Similar nest defence strategies within pairs increase reproductive success in the eastern bluebird, Sialia sialis

Animal Behaviour 100 (2015) 174e182

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Similar nest defence strategies within pairs increase reproductive success in the eastern bluebird, Sialia sialis Jennifer L. Burtka, Jennifer L. Grindstaff* Department of Integrative Biology, Oklahoma State University, Stillwater, OK, U.S.A.

a r t i c l e i n f o Article history: Received 8 August 2014 Initial acceptance 16 September 2014 Final acceptance 20 November 2014 Published online MS. number: A14-00657R Keywords: behavioural compatibility nest defence pair coordination personality simulated territorial intrusion

Recent research suggests that individuals across a variety of taxa express consistent behavioural differences, or personality, which may affect reproductive success. Most previous studies of avian systems investigated the effects of individual personality on offspring recruitment and other fitness correlates, even in species with biparental care. Here we tested the potential for behavioural similarity within mated pairs of wild eastern bluebirds to impact reproductive success. Specifically, we quantified nest defence behaviour of males and females to address three hypotheses: (1) the individual personality hypothesis, which predicts that individuals with more aggressive personalities will have more nestlings survive to fledging; (2) the pair coordination hypothesis, which predicts similarly behaving pairs will have more nestlings survive to fledging; and (3) the pair intensity hypothesis, which predicts pairs with more aggressive personalities will have more nestlings survive to fledging. Pairs that had similar nest defence strategies produced more fledglings in support of the pair coordination hypothesis. We found no support for either the individual personality hypothesis or the pair intensity hypothesis. Thus, particularly in species with biparental care, it is important to consider the behaviour of both pair members to predict effects on reproductive success. © 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Although individual behaviour has been assumed to be flexible, recent research suggests that plasticity in individual behaviour is instead constrained by consistent individual behavioural differ
ale, ences (reviewed in: Dall, Houston, & McNamara, 2004; Re Reader, Sol, McDougall, & Dingemanse, 2007; Sih, Bell, & Johnson, 2004; Stamps & Groothuis, 2010; D. S. Wilson, 1998) and maintained by natural selection (D. S. Wilson, 1998). The terms per
ale et al., 2007) and sonality (Gosling, 2001), temperament (Re behavioural type (Bell, 2007; Sih & Bell, 2008; Sih et al., 2004) have all been used to describe consistent behavioural expression either across situations, consistent within the same context over time, or consistent across contexts at various times (Sih & Bell, 2008; Sih et al., 2004; Stamps & Groothuis, 2010). For the purposes of this paper, we will refer to consistent individual behaviour as a personality because behaviour was analysed temporally and not across contexts. In nonhuman species, consistent differences in behaviour are attributed to individual survival and recruitment advantages (Smith & Blumstein, 2008). In great tits, Parus major, fast-exploring

* Correspondence: J. L. Grindstaff, Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, OK 74078, U.S.A. E-mail address: [email protected] (J. L. Grindstaff).

females and slow-exploring males survived better in years with less food, with the reverse pattern during rich years (Dingemanse, Both, Drent, & Tinbergen, 2004). Likewise, activity and aggression levels in female North American red squirrels, Tamiasciurus hudsonicus, had a year-dependent effect on recruitment and survival, with more active and aggressive females having faster-growing offspring or more juveniles surviving overwinter, respectively, in some years
ale, & Boutin, 2007). Similarly, bolder but not in others (Boon, Re male rams (Ovis canadensis) survived longer compared to shyer
ale, individuals and had more reproductive success in later years (Re Martin, Coltman, Poissant, & Festa-Bianchet, 2009). In avian systems, analysis at the individual level reveals mixed support for a relationship between personality expression and fitness correlates. In general, nest defence behaviour is thought to be linked directly to offspring survival or to trade-offs affecting € nen, nestling success (Montgomerie & Weatherhead, 1988; Rytko 2002). For example, more aggressive male western bluebirds, Sialia mexicana, fed their mates less frequently during incubation and consequently had fewer nestlings fledge (Duckworth, 2006). In contrast, female Ural owls, Strix uralensis, that defended their nests more aggressively recruited more offspring (Kontiainen et al., 2009). Although assessments at the individual level may reveal sex-specific advantages of differing personalities, investigating the degree of similarity in personality expression within socially mated

http://dx.doi.org/10.1016/j.anbehav.2014.12.004 0003-3472/© 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

