Personality-dependent nest site selection and nest success during incubation in a wild population of chestnut thrush Turdus rubrocanus

doi:10.21203/rs.3.rs-1985470/v1

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Personality-dependent nest site selection and nest success during incubation in a wild population of chestnut thrush Turdus rubrocanus

https://doi.org/10.21203/rs.3.rs-1985470/v1

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Within the same species population, individuals with different personality traits may choose different habitats, which could result in different reproductive fitness. In birds, little is known about how individuals respond to nest site selection basing on their personality traits. Here, we address this knowledge gap and investigate whether an individual’s personality (activity and breathing rate) can affect patterns of nest site selection at different spatial scales in a wild population of chestnut thrush (Turdus rubrocanus) and determine whether nest site characteristics and female personality traits affect clutch size and nest success during incubation. We found that neither activity nor breathing rate was associated with large-scale nesting habitat variables. At the fine-scale level, more active females chose nest sites with greater nest lateral concealment, whereas females with lower breathing rate chose nest sites with lower concealment above the nest. Females with higher breathing rates laid smaller clutch sizes than individuals with lower breathing rate. Nests with greater vegetation concealment above nests and females with lower breathing rate had higher nest success during incubation. This work highlights the importance of understanding the relationships between personality and nest site selection in birds, and the role of female personality traits in reproductive success.

nest survival

nest site selection

animal personality

generalized linear mixed models

Chestnut thrush

Individuals with consistent behavioral differences over time and/or across contexts is defined as animal personality ^1–3. Having been studied across many animal taxa ⁴, animal personality is now known to play important roles in sexual selection ^5–7, parental care ^8,9 and other life history traits ^10,11. For example, female zebra finch (Taeniopygia guttata) chose mates with similar personality traits ¹², and parents with similar personality traits have higher reproductive success ^13–15. Recently, quantifying spatial distribution patterns of individuals within a population based on animal personality has attracted increasing interest ^16–18. Personality could reflect an individual ability to cope with environmental conditions, which may in turn lead to personality-dependent distribution ^19,20, which forms the premise of the personality-matching habitat choice hypothesis ^17,19,21.

Nest site selection at different spatial scales (i.e. large- and fine-scale) is an important process for successful breeding ^22,23, and is affected by many factors, such as food resource and predator abundance ^24,25. Recent studies have found that individual differences in personality traits are known to be related to large-scale nest site selection ^17,26,27. For example, bold females select nest sites with greater concealment and which are located further from landscape features with higher predation risk ²⁸ or from areas of anthropogenic disturbance (Zhao et al. 2016). However, to our knowledge, less is known about how personality traits affect patterns of fine-scale nest site selection in birds. Therefore, to gain an understanding of personality-dependent nest site selection requires an comprehensive examination of animal personality differences at different spatial scales.

Fine-scale nest site selection is also crucial to reproductive fitness in birds ^22,23, affecting individual reproductive strategy and survival ^29–31. Nests with better concealment can have larger clutch sizes ^24,32, yet clutch size could also be affected by personality traits ³³, with bold females known to lay larger clutch sizes than shy individuals (Zhao et al. 2016). Furthermore, predations is the main cause of nest failure in many passerines ^34,35, and nests with more concealment could reduce nest predations in birds ^31,34. Nest defense is negatively associated with levels of nest predation ^36,37, and different personality traits may cause different responses to nest predators ³⁸. We suggest therefore, that personality traits may be a significant factor that affects avian reproductive success ^17,39. To date, few studies have investigated how nest site characteristics and personality traits affect the nest success during incubation, thus overlooking the potential role of female personality traits in reproduction.

