Research

OIKOS
Allee effects under climate change

Luděk Berec

L. Berec (http://orcid.org/0000-0002-2419-3324) ✉ (berec@entu.cas.cz), Centre for Mathematical Biology, Inst. of Mathematics, Faculty of Science, Univ.
of South Bohemia, Branišovská 1760, CZ-37005 České Budějovice, Czech Republic, and: Czech Academy of Sciences, Biology Centre, Inst. of Entomology,
Dept of Ecology, Branišoská 31, CZ-37005 České Budějovice, Czech Republic.

Oikos Understanding how climate change affects population dynamics is crucial for assessing
128: 972–983, 2019 future of biodiversity. Here I ask how can Allee effects, occurring when mean individ-
doi: 10.1111/oik.05941 ual fitness is reduced in rare populations, respond to increasing temperature. Despite
the role Allee effects play in ecology of invasive, threatened and harvested populations,
Subject Editor: Björn Rall impacts of climate change on Allee effects are practically unknown. Analysis of two
Editor-in-Chief: Dries Bonte population models reveals that whereas the Allee effect driven by predation gener-
Accepted 25 January 2019 ally weakens as temperature increases, the Allee effect due to need of finding mates is
predicted to become stronger when warming occurs. For the former model, the meta-
bolic theory suggests that with increasing temperature prey growth rate should increase
faster than predator attack rate. Increasing temperature thus weakens the Allee effect.
In the latter, gypsy moth population model, mating rate increases with warming due
to enhanced female−male encounter rate and temperature-induced modifications in
female and male adult emergence distributions. However, male and female mortality
rates increase, too and the net effect is strengthening of the Allee effect. These results
have repercussions also for pest control, indicating that augmentation of biocontrol
agents may perhaps be not as effective as using pesticides or disrupting mating.

Keywords: global warming, metabolic theory

Introduction
Understanding how climate change impacts population and community dynamics
is crucial for assessing potential changes in global biodiversity (Pereira et al. 2010,
Bellard et al. 2012). Many predictions are quite warning. These include reduced popu-
lation sizes or densities, elevated risk of population extinctions, enhanced frequency of
non-native species invasions, increased pest species activity in their native habitats and
shifts in geographical species ranges (Pereira et al. 2010, Bellard et al. 2012). On the
other hand, enhanced temperature variation (Berec et al. 2013, Lawson et al. 2015),
thermal acclimation (Sentis et al. 2015) and warming-induced changes to body size
(Osmond et al. 2017, Sentis et al. 2017) were all suggested to at least alleviate some of
the negative impacts of global warming.
A growing interest in impacts of global warming on community dynamics has
recently showed up, focusing on individual predator−prey interactions (Dell et al.
––––––––––––––––––––––––––––––––––––––––
© 2019 The Author. Oikos © 2019 Nordic Society Oikos
www.oikosjournal.org

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2014, Fussmann et al. 2014, Gilbert et al. 2014, Sentis et al. (a) x 10−6
2015, Osmond et al. 2017, Uszko et al. 2017), tri-trophic 1
food chains (Binzer et al. 2012, Sentis et al. 2017) and even logistic−like growth
complex food webs (Binzer et al. 2016). In all these stud- weak Allee effect

Per capita growth rate g(BR)

strong Allee effect
ies, the basal species (i.e. the prey species at the lowest food 0.5 fatal Allee effect
web level) were assumed to follow logistic dynamics. None
of these studies thus covered the case of a positive relation-
ship between the per capita population growth rate and
population density, a phenomenon termed the Allee effect 0
and observed or at least presumed to occur in many plant
and animal populations (Stephens and Sutherland 1999,
Courchamp et al. 2008). −0.5
Allee effects are not just a marginal theoretical construct,
but a vital process affecting many important and applied
aspects of population dynamics. These include chance of
invading populations to establish and spread (Tobin et al. −1
0 1 2 3 4 5
2011, Vercken et al. 2011), risk of small and threatened popu- Prey biomass−density BR
lations to go extinct (Brashares et al. 2010, Crates et al. 2017)
and danger of economically important populations of getting
(b) x 10−6
overharvested (Hutchings 2015, Haider et al. 2017). In all 1
these areas of applied ecology, acquaintance of presence and BC = 0.025
strength of Allee effects is crucial (Stephens and Sutherland Per capita growth rate g(BR) BC = 0.045
1999, Courchamp et al. 2008). Understanding whether Allee
effects can (dis)appear due to climate change and how they 0.5
can respond to it is thus of paramount importance for both
basic and applied ecology.
Allee effects occur when the per capita population growth 0
rate declines with decreasing density in rare populations, and
are classified as weak, strong or fatal (Fig. 1a; Stephens et al.
1999, Boukal and Berec 2002, Courchamp et al. 2008).
−0.5
Populations with weak Allee effects have positive per capita
growth rates at any density. If an Allee effect is strong, a criti-
cal population density, termed the Allee threshold, exists such
that the population practically declines to extinction when −1
0 1 2 3 4 5
reduced below the Allee threshold. Finally, fatal Allee effects
occur when the per capita growth rate is negative at any pop- Prey biomass−density BR
ulation density. Since fitness components of many species are Figure 1. Per-unit-biomass prey growth rate g(BR) (7) under an Allee
influenced by temperature (ectotherms comprise over 99% effect. (a) Possible types of Allee effect: weak (black solid,
of all species; Atkinson and Sibly 1997), the type of Allee BC = 0.01 g m−2), strong (black dashed, BC = 0.03 g m−2) and fatal
effect (weak, strong or fatal) and the Allee threshold in case of (black dash-dot, BC = 0.06 g m−2). Logistic-like growth occurs if
strong Allee effects may be temperature-dependent and hence predator biomass-density is low enough (grey, BC = 0.002 g m−2). (b)
respond to warming. Strong Allee effect: the black dots are the respective Allee thresholds
Intriguingly, impacts of increasing temperature on the and the gray lines are the respective tangent lines to g(BR) at these
strength and more fundamentally on a possibility of (dis) thresholds. The slope of these tangent lines is the Allee slope. Other
appearance of Allee effects remain virtually unexplored. parameters as in Table 1; mR = 10−4 g, mC = 10−3 g, T = 15 K.
Current knowledge is limited to a modeling study of the
invasive spiny water flea Bythotrephes longimanus subject and thus comprises different mechanisms to be affected by
to enhanced mating difficulties at lower densities (a source temperature.
of Allee effect; Gascoigne et al. 2009), in which the Allee
threshold was shown to decline with increasing water tem- Allee effects driven by predation
perature (Wittmann et al. 2011). Here I explore how could
Allee effects respond to climate change. Specifically, model- Methods
ing is used to examine how could the type of Allee effect
(weak, strong or fatal) and the Allee threshold in case of A predation-driven Allee effect occurs in the prey
strong Allee effects vary with temperature. In any of the fol- population when individual prey are more vulnerable to
lowing two sections I present a population model and its predation as prey density declines (Gascoigne and Lipcius
analysis. Each model has a different source of Allee effect 2004, Courchamp et al. 2008, Kramer and Drake 2010).