Female nest defence intensity

pairs may provide additional insight into factors affecting behaviour in species that engage in biparental care. Relative to individual behaviour, few studies have investigated the effects of personality within pairs on measures of offspring success. This is particularly important for species with biparental care as conflicts over parental investment may influence fitness (Lehtonen, Wong, Svensson, & Meyer, 2011; McNamara, Houston, Barta, & Osorno, 2003; Royle, Hartley, & Parker, 2002). Furthermore, mate choice and behavioural compatibility may have fitness implications. Studies of mate choice have revealed that pairs that associate with chosen rather than experimenter-selected mates benefit from higher reproductive success (Drickamer, Gowaty, & Wagner, 2003; Gjesdal, 1977; Ryan & Altmann, 2001), and behaviourally compatible pairs benefit from higher fertilization success (Drickamer et al., 2003; Sinn, Apiolaza, & Moltschaniwskyj, 2006), better offspring condition (Both, Dingemanse, Drent, & Tinbergen, 2005; Harris & Siefferman, 2014; Schuett, Dall, & Royle, 2011) and better parental coordination, resulting in more offspring reared to independence (Spoon, Millam, & Owings, 2006). In a wild population of great tits, pairs that mated with similarly behaving fastor slow-exploring partners had higher recruitment than dissimilar mates in some years but not in others (Dingemanse et al., 2004). To address the potential for behavioural similarity within pairs to impact fitness, we investigated the effects of nest defence behaviour and nest visit rate on reproductive success in a wild population of eastern bluebirds. In this population, females demonstrate strongly repeatable nest defence behaviour and males behave more plastically (Burtka & Grindstaff, 2013). Eastern bluebirds often remain mated throughout the breeding season and both parents care for nestlings and engage in nest defence behaviour (Gowaty & Plissner, 1998). We also examined differences in reproductive success and parental care within pairs that had similar defensive personalities to determine whether the intensity of nest defence behaviour affected offspring growth or reproductive success. Because eastern bluebirds engage in biparental care, we constructed four scenarios identifying potential behavioural defence strategies within pairs (Fig. 1). These within-pair strategies range from both the male and female showing high or low nest defence intensity (scenarios 2 and 4, respectively) to the male and female showing opposite intensities, in which one sex defended

Scenario 1 Male defence – low Female defence – high

Scenario 2 Male defence – high Female defence – high

Scenario 4 Male defence – low Female defence – low

Scenario 3 Male defence – high Female defence – low

Male nest defence intensity Figure 1. Schematic of potential relationships between nest defence intensities of male and female eastern bluebirds to illustrate expectations under the individual personality hypothesis, the pair coordination hypothesis and the pair intensity hypothesis.

175

more intensely than the other (scenario 1: females > males; scenario 3: females < males). From these scenarios, we tested three novel hypotheses and made the following predictions: (1) the individual personality hypothesis, in which individuals with more aggressive personalities will have more nestlings survive to fledging and will have higher brood growth rates (reproductive success for individuals within scenario 2 > scenarios 1 and 3 > scenario 4); (2) the pair coordination hypothesis, in which similarly behaving pairs will have more nestlings survive to fledging and will have larger and faster-growing broods than dissimilar pairs (reproductive success for scenarios 2 and 4 > scenarios 1 and 3); and (3) the pair intensity hypothesis, in which pairs with similar behavioural strategies and more aggressive personalities will have more nestlings survive to fledging and larger and fastergrowing broods (reproductive success for scenario 2 > scenario 4 > scenarios 1 and 3). We assessed eastern bluebird personalities utilizing a naturally occurring invasive competitor, the house sparrow, Passer domesticus, rather than relying on conventional models using humans or stuffed predators or capturing and testing birds in the laboratory to assess the relevance of nest defence behaviour in its natural context. METHODS Model Organism Eastern bluebirds are socially monogamous altricial passerines. Bluebirds lay one egg per day and clutch sizes range from three to seven eggs (Gowaty & Plissner, 1998). Pairs in this population produce up to three broods per season, although a fourth is sometimes attempted if an earlier brood is depredated. Both males and females feed nestlings, but only females brood young. Eastern bluebirds typically breed in open habitats and are obligate secondary cavity nesters (Gowaty & Plissner, 1998) that frequently compete with house sparrows, European starlings, Sturnus vulgaris, and tree swallows, Tachycineta bicolor, for access to limited nest sites (Gowaty & Plissner, 1998; Meek & Robertson, 1994; Newton, 1994). We chose house sparrows for this study because they are a frequent competitor in this population (Pogue & Schnell, 1994) and cannot be excluded from entering artificial nestboxes by altering the entrance hole diameter. Although house sparrows typically colonize near or within human-made structures (Lowther & Cink, 1992), both house sparrows and eastern bluebirds nest in and defend constructed nestboxes (Pogue & Schnell, 1994). House sparrows can displace bluebirds from a nesting site (Estabrook, 1907; Zeleny, 1976) and will destroy eggs and kill both adults and nestlings to compete for nestbox space (Gowaty, 1984). In this population, we have observed eastern bluebirds and house sparrows competing for access to nest sites and have also documented house sparrows displacing adults and killing nestlings at established boxes. House sparrow nesting material was removed from the nestboxes throughout the duration of this study to discourage sparrow breeding. Study Site This study was conducted on bluebird trails in and around Stillwater, Oklahoma (36
060 56.5700 N, 97
030 35.1500 W). Eastern bluebird nestboxes (N ¼ 144) were mounted ~1.5 m above the ground on T-posts or wooden fence posts bordering fenced rangeland, agricultural fields, or open areas owned by the city, Oklahoma State University, or private landowners. Boxes were located at least 50 m away from one another. Nestboxes were monitored twice weekly during 1 Marche1 September 2009 and 2010. Nests were checked daily once a

