Download Contributed Paper Interactions between Ecological Traits and Host

Contributed Paper
Interactions between Ecological Traits and Host Plant
Type Explain Distribution Change in Noctuid Moths
NIINA MATTILA,∗ JANNE S. KOTIAHO,∗ † VEIJO KAITALA,‡ ATTE KOMONEN,§
AND JUSSI PÄIVINEN∗∗
∗
Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FI-40014, Finland
†Natural History Museum, University of Jyväskylä, P.O. Box 35, FI-40014, Finland
‡Department of Biological and Environmental Science, University of Helsinki, P.O. Box 65, FI-00014, Finland
§Faculty of Forest Sciences, University of Joensuu, P.O. Box 111, FI-80101, Finland
∗∗
Natural Heritage Services of Metsähallitus, Jyväskylä, P.O. Box 36, FI-40101, Finland
Abstract: The ecological traits of species determine how well a species can withstand threats to which it is
exposed. If these predisposing traits can be identified, species that are most at risk of decline can be identified
and an understanding of the processes behind the declines can be gained. We sought to determine how body
size, specificity of larval host plant, overwintering stage, type of host plant, and the interactions of these
traits are related to the distribution change in noctuid moths. We used data derived from the literature and
analyzed the effects of traits both separately and simultaneously in the same model. When we analyzed
the traits separately, it seemed the most important determinants of distribution change were overwintering
stage and type of host plant. Nevertheless, ecological traits are often correlated and the independent effect
of each trait may not be seen in analyses in which traits are analyzed separately. When we accounted for
other correlated traits, the results were substantially different. Only one trait (body size), but 3 interactions,
explained distribution change. This finding suggests that distribution change is not determined by 1 or 2
traits; rather, the effect of the traits depends on other interacting traits. Such complexity makes it difficult to
understand the processes behind distribution changes and emphasizes the need for basic ecological knowledge
of species. With such basic knowledge, a more accurate picture of the factors causing distribution changes
and increasing risk of extinction might be attainable.
Keywords: distribution change, ecological traits, Lepidoptera, Noctuidae, predictive conservation science
Las Interacciones entre Atributos Ecológicos y Tipo de Planta Huésped Explican el Cambio de Distribución de
Mariposas Nocturnas
Resumen: Los atributos ecológicos de las especies determinan qué tan bien una especie puede resistir las
amenazas a que está expuesta. Si se pueden identificar estos atributos que contribuyen a la predisposición,
las especies que están en mayor riesgo de declinación pueden ser identificadas y los procesos que subyacen
en las declinaciones pueden ser entendidos. Buscamos determinar la relación entre el tamaño corporal, la
especificidad de planta hospedera de larvas, la etapa hibernación, el tipo de planta huésped y las interacciones de estos atributos con el cambio de distribución de mariposas nocturnas de la familia Noctuidae.
Utilizamos datos derivados de la literatura y analizamos los efectos de los atributos, tanto por separado
como simultáneamente, en el mismo modelo. Cuando analizamos los atributos por separado, pareció que los
determinantes del cambio de distribución más importantes fueron la etapa de hibernación y el tipo de planta
huésped. Sin embargo, los atributos ecológicos a menudo están correlacionados y el efecto independiente
de cada atributo puede no ser visto en análisis separados. Cuando consideramos atributos correlacionados,
los resultados fueron sustancialmente diferentes. Solo un atributo (tamaño corporal), pero tres interacciones,
explicaron el cambio de distribución. Este hallazgo sugiere que el cambio de distribución no está determinado
∗ email
[email protected]
Paper submitted May 26, 2008; revised manuscript accepted October 3, 2008.
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Conservation Biology, Volume **, No. *, ***–***
C 2008 Society for Conservation Biology
DOI: 10.1111/j.1523-1739.2008.01138.x
Species’ Ecological Traits and Distribution Change
2
por uno o dos atributos individuales; más bien, el efecto de los atributos depende de otros atributos interrelacionados. Tal complejidad dificulta el entendimiento de los procesos que subyacen en los cambios de
distribución y enfatiza la necesidad de conocer la ecologı́a básica de las especies. Con tal conocimiento básico,
se puede obtener una visión más precisa de los factores que causan cambios en la distribución e incremento
del riesgo de extinción.