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This happens, for example, when a logistically growing body masses and are commonly factored as (Kalinkat et al.
prey (or resource) population of a biomass-density BR is 2013, Binzer et al. 2016, Sentis et al. 2017)
attacked by a predator (or consumer) population with a
Holling type II (i.e. decelerating) functional response
and a constant biomass-density BC (Gascoigne and R C  T −T 
a = a0mRsa mCsa exp  − E a 0 (4)
Lipcius 2004, Courchamp et al. 2008, Berec et al. 2018).  kTT0 
Denoting by r and K the maximum per-unit-biomass prey
growth rate and the prey carrying capacity (in terms of
biomass), respectively, by a the predator attack rate and R C  T −T 
by h the predator handling time, the corresponding prey h = h0mRsh mCsh exp  − E h 0 (5)
population model is  kTT0 

Here mC is the predator body mass, while the other param-

dBR  B  aBR
= rBR 1 − R  − BC (1)
dt  K  1 + ahBR
The assumption of constant predator biomass-density
BC is a reasonable approximation e.g. when the preda-
tor’s assimilation efficiency is low and/or the predator is
a generalist with dynamics largely dependent on other,
unstudied prey species (Gascoigne and Lipcius 2004,
Berec et al. 2018). With model 1, I examine how the type
and strength of Allee effect vary with temperature. I note
that model 1 is formally equivalent to the basal species
(i.e. the prey species at the lowest food web level) equa-
tion of many recent models exploring impacts of climate
change on community dynamics (Binzer et al. 2012, 2016,
Dell et al. 2014, Fussmann et al. 2014, Gilbert et al. 2014,
Sentis et al. 2015, 2017, Osmond et al. 2017, Uszko et al.
2017).
Interpreting model 1 in terms of biomass-densities
instead of densities of individuals makes possible to use
the metabolic theory of ecology and thus express relevant
model parameters in terms of body mass and temperature
(Brown et al. 2004). Body mass and temperature depen-
dence of the maximum per-unit-biomass prey growth rate
r is commonly formalized as (Binzer et al. 2012, 2016,
Sentis et al. 2017)
 T −T 
r = r0mRsr exp  − Er 0 (2)
 kTT0 
where r0 is the normalization constant independent of body
mass and temperature, mR is the prey body mass, sr is the
allometric exponent, Er is the activation energy (eV), k is the
Boltzmann’s constant (8.62 × 10−5 eV K−1), T is the absolute
temperature (K) and T0 is the normalization temperature (K;
here 20°C = 293.15 K). Similarly, the prey carrying capacity
K can be expressed as (Binzer et al. 2012, 2016, Sentis et al.
2017)
 T −T 
K = K 0mRsK exp  − E K 0 (3)
 kTT  0
where K0 is the normalization constant independent of body
mass and temperature, sK is the allometric exponent and EK
is the respective activation energy. The predation-related
parameters a and h of model 1 feature both prey and predator
eters have a meaning analogous to the respective ones for r
and K. The specific values used to parameterize Eq. 2–5 are
summarized in Table 1.
To explore impacts of warming on the type and strength
of Allee effect, the temperature T is varied. I vary also
the predator biomass-density BC, which will allow one to
speculate on what happens if BC itself is subject to climate
change. Indeed, the predator biomass-density BC, due to
its link to dynamics of the predator’s primary prey, may
increase or decrease with warming (Vasseur and McCann
2005). For each combination of T and BC, I determine
the type of Allee effect (weak, strong or fatal) and the prey
biomass-density at positive stable equilibrium. If a strong
Allee effect occurs I further calculate the Allee threshold
and the Allee slope. The concept of Allee slope, recently
introduced by Walter et al. (2017) and defined as a mag-
nitude of positive relationship between the per capita (here
per-unit-biomass) population growth rate and density (here
biomass-density) in the vicinity of the Allee threshold,
has important implications for population dynamics and
persistence (Walter et al. 2017).
For the parameter values specified in Table 1, the prey
carrying capacity K declines as the temperature T increases.
However, contrary to the prediction of the metabolic theory,
some studies reported temperature-independent carrying
capacity (Enquist and Niklas 2001) or even its positive rela-
tionship with temperature (DeLong and Hanson 2011); see
Table 1. Parameter values for the body mass and temperature-
dependent relationships (Eq. 2–5). Values for the maximum per-unit-
biomass growth rate r (s−1) are from Savage et al. (2004) and
Sentis et al. (2017), those for the carrying capacity K (g m−2) are from
Meehan (2006) and Fussmann et al. (2014), and those for the attack
rate a (m2 s−1) and the handling time h (s) are from Binzer et al.
(2016) and Sentis et al. (2017). Body masses are considered in grams
(g). The last line indicates whether the respective parameters increase
(↑) or decrease (↓) with increasing temperature T.
Parameter (x) r K a h
Unit s−1
gm −2 2 −1
m s s
x0 1.55 × 10−7
−0.25
31.19
0.28
2.04 × 10−6
0.25
15.68 × 103
−0.45
s x(R )
× × −0.8 0.47
s Cx
Ex (eV) 0.84 −0.71 0.38 −0.26
Increase in T ↑ ↓ ↑ ↓

