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Behavioral Ecology and Sociobiology (2021) 75:115
https://doi.org/10.1007/s00265-021-03054-9
ORIGINAL ARTICLE
Fear ofsex: sexual conflict exposed asavoidance inaparthenogenetic
invertebrate
MarcusLee1 · CarlotaSolanoUdina1,2 · Lars‑AndersHansson1
Received: 22 March 2021 / Revised: 7 July 2021 / Accepted: 13 July 2021
© The Author(s) 2021
Abstract
Males and females often have divergent evolutionary interests, generating sexual conflicts. This is particularly true in organ-
isms that exhibit facultative sexuality, whereby females are capable of reproducing without fitness costs of mating. Here, we
provide the first documented evidence with quantitative tracking showing that sex interacts with social context to determine
space-use of females, in a pattern resembling predator avoidance. To achieve this, we labelled Daphnia magna with fluores-
cent nanoparticles and utilized a 3-D tracking platform to record pairs of individuals swimming. The recordings comprised
either same-sex or opposite-sex pairings. We found that females swam faster, deeper, more horizontally, and more linearly
when exposed to males than when exposed to females. Simultaneously, we found that male behavior did not differ depending
on swimming partner and, importantly, we observed no sexual dimorphism in swimming behaviors when swimming with
the same sex. Our results suggest that the presence of males in a population has the potential to influence the distribution of
individuals, similarly to known threats, such as predation. This highlights that sexual conflict has clear spatial consequences
and should be considered in such ecological frameworks, like the Landscape of Fear (LOF) concept. In a broader context,
the connection of the evolutionary and social concept of sexual conflict and the ecological concept of LOF may improve
our understanding of population dynamics and the spatial and temporal distribution of individuals in natural ecosystems.
Signicance statement
Despite the wealth of studies that detail how predators affect their prey’s spatial behaviors, studies on the role of sex and
social context on spatial behavior are rare. Addressing this dearth of information, we studied the swimming behaviors of
an organism that can reproduce with or without sex, when exposed to an individual of either the same or opposite sex. We
found no difference between the sexes in swimming behaviors; however, we revealed that females avoided males by swim-
ming deeper in the water column, reminiscent of the response to predation. Our results highlight that social conflict between
the sexes strongly affects the demographics of a population and may therefore have a substantial role in the spatial ecology
of organisms in the wild.
Keywords Spatial ecology· Daphnia magna· Landscape of Fear (LOF)· Predation risk· Intersexual conflict
Introduction
A central challenge in ecological research is to understand
the mechanisms behind differences in inter- and intraspecific
spatial and temporal distributions of organisms. Interspecific
Communicated by D. J Hosken.
Marcus Lee and Carlota Solano Udina contributed equally
* Marcus Lee
marcus.lee@biol.lu.se
Carlota Solano Udina
carlota.solano.udina@upm.es
Lars-Anders Hansson
lars-anders.hansson@biol.lu.se
1 Department ofBiology, Aquatic Ecology, Lund University,
Lund, Sweden
2 Departamento de Sistemas y Recursos Naturales,
Universidad Politécnica de Madrid, Silwood Park, Madrid,
Spain
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Behavioral Ecology and Sociobiology (2021) 75:115
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differences are predominantly caused by competitive inter-
actions or governed by predator distribution and behavior.
For example, elk (Cervus elaphus) move from grassland to
forested areas due to the presence of wolves (Canis lupus),
or dugongs (Dugong dugon) utilize deeper waters to avoid
predation from shallow water inhabiting tiger sharks (Gale-
ocerdo cuvier) (Wirsing and Ripple 2011). With respect to
intraspecific differences in distribution, sexual segregation is
well-documented across many different taxa (Ludynia etal.
2013; Wang etal. 2018; Zak etal. 2020). Various causal
mechanisms have been proposed, such as dimorphism cre-
ating different nutritional requirements, thereby segregat-
ing males and females outside the breeding season (Li etal.
2017), or avoidance of male harassment by females that have
already mated (Ide 2011). Therefore, a general pattern may
be that the intraspecific distribution of individuals might
differ as a result of sexual conflict.
