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EV-1
The lost generation hypothesis: could climate change drive
ectotherms into a developmental trap?
Hans Van Dyck , Dries Bonte , Rik Puls , Karl Gotthard and Dirk Maes
H. Van Dyck (hans.vandyck@uclouvain.be), Earth and Life Inst., Universit é Catholique de Louvain (UCL), BE-1348 Louvain-la-Neuve,
Belgium. – D. Bonte and R. Puls, Dept of Biology, Ghent Univ., DE-9000 Ghent, Belgium. – K. Gotthard, Dept of Zoology, Stockholm Univ.,
SE-106 48 Stockholm, Sweden. – D. Maes, Res. Inst. for Nature and Forest (INBO), BE-1070 Brussels, Belgium.
Climate warming aff ects 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 distort the quality of information given by
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. is 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 northwestern
Europe may be an example of a developmental trap. is formerly widespread, bivoltine (or even multivoltine) butterfl y
has become a conundrum to conservationist biologists. A split-brood fi eld 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.
Climate change and phenology
For a wide range of taxonomic groups, there is ample
evidence of the impacts of global warming on their occur-
rence in both space and time (Parmesan 2007). e most
widely documented responses since the early days of cli-
mate change research involve phenological shifts (Angilletta
2009). Phenology is the temporal dimension of an organ-
ism ’ 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 fi tness.
e observed phenological patterns in plants and ani-
mals 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).
ermally-sensitive traits that aff ect phenology, including
for example growth rate and development time, may also
be infl uenced by interaction eff ects between genes and the
environment (Barton et al. 2014). So far, the majority of
documented responses to climate change appear to be exam-
ples 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 maladap-
tive. 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 signifi cant short-term consequences
for population abundance under novel conditions. Hence,
it can be a factor of signifi cance for conservation under
climate change in addition to other factors including: 1) the
shrinking of populations of cold-adapted species (Turlure
et al. 2010), 2) local extinctions due to extreme weather
conditions (McLaughlin et al. 2002), and 3) phenological
© 2015 e Authors. Oikos © 2015 Nordic Society Oikos
Subject Editor: Jessica Abbott. Editor-in-Chief: Dustin Marshall. Accepted 21 November 2014
Oikos 000: 001–008, 2015
doi: 10.1111/oik.02066
EV-2
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 (V é gv á ri et al. 2014). is, in turn, may provide
opportunities for an increase in the number of generations
per year (i.e. voltinism; Altermatt 2010). is issue has par-
ticularly 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 signifi cant thresholds (Ge
et al. 2005, Tobin et al. 2008). Although patterns of earlier
appearances and an increase in voltinism have been docu-
mented 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 ectother-
mic organisms is how calendar date relates to ‘ thermal time
windows ’ or degree-days. Degree-days provide an accumu-
lated 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 the phenological event of interest (Trudgill
et al. 2005). As phenology determines the set of environ-
mental conditions experienced at a particular stage of the
life cycle (e.g. specifi c degree-days thresholds), it may in
turn aff ect decision making by organisms as they rely upon
environmental cues and internal response systems that were
functional in their evolutionary history.
e fi eld 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 fi eld have dealt with
maladaptive habitat and resource use in anthropogenic envi-
ronments, although the signifi cance 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 knowl-
edge, we are not aware of studies dealing explicitly with devel-
opmental 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 season ends before develop-
ment is completed, the insect risks losing this generation
(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 diff erent frameworks (e.g. invasive
species) are highly relevant to this issue, as we will discuss
below.
In this paper, we outline the potential signifi cance 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-season studies to bet-
ter understand population consequences (Karlsson 2014).
Whilst the dominant diapause-inducing cue (photoperiod)
will be unaff ected by global climate change, higher tempera-
tures may modify rates of development, leading to a decou-
pling of synchrony between diapause-sensitive life-cycle
stages and critical photoperiods for diapause induction (Bale
and Hayward 2010). We were particularly inspired by the
case of the wall brown butterfl y Lasiommata megera . is
butterfl y used to be widespread, but over the last few decades
it has shown a dramatic decline in nortwestern Europe (Van
Dyck et al. 2009). Based on the literature and on results from
an exploratory translocation experiment, we infer the possi-
bility 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 devel-
opmental 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, V ä lim ä ki et al.
2012). Southern genotypes that disperse northwards could
be considered as being pre-adapted to ‘ northern ’ condi-
tions under climate change. However, these southern types
could in principle have their range expansion restricted
by developmental traps. For example, in laboratory and
fi eld experiments, Dalin et al. (2010) demonstrated latitu-
dinal variation in how the chrysomelid beetle Diorhabda
carinulata responded to day length for diapause induc-
tion and how the responses aff ected insect voltinism across
the introduced range. is 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.
