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The lost generation hypothesis: could climate change drive ectotherms into a
developmental trap?
Hans Van Dyck1, Dries Bonte2, Rik Puls2, Karl Gotthard3 and Dirk Maes4
1Behavioural Ecology & Conservation Group, Earth and Life Institute, Université catholique de Louvain
(UCL), Louvain-la-Neuve, Belgium – 2Terrestrial Ecology Unit, Department of Biology, Ghent
University, Ghent, Belgium – 3Department of Zoology, Stockholm University, Sweden – 4Research
Institute for Nature and Forest (INBO), Brussels, Belgium
Corresponding author: Hans Van Dyck ([email protected])
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Abstract:
Climate warming affects the rate and timing of the development in ectothermic organisms. Short-
living, ectothermic organisms (including many insects) showing thermal plasticity in life-cycle
regulation could, for example, increase the number of generations per year under warmer
conditions. However, changed phenology may challenge the way organisms in temperate climates
deal with the available thermal time window at the end of summer. Although adaptive plasticity is
widely assumed in multivoltine organisms, rapid environmental change could blur the relationship
between the environmental cues that organisms use to make developmental decisions.
Developmental traps are scenarios in which rapid environmental change triggers organisms to
pursue maladaptive developmental pathways. This occurs because organisms must rely upon current
environmental cues to predict future environmental conditions and corresponds to a novel case of
ecological or evolutionary traps. Examples of introduced, invasive species are congruent with this
hypothesis. Based on preliminary experiments, we argue that the dramatic declines of the Wall
Brown (Lasiommata megera) in NW Europe may be an example of a developmental trap. This
formerly widespread, bivoltine (or even multivoltine) butterfly has become a conundrum to
conservationist biologists. A split-brood field experiment with L. megera indeed suggests issues with
life-cycle regulation decisions at the end of summer. In areas where the species went extinct
recently, 100% of the individuals developed directly into a third generation without larval diapause,
whereas only 42.5% did so in the areas where the species still occurs. Under unfavourable autumn
conditions, the attempted third generation will result in high mortality and eventually a lost or
‘suicidal’ third generation in this insect with non-overlapping, discrete generations. We discuss the
idea of a developmental trap within an integrated framework for assessing the vulnerability of
species to climate change.
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Introduction: climate change and phenology
For a wide range of taxonomic groups, there is ample evidence of the impacts of global warming on
their occurrence in both space and time (e.g. Parmesan 2007). The most widely documented
responses since the early days of climate change research involve phenological shifts (Angilletta
2009). Phenology is the temporal dimension of an organism’s natural history as it captures the timing
of the life cycle over the year (i.e. when it will develop, reproduce and enter dormancy). As a result,
phenology is a major structuring element of an organism’s ecology and evolution (Forrest and Miller-
Rushing 2010). In temperate and boreo-artic regions, the timing of particular life cycle stages and
phenomena is essential for an organism’s fitness.
The observed phenological patterns in plants and animals in response to global warming are
generally congruent with an earlier spring and a prolongation of the favourable period of the year for
growth and reproduction (Parmesan and Yohe 2003; Menzel et al. 2006). In principle, this can be the
result of genetic changes by natural selection (G), plastic responses (E) or genetic changes in reaction
norms (GxE). In some cases, there is evidence of additive genetic variation for phenology-related
traits (Van Asch et al. 2007). Thermally-sensitive traits that affect phenology, including for example
growth rate and development time, may also be influenced by interaction effects between genes and
the environment (Barton et al. 2014). So far, the majority of documented responses to climate
change appear to be examples of phenotypic plasticity (Gienapp et al. 2008; Valtonen et al. 2011;
Schilthuizen and Kellermann 2013). Plastic responses require, however, reliable environmental cues
to provoke a phenotypic response (Reed et al. 2010).
Changes in phenology can be either adaptive or maladaptive. Evolutionary biologists are usually not
very excited about maladaptive plasticity as selection will wipe it out, but from a population
dynamics viewpoint, maladaptive phenology may have significant short-term consequences for
population abundance under novel conditions. Hence, it can be a factor of significance for
conservation under climate change in addition to other factors including: i) the shrinking of
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populations of cold-adapted species (Turlure et al. 2010), ii) local extinctions due to extreme weather
conditions (e.g. McLaughlin et al. 2002), and iii) phenological mismatches between resources and
consumer (Saino et al. 2011; Nakazawa and Doi 2012). Adaptive responses to seasonal environments
have received much attention and stimulated the construction of several life history models of
optimal growth and development (Gotthard 2008), but the potential of maladaptive temporal
responses should not be ignored under altered organism-environment interactions under climate
change.
Short-living, ectothermic organisms, such as many insects, are of particular interest in this context.
