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From nestling to adult: personality traits are consistent within but not across life stages in a wild songbird

In: Behaviour
Authors:
Andrew C. Katsis College of Science and Engineering, Flinders University, Adelaide, SA 5005, Australia
Konrad Lorenz Research Center for Behavior and Cognition and Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

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Lauren K. Common College of Science and Engineering, Flinders University, Adelaide, SA 5005, Australia

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Mark E. Hauber Department of Evolution, Ecology, and Behavior, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

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Diane Colombelli-Négrel College of Science and Engineering, Flinders University, Adelaide, SA 5005, Australia

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Sonia Kleindorfer College of Science and Engineering, Flinders University, Adelaide, SA 5005, Australia
Konrad Lorenz Research Center for Behavior and Cognition and Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria

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Open Access

Abstract

Personality traits can remain consistent throughout adult life, but it is less clear when these behavioural differences first arise and whether they are maintained across ontogenetic stages. We measured personality across three life stages (nestling, fledgling, and adult) in a wild population of superb fairy-wrens (Malurus cyaneus). We assessed (1) boldness (response to human handling, at all three stages), (2) exploration (response to a novel environment, in fledglings and adults) and (3) aggressiveness (response to mirror-image stimulation, in fledglings and adults). Personality differences were often consistent within life stages but never across them: specifically, aggressiveness was repeatable in fledglings and all three traits were repeatable in adults. We had insufficient statistical evidence for the presence of behavioural syndromes between any of our three personality traits, either at the fledgling or adult stages. Our results suggest that long-term personality traits may not become entrenched until adulthood in this species.

1. Introduction

Individuals within a population often exhibit behavioural differences that are consistent over time and across contexts, also known as personality (Réale et al., 2007; Laskowski et al., 2022). An individual’s behaviour can be considered consistent even if its absolute behavioural scores change over time, provided their rank order within a group is maintained (Stamps & Groothuis, 2010). Personality traits are partly heritable (Dochtermann et al., 2015) but are also influenced by environmental and social factors (Carere et al., 2005; Frost et al., 2007; Rödel & Meyer, 2011).

Although personality traits can persist for substantial proportions of an individuals’ lifespan (e.g. Hall et al., 2015; Wuerz & Krüger, 2015; Thys et al., 2017; Bubac et al., 2018), we still have an incomplete understanding of when individual behavioural differences first arise and to what extent they are maintained across development (Stamps & Groothuis, 2010; Cabrera et al., 2021). In metamorphic insects, there is evidence that personality remains stable across distinct developmental stages, especially in heterometabolous species (i.e. those that undergo ‘weak’ metamorphosis; Amat et al., 2018). In vertebrate taxa, juveniles can exhibit personality traits (e.g. Brommer & Kluen, 2012; Castanheira et al., 2013; Rödel et al., 2015) but there is only mixed evidence that these traits are maintained across sexual maturity (reviewed by Cabrera et al., 2021). In Australian zebra finches (Taeniopygia castanotis), differences in activity levels were consistent between the nestling and adult stages, suggesting that personalities are established shortly after hatching and persist across development (McCowan & Griffith, 2014). Several other studies also show that individuals behave consistently between the juvenile and adult stages, but only for some of the assessed behavioural traits (Herde & Eccard, 2013; Petelle et al., 2013; Kelley et al., 2015; Wuerz & Krüger, 2015).

Understanding when behavioural differences remain consistent during development — and when they change — can offer insights into the physiological, environmental, and social factors that shape personality at the proximate level (Stamps & Groothuis, 2010). For example, if personality is directly linked to physiological processes such as metabolism or hormone levels (Careau et al., 2008), then personality traits may become less stable during developmental periods in which individuals undergo major physiological changes (e.g. during sexual maturation; Stamps & Groothuis, 2010). Alternatively, if personality is more strongly influenced by ‘external’ factors such as environment or social context, then shifts in individuals’ personality may instead occur following migration or natal dispersal (Stamps & Groothuis, 2010). Of course, these hypotheses are not necessarily mutually exclusive: they may operate in concert, with environmental conditions mediating the relationship between behaviour and physiology (Montiglio et al., 2018).