All taxa that reproduce sexually are likely to encounter
some form of sexual conflict (Parker 1979), suggesting that
the outcome of male–female interactions has divergent evo-
lutionary optima for the two sexes (Chapman etal. 2003).
Due to the impact of sexually antagonistic evolution, sexual
conflict has been espoused as a major mechanism of evo-
lution (Hosken and Snook 2005), with the ultimate conse-
quences being the potential to lead to divergence within and
between species (Parker and Partridge 1998; Gavrilets etal.
2001; Chapman 2018; Janicke etal. 2018). Such conflicts
between the sexes can occur over various traits, including
mating frequency, fertilization, and clutch size (Chapman
etal. 2003). Generally, it is assumed that males benefit from
maximizing such traits like mating frequency; however,
females should favor lower mating rates due to the costs
of sex (Gavrilets etal. 2001). These costs arise from many
sources such as increased infection rates from contact with
conspecifics (Thrall etal. 2000), fitness reducing seminal
fluid accessory gland proteins introduced during copulation
(Wigby and Chapman 2005), physical damage due to trau-
matic insemination (Stutt and Siva-Jothy 2001) or due to
penile structures that prevent females escaping during copu-
lation (Lange etal. 2013), increased energy demands (Nicol
etal. 2019), and even increased predation risk (Magnhagen
1991).
One strategy females may employ to minimize such
costs of mating is to avoid superfluous copulations such as
if already mated. This is hypothesized to be more preva-
lent when the cost of mating is high and, therefore, females
are more likely to be selective (Bleu etal. 2012). In most
populations, irrespective of the fitness costs of mating, the
requirement to mate in order to achieve any “fitness” may
dampen the strength of these avoidance behaviors. In facul-
tatively sexual populations however, females are potentially
decoupled from the obligation to mate due to being able
to reproduce asexually (Brewer 1998; Gerber and Kokko
2016). This may then lead to strong behavioral avoidance
of males due to the potentially strong costs associated with
mating. In such populations, it has been colorfully stated that
the sequence of events in male behavior during reproductive
attempts is fundamentally indistinguishable from predation
attempts (Gerritsen and Strickler 1977; Brewer 1998). If
true, this suggests that the male poses a potential risk to fit-
ness for the female and consequently, the demographics of a
population may have a substantial role in the spatial ecology
of the population.
Daphnia magna is a common facultatively sexual fresh-
water cladoceran. Predominantly, Daphnia reproduce asexu-
ally but under certain suboptimal environmental conditions,
such as at high population densities, they often switch to
a sexual reproductive phase (Kleiven etal. 1992; Haltiner
etal. 2020). This switch means that they produce a maxi-
mum of 2 genetically non-identical eggs through recombina-
tion, instead of bearing an asexual clutch of up to 110 live
clones (Gerber etal. 2018). Change in reproductive mode is
not a one-way street, and females can continue to alternate
strategies between broods. Therefore, females may be under
strong pressure to avoid potentially costly mating events if in
the asexual phase or already mated, and could conceivably
adopt different swimming behaviors as a proactive avoidance
measure. Multiple studies have investigated how swimming
behaviors differ between sexes of many cladocerans (D. puli-
caria (Brewer 1998); D. obtusa (La etal. 2014); Polyphe-
mus pediculus (Butorina 2000); Chydorus sphaericus (Van
Damme and Dumont 2006)); however, most studies inves-
tigate interactions between the sexes, and therefore focus
on group behavior or the mating behavior in high density
environments. To the best of our knowledge, no studies have
investigated how changes in the sex ratios affect an individ-
ual’s swimming behavior, leading to that our understanding
of sexual conflicts in a spatial context is still elusive.
Hence, the purpose of our study is to disentangle the indi-
vidual behavioral responses of D. magna in the presence of
conspecifics. We hypothesize that the potential reduction
in fitness due to sexual reproduction will cause females to
display avoidance behaviors when paired with males. Using
3-D tracking of individual animals, we were able to quantify
the speed at which males and females swim, their average
swimming depth, and the tortuosity (or the linearity) of their
swimming paths, i.e., we were able to map the individual
behavior in different social contexts.
