Introduction
Animal personality, defined as inter-individual consistent differences
in behaviour across time and context has received growing interest in
the past two decades (e.g. Roche et al., 2016). Personality studies have
important ecological and evolutionary implications determining such
aspects as: space use, species geographic distributions, tendencies to
be invasive, response to environmental change, speciation rates, social
interactions and fitness consequences (e.g. Briffa and Weiss, 2010;
Lichtenstein et al., 2017, 2017; Sih et al., 2004). Repeatability is a
highly informative metric that provides a standardized estimate of
consistency of individuality, that is, personality (Roche et al., 2016).
However, several aspects of animal personality research currently face
intense criticism. For instance, there is a underrepresentation of field
studies compared to lab-based tests (Archard and Braithwaite, 2010).
Also, the amount of studies on invertebrate personality is drastically
disproportionate to the number of species and behavioural traits (e.g.
Kralj-Fišer and Schuett, 2014). Further, most studies concerns the “Big
Five” of animal personality (boldness, aggressiveness, sociability,
exploration and activity), ignoring other traits that may bring in-depth
understanding of the phenomena and the possible associations between
commonly and rarely measured traits (Koski, 2014). Finally, metrics of
the personality traits should be chosen with caution in order to be
applicable for a given study organism and to represent ecologically
relevant information (Carter et al., 2013).
Compared with the large number of laboratory experiments on captive and
captive-bred animals, few studies have focused on personality in the
wild (Archard and Braithwaite, 2010; Carere and Maestripieri, 2013;
Fisher et al., 2015b; Hertel et al., 2020). This skew is unfortunate
since lab-based experiments often are affected by a number of
constraints: e.g. captivity stress, selective trapping, learning,
homogeneity of the laboratory environment, artificial and relaxed
selection and reduced pool of potential mates (reviewed by Archard and
Braithwaite, 2010). As a consequence, individuals in laboratory
conditions may behave in ways not representative for the natural
environment and hence showing ecologically irrelevant behavioural
patterns (Niemelä and Dingemanse, 2014).
Because of this potential for ecologically irrelevant behavioural
patterns in the lab it is important to validate the relevance of
findings in the lab with corresponding field studies. Studies designed
to compare lab-based and field-based assessments of personality show
different results, some fail to find any correlations between lab and
field behaviour whereas others provide similar personality estimates in
the two environments. For example, studies on crickets showed
repeatability of exploration and activity both in laboratory and natural
conditions. However, shyness was repeatable in artificial conditions
only (Fisher et al., 2015b). Study on zebra finches showed personality
both in laboratory and field conditions, but there was no correlation
between the two situations (McCowan et al., 2015). In a recent example
on sea anemones, Osborn and Briffa (2017) showed that the transition
from field to laboratory environment might influence personality
assessments. Results from this kind of transplant experiments can
therefore be biased by the translocation itself (Niemelä and Dingemanse,
2017). On the other hand, studies on great tits (Cole and Quinn, 2012)
or striped mice (Yuen et al., 2016) showed that individuals behaved
consistently both in the laboratory and field. The above examples denote
that well-designed assessment of personality in a model organism
measured in natural field conditions may be of high applicability for
understanding the ecological and evolutionary consequences of animal
personality (Wolf and Weissing, 2012) in natural populations (Archard
and Braithwaite, 2010; Osborn and Briffa, 2017).
Despite the fact that invertebrates represent the most numerous group of
animals on Earth (Larsen et al., 2017; Stork, 2018), personality studies
on this taxa are still scarce when compared to studies on vertebrates
(Gosling, 2001; Kralj-Fišer and Schuett, 2014; Mather and Logue, 2013).
However, in recent years insects started to play an important role in
animal behavioural research (Keiser et al., 2018). This is because
insects’ sexual and social behaviours represent a great variety of
phenomena that are rare or absent in vertebrates, providing new
possibilities for addressing ecological or evolutionary questions on
personality causes and consequences (Carere and Maestripieri, 2013).
Also studies on insects in many instances are less ethically
controversial and less time consuming because of a shorter lifespan when
compared to vertebrates (Córdoba-Aguilar et al., 2018). However, studies
on insect personality in natural conditions without handling and
captivity trauma are rare (e.g. Fisher et al., 2015b).
Beyond ‘ The big five’ (boldness, aggressiveness, exploration, activity
and sociability) which became the blueprint for animal personality
studies (Mather and Logue, 2013; Réale et al., 2007; Van Oers and
Naguib, 2013), we have limited understanding of other personality
aspects. For example, behaviours related to mating have an extraordinary
role in species ecology and evolution, but these behavioural traits have
received relatively little attention in animal personality studies
(Koski, 2014). For instance, The term ‘sociability‘ is being used as a
proxy for a whole range of behaviours. These include: hiding in presence
of a conspecifics’ smell (Cote et al., 2008), grooming in chimpanzees
(Koski, 2011), aggregation at food sources in fruit flies (Scott et al.,
2018), tendency to shoal in mosquitofish (Brodin et al., 2019) and
mating behaviours (Sih et al., 2014). It is possible that the same
test/metric may actually measure different traits in two different
species (Koski, 2014). For instance, testing response to a predator (as
a proxy of boldness) in open areas, which is used for e.g. kangaroos
(Blumstein and Daniel, 2003), may not be adequate for a passerine, which
usually inhabits, and are preyed upon, in more closed habitats
(Whittingham et al., 2004). Also, multiple tests of one personality
trait, could be of higher validity in describing a given trait (Carter
et al., 2013), as has been done on guppies (Poecilia reciculata )
where boldness was measured in three experiments (Burns, 2008).
Already established model organisms (i.e., non-human species
representing a larger group of organisms used for comparative and
integrative research on specific scientific problems, Leonelli and
Ankeny, 2013), intensively bred and studied under lab-conditions over
several decades, have their limitations and may not be very useful as
models for some lines of research. For instance, one of the most
significant model organisms, the fruitfly (Drosophila
melanogaster ), intensively used for testing molecular mechanisms of
behaviour (Kain et al., 2012; Roberts, 2006; Sokolowski, 2001), has been
reared for many generations in homogeneous, non-natural, environments of
molecular biology laboratories. This have more than likely resulted in
the species adaptation to stable environments and a change in its
behavioural reaction to novel conditions when compared to natural
populations (Archard and Braithwaite, 2010). For example, a recent study
of how anxiolytic pharmaceuticals can affect zebrafish behaviour showed
that the behaviour of wild zebrafish was changed by the exposure to the
anxiolytic, while the lab-reared zebrafish was unaffected (Vossen et
al., 2020). Hence, to increase the ecological relevance of studies
including behavioural traits we need to both expand the number and
taxonomic breadth of model organisms, as well as re-stock or replace
existing lab-populations (Behringer et al., 2009; Leonelli and Ankeny,
2013).
Here, we report a set of behavioural traits tested for their
repeatability over time and contexts in the damselfly Calopteryx
splendens measured in natural field conditions. We measured traits
related to three behavioural axes: (i) courtship behaviour, (ii)
aggressiveness and (iii) boldness. Since this is the first study onC. splendens personality in the wild, we test three traits within
each behavioural axis to make sure they are applicable to this study
system (Carter et al., 2013). The repeatability was assessed in two
different contexts: on undisturbed original patches (males’ territories)
and after partial deterioration of a territory. Our results indicate
that C. splendens is an excellent model for studies on animal
personality and behavioural syndromes in nature.