974
also discussions in Vasseur and McCann (2005), Dell et al.
(2014) and Gilbert et al. (2014). Moreover, K is not a model
parameter linked to a specific process, but rather a complex
outcome of population dynamics. Therefore, I examine also
impacts of neutral or positive relationships between the
temperature T and the prey carrying capacity K. In addi-
tion, I study a version of model 1 in which the prey popula-
tion grows exponentially rather than in a logistic manner.
This is not a problem in the context of this study, since
Allee effects affect population dynamics predominantly at
low (biomass-)densities where within-species competition is
likely comparably weak.
Results
Model 1 has up to two positive equilibria. Assuming BC > 0
(otherwise BR = K is the only positive equilibrium of prey),
these can be obtained by setting the right-hand side of model
1 to zero and solving the resulting equation for the prey
biomass-density BR:
( K −1 / (ah )) ± ( K −1 / (ah )) ( )
2
+ 4 K / ( ah ) 1 − ( a / r ) BC
BR1,2 =
2 with biomass-densities just above those thresholds grow
With the per-unit-biomass prey growth rate denoted as
1 dBR  B  aBC
g ( BR ) = × = r 1 − R  −
BR dt  K  1 + ahBR
an Allee effect occurs if g(BR) increases close to the zero prey
biomass-density BR = 0, that is, if g′(0) = −r/K + BCa2h > 0
or equivalently BC > r/(a2hK). Otherwise, the prey popu-
lation growth is logistic-like, with g′(BR) < 0 at any BR ≥ 0.
An Allee effect is weak (one stable positive equilibrium)
if g(0) = r − aBC > 0 or equivalently BC < r/a, strong (two
positive equilibria of which the higher is stable and the
lower is unstable) if g(0) < 0 or equivalently BC > r/a and the
expression under the radical of Eq. 6 is positive, and fatal
(no positive equilibrium) if g(0) < 0 or equivalently BC > r/a
and the expression under the radical of Eq. 6 is negative
(Fig. 1a). In case a strong Allee effect occurs, the lower, unsta-
ble equilibrium is the Allee threshold and the slope of the
tangent line to g(BR) at the Allee threshold is the Allee slope
(Fig. 1b; Walter et al. 2017).
It is instructive to first look at how changes in any single
parameter in model 1 affect the type and strength of any
potential Allee effect. With the expressions from the previ-
ous paragraph it is not difficult to see that when the maxi-
mum per-unit-biomass prey growth rate r decreases or when
the predator attack rate a or biomass-density BC increase, the
chance of an Allee effect to occur increases and an Allee effect
shifts from weak to strong and eventually to fatal (Fig. 1a).
Similarly, increasing the prey carrying capacity K or the preda-
tor handling time h raises the chance of an Allee effect to occur.
For the parameters specified in Table 1, Allee effects gen-
erally weaken as the temperature T increases. Depending on
the actual predator biomass-density BC, Allee effects change
from fatal to strong, from strong to weak, or from weak
to a logistic-like prey growth (Fig. 2a). The temperature at
which strong Allee effects become weak corresponds to when
g(0) = r − aBC = 0 or equivalently when BC = r/a. As tempera-
ture grows, both the prey growth rate r and the predator
attack rate a increase, yet r increases at a higher rate than
a (Er > Ea in Table 1) and so Allee effects weaken with T.
Similarly, the temperature at which fatal Allee effects become
strong corresponds to when the expression under the radical
of Eq. 6 equals zero or equivalently when BC = r(1 + ahK)2/
(4a2hK). Although we cannot infer much from this formula,
Fig. 2a suggests that this boundary can be parabolic. Indeed,
for values of BC around 0.017 Allee effects can change with
warming first from strong to fatal and later from fatal back
to strong (Fig. 2a). Still, even though here an increase in
temperature may rather worsen things and cause population
extinction, the general pattern appears to be that increasing
temperature alleviates any Allee effect present.
For strong Allee effects, Allee thresholds are smaller at
higher temperatures (Fig. 2b). Moreover, Allee slopes are
steeper at higher temperatures (Fig. 2c). Smaller Allee thresh-
(6) olds are thus more clearly distinguished: prey populations
faster and hence escape from staying close to them more
easily (Fig. 1b). On the contrary, larger Allee thresholds are
more blurred: prey populations with biomass-densities just
(7)
above those thresholds grow slowly and are thus vulnerable
to extinction for a prolonged period of time, especially when
subject to repeated perturbations (Fig. 1b; Meyer 2016). The
prey populations subject to Allee effects driven by predation
are less vulnerable to extinction at higher temperatures also
from this perspective.
While the Allee threshold declines with increasing tem-
perature (Fig. 2b), the positive stable equilibrium decreases,
too (Fig. 2d). An important practical question then is how
their difference changes with temperature. This difference is
a measure of prey population resilience to perturbations in
its biomass-density, as it represents the minimum magnitude
of single perturbation required to get prey below the Allee
threshold, right to the basin of attraction of the stable extinc-
tion equilibrium (Meyer 2016). Interestingly, this (common)
measure of population resilience declines with warming
(Fig. 3).
As discussed above, the prey carrying capacity K may be
unaffected by temperature or even increase with warming.
Since increasing K decreases chances of an Allee effect to occur
and increases the critical predator biomass-density above
which strong Allee effects become fatal, these alternative
relationships between the prey carrying capacity and temper-
ature only corroborate the general prediction that warming
weakens Allee effects driven by predation (Supplementary
material Appendix 1 Fig. A1, A2). Moreover, under both
temperature-independent and positively temperature-
dependent prey carrying capacity, the prey biomass-density
at positive stable equilibrium increases with temperature
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Figure 2. Dependence on the temperature T and the predator biomass-density BC of the (a) Allee effect type, (b) Allee threshold, (c) Allee
slope and (d) prey positive stable equilibrium. Parameters as in Table 1; mR = 10−4 g, mC = 10−3 g. Color legend in panel (a): white = logistic-
like growth, red = weak Allee effect, green = strong Allee effect, blue = fatal Allee effect. Color legend in panels (b–d): the respective variable
increases in the direction from dark blue to dark red.

