation of important enzymes (Ratkowsky et al.
2005; Dell et al. 2011). Finally, the location of Topt may represent an
independently evolving trait related to the thermal optima of performancelimiting enzymes (Somero 2002), a balance between the rate-increasing and
rate-depressing processes of the rise and fall phases (Logan et al. 1976), or a
temperature window where an organism’s supply and demand of oxygen is
in balance (Pörtner 2002).
3
The Universal Temperature Dependence hypothesis
The slope of the rising phase has recently attracted considerable interest,
largely due to the fact that Brown et al. (2004) used this relationship as one
of the cornerstones in their influential Metabolic Theory of Ecology (MTE).
According to the MTE, the effect of temperature on biological rate traits can
be modelled using the Boltzmann-Arrhenius equation:
R = b0 e-E/kT
(1)
where R is the rate, E is the activation energy (in units eV), k is Boltzmann’s
constant (8.62 x 10-5 eV K-1) an T is the temperature in Kelvin. The
parameter E describes the slope of the relationship between the natural
logarithm of a rate trait and temperature (at the scale of -1/kT). MTE
postulates that the activation energy term, E, can only take on values
between 0.6 eV and 0.7 eV, with a mean value across traits of 0.65 eV. This is
known as the “Universal Temperature Dependence” (UTD) hypothesis
(Brown et al. 2004). Recently, Dell et al. (2011) showed that E varies
considerably between traits, species and habitats. Paper II is the first
empirical test of this hypothesis below the species level and for full-sib
families. It is also the first to use a strong, geographic sampling design.
Context-dependent thermal performance
TPCs estimated under controlled laboratory conditions are sometimes
interpreted as if they represent a fundamental physiological property of an
organism. We may, for example, be inclined to call a species a thermal
specialist if we find that it only grows under a very narrow range in the
laboratory. This, however, represents an oversimplification. Instead, TPCs
represent the performance of an individual under one specific set of
conditions and at a given point in time. There is a large literature on how
experimental manipulations of environmental variables (light, temperature,
water, etc.) in the laboratory can modify various aspects of physiological
traits (e.g. location of thermal optima or tolerance range) (Huey & Berrigan
1996; Chown et al. 2009; Cooper et al. 2010). When this occurs in the
laboratory it is called acclimation. Whereas facultative modification of
physiological traits by environmental factors in the field is called
acclimatization (Wilson & Franklin 2002). Furthermore, the expression of
physiological traits can also change over time, both in relation to an
individuals’ physiological age (Spence et al. 1980; Berger et al. 2011) and in
4
relation to the time-scale of exposures to environmental factors (Schulte et
al. 2011). Traditionally, acclimation responses have been studied mainly
from a mechanistic, physiological perspective and the observed patterns
have been assumed to be of adaptive significance. This is known as the
beneficial acclimation hypothesis (Leroi et al. 1994; Huey & Berrigan 1996).
More recently, there has been a surge in interest in critically evaluating
whether acclimation responses really are adaptive, and to quantify their
costs and benefits (Wilson & Franklin 2002; Woods & Harrison 2002;
Kristensen et al. 2008)
Thermal performance and life history theory
The performance trait that I focus on in this thesis is individual growth rates
– the rate at which an individual increase in size during. Growth rate is an
important performance trait as size is positively correlated with mating
success, fecundity, survival and development time (Kingsolver & Huey 2008)
and for the outcome of competitive and aggressive encounters (Rudolf
2007). But growing fast comes at a cost, and growth rates are involved in
many trade-offs, making it necessary to consider the temperaturedependence of growth rates within the framework of life history theory (Roff
2002). The trade-off between the age and size at reproduction is perhaps one
of the most important in organisms with complex life cycles (i.e. those that
make an abrupt habitat shift when transitioning between life stages). Early
reproduction allows the completion of more generations in a given amount
of time. This affects the intrinsic rate of increase, r (Kingsolver & Huey
2008). Later reproduction, on the other hand, leaves more time available for
growth, which allows individuals to grow bigger. This mainly affects the net
reproductive rate, R0 (Kingsolver & Huey 2008). The optimal investment in
development or growth will shift depending on the costs and benefits of
attaining a large size or maturing early (Abrams et al. 1996). High growth
rates are also involved in trade-offs with predation risk. Fast growth requires
more resources, making it necessary for fast-growing individuals to forage
more. This likely causes them to be more exposed to predators (Rowe &
Ludwig 1991). These and other trade-offs are necessary to consider in order
to derive realistic predictions about patterns of thermal adaptation, and for
interpreting the results from comparative physiological studies.
5
The evolutionary ecology of thermal adaptation
Adaptation to temperature represents a balancing act between many
complex processes, both abiotic and biotic. Latitudinal, continental and local
patterns of temperature variation form the abiotic backdrop of thermal
adaptation. From the equator to the poles, average temperatures decrease,
and seasonality of temperature increase (Piper & Stewart 1996; Angilletta
2009). Seasonality of temperature also varies along longitudinal clines:
temperature seasonality increase from the coasts to the interior of large land
masses. Light, similarly, varies with latitude, with nearly equally long days
and nights year round at the equator, but with increasingly long summer
days and winter nights towards higher latitudes (Bradshaw & Holzapfel
2007). This affects patterns of diurnal temperature fluctuation. Average,
seasonal and diurnal temperature patterns also depend on local factors such
as altitude and topography (Kang et al. 2000). Aquatic and especially marine
habitats display greatly reduced fluctuations due to the high capacity of
water to store heat (Angilletta 2009). Different terrestrial vegetation types
also differ strongly in thermal characteristics. Together, this ensures that
each population along a latitudinal gradient will experience a unique set of
thermal conditions. Because of gene flow from populations that may be
exposed to a radically different thermal regime, thermal strategies at a local
scale will in part depend on the local selection regime, but also on selection
acting in other parts of a species’ range. To what extent patterns of thermal
adaptation reflect optimization to local environmental conditions or
evolutionary constraints represents a major unresolved question in thermal
biology (Gilchrist & Kingsolver 2001).
But thermal strategies also strongly depend on the biotic environment.
Changes in temperature will affect the performance and competitive ability
of individuals differentially provided they differ in any aspect of thermal
performance. Thus, thermal performance will have an important influence
on ecological processes, and ecological interactions will have an important
influence on the evolution of thermal performance. In many ways,
temperature can be considered as one of the axes of an organism’s ecological
niche. The benefits that it gains from performing at a given temperature
depend not only on the frequency by which it experience that temperature,
but also on the behavior of the individuals with which it interacts with at that
temperature (Magnuson et al. 1979; Mitchell & Angilletta Jr 2009).