Palabras Clave: atributos ecológicos, cambio de distribución, ciencia de conservación predictiva, Lepidoptera,
Noctuidae
Introduction
Understanding the underlying causes of distribution
changes and extinction risk is of vital importance for predictive conservation science (Cardillo et al. 2004; Kotiaho
et al. 2005). Without this understanding, scarce resources
available for management of species may be misallocated.
Because the biology of a species determines how well it
can withstand the threats to which it is exposed (Cardillo
et al. 2004), it is essential to understand the biological
or ecological correlates of distribution changes. If the
predisposing traits can be identified, we may be able to
predict which species are biologically most vulnerable
and hence initiate conservation efforts when their populations are still viable.
A few researchers have identified ecological traits of
species that can predict distribution change (e.g., Conrad et al. 2004; Kotiaho et al. 2005; Mattila et al. 2006).
Nevertheless, even when it seems that some traits are
connected to distribution change, the correct biological
reasons why these traits predispose a species are still unknown. This is because in correlative studies, the trait under the study may not be the cause of the observed effect,
but may be correlated with some other trait that is the actual cause. Unfortunately, the nature of these phenomena
is such that they are not really amenable to manipulative
experiments that would provide a better understanding
of the causative pathways. Because of the potential correlated effects, results may be misinterpreted when trying
to come up with biological explanations for why some
traits have an effect on distribution change. By aiming
at identifying the actual predisposing traits and connecting these to various threats important knowledge can be
gained for use in conservation and management. Nevertheless, it is not always easy to explain these connections
because of the cumulative effects of multiple threats and
interactions between separate threats.
In a previous study we reported on the distribution
decline and on the ecological determinants of extinction
risk and distribution decline in Finnish noctuid moths
(Mattila et al. 2006). Comparable declines among noctuid moths have also been reported from the British Isles
(Conrad et al. 2006). In our previous study we concluded
that many of the ecological traits we studied had effects
on extinction risk, but the only ecological trait that ex-
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plained the distribution change was the overwintering
stage. Nevertheless, the overwintering stage is related to
the type of larval host of macrolepidoptera (Niemelä et al.
1982; Virtanen & Neuvonen 1999), and in this study we
sought to determine the effects of overwintering stage,
body size, specificity of larval host plant, and type of host
plant on the distribution change of noctuid moths.
Methods
Overall, 404 noctuid moth species (Lepidoptera, Noctuidae) occur in Finland (Huldén et al. 2000). We considered the 306 moth species that have a resident or fluctuating population in Finland (Huldén et al. 2000) and
classified them according to their larval host plant (see
later). One hundred sixty-three species had clearly definable host plant types, and we included only these species
in our analyses. We tested ecological traits and host plant
type separately and simultaneously in the same model
to remove the correlated effects of other traits and to
determine possible interactions between the traits.
Distribution Change
In the Atlas of Finnish Macrolepidoptera (Huldén et al.
2000), the distribution of species is given as the number
of occupied 10 × 10 km grid cells in the national coordinate system. In the atlas distribution data are divided
into observations before 1988 and observations between
1988 and 1997. We used the difference in these distributions (number of occupied 10 × 10 km grid cells) to
estimate the distribution change for each species. In all
analyses we expressed the change in relative scale in
percentages such that positive percentages indicate increased distribution and negative values indicate reduced
distributions. Because the atlas covers all reliable observations in the last 250 years, the timescales are unequal,
the earlier being much greater. Nevertheless, there were
more observations recorded during the later period (figure 14 in Huldén et al. 2000). We acknowledge that it
is possible that the inequality of the time periods and
the difference in observation activity may bias the overall
magnitude of the distribution change. Nevertheless, this
bias is unlikely to explain our main findings. We cannot
Mattila et al.
think of any simple mechanism for why the possible bias
should correlate with the ecological traits.
Type of Larval Host Plant and Species-Specific Ecological
Traits
We based type of larval host plant on Huldén et al. (2000).
There were several types of host plants into which only a
few species were classified. To retain even some power
in our analyses, we included only species that used the
3 most abundant and easily demarcated types of host
plants: species feeding on herbs (n = 65), grasses (n =
59), and broadleaved trees (n = 39).
In addition to the overwintering stage, we included
body size (measured as male wing span) and larval–host
plant specificity in our analyses. For some species, there
were no data for some of the traits; thus, sample sizes
varied between the analyses.