Both their larval development and adult activities are strongly sensitive to climatic conditions.
Moreover, as they are short-lived with often one or more generations per year, changing climatic
conditions may have considerable impact on their life-cycle regulation. Insects can take advantage of
an early start in spring, as they may experience an extended time horizon for development and
reproduction under changed thermal conditions (e.g. Végvári et al. 2014). This, in turn, may provide
opportunities for an increase in the number of generations per year (i.e. voltinism; Altermatt 2010).
This issue has particularly attracted attention in applied entomology as several pest species of crops
and tree stands can have pronounced negative impacts if they occur with multiple generations per
year and grow above economically significant thresholds (Ge et al. 2005; Tobin et al. 2008). Although
patterns of earlier appearances and an increase in voltinism have been documented in a number of
species, there is still much to learn about the mechanisms causing adaptive responses, but also about
those cases where there is a lack of adaptive response.
Changed phenology is typically expressed in a human-biased way using calendar date. However,
what really matters for the development and life cycle regulation of ectothermic organisms is how
calendar date relates to ‘thermal time windows’ or degree-days. Degree-days provide an
accumulated energetic measure relevant for the development and growth of the focal species based
on the sum of mean daily temperatures above a given threshold from a meaningful starting date till
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the phenological event of interest (Trudgill et al. 2005). As phenology determines the set of
environmental conditions experienced at a particular stage of the life cycle (e.g. specific degree-days
thresholds), it may in turn affect decision making by organisms as they rely upon environmental cues
and internal response systems that were functional in their evolutionary history.
The field of cue-response systems and maladaptive behaviour that leads to ecological and
evolutionary traps under human-induced rapid environmental change has attracted much attention
the last decade (Robertson et al. 2013). So far, most studies in this field have dealt with maladaptive
habitat and resource use in anthropogenic environments, although the significance of ecological
novelty and the potential emergence of traps in a context of climate change and shifts in timing have
been acknowledged in the recent literature (Sih et al. 2011). To the best of our knowledge, we are
not aware of studies dealing explicitly with developmental traps under climate change that fool
organisms to make erroneous decisions during development because of altered cue accuracy. For
example, a developmental trap could occur when a larval insect, which relies upon environmental
cues for winter diapause induction, interprets novel climatic conditions as suitable for direct
development. However, if the climatic conditions strongly deteriorate before development is
completed, this generation will likely be lost (Fig. 1). In many (potentially) multivoltine insects, life-
cycle regulation is mainly based on the photoperiod experienced during key phases of the
development (Friberg et al. 2011). We may expect that the information on seasonal change –
conveyed by the photoperiod – is blurred by rapid warming. Some studies presented in different
frameworks (e.g. invasive species) are highly relevant to this issue, as we will discuss below.
In this paper, we outline the potential significance of the developmental trap concept for short-living
ectothermic organisms. We focus on diapause induction at the end of the season under temperate-
zone conditions when such organisms have to decide on adding another generation within the same
growing season, or alternatively, entering a developmental pathway of arrested development. So far,
most phenology-related work has focused on early-season phenology, but there is a need for late-
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season studies to better understand population consequences (Karlsson 2014). Whilst the dominant
diapause-inducing cue (photoperiod) will be unaffected by global climate change, higher
temperatures may modify rates of development, leading to a decoupling of synchrony between
diapause-sensitive life-cycle stages and critical photoperiods for diapause induction (Bale & Hayward
2010). We were particularly inspired by the case of the Wall Brown butterfly, Lasiommata megera.
This butterfly used to be widespread, but over the last few decades it has shown a dramatic decline
in NW Europe (Van Dyck et al. 2009). Based on the literature and on results from an exploratory
translocation experiment, we infer the possibility of a developmental trap in L. megera as an
explanation of its regional population decline and we discuss the broader relevance of such a
phenomenon for species showing developmental plasticity and multivoltinism in combination with
altered phenology under changing environmental conditions.
Range dynamics, climate change and maladaptive decisions
One convincingly demonstrated consequence of climate change is range shift and pole ward
expansion (Parmesan and Yohe 2003; Hickling et al. 2006). However, it is also expected that there
will be interactions between climate change and latitudinal clines in phenology and life-cycle
regulation (Bradshaw and Holzapfel 2001; Välimäki et al. 2012). Southern genotypes that disperse
northwards could be considered as being pre-adapted to “northern” conditions under climate
change. However, these southern types could in principle have their range expansion restricted by
developmental traps. For example, in laboratory and field experiments, Dalin et al. (2010)
demonstrated latitudinal variation in how the chrysomelid beetle responded to day length for
diapause induction and how the responses affected insect voltinism across the introduced range. This
beetle, which was introduced for biocontrol, failed to establish south of 38 N latitude because of a
mismatched critical daylength response for diapause induction. Likewise, developmental mismatches
may have the potential to restrict range-expansion in response to climate change.