Thus, thermal adaptations must be considered as the joint outcome of
both environmental (e.g. temperature differences across latitudes,
seasonality of temperature, the magnitude of diurnal temperature
fluctuations, etc.), ecological (e.g. seasonal variation in predator abundance,
prey availability, community composition, and the life histories and thermal
strategies of predators, mutualists and competitors) and evolutionary factors
6
(evolutionary constraints on the shape of TPCs, gene flow from other
populations, frequency dependent selection from biotic and abiotic factors,
genetic drift, etc.). Recently, several theoretical models have produced
testable hypotheses about how environmental, ecological and evolutionary
factors may drive patterns of thermal adaptation (Hughes & Grand 2000;
Mitchell & Angilletta Jr 2009). Empirical studies with the aim to test
predictions about the interacting effects of these factors are necessary to
advance the field of thermal biology.
Aims
This introduction was meant to convey one important point: that an
understanding of how organisms adapt to thermally heterogeneous
environments will require a careful consideration of many different aspects
of thermal performance – both separately and jointly, over both time and
space, and from the level of enzymes to organisms and ecosystems (Clarke
2003; Pörtner et al. 2006). The focus of this thesis lies on two of aspects of
thermal adaptation: performance breadth and variation in the plasticity (i.e.
the slope) of the rising phase of TPCs. My aim was to test theoretical
predictions about how thermal breadth and plasticity of the rising phase of
TPCs vary across levels of biological organization, over time, and in relation
to the ecology and life history of different species. Thus, I have studied
variation in temperature-responses among species in relation to
environmental variation and life history (Paper I), over different
hierarchical levels from families, populations, latitudes and species (Paper
II), over the lifetime of individual organisms (Paper IV) and in relation to
interactions between competing species (Paper V). I also evaluated the
genetic diversity and differentiation of the studied populations using
microsatellites (Paper III) to back up observed patterns of thermal
adaptation with estimates of gene flow and differentiation at neutral loci.
Research questions
1) Can latitudinal variation in thermal performance breadth be predicted
based on how thermal variation is partitioned among and within generations
as predicted by optimality models? How can we quantify within- and amonggeneration temperature variation across latitudes in a group of aquatic
organisms with a complex life cycle? (Paper I)
7
2) Is the slope of the rising phase of the thermal performance curves of
growth rates constrained by metabolism? If not, over what levels of
biological organization do we find variation in the temperature-dependence
of growth rates? What is the role of gene flow in preventing or enabling
thermal adaptation across species’ range? (Paper II and III)
3) What is the role of thermal acclimation and phenological timing for
species living in seasonal environments? What aspects of a species’ thermal
environment or life history strategy favour strong acclimation responses?
(Paper IV)
4) To what extent can information from controlled laboratory experiments
be used to predict the growth performance of individuals in nature? How
does inference competition affect the growth performance of damselflies at
different temperatures? (Paper V)
STUDY SYSTEM
My study system consist of six species of damselflies (Insecta: Odonata:
Zygoptera) in the genus Coenagrion. The six species were chosen on the
basis of their latitudinal pattern of distribution in Europe (Figure 2). Thus,
these species represent two northern species (C. armatum and C.
johanssoni) that are exclusively found in the boreal parts of northern
Europe, two central species (C. puella and C. pulchellum) whose ranges
spans much of Central Europe, and two southern species (C. mercuriale and
C. scitulum) that are restricted to Southern Europe. My sampling scheme
involved collecting eggs and DNA samples of each species from populations
near the northern and southern range margin, as well as within the core part
of each species’ range (represented by red squares in Figure 2)
Odonates (dragonflies and damselflies) are an ancient group of insects,
with an evolutionary history deeply rooted in tropical areas (Grimaldi &
Engel 2005). Some of the thermal characteristics of ancestral, tropical
odonates appears to have remained largely unchanged as they have
expanded into temperate areas. Thermal requirements for egg development
are consistently among the highest of any insect order (Pritchard et al. 1996).
Optimal temperatures for growth and activity fall above 20°C in all stages
(Leggott & Pritchard 1985, 1986). Odonates are nevertheless a highly
successful group in temperate environments, often being dominant
predators in many aquatic ecosystems, in particular those that lack fish
(Benke 1976). By studying how odonates have adapted to temperate
8
Figure 2. Map showing the
European distribution of the six
studied species. The location of
the
sampled
latitudinal
populations are shown as red
squares. Each square represent
three nearby sub-populations.
Note differences in distribution
pattern, with two North European
(a,b), two Central European (c,d)
and two South Eropean (d,e)
species. Maps are reproduced
from
Askew
(2004)
with
permission from Apollo books.
environments it is possible to gain an understanding of the types and
sequence of adaptations that enables or hinders low-latitude taxa to colonize
temperate environments.
The genus Coenagrion (Odonata: Zygoptera: Coenagrionidae) is one of
the most species-rich temperate zygopteran lineages with about 20 species in
the Palaearctic region and some additional representatives in the Nearctic
region (Dijkstra & Lewington 2006). Adults are typically active in spring and
summer. Mating takes place near the aquatic larval habitat. Depending on
the species, the habitat consists of a pond, a shallow lake or a slowly running
small stream (Askew 2004). A single female usually mates with multiple
males. This has resulted in an intense sperm competition between males.
Upon contact, a male first remove the sperm package deposited by the
previous male before transferring his own sperm (Miller & Miller 1981;
Waage 1986). Eggs are deposited in aquatic plants.
9
The aquatic larvae hatch after a brief period of embryonic development
(Waringer & Humpesch 1984). Damselfly larvae are generalist predators of
smaller invertebrates. Both interference and exploration competition as well
as intra-guild predation and cannibalism is common in damselfly larvae
(McPeek & Crowley 1987; Johansson 1993, 1996; Anholt 1994). Winters are
spent in the larval stage. In fall, Coenagrion larvae enter a facultative
diapause in which cold tolerance is increased and development is retarded or
completely stopped (preventing premature emergence) (Norling 1984;
Corbet 1999). Diapause is initiated by both low temperatures and short
photoperiods (Pritchard 1989).