and so does population resilience (Supplementary material
Appendix 1 Fig. A1, A2). Last but not least, the results of the
model with exponential prey growth are comparable to those
of the models in which the prey population grows in a logistic
manner (Supplementary material Appendix 1 Fig. A3). These
results also suggest a potential mechanisms behind a non-
monotonic boundary between strong and fatal Allee effects
observed in Fig. 2a. Comparison of this figure with Fig.
A1a, A2a indicates that low negative values of the activation
energy EK of the prey carrying capacity may govern this non-
monotonicity: in the latter two figures one cannot get a fatal
Allee effects from a strong one just by increasing temperature.
Model 1 does not cover a situation where the predator
is a specialist and through a numerical response is dynami-
cally linked to its (primary) prey. The major reason for not
studying this situation is that even with a Holling type II
functional response such predator does not trigger an Allee
effect in its prey (Kot 2001). Also, this situation has been
studied repeatedly (Vasseur and McCann 2005, Dell et al.
2014, Gilbert et al. 2014, Osmond et al. 2017, Uszko et al.
2017). These studies reveal, among other things, that a nega-
tive relationship between temperature and body size may
reduce impacts of warming on consumer−resource dynamics
(Osmond et al. 2017), that increasing temperature may cause
a transition in predator−prey dynamics from coexistence
at a stable equilibrium to sustained predator−prey cycling
(Vasseur and McCann 2005), and that predator biomass-
density may initially increase with warming and later decrease
(Vasseur and McCann 2005). The latter two predictions are
especially important from our perspective, since the preda-
tor biomass-density BC may respond to warming through the
interaction with its (unmodeled) primary prey. One can envi-
sion drawing an anticipated predator trajectory in the T − BC
plots like in Fig. 2 or Supplementary material Appendix 1

976
 0.03 males or females as Gaussian distributions with means (i.e.