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Phenological adaptations in insects have led to well-developed theoretical perspectives on optimizing
development time and body size in a seasonal environment along latitudinal clines (e.g. clinal “saw-
tooth” pattern; Roff 1980; Nylin & Svärd 1991). Theory predicts different patterns for univoltine and
bivoltine life cycles and season length, which may result in complex latitudinal patterns for life history
traits and size. However, latitude is not always a good predictor. In recent work on the voltinism,
body size and temperature in North American Papilio butterflies, it was shown that latitude is not
always a good predictor of population responses due to the existence of local “climatic cold pockets”.
Temperatures in northern Michigan and Wisconsin appeared to have historically strong body size
constraints, but this has rapidly changed during the recent decade with local summer warming
(Scriber et al. 2014). According to the authors, the effects on body size are most likely a result of
phenotypic plasticity. Climate change is likely to induce altered eco-evolutionary dynamics across the
range of many insects. Southern genotypes that disperse northwards could be considered as being
pre-adapted to “northern” conditions under climate change, but these southern types could in
principle face problems with interpreting local environmental cues (e.g. photoperiod) to make
appropriate decisions on life-cycle regulation including late summer diapause induction.
The question of how range-shift and developmental traps may interact is further confounded by the
fact that a species may have populations that differ in phenology and voltinism within the same
region (e.g. Krumm et al. 2008). For example, in in those areas where the butterfly Pieris napi on the
British Isles has a second and third brood; , a significant part of the pupae derived from the spring
generation are diapause pupae and do not develop into butterflies until the following year (Lees &
Archer 1980). Such a pattern could be the result of multiple colonization events from different source
regions with different phenological profiles, or of phenologically aberrant sub-populations with
unusual local topographies and hence microclimates (Shapiro 1975). Another reason for the co-
existence of different developmental profiles and phenologies could be bet-hedging (Danforth 1999).
Hence, the picture of one species-specific phenological type in one particular area may hardly do
justice to the complex situation which prevails for several multivoltine species.
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The first step towards predicting voltinism changes and the potential for developmental traps in
response to climate change is to understand the evolution of these characteristics. Insects indeed
show great diversity in their life styles, including diapause induction, and similar responses among
species or populations might be the result of convergent evolution but through different mechanisms
(Masaki 1999). Therefore, more case studies are needed to better understand the processes that
lead to specific phenological responses and their consequences for life-cycle regulation (e.g. diapause
induction) under climate change. In this case, zones of transition between different levels of
voltinism are of particular interest (Nylin and Svard 1991). Although adaptive plasticity is widely
assumed in multivoltine organisms, human-induced rapid environmental change could blur the
relationship between the environmental cues organisms use to make developmental decisions on
the one hand and the anticipated state of the environment on the other. This, in turn, opens the
possibility of a developmental trap making organisms opt for a low fitness developmental pathway
relative to the prevailing environmental conditions. The key point is that changed phenology may
challenge the way ectotherms deal with the available time horizon for development and
reproduction at the end of the summer season, which in turn may result in high mortality.
Parallels with invasive, introduced species
Both climate change and biological invasions involve the ability of organisms to deal with new
environmental conditions outside the range experienced in the population of origin. While the fields
of climate change and biological invasions have largely developed independently (Ward and Masters
2007), researchers interested in climate change effects are likely to get insights and ideas from
studies on introduced pest species.
An analogue to the climate change induced ‘developmental trap’ is the situation in which an invading
species produces a mismatched number of generations due to cue responses evolved under the
selection regime of the area of origin (the ghost of selection past). For example, during the early
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stages of range expansion in Japan, the green stink bug Nezara viridula induced diapause much later
than local native species, resulting in significant reproductive losses (Musolin 2007). As another
example, the weevil species Hyperodes bonariensis native to South America was introduced in New
Zealand where it continued to show a ‘relic diapause’, which was maladaptive under the new
environmental conditions (Goldson and Emberson 1980).
Developmental traps may also occur in conjunction with more complicated interactions with the
biotic environment. For example, the
cotton bollworm (Helicoverpa armigera), a major pest species, has been shown to produce a fifth
generation in northern China that ultimately resulted in a suicidal generation. In this case however,
the proportion that did so varied with host crop (Ge et al. 2005).
Changes in voltinism may also interact with other life-history traits of the organism. Far example, the
introduction of the fall webworm Hyphantria cunea in Japan resulted in a part of the colonized range
into a shift to a trivoltine life style. Voltinism in the webworm, however, is related to the number of
instar-stages during development, which is in turn correlated with developmental period, pupal
weight, and forewing length (Gomi et al. 2003).