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completed nest was discovered to document the appearance of a first egg. After the laying date of the first egg was documented, nestboxes were checked twice weekly during regular monitoring. Clutches were considered complete when no additional eggs were recorded during the semi-weekly checks. Boxes were then checked daily starting 10 days after the final egg was laid to determine hatch date (day 0). After hatching date was documented, nest checks were performed twice weekly until nestling day 14. At nestling day 14, nests were again checked daily to determine fledging date and the number of nestlings surviving to fledging. Adult Capture and Measurements Most adults were captured using a modified prop trap (Friedman, Brasso, & Condon, 2008; Robinson, Siefferman, & Risch, 2004) after offspring had hatched, although many females were captured during late incubation (~4e6 days before hatching). All adults were banded with a U.S. Geological Survey metal leg band and a unique combination of three colour bands for easy field identification. Nestling Measurements To distinguish individual nestlings, we painted the nails with various colours of nail polish 5 days after hatching. We then returned to the nest on day 11 to band nestlings with a U.S. Geological Survey metal leg band. Nestlings were weighed to the nearest 0.1 g using a digital scale on days 5 and 14. Day 14 mass measurements were used because eastern bluebird nestlings asymptote in mass on day 13 (Pinkowski, 1975) and day 14 measurements approximate nestling body mass at the time of fledging (Siefferman & Hill, 2003). Day 5 mass measurements were subtracted from day 14 measurements for each nestling and averaged for the brood to determine the average mass change for each brood. On day 14, the right wing was flattened and measured to the nearest 0.25 mm using a wing rule and tarsus length was measured with digital callipers to the nearest 0.01 mm in triplicate. The median measurement was used to determine nestling body condition by calculating the residuals from a regression of day 14 mass on day 14 tarsus length (Schulte-Hostedde, Zinner, Millar, & Hickling, 2005). Body condition was calculated for each nestling and then averaged within the brood to calculate the average brood condition on day 14. We used the number of nestlings that successfully fledged as a measure of reproductive success. Nest Defence Behaviour We conducted simulated territorial intrusions with a live male house sparrow to quantify nest defence intensity (Burtka & Grindstaff, 2013; Grindstaff, Lovern, Burtka, & Hallmark-Sharber, 2012). In brief, nest defence trials occurred on nestling days 7e9 and between the hours of 0700 and 1300 hours Central Standard Time (CST). Male house sparrows were captured at least 1.5 km away from focal nestboxes. For trials, one male sparrow was placed in a galvanized wire cage (23  23  30.5 cm) secured to the top of the nestbox and covered with a cloth. The 2 min trial began when the sparrow was revealed after both eastern bluebird parents were spotted within 100 m of the nestbox. Parental nest defence intensity was quantified by counting the numbers of hovers and attacks displayed by each parent within 0.5 m of the sparrow cage. Individuals were then scored on an ordinal scale of 1e6 with 6 as the most aggressive using the number of hovers and attacks as criteria (sensu Burtka & Grindstaff, 2013; Duckworth, 2006; Grindstaff et al., 2012). Birds that did not attack the caged sparrow and did not fly or hover near the cage were assigned a score of