EV-3
Phenological adaptations in insects have led to well-
developed theoretical perspectives on optimizing develop-
ment time and body size in a seasonal environment along
latitudinal clines (e.g. clinal ‘ saw-tooth ’ pattern; Roff 1980,
Nylin and Sv ä rd 1991). eory predicts diff erent 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 pre-
dictor. In recent work on the voltinism, body size and tem-
perature in North American Papilio butterfl ies, 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 induced strong constraints on body size,
but this has rapidly changed during the recent decade with
local summer warming (Scriber et al. 2014). According to
the authors, the eff ects 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.
e question of how range shift and developmental traps
may interact is further confounded by the fact that a species
may have populations that diff er in phenology and voltinism
within the same region (Krumm et al. 2008). For example,
in those areas where the butterfl y Pieris napi has a second
and third brood, a signifi cant part of the pupae derived
from the spring generation are diapause pupae and do not
develop into butterfl ies until the following year (Lees and
Archer 1980). Such a pattern could be the result of mul-
tiple colonization events from diff erent source regions with
diff erent phenological profi les, or of phenologically aberrant
sub-populations with unusual local topographies and hence
microclimates (Shapiro 1975). Another reason for the co-
existence of diff erent developmental profi les and phenologies
could be bet-hedging (Danforth 1999). Hence, the picture
of one species-specifi c phenological type in one particular
area may hardly do justice to the complex situation which
prevails for several multivoltine species.
e fi rst step towards predicting voltinism changes and
the potential for developmental traps in response to climate
change is to understand the evolution of these characteris-
tics. 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 evo-
lution but through diff erent mechanisms (Masaki 1999).
erefore, more case studies are needed to better understand
the processes that lead to specifi c phenological responses
and their consequences for life-cycle regulation (e.g. dia-
pause induction) under climate change. In this case, zones
of transition between diff erent levels of voltinism are of
particular interest (Nylin and Sv ä rd 1991). Although adap-
tive 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. is,
in turn, opens the possibility of a developmental trap mak-
ing organisms opt for a low fi tness developmental pathway
relative to the prevailing environmental conditions. e key
point is that changed phenology may challenge the way ecto-
therms 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 con-
ditions outside the range experienced in the population
of origin. While the fi elds of climate change and biologi-
cal invasions have largely developed independently (Ward
and Masters 2007), researchers interested in climate change
eff ects are likely to get insights and ideas from studies on
introduced pest species.
An analogue to the climate change induced ‘ develop-
mental 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 stages of range expansion in Japan, the green stink bug
Nezara viridula induced diapause much later than local native
species, resulting in signifi cant 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 fi fth genera-
tion 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. For example, the introduc-
tion 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 butterfl y under
dramatic decline
Butterfl ies are popular study organisms for ecology, evolu-
tion 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 (Dennis
and Shreeve 1991, Roy and Sparks 2000). Butterfl ies are
also the subject of well-established recording schemes pro-
viding useful spatial and temporal datasets on change in
abundance and occurrence (Forister and Shapiro 2003, Van
Swaay et al. 2008). Moreover, their life styles strongly relate
to the thermal dimension of the environment in time and
space as they are fl ying, sun-basking organisms in the adult
EV-4
L. megera always occurs in two generations per year, but in
warm summers a partial third generation may occur. Com-
paring the phenology patterns of the period 1981 – 2000 and
2001 – 2010 in Belgium indicated an overall increased occur-
rence of the third generation (Maes et al. 2013). However,
the pattern diff ers between the inland area, where L. megera
has disappeared, and the coastal area, where it still occurs
(Fig. 2). In the coastal populations, the third generation has
become relatively more abundant in the period 2001 – 2010
than in the period 1980 – 2000. In the inland populations this
generation has become much longer in the recent period, but
the phenology fi gure is ‘ blurred ’ in this case by the gradual
extinctions in the local inland populations.
In a split-brood breeding experiment in the fi eld, we
tested whether developmental decisions are diff erent 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 genera-
tion), we introduced a total of 253 young caterpillars of
L. megera into four diff erent Belgian sites (two inland sites
and two coastal sites) where they could grow and develop on
potted host grass (greenhouse-reared Festuca rubra ) in indi-
vidual enclosures. e sites were at similar latitude (between
51 ° 07 ′ and 51 ° 21 ′ ), but the two inland sites were located ca
140 km to the east compared to the coastal sites. Interest-
ingly, 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 conspecifi cs 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 off spring
are still small caterpillars in both regions (i.e. August –
September). Photoperiod was obviously not diff erent
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 diff erence 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
signifi cantly warmer in the inland sites than in the coast
sites (Maes and Van Dyck unpubl. data based on meteoro-
logical records). Most climate change studies rely on general
ambient temperature data, but these do not necessarily
refl ect 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 congru-
ent with the hypothesis. Our split-brood fi eld 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 with-
out 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.
is, in turn, will have strong population consequences
aff ecting the abundance of the species in the next spring
generation as we are in a scenario of non-overlapping, discrete
stage and usually less mobile ectotherms in the larval stages
(Clench 1966, Dennis 1993, Kingsolver 1989, Bryant et al.