Developmental trap hypothesis and a butterfly under dramatic decline
Butterflies are popular study organisms for ecology, evolution and conservation (Watt and Boggs
2003). Also in the context of responses to weather and climate change, they attracted much
attention over the last decades (e.g. Dennis and Shreeve 1991; Roy and Sparks 2000). Butterflies are
also the subject of well-established recording schemes providing useful spatial and temporal datasets
on change in abundance and occurrence (Forister and Shapiro 2003; van Swaay et al. 2008).
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Moreover, their life styles strongly relate to the thermal dimension of the environment in time and
space as they are flying, sun-basking organisms in the adult stage and usually less mobile ectotherms
in the larval stages (e.g. Clench 1966; Dennis 1993; Kingsolver 1989; Bryant et al. 2000). Several
butterfly studies addressed phenological shifts (e.g. Stefanescu et al. 2003; Diamond et al. 2011), but
whether the concept of a developmental trap is applicable remains to be analyzed.
In this context, we are particularly interested by the case of the Wall Brown butterfly Lasiommata
megera (Linnaeus, 1767). This widespread grassland butterfly has become a conundrum to
conservation biologists. Although the species used to be abundant and widespread across its
European range, it has declined dramatically over the last few decades both in distribution and
abundance in NW Europe, even reaching levels of conservation concern in some areas (Van Dyck et
al. 2009; Maes et al. 2012). Populations of L. megera in northern and southern Europe are, however,
stable and sometimes even expanding (van Swaay et al. 2013). The population decline in NW-Europe
(i.e., Belgium, The Netherlands and The UK) appears to show a typical spatial pattern; inland
populations showed the strongest declines (resulting in several currently L. megera free areas,
whereas it used to be one of the most widespread and stable species until the early 1990s), but
populations close to the seaside are still surviving. Although L. megera has experienced habitat loss
and wild flower declines in different types of grassland in landscapes under intense human use
(WallisDeVries et al. 2012), the dramatic decline and the typical spatial pattern of the response is not,
or far less, reflected in other butterflies susceptible to similar habitat and resource issues (e.g. Small
Heath Coenonympha pamphilus; Maes et al. 2012). Therefore, conservation biologists are in search
of a sound explanation for its strong and rapid decline.
We argue that L. megera has the biological profile of a candidate species for experiencing a
developmental trap. The species overwinters as a half-grown caterpillar (3rd instar), and the decision
to develop directly into a third generation, or alternatively to diapause, is made as a young larva
(before the 3rd instar, although the exact time window of sensitivity is not yet known). In the
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northern part of its range, the species is bivoltine and to the south and southeast of Europe it occurs
in 3 or 4 overlapping generations even in intensively farmed areas (e.g. Slovenia; Verovnik et al.
2012; Fig. 1). Intriguingly and opposite to related satyrine butterflies (e.g. Pararge aegeria; Nylin et
al. 1989), univoltine populations are not known in L. megera. Hence, in northern Europe it only
occurs in areas where it is able to complete two generations (Nylin and Svärd 1991). This suggests
that it has lost the (genetic) ability of a univoltine life cycle that would require inducing larval
diapause even if environmental conditions still remain suitable for a certain time period. This implies
a major difference in life history with the very closely related species L. maera, which is univoltine in
Sweden, but bivoltine further south (Gotthard et al. 1999). Developmental decisions in response to
day length depend in this species on the seasonal state of the larvae. The relationship between
growth rate and temperature of L. maera was found to be highly dependent on the level of time-
stress resulting from the day-length regime (Gotthard et al. 2000).
We will focus on three lines of circumstantial evidence that regional warming may affect late summer
diapause induction in L. megera in NW Europe. In this region, L. megera always occurs in two
generations per year, but in warm summers a partial third generation may occur. Comparing the
phenology patterns of the period 1981-2000 and 2001-2010 in Belgium indicated an overall increased
occurrence of the third generation (Maes et al. 2013). However, the pattern differs between the
inland area, where L. megera has disappeared, and the coastal area, where it still occurs (Fig. 2). ??
The third generation has become bigger in the period 2001-2010 than in the period 1980-2000 in the
coastal population and has become much longer in the inland populations in the recent period. The
third generation in the phenology figure of the inland populations is “blurred”? by the gradual
extinction of the local populations??