In this study, we extend the previous research of Zhao et al. (2016) of a wild breeding population of chestnut thrush Turdus rubricanus to investigate whether nest site selection and nest success during incubation are related to female’s personality traits. We use two measures of animal personality - breathing rate and activity - which are easily measurable and repeatable in our study population ^15,26. Although breathing rate is considered by some as a physiological trait-reflecting stress response ^40,41, many authors have argued a strong case for personality to be measured (or as a proxy) by breathing rate, as the two appear to be very closely linked ^42–47. In chestnut thrushes, only females participate in nest site selection, incubation and brood nestlings ¹⁵, which is suitable to explore the relationship between personality and nest site selection and nest success during incubation.

Our objectives of this study are three-fold: (1) to examine whether the large- and fine-scale nest site characteristics were associated with female personality traits. We predicted that females with lower breathing rate and activity select nest sites near the human residences and in more concealment areas. (2) to examine whether the nest site characteristics, and female personality traits were associated with clutch size. We predicted that nests with more concealment and females with lower breathing rate had larger clutch size. (3) to examine whether the nest site characteristics, and female personality traits related to nest success during incubation. We predicted that nests with more concealment and females with lower breathing rate had higher nest survival rate during incubation.

Personality traits and nest site characteristics

In 2013–2016, we measured the breathing rate test 415 times in 290 different chestnut thrushes (129 males and 161 females) and activity test 377 times in 266 different individuals (117 males and 149 females). Both activity and breathing rate were repeatable with individuals across time (Table 1). In total, we also collected the nest site characteristics of 125 female chestnut thrushes that also were measured for activity and breathing rate from 2013 to 2016. We found that neither activity nor breathing rate was associated with large-scale habitat variables (Table 2). More active females chose nest sites with greater nest lateral concealment (Table 2, Fig. 1a), whereas females with lower breathing rate chose nest sites with lower concealment (i.e. more open vegetation) above the nest (Table 2, Fig. 1b).

Table 1

Repeatability of activity and breathing rate in chestnut thrush. N_ind = total number of individuals, and R = repeatability (R), and range = range of traits.
Trait	N_ind	Range	R	P
Activity	266	0-19.053	0.297	0.001
Breathing rate	290	54–184	0.506	< 0.001
Activity is represented as the square root of the number of movements in the simple cage test. Breathing rate is defined as the number of breast movements during 60 s while being handled. The LMMs of activity and breathing rate were used to calculate the repeatability and can be found in Table A1.

Table 2

The relationship between nest site characteristics and personality in chestnut thrushes. Significant predictors are highlighted in bold.
Predictors	Factor	Estimate	χ2	P
Nest height	Breathing rate	-0.007	1.289	0.256
	Activity	0.027	0.605	0.437
Nest lateral concealment	Breathing rate	0.002	0.657	0.418
	Activity	0.030	5.186	0.023
Concealment above the nest	Breathing rate	0.005	5.403	0.020
	Activity	-0.001	0.001	0.998
Concealment below the nest	Breathing rate	-0.002	0.586	0.444
	Activity	0.009	0.365	0.546
Distance to human settlement	Breathing rate	0.613	0.792	0.374
	Activity	-2.661	0.418	0.518
Distance to farmland (m)	Breathing rate	-0.118	0.670	0.413
	Activity	-0.689	0.640	0.424
Distance to road (m)	Breathing rate	0.121	0.049	0.826
	Activity	-1.934	0.355	0.551

Personality traits and clutch size

Clutch size was associated with breathing rate: females with higher breathing rate laid smaller clutch sizes (Table 3), but clutch size was not related to other nest site characteristics, body mass or activity (Table 3).

Table 3

Predictors of clutch size in nests of chestnut thrushes. Significant predictors are highlighted in bold.
Predictors	Estimate	χ2	P
Breathing rate	-0.020	5.536	0.019
Activity	0.028	0.355	0.551
Body mass	0.005	0.349	0.554
Nest height	-0.020	0.024	0.876
Nest lateral concealment	-0.348	0.884	0.347
Concealment above the nest	-0.214	0.333	0.564
Concealment below the nest	-0.004	0.001	0.990
Distance to human settlement	-0.001	1.148	0.284
Distance to farmland (m)	-0.007	1.395	0.238
Distance to road (m)	-0.001	0.155	0.694

Personality traits and nest success during incubation

From 2013 to 2016, nest fate during incubation was recorded in 123 nests (24 nests failed and 99 nests successful hatched). Female breathing rate and concealment above the nest were associated with nest success during incubation: nests with greater concealment by vegetation above the nests and nests of females with lower breathing rate had higher nest success during incubation, while there were no other significant predictors of nesting success (Table 4).

