Abstract
Urban developments and human activities are encroaching on our natural habitats at a rapidly increasing rate, placing many species under stress from anthropogenic disturbance. Animal personality can influence how individuals tolerate disturbance in their environment. We examined the relationships between boldness and breeding success in a highly anthropogenically disturbed population of little penguins (Eudyptula novaehollandiae) on Granite Island, South Australia. We measured boldness in individual penguins both at the nest (in response to a simulated nest intrusion; nest defence scores) and away from the nest (in response to a human approach; alert and flight initiation distances). We first assessed the repeatability of boldness across time and contexts, and then determined the relationships among boldness, parental care behaviours (return rate to the nest, feed rate to chicks, and number of overnight stays) and breeding success (number of chicks fledged). Nest defence scores were highly repeatable across months and years. Responses to a human approach (alert and flight initiation distances) were not repeatable, with penguins increasing their flight initiation distance across repeated trials. Mean nest defence scores positively correlated with the first flight initiation distance recorded, supporting the idea that both responses may be mediated by the same underlying personality trait (boldness). Neither nest defence score nor response to human approach predicted parental care or breeding success. Our results suggest that constant exposure to anthropogenic disturbance may have negative effects on little penguins and highlight the importance of limiting interactions between human visitors and penguins.
1. Introduction
Human infrastructure and activities are increasingly encroaching on natural environments, causing significant overlap between human activities and birds’ habitats (Brawn et al., 2001; Matuoka et al., 2020). Because most birds consider humans a potential predation threat (Beale & Monaghan, 2004), anthropogenic disturbance can impose significant fitness costs on individuals by increasing their time spent on avoidance and vigilance behaviours (Arroyo & Razin, 2006). This, in turn, can have energetic costs and reduce the amount of time spent on other behaviours necessary for survival and reproduction, such as hunting/foraging or providing care to offspring (Frid & Dill, 2002; Arroyo & Razin, 2006; Merrall & Evans, 2020). Evidence of these disruptions to birds’ behavioural time budgets has been found across many species, including in six passerine bird species (feeding behaviour; Merrall & Evans, 2020), Snares penguins (Eudyptes robustus) (rest behaviour; Ellenberg et al., 2012) and bearded vultures (Gypaetus barbatus) (nest attendance, Arroyo & Razin, 2006). Repeated disruptions to behavioural time budgets can have long-term impacts on individual fitness and population survival (Burger, 1991; Schummer & Eddleman, 2003).
Some individuals, however, are better equipped to cope with such disturbances, through variations in their morphology, life history, or behaviour (Jiménez et al., 2013; Dharmarajan et al., 2021; Pérez-Ortega & Hendry, 2023). Personality traits, defined as consistent inter-individual behavioural differences (Réale et al., 2007; Laskowski et al., 2022), may be particularly informative for determining how individuals respond to environmental disturbances (Cockrem, 2013; Nicolaus et al., 2016; Arroyo et al., 2017). Personality traits are often measured along five broad behavioural axes: boldness, exploration, activity, aggressiveness, and sociability (Réale et al., 2007) and correlations between personality traits can be described as behavioural syndromes (Sih et al., 2004). On the proactive-reactive axis, for example, ‘proactive’ individuals tend to be bold, aggressive, fast-exploring, and active, while ‘reactive’ individuals tend to be shy, non-aggressive, slow-exploring, and inactive (Sih et al., 2004; Devost et al., 2016).
In birds, proactive personality traits may attenuate the effects of anthropogenic disturbance (Arroyo et al., 2017): highly bold or aggressive individuals may be more tolerant of humans (Arroyo et al., 2017; Rabdeau et al., 2021) and more likely to reside near anthropogenically disturbed areas (Carrete & Tella, 2010). For example, in Montagu’s harriers (Circus pygargus), bold individuals nested closer to human infrastructure than their shyer conspecifics (Rabdeau et al., 2021). This is consistent with the personality-matching hypothesis, where individuals select habitats compatible with their personality phenotype (Carrete & Tella, 2010; Cote et al., 2010; Holtmann et al., 2017; Rabdeau et al., 2021). Proactivity has also been linked to heightened antipredator behaviours in the white-collared blackbird (Turdus albocinctus) (Li et al., 2020), superb fairy-wren (Malurus cyaneus) (Bilby et al., 2022), and great tit (Parus major) (Tilgar & Koosa, 2019), with the latter also returning to their territory more rapidly than slow-explorers after exposure to disturbance (Cole & Quinn, 2014). Parental personality traits are also known to influence breeding success (Mutzel et al., 2013; Patrick & Weimerskirch, 2014) via component traits, such as foraging success, chick provisioning, or nest defence (Réale et al., 2007). Breeding success is vital for population stability and for the perseverance of highly disturbed and threatened populations (Böhning-Gaese et al., 1993; Schmidt, 2003). Because nest attendance rates can significantly affect breeding success (Arroyo & Razin, 2006), proactive individuals’ tendency to return to or stay at the nest following disturbance (Cole & Quinn, 2014) could increase breeding success in environments with frequent human visitation. As a result, some bird populations in urbanised or highly disturbed areas have shifted towards behavioural homogeneity, potentially due to selection for proactive personality phenotypes (Ellenberg et al., 2009; Lin et al., 2012; Arroyo et al., 2017). Therefore, understanding the link between personality, tolerance towards anthropogenic disturbance, and breeding success may be a crucial step towards the conservation of threatened populations impacted by anthropogenic disturbance.