Predator biomass−density BC
Resilience dates of peak emergence) µM and µF (and with µF > µM due to
0.025 protandry) and SD σM and σF for males and females, respec-
tively (Robinet et al. 2007). Since the exact date of peak male
0.02
emergence (µM) by itself does not affect an overlap between
0.015 male and female maturation distributions and hence the
strength of Allee effect, µM is set arbitrarily to 5σM so that
0.01 virtually no males emerge before day 0 (Robinet et al. 2008,
Walter et al. 2015). Mating dynamics are then described by
0.005 a continuous-time mating model. Denoted by R, the mat-
ing model outputs the number of females Ft m that success-
0 fully reproduce by the end of mating season. Each of the
0 10 20 30
Temperature T
mated females lays one egg mass composed of λ eggs, time
is enhanced by one (generation) and the just described life
Figure 3. Dependence on the temperature T and the predator bio- cycle is repeated. This gives the following model of between-
mass-density BC of the prey population resilience, defined here as generation dynamics:
the difference between the prey biomass-density at the positive sta-
ble equilibrium and the Allee threshold, under strong Allee effects.
Parameters as in Table 1; mR = 10−4 g, mC = 10−3 g. Color legend as in
( ( )
J t +1 = λFt m = λR J t a 1 − p W , µ M , µ F , σ M , σ F ) (8)
Fig. 2. I now describe the continuous-time mating model R. Whereas
females of the gypsy moth mate only once, males may mate
Fig. A1–A3 and see what happens to the Allee effect type and multiply. The mating model thus considers five moth states,
strength. For example, cycling dynamics of BC would mean each expressed in terms of density (numbers per hectare):
that the strength of Allee effect and even its type may fluctu- virgin females (V), fertile males searching for females (Ms),
ate. Alternatively, a possible hump-shaped form of the preda- virgin female–fertile male couples (Q), fertile males tempo-
tor biomass-density BC as a function of temperature would rarily resting after mating (Mr) and mated females (Fr). Virgin
mean strengthening Allee effects initially and their weakening females and fertile males encounter at the rate z and have the
later on. In any case, the presented results allow for a variety probability c that courting is successful. If this is the case,
of predictions of this kind. tq is the mean time spent in the couple. Males need to rest
after each mating; let their mean resting time be tr. Within
Allee effects due to need of finding mates the mating season, males and females die at rates dM and dF,
respectively. Since mated females Fr are supposed to oviposit
Methods shortly after mating, they are assumed not exposed to mor-
tality. These assumptions leave the following mating season
A mate-finding Allee effect occurs when individual females model (Blackwood et al. 2012):
have enhanced difficulty to locate (compatible) mates
as population density declines (Courchamp et al. 2008, dV
Gascoigne et al. 2009, Shaw et al. 2018). This Allee effect has
dt
( )
= 0.5 J t a 1 − p WN (µ F , σ F ) − zVM s
been demonstrated, for example, in the gypsy moth Lymantria
1
dispar, a pest of North American forests (Tobin et al. 2009). In
this species, males mature and emerge before females, a phe-
(
+ d M Q − d FV + 1 − c Q
tq
)
nomenon termed protandry (Robinet et al. 2007). Protandry dM s
affects the degree to which males and females are tempo-
dt
( )
= 0.5 J t a 1 − p WN ( mM , sM ) − zVM s
rally segregated and hence affects the strength of Allee effect
1 1
(Robinet et al. 2008, Blackwood et al. 2012, Walter et al.
2015). In the following paragraphs, I review the gypsy moth
(
+ d FQ − d M M s + 1 − c Q + Mr
tq tr
) (9)
population model due to Blackwood et al. (2012) and mod- dQ 1
ify it by introducing temperature dependencies in it. = zVM s − d M Q − d F Q − Q
The gypsy moth is a species with non-overlapping genera- dt tq
tions. Within a generation starting at time t, a proportion a dM r 1 1
of Jt eggs survive through the larval to pupal stage after under- = −d M M r + c Q − M r
dt tq tr
going background mortality. Pesticides may be applied at the
larval stage and only a proportion 1 − p of larvae then survive. dFr 1
=c Q
A fraction W of pupae then avoid predation by rodents so dt tq
that eventually Jta(1 − p)W pupae emerge. There is a 1:1 sex
ratio at birth. Adults do not emerge all at once. One may The first term in the equation for virgin females V says that
envision temporal distributions of the dates of emergence of there are 0.5 Jta(1–p)W females ready to mature and emerge