Table 4

Predictors of clutch success of nesting chestnut thrushes. Significant predictors are highlighted in bold.
Predictors	Estimate	χ2	P
Breathing rate	-0.053	4.132	0.042
Activity	0.214	1.793	0.181
Nest height	-0.490	1.742	0.187
Nest lateral concealment	0.796	0.522	0.470
Concealment above the nest	1.884	3.915	0.048
Concealment below the nest	-0.812	0.805	0.370
Distance to human settlement	-0.004	1.539	0.215
Distance to farmland (m)	0.001	0.001	0.978
Distance to road (m)	-0.004	1.779	0.182

Our results found that breathing rate and activity were related to fine-scale nest site selection of chestnut thrushes: more active females chose nest sites with greater nest lateral concealment, and females with lower breathing rates selected nest sites with lower concealment above the nest. Moreover, we found that clutch size was associated with breathing rate of females, but not body mass or nest site characteristics. Interestingly, we found that nest success during incubation was associated with personality traits and fine-scale nest site characteristics in chestnut thrushes.

Previous studies have found that larger-scale nest site selection can be personality-dependent in some species ^17,26,28,48. In contrast to previous studies, we found that fine-scale nest site characteristics were associated with personality traits in chestnut thrushes. Furthermore, we found that the activity was positively related to lateral nest concealment. Increased activity may make individuals more conspicuous to visual predators ⁴⁹, as has been noted for Siberian Chipmunk (Tamias sibiricus) and Large Hawk Cuckoo (Cuculus sparverioides) ⁵⁰, whereas greater lateral concealment of nests could reduce the ability of predators to locate nests. In our study, females with lower breathing rates nested at sites with lower vegetation concealment above the nest, in contrast with the findings by Seltmann, et al. ²⁸ who found that bold females chose sites with greater concealment and that were located further from the high-risk shoreline environment. Nest site selection reflects a trade-off between visibility and concealment ^51,52: greater concealment may have higher nest success, but may increase the predation risk for females ²⁸. Lower vegetation concealment above nests could also increase female exposure to predators, leaving females to make a rapid decision to quickly escape or to fight with predators. Thus, in our study population, lower breathing rate females have to make a trade-off between their own survival and nest success during incubation.

The pace-of-life syndrome (hereafter POLS) hypothesis predicts individuals with different personality traits make a trade-off between allocations to current and future reproduction ^53,54, with more active individuals placing greater investment in their current reproduction season. Our results provide some support for this in that breathing rate of females was negatively related to clutch size (see also Zhao, et al. ²⁶. However, some studies have found that female personality traits are not related with either clutch or brood size ^9,55,56. These different results may be affected by the interaction of individual age and personality types. Dingemanse, et al. ³³ found that individuals with lower exploratory rates produced moderate-sized clutches throughout their lives, whereas faster-paced explorers produced moderate-sized clutch when young, but clutch size decreased with age. Currently there is no suitable method to actually age chestnut thrushes in the field because we captured so few individuals across years, and further studies are needed to provide further empirical evidence of the POLS hypothesis.

We failed to find any relationships between nest site characteristics and clutch size in chestnut thrushes, in contrast to several other studies ^31,57. One potential explanation for this: chestnut thrushes produce greater clutch size at nesting sites with lower predation risk but have reduce clutch sizes in higher predation risk nesting sites ^58,59. Hu, et al. ⁵⁰ found that in our study site, there are a number of natural nest predator species including small mammals and cuckoo species, and almost 50% of chestnut thrush nests fail due to nest predation ⁶⁰. In this scenario, such high nest predation risk may dilute the positive effects of fine-scale nest site characteristics.