Specifically, we expect that due to the sexual dimorphism
in size (Mitchell 2001), females will swim faster than males,
and when swimming with the opposite sex, this speed will
increase. Similarly, due to depth serving as a refuge from
many threats, such as predation and ultraviolet radiation
(UVR) (Hansson and Hylander 2009b; Ekvall etal. 2015,
2020), we predict that females exposed to males will swim
deeper in the water column than either males or females
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Behavioral Ecology and Sociobiology (2021) 75:115
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swimming with females. Multiple observations of zooplank-
ton have described male “scanning” behavior which involves
males swimming more horizontally than vertically in a bid
to increase encounter chance with a female (Gerritsen 1980;
Brewer 1998). Therefore, we predict that males will swim
more linearly and more horizontally than females, with this
effect being more pronounced when swimming with the
opposite sex. In short, using 3-D tracking, we are able to
provide the first insights into how sexual conflict interacts
with an individual’s social context, thereby causing spatial
variation in swimming behavior.
Methodology
Culture conditions
D. magna used in this experiment were isolated from a
laboratory culture on the 12 August 2019, which was origi-
nally inoculated with several genotypes from a population
in Lake Bysjön (55.6753 lat, 13.5452 long) in southern
Sweden. They were maintained at high densities in a 400-L
plastic mesocosm at 20°C with a 16h:8h light:dark photo-
period and routinely fed with a predominantly Tetradesmus
obliquus (formerly Scenedesmus obliquus) algal suspension.
Once isolated, D. magna were sexed using a stereomicro-
scope (Olympus SZX7, Japan). Males were identified by
three characteristic morphological traits: (1) the smaller
and rounder rostrum in comparison to females, (2) the elon-
gated and motile antennules, and (3) the pronounced hook
at the end of the first leg (Mitchell 2001). Females were
identified by the absence of these traits. The sex ratio of the
initial population was approximately 10:1 (female:male).
After being sexed, D. magna were maintained in single sex
populations of 30 individuals per liter at the same tempera-
ture and photoperiod as the source population and fed with
the same algal suspension adlibitum until being assayed.
The behavioral assays took place over the period of 21–23
August 2019, that is, individuals were only isolated within
their own sex for between 9 and 11days; therefore, later
exposure to the opposite sex was not a novel experience.
Experimental design
In order to determine swimming behaviors of individual
Daphnia, we used a proven protocol (Ekvall etal. 2013;
Palmér etal. 2016; Langer etal. 2019). This required label-
ling each individual with either red or yellow nanoparticles
(Qdot™ ITK™ Carboxyl Quantum Dots; Life Technolo-
gies Corporation, USA) that fluoresce when excited by blue
light (465nm). This allowed us to identify both recorded
individuals simultaneously. The labelling process involved
binding the quantum dots to the carapace of the organism
by incubating individual Daphnia in 2-ml centrifuge tubes
with 250-µl aged tap water and 33-µl quantum dot labelling
solution for 1h in the absence of light, before removing the
excess solution by rinsing the organism with aged tap water
(Langer etal. 2019). Once the Daphnia were labelled, they
were recorded in a Plexiglas aquarium (0.2 × 0.2 × 0.75m;
filled with only aged tap water) with four cameras (Pike
F-210C color cameras, Allied Vision Technologies GmbH)
positioned as vertical stacked stereopairs towards the aquar-
ium to allow 3-dimensional positioning to be acquired, and
the only light source was a lighting array above supplying
blue light–emitting diodes with peak emission at 465nm
(VANQ Technology). The surface light intensity was
223.4μmol m−2 s−1 at the top and 78.2μmol m−2 s−1 at the
bottom (see Langer etal. 2019) which has previously been
equated to a night-like condition (Ekvall etal. 2020). To dis-
cern the effects of conspecific sex on an individual’s swim-
ming behavior, the Daphnia were recorded in pairs. This
produced three sex combinations or “treatments”: females
recorded with females (n = 19), males with males (n = 20)
and females with males (n = 22). The pairs of individuals
were obtained from separate holding aquaria (see above),
and introduced to the tracking aquarium simultaneously.