1. Birds that did not attack the caged sparrow, but flew or hovered near the cage one to five times were assigned a score of 2. Birds that did not attack the caged sparrow, but flew or hovered near the cage more than five times were assigned a score of 3. Birds that attacked the caged sparrow one to five times were assigned a score of 4. Birds that attacked the caged sparrow six to nine times were assigned a score of 5. Birds that attacked the caged sparrow more than nine times were assigned a score of 6. Pairs were subjected to a simulated territorial intrusion with a novel sparrow at each successive breeding attempt between one and four times per season. Bluebird social pairs were also presented with an identical empty cage to serve as a control. This control ensured that bluebirds were reacting to the presence of a house sparrow and not to the cage or the presence of observers. The cage was mounted on the box and revealed in the same manner as during the house sparrow trial. Parental behaviour was recorded for 2 min. Control trials occurred on nestling days 6e9 but not on the same day as a trial with a house sparrow. None of the bluebirds displayed nest defence behaviour during the control trials. Parental Care In 2009, we filmed parental behaviour on two separate days on nestling days 6e8 to determine the relationship between parental nest defence behaviour and parental visit rate. The methods used to quantify parental visit rate follow those outlined in Grindstaff et al. (2012). Parental behaviour was recorded between 30 min after sunrise and 1030 hours CST. We recorded two 60 min segments on two separate days. We analysed the repeatability of male and female parental behaviour from these two separate observations. The number of visits (trips/2 h) and the time that each adult spent inside the box (s/2 h) were recorded for each parent. For analyses comparing pair behaviour, we recalculated visit rate and time per nestling by adding both adult measurements together and then divided by the brood size (‘pair trips per nestling per 2 h’ and ‘pair time (s) per nestling per 2 h’, respectively) to control for variation caused by brood size. Ethical Note Research was approved by the Oklahoma State University Institutional Animal Care and Use Committee (IACUC; Protocol number: AS095). Bluebird banding was conducted under a U.S. Geological Survey banding permit (J.L.G.; Permit number 23593). No nests were abandoned as a result of trapping of females during incubation and nestlings were not harmed by marking or weighing. Statistical Analysis All statistical analyses were conducted in SAS (v. 9.2, SAS Institute Inc., Cary, NC, U.S.A.). Individuals or pairs were represented in the data set from one to six times. Males and females were run separately in analyses involving the influence of individual behaviour on a particular variable. We used independent two-tailed t tests to determine whether any of the measured variables differed between years. Birds that were given simulated territorial intrusions multiple times within a year or between years were randomly selected to appear only once in this data set to avoid pseudoreplication (males: 2009 (N ¼ 37), 2010 (N ¼ 38); females: 2009 (N ¼ 41), 2010 (N ¼ 46)). In other analyses testing differences between years, all nests were included in the data set as we were only considering differences between brood averages and not between sexes (2009: N ¼ 83; 2010: N ¼ 75).

J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

covariance to incorporate unequally spaced measurements (Littell, Milliken, Stroup, Wolfinger, & Schabenberger, 2006). We used the Kenward Rodger method to approximate denominator degrees of freedom. We selected models based on those that minimized Akaike's information criterion (Littell et al., 2006) and removed all nonsignificant covariates and interactions (P > 0.05) using backwards stepwise selection until the simplest model was obtained. In significant models with categorical fixed factors, Hochberg's (1988) GT2 post hoc multiple comparison method was used to reduce the likelihood of type I error due to an unbalanced design. RESULTS We did not detect a significant difference between male and female nest defence intensity (t159 ¼ 1.17, P ¼ 0.25). Mean intensity scores (±SE) were 3.57 ± 0.21 and 3.26 ± 0.18 for males and females, respectively. However, there was a significant positive correlation between male and female nest defence intensity scores within pairs (F5,85 ¼ 7.61, P < 0.01; Fig. 2). There was no relationship between visit rates (trips per nestling per 2 h: F1,41 ¼ 2.56, P ¼ 0.12) or time spent at the nest (s per nestling per 2 h: F1,41 ¼ 0.40, P ¼ 0.53) within pairs. Males and females did not differ in visit rate (t57 ¼ 1.51, P ¼ 0.14; mean ± SE trips per nestling per 2 h: males: 3.30 ± 0.28; females: 2.65 ± 0.34), although females spent more time in the box than males (t57 ¼ 3.27, P < 0.01; mean ± SE s per nestling per 2 h: males: 49.86 ± 5.44; females: 252.70 ± 64.98). Repeatability of Parental Behaviours We first tested whether our two measures of parental care were related to one another. In females, visit rate was not significantly related to time spent in the nestbox (F1,65.3 ¼ 0.61, P ¼ 0.44). In contrast, male visit rate was significantly related to time spent in the nestbox (F1,54.2 ¼ 44.32, P < 0.0001). The number of visits females made to the nestbox during parental care trials was significantly repeatable (MSA ¼ 20.10; MSW ¼ 6.85; t ¼ 0.40, SE ¼ 0.09; F47,88 ¼ 2.93, P < 0.0001). Similarly, the number of visits males made to the nestbox was also significantly repeatable (MSA ¼ 15.79, MSW ¼ 7.90; t ¼ 0.26, SE ¼ 0.10; F42,77 ¼ 2.00, P ¼ 0.0042). The