Odonates are well known for their highly plastic life histories. The
number of generations per year (referred to as voltinism) decrease with
increasing latitude (Norling 1984; Corbet et al. 2006). Thus, the southern
species in this study are univoltine (one generation/year) over most of their
range, although there are indications that some species may complete two
generations per year in North Africa (Jacquemin & Boudot 1999). Central
European species are likely univoltine over much of their range whereas
north European species require two or even more years to complete their
development (Norling 1984; Corbet et al. 2006). Variation in voltinism is
important with regards to the subject of this thesis for several reasons. The
first is related to the thermal niche: variation in voltinism have a strong
influence on how seasonally varying temperatures are partitioned within and
between larval generations, which I explore in detail in Paper I. The second
is related to the fitness consequences of growing fast: depending on the size
individuals reach at the end of the growth season, large individuals will
develop directly into adult at the beginning of the next growth season,
whereas smaller individuals will prolong their life cycle and require one
more year to complete their development (Norling 1984; Buskirk 1992). This
phenomenon is known as cohort splitting and is explored further in Paper
IV. Individuals reaching maturity in one instead of two years will effectively
double the intrinsic rate of population increase, r (Roff 2002; Kingsolver &
Huey 2008). This means that growing fast can be of immense importance for
individual damselflies, further motivating the choice of growth rates as the
trait studied in this thesis.
Besides affecting development time, variation in growth rates is
important for damselfly larvae as growth rates affect the relative size of
individuals. Size differences is an important aspect of the life history of
damselfly larvae: the strength and direction of intraguild predation,
cannibalism and competition strongly depend on relative size differences
between larvae (Polis et al. 1989; Buskirk 1992; Rudolf 2007). In addition,
the size of final-instar larvae is correlated with adult size, which is an
important determinant of longevity, fecundity and mating success in
damselflies (Banks & Thompson 1987; Thompson et al. 2011).
10
METHODS
Experiment 1: Thermal sensitivity of growth rates across
latitudes
This experiment was used for Paper I, II and IV and was conducted over a
period of three years, between 2008 and 2010. I reared larval damselflies
individually at three or four temperatures to estimate the effects of
temperature on larval growth rates. For each species, I acquired eggs from
females collected near the northern and southern limits of its range, and
from the center of its range (Figure 2). At each of these latitudes, I sampled
between two and four populations (i.e. separate water bodies). From each
population, I collected eggs from about 5 females, making the total sample
size about 15 egg clutches at each latitude. Egg clutches were brought to the
laboratory in Umeå, Sweden or Leuven, Belgium and reared at the following
fixed temperatures: 16.3°C, 19.5°C, 21.5°C and 24.0°C (24.0°C added during
2009 and 2010). The experiment was a full-sib design: 15 or 20 offspring
from each female were randomly divided between the three or four
temperature treatments (five per temperature). Thus, full-sib larvae were
nested in families nested in populations nested in latitudes nested in species.
In total, I reared more than 5000 individual larvae from over 200 familygroups.
Larvae were fed six days a week on brine shrimps (Artemia salina) and
the head width of each individual was measured at the age of 0, 42, 84 and
126 days. Using these data, I fitted individual growth trajectories as a thirddegree polynomial function between head width and time. Individual, sizecorrected relative growth rates (RGRs) were calculated as the slope of the
growth trajectory when an individual had reached 1/5th the adult head width.
This method accounts for differences between species in both initial and
final size (Rose et al. 2009). See below under Paper I, II and IV for details
and results from this experiment.
Experiment 2: Effects of competition and temperature on
growth rates
The second experiment, used for Paper V, was a microcosm experiment
designed to test how the thermal sensitivity of growth rates depend on
competitive interactions between and within species. I selected two species
from the first experiment: the northern C. armatum and the central C.
pulchellum. The reasons for choosing these species were threefold. First, the
latter species is expanding its range northwards into the range of the former
(Hickling et al. 2005). Thus, I was interested in the population dynamics of
11
these species when they come into contact. Second, Experiment 1 revealed
that the two species differ in the thermal sensitivity of growth rates. And
finally, the two species were possible to distinguish from each other in the
larval stage based on morphological characters.
I set up 48 microcosms (3L water volume), each containing 30 newly
hatched damselfly larvae, aquatic snails, macrophytes and microorganism
from a natural pond. Larvae were continuously fed Artemia salina and
Daphna magna. The experimental design was as follows: two damselfly
species, two temperatures (16°C and 21°C) and two competition treatments
(intra- and interspecific competition). Thus, one third of the microcosms
contained only C. armatum (intraspecific), one third contained only C.
pulchellum (intraspecific) and one third contained both species (interspecific
competition). The microcosms were run for 126 days and the head width of
individuals was checked at day 0, 42, 84 and 126 as in the first experiment.
To calculate relative growth rates from these data, I used the same growth
model as in Experiment 1. However, since I could not keep track of
individual larvae, I used a stratified resampling approach. I ranked
individual observations based on their relative size at each measurement
event, and iteratively fitted the growth model using those data points that
had the same rank order within each measurement event. I was interested
both in the growth rates and in changes in the size distribution of larvae over
time. More details and results from this experiment can be found in Paper
IV.
PAPER I: THERMAL BREADTH
DECREASE WITH LATITUDE
In Paper I, I show that the thermal breadth of growth rates becomes
narrower towards higher latitudes. I propose that this reflect a combination
of rapid seasonal transitions in high-latitude environments together with
that damselfly larvae enter diapause at low temperatures.
The aim of this paper was to test the predictions from two theoretical
models that have explored how thermal breadth depends on environmental
variation. The first is by Lynch & Gabriel (1987) and the second by Gilchrist
(1995). The main difference between these two models lies in how
performance is assumed to affect fitness. In Lynch & Gabriel’s model,
performance affects fitness by increasing survival, whereas in Gilchrist’s
model, performance affects fitness through increasing fecundity. Either of
these fitness mechanisms may apply to growth rates (Arendt 1997; Roff
2002). If growth rates mainly affect survival, thermal breadth should
12
increase with increasing thermal heterogeneity within generations (Lynch &
Gabriel 1987). If growth rates affect fitness by increasing fecundity, thermal
breadth should depend on how environmental variation is partitioned
among relative to within generations (Gilchrist 1995).