They were given 1min of acclimatization before the 3-min
recording began. This setup allowed us to extract multiple
metrics of swimming behavior, such as the individual’s
speed, depth, horizontal direction changes (horizontal net
displacement ratio [HNDR]), and the tortuosity of their
swimming path (net gross displacement ratio [NGDR]), as
well as calculating the distance between individuals. The
water was then replaced between trials to prevent lingering
chemical cues influencing subsequent recordings. Due to the
nature of the experiment, blinding was not possible.
Data handling andstatistical analysis
We used a custom-built MATLAB application (Palmér etal.
2016; The MathWorks, Inc. 2017) to extract the Daphnia’s
3D positions from the recordings. Using the 3D coordinates,
depth was extracted as Z coordinates, and speed was calcu-
lated as the gross distance travelled every second. HNDR
was calculated as the ratio of horizontal distance travelled
to the gross distance travelled every second. Similarly, the
NGDR was calculated as the ratio of net distance travelled
to the gross distance travelled every second. Therefore, for
either ratio, the more vertical or indirect the swimming path,
the lower the ratios, and conversely, the more horizontal or
linear the path, the higher the HNDR and NGDR, respec-
tively. Due to the recording frame rate (6 fps) producing
between 360 and 1080 points per variable, all variables were
averaged using the median values as to limit the influence
of extreme values. Henceforth, all “averages” discussed
refer to the median. Statistical analysis was subsequently
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Behavioral Ecology and Sociobiology (2021) 75:115
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conducted in R version R v3.6.2 (R Core Team 2019). Fig-
ures were also drawn with R v3.6.2 utilizing the package
“ggplot2” (Wickham 2016). The data and code for this study
are archived online (Lee etal. 2021a, b).
To examine the effects of sex and conspecific sex on
speed, we performed a linear mixed model using the pack-
age “nlme” (Pinheiro etal. 2021). Average speed served as
the dependent variable, and “sex,” “conspecific sex,” and
their interaction were used as fixed effects with the record-
ing ID serving as a random effect to account for the non-
independence of recording individuals in pairs. Size was
also included as a covariate for the analysis of average speed,
due to larger individuals having the potential to swim faster
(Dodson and Ramcharan1991; Hylander etal. 2014). Due
to the physical constraints of the experimental arena, we
treated the average depth as a ratio of vertical position for
the analysis, i.e., occupied depth in relation to of the total
available depth. As depth, horizontal movements (HNDR),
and tortuosity (NGDR) variables represent ratios derived
from continuous numbers, we employed beta regression
mixed models (Douma and Weedon 2019). “Sex,” “con-
specific sex,” and their interactions were also used in these
models as fixed effects with the recording ID as a random
effect. All models were graphically investigated, and the
examination of significant differences in main effects was
conducted using the post hoc Tukey’s test. In the case of the
dependent variable depth, we note that the model appears
over-dispersed; however, other forms of modelling provide
less accuracy due to the methodological design. To provide
easier interpretation of the results, we back transformed the
depth variable to show actual depth as opposed to a ratio of
vertical position.
Results
Speed
Swimming speed was, as expected, influenced by size
with larger individuals swimming faster than smaller ones
(Table1; online resource Fig. S1.). Yet, when accounting
for size, we found no single effect of sex on swimming
speed. There was, however, an effect of swimming partner
on the speed, as different sex pairs show distinct speeds,
while same-sex pairs show no difference. Importantly, we
observed a strong interaction between sex and the swimming
partner. This effect was entirely driven by the females swim-
ming faster when swimming with a male than with a female
(Tukey’s test; p = 0.003). Specifically, females from same-
sex pairs swam approximately 32% slower than females
swimming with the opposite sex (Fig.1a). Males did not
adjust swimming speed with different swimming partners
(Tukey’s Test; p = 0.93) swimming at 13.81mm s−1 (± 1.14
SE) with females and 13.05mm s−1 (± 1.08 SE) with other
males.