As the effects of personality on fitness are context-dependent, it is important to consider how anthropogenic disturbance may affect reproductive behaviours, and the trade-offs that this may impose. Although it has been suggested that proactive parents defend their offspring more vigorously in anthropogenically disturbed environments (Amy et al., 2010; Arroyo et al., 2017; Tilgar & Koosa, 2019), there is also evidence that reactive parents seem to raise healthier offspring (Mutzel et al., 2013; Traisnel & Pichegru, 2019), suggesting a potential trade-off between the quality and quantity of offspring. Such a trade-off was present in Eurasian blue tits (Cyanistes caeruleus), where fast-explorers had larger clutch sizes but produced offspring with reduced body mass (Mutzel et al., 2013). Proactive individuals may, therefore, have greater reproductive outputs in disturbed environments; however, this could lead to decreased long-term survival of individuals or the production of lower-quality offspring (Dochtermann et al., 2015; Arroyo et al., 2017). As such, the relationship between personality and breeding success is complex, and which personality traits prove to be advantageous for breeding may depend on the circumstances faced by a population.
Seabirds are the most vulnerable group of birds, with nearly one-third of species classified as threatened worldwide (reviewed by Dias et al., 2019). Commonly bio-indicators for marine health (Croxall et al., 2002; Lascelles et al., 2012), seabirds are highly impacted by multiple disturbances, including climate change and fluctuations in prey distribution and abundance (reviewed in Croxall et al., 2012; Dias et al., 2019). Such pressures may be compounded by the negative consequences of living near humans (Arroyo & Razin, 2006; Frid & Dill, 2002; Costello & Colombelli-Négrel, 2023), as significant overlap between human and seabird habitat places seabirds at the frontline for anthropogenic disturbance (Watson et al., 2014; Mercker et al., 2021). Consequences of anthropogenic disturbance include decreased access to nest sites, physical disturbances, and alteration of time budgets (French et al., 2019; Costello & Colombelli-Négrel, 2023; Iasiello & Colombelli-Négrel, 2023).
Australian little penguins (Eudyptula novaehollandiae, formerly Eudyptula minor) are highly affected by anthropogenic disturbance (Carroll et al., 2016; Chiew et al., 2019; Costello & Colombelli-Négrel, 2023). As the only resident penguin species on mainland Australia along the southern coastlines, they are a significant ecotourism attraction (Dann & Chambers, 2013). Although listed as ‘Least Concern’ on the IUCN Red List (IUCN, 2022), some local populations in South Australia have been brought to the brink of local extinction (Wiebkin, 2011; Johnson & Colombelli-Négrel, 2021). The little penguin colony on Granite Island, South Australia, located near a densely populated coastal city with unregulated human traffic, is perhaps one of the most anthropogenically disturbed populations (Costello & Colombelli-Négrel, 2023). Sharp declines in this population over the last two decades have been attributed to a combination of factors: predation by natural and introduced predators, such as long-nosed fur seals (Arctocephalus forsteri), red foxes (Vulpes vulpes) and black rats (Rattus rattus) (Colombelli-Négrel, 2015; Colombelli-Négrel & Tomo, 2017; Costello & Colombelli-Négrel, 2023); fluctuations in environmental conditions, including sea surface temperatures and wind speeds (Johnson & Colombelli-Négrel, 2021); declines in fish abundance (Colombelli-Négrel et al., 2022); high juvenile mortality (Colombelli-Négrel, 2015); and anthropogenic disturbance (Costello & Colombelli-Négrel, 2023). Anthropogenic disturbances on Granite Island include loud noises (which decrease breeding success in other species; Arroyo & Razin, 2006), white light/camera flashes (which can blind penguins for several days), on-and off-leash dogs, physical intrusions into nests, people chasing penguins, and bikes/skateboards travelling at high speeds through crossing areas (Colombelli-Negrel, 2018, 2019; Costello & Colombelli-Négrel, 2023). A recent study by Colombelli-Négrel & Katsis (2021) found that little penguins on Granite Island were bolder towards a simulated nest intruder than those at three other South Australian colonies (Emu Bay, Penneshaw and Troubridge Island) that experience significantly less disturbance. This finding strongly suggests either that penguins on Granite Island show behavioural plasticity by acclimating to humans or that there is a link between personality and tolerance towards human disturbance in this population.