Few studies have explicitly tested these predictions (Angilletta 2009). In
part, this is related to the challenges involved in quantifying temperature
variation among and within generations. This is especially challenging in
aquatic organisms because water temperature data is not generally available
in the same way as air temperature data. To deal with these problems, I
combine simulations of water temperature and damselfly life cycles with
empirical data on the thermal breadth of the six species from Experiment 1.
This paper is a comparative study of difference between species. Thus, I only
used data from central populations.
Model 1: lake temperature across latitudes
My first step was to produce realistic temperature profiles for representative
water bodies along the latitudinal gradient. To do this, I took advantage of
the recently developed lake model FLake (Mironov 2008). FLake was
intended to model feedback loops between the atmosphere and lakes for
weather forecasting, but it can also be used to model the temperature
evolution of lakes of a user-specified depth and turbidity anywhere in the
world. The model requires input data such as air temperature, solar
radiation, cloud cover and wind speed. This information is available in
publicly available global databases. I ran a total of 18 FLake simulations
using weather data from each of the areas where the six damselfly species
were sampled (see Figure 2). This allowed me to characterize patterns of
temperature variation along the entire 3,600 km latitudinal transect. The
weather data came from the ECMWF Era-Interim dataset for the years 19992009 at 12h intervals (Simmons et al. 2007).
Model 2: larval life cycles and temperature variation
In this model, I considered how environmental variation was partitioned
among and within damselfly generations. I incorporated two important
aspects of the life history of damselflies in this model: 1) that damselfly
larvae enter diapause during winter; and 2) that the generation length
increase with latitude (Corbet 1999; Corbet et al. 2006). With regards to
diapause, I assumed that temperatures below 8°C were not meaningful for
the evolution of thermal breadth of growth rates, as damselflies do not grow
at temperatures below 8-10°C (Corbet 1999). Next, I defined the length of a
13
Figure
3.
Representative
temperature profiles (surface
water temperature) for shallow
lakes at different latitudes.
Temperature data comes from
FLake
simulations
using
meteorological
data
from
Northern Sweden (a), Belgium
(b) and Southern Spain (c).
Data from three separate years
(2000-2002) are shown in light
gray, medium gray and black,
respectively.
generation based on the number of degree-days needed to complete larval
development (based on my own laboratory data). Running these life cycle
simulations using water temperature data from Model 1, I was able to
quantify how water temperature variation was partitioned within and
between damselfly generations across latitudes.
Results and discussion
The life cycle simulations revealed the following patterns. First, withingeneration thermal variability decreased towards higher latitudes. Second,
the relative amount of among-to-within generation temperature variation
peaked at mid-latitudes (~50°N). The latter was due to a voltinism shift from
a univoltine to a semivoltine life cycle. The finding that within-generation
variation decrease with latitude may at first appear surprising, since highlatitude environments are characterized by dramatic seasonal fluctuations in
temperature. This result, however, arise due to the fact that seasonal
14
transitions are more rapid in high-latitude environments together with that
larvae enter diapause at low temperatures. Thus, in low-latitude
environments, temperatures change slowly over the year and only rarely
reach below the diapause threshold (Figure 3C). As a consequence, lowlatitude damselflies spend a considerable amount of time growing at lowand intermediate temperatures (e.g. 10-15°C), (Figure 3C), which greatly
increase within-generation variability. At higher latitudes, a considerable
part of the year is spent in diapause, during which time no selection on
growth performance is expected to occur (Figure 3A). When winter is over,
temperatures rise rather rapidly up to about ~15-20°C. As a consequence,
individuals spend much less time at low and intermediate temperatures and
within-generation variability is greatly reduced during the relatively brief
period each year when growth occurs (Figure 3A).
Comparing the TPCs of growth rates of the six species, I found that
thermal breadth decreased with latitude. I was unable to measure thermal
breadth directly as the entire experimental thermal range (16°C - 24°C) was
found to lie within the initial, rising phase of all six species. However, the
differences between species were sufficiently strong that it was clear that
high-latitude species focus their growth to a narrow range of relatively high
temperatures (i.e. thermal specialization), whereas low-latitude species grow
relatively fast over a much broader range of temperatures (i.e. thermal
generalization), with central species being intermediate.
Thus, the
latitudinal pattern of thermal breadth of these species supported the Lynch
& Gabriel (1987) prediction that performance breadth decrease with
decreasing within-generation variation across latitudes. But it is important
to note that the direction of both the predicted and observed pattern of
thermal breadth evolution was not that which may intuitively be expected.
Instead, thermal breadths were narrower in the most thermally
heterogeneous environments. But due to the presence of a larval diapause,
much of this variation may not be of very great importance to the growth of
individual larvae.
PAPER II & III: GROWTH RATES DO
NOT SCALE WITH METABOLISM
In Papers II and III, I show that the slope of the rising phase of TPCs (E) of
growth rate increase with latitude both within and between species, and that
the within-species latitudinal trend in E is maintained despite strong gene
flow. I therefore propose that E is a trait involved in local adaptation. This
15
rejects a key prediction from the Metabolic Theory of Ecology (MTE) (Brown
et al. 2004), that the slope of the rising phase of TPCs should be tightly
constrained by metabolism.
In Paper II, I estimated E (the slope of the relationship between growth
rate and temperature at the Arrhenius scale of -1/kT; see Eq. [1]) for each
full-sib family in Experiment 1. With six species, three latitudes from each
species, three populations from each latitude and about five families from
each population, I was able to quantify variation in E both within and
between species along the full 3,600 km latitudinal gradient. In total, I was
able to estimate E for 209 family-groups, represented by 2924 individuals.
In Paper III, I analyzed microsatellite data (between 7 and 12 loci) from
about 30 adults collected from each of the populations that were used to
estimate variation in E (with the exception of C. scitulum). With these data,
we estimated genetic diversity in each latitudinal population, differentiation
between sub-populations within latitudes, and migration rates between
latitudes.
Results and discussion
I found that the average activation energy of damselfly growth rates was
significantly higher (i.e. the slope of the rising phase of TPCs were steeper)
than the 0.6-0.7 eV range predicted by the MTE. In addition, E varied
considerably both within and between species. The strongest trend was that
temperature-responses became steeper with increasing latitude. In four out
of six species, I found a significant, positive latitudinal trend within species.