6

Female nest defence intensity

We found no significant differences between years in average brood condition at day 14 (t156 ¼ 0.07, P ¼ 0.95), average brood mass change between days 5 and 14 (t156 ¼ 0.62, P ¼ 0.54), average brood mass on nestling day 14 (t156 ¼ 0.37, P ¼ 0.71), or nest defence behaviour of either sex (males: t73 ¼ 0.28, P ¼ 0.78; females: t84 ¼ 1.21, P ¼ 0.23). However, we did detect a year effect for the average brood wing length on day 14 (t156 ¼ 2.05, P ¼ 0.04). Nestlings in 2009 had a higher average wing length than nestlings in 2010. Thus, year was included as an initial covariate in all subsequent analyses involving wing length as a dependent variable, but not in other analyses. Repeatability (t) of parental behaviour was calculated separately for males and females from the intraclass correlation coefficients (Lessells & Boag, 1987). Standard errors were calculated following Becker (1984). To test the pair coordination hypothesis, we determined the similarity of defence strategies within a breeding pair by subtracting the female aggression score from the male score. We grouped pairs into three categories (hereafter referred to as ‘pair score’) corresponding with the directional degree of behavioural similarity. Pairs that received the same nest defence intensity score or that differed in their intensity by one point were categorized as ‘similar’ in behaviour and were placed into one category (F z M; N ¼ 63). Pairs in which the female was more aggressive than her male partner by more than two points were placed in a second category (F > M; N ¼ 8), and pairs in which the male was more defensive than the female by two points (F < M; N ¼ 22) were placed into a third category. To avoid pseudoreplication for individuals that changed mates within or between seasons, we randomly selected one observation from those pairs, although pairs that maintained the same mate within a breeding season were included multiple times and were incorporated into the statistical model (N ¼ 66 unique pairs). To test the pair intensity hypothesis, we regrouped pairs in the F z M category (same score or a difference of one point in nest defence intensity; N ¼ 50 unique pairs) into five categories: F > M: pairs where the female was more defensive than the male by one point (N ¼ 14); F z M low: pairs in which both the male and female received a score of 1 or 2 (N ¼ 12); F z M moderate: pairs in which both the male and female received a score of 3 or 4 (N ¼ 10); F z M high: pairs in which both the male and female received a score of 5 or 6 (N ¼ 6); and F < M: pairs where the male was more defensive than the female by one point (N ¼ 21). The main goal was to determine whether individual or pair nest defence behaviour affected the number of nestlings that survived to fledging, nestling growth and parental care. To incorporate individuals that were tested repeatedly throughout the breeding season, we used general linear mixed models with individual identification number as the repeating subject. For pair analyses, unique pairs were assigned a two-string letter code that was used as the repeating subject. Repeated individuals or repeated pairs were assigned sequential trial numbers (1e6) depicting the number of times an individual or a pair appeared in the data set. This trial number was then incorporated as a nested effect. In analyses involving nest defence scores of pairs or individuals, either the pair score or the individual score was incorporated as a fixed effect. A previous study revealed that brood size did not influence nest defence intensity (Burtka & Grindstaff, 2013), so brood size was not included as a covariate in analyses. Depending on the independent variable, either the day 0 Julian date, the Julian date of the simulated territorial intrusion, or the Julian date of the first videotaped parental care trial was initially included as a covariate to account for behavioural changes due to season. We selected the closest covariate based on proximity to the independent variable. After extensively modelling the covariance structures, we used an unstructured

177

5

4

3

2

1 1

2 3 4 5 Male nest defence intensity

6

Figure 2. Relationship between nest defence intensity of male and female eastern bluebirds within socially mated pairs (N ¼ 66). Circle size is indicative of the number of overlapping points: small circles (N ¼ 5 individuals); medium circles (N ¼ 10 individuals); large circles (N ¼ 15 individuals).

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J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

time females spent inside the nestbox during visits was not significantly repeatable (MSA ¼ 507 193; MSW ¼ 377485; t ¼ 0.11, SE ¼ 0.09; F47,88 ¼ 1.34, P ¼ 0.12). Male time spent inside the nestbox was repeatable across trials (MSA ¼ 4448, MSW ¼ 1905; t ¼ 0.31, SE ¼ 0.10; F42,77 ¼ 2.33, P ¼ 0.0006). Test of Individual Personality Hypothesis There was no relationship between individual parental nest defence intensity and the number of nestlings that successfully fledged for either sex (Table 1). Similarly, we found no relationships between individual nest defence intensity and any of the measures of nestling growth (Table 1). Furthermore, parental nest defence intensity was not related to other measures of parental care (Table 1). None of the measures of nestling growth or status on day 14 were related to parental care (Table 2). Interestingly, there was a significant negative relationship between male visit rate and the number of nestlings that survived to fledging (Table 2). We initially detected a similar relationship in females. There was a significant negative relationship between the time per nestling that females spent inside the nestbox and the number of successful fledglings (F1,65 ¼ 7.70, P ¼ 0.01). However, this relationship was primarily due to the influence of three females that spent more than 1500 s inside the nestbox. If these females were removed from the analysis, the relationship between time per nestling and reproductive success was no longer significant (Table 2).