In this study, we examined the relationships between boldness and breeding success in little penguins on Granite Island. First, we measured individual boldness using two in situ behavioural assays: (1) a standardised nest intrusion, recording the strength of the penguin’s defensive response (‘nest defence score’) (Colombelli-Négrel & Katsis, 2021); and (2) a human approach assay, recording the penguin’s alert distance and flight initiation distance when walking on land (Blumstein, 2003). We predicted that individual differences in boldness would be repeatable both across time (as previously found by Colombelli-Négrel & Katsis (2021)) and across contexts — i.e. that penguins that were bold at the nest (i.e., with high nest defence scores) would also be bold when approached by humans (i.e., would show low alert and flight initiation distances; Arroyo et al., 2017; Rabdeau et al., 2021). Second, we measured three component traits (sensu Réale et al., 2007) related to parental care (return rate to the nest, feed rate to chicks, and number of overnight stays) and one composite trait related to breeding success (number of chicks fledged). We predicted that in this highly disturbed environment, bold individuals would produce more offspring than shy individuals. We also expected an association between personality and parenting strategy, with shy individuals investing more time in parental care, as previously observed in other bird species (Mutzel et al., 2013; Patrick & Weimerskirch, 2014; Zhao et al., 2016; Collins et al., 2019).
Map of Granite Island Recreation Park (35.5641°S, 138.6307°E), which is located in Encounter Bay on the Fleurieu Peninsula, about 100 km south of Adelaide, South Australia. Depicted are the northern and southern shorelines, and the location of the penguin nests (numbered 1–10) used in this study. Note that the penguins in nest 7 were a non-breeding pair.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
2. Methods
2.1. Study site
Granite Island Recreation Park (35.5641°S, 138.6307°E) is located in Encounter Bay on the Fleurieu Peninsula, about 100 km south of Adelaide, South Australia (National Parks and Wildlife Service, 2023). Vegetated with native trees, grasses and shrubs, the 26-ha island comprises cliffs and granite shorelines and is connected to the mainland by a 600-m causeway, which is open to the public at all times (National Parks and Wildlife Service, 2023). The island is a major tourist attraction, drawing up to 800 000 visitors annually (National Parks and Wildlife Service, 2023). The island’s north shore attracts the largest number of visitors, with a café, horse-drawn tram, and jetty, and many fishing hotspots (Figure 1). The north shore is also illuminated at night by bright streetlights, which can interfere with nest attendance in little penguins (Rodríguez et al., 2016). The island’s south shore experiences significantly less traffic, with scenic lookouts and a walking trail along the rocky granite cliffs (Figure 1). Thus, penguins nesting on the south side of the island experience less anthropogenic disturbance (Colombelli-Négrel, 2015; Costello & Colombelli-Négrel, 2023).
2.2. Study species
Little penguins are monogamous, with breeding efforts shared equally between males and females (Chiaradia & Kerry, 1999; Kemp & Dann, 2001). In the Granite Island colony, breeding occurs asynchronously from late winter (June to August) to early autumn (March to May). Across a breeding season, pairs will typically rear 1–2 clutches, each consisting of 1–2 eggs (Chiaradia & Nisbet, 2006). Incubation typically lasts four weeks, and is followed by a three-week guard period, during which parents alternate between staying with the chicks and fishing at sea (Chiaradia & Nisbet, 2006). The post-guard period, during which both parents fish during the day (Chiaradia & Kerry, 1999; Numata et al., 2000; Kemp & Dann, 2001) and leave their chicks alone in the burrow to return only every 1–5 days to feed them, typically lasts from three weeks of age until fledging at approx. 8 weeks (Chiaradia & Nisbet, 2006; Saraux et al., 2011). Parents have a meticulous return schedule, unless they are unable or unwilling to come ashore (e.g. due to changes in prey abundance, extreme weather, or unexpected barriers such as predators, boats, or changes to the landing site; Chiaradia et al., 2007).
2.3. Study population
We gathered all data over the 2021 (August 2021–March 2022) and 2022 (July 2022–March 2023) breeding seasons and combined those with previous data collected during the 2020 breeding season by Colombelli-Négrel & Katsis (2021). The most recent census conducted in October 2022 estimated the little penguin population on Granite Island as 22 adult penguins (Colombelli-Négrel, unpublished data). However, our new study focused only on the penguin pairs known to be actively breeding (plus one non-breeding pair sampled in 2020; nest 7 in Figure 1), which reduced our sample size to 10 pairs (two on the south shore and eight on the north shore, totalling 20 individual birds). Little penguin pairs were identified by the geographic location of their nests (Reilly & Cullen, 1981), which included artificial nests, excavated burrows, cave systems, or scrapes under vegetation (all hereafter referred to as ‘nests’) (Colombelli-Négrel, 2019). Following previously described methods (see Colombelli-Négrel & Smale, 2018; Colombelli-Négrel & Katsis, 2021; Schaefer & Colombelli-Négrel, 2021), individual penguins were sexed, and their identity verified during or after each experiment/observation, based on photographic comparisons of their morphology and bill depth and shape (Figure 2). While we sampled birds across multiple years, we are confident that the individuals were the same across years based on both photographs and the species’ documented long-term nest fidelity (Reilly & Cullen, 1981; Colombelli-Négrel, pers. obs.).