Subsequent analyses showed that the best environmental predictors of the
slope of temperature-responses were a positive correlation between E and
temperature seasonality, and a negative correlation with average
temperature during the summer months. The population genetic analyses
revealed that gene flow is strong over much of the ranges of these species
(although the Pyrenees formed a strong barrier to dispersal in C. puella and
C. mercuriale). Clearly, latitudinal differences in E are not a product of
genetic drift. Thus, the slope of the rising phase of TPCs is very likely
involved in how latitudinal populations adapt to local environmental
conditions.
The finding that E varies with latitude has important implications for
several aspects of our understanding of temperature-responses. First, all
damselfly populations that had slopes close to the “universal” value of 0.65
eV where located within the southern range of the latitudinal gradient
(between 35° and 50°N). Coincidentally, this perfectly matches the
latitudinal band where the vast majority of previous research on insect
temperature responses has been carried out (reviewed by Irlich et al.
16
[2009]). Based on this, I suggest that the universal value of 0.65 eV may
simply represent the average value within a restricted geographic area where
the vast majority of researchers work. It is clear that carefully designed,
spatially extensive studies such as mine will be important for gaining a better
understanding of how temperature-responses have evolved in response to
environmental and ecological factors.
The population genetic analyses revealed that migration is asymmetrical
in these species: total migration towards south (i.e. from northern to central,
or from central to southern populations) was higher than total migration
towards north. This could arise if there is a higher propensity to disperse
towards south, although there is no clear reason why this would be the case
here. Instead, it seems likely that migrants going south are more successful
than migrants going north. This may reflect differences in the growth
strategies of “northern“ and “southern” genotypes, elaborated in Paper I
and Paper II. Northern genotypes focus growth to periods of beneficial
conditions, and stop growing relatively early in the season. Southern
genotypes, on the other hand, continue to grow later in the season and
appears to invest more in growing fast over a broader range of temperatures.
A southern strategy in a northern environment may thus be strongly selected
against, as an individual will still attempt to grow under adverse conditions
towards the end of the growth season. A northern strategy in a southern
environment, on the other hand, may be under less strong selection.
Although the northern genotypes will likely grow sub-optimally compared to
locally adapted genotypes because they fail to exploit the full length of the
growth season, this may not translate into increased mortality to the same
extent as when southern genotypes confront high-latitude environments.
PAPER IV: THERMAL PERFORMANCE
SHIFTS DURING ONTOGENY
In Paper IV, I look at how the temperature-dependence of individual
growth rates change over the ontogeny of individual larvae. I contrast this
with information about how the thermal environment differs between larvae
of different age-classes in the field. The aim was to test the hypothesis that
acclimation of temperature-specific growth rates have evolved to allow
individuals to track changes in environmental temperatures during
ontogeny. Few studies have quantified differences between species in the
strength of acclimation responses. Even fewer have considered the
17
environmental factors that may select for strong or weak acclimation
responses.
I modelled the life cycle of damselflies in relation to temperature
variation in the field in order to derive predictions about how the strength of
acclimation depends on changes in the thermal niche among age-classes. In
this model, I bring together two types of phenological information on the
timing of damselfly reproduction. First, I reviewed the zoological literature
for information about the flight periods of Coenagrion sp. in different parts
of Europe. Using this information, I was able to predict the start and end of
the flight period for each species in the area where it was sampled. Second, I
used data from Lowe et al. (2009) on the seasonal timing of egg laying within
the flight season. This revealed that most eggs are laid relatively early during
the flight season. I incorporated this information into a model that I used to
simulate the hatching date of 1000 individuals of each species in the area
where they were sampled. The thermal environment that these indiviudals
would experience during different parts of their life cycle were estimated by
coupling individuals’ hatching dates to temperature data from the FLake
simulations.
I quantified the growth rates of individuals during early (day 0-42),
intermediate (day 42-84) and late (day 84-126) ontogeny using data from
Experiment 1. In organisms with determinate growth, absolute growth rates
decrease with size. To account for this, I used the growth trajectories of the
fastest-growing individuals as a “reference trajectory” in order to calculate
size-corrected growth rates during early, intermediate and late ontogeny. I
quantified the strength of acclimation by assessing how much the slope of
temperature responses changed during ontogeny – if acclimation responses
are strong, individuals will grow almost equally well at all temperatures after
having spent some time at the rearing temperatures (and the slope of
temperature responses will decrease over the ontogeny).
Results and discussion
My main finding were that acclimation responses differed between species.
Acclimation responses were strongest in species inhabiting the least seasonal
environments (i.e. southern European species), with thermally specialized,
north European species displaying the weakest acclimation responses. The
environmental factor that best predicted the strength of acclimation was
whether a species experienced slowly or rapidly changing temperatures
during ontogeny. My interpretation of this is that acclimation may indeed be
important for allowing individuals to track changes in temperature during
ontogeny, but that acclimation responses are costly and that the strength of
acclimation will depend on the relative costs and benefits of acclimating. If
18
acclimation was not costly, we would expect high-latitude species to display
very strong acclimation responses, the opposite to what I found. Thus, as
long as temperatures change slowly (in low-temperate environments),
individuals are able to track changes in temperature by acclimating. These
individuals will be favoured by selection as they can grow better than nonacclimating individuals both immediately following hatching when
temperatures are warm and stable, as well as towards the end of the growth
season when temperatures are lower and more variable. At higher latitudes,
temperatures drop so rapidly in autumn, that acclimating at a sufficient rate
will be exceedingly costly or even physiologically impossible. In addition,
there will be less to gain from acclimating, as less time will be spent at any
given temperature. This is to my knowledge a novel hypothesis about the
strength of acclimation responses that should be further tested in systems
that display greater differences between species in the seasonal timing of
reproduction and growth.
PAPER V: COMPETITION AND
TEMPERATURE MODIFIES GROWTH
RATES
In paper V, I show that intra- and interspecific interactions alters the slope
of temperature-responses. This paper is based on data from Experiment 2.
This study was motivated by recent interest in incorporating information
about the slope of the rising phase of TPCs into predictive models of
ecosystem responses to climate change (Montoya & Raffaelli 2010;
Woodward et al. 2010). Individual growth rates are relevant in this context
as they determine the strength and direction of ecological interactions
(Rudolf 2006; Binzer et al. 2012). They also affect population size structure,
with important implications for community dynamics (De Roos et al. 2003;
Persson & De Roos 2006). Growth rate is a complex trait that depends on
food density, food quality, behavior, size-dependent mortality, metabolism
and respiration, among other factors (Baker 1982; Anholt 1990; McPeek
2004). It is therefore far from certain that differences in growth rates
observed under controlled laboratory experiments are representative of
individuals’ performance under more realistic conditions. To test this, I
reared C. armatum and C. pulchellum in microcosms (30 individuals in 3L
microcosms) at two temperatures, either with members of its own species, or
in equal proportions of both species. The growth patterns of individuals
19
reared under these conditions were contrasted with the results from
Experiment 1.