We based overwintering stages on the Atlas of Finnish
Macrolepidoptera (Huldén et al. 2000). Overwintering
stages of Finnish noctuid moths are egg, larva, pupa, and
adult. The very few species overwintering as adults were
not included in our analyses. We also excluded species
that overwinter twice or an unspecified number of times
to avoid problems in classifying the overwintering stages.
We derived average body size (wing span) from
Mikkola and Jalas (1977, 1979). Mean body size was that
of 25 individuals. In some rare species, we used measurements from fewer individuals. We arbitrarily decided to
use male size, but this is unlikely to have any effect on
the results because male and female body size correlate
strongly and positively (Pearson correlation, r = 0.98,
n = 163, p < 0.001).
Specificity of larval host plants was classified into 3 categories: monophagous, oligophagous, and polyphagous
species. Monophagous species use only one host plant
species, oligophagous species use plant species in one
genus, and polyphagous species use plant species from
more than one genus. Data on larval host plants were
derived from Mikkola and Jalas (1977, 1979) and Huldén
et al. (2000).
Phylogeny
Closely related species tend to share many characters
through common descent rather than through independent evolution. Thus, statistical methods that treat such
characters as independent may be problematic (Harvey
& Pagel 1991; Harvey & Purvis 1991). The method of
independent contrasts can be used with phylogenetic
information to transform interspecific data into values
that can be analyzed with standard statistical methods
(Harvey & Pagel 1991; Purvis & Rambaut 1995). Nevertheless, if a phylogeny is not properly resolved, as is
the case in noctuid moths, any correction based on it
may be incorrect. Moreover, what is often not recognized is that there are a few rather strict assumptions
3
that must be met before the phylogenetically independent contrasts are in fact phylogenetically independent
(Freckleton 2000). If the assumptions cannot be met, one
cannot rely on the results from phylogenetic corrections.
For these reasons, we derived our results from the original
species data without correcting for phylogeny. Overall,
we are relatively confident our results were not biased
by the current phylogeny. This is because in our previous manuscript on noctuid moths (Mattila et al. 2006),
we applied the method of phylogenetically independent
contrasts (Purvis & Rambaut 1995) whenever it was possible, and in these analyses correcting for phylogeny did
not change the conclusions that were based on the uncorrected analyses.
Statistical Analyses
We used analysis of variance (ANOVA) and linear regression models to analyze the effects of each trait separately. These were followed by pairwise comparisons
(Tukey test). In simultaneous analyses in which the effects of other traits were controlled for, we used analysis
of covariance (ANCOVA). We entered all main effects
and interactions up to 3-way interactions into the model
and then applied a stepwise removal of nonsignificant
interactions. Removal was initiated from the least significant interaction at the highest-order interactions and
removal ceased when the first interaction reached the set
probability level. When there were interactions between
traits, simple-effects tests followed by appropriate pairwise comparisons were used to investigate the interactions in detail. Comparisons became excessively numerous, so to maintain the clarity of presentation, we report
only results for which the probability level was <0.060.
We conducted statistical analyses in SPSS (version 13.0
for Windows; SPSS, Chicago, Illinois).
Critique of Atlas Data
Butterfly atlas data are often criticized because they usually do not include recorder effort. Without this information, observations can accumulate for certain areas
(Dennis et al. 1999). Records of observations are lowest
in areas where the human population is most sparse and
greatest where it is dense (Heath et al. 1984; Dennis &
Williams 1986). Long-term monitoring schemes can also
bias the observed distribution (Pollard & Yates 1993). In
1993 a moth-monitoring scheme was initiated in Finland
(Väisänen 1993). About 100 monitoring locations were
evenly distributed across Finland, which may have a slight
balancing effect if earlier observations were focused on
particular areas. Overall, we believe that in Finland there
are fewer problems with biases in observations than in
many other countries because Finnish legislation includes
a legal concept of "everyman’s right." Everyman’s right allows people right of access to almost any land without
requiring the landowner’s permission. Consequently, it
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Species’ Ecological Traits and Distribution Change
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Table 1. Pairwise comparisons (Tukey test) between overwintering
stages and host types on distribution change of noctuid moths.