Infra-red photographs showing sexually dimorphic differences between (A) male and (B) female little penguins. Males have a greater bill height with a more prominent and curved maxilla, while females have a more slender bill with little prominence of the maxilla. Unique morphological differences (most notably bill shape) between two different females (C) and (D) are also displayed.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
2.4. Nest defence scores
To measure boldness at the nest, we assessed each subject’s response to a standardised human nest intrusion (perceived predator). Following methods previously described in Colombelli-Négrel & Katsis (2021), we used a standardised protocol to approach each nest (starting distance could not be controlled due to the topography) and then inserted into the nest a 1.5-m pole with a tennis ball on the end; it was held 50 cm from the penguin for 30 s. These assays were only performed when there was a single penguin in the nest. A GoPro Hero 5 camera (GoPro, San Mateo, CA, USA) mounted behind the tennis ball recorded the penguin’s response, which we later reviewed and scored on a discrete ordinal scale ranging from 0 (least bold) to 7 (most bold) (described in Table 1). Colombelli-Négrel & Katsis (2021) previously showed that subjects’ nest defence scores were highly repeatable (
Ethogram of the scoring system used to quantify nest defence scores (from Colombelli-Négrel & Katsis, 2021).
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
2.5. Alert and flight initiation distances
To measure boldness in a different context, we assessed the subjects’ alert distance and flight initiation distance in response to a standardised human approach. Alert distance was the distance (in m) at which the subject became alert to the approaching human and flight initiation distance was the distance (in m) at which the subject began to flee from that same threat (Blumstein, 2003; Tätte et al., 2018; Hammer et al., 2022). We conducted all approach assays 0–2 h after sunset when penguins were most likely to return to their nests (Chiaradia et al., 2007; Rodríguez et al., 2016). We approached the penguins as they crossed from the sea to their nests, using a constant approach rate from a standardized distance of about 15 m. We refer to these data as “experimental alert and flight initiation distances”. We also recorded penguin group size (typically 1–3) at the time of the approach. We identified penguins after they were approached by observing their bill morphology and the nest to which they returned. Penguins in nests 1–7 (see Figure 1) were tested 1–6 times (3.4 ± 1.6). Due to safety and accessibility concerns, the four penguins in nests 8 and 9 on the south shore and the pair in nest 10 on the north shore of the island were excluded from these assays (Figure 1) (final sample size,
We also recorded observational alert and flight initiation distances from little penguins in response to unregulated human wanderers at night. To do so, we observed little penguins from about 20 m away 0–2 h after sunset, as wanderers walked near them. The proximity threshold was again 15 m. We recorded alert distance, flight initiation distance, and penguin group size. In addition, we recorded the number of people approaching each penguin, whether the people were using torches (yes/no), and whether the people were actively looking (waiting or patrolling along known penguin routes) for penguins (yes/no). We recorded 3.2 ± 1.9 observations for each penguin (range 1–7). The pair from nest 10 and the female from nest 6 (Figure 1) were excluded from these observations, as there was no nearby human traffic (final
2.6. Breeding success
To obtain footage of little penguin parental care, we installed infrared motion sensor cameras (Argus 2, Reolink, Ashmore, QLD, Australia) outside nine nests on the northern and southern shores between August 2021 and March 2023 (excluding nest 7, as this pair did not breed; Figure 1). We installed each camera 2 m from the nest at a height of 30 cm. We programmed the cameras to detect and record any movements for a period of three hours, beginning 30 min before sunset (encompassing the period during which little penguins are most likely to feed their chicks; Chiaradia & Kerry, 1999). Once the motion sensor was triggered, the cameras recorded for 30–180 s. A single observer (A.S.) manually analysed camera footage, covering two weeks of the post-guard period (avoiding later chick stages when parents stop returning) for each breeding pair and totalling 45 h. We measured three behaviours over this two-week period: (1) return rate, the percentage of nights that the penguin returned to the nest; (2) feed rate, the percentage of nights that the penguin fed the chick (previously identified as the primary factor influencing offspring food intake and growth rates; Chiaradia & Nisbet, 2006); and (3) overnight stays, the percentage of nights that the penguin stayed overnight in the nest; as well as (4) breeding success, the number of chicks fledged per breeding pair per year in 2021 and 2022.
