Disscussion
We report for the first time personality in a natural population of the
damselfly C. splendens measured in the wild. We show
cross-context repeatability in most of the traits studied. Traits
related to both courtship and boldness axes showed repeatability values
close to the average value of behavioural repeatability across over 750
studies of various behavioural traits and taxa (Bell et al., 2009). Our
research responds to the need to study personality in natural field
conditions in order to assess ecologically relevant situations and
contexts (e.g. Archard and Braithwaite, 2010; Hertel et al., 2020).
Further, our study indicates that C. splendens is likely suitable
to become a model organism in behavioural studies.
Generally, individuals’ latency to approach a rival and number of bites
are one of the most commonly used indicators of aggressiveness and show
high repeatability in most studies (Keiser et al., 2018). In our case,
absence or low repeatability for both reaction to intruder and number of
bites (Tab.2), are in contrast to that trend, and are also in contrast
to an earlier meta-analysis (Bell et al., 2009). However, in crickets,
Fitzsimmons and Bertram (2013) showed low repeatability of aggression
scores (quantified from the duration and frequency of agonistic
behaviours during contest). The authors suggested that the trait
plasticity was an effect of social environment as well as the insect
physiology (Fitzsimmons and Bertram, 2013). In our study, the intruder
male was chosen randomly, and we did not take measures of their
physiological condition, which might have been useful for a deeper
understanding of our result. Also, we propose that future studies should
be using a mirror (e.g. Balzarini et al., 2014) instead of an actual
rival, and that this would bring more controlled and comparable metrics
of aggression. In the case of banded demoiselle, the time needed for
reaction to rival male might also be strongly influenced by the social
environment (Bell et al., 2009). In this species antagonistic behaviours
depend on whether the potential rival male is a neighbour, a wandering
male or an actual opponent. It has been shown that neighbouring
territorial males avoid contest (Briffa and Weiss, 2010; Golab et al.,
2017; Gordon, 1997; Maynard Smith and Parker, 1976). Also,
non-territorial C. splendens males show a characteristic
wandering behaviour, that is, patrol larger sections of a river looking
for territories or mates. During this activity non-territorial males may
either pass a given territory, approach the resident and retreat
immediately or approach and initiate a conflict of varying intensity
(Koskimäki et al., 2009; Panov and Opaev, 2013). Resident males have to
evaluate which of the three type of males he is facing for every
interaction and react adequately to the situation.
With regard to biting an intruder, based on our data and earlier
studies, we suggest that this trait probably is unsuitable for
personality measures. The biting behaviour requires a situation when the
head (mandible) of the resident male approaches the part of the
opponent’s body that is ‘suitable for biting’. In aerial contest (Marden
and Waage, 1990) biting the intruder may arise by chance, depending of
the direction/intensity/frequency of the chasing damselflies movements.
Also, some parts of the body may simply be harder to bite, for instance
the centre of a wing area. Additionally, despite the fact that
dragonflies have one of the most advanced visual systems among insects
(Bybee et al., 2012) and can compute flight trajectory of their prey
(Olberg, 2012) there is no evidence that odonates would be able to
compute their opponents body movements during fighting in order to
precisely bite one another. Summarizing the above, we conclude that the
time for reaction to the opponent and number of bites in C.
splendens are plastic traits, depending on either social, environmental
or physical factors, or a combination of them all and hence are not
useful for personality studies in calopterygids.
In contrast, the number of hits seemed to be a better proxy of
aggression in C. splendens in the wild. Generally,Calopteryx spp. males compete for resources during aerial
contests (Marden and Waage, 1990), but most of the disputes are brief
pursuit flights after which an intruder is chased away. During escalated
longer aerial fights some collision or hitting can occur (Rüppell et
al., 2005; Golab pers. observ.). The above discussed results illustrates
the importance of choosing the right test for estimating a personality
trait (Sih and Bell, 2008) and developing multiple proxies for a given
behavioural axis might be crucial to identify the most suitable test for
the targeted trait in a given species (Carter et al., 2013).