977
during the mating season and that the individual emergence
dates follow a Gaussian distribution with mean (the peak
date) µF and SD (maturation dispersion) σF. The first term
in the equation for fertile searching males Ms has an analo-
gous meaning. The second term zVMs in the equations for
V and Ms represents the number of encounters between vir-
gin females and searching males and hence pairs formed per
unit time. It is this rate which, for any fixed temperature, is
responsible for occurrence of the mate-finding Allee effect in
the gypsy moth population (Berec 2018, Shaw et al. 2018).
Since no adults are present in the population at the begin-
ning of mating season, all five state variables of the mating
model 9 are initially set to zero. It is the inflow of emerging
adults that makes these variables positive as time proceeds.
The number of successfully mated females at the end of mat-
ing season is Ft m = Fr (t ) . Here τ is the length of mating
season, assumed to end 5σF days after µF so that virtually
no females emerge beyond that day (Robinet et al. 2008,
Walter et al. 2015). All parameters involved in model 9 are
listed in Table 2.
I now make some parameters of the models 8 and 9
temperature-dependent. Walter et al. (2015) showed that
both the degree of protandry (i.e. µF − µM) and maturation
dispersion (i.e. σM and σF, assumed equal) increased with
northing or elevation of the population’s location:
µ F − µ M = −3.639 × 10−3 + 1.112 × 10−3 elevation
+ 8.401 × 10−7 northing
σ M = σ F = 23.09 + 1.172 exp (elevation/1000)
−5 −12
− 1.358 × 10 northing + 2.067 × 10 northing
Both elevation and northing are measured in meters. Since
higher northing or elevation generally mean lower (mean)
temperature, both these quantities tend to decrease with
increasing (mean) temperature. I arbitrarily choose Logan,
WV, USA, as a reference location in the middle of gypsy moth
infestation area, for which northing is about 4 188 839 meters,
elevation is about 207 meters and (yearly average maximum)
Table 2. Parameters of the gypsy moth model (Eq. 8, 9). After Blackwood et al. (2012).
Parameter Value(s)
λ 546
a 0.05
p Varies
W 0.84
µM 5σM
σM Varies
µF Varies
σF σM
z 0.15
tr 1 mean resting time for males after mating
tq 0.0042
c 0.91
dM 1.67
dF 0.73
τ µF + 5σF
978
temperature is 19.89°C (<www.usclimatedata.com/cli-
mate/logan/west-virginia/united-states/uswv0442>). As far
as I know, protogynous gypsy moth populations for which
µF < µM do not exist. Still, setting elevation and northing
to zero in Eq. 10 gives µF < µM. However, the relationships
derived by Walter et al. (2015) are statistical fits and as such
have questionable validity for extrapolating to areas outside
of the gypsy moth range in North America. Moreover, the
values of protandry generated by these fits for model 9 never
became negative.
Furthermore, I assume a constant temperature lapse rate
(i.e. decrease of temperature with altitude) of 6.5°C km−1,
the commonly used overall average rate (Minder et al. 2010).
Hence,
(
T = T (Logan ) + 0.0065 × elevation (Logan ) − elevation ) (11)
From Eq. 11 elevation can be calculated as a function of
temperature and plugged in Eq. 10. Since I am interested
here just in trends and conceptual understanding of impacts
of climate change on Allee effects, precise numbers are less
important, especially since different values produce analogous
results.
Analogously to the parameters of model 1, the back-
ground mortality rates dM and dF can be made dependent on
body size and temperature:
(10)  T −T 
d X = d 0X mXsd exp  − E d 0 (12)
 kTT0 
2
where X = M or F, sd = −0.31 and Ed = 0.69 eV (Sentis et al.
2017); both dM and dF thus increase with warming. Assuming
that the male and female body masses are mM = 0.5 g and
mF = 2 g (values that lie within the range of pupal weights,
Patrick C. Tobin, pers. comm.; intriguingly, adult body
masses do not appear to have been reported in the literature
so I use the pupal body weights as a proxy), I estimate the
constants d 0M and d 0F so that dM = 1.67 and dF = 0.73 at
Definition Unit
number of eggs per egg mass –
fraction of eggs surviving to pupation –
fraction of larvae killed by pesticides –
fraction of pupae surviving rodent predation –
peak date of male emergence day
standard deviation of male emergence day
peak date of female emergence day
standard deviation of female emergence day
encounter rate between females and males day−1
day
mean time spent per day in a couple (6 min) day
probability of successful courting day
background mortality rate for males day−1
background mortality rate for females day−1
mating season length day
T = T0 = 19.89°C as in Table 2, giving d 0M = 1.36 and
d 0F = 0.91 .
Activity and movement rate are also generally functions of
temperature (Dell et al. 2014). Therefore, the encounter rate
z between virgin females and searching males likely depends
on temperature, too. To quantify this dependence, one may
use a relationship originally derived for the consumer attack
rate of the resource (Osmond et al. 2017). Assuming non-
flying virgin females (as is the case of gypsy moths in the
North American forests) and velocity v for searching males,
the encounter rate z is
 T −T 
z = z0v0mMsv exp  − Ev 0 (13)
 kTT0 
where sv = 1 and Ev = 0.46 eV (Osmond et al. 2017). Again, I
estimate the product z0v0 so that z = 0.15 at T = T0 = 19.89°C
as in Table 2, which gives z0v0 = 0.3. The positive activation
energy Ev implies that the encounter rate z increases with
warming.
Other model parameters may respond to warming, too.
Experimental results of Thompson et al. (2017) suggest
that the proportion of eggs surviving to the 4th instar or
to pupation, which may be positively linked to the param-
eter a, might remain unaffected by temperature or decline
with warming. Similarly, the body mass at the 4th instar or
the pupal mass, which both may be positively related to the
number of eggs per egg mass λ, appeared to remain unaf-
fected by temperature or declined with warming. Moreover,
since activity is expected to increase with warming (Dell et al.
2014, Osmond et al. 2017), mean resting time tr of just
mated males might increase, too. However, male gypsy moths
mate only during the daylight hours and only once per day
(Blackwood et al. 2012). Therefore, the value of tr = 1 day
used in model simulations could stay unaffected by changes
in temperature.
For the gypsy moth model, the Allee threshold can be
defined as the number of egg masses per hectare below
which the population declines toward extinction and
above which it grows (Blackwood et al. 2012). In other
words, the population goes extinct if the number of mated
females at the end of mating season is lower than the
number of egg masses at the beginning of the respective
generation and grows if this is not the case. To estimate
the Allee threshold, I conducted simulations of the gypsy
moth model for an increasing number of egg masses and
determined the minimum number of egg masses for which
the gypsy moth population grew rather than declined.
Moreover, I determined this minimum number for sev-
eral values of the pesticide efficiency p. This is also because
pesticide efficiency might depend on temperature, too.
Indeed, the toxicity of two pyrethroids and a spinosyn on
the European corn borer Ostrinia nubilalis were found to
decrease as post-exposure temperature increased (Musser
and Shelton 2005).
Results
Also here, it is instructive to first look at how changes in
any single model parameter impact the Allee effect strength
or the Allee threshold value. Obviously, by increasing λ, a
and W or by decreasing p the Allee effect weakens and the
Allee threshold declines. Moreover, by increasing the degree
of protandry µF − µM and background mortalities dM and dF
or by decreasing the encounter rate z between virgin females
and searching males the Allee threshold becomes larger.
Maturation dispersion has a non-uniform effect (Fig. 4a).
With increasing σM = σF, any effect of protandry gets reduced
as the male and female distributions of the emergence date
increasingly overlap. This initially enhances the mating suc-
cess and hence decreases the Allee threshold. However, when
σM = σF become large enough, the distributions become quite
flat and the mating success low throughout the whole mat-
ing season. Finally, by increasing c and by decreasing tq or tr
mating becomes more efficient and coupling or resting males
return to the searching state faster, respectively, so the Allee
threshold declines.
For any pesticide efficiency p, higher temperatures weaken
the Allee effect (i.e. decrease the Allee threshold) via modify-
ing the female and male adult emergence distributions and
increasing the female−male encounter rate z (Fig. 4b), while
strengthening the Allee effect (i.e. increasing the Allee thresh-
old) via increasing the background mortality rates dM and dF
(Fig. 4c). The net effect of increasing temperature is then an
increasingly stronger Allee effect (Fig. 4d). I note that a sin-
gle continuous spraying of the infested area by the bacterial
pesticide Bacillus thuringiensis kills about 80% of larvae, i.e.
p = 0.8 (Blackwood et al. 2012). If the population is at a den-
sity, one may eradicate it by increasing the Allee threshold
above that density. Consequently, if for any fixed value of p
the Allee threshold increases with temperature, then at higher
temperatures the same Allee threshold value can be attained
with lower pesticide efficiency. Alternatively, even if the
population density always remains above the Allee threshold,
lower perturbations in population density suffice to suppress
the population below it at higher temperatures. A potential
decline in the pesticide efficiency p with increasing temper-
ature may reverse this pattern. This can be seen in Fig. 4d
when, for example, p = 0.8 at 20°C is reduced to p = 0.6 at
30°C. Contrarily, if warming is accompanied by a decrease
in the number of eggs per egg mass and the proportion of
eggs that survive to become adults in the absence of pesticides
and pupal predation (i.e. by a decrease in the value of λa;
Thompson et al. 2017), the Allee threshold would increase
with temperature at a rate higher than in Fig. 4d.
Discussion
Do Allee effects become weaker or stronger when tempera-
ture increases? And do Allee thresholds decrease or increase
with warming when the Allee effects are strong? The two
models I examined in this study provide contrasting results.
979
 (a) (b) 140
10
10
8 6
4 120
8
100
Protandry: µF − µM