2.7. Statistical analysis
We used R v. 4.1.2 (R Core Team, 2021) for all statistical analyses. All linear mixed models (LMMs) were performed using the package lme4 v. 1.1-32 (Bates et al., 2015). All model diagnostics were performed using the DHARMa package v. 0.4.6 (Hartig, 2022). We tested the suitability of our models via visual inspection of diagnostic plots and using Shapiro–Wilk tests (
2.7.1. Repeatability analyses
We examined the repeatability of our boldness measures using the package rptR v. 0.9.22 (Stoffel et al., 2017), which relies on models fitted using the lme4 package. For each boldness measure, we calculated the adjusted repeatability (adjusted R), which is the proportion of total variance in a trait explained by differences between individuals, after accounting for potential confounds (Nakagawa & Schielzeth, 2010). We then tested the statistical significance of assay repeatability using a likelihood ratio test with a null hypothesis of
2.7.2. Nest defence scores
To examine the repeatability of nest defence scores, we first performed an LMM with ‘nest defence score’ as the response variable and ‘sex’, ‘trial number’ and ‘days since first trial’ as fixed effects. ‘Individual’ was included as a random effect to control for multiple testing of individual penguins. We initially included ‘nest’ as an additional random effect to control for the non-independence of breeding partners who shared a nest; however, ‘nest’ did not significantly explain any variation in nest defence scores and was ultimately removed to avoid model overparameterisation.
2.7.3. Experimental alert and flight initiation distances
To examine the repeatability of experimental alert and flight initiation distances, we performed two LMMs with ‘experimental alert distance’ and ‘experimental flight initiation distance’ as the response variables, respectively. Both models included ‘sex’, ‘trial number’ and ‘penguin group size’ as fixed effects and ‘individual’ as a random effect. Once again, we initially included ‘nest’ as an additional random effect to control for the non-independence of breeding partners, but this did not explain any variation in the response variables and was subsequently removed from the model.
2.7.4. Observational alert and flight initiation distances
To examine the repeatability of observational alert and flight initiation distances, we performed two LMMs with ‘observational alert distance’ and ‘observational flight initiation distance’ as the response variables, respectively. Both models included ‘sex’, ‘trial number’, ‘penguin group size’ and ‘number of people’ as fixed effects, with ‘individual’ and ‘nest’ as random effects to control for breeding partners sometimes being observed together. We did not include ‘light’ (yes/no) or ‘actively looking’ (yes/no) in either model because our dataset contained very little variation in these variables.
2.7.5. Correlation tests
We performed correlation tests to examine the relationship between our measures of boldness and between boldness and parental care behaviours. All variables were assessed for normality using Shapiro–Wilk tests and the ggpubr package (Kassambara, 2020) for visual assessment of histograms and Q–Q plots. We then assessed the correlation between variables using Pearson’s correlation tests for normally distributed data or non-parametric tie-adjusted Spearman’s correlation tests for data that did not follow a normal distribution (cor.test function in R). We performed LMMs to examine the relationship between boldness and breeding success.
2.7.5.1. Correlation between boldness metrics.
To examine the relationship between boldness at the nest and boldness towards an aproaching human, we tested the correlation between ‘mean nest defence score’ and ‘first experimental flight initiation distance’, as well as between ‘mean nest defence score’ and ‘first observational flight initiation distance’ (first response was used rather than mean response, as flight initiation distance increased with repeated trials) (Table 4).
2.7.5.2. Correlation between boldness and breeding success.
We examined the relationship between ‘mean nest defence score’ and the breeding metrics: (1) ‘return rate’; (2) ‘feed rate’; and (3) ‘overnight stays’. We repeated these correlation analyses using ‘first experimental flight initiation distance’ instead of ‘nest defence score’ to see if using the alternative metric of boldness showed different results.
To examine the relationship between mean nest defence score and first experimental flight initiation distance with the number of chicks fledged across the 2021 and 2022 breeding seasons, we performed an LMM with ‘fledging success’ as the response variable and ‘year’, ‘mean nest defence’ and ‘first experimental flight initiation distance’ as fixed effects. ‘Nest’ was included as a random effect as members of a breeding pair were not independent.
3. Results
3.1. Repeatability of nest defence score
Across this study, we obtained nest defence scores for 19 individuals. Subjects were tested 2.4 ± 0.6 times (range 1–3), with a mean ± SE nest defence score of 3.2 ± 1.6 (range 0.33–6) (see Table S1 in supplementary material for individual means). Neither sex nor trial number significantly predicted nest defence score (Table 2, model 1), nor did the number of days since the bird’s first trial (Table 2, model 1). Differences in nest defence scores were significantly repeatable between individuals (Table 3, Figure 3), despite some trials being performed up to 593 days after their first trial by Colombelli-Négrel & Katsis (2021) (see Table A2 in the Appendix).