Depth
Swimming partner also influenced the focal individual’s
swimming depth whereby same-sex pairs swam higher in
the water column than opposite sex pairs (Table2). There
was also evidence that males preferred swimming higher
in the water column than females. Similar to speed, there
was a clear interaction effect of sex and swimming partners
with females having an estimated mean swimming depth of
586mm (± 38 SE) when swimming with a male, whereas
swimming with another female averaged 379mm (± 39
SE) (Tukey’s test; p = < 0.001), that is, females swam 64%
deeper in the presence of a male than of a female (Fig.1b).
Males however had similar depth preferences irrespective of
the swimming partner’s sex (Tukey’s Test; p = 0.97).
HNDR
Horizontal movements (HNDR) did not conform to prior
expectations, since males swimming with females were less
likely to perform horizontal movements than their female
counterparts (Fig.1c). The sex of the swimming partner also
had a notable impact on the ratio of horizontal movements,
with females in same-sex pairs being less likely to perform
horizontal movements than with the opposite sex. The inter-
action of sex and swimming partner sex also emerged as
significant. This appears to be driven by females paired with
males, as they were 15% more likely to swim horizontally
than their male counterparts, or 11% more likely to swim
horizontally than females exposed to a female (Tukey’s tests;
p < 0.001 and p = 0.004 respectively). Males in comparison
did not differ in HNDR when exposed to a female or to a
male (Tukey’s test; p = 0.99).
Table 1 Linear mixed-effects
model results with recording
ID as the random effect using
the lme function to account for
the heterogeneity in variance
among groups
Fixed effects Estimate s.e d.f t value Pr ( >|t|)
Average speed Size 7.72 3.14 59 2.461 0.017
Sex -0.84 1.91 59 -0.443 0.66
Conspecific sex -4.67 1.27 58 -3.684 < 0.001
Sex × conspecific sex 3.91 1.71 58 2.289 0.026
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Behavioral Ecology and Sociobiology (2021) 75:115
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NGDR
The tortuosity (NGDR) of an individual’s swimming path
showed considerable influence of all main fixed effects.
Female Daphnia exposed to a male were more likely to have
linear swimming paths than their male partners (Fig.1d),
and female same-sex pairs were also more likely to swim
more linearly than females with males. The interaction
Fig. 1 Effects of sex and
conspecific sex on various
metrics of swimming behavior
in Daphnia magna. The sub-
plots refer to (a) average speed
considering size as a covariate,
(b) average depth, (c) average
ratio of horizontal to vertical
movements (HNDR) with 1
being completely horizontal and
0 being completely vertical, and
(d) the average net to gross dis-
placement ratio (NGDR) with
higher values indicating a lower
turning rate. All subplots show
the model estimates ± 2 SE with
raw values (individuals) plotted
as faded points. The dashed
lines in subplot (b) represent the
boundaries of the water column
Table 2 Results from
generalized linear mixed-effects
beta regression models with
variable ϕ
All models used the recording ID as a random effect
Fixed effects Estimate s.e d.f z value Pr ( >|z|)
Average depth Sex − 1.073 0.411 113 − 2.610 0.009
Conspecific sex − 1.252 0.368 113 − 3.406 < 0.001
Sex × conspecific sex 1.110 0.503 113 2.205 0.027
Average HNDR Sex − 0.717 0.171 115 − 4.185 < 0.001
Conspecific sex − 0.586 0.167 115 − 3.514 < 0.001
Sex × conspecific sex 0.556 0.217 115 2.558 0.011
Average NGDR Sex − 0.819 0.197 115 − 4.168 < 0.001
Conspecific sex − 0.462 0.192 115 − 2.411 0.016
Sex × conspecific sex 0.710 0.249 115 2.854 0.004
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between both sex and the sex of the swimming partner
yielded an effect, which once again was solely driven by
females paired with males. Females were approximately 15%
more likely to swim linearly than their male counterparts
(Tukey’s test; p < 0.001).