Table 2 Results from final general linear mixed models assessing the effects of individual parental care of eastern bluebirds on reproductive success, brood growth rates and offspring size and condition on day 14 Sex

Dependent variable

Independent variable

df

F

P

Male

Reproductive success

Visit rate (trips/nestling)

1, 57

3.35

0.01

1, 1, 1, 1, 1, 1,

53 53 53 53 53 57

0.22 0.13 0.54 1.78 0.03 3.04

0.64 0.72 0.46 0.19 0.87 0.09

1, 1, 1, 1, 1, 1,

53 53 53 53 54 65

0.57 0.30 0.00 3.48 0.28 0.06

0.45 0.59 0.98 0.07 0.60 0.81

1, 1, 1, 1, 1, 1,

60 60 60 60 61 62

2.56 1.54 1.91 1.19 1.02 2.72

0.11 0.22 0.17 0.28 0.32 0.10

1, 1, 1, 1, 1,

60 60 60 60 61

0.02 0.00 0.00 2.36 0.29

0.90 0.99 0.95 0.13 0.59

Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition Reproductive success

Female

Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition Reproductive success Avg. Avg. Avg. Avg. Avg.

Test of Pair Coordination Hypothesis There was a significant effect of pair defensive tactics on reproductive success (Table 3). Pairs that defended similarly and pairs in which the male was more aggressive than the female had more nestlings fledge successfully compared to pairs in which the female defended more intensely than the male (Table 4, Fig. 3). To test for assortative mating on the basis of nest defence strategy, we conducted a test of independence after assigning both the male and female member of each pair to either a low nest defence intensity category (scores 1e3), or a high nest defence intensity category (scores 4e6). We found that bluebirds were mated assortatively on the basis of nest defence intensity (c2 1 ¼ 30:46, N ¼ 122, P < 0.001). We found no other relationships between pair nest defence measures and any nestling growth variables (Table 3). Furthermore, the combined pair visit rate and time at the nestbox were not predictive of any measures of brood status (Table 5).

Table 1 Results from final general linear mixed models testing the effect of individual nest defence scores of male and female eastern bluebirds based on measures of reproductive success, nest visit rate and brood growth rates and condition on day 14 Sex

Dependent variable

df

Male

Reproductive success Visit rate (trips/nestling) Time at box (s/nestling) Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition Reproductive success Visit rate (trips/nestling) Time at box (s/nestling) Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition

5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5, 5,

Female

124 49 49 113 113 113 113 113 145 55 55 129 129 129 129 129

F

P

0.57 1.16 0.65 0.32 0.91 1.74 0.41 0.96 0.92 0.36 0.29 0.50 0.68 1.15 0.51 0.57

0.72 0.34 0.66 0.90 0.48 0.13 0.84 0.45 0.47 0.87 0.92 0.78 0.64 0.34 0.77 0.73

Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition Reproductive success

brood brood brood brood brood

Time at box (s/nestling)

Visit rate (trips/nestling)

Time at box (s/nestling)

mass change (g) day 14 mass (g) day 14 wing (mm) day 14 tarsus (mm) day 14 condition

However, we did find a nonsignificant tendency for a positive relationship between the time that pairs spent at the nestbox and reproductive success (Table 5). Test of Pair Intensity Hypothesis When we focused our analysis on pairs with similar defensive strategies (F z M as described in the Methods), we found no Table 3 Results from final models testing the effect of similarity in nest defence behaviour within pairs of eastern bluebirds on reproductive success, nest visit rate and offspring growth Dependent variable

df

Reproductive success Visit rate (trips/nestling) Time at box (s/nestling) Avg. brood mass growth (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition

2, 2, 2, 2, 2, 2, 2, 2,

88 48 47 80 80 81 80 80

F

P

5.64 0.30 0.15 0.31 0.21 0.45 1.08 0.13

0.01 0.74 0.86 0.74 0.81 0.64 0.34 0.88

Table 4 Results of Hochberg's pairwise comparison for differences in reproductive success of eastern bluebirds in each pair defence category Group 1

Group 2

t88

P

F>M F>M F
FzM F
2.52 3.34 1.75

0.01 <0.01 0.23

F > M (N ¼ 8): females received a higher nest defence intensity score than males by two or more points; F z M (N ¼ 63): males and females received the same nest defence intensity score or differed by one point; F < M (N ¼ 22): males received a higher nest defence intensity score than females by two or more points.

b

5

b

a

4 3 2 1 0

F>M

F

F
M

Similarity category Figure 3. Box plot showing the median (heavy lines within boxes), 25% and 75% quartiles (boxes) and 1.5 times the interquartile range (whiskers) for the number of successful fledglings for eastern bluebird pairs with different behavioural strategies. Pair behaviour is divided into three categories depending on the degree and direction of similarity. F > M: the female was more aggressive than the male by more than two points; F z M: pair members received the same intensity scores or differed by one point; F < M: the male was more aggressive than the female by two points. Letters above each bar indicate significant differences between groups.