Results from linear mixed models examining which factors influenced boldness in little penguins on Granite Island.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
Output from repeatability analyses examining boldness in little penguins.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
Nest defence scores across repeated trials in little penguins (mean ± SE). A score of 0 indicated a shyer response to a standardized nest intrusion while a score of 6 indicated a bolder response. F, female; M, male.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
3.2. Repeatability of experimental alert and flight initiation distances
We gathered experimental alert and flight initiation distances for 14 individuals, which were tested 3.4 ± 1.6 times (range 1–6). The mean experimental alert distance was 9.34 ± 1.4 m (range 7–12.25 m) (see Table A1 in the Appendix for individual averages). Sex, trial number, and penguin group size did not predict experimental alert distance (Table 2, model 2), and experimental alert distance was not significantly repeatable Table 3, Figure 4A). The mean experimental flight initiation distance was 7.18 ± 1.3 m (range 5–10.67 m). Sex and penguin group size had no effect on experimental flight initiation distance; however, trial number showed a near-significant trend (Table 2, model 2), with penguins fleeing at a greater distance in later trials (Figure 4B). Differences in experimental flight initiation distance were not significantly repeatable between individuals (Table 3, Figure 4B).
Responses of little penguins to a standardised human approach assay across multiple trials. (A) Experimental alert distance was the distance (in m) at which the subject became alert to the approaching human. (B) Experimental flight initiation distance was the distance (in m) at which the subject fled from the approaching human. F, female; M, male.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
3.3. Repeatability of observational alert and flight initiation distances
We measured observational alert and flight initiation distances for 13 individual penguins, which were observed 3.15 ± 1.88 times (range 1–7). The mean ± SE observational alert distance was 9.9 ± 2.1 m (range 7–14 m). Neither sex nor penguin group size affected observational alert distance. However, trial number and number of people did have significant effects (Table 2, model 4): penguins had higher observational alert distances in later trials (Figure 5A) and decreased their observational alert distance as the number of people in the group increased (Table 2, model 4). Between-individual differences in observational alert distances were not significantly repeatable (Table 3). Between-nest differences in observational alert distance were significantly repeatable, most likely because breeding partners were often observed simultaneously during the same human approach (Table 3). The mean observational flight initiation distance was 6.44 ± 2.64 m (range 2–13 m). Neither sex nor number of people influenced observational flight initiation distance. However, trial number and penguin group size both had significant effects, whereby penguins fled at greater distances in later trials (Figure 5B) and fled at shorter distances when in pairs (Table 2, model 5). Differences in observational flight initiation distance were not significantly repeatable between individuals but were repeatable between nests (Table 3).
Response of little penguins to uncontrolled human approaches during ad hoc observations. (A) Observational alert distance was the distance (in m) at which the subject became alert to the approaching human. (B) Observational flight initiation distance was the distance (in m) at which the subject fled from the approaching human. F, female, M, male.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
3.4. Correlation between boldness metrics
Correlation tests showed a significant correlation between the mean nest defence score and first experimental flight initiation distance (Table 4), whereby bolder birds (higher mean nest defence scores) fled at shorter distances during a standardized human approach (Figure 6). However, there was no significant correlation between mean nest defence score and the first observational flight initiation distance response (Table 4).
Correlations between nest defence score, experimental alert (AD) and flight initiation distances (FID), and parental care (return rate, feed rate and number of nights the penguins stayed overnight in the nest).
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
Scatterplot showing the negative correlation between mean nest defence score (in response to simulated territory intrusions) and first experimental flight initiation distance (in response to a standardised human approach) in little penguins on Granite Island. Higher nest defence scores and lower flight initiation distances both indicated greater individual boldness. F, female; M, male.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
3.5. Correlation between boldness and breeding success
Mean nest defence score correlated with neither return rate, feed rate, number of overnight stays in the nest (Table 4), nor the number of chicks fledged across both breeding seasons (Table 5). Similarly, first experimental flight initiation distance did not correlate with return rate, feed rate, number of overnight stays in the nest (Table 4), or chicks fledged across both breeding seasons (Table 5). The number of chicks fledged was significantly lower in 2022 compared to 2021 (Table 5).
4. Discussion
Personality has been identified as a factor affecting how well individuals cope with anthropogenic disturbance (Réale et al., 2007; Mutzel et al., 2013; Tilgar & Koosa, 2019). As seabirds are the most threatened group of birds and are increasingly exposed to anthropogenic disturbance (reviewed in Croxall et al., 2012; Dias et al., 2019), understanding how personality traits help them cope with disturbance could be vital for their conservation. On Granite Island, little penguins are subject to high levels of human disturbance and exhibit elevated levels of boldness in response to a standardised nest intrusion compared to other colonies in South Australia (Colombelli-Négrel & Katsis, 2021). In this study, we found that boldness during simulated nest intrusions was repeatable in this population over periods of more than a year and that individual differences in boldness were consistent across contexts — that is, individuals with high nest defence scores were also bolder during a human approach assay. There was no evidence, however, for a relationship between boldness and breeding behaviour (return rate, feed rate, overnight stays) or breeding success (number of offspring fledged). These findings stress the need to examine multiple personality traits, such as aggression or exploration, and different breeding metrics, such as chick body condition, to gain a better understanding of how these processes interact (Mutzel et al., 2013; Patrick & Weimerskirch, 2014; Traisnel & Pichegru, 2019).