When multiple personality traits correlate with each other, they are said to form a behavioural syndrome (Sih et al., 2004a,b). Several hypotheses have been proposed for the presence of behavioural syndromes. Under the ‘constraint’ hypothesis, personality traits correlate with each other because they share proximate genetic or physiological mechanisms. This means that behavioural syndromes should be difficult to break apart because selection on one personality trait unavoidably affects all others (Sih et al., 2004a,b). This prediction has been supported by observational studies in which behavioural syndromes were similar between populations (Alcalay et al., 2015) or remained stable across development even when their constituent traits did not (Bell & Stamps, 2004). Alternatively, the ‘adaptive’ hypothesis proposes that personality traits are independently plastic to environmental factors, such as predation pressure (Bell & Sih, 2007; Dingemanse et al., 2007; Dhellemmes et al., 2020). Hence, syndromes may be favoured only in certain ecological conditions and represent an adaptive outcome of selection (Sih et al., 2004a; Smith & Blumstein, 2012). This hypothesis also has some empirical support, whereby behavioural syndromes were unstable over time (Class & Brommer, 2015; Wuerz & Krüger, 2015) or differed between concurrent populations (Dingemanse et al., 2007).

In this study, we measured the consistency of three personality traits — boldness, exploration and aggressiveness — and their syndromes across life stages in a wild population of superb fairy-wrens (Malurus cyaneus). In this passerine species, adult exploration behaviour is known to be repeatable over several years, representing a significant proportion of the species’ average lifespan (Hall et al., 2015). Here, we measured (1) boldness using two handling assays in nestlings, fledglings, and adults; (2) exploration using a novel environment test in fledglings and adults; and (3) aggressiveness using a mirror stimulation test in fledglings and adults. For each of these traits, we assessed individual consistency both within and across life stages (Stamps & Groothuis, 2010). We predicted that all three personality traits would be consistent across life stages. In fledglings and adults, we also correlated boldness, exploration, and aggressiveness to test for the presence and stability of behavioural syndromes. We predicted that all three personality traits would correlate positively with each other in adults (consistent with a proactive-reactive behavioural syndrome; Koolhaas et al., 1999) but did not have an a priori prediction about the stability of this syndrome across development.

2. Methods

2.1. Study site and study species

Since 2010, we have monitored a wild population of superb fairy-wrens at Cleland Wildlife Park (34°58′S, 38°41′E), 25 km south-east of Adelaide, SA, Australia. Superb fairy-wrens generally live in breeding pairs or small, cooperatively breeding family groups (Dunn et al., 1995). During the breeding season (September to January), females lay a clutch of 2–4 eggs and incubate them for 14 days (Rowley & Russell, 1997). Nestlings fledge at age 10–14 days and become nutritionally independent at approx. 40 days old (Rowley & Russell, 1997). In their first year, female offspring almost always disperse from their natal territory while male offspring often remain as helpers in their family group (Mulder, 1995). Offspring reach sexual maturity at the end of their first year (Rowley & Russell, 1997). All fairy-wrens in our study population were uniquely banded with three plastic colour bands to allow identification in the field, plus an aluminium band issued by the Australian Bird and Bat Banding Scheme. Adults were sexed based on their plumage characteristics (Rowley & Russell, 1997), while nestlings and fledglings were sexed by genetic analysis of a 10–50-μl blood sample, collected by brachial venepuncture with a 30G needle and stored on FTA® cards (Smith & Burgoyne, 2004). This analysis was commercially performed (Australian Genome Research Facility, Melbourne, Australia) via established molecular techniques, using three primer pairs for which male birds are homogametic and females are heterogametic (CHD1F/CHD1R, P2/P8 and 2550F/2718R; Griffiths et al., 1998; Fridolfsson & Ellegren, 1999; Lee et al., 2010). Some nestlings ( N = 25) and a fledgling ( N = 1) from the 2021 breeding season were of unknown sex.