Bird species that construct open-cup nests could benefit from greater nest concealment ^61,62. In our study, female chestnut thrushes that chose nest sites with greater concealment above the nests had a higher survival rate during incubation, which may suggest that aerial predators such as Large Hawk Cuckoo (Cuculus sparverioides) and Elliot’s Laughingthrush (Garrulax elliotii) ⁵⁰ pose a particular risk at our study site. Furthermore, our results differ from Zhao and Sun ⁶⁰ who found that concealment of nests from below was positively correlated with better daily nest survival rates. Inter-annual differences in predator species abundance and use of different nest stages in both studies may account for the different results between these two studies e.g. we only focused on the incubation period whereas Zhao and Sun ⁶⁰ examined all nest stages from nest development to nestling stage.

Our results showed that female chestnut thrushes with lower breathing rates were more likely to be successful during incubation. It is possible that lower breathing rate females could be more successful at efficiently defending their nests against predators when they are incubating. Breathing rate has been regarded as an indicator of boldness ^54,63,64 with a lower breathing rate reflecting more bolder females, which may then respond more boldly to drive away or fight with nest predators ⁶⁵, thus contributing to lower nest failure and higher nest success rates ^66,67. Furthermore, boldness can covary with other personality traits, comprising of a suite of behaviors or ‘behavioral syndromes’ ², such as aggression and exploratory, which may further promote individuals to participate in nest defense ³⁶. Further investigations are needed to identify the relationship between personality traits and nest defense by visual and acoustic stimulus experiments.

In conclusion, this study provides some of the first evidence to show the relationship between personality traits and fine-scale nest site selection, in support of the personality-matching habitat choice hypothesis. Breathing rate was associated with clutch size, thus providing some support for the pace-of-life syndrome hypothesis. Our study also identified a relationship between nest success during incubation and personality traits. Collectively, these findings highlight an important linkage between fine-scale nest site selection and nest success with certain personality traits in birds, and makes a valuable contribution to addressing the knowledge gap in our understanding of the roles of personality traits in animal reproduction.

Study area

This study was conducted during 2013–2016 on a wild breeding chestnut thrush population located at the north edge of the Lianhuashan Nature Reserve, Gansu Province, in central China (34°40’N, 103°30’E). More detail information about the reserve and local climate can be found in Sun, et al. ⁶⁸. In our study area, only female chestnut thrushes select nest sites, in which they build open-cup nests in trees and shrubs during early May to late June ^50,60. We searched for nests of chestnut thrushes from late April to early July in each year of the study. Clutch size was recorded when female began to incubate, and nests were monitored until nest fate was determined.

Nest site characteristics

We collected seven nest site characteristics when the nest fate failed or successfully fledge. Two scales of nest site characteristics were measured: large-scale which included distance of nest to human residences (m), distance of nest to farmland (m), distance of nest to the nearest road (m); and fine-scale measurements which included nest height (to the nearest 0.1 m), nest lateral concealment, and concealment above and below the nest. To minimize variation estimated by different observers, the same person (YB Hu) measured all nest site characteristics. All measurements followed Hu, et al. ⁵⁰: nest height was defined as the distance from the nest to the ground, to the nearest 0.1 m; nest lateral concealment was measured as the estimated vegetation cover from the most obvious direction at a distance of 3 m after observer checked from all directions. Concealment above and below the nest were recorded by estimating the percentage of vertical vegetation cover at 1 m above and 1 m below each nest, respectively. In addition, we recorded the location of all nests using a Global Positioning System (GPS) receiver, and then used the ArcGIS 10.2 (ESRI, Inc., Redlands, CA, USA) to measure the distances to human residences, roads and farmland habitat (to the nearest 1 m).