Results from a linear mixed model examining the relationship between mean nest defence score and first experimental flight initiation distance with breeding success (number of chicks fledged) of little penguins across the 2021 and 2022 breeding seasons.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
In other seabird species, boldness has previously been identified as a repeatable personality trait (Patrick et al., 2013; Harris et al., 2020; Hammer et al., 2022). In our study of little penguins, nest defence response (our measure of boldness) was repeatable across months and years (adjusted
Humans are a perceived predation threat to seabirds (Beale & Monaghan, 2004). Optimal escape theory suggests that individuals will only flee a perceived threat when the risk of staying outweighs the benefits (Azaki & Cresswell, 2021). In our study, little penguins increased their flight initiation distance over multiple human approach trials. As locomotion on land is slow and energy-demanding for little penguins, their decision to flee at greater distances suggests that the penguins increasingly perceived the experimenter as a predation risk over multiple encounters. This aligns with the findings of Chiew et al. (2019), who found that close human proximity can induce fear responses in little penguins. Similarly, Carroll et al. (2016) reported that little penguins do not habituate to human handling and in subsequent human encounters secrete elevated levels of the stress hormone corticosterone and show behaviours indicative of acute stress. Frequent exposure to corticosterone can lead to chronic stress, with energy diverted away from vital activities, such as homeostasis, growth, foraging, and reproduction, which can lead to an energy deficit (McEwen & Wingfield, 2003; Carroll et al., 2016). Similarly, in Snares penguins, human-naïve individuals had lower heart rate responses towards an approaching human compared to those that had previously been filmed and researched in an intrusive manner, further suggesting that penguins may experience lasting effects from human encounters (Ellenberg et al., 2012).The relationship between anthropogenic disturbance and stress may be important to examine further in the Granite Island penguin colony due to the sharp decline in population size compared to other nearby colonies, which do not experience as much disturbance (Colombelli-Négrel & Katsis, 2021; Costello & Colombelli-Négrel, 2023). In future research, it would be insightful to measure corticosterone levels (Carroll et al., 2016) or heart rate (Schaefer & Colombelli-Négrel, 2021) when examining the relationship between human disturbance, stress, and personality in this species. More broadly, these findings provide further evidence that human activities are having negative impacts on seabird populations (Arroyo & Razin, 2006; Frid & Dill, 2002; Costello & Colombelli-Négrel, 2023).
During our observations of penguin-human encounters, little penguins became alert to small groups of people at greater distances compared to large groups of people. This could have negative implications on Granite Island, where penguins most commonly encounter small groups of people and, hence, may be more frequently disrupted by them. Although this pattern seems counterintuitive, similar trends have been observed in other seabird species, such as Eurasian oystercatchers (Haematopus ostralegus), which decreased their flight initiation distance as the number of people present increased, suggesting that larger groups of people may represent a smaller threat or that the birds may habituate to human presence as the number of people present grows (Azaki & Cresswell, 2021). However, this does not explain our observations on Granite Island, as penguins encountered groups of people of different sizes at various times. It is possible that visitors in smaller groups come to the island explicitly to search for penguins. However, whether people were actively looking for penguins or using torches did not influence either observational alert or flight initiation distances, despite a previous study by Costello & Colombelli-Négrel (2023) on this population finding that the use of white torches by members of the public was correlated with decreased penguin noise and a late return from sea. It should be noted, however, that most people observed during this study were actively looking for penguins, which could have influenced this result. It is also possible that small groups of people were louder or that large groups were observed less frequently, which remains to be tested further. It should also be noted that some penguins became alert to approaching threats from up to 15 m away, which suggests that the current recommendations to minimise anthropogenic disturbances on the island (such as a 5-metre buffer distance between humans and penguins, not using white torches or flash photography, etc...) may need to be revised. These findings have broader implications for other seabird populations that are the subject of tourism without guided tours or protocols to control human disturbance (Yorio et al., 2001).
Proactive birds are more likely to be tolerant of humans and to reside closer to anthropogenically disturbed areas and infrastructure (Carrete & Tella, 2010; Arroyo et al., 2017; Rabdeau et al., 2021). Colombelli-Négrel & Katsis (2021) previously showed that little penguins on Granite Island were bolder (defended their nests more vigorously) than those on islands with less anthropogenic disturbance. It is presently unclear whether this increase in population-level boldness is adaptive, since humans are rarely a direct predation threat to penguins. Instead, behavioural shifts that occur in response to human disturbance may be maladaptive during encounters with genuine predators, such as red foxes (Geffroy et al., 2015). While habituation to frequent anthropogenic disturbance has been observed in other avian species (Metcalf et al., 2000; Ellenberg et al., 2009; Blumstein, 2014), this can increase their vulnerability to predators if they become accustomed to non-lethal disturbance (Geffroy et al., 2015). Stronger responses to human encounters may also have negative effects on fitness, via increased corticosterone and stress response (Ellenberg et al., 2012; Carroll et al., 2016). Thus, it may be beneficial for future studies to examine the benefits and drawbacks of habituation to humans in anthropogenically disturbed species and populations.