Figure 1.
Figure 1.

Timeline of behavioural variables measured in nestling, fledgling, and adult superb fairy-wrens. Boldness variables (B, using human handling assays) were measured at all three stages, while exploration (E, using a novel environment test) and aggressiveness (A, using a mirror stimulation test) variables were measured in fledglings and adults. Illustrations by Lauren K. Common.

Citation: Behaviour 160, 8-9 (2023) ; 10.1163/1568539X-bja10224

2.2. Overview of experimental methods

For this study, we monitored breeding activity in 25 fairy-wren territories across three consecutive breeding seasons (September 2019–January 2020, September 2020–February 2021, and September 2021–January 2022). If we discovered a nest during building, we checked for egg laying every three days; if discovered during incubation, we candled the eggs to estimate their age. Around the expected hatch date, we checked nests at least daily so that we knew the hatchlings’ age to the nearest day.

We measured fairy-wren behaviour in nestlings, fledglings, and adults (see Figure 1). We measured boldness using two human handling assays (back test and processing test), exploration using a novel environment test, and aggressiveness using a mirror stimulation test. Our assay timeline is briefly summarised below:

  1. (1) On the same day that we banded nestlings (approx. 8 days post-hatching), we also measured their boldness.
  2. (2) At least one week after leaving the nest, fledglings were captured using mist-nets so that we could measure their boldness, exploration, and aggressiveness.
  3. (3) Adult birds (aged 1+ years) were captured using mist-nets so that we could measure their boldness, exploration, and aggressiveness.

Fledglings and adults usually undertook all three personality assays on the same day, but occasionally we only measured boldness ( N = 4 fledglings, 16 adults) or only measured exploration and aggressiveness ( N = 11 fledglings).

Figure 2.
Figure 2.

Assays used to measure superb fairy-wren personality at different life stages. (a) boldness measured in an 8-day-old nestling using a back-test handling assay; (b) boldness measured in an adult male using a back-test handling assay; (c) the flight cage used to assess exploration and aggressiveness in fledglings and adults, with the mirror revealed and a fairy-wren observing its mirror image.

Citation: Behaviour 160, 8-9 (2023) ; 10.1163/1568539X-bja10224

2.3. Handling assays (boldness)

We quantified boldness using two human handling assays, drawing on methodologies developed by Brommer & Kluen (2012). Response to human handling has been identified as a consistent behavioural trait in both nestling and adult blue tits (Cyanistes caeruleus; Brommer & Kluen, 2012; Kluen et al., 2014).

When nestlings were 8 days old (occasionally 7 or 9 days old), we removed them from the nest to fit identifying colourbands, take morphometric measurements, and measure their boldness. In our first assay, the nestling was immobilised on its back in the experimenter’s palm, with one thumb gently held over its chest to keep the bird in place (the ‘back test’; Hessing et al., 1993; Hall et al., 2015; Katsis et al., 2021) (Figure 2a). We then counted the number of nestling struggles over a 30 s period, which we called ‘back-test response’ (the inverse of the variable ‘docility’ in Brommer & Kluen, 2012). After this, we measured four morphometric variables: tarsus length (to the nearest 0.1 mm, using a sliding calliper), head-bill length (nearest 0.1 mm, sliding calliper), wing length (nearest mm, butt-ended ruler) and mass (nearest 0.1 g, spring balance in 2019 and electronic balance in 2020 and 2021). As our second handling assay, we noted whether the nestling struggled during each of these four measurement procedures and then assigned a score on a discrete ordinal scale from 0 (did not struggle during any procedure) to 4 (struggled during all four procedures). This nestling score was then multiplied by 1.25 to allow comparison with the fledgling and adult scores (which were measured on a 0–5 scale, see below). We called this variable ‘processing response’ (equivalent to ‘handling aggression’ in Brommer & Kluen, 2012). To ensure that handling style was similar across subjects, most handling assays (97%) were performed by a single experimenter (ACK). To minimise possible time-of-day effects, most assays (93%) were conducted in the morning (8 am–12 pm).