Comparison
Mean difference
SE
p
11.47
24.57
13.10
−13.99
−21.81
−7.82
5.37
5.42
4.98
4.93
5.55
5.66
0.085
<0.001
0.025
0.014
<0.001
0.353
Egg–larva
Egg–pupa
Larva–pupa
Herbs–grasses
Herbs–broadleaved trees
Grasses–broadleaved trees
is likely that in Finland observations are more evenly distributed and not accumulated into areas of public use. In
addition, the Lepidoptera fauna of Finland is considered
one of the best known in the world (Lepidopterological Society of Finland 2005). In addition, Finland has a
large number of lepidopterists in proportion to the population (Lepidopterological Society of Finland 2005), and
observation activity has increased over time (Huldén et al.
2000).
An additional complication in the atlas data is that declines are only detected when species are lost from the
entire grid square. There can be several populations of
given species within each square, and a species may have
to decline to a small fraction of its former abundance before declines are noticed on distribution maps (Thomas
& Abery 1995). For this reason, the grid methodology
(e.g., Mattila et al. 2006) is likely to underestimate the
true magnitude of moth declines.
Results
Separate Analyses for Each Trait
Type of host plant was related to distribution change
(ANOVA, F 2,160 = 8.56, p < 0.001, R2 = 0.10). Species
feeding on herbs declined more than species feeding on
trees or grasses, but there was no difference between
species feeding on trees and grasses (Table 1). Overwintering stage also had an effect on distribution change
Table 2. Analysis of covariance of the effects of ecological traits on
distribution change in noctuid moths (R 2 = 0.33).
Source
Overwintering stage
Host plant type
Body size
Larval specificity
Host plant type∗
overwintering stage
Host plant type∗
larval specificity
Overwintering∗
larval specificity
Error
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MS
F
p
η2
2
2
1
2
4
1824.65
1162.09
4894.66
1844.74
2440.54
2.93
1.87
7.86
2.96
3.92
0.057
0.159
0.006
0.055
0.005
0.039
0.025
0.052
0.040
0.099
4
2529.56
4.06
0.004
0.102
4
2288.27
3.67
0.007
0.093
143
622.88
df
Table 3. Number of species in each combination category of larval
specificity and overwintering stage and larval specificity and host plant
type.
Larval
specificity
Monophagous
Oligophagous
Polyphagous
Overwintering
stage, n
egg, 6
larva, 2
pupa, 8
egg, 7
larva, 2
pupa, 4
egg, 31
larva, 57
pupa, 46
Host plant
type, n
herbs, 6
grasses, 6
trees, 4
herbs, 4
grasses, 5
trees, 4
herbs, 55
grasses, 48
trees, 31
(ANOVA, F 2,160 = 10.42, p < 0.001, R2 = 0.12). Pupal
overwinterers declined more than egg or larval overwinterers, but there was no difference between egg and larval
overwinterers (Table 1). Larval specificity and male size
had no effect on distribution change (ANOVA, F 2,160 =
0.03, p = 0.974; linear regression F 1,161 = 1.03, p = 0.312
and slope B = −0.345, SE 0.340, respectively).
Simultaneous Analysis for All Traits
After controlling for the other traits, body size had an
effect on distribution change (Table 2): larger species declined more than smaller ones (B = −0.902 [SE 0.322],
t = −2.803, p = 0.006). Simultaneous analysis revealed
3 significant interactions: host plant type and overwintering stage; type of host plant and larval specificity; and
overwintering stage and larval specificity (Table 2). The
number of species in each trait-combination category is
in Tables 3 and 4.
Type of host plant affected distribution change in larval overwinterers (simple effects test, F 2,143 = 4.131,
p = 0.018) such that species feeding on herbs or on
broadleaved trees declined more than species feeding on
grasses (pairwise comparisons, p = 0.024 and p = 0.038,
respectively).
Overwintering stage affected the distribution change
in species feeding on broadleaved trees (simple effects
test, F 2,143 = 6.110, p = 0.003). Larval and pupal
Table 4. Number of species in each combination category of
overwintering stage and host plant type.
Overwintering stage
Egg
Larva
Pupa
Host plant type, n
herbs, 6
grasses, 18
trees, 20
herbs, 24
grasses, 35
trees, 2
herbs, 35
grasses, 4
trees, 17
Mattila et al.
overwinterers declined more than egg overwinterers
(pairwise comparisons p = 0.005 and p = 0.004, respectively).