Measurement of personality traits

Two personality traits, activity and breathing rate, were measured in 2013–2016. Activity was measured between 0900 and 1700 by using a simple cage test based on Kluen at al. 2012 and adapted by Zhao, et al. ²⁶ and Lou, et al. ¹⁵. We recorded the activity behaviors (such as walk, hop and fly) for 5 min after a ten-minute acclimatization in the cage (size: L 60 × W 36 × H 60 cm) using JVC (GZ-E265AC). JWatcher software was used to analyse all recorded activity data (Blumstein et al. 2006). We calculated weighted activity scores as the following formula, to account for differences in energy expenditure: activity score = walks × 1 + hops × 2 + flights × 3 ^15,26. Breathing rate was measured by using the handling stress test, and we recorded the total number of breast movements within 60 seconds ^15,26. In general, we assumed that birds with lower breathing rates are bolder than those with higher rates ^26,63.

Ethics declarations

All birds were captured under a bird ringing license issued from the China Bird Banding Center. All methods were carried out in the study were in accordance with the guidelines and regulations of the Animal Care and Use Committee of the Institute of Zoology, the Chinese Academy of Sciences. All experimental protocols were approved by Institute of Zoology, the Chinese Academy of Sciences, Permission number 2013/ 108. To reduce human disturbance during the incubation period, only one person checked each nest at a distance of over four m from the nest. We only checked nests during good weather conditions, when the ambient temperature was relatively high. Mist netting was done only under suitable weather conditions (no precipitation and low wind speed). Birds were trapped and released into the wild within 70 minutes near the trapping locations. No trapping-related mortality or nest abandon were recorded for females.

Statistical analyses

We constructed linear mixed models (LMMs) with individual identity as a random variable to calculate the repeatability of breathing rate and activity. In the model, activity was square root transformed to meet Gaussian distribution of residuals. To control for confounding factors, seven predictor variables were included in each model: date (Julian date), year, sex, test sequence of activity and breathing rate (i.e., 1: first, 2: second or 3: third test), time of day (where 1200 = 0, 1300 = 1, 1100 = -1, etc.), context (i.e., 1: before breeding, 2: incubation or 3: nestling period) and body mass. All continuous variables were mean centered and standardized. Likelihood ratio test (LRT) between the models with and without the random effect (bird ID) was used to test the statistical significance of the repeatability. We used the LMMs of breathing rate and activity to run 1000 simulations using the arm package ⁶⁹, and then used the average best linear unbiased predictors (BLUPs) for the intercepts of each individual as the personality score in the following analyses ³³.

Seven separate general linear mixed models (GLMMs) were used to examine the relationships between personality traits and each nest-site characteristic, including female breathing rate and activity as fixed effects. First, we used a GLMM to analysis the effects of nest-site characteristics, female body mass, activity and breathing rate on clutch size. A GLMM with binomial distribution was used to investigate whether nest success during the incubation period was affected by nest-site characteristics, females’ activity and breathing rate. Collinearity of fixed effects were examined to ensure the Variable Inflation Factor (VIF) with values < 2.5 ⁷⁰. In all GLMMs, we included female ID as random effect because some repeated measurements of females among years. We also added year as a random effect to reduce the effects of environmental variations among years. All LMMs and GLMMs were fitted with lmer and glmer functions from the lme4 package ⁷¹. All statistics were performed with R software (v. 3.2.2)⁷².

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Project 31472012 and 32070452).

Author contributions

Yingqiang Lou, Yuehua Sun design the work. Yingqiang Lou, Qingshan Zhao, Lijun Chen, Yunbiao Hu and Yun Fang performed the experiments in the wild, and help on the analysis of the data and edited the manuscript. Yingqiang Lou and Yuehua Sun wrote the first draft manuscript. Huw Lloyd help with the manuscript preparation and English writing. All authors reviewed the manuscript.

Conflict of interest

The authors declare that they have no competing interests.

Data availability statement

All data were presented in the supplemental materials.

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No competing interests reported.

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Personality-dependent nest site selection and nest success during incubation in a wild population of chestnut thrush Turdus rubrocanus

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