2000). Several butterfl y studies addressed phenological shifts
(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 butterfl y Lasiommata megera . is
widespread grassland butterfl y 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 northwestern 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). e
population decline in northwestern Europe (i.e. Belgium,
the Netherlands and 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 habi-
tat loss and wild fl ower declines in diff erent 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, refl ected in other butterfl ies
susceptible to similar habitat and resource issues (e.g. small
heath Coenonympha pamphilus ; Maes et al. 2012). erefore,
conservation biologists are in search of a sound explanation
for its strong and rapid decline.
We argue that L. megera has the biological profi le of a
candidate species for experiencing a developmental trap. e
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 sensitiv-
ity is not yet known). In the northern part of its range, the
species is bivoltine and to the south and southeast of Europe
it occurs in three or four overlapping generations even in
intensively farmed areas (e.g. Slovenia; Verovnik et al. 2012;
Fig. 1). Intriguingly and opposite to related satyrine but-
terfl ies (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 Sv ä rd 1991). is suggests that it has
lost the (genetic) ability of a univoltine life cycle that would
require inducing larval diapause even if environmental con-
ditions still remain suitable for a certain time period. is
implies a major diff erence in life history with the very closely
related species L. maera , which is univoltine in Sweden, but
bivoltine further south (Gotthard et al. 1999). Developmen-
tal decisions in response to day length depend in this species
on the seasonal state of the larvae. e 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 aff ect late summer diapause induc-
tion in L. megera in northwestern Europe. In this region,
EV-5
Figure 1. Schematic representation of the shift from a bivoltine to a threevoltine life style in the wall brown butterfl y 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 fi tness outcome because of a developmental trap with potentially
strong impacts on local population persistence.
generations. In such cases, the long-term population growth
rate is determined by its geometric mean and unusual low val-
ues will have a strong impact on persistence. In some insects,
there is a developmental buff er against seasonal variability
caused by within-population variation in diapause induc-
tion. Our working hypothesis for L. megera in northwestern
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 eff ect
is less severe in the populations closer to the seaside which
were less exposed to warming eff ects. Given the magnitude
of the eff ect, as suggested by our fi eld experiment, inland
populations can be rescued by recolonisation by pre-adapted
genotypes, or types on which natural selection can adjust
the reaction norms of the developmental response, rather
than by selection from standing genetic variation. Given
the highly fragmented nature of remaining populations and
the absence of substantial standing genetic variation, a fast
rescue is thus not likely. 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 diff erent 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 environ-
mental factors to explain the dramatic decline of L. megera
in northwest-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 fi rst appearance and increased voltinism, in short-
living ectothermic organisms such as insects, there is still
much to learn about the diversity of mechanisms or pro-
cesses that cause (mal)adaptive responses. If the relationship
between environmental cues and the developmental response
is blurred under ‘ novel ’ seasonal conditions, it opens the pos-
sibility of a developmental trap. We argue that this fi eld 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 dis-
tances to track climate, especially if combined with dispersal
limitation due to habitat fragmentation, can cause a lag in
EV-6
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 butterfl y recording scheme (for details we refer to
Maes et al. 2012, 2013). To visualize the phenology patterns in the two periods (n ⫽ 1064 and n ⫽ 922 recordings, respectively), we fi tted
a smoother through the relative number of observations per day using the geom_density function in the ggplot2 package (Wickham 2009)
in R ver. 3.1.1.
the response to new climatic conditions (Moritz and Agudo
2013). e phenomenon of a developmental trap may also
open a new perspective on climate debt eff ects (i.e. limited
ability of organisms to track rapid climate change; Travis
et al. 2013) within the core of the distribution range of cer-
tain species. Climate debt has been shown in, for example
birds and butterfl ies, at the northern edge of their range
(Devictor et al. 2012). If populations in transition zones
between diff erent 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 diffi cult to make sound predictions
on the general signifi cance of developmental traps across
species and climate zones. Under variable conditions the
co-occurrence of diff erent developmental patterns within a
generation may provide resilience at the population level
(Pavan et al. 2013). We argue that the profi le 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
fi eld of the ecology and evolution of phenology. Integrat-
ing life-history theory, developmental biology, biogeogra-
phy 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
EV-7
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Acknowledgements – We thank Nadiah Kristensen and Tom Oliver
for comments that helped improve the manuscript. is 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. is is publication BRC 328 of
the Biodiversity Research Centre (Earth and Life Institute, UCL,
Louvain-la-Neuve).
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