Results and discussion
I found that temperature responses were steeper when individuals were
reared in the presence of competitors than when reared individually.
Although I was not able to determine the mechanistic basis for this finding, it
clearly demonstrates that it will be very difficult to predict ecosystem
responses to climate change by extrapolating from laboratory experiments of
single species. Growth rates and other complex traits do not simply reflect a
physiological property of an organism at a given temperature. Instead, they
are shaped by trade-offs between many temperature-dependent processes
such as predation rates, attack rates, inference competition, food acquisition,
digestion, respiration and metabolism (Clarke 2003).
I also found that the size structure of larval cohorts were dependent on
both temperature and competion. However, the joint effect of these
processes would not be possible to predict if they were studied in isolation. A
notable finding was that some individuals were able to grow as fast as, or
even faster, at 16°C than at 21°C. This occurred even though the vast
majority of individuals grew considerably slower at the former temperature.
A combination of high food intake rates and high growth efficiency is thus
able to completely overcome the rate-depressing effects of low temperatures.
CONCLUDING REMARKS
To conclude, I found variation in the thermal sensitivity of damselfly growth
rates over multiple levels of biological organization: within and among
species, over individuals’ ontogeny and depending on the ecological context.
My main finding is that the slope of temperature responses increases with
latitude, both within and between species. This has important implications
for our understanding of how temperature affects biological systems, as it
rejects the hypothesis that the slope of the rising phase of TPCs is
fundamentally constrained by metabolism. On the contrary, my findings
revealed that differences in the slope of the rising phase of TPCs can evolve
despite strong gene flow between populations. Based on this, and the results
from several recent reviews (Irlich et al. 2009; Dell et al. 2011; Englund et al.
2011), it is clear that temperature affects biological rate traits in much more
complex ways than what has been widely appreciated. I have highlighted
several aspects of the life history and ecology of damselflies that may
20
generate variation in temperature responses. In order to understand
latitudinal patterns of thermal adaptation, we must clearly investigate the
interacting effects of life history, ecology and environmental variation.
I also found that damselflies become increasingly thermally specialized
(steeper reaction norms) towards higher latitudes. This may reflect that
damselflies spend an increasingly large part of the year in diapause towards
higher latitudes, which results in that growth only takes place during periods
of relatively warm and stable temperatures. Consequently, my findings
support the idea that thermal specialists are favoured when the amount of
within-generation variation is small (Lynch & Gabriel 1987). However, this
shows that we risk to mischaracterize latitudinal temperature clines if we do
not carefully consider the life history of the studied species (Angilletta 2009;
Clusella-Trullas et al. 2011).The fact that food availability, predation and
other important ecological factors also display seasonal fluctuations may
further cause damselflies to focus their growth efforts to periods of relative
warmth. Although I cannot conclusively show that the evolution of a larval
diapause have preceded thermal specialization in this case, these species
appears to conform with the model proposed by Bradshaw and colleagues
(Bradshaw et al. 2000, 2004). This stipulates that organisms first evolve
diapause thresholds that allow them to survive in a novel temperate
environment, followed by changes in thermal sensitivity.
I also highlight the importance of considering the seasonal timing of
major life history events when deriving predictions about thermal
adaptation. In particular, I show how the seasonal timing of reproduction
can have strong effects on the conditions that individual larvae experience
during ontogeny. I find that the rate of change of the thermal niche during
ontogeny may be an important factor for understanding the costs and
benefits of thermal acclimation.
Finally, I show that the inferences we make about how temperature affects
growth rates of damselflies depends on the methodological context.
Temperature-responses were steeper when larvae were able to compete with
other individuals, and species differed in how strong this effect was.
Information on temperature-responses estimated in the laboratory is
currently used to predict ecosystem responses to climate change. My
findings raise questions about how realistic these models are.
I have only scratched the surface of the complex ways in which ecology,
life history and environmental variation shapes the evolution of temperature
responses. My research suggests several fields of inquiry that merits further
attention. In particular, is the timing of reproduction in damselflies shaped
by the thermal requirements of early-instar larvae? Or has the thermal
requirements of larvae evolved to match the environment they experience
due to the flight periods of adults? Similar studies that investigate thermal
sensitivity in different instars in species that differ in the timing of
21
reproduction would be able to answer these questions. It would also be
important to identify the mechanisms that give rise to differences in
temperature responses with or without competition. Investigations of the
effects of temperature on feeding, digestion, predation and several other
traits, both in isolation and in the presence of competitors, would help us
understand how these processes scales with temperature and competition.
By focusing on differences between species in feeding and aggression
behavior it would be possible to find out why one of our species was strongly
affected by competition, whereas the other was not. My work shows that it is
impossible to understand the costs and benefits of growth rates under
realistic conditions without considering the trade-offs between rapid growth
and size structure, survival, development rate and mating success. This will
require a much better understanding of the fitness consequences of
performance. Many optimality models assume that performance affect
fitness either purely additively through fecundity or purely multiplicatively
through survival. This is most likely unrealistic. We should instead focus on
quantifying the contribution of performance to different components of
fitness, such as development time, fecundity, survival and mating success.
This needs to be done across a range of environmental and ecological
conditions. Organisms depend on so many different aspects of their biotic
and abiotic environment, that each display seasonal and diurnal oscillations.
I believe that the best way to gain an understanding of how performance and
species interactions depend on temperature is to simultaneously study as
many aspects of performance and fitness as possible under natural
conditions. Transplantation experiments under near-natural conditions can
provide the much needed realism that allows organisms to display their full
suite of behavioral adaptations, while still allowing researchers to modify
important environmental variables. With this thesis, I hope to have shed
some light on the processes that shape latitudinal patterns of thermal
adaptation in organisms with complex life cycles and where body
temperature is highly or completely dependent on ambient temperatures.