Type of host plant had an effect on distribution change
in monophagous species (simple effects test, F 2,143 =
4.236, p = 0.016) such that species feeding on herbs
declined more than species feeding on grasses or on
broadleaved trees (pairwise comparisons p = 0.005 and
p = 0.022, respectively).
Larval specificity had an effect on distribution change
in species feeding on herbs (simple effects test, F 2,143 =
4.468, p = 0.013) and on species feeding on broadleaved
trees (F 2,143 = 4.472, p = 0.013). For species feeding on herbs, monophagous species declined more than
oligophagous or polyphagous species (pairwise comparisons p = 0.006 and p = 0.007, respectively). In species
feeding on broadleaved trees, oligophagous species declined more than monophagous or polyphagous species
(pairwise comparisons p = 0.034 and p = 0.003, respectively).
Overwintering stage had an effect on distribution
change of monophagous (simple effects test, F 2,143 =
3.546, p = 0.031), oligophagous (F 2,143 = 3.554, p =
0.031), and polyphagous (F 2,143 = 8.653, p < 0.001)
species. In monophagous species larval overwinterers
declined more than pupal overwinterers (pairwise comparisons p = 0.009), whereas in oligophagous species,
pupal overwinterers declined more than egg overwinterers (p = 0.009). In polyphagous species larval and pupal overwinterers declined more than egg overwinterers
(pairwise comparisons p = 0.033 and p < 0.001, respectively).
The effect of larval specificity on distribution change
was nearly significant in egg and in larval overwinterers (simple effects test, F 2,143 = 2.912, p = 0.058 and
F 2,143 = 2.919, p = 0.057, respectively) and clearly
significant in pupal overwinterers (simple effects test,
F 2,143 = 6.032, p = 0.003). In egg overwinterers
monophagous species declined more than oligophagous
or polyphagous species (pairwise comparisons p = 0.043
and p = 0.024, respectively). In larval overwinterers
monophagous species declined more than polyphagous
species (pairwise comparisons p = 0.024). In pupal
overwinterers oligophagous species declined more than
monophagous or polyphagous species (pairwise comparisons p = 0.001 and p = 0.045, respectively), and
polyphagous species declined more than monophagous
species (p = 0.011).
Discussion
When we analyzed the traits separately, it seemed that
overwintering stage and type of host plant were both important determinants of the distribution change. The ef-
5
fect of overwintering stage may be connected to climate
change because there is a gradual change of the overwintering stages over a latitudinal gradient (Virtanen &
Neuvonen 1999). Species overwintering as eggs are usually southern species (Virtanen & Neuvonen 1999) that
are limited by the climate and thus may have benefited
from warming climate. On the other hand, the reason
species feeding on trees seem to have succeeded better
may be due to changes in grassland and forest management (e.g., the widespread decrease of open habitats and
afforestation [Mikkola 1997]). Nevertheless, overwintering stage and type of host plant are correlated (Niemelä
et al. 1982; Virtanen & Neuvonen 1999), and these kinds
of correlations among traits may confound conclusions
about their role in influencing the observed changes in
lepidopteran fauna. Thus, traits should also be analyzed
simultaneously to partial out the correlated effects and to
determine the possible interaction effects between the
traits.
When we analyzed all traits in a single model, factors
contributing to the distribution change were much more
complicated than our first analysis led us to believe. Distribution change was not similarly affected by overwintering stage in all host plant types; the role of larval specificity seemed to depend on type of host plant and on
overwintering stage. Indeed, the distribution change was
determined by body size and by 3 interactions: type of
host plant and overwintering stage; type of host plant
and larval specificity; and overwintering stage and larval
specificity.
Type of Host Plant and Overwintering Stage
Among tree-feeding species, egg overwinterers were the
most successful. Warming climate may have increased
the advantage of this trait combination. Species that overwinter as an egg and feed on trees are often not covered
by insulating snow because eggs are laid on trees (Virtanen & Neuvonen 1999). Without insulating snow cover
these species are more prone to climatic variations and
may thus benefit from warming climate, whereas thinning snow cover may decrease the overwintering success
of pupae and larvae, stages that are usually covered by
snow. Egg overwinterers tend to fly late in the summer
or in the autumn, and warmer weather during autumns
may benefit these species when adults have a longer time
to reproduce and disperse. Egg overwinterers may also
be advantaged by warmer springs because species that
lay their eggs on trees do not lose contact with their host
plants and are ready to feed in the spring when leaves
start to develop.