significant effect of pair nest defence intensity on reproductive success (Table 6). Nest defence intensity of similarly behaving birds did not influence average brood condition or average wing length or body mass on day 14 (Table 6). However, we did detect a significant difference in average brood mass change within pairs that defended similarly (Table 6), but the conservative post hoc Hochberg's adjustment revealed a lack of any significant pairwise comparisons between categories. Offspring of pairs in which the female defended more aggressively than the male tended to gain the most mass between days 5 and 14. There was also no relationship between pair visit rate and nest defence intensity (Table 6), but pairs in which both male and female defended utilizing highly aggressive behaviours (a score of 5 or 6) spent more time in the nestbox than less aggressive pairs, even when pairs that spent more than 1500 s inside the nestbox were removed from the analysis (Table 6, Fig. 4). DISCUSSION Although individual personality expression is the focus of many studies, strategies within a mated pair may be of central Table 5 Results from final general linear mixed models testing the effect of parental nest visit rate by both members of a pair on reproductive success and offspring growth in eastern bluebirds Dependent variable

Independent variable

df

F

P

Reproductive success

Pair visit rate (trips/nestling)

1, 55

1.95

0.17

1, 1, 1, 1, 1, 1,

52 51 51 51 53 54

0.03 1.55 0.77 0.28 0.03 3.77

0.87 0.22 0.38 0.60 0.87 0.06

1, 1, 1, 1, 1,

52 52 51 51 52

0.21 0.20 0.14 1.35 0.00

0.65 0.65 0.71 0.25 0.99

Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition Reproductive success Avg. Avg. Avg. Avg. Avg.

brood brood brood brood brood

mass change (g) day 14 mass (g) day 14 wing (mm) day 14 tarsus (mm) day 14 condition

Pair time at box (s/nestling)

179

Table 6 Results from final models comparing nest defence intensity strategy of eastern bluebird pairs that defended similarly in the simulated territorial intrusion and reproductive success, nest visit rate and offspring growth

6

Dependent variable

df

Reproductive success Visit rate (trips/nestling) Time at box (s/nestling) Avg. brood mass change (g) Avg. brood day 14 mass (g) Avg. brood day 14 wing (mm) Avg. brood day 14 tarsus (mm) Avg. brood day 14 condition

4, 7, 4, 4, 4, 4, 4, 4,

56 22 24 49 49 49 49 49

F

P

0.53 0.54 2.88 2.59 1.13 1.92 0.56 1.13

0.71 0.80 0.04 0.05a 0.35 0.12 0.69 0.35

Pair members that defended similarly (category F z M) were reclassified into five groups depicting the level or direction of nest defence intensity: F > M: females were more defensive than males by one point; F < M: males were more defensive than females by one point; F z M low: pair members defended equally with a score of 1 or 2; F z M moderate: pair members defended equally with a score of 3 or 4; F z M high: pair members defended equally with a score of 5 or 6. a Post hoc tests revealed no significant differences between groups for average brood mass change between nestling days 5 and 14.

importance, especially in species that have biparental care. This study tested three hypotheses in relation to individual and pair nest defence behaviour: (1) the individual personality hypothesis, which predicts that individuals with more aggressive personalities will have high reproductive success and brood growth rates; (2) the pair coordination hypothesis, in which similarly behaving pairs are predicted to have more nestlings survive to fledging and higher offspring growth rates than pairs that are dissimilar in behaviour; and (3) the pair intensity hypothesis, which predicts that within similarly behaving pairs, those pairs with aggressive personalities will have higher reproductive success and nestlings with higher growth rates (Fig. 1). As we demonstrated, reproductive success was not related to individual nest defence behaviour or overall nest defence intensity of the pair, but rather

1200 Pair time (s) at box per nestling per h

Reproductive success (nestlings fledged)

J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

b

1000 800 600

a

400 a

a

a

200 0 F>M

F M F M F M moderate high low Intensity category

F
Figure 4. Box plot showing the median (lines within boxes), 25% and 75% quartiles (boxes) and 1.5 times the interquartile range (whiskers) for the amount of time that eastern bluebird pairs spent inside the nestbox within similarly behaving pairs that defended with varying intensities. Pair behaviour is divided into five categories depending on the degree and direction of similarity. F > M: the female was more aggressive than the male by 1 point; F z M low: the male and female received a score of 1 or 2; F z M moderate: the male and female received a score of 3 or 4; F z M high: the male and female received a score 5 or 6; F < M: the male was more aggressive than the female by 1 point. Letters above each bar represent significant differences between groups.