ACKNOWLEDGEMENTS
I would like to thank Frank Johansson and Malin Nilsson for providing
valuable comments on earlier versions of this thesis. The research was
funded by grants from the Swedish Research Council Formas to Viktor
Nilsson-Örtman and Frank Johansson; from the Fund for Scientific
Research-Flanders (FWO) to Marjan De Block; from FWO and the
KULeuven research fund to Robby Stoks; and from Umeå University and the
Academy of Finland to Helena Johansson.
22
AUTHOR CONTRIBUTIONS
Paper I
Viktor Nilsson-Örtman, Robby Stoks and Frank Johansson conceived the
study. VNÖ, RS, FJ and Marjan De Block performed the laboratory
experiment. VNÖ developed the computer model, analyzed data, and wrote
the paper; and RS, MDB, and FJ contributed to writing.
Paper II
Viktor Nilsson-Örtman, Robby Stoks, Marjan De Block, Helena Johansson
and Frank Johansson conceived the study and performed the laboratory
experiment; VNÖ analyzed data, developed the computer models, and wrote
the manuscript; RS, MDB, HJ and FJ contributed to writing.
Paper III
Viktor Nilsson-Örtman, Robby Stoks, Helena Johansson and Frank
Johansson conceived the study and carried out the fieldwork. HJ genotyped
the samples, analyzed the data and wrote the manuscript. FJ, RS and Pär K.
Ingvarsson contributed to writing.
Paper IV
Viktor Nilsson-Örtman, Robby Stoks and Frank Johansson conceived the
study. VNÖ, RS, FJ and Marjan De Block performed the laboratory
experiment. VNÖ analyzed data, developed the computer models, and wrote
the manuscript. FJ contributed to writing.
Paper V
Viktor Nilsson-Örtman , Robby Stoks and Frank Johansson concieved the
study. VNÖ carried out the field work, performed the laboratory experiment,
analyzed data and wrote the paper. FJ contributed to writing.
23
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THANKS
First of all, I wish to thank all the people that made the field work part of this
thesis possible. Either by guiding me to the right sites or helping me in the
field. Before I give any names, I would like to thank everybody who has ever
submitted a sighting to a records database, published a faunistic note,
carried out a survey of their local patch, written a regional atlas, deposited a
specimen in a museum, or in any other way contributed to our knowledge
about the earth’s biodiversity. Thank you, science would be a dark and lonely
place without you.
In Andalucia, a special thanks goes to Florent Prunier – because of you, I am
dying to get back to the Sierra de Cazorla. And thank you Raúl Santos
Quirós, Daniel Grand and José Luis Pérez Bote for pointing me in the
direction of the right people and regions. Thank you Adolfo Cordero-Rivera,
for inspiring me and for helping me through the necessary paperwork. Y
tambien un gran agradecimiento a La Dirección General de Gestión del
Medio Natural, y a la Consejería de Medio Ambiente, Junta de Andalucia.
Estoy muy agradecido.
In Catalonia, I am forever indebted to Oxygastra, the odonate study group of
Catalonia. You are doing an amazing work in documenting the dragonflies
and damselflies of this spectacular region. I cannot fully express my
gratitude towards the García family. Josep, Assumpta, David and Marta –
thank you for your hospitality, invaluable help in the field and for taking me
to the Fogueres de Sant Joan. Your kindness and generousity was
overwhelming. A big thanks also goes to Mike Lockwood for getting me in
contact with these wonderful people and for helping me while in Catalunya.
And thank you Xavier Maynou. The day we spent in Mura and the evening at
your house formed one of the best days of my travels. It was nice to meet
someone that shares my passion for things written in old books.
In France, I would had been completely lost without the help of Cyrille
Deliry, Philippe Lambret, Cedric Vanappelghem and Xavier Houard. Thank
you so much Cedric and Xavier for not only guiding me to some great places
for damselflies, but also to some amazing dining.
I Sverige vill jag särskilt tacka Åke Hedman. Dina kunskaper om Medelpads
trollsländor har varit oersättiga. Tack också till Tommy Karlsson, utan din
hjälp hade jag kanske aldrig lyckats få tag på den gäckande
griptångsflicksländan eller fått se det vackra Appeldalen.
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In my search for phenological data, I am grateful for the help of Vincent J.
Kalkman, Maarten De Groot, Klaus-Jürgen Conze, Holger Hunger, Roberto
Sindaco, Xavier Maynou and the Oxygastra team, David Molina and Ximo
Baixeras in Valencia, Adolfo Cordero-Rivera and Frank Suhling.
In Leuven, I had the best of times when I visited my dear collaborators
Robby and Marjan. I would never had been able to complete this work
without you. Also, I will never forget the night when I saw my first fire
salamander, in the pitch dark and pouring rain in the Meerdaalbos. And
thank you, Lieven and Janne. It was great to hang out at the department
together with you
Thank you Jochen Rodenkirchen for your beautiful photographs.
And a big thanks to Richard Askew and Peder Skou for allowing me to use
the maps from Richard’s book.
TACK
Mest av allt vill jag tacka Frank. Du har varit den bästa handledare jag
kunnat tänka mig. Det första ord jag kommer att tänka på är förtroende.
Oavsett om jag velat lägga ner ett par månader på att gräva efter slovensk
litteratur om trollsländor eller stånga min panna blodig mot någon
obegriplig metereologisk databas så har du alltid litat på mig. Du har alltid
vetat att när tiden väl var mogen, så skulle jag skärpa mig och få saker
gjorda. Och så fort mina irrfärder varit på väg att krascha ner i en mörk grop
så har du funnits där och styrt mig på rätt spår igen genom att prata eller
skriva några kärnfulla meningar som förklarar hur allt hänger ihop. Det, för
mig, är handledning när den är som bäst. Att forska tillsammans med dig har
varit bland det roligaste jag gjort.
Tack Pelle, för att du alltid hjälpt mig när jag kommit instormande på ditt
kontor efter att motvilligt tvingats inse att jag inte klarar allting själv. Jag
önskar bara att jag hade haft vett att utnyttjat dina fantastiska kunskaper
ännu mer.
Och Anders Nilsson! Var ska jag ens börja? Du är en av de viktigaste
orsakerna till att jag över huvud taget vill forska. Ända sedan första kursen
på biologprogrammet har jag sett upp till din ständiga nyfikenhet. Varenda
32
gång jag klivit in på ditt kontor har jag vetat att du hittat någon ny tråd att
nysta i. Jag har heller aldrig mött någon med din känsla för text. Du
behandlar ett korrektur med samma känsla som Guy Clark behandlar sin
gitarr.