Among larval overwinterers, type of host plant had an
effect such that species feeding on grasses declined the
least. There were only 2 larval overwinterers that feed on
trees in the data set, so the difference between species
feeding on trees and on grass was not necessarily general.
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The difference in distribution change among larval overwinterers that feed on herbs and on grass might be related to the unequal decline of herbs and grasses caused
by changes in land use (Mikkola 1997). Why this is not
shown among other overwintering stages is a question
that requires further attention.
Host Plant Type and Larval Specificity
In polyphagous species it seemed that type of host plant
type was not important because all polyphagous species
succeeded quite well, whereas in monophagous species
those feeding on herbs declined the most. This may again
be explained by changes in land use because herbs have
suffered especially from changes in land use (Mikkola
1997). Being dependent on only one host plant makes
species more prone to extinction (Koh et al. 2004; Kotiaho et al. 2005; Mattila et al. 2006), and stability of resource availability affects extinction risk of moth populations (Nieminen 1996). Herbs and grasses are more likely
to suffer from instability than large, more tolerant, and
deep-rooted trees. It is also predicted that the abundance
of deciduous trees increases as climate warms (Kuusisto
et al. 1996).
Larval specificity is also connected to dispersal ability (Warren et al. 2001) and monophagous moth species
have been reported to have lower migration rates than
oligophagous or polyphagous species (Nieminen et al.
1999). In addition, dispersal ability can be an important
factor in distribution change, but unfortunately data on
dispersal ability of noctuid moths are not available. In
butterflies the general trend seems to be that mobile generalist species are increasing (Warren et al. 2001; Kotiaho
et al. 2005), and this same pattern may be true in noctuid
moths as well.
Overwintering Stage and Larval Specificity
In oligophagous and polyphagous species egg overwinterers fared best, whereas in monophagous species egg
overwinterers declined the most. We have no comprehensive explanation for these results, but overwintering
as an egg is a southern adaptation (Virtanen & Neuvonen
1999) and southern species at the edge of their distribution may have an ability to track the warming climate.
Polyphagous and oligophagous species have better dispersal ability (Warren et al. 2001; Komonen et al. 2004)
and use a wider array of resources because they feed
on several species. These facts may explain the better
success of polyphagous and oligophagous species.
Body Size
Larger-sized moths were predisposed to distribution decline. This effect was revealed only when analyzed simultaneously with the other traits. It is generally assumed
that large species are more sensitive to habitat fragmentation because of greater space use and food-resource re-
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quirements (Cyr 2000), but this assumption ignores the
fact that large species may also, because of their higher
mobility (Komonen et al. 2004), be able to use multiple
patches (Hambäck et al. 2007). Therefore, small and large
species may be affected by different aspects of fragmentation: small species may be most affected by the path size
reduction, whereas large species may be more affected
by the total amount of suitable habitat in the landscape
(Hämbäck et al. 2007). Body size is connected to specificity of larval host plant in geometrid and noctuid moths,
and more specialized species are smaller (Niemelä et al.
1981; Lindström et al. 1994). This may lead to the conclusion that smaller size predisposes moths to distribution
decline. Nevertheless, when the effect of larval specificity
was removed, the result was just the opposite; larger size
actually predisposed a group to distribution decline.
Conclusions
When the traits of noctuid moths were analyzed separately, overwintering stage and type of host plant affected
distribution change. Nevertheless, when we analyzed the
traits simultaneously, interesting interactions were revealed and body size predicted distribution change. This
suggests that distribution change is not determined by
only a single trait and that the effect of certain traits
may depend on the other interacting traits. Such complexity makes it difficult to understand the processes behind distribution changes and emphasizes the need for
basic ecological knowledge of species. With such basic
knowledge, a more accurate picture of the factors causing distribution changes and risk of extinction may be
attainable.
Acknowledgments
We thank the "Monday coffee club" members, M. Luoto, and 2 anonymous referees for their valuable comments on the manuscript. This study was supported by
the Academy of Finland and by the Center of Excellence
in Evolutionary Research.
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