Allee threshold
6 80
95
7 3
60
4
40
2
2 20

0 0
2 4 6 8 10 10 15 20 25 30
Standard deviation: σM = σF Temperature T

(c) 140 (d) 140

120 120
p = 0.8
100 p = 0.6 100
Allee threshold

Allee threshold

p = 0.4 p = 0.8
80 80
p = 0.2 p = 0.6
60 p = 0.0 60 p = 0.4
p = 0.2
40 40 p = 0.0
20 20

0 0
10 15 20 25 30 10 15 20 25 30
Temperature T Temperature T

Figure 4. Dependence of the Allee threshold on (a) phenology of the gypsy moth and (b–d) temperature under various parameters affected
by temperature and several values of the pesticide efficiency p. In panel (b), only the female and male adult emergence distributions (i.e.
protandry µF – µM and maturation dispersion σM = σF; light gray), only the female–male encounter rate z (dark gray), or both adult emer-
gence distributions and z (black) are made temperature-dependent in the gypsy moth model, for p = 0.8 (solid lines), p = 0.6 (dashed lines)
and p = 0.4 (dash-dot lines); I note that p = 0.8 (80% larvae dying due to pesticides) corresponds to a realistic single continuous spraying of
the infested area by the bacterial pesticide Bacillus thuringiensis (Blackwood et al. 2012). In (c), only the male and female background mor-
tality rates dM and dF, respectively, are made temperature-dependent in the gypsy moth model. Panel (d) then demonstrates the net effect of
temperature, since here µF – µM, σM = σF, z, dM and dF are all assumed temperature-dependent. The temperature profiles are calculated from
Eq. 10, 11 and correspond to Logan, WV, USA; the yearly average maximum temperature in Logan is 19.89°C (dotted vertical line in
panels (b–d)). In panel (a), the Allee threshold increases in the direction from dark blue to dark red.

Whereas the Allee effect driven by predation generally weak-
ens and the Allee threshold tends to decrease when tempera-
ture increases, the model with the Allee effect due to need
of finding mates predicts that the Allee threshold should
increase with warming. These contrasting results likely reflect
different mechanisms that trigger individual Allee effects
and hence different temperature-dependent parameters. For
the model with predation-driven Allee effect, the metabolic
theory suggests that warming increases the per-unit-bio-
mass prey growth rate faster than the predator attack rate.
Increasing temperature thus weakens the Allee effect. For the
model with mate-finding Allee effect, warming increases the
mating rate, via increasing female−male encounter rate and
modifying female and male adult emergence distributions.
However, it increases male and female mortality rates, too
and the net effect is a stronger Allee effect. This summary is
overstating the simplicity of the results a bit, since I also show
that changes in the predator biomass-density BC in the first
model and in the pesticide efficiency p in the gypsy moth
model may under some circumstances reverse these predic-
tions. Nevertheless, given that there are many aspects of an
organism’s fitness that might change with temperature, it pro-
vides a neat way of generalizing across these from the two
model examples examined in this study.