Although parental personality traits are known to influence breeding success in other avian species (Mutzel et al., 2013; Patrick & Weimerskirch, 2014), in our study individual boldness (whether at the nest or towards an approaching human) did not correlate with any of our parental care or breeding success variables. While this lack of correlation could be influenced by our small sample size, which was constrained due to the small population, other factors need to be considered. Return rate and feed rate do not necessarily directly indicate the quality of food being fed to the chicks (Chiaradia & Nisbet, 2006), nor does the number of fledglings necessarily equate to the number of offspring that survive to reproductive maturity (Colombelli-Négrel, 2015). Chicks that are healthier when they fledge may have a greater chance of long-term survival (Chiaradia & Nisbet, 2006), which suggests that the quality rather than quantity of parental provisioning may need to be considered. In other seabird species, proactive individuals often have greater foraging success compared to their reactive conspecifics (Patrick & Weimerskirch, 2014; Krüger et al., 2019; Harris et al., 2020). For example, bold wandering albatrosses (Diomedea exulans) gained more mass per foraging trip compared to their shy conspecifics (Patrick & Weimerskirch, 2015). More aggressive Cory’s shearwaters (Calonectris borealis), black-browed albatross and black-legged kittiwakes (Rissa tridactyla) had greater foraging consistency (Patrick & Weimerskirch, 2014; Krüger et al., 2019; Harris et al., 2020). Aggressive individuals also outcompeted less aggressive individuals for food resources closer to the colony, forcing the less aggressive individuals to travel greater distances, especially during periods of low resource abundance (Patrick & Weimerskirch, 2014; Krüger et al., 2019; Harris et al., 2020). Furthermore, in African penguins (Spheniscus demersus), more aggressive individuals pursued prey with greater intensity (Traisnel & Pichegru, 2019). Therefore, it may be necessary to investigate other personality traits, such as aggression or exploration, as these may have a greater effect on breeding success than boldness. Other metrics of breeding success, such as chick body condition, could also provide a more comprehensive understanding of why some individuals raise more, or healthier, offspring. Additionally, this brings into consideration whether personality may have a greater effect on individual survival rather than breeding success.
To conclude, our study found that boldness was a consistent behavioural trait in little penguins not only across time (nest defence score only) but also across contexts (a penguin’s nest defence score correlated with flight initiation distance during its first human approach assay). Over multiple human approach assays, penguins were increasingly vigilant towards humans, becoming alert and fleeing at greater distances over multiple encounters. These findings suggest that regular exposure to anthropogenic disturbance could have negative ongoing effects on penguins, requiring mitigation strategies to limit the interaction of penguins and human visitors. Although we did not find any correlation between boldness and breeding success, there are many future avenues for research that could help us understand why boldness may be under selection. It is important to consider whether behavioural diversity may help mediate the effects of changing external factors (Carrete & Tella, 2010). Thus, the loss of behavioural diversity due to intense selection pressures, such as anthropogenic disturbance, may alter the proportion of personality traits within a population, potentially causing it to be less robust in the long-term. Future studies examining the consequences of personality differences on tolerance to disturbance and breeding success should focus on the long-term impacts of selection or behavioural plasticity.
Corresponding author’s e-mail address: diane.colombelli-negrel@flinders.edu.au
Acknowledgements
Special thanks to Stephen Hedges and all the Granite Island little penguin monitoring volunteers who assisted with fieldwork. This research was approved by the Flinders University Animal Welfare Committee (E449/BIOL AR4825) and supported by a scientific permit (Y26040). A total of 20 birds were tested in this study, and all experiments were minimally invasive, with nest defence tests limited to 30 s and only repeated up to three times. No birds were handled in any part of this study. Only red-light torches were used when identifying individual penguins on the nest or during the night, as white light can blind penguins for several days. This work was supported by the Waterhouse Club, Friends of Encounter Birds, the Save Granite Island Penguins Committee, and the Sir Mark Mitchell Foundation. D.C.-N. conceived the study; D.C.-N. and A.C.K. designed the experiments and commented on the paper. A.S. and D.C.-N. (in 2020) collected the data; A.S. analysed the data and wrote the first draft of the paper.
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Appendix
A.1. R code used in this study
List of little penguins observed for this study, including their mean boldness scores (nest defence score, alert distance, flight initiation distance), parental care (return rate, feed rate) and breeding success (number of chicks fledged in 2021 and 2022).
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
Number of days since the first nest defence trial was performed on the penguins.
Citation: Behaviour 2025; 10.1163/1568539X-bja10293