We captured fledglings and adults using mist-nets and measured their boldness using two human handling assays (with minor changes to the nestling protocol described above). To measure back-test response, birds were held in the ‘bander’s grip’ and gently tilted onto their back to commence the assay (adapted from Kluen et al., 2014; Bilby et al., 2022) (Figure 2b). To measure processing response, we noted whether the subject struggled during each of five measurement procedures and assigned a score from 0 (did not struggle during any procedure) to 5 (struggled during all five procedures). For this assay, we measured the same four morphometric variables described above (tarsus length, head-bill length, wing length) plus tail length (nearest mm, using a ruler). Handling assays were performed by one of four handlers and the back tests were video-recorded so that scores could be confirmed by a single experimenter (ACK). Fledglings were captured at least one week after leaving the nest (mean ± SE age at first capture: 31.0 ± 1.3 days, range 19–59; also 9 fledglings of uncertain age).

2.4. Novel environment test (exploration)

After capture and processing, fledglings and adults were transferred in cotton bags to an onsite building where we quantified their exploration using a novel environment test (Verbeek et al., 1994). The bird was placed individually in a small wooden release box (dimensions 170 × 115 × 90 mm) and allowed 5 min to acclimate. The door to the release box was then raised, allowing the bird to enter the novel environment: a metal flight cage of dimensions 700 × 450 × 450 mm (Figure 2c). On one side of the cage, we positioned a camera (GoPro Hero 7 Black) that recorded the birds’ movements. The cage was divided into 13 discrete sectors that subjects could visit: three wooden perches, four floor quadrants, four cage walls, the cage ceiling, and the release box. As measures of exploration, we recorded: (1) ‘unique sector visits’, the number of unique sectors visited in 5 min following emergence; and (2) ‘total sector visits’, the total number of sectors visited (including repeat visits) during this same period (Bilby et al., 2022; Colombelli-Négrel et al., 2022).

2.5. Mirror stimulation test (aggressiveness)

The novel environment test was immediately followed by a mirror stimulation test (Svendsen & Armitage, 1973). Five minutes after the bird entered the novel environment, we began the mirror stimulation test by remotely raising a curtain at one end of the cage to reveal a mirror (30 × 40 cm). Fairy-wrens often respond to their mirror image by approaching or making physical contact with the reflective surface, which is generally interpreted as an aggressive response (Hall et al., 2015; Leitão et al., 2019; Jones et al., 2022). Over the next 3 min we recorded: (1) ‘mirror contacts’, how many times the subject made physical contact with the mirror; and (2) ‘time near mirror’, the duration spent near the mirror (i.e. in the three nearest sectors, excluding time spent making contact with the mirror; Bilby et al., 2022). After the mirror stimulation test, the bird was recaptured by hand and released at its point of capture. Behaviour in the novel environment and mirror stimulation tests was manually scored from the recorded videos using the software Solomon Coder v. beta 19.08.02. For consistency, all novel environment and mirror stimulation tests were conducted and scored by a single experimenter (ACK).

2.6. Statistical analysis

All statistical analyses were performed with the software R v. 4.2.3 (R Core Team, 2023). Univariate linear mixed models (LMMs) used the ‘lmer’ function in lme4 package v. 1.1-32 (Bates et al., 2015), while multivariate generalised linear mixed models (GLMMs) used the package MCMCglmm v. 2.34 (Hadfield, 2010). In the handling assays, back-test response and processing response were positively correlated (