In a split-brood breeding experiment in the field, we tested whether developmental decisions are
different in the areas where populations have disappeared (i.e. inland area) and in areas where
populations still occur (i.e. coastal area). At the time of the second generation (i.e. summer
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generation), we introduced a total of 253 young caterpillars of L. megera into four different Belgian
sites (two inland sites and two coastal sites) where they could grow and develop on potted host grass
(greenhouse-reared Festuca rubra) in individual enclosures. The sites were at similar latitude
(between 51°07’ and 51°21’), but the two inland sites were located c. 140 km to the east compared
to the coastal sites. Interestingly, 100% of the caterpillars in the inland sites developed directly to the
adult stage (i.e., a third generation), whereas only 42.5% of the conspecifics in the coastal sites did
so.
In order to explore potential cues for developmental decisions in L. megera, we analyzed ambient
temperatures during the period in which the second generation offspring are still small caterpillars in
both regions (i.e. August-September). Photoperiod was obviously not different between the areas,
but temperature clearly was. During the experiment, ambient temperature was on average 0.5°C
warmer on the inland sites compared to the coastal sites. However, this difference was much
stronger at the level of the caterpillars on the host plants (i.e., 5 cm above ground-level the inland
sites were on average 1.2°C warmer than the coastal sites; data logger measurements i-buttons).
Over the last 30 years, daily temperature during the period of the second (and third) generation
increased and has been significantly warmer in the inland sites than in the coast sites (Maes D. & Van
Dyck H., unpubl. data based on meteorological records). Most climate change studies rely on general
ambient temperature data, but these do not necessarily reflect operational temperatures in relevant
microhabitats and climates of insects (Bennie et al. 2014).
Although these observations do not provide a ‘smoking gun’ for a developmental trap in L. megera,
they are congruent with the hypothesis. Our split-brood field experiment suggests problems with life
cycle regulation decisions at the end of summer in areas where the species went extinct, but much
less so in areas where populations still occur. In the former areas, all individuals developed directly
without going into larval diapause. If direct development in autumn is a bad option – at least in some
years – such a developmental trap may lead to a ‘suicidal’ third generation. This, in turn, will have
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strong population consequences affecting the abundance of the species in the next spring generation
as we are in a scenario of non-overlapping, discrete generations. In such cases, the long-term
population growth rate is determined by its geometric mean and unusual low values will have a
strong impact on persistence. In some insects, there is a developmental buffer against seasonal
variability caused by within-population variation in diapause induction. Our working hypothesis for L.
megera in NW Europe states that changed thermal conditions in the inland populations have created
a mismatch between the seasonal cue and the diapause induction response, whereas this effect is
less severe in the populations closer to the seaside which were less exposed to warming effects.
Given the magnitude of the effect, as suggested by our field experiment, inland populations could
only be rescued by recolonisation by pre-adapted genotypes, or types on which natural selection can
adjust the reaction norms of the developmental response. Interestingly, northern genotypes would
be the best to rescue these L. megera populations as they have adapted to enter diapause at longer
day lengths. It is now warranted to start a detailed research program on the environmental cues
(combinations of photoperiod and temperature) and responses of different populations of L. megera,
including transplant experiment, to test these ideas. Of course, the idea of developmental trap does
not exclude the additional or synergetic role of other environmental factors to explain the dramatic
decline of L. megera in NW-Europe.
Conclusion and perspectives
Several studies on the ecological responses of climate change have addressed patterns of
phenological change. Although there is clear evidence for some general patterns, including earlier
first appearance and increased voltinism, in short-living ectothermic organisms such as insects, there
is still much to learn about the diversity of mechanisms or processes that cause (mal)adaptive
responses. If the relationship between environmental cues and the developmental response is
blurred under ‘novel’ seasonal conditions, it opens the possibility of a developmental trap. We argue
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that this field needs more attention and studies on phenology and development of species that have
been introduced outside their range and climatic space help developing ideas.
In lowland areas, the requirement to move larger distances to track climate, especially if combined
with dispersal limitation due to habitat fragmentation, can cause a lag in the response to new
climatic conditions (Moritz & Agudo 2013). The phenomenon of a developmental trap may also open
a new perspective on climate debt effects (i.e. limited ability of organisms to track rapid climate
change; Travis et al. 2013) within the core of the distribution range of certain species. Climate debt
has been shown in, for example birds and butterflies, at the northern edge of their range (Devictor et
al. 2012). If populations in transition zones between different degrees of voltinism are trapped, then
it could create – at least temporarily – holes in the distribution of such a species.
At this stage, it is difficult to make sound predictions on the general significance of developmental
traps across species and climate zones. Under variable conditions the co-occurrence of different
developmental patterns within a generation may provide resilience at the population level (Pavan et
al 2013). We argue that the profile of species particularly susceptible to developmental trapping are
multivoltine species that show strong thermal plasticity of development and use photoperiod as an
important cue for life-cycle regulation. Of course, the vulnerability of species to this process is always
determined by a combination of exposure and intrinsic sensitivity (Williams et al. 2008). More
generally, our forum paper calls for putting more emphasis on sensory ecology (cue-response
system) in the field of the ecology and evolution of phenology. Integrating life-history theory,
developmental biology, biogeography and climate research by focusing on developmental traps
provides an exciting scope for integrative biology that will help to better understand the mechanisms
of the diverse temporal and ultimately population impacts of climate change.