Tack Martin för den tid som vi överlappade varandra i forskargruppen. Jag
var verkligen lyckligt lottad som fick dela kontor med dig under denna
känsliga inkuberingstid. Tack för att du gjorde mig peppad på R och
introducerade mig för Zotero – du är en matchmaker av rang.
Helena, det har varit fruktansvärt roligt att göra fältjobb, prata text och
forskning med dig. Jag undrar om jag någonsin kommer att bli så
strukturerad som du.
And also to you, Owen – big thanks for helping me with the writing, and for
keeping me good company at the UFC games
På EMG vill jag annars särskilt tacka Folmer och Göran, för goda samtal om
forskning. Tack Katarina och Stefan för att ni gjort det roligt att vara
fikarummet – och för att ni sett till att jag inte blivit för stor på mig. Tack
Birgitta, Mattias och Ingrid för att ni stått ut med mitt obefintliga minne för
hur man fyller i en blankett.
Och tack så mycket till Szymon, Annelie and Andreas för all hjälp på plan 2!
Szymon, you deserve a whole page of thanks all by yourself. You have been
such a good friend and collaborator throughout these years. I hope you will
be able to do precisely what you want for the rest of your life.
And thank you Melanie for being such a generally awesome person.
Tack till Norrlands Entomologiska Förening för att ni hjälpt mig att behålla
perspektiven på tillvaron. Många skulle kanske säga att mina flicksländor var
obskyra så de räcker och blir över. Men ni i NEF förstår att dessa bara är ett
populistiskt kuttersmycke i kampen om forskningsbidragen, och att det som
verkligen betyder något här i världen är alla slemsvampbaggar, bastflugor,
smalbin, barkgnagare, broksteklar och andra skörvar som förtjänar att
tilltalas vid sina rätta namn. Så tack Andreas, Folke, Sven, Ylva, Roger, Per,
Nils, Benedicte, Sara och Magnus. Och särskilt tack till Johannes och
Anders, som en gång i världen tände gnistan i mig genom att hålla i världens
bästa kurs. Don't let the bastards get you down!
33
En liknande och minst lika viktig roll har Svenska Malaisefälleprojektet
spelat både före och under min doktorandtid. Utan er hade jag inte stått här
idag. Särskilt tack till Kajsa och Dave för att ni trodde på mig! Och tack Julia,
Sibylle, Pelle, Mattias och Svante för en episk sommar. På Naturhistoriska
Riksmuseet vill jag särskilt tacka Kevin och Julio, som inspirerat mig mer än
ni kan ana. Tack också till Niklas, Rasmus, Hege, Bert och Yngve som fått
mig att känna mig välkommen på denna plats som fascinerat mig sedan jag
var barn.
Men jag ska heller inte glömma fåglarna, och öarna. På Stora Fjäderägg vill
jag tacka Lars och Niklas för att ni gav mig en plats att ständigt längta
tillbaka till. Och tack till båtkonsortiet och Johan Forssell för att ni såg till att
Fjäderägg fick konkurrens i form av Holmögadd, Lövöbådan, Svartlass,
Måkläppen och Tärnören. Tack Jocke för alla kortare eller längre turer, i
med- eller motgång, höst eller vår, storm eller stiltje, till stora eller små öar,
och med mycket eller lite fokus på fåglarna. Jag kommer sakna detta mycket.
I Umeå – ni är för många och ni har betytt för mycket för att jag ska kunna
göra det rättvisa här. Jag tänker ta det i någon form av kronologisk ordning,
som ett monument över mina sju år i Umeå. Tack Lovisa för att du fick mig
att vilja flytta till Umeå, och för att jag fick bli din och dina vänners vän. Tack
Anna Östman för att du är ett geni. Kjell Wågberg – jag kommer alltid att
tänka på dig och ditt avundsvärda liv när jag har viktiga beslut att fatta. Tack
Erik och Jenny för att ni alltid haft plats för mig i ert hem och i era liv. Mats
och Ingeborg – tack för att Fågelstigen fick bli som ett andra hem för mig.
Och Stina, Nina, Viktor Wennberg, Johanna Helander, Johanna Eriksson,
Anna Philipsson, Anna Fransson, Kolbjörn, Laura Zagar, Jonas Gidlund och
Ola Norlander – ni är de finaste vännerna som finns. Tack Micke från Lund,
Pernilla Berglund, Maxime, Micke Data, Oskar Franklin, Martina Nygren,
Carl Åkerlund och alla ni som gjort Umeå till en plats där jag bara behövt
lämna lägenheten för att träffa någon som gör mig glad.
Tack Björn för att det var så great att bo med dig, maxa bandbredden, trasha
soffor och lyssna på Slayer, eller bara äta frukost i tystnad. Och tack Erik för
det fina år vi fick bo tillsammans. Tack Smilla för all den värme och ro du gav
varenda dag som jag fick vara med dig.
Tack Pelle, Oscar, Mattias, Anna och Lovisa för kryssfezterna.
Tack Krutröken för sommarkvällarna. Tack Ola och Lotta för värmen både
på och utanför plan.
34
Och Pontus, Ida-Maria, David och Andreas – alla sitcoms på tv är bara bleka
kopior av våra kaffepauser i KBC-fiket.
I Uppsala, Portland och Ottawa – tack Björn för djur-, växt- och
statistikpeppen.
I Stockholm – tack Jörgen och Klara för stughäng, natur- & kultursamtal,
fladdermuslyssning och vinterpromenader. Tack Anthon och Caroline, jag
älskar att komma hem till er och se vad som hänt sedan jag var där senast.
I Göteborg – tack Johan, Hanna, Erik, Helena, Alexander, Jakob och PerAnders för att ni sett till att jag inte behövt ångra mitt beslut att lämna
Umeå. Tack också Linnéa och Per för de första av många (hoppas jag!) road
trips och katthäng. Tack Lovisa för att du alltid står upp för
neanderthalsmänniskornas rättigheter. Och tack Siska för att du räddade
mig från garanterad katastrof under slutfasen av avhandlingsarbetet!
I Åsaka – tack Eva och Åke för att ni är världens snällaste. Jag menar det.
Slutligen tack till min familj. Mamma, Pappa – ni är bäst. Lisa, Fia, Johan,
Jesper, Göran – älskar er. Tova, Sigge, Vega, Lilith – tack för att ni finns.
Och Malin.
35