The time a resident male needed to react to an approaching female showed
individual consistency (Tab. 2). The trait may appear similar to the
reaction to an intruder, which was not repeatable, but when reacting to
a female the resident male wants to attract rather than chase away
(Corbet, 1999). In addition, the two traits related to courtship: dive
display and engagement were also consistent and, as such, potentially a
good metric for personality. Consistent engagement to mating displays
has also been shown for instance in male guppies (Biro et al., 2016;
Magellan and Magurran, 2007). This is all in accordance with theory that
predicts consistency in mating behaviours since it reduces cognitive
costs for potential mates (Dall et al., 2004). Also, given that
personality traits are heritable (Korsten et al., 2013; Réale et al.,
2007) and the offspring environment is predictable, female (choosing
partner) can assess what behavioural traits would be adaptive for her
offspring and choose a sexual partner of a beneficial behavioural
profile. But on the other hand, highly variable or unpredictable
environments would favour behavioural plasticity rather than consistency
(Dingemanse et al., 2010). Hence, there are studies showing no
personality in mating-related behaviours as for example research on
subdominant reindeers, whose propensity to enter/visit mating group is
based on proximate factors such as the group sex ratio and a day of
mating season (Strong, 2015).
Among insects one of the most advanced personality research in the wild
has been conducted on crickets. In an interesting and large-scale
project “Wild Crickets” (https://www.wildcrickets.org/) a group
of researchers studied personality both in the field and in the
laboratory. They found that individual behavioural consistency is steady
over adult lifetimes (Fisher et al., 2015a) and that personality in
captivity not always predicts personality in nature (Fisher et al.,
2015b). This is in line with another study on crickets Gryllus
campestris showing that handling procedure in translocation experiments
may bias repeatability estimates (Niemelä and Dingemanse, 2017). In our
study we did not compare field with lab-based experiments. However,
since there is growing evidence that gene expression can be
significantly modified by environmental factors (Niemelä and Dingemanse,
2014) and artificial conditions can impose additional unnatural
stressors (Archard and Braithwaite, 2010), we conclude that field
studies are superior, in ecological relevance, compared to lab-based
experiments on most animals including adult calopterygid damselflies.
More specifically, the methods presented in this study are particularly
promising for studying adult damselfly behaviour since they reduced
handling trauma, did not influence natural/free behaviour of damselflies
during the observations (Golab – pers. obs.) and prevented damselflies
from adjusting/habituating to the procedure (Archard and Braithwaite,
2010; Hilfert-Rüppell, 1999).
One common difficulty when studying animal personality in the field is
controlling environmental heterogeneity (Bell, 2004; Dingemanse and
Réale, 2013; Quinn et al., 2009). In our experiments environmental
factors were natural and many were standardized for: microclimate
(sunlight penetration, air temperature, wind speed), water quality
(current, temperature velocity), composition and structure of
macrophytes (Gibbons and Pain, 1992; Guillermo-Ferreira and Del-Claro,
2011; Hilfert and Ruppell, 1997; Hilfert-Rüppell, 1999; Siva-Jothy et
al., 1995, 1995; Siva-Jothy and Hooper, 1995) and predation (Golab and
Sniegula, pers. obs., details in methods). This adds a robustness to our
results that often can be lacking in animal personality field-studies
due to varying environmental conditions.
Here we emphasise that Calopteryx spp. express other ecologically
important behaviours, beyond the “Big Five”(Keiser et al., 2018), that
could be potentially useful for future personality studies (Koski,
2014). These traits include: territory patrolling (Corbet, 2004; Golab
et al., 2017), gathering of non-territorial males (Golab et al., 2013)
and a very elaborated repertoire of courtship behaviours (Corbet, 2004;
Rüppell et al., 2005).
To summarize, our work is the first that demonstrate behavioural
repeatability in an adult damselfly in the wild. Our results suggest
that adult C. splendens is a very promising model organism for
studying insect personality under ecologically relevant natural
conditions. The species has an elaborate repertoire of behaviours that
can be easily observed and measured swiftly using only the naked eye. In
addition, they also have a strong site fidelity which enables controlled
and relevant manipulations of key environmental parameters. We suggest
that our study represents the natural variability that exists in studied
behaviours of this species. Two of the traits related to aggressiveness
were not consistent and should hence not be useful for personality tests
or experiments. This emphasises the need of proper trait selection when
aiming to understand ecological implications of differences in
individual behaviour.