Acknowledgements
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We thank Nadiah Kristensen, Tom Oliver and an anonymous referee for comments that helped
improve the manuscript. This research was supported by research grant ARC no. 10/15-031 to HVD,
PAI-IUAP research grant ‘Speedy’ (PAI grant no. P7/04) to HVD and DB, and the strategic research
programme EkoKlim at Stockholm University to KG. This is publication BRC XX of the Biodiversity
Research Centre (Earth and Life Institute, UCL, Louvain-la-Neuve).
References
Altermatt, F. 2010. Climatic warming increases voltinism in European butterflies and moths. – Proc. R.
Soc. B 277: 1281-1287.
Angiletta, M. J. Jr. 2009. Thermal Adaptation. A Theoretical and Empirical Synthesis. – Oxford Univ.
Press.
Bale, J. S. and Hayward, S. A. L. 2010. Insect overwintering in a changing climate. – J. Exper. Biol. 213:
980-994.
Barton, M. et al. 2014. Co-gradient variation in growth rate and development time of a broadly
distributed butterfly. – PLoS ONE 9: e95258.
Bennie, J. et al. 2014. Seeing the woods for the trees – when is microclimate important in species
distribution models? – Glob. Change Biol. 20: 2699–2700.
Bradshaw, W. E. and Holzapfel, C. M. 2001. Genetic shift in photoperiodic response correlated with
global warming. – Proc. Natl. Acad. Sci. USA 98: 14509-14511.
Bryant, S. R. et al. 2000. Thermal ecology of gregarious and solitary nettle-feeding butterfly larvae. –
Oecologia 122: 1-10.
Clench, H. K. 1966. Behavioral thermoregulation in butterflies. – Ecology 47: 1021-1034.
15
336
337
338
339
340
341
342
343
344
345
346
347
348
349
350
351
352
353
354
355
356
357
2930
Dalin, P. et al. 2010. Seasonal adaptations to day length in ecotypes of Diorhabda spp. (Coleoptera:
Chrysomelidae) inform selection of agents against Saltcedars (Tamarix spp.). – Environ. Entomol. 39:
1666-1675.
Danforth, B. N. 1999. Emergence dynamics and bet hedging in a desert bee, Perdita portalis. – Proc.
R. Soc. (B) 266: 1985-1994.
Dennis, R. L.H. 1993. Butterflies and climate change. – Manchester Univ. Press, Manchester.
Dennis, R. L. H. and Shreeve, T. G. 1991. Climatic change and the British butterfly fauna: opportunities
and constraints. – Biol. Conserv. 55: 1-16.
Devictor, V. et al. 2012. Differences in the climatic debts of birds and butterflies at a continental
scale. – Nature Clim. Change 2: 121-124.
Diamond, S. E., et al. 2011. Species’ traits predict phenological responses to climate change in
butterflies. – Ecology 92: 1005-1012.
Forrest, J. and Miller-Rushing, A. J. 2010. Toward a synthetic understanding of the role of phenology
in ecology and evolution. – Phil. Trans. R. Soc. (B) 365: 3101-3112.
Forister, M. L. and Shapiro, A. M. 2003. Climatic trends and advancing spring flight of butterflies in
lowland California. – Glob. Change Biol. 9: 1130-1135.
Friberg, M. et al. 2011. Asymmetric life-history decision-making in butterfly larva. – Oecologia 165:
301-310.
Ge, F. et al. 2005. Quantification of diapausing fourth generation and suicidal fifth generation cotton
bollworm, Helicoverpa armigera, in cotton and corn in northern China. – Entomol. Exper. Appl. 116:
1-7.
16
358
359
360
361
362
363
364
365
366
367
368
369
370
371
372
373
374
375
376
377
378
3132
Gienapp, P. et al. 2008. Climate change and evolution: disentangling environmental and genetic
responses. – Molec. Ecol. 17: 167–178.
Goldson, S. L. and Emberson, R. M. 1980. Relict diapause in an introduced weevil in New Zealand. –
Nature 286: 489-490.
Gomi, T. et al. 2003. Local divergence in developmental traits within a trivoltine area of Hyphantria
cunea Drury (Lepidoptera: Arctiidae). – Entomol. Science 6: 71–75.
Gotthard, K. 2008. Adaptive growth decisions in butterflies. – BioScience 58: 222-230.