980
 The assumption of constant predator biomass-density BC
behind the predation model 1 is a reasonable approximation
e.g. when the predator’s assimilation efficiency is low and/
or the predator is a generalist with dynamics largely depen-
dent on other, unstudied prey species (Gascoigne and Lipcius
2004, Berec et al. 2018). Alternatively, one may think of the
predator as a biocontrol agent and of BC as a level of preda-
tor density-biomass maintained by releasing these agents to
establish a new or augment a naturally occurring population
(van Lenteren 2012). This interpretation makes possible to
see both examined models as containing a population control
means (biocontrol agent versus pesticide) and discuss how its
use affects pest species dynamics when temperature increases.
In the first model, it is necessary to keep track of decreas-
ing Allee thresholds by increasing BC. Similarly, in the second
model, it is necessary not to let pesticide efficiency deteriorate
too much, in view of this possibility being reported (Musser
and Shelton 2005). This reasoning also indicates that aug-
mentative pest control may perhaps be not as effective as
using pesticides or disrupting mating, an inference already
made by Blackwood et al. (2012) in a somewhat different
context.
It is worth emphasizing that the predictions of the pre-
dation model would be reversed (i.e. the Allee effect would
strengthen with warming) also if the activation energy of the
predator attack rate a exceeded that of the per-unit-biomass
prey growth rate r, Ea > Er . From the pest control (or even
pest eradication) perspective, an increase in the Allee thresh-
old with temperature may generally be perceived as some-
thing positive (higher Allee thresholds mean more effective
pest control; Tobin et al. 2011). On the other hand, an
increase in the Allee threshold with warming would imply
elevated extinction risk of populations also in their native
habitats where this should be prevented, even if only to pre-
serve native biodiversity.
The findings based on the predation model 1 suggest that
the perception of impacts of climate change depends in part
on how one quantifies risk or resilience. On one hand, the
Allee threshold declines with warming and hence the critical
biomass-density below which the population goes extinct.
However, at the same time the prey equilibrium biomass-
density decreases at a higher rate than the Allee threshold.
Consequently, their difference, a common measure of popu-
lation resilience (Meyer 2016), declines, too. Perturbations
from the prey equilibrium biomass-density, likely of increas-
ing importance as climate change will continue, may thus
threaten a population more as temperature increases despite
decreasing Allee thresholds. Even though this prediction
holds specifically when the prey carrying capacity K declines
with warming as predicted by the metabolic theory of
ecology (Brown et al. 2004), it points to a possibility that
predictions of the effects of climate change on population
dynamics may more generally depend on how we quantify
risk or resilience.
The Allee slope is a recently introduced Allee effect char-
acteristic that aims to describe behavior of the per capita
population growth rate in the vicinity of Allee threshold
(Walter et al. 2017). It can be thought of as a measure of how
fast the population can get away from the Allee threshold
when it occurs close to it or how resistant it is to repeated
small-scale perturbations that push the population close to
the Allee threshold (Meyer 2016). The Allee slopes were
found to increase with warming in the predation model 1,
making smaller Allee thresholds more identifiable and popu-
lations running out of them faster. It is not difficult to show
that for model 1 the Allee slope increases with the square
of per-unit-biomass prey growth rate r, which in turn not
only increases with temperature but has the largest (even in
the absolute value) activation energy. Hence, it is r that pri-
marily determines how the Allee slope responds to warming.
With higher Allee slopes, it may be easier to tune population
management around Allee thresholds and better protect the
endangered populations as well as better fight the unwanted
ones. Allee slopes thus appear to be an important characteris-
tic of Allee effects (Walter et al. 2017).
Up to now, just a single study appears to have examined
an effect of warming on Allee effects. Outcomes of a detailed
model describing the life history of invasive cladoceran
Bythotrephes longimanus suggest that as water temperature
will increase the Allee threshold will decrease, facilitating
Bythotrephes invasions into non-native habitats as global
warming proceeds (Wittmann et al. 2011). This prediction
falls in line with the results of predation model 1 that Allee
effects become weaker and the Allee thresholds smaller as
climate change continues. Hopefully further specific as well
as general models will be developed in which responses of
Allee effects to warming are under scrutiny. One such ave-
nue could consider responses of Allee effects to changes in
temperature variability. Indeed, in some environments popu-
lations were found affected more by changes in climate vari-
ability than in climate mean (García-Carreras and Reuman
2013) and increases in environmental variance were found
to alter or even reverse effects of changes in environmental
mean (Lawson et al. 2015). Despite recent interest in impacts
of environmental noise variance and color on the popula-
tion extinction risk (Ovaskainen and Meerson 2010, van
de Pol et al. 2011, Mustin et al. 2013), just a single study
considered a population subject to an Allee effect. This study
showed that as the noise became increasingly autocorrelated
the mean time to population extinction decreased (Levine
and Meerson 2013). However, to make their analysis trac-
table, Levine and Meerson (2013) somewhat unrealistically
assumed that the Allee threshold and carrying capacity were
quite close to one another. Impacts of environmental noise
variance and color on populations subject to an Allee effect
thus still await exploration.
Acknowledgements – Funding – I acknowledge funding by the
Grant Agency of the Czech Republic (grant no. 15-24456S) and
institutional support RVO:60077344 from the Biology Centre.
Conflicts of interest – I declare I have no conflict of interest.
981
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