Discussion
Sexual conflict is a widespread social phenomenon among
sexually reproducing organisms with the potential to shape
macroevolutionary patterns (Bonduriansky 2011). Despite
the prevalence of obligately sexual organisms, there are
numerous examples of alternative reproduction strategies,
including facultative sexuality (Burke and Bonduriansky
2017; Kobayashi 2019) among, for example, numerous
common and globally distributed organisms, such as many
crustacean taxa. Here, we show that facultatively sexual
D. magna females modify their behavior when exposed
to males, swimming faster, deeper, more horizontally, and
straighter than when exposed to other females. In contrast,
males do not alter swimming behavior depending on their
swimming partners’ sex. This finding suggests that the costs
of sexual reproduction for females trigger their avoidance of
conspecific males.
Past studies of the genus Daphnia have frequently looked
at mating behaviors, and generally focused on how males
increase their probability of encountering a female (Brewer
1998), neglecting how females act in these situations. This
is often a consequence of the methodological design, which
requires both males and females to be present in order to
observe potential mating events. However, in nature, there
are often times when males will be absent and curiously, few
studies use single sex populations as controls, and yet extract
and discuss the behavior of females (Brewer 1998). Here, we
provide this missing information and observe single sex and
opposite sex pairings.
In several studies, it has been discussed that D. pulicaria
males swim twice as fast as females in a bid to increase
encounter rates via “scanning” behaviors similar to other
zooplankton taxa (Brewer 1998). The scanning behaviors
are characterized by more horizontal and linear movements
(Gerritsen 1980), and have even been suggested to be wide-
spread in the planktonic community as they are found in
copepods from both marine and freshwater environments,
as well as in Daphnia species (Gerritsen 1980; La etal.
2014). Intuitively, this appears logical as, if males can
exploit a single plane with relatively straight movements, it
increases the probability of encountering randomly distrib-
uted resources, such as females (Dusenbery 1992; Visser
2007). D. magna, however, do not appear to echo this pattern
as, when accounting for size, we show here that males do
not swim faster than females, and only females alter their
speed according to their swimming partners. Moreover,
we observed that females appear more likely to perform
more horizontal and straighter movements when exposed to
males, although we cannot exclude that this may be an arte-
fact since females cannot swim further in the vertical plane
when reaching the bottom and were therefore forced to swim
more horizontally. Despite this, males do not appear to differ
from females when in same-sex pairings nor when paired
with a female, which supports our view that this “scanning”
behavior does not occur in D. magna and calls into question
whether this is indeed a widespread behavior in zooplank-
ton (Brewer 1998). Instead, our results give credence to the
notion that males’ likelihood of reproducing relies heav-
ily on chance encounters with sexually responsive females
(Kawatsu 2013; Gerber and Kokko 2016).
Despite the lack of similarity in the previous swimming
behaviors recorded with other species, the use of depth as
a refuge is well described for D. magna. They use deeper
waters to attenuate harmful ultraviolet radiation (UVR) and
avoid predation from visually hunting predators, such as fish
(Hansson and Hylander 2009b). Similarly, our data show
that female Daphnia respond to males in a pattern resem-
bling a threat response (online resource Fig. S2), i.e., the
female avoids the male by diving deeper. Despite the clear
overall response, not all females resided deeper in the water
column. This variation in optimal depth may be a result of
sexual receptivity, although we cannot rule out other fac-
tors such as genetic variation or energetic state which likely
contribute to this trait. Interestingly, males did not display
a propensity to follow the majority of females to the deeper
waters, which strengthens findings from previous studies
showing males to only be able to follow females for a few
body lengths (Brewer 1998); however, to what degree this
is male sensory limitations or choice in pursuit is unknown.
Furthermore, we did not observe any explicit following of
partners in any treatment group when looking at the distance
between individuals (data not shown).