Gotthard, K. et al. 1999. Seasonal plasticity in two satyrine butterflies: state-dependent decision
making in relation to daylength. – Oikos 84: 453-462.
Gotthard K., et al. 2000. Individual state controls temperature dependence in a butterfly
(Lasiommata maera). – Proc. R. Soc. (B) 267: 589-593.
Hickling, R. et al. 2006. The distributions of a wide range of taxonomic groups are expanding
polewards. – Glob. Change Biol. 12: 450-455.
Karlsson, B. 2014. Extended season for northern butterflies. – Int. J. Biometeorol. 58: 691-701.
Kingsolver, J. G. 1989. Weather and the population dynamics of insects: integrating physiological and
population ecology. – Physiol. Zool. 62: 314-334.
Krumm, J. T. et al. 2008. Genetic variability of the European corn borer, Ostrinia nubilalis, suggests
gene flow between populations in the Midwestern United States. – J. Insect Sci. 8: 72.
Lees, E. & Archer, D. M. 1980. Diapause in various populations of Pieris napi L. from different parts of
the British Isles. – J. Res. Lepid. 19: 96-100.
Maes, D. et al. 2012. Applying IUCN Red List criteria at a small regional level: a test case with
butterflies in Flanders (N-Belgium). – Biol. Conserv. 145: 258-266.
17
379
380
381
382
383
384
385
386
387
388
389
390
391
392
393
394
395
396
397
398
399
400
3334
Maes, D. et al. 2013. Butterflies in Flanders: New knowledge for better action (in Dutch with English
summary). – Uitgeverij Lannoo, Tielt.
Masaki, S. 1999. Seasonal adaptations of insects revealed by latitudinal diapause clines. – Entomol.
Sci. 2: 539-549.
McLaughlin, J. F. et al. 2002. Climate change hastens population extinctions. – Proc. Natl. Acad. Sci.
USA 99: 6070-6074.
Menzel, A. et al. 2006. European phenological response to climate change matches the warming
pattern. – Glob. Change Biol. 12: 1969-1976.
Moran, E. V. and Alexander, J. M. 2014. Evolutionary responses to global change: lessons from
invasive species. – Ecol. Lett. 17: 637-649.
Moritz, C. and Agudo, R. 2013. The future of species under climate change: resilience or decline? –
Science 341: 504-508.
Musolin, D. L. 2007. Insects in a warmer world: ecological, physiological and life-history responses of
true bugs (Heteroptera) to climatic change. – Glob. Change Biol. 13: 1565-1585.
Nakazawa, T. and Doi, H. 2012. A perspective on match/mismatch of phenology in community
contexts. – Oikos 121: 489–495.
Nylin, S. and Svärd, L. 1991. Latitudinal patterns in the size of European butterflies. – Ecography
14: 192–202
Nylin, S. et al. 1989. Seasonal plasticity in growth and development of the speckled wood butterfly,
Pararge aegeria (Satyrinae). – Biol. J. Linn. Soc. 38: 155-171.
Parmesan, C. 2007. Influences of species, latitudes and methodologies on estimates of phenological
response to global warming. – Glob. Change Biol. 13: 1860-1872.
18
401
402
403
404
405
406
407
408
409
410
411
412
413
414
415
416
417
418
419
420
421
422
3536
Parmesan, C. and Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across
natural systems. – Nature 421: 37-42.
Pavan, F. et al. 2013. Occurrence of two different development patterns in Lobesia botrana
(Lepidoptera: Torticidae) larvae during the second generation. – Agri. Forest Entomol. 15: 398-406.
Reed, T. E. et al. 2010. Phenotypic plasticity and population viability: the importance of
environmental predictability. – Proc. R. Soc. (B) 277: 3391-3400.
Robertson, B. A. et al. 2013. Ecological novelty and the emergence of evolutionary traps. – Trends.
Ecol. Evol. 28: 552-560.
Roff, D. A. 1980. Optimizing development time in a seasonal environment: the ‘ups and downs’ of
clinal variation. – Oecologia 45: 202-208.
Roy, D. B. and Sparks, T. H. 2000. Phenology of British butterflies and climate change. – Glob. Change
Biol. 6: 407–416.
Saino, N. et al. 2011. Climate warming, ecological mismatch at arrival and population decline in
migratory birds. – Proc. R. Soc. (B) 278: 835-842.
Schilthuizen, M. and Kellermann, V. 2013. Contemporary climate change and terrestrial
invertebrates: evolutionary versus plastic changes. – Evol. Appl. 7: 56-67.
Scriber, J. M. et al. 2014. Adaptations to « thermal time » constraints in Papilio: Latitudinal and local
size clines differ in response to regional climate change. – Insects 5: 199-226.
Shapiro, A.M. 1975. Photoperiodic responses of phenologically aberrant populations of pierid
butterflies (Lepidoptera). – Great Basin Nat. 35: 310-316.
Sih, A. et al. 2011. Evolution and behavioural responses to human-induced rapid environmental
change. – Evol. Appl. 4: 367–387.
19
423
424
425
426
427
428
429
430
431
432
433
434
435
436
437
438
439
440
441
442
443
444
3738
Stefanescu, C. et al. 2003. Effects of climatic change on the phenology of butterflies in the northwest
Mediterranean Basin. – Glob. Change Biol. 9: 1494-1506.
Tobin, P. C. et al. 2008. Historical and projected interactions between climate change and insect
voltinism in a multivoltine species. – Glob. Change Biol. 14: 951-957.
Travis, J. M. J., Delgado, M., Bocedi, G., Baguette, M., Bartoń, K., Bonte, D., Boulangeat, I., Hodgson, J.
A., Kubisch, A., Penteriani, V., Saastamoinen, M., Stevens, V. M. and Bullock, J. M. (2013), Dispersal
and species’ responses to climate change. - Oikos, 122: 1532–1540.
Trudgill, D. L. et al. 2005. Thermal time: concepts and utility. – Annals Appl. Biol. 146: 1–14.
Turlure, C. et al. 2010. Microclimatic buffering and resource-based habitat in a glacial relict butterfly:
significance for conservation under climate change. – Glob. Change Biol. 16: 1883–1893.
Välimäki, P. et al. 2012. Latitudinal clines in alternative life histories in a geometrid moth. – J. Evol.
Biol. 26: 118-129.
Valtonen, A. et al. 2011. Environmental controls on the phenology of moths: predicting plasticity and
constraint under climate change. – Oecologia 165: 237-248
Van Asch, M. et al. 2007. Predicting adaptation of phenology in response to climate change, an insect
herbivore example. – Glob. Change Biol. 13: 1596–1604.
Van Dyck, H. et al. 2009. Declines in common, widespread butterflies in a landscape under intense
human use. – Conserv. Biol. 23: 957-965.
Van Swaay, C. A. M. et al. 2008. Butterfly monitoring in Europe: methods, applications and
perspectives. – Biodiv. Conserv. 17: 3455-3469.
van Swaay, C. A. M. et al. 2013. The European Grassland Butterfly Indicator 1990-2011. – European
Environmental Agency, Copenhagen, Denmark.
20
445
446
447
448
449
450
451
452
453
454
455
456
457
458
459
460
461
462
463
464
465
466
3940
Végvári, Z. et al. 2014. Life-history traits and climatic responsiveness in noctuid moths. – Oikos.
doi: 10.1111/oik.01655.
Verovnik, R. et al. 2012. Atlas of butterflies (Lepidoptera: Rhopalocera) of Slovenia. – Centre for
Cartography of Fauna and Flora, Slovenia.
WallisDeVries, M. F. et al. 2012. Changes in nectar supply: a possible cause of widespread butterfly
decline. – Curr. Zool. 58: 384-391.
Ward, N. and Masters, G. J. 2007. Linking climate change and species invasion: an illustration using
insect herbivores. – Glob. Change Biol. 13: 1605-1615.
Watt, W. B. and Boggs, C. L. 2003. Butterflies as model systems in ecology and evolution – Present
and future. In: Butterflies: Ecology and Evolution Taking Flight (eds. Boggs, C. L., Watt, W. B. and
Ehrlich, P. R.). – The University of Chicago Press, Chicago, pp. 603-613.
Williams, S. E. et al. 2008. Towards an integrated framework for assessing the vulnerability of species
to climate change. – PLoS Biol. 6: e325.
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Figures
Figure 1. Schematic representation of the shift from a bivoltine to a threevoltine life style in the Wall
Brown butterfly (Lasiommata megera) relative to latitude in Europe. At intermediate latitudes a
third, partial generation may occur. If regional warming interacts with the cue-response system of
life-cycle regulation (i.e. larval diapause induction), then all individuals develop into a third
generation. According to the ‘lost generation hypothesis’ this may constitute a low or even zero
fitness outcome because of a developmental trap with potentially strong impacts on local population
persistence.
Figure 2. Phenological pattern of L. megera in inland populations (a) and coastal populations (b) in Flanders (north Belgium) in recent years (2001-2010) and in the previous period (1981-2000). Data are based on an extensive butterfly recording scheme (for details we refer to Maes et al. 2012 and 2013). The phenology figures were made by fitting a smoother through the relative number of observations per day during the periods 1981-2000 (red) and 2001-2010 (blue).
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Figure 1
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Fig. 2.
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