The consequences of the observed avoidance may
have far-reaching effects on the population dynamics. For
instance, the energetic cost of performing avoidance behav-
iors has been demonstrated to reduce population growth in a
facultatively sexual invertebrate (Nelson 2007). Also, male
Daphnia in particular have been shown to be more positively
phototactic than females (De Meester 1993), which suggests
they inhabit higher strata than females, which may thereby
explain the female use of depth as a refuge, as shown in our
study. However, for the females inhabiting deeper waters,
there are further potential metabolic costs. For example,
if in a sufficiently deep lake, the temperature gradient in
the deeper waters may reduce metabolic rates (Dawidow-
icz and Loose 1992), coupled with lower food availability
and quality, which suggests that population growth would
be retarded. That said, it is well established that D. magna
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Behavioral Ecology and Sociobiology (2021) 75:115
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perform diel vertical migration (DVM) as a foraging strat-
egy to avoid the higher predation risk and UVR during the
day, foraging in the food-rich surface waters during the
night (Hansson and Hylander 2009a, b). This strategy could
mitigate some of the potential costs of males inhabiting the
higher strata, especially if mating success is increased with
light availability. Under this scenario, our results suggest
that sexual conflict could be a further selective pressure con-
tributing to the evolution of this DVM behavior.
In accordance with our findings, the sequence of events
by males during reproductive attempts has previously
been mentioned as being indistinguishable from preda-
tion attempts (Gerritsen and Strickler 1977; Brewer 1998).
Predator–prey interactions in a spatially explicit context
have been extensively studied (Miller etal. 2014; Fortin
etal. 2015; Schmitz etal. 2017), whereas the spatial ecol-
ogy of sexual conflict has received relatively little attention.
An emergent framework within the predator–prey domain
aimed at clarifying and refocusing the effort to understand
the spatial effects of risk is the “Landscape of Fear” (LOF)
(Laundré etal. 2001, 2010, 2014; Brown and Kotler 2004;
Gaynor etal. 2019). The LOF has been defined as the spatial
variation in prey perception of predation risk. In order to
proactively minimize such risks, the LOF concept suggests
that two behavioral strategies may be employed, and they are
(1) avoiding areas of high predation risk and (2) modifying
behavior in a location to reduce the probability of predation
(Gaynor etal. 2019). Replacing the word “predation” with
“mating,” we see that Daphnia do indeed avoid areas of
high risk, i.e., where males are located. Therefore, based on
the potential for sexual conflict in this facultatively sexual
species (Gerber and Kokko 2016), we suggest that wher-
ever there are probable fitness costs, this framework could
be applied. Our results highlight that demographic features
such as reproductive mode or sex ratios which vary over the
season may be an important factor in the perception of risk
for female individuals and is an avenue for further research.
In conclusion, we observe here that males and females of
D. magna lack sexual dimorphism in swimming behaviors.
However, when in the presence of the opposite sex, females
demonstrate behaviors consistent with strong male avoid-
ance, leading to a skewed depth distribution among sexes.
These avoidance behaviors are analogous to other threat
responses, such as to predation risk or ultraviolet radiation,
which have been shown to have fitness consequences. There-
fore, we advocate that incorporating predominantly evolu-
tionary concepts, such as sexual conflict, to the ecological
frameworks, like the Landscape of Fear, has the potential to
improve our understanding of the mechanisms determining
the distributions of individuals in space and time.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s00265- 021- 03054-9.
Acknowledgements We would like to thank Giuseppe Bianco and
Charlie Cornwallis for helpful discussions. We would also like to thank
Kevin Jones for experimental assistance.
Author contribution All authors conceived the project and contributed
to writing. CSU and ML collected data. ML performed the data analy-
sis and wrote the first version of the manuscript.
Funding Open access funding provided by Lund University. Financial
support was provided by the Swedish Research Council (VR) grant #
2016–03552 and the Royal Physiographic Society.
Data availability Data supporting the results are available online in
the Dryad data repository at https:// doi. org/ 10. 5061/ dryad. 2ngf1 vhm8.
Code availability The code used to analyze the data is available online
in the Zenodo repository at http:// doi. org/ 10. 5281/ zenodo. 51127 15.
Declarations
Ethics approval All animal handling and husbandry was conducted in
accordance with approved institutional guidelines. The license M182-
15 was granted by the Malmö/Lund authority for ethics of animal
experimentation.
Consent to participate Not applicable.
Consent for publication Not applicable.
Conflict of interest The authors declare no competing interests.
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