180

J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

reproductive success was most impacted by asymmetry in nest defence intensity within mated pairs in support of the pair coordination hypothesis. Pairs of eastern bluebirds that defended similarly and in which the male was more aggressive than the female produced more fledglings compared to nests where the female was more aggressive than the male. In addition, bluebirds were mated assortatively on the basis of nest defence intensity. Of the three categories indicating mate similarity in nest defence behaviour, we had the greatest number of pairs in the similar category (F z M; N ¼ 63) compared to the groups where females had more aggressive male partners (F < M; N ¼ 22) and pairs where the female was more aggressive than the male (F > M; N ¼ 8). Thus, asymmetries in nest defence between pair members had the greatest impact on reproductive success when females defended aggressively and males did not. Overall, we found little support for the pair intensity hypothesis; there was no relationship between the level of aggression expressed and reproductive success within pairs that behaved similarly against a house sparrow intruder. Within pairs that defended similarly, there was a significant effect of nest defence intensity on the average change in brood mass during the nestling period, but none of the post hoc comparisons were significant and pairs that defended most intensely did not produce offspring that gained the most mass. Thus, the intensity of nest defence within a pair may not be as important as the coordination of behaviour within pairs. Previous studies have also demonstrated that mated pairs with more similar personalities successfully rear more young to independence (Dingemanse et al., 2004; Spoon et al., 2006) or rear young in better body condition (Both et al., 2005; Harris & Siefferman, 2014; Schuett et al., 2011). In cockatiels, Nymphicus hollandicus, behaviourally compatible pairs showed increased coordination and less parental conflict while incubating eggs: only one parent at a time incubated and the nest was left unattended less frequently compared to less compatible pairs, which resulted in greater hatching success (Spoon et al., 2006). Our results also support findings from a study of competitive interactions between eastern bluebirds and tree swallows in North Carolina, U.S.A. Bluebird pairs with similar levels of aggressive nest defence against conspecific intruders nesting in areas with high densities of tree swallows produce heavier fledglings than pairs that mate disassortatively (Harris & Siefferman, 2014). In this North Carolina population, which is at the front of a natural range expansion of tree swallows, Harris and Siefferman (2014) found no relationship between similarity of nest defence behaviour to an eastern bluebird intruder and offspring mass in areas of low tree swallow density. In contrast, tree swallows are rarely observed at our study site (N ¼ 1 in 5 years), and we found benefits of similar nest defence behaviour within pairs throughout the study site, which includes areas of low and high house sparrow density (Burtka & Grindstaff, 2013). We also found a trend for a relationship between attendance of the nestbox and reproductive success, providing additional support for the importance of pair coordination in the behaviour of native species competing for limited nesting sites with an invasive competitor. We were unable to determine whether adults simply adjust their behaviour to mimic the defensive strategy of their mate, although repeatability data from this population suggest that individuals may be relatively fixed in their level of nest defence intensity. We analysed the repeatability of nest defence behaviour within and between years and found that eastern bluebird females were highly repeatable in nest defence behaviour and males were repeatable in 2010 but not in 2009 or across years. Although eastern bluebird females were more predictable in nest defence strategy than males, both sexes still demonstrated repeatable behaviour indicative of personality (Burtka & Grindstaff, 2013).

Females with fixed behavioural strategies may rely on cues from males to indicate behavioural compatibility during pair bond formation rather than coordinating parental effort after pair bond formation. There is some evidence from other systems that supports female mate selection on male personality (Kralj-Fiser,
r, & Schneider, 2013; Schuett et al., Sanguino Mostajo, Preik, Peka 2011; Schuett, Tregenza, & Dall, 2010). Because we did not quantify nest defence behaviour of pair members in isolation, we cannot exclude the hypothesis that individuals with low nest defence intensity generally increase the intensity of their defensive responses when paired with an individual that displays high nest defence intensity. However, the limited data we had for females that switched mates between years or within seasons but maintained consistent levels of nest defence behaviour did not support this hypothesis. Future experimentation is needed to quantify nest defence intensities of pair members in isolation and to determine whether sexual selection is acting on personality in this population. It would also be interesting to determine whether females showing a specific personality repeatedly select similar males in successive years. Our two measures of parental care, the number of visits and time spent inside the nestbox, were significantly correlated within males but not within females. In bluebirds, only females brood young and bluebird nestlings are able to thermoregulate independently at 5e8 days posthatch (Gowaty & Plissner, 1998). We recorded parental care twice between nestling days 6e8; thus, our first measure of parental care probably reflects attendance to both feed and warm nestlings. The amount of time that females spend inside the nestbox is likely to be much more sensitive to environmental conditions and nestling age than male attendance time. This hypothesis is supported by our analyses of the repeatability of parental behaviour. Both the visit rate and the time spent inside the nestbox were moderately repeatable in males, whereas only nest visit rate was significantly repeatable in females. Parental provisioning behaviour is, therefore, another component of eastern bluebird personality (Barnett, Thompson, & Sakaluk, 2012; Mutzel, Dingemanse, Araya-Ajoy, & Kempenaers, 2013). Within bluebird pairs that defended similarly, we found that pairs with aggressive personalities spent more time inside the nestbox compared to those with other strategies. Pair defensive strategy may be positively linked to nest attentiveness or vigilance. Despite research that supports a trade-off between vigilance and other measures of parental care (e.g. Rosa & Murphy, 1994), aggressive behaviour has been linked to boldness (Verbeek, Boon, & Drent, 1996) and exploration (Carere, Drent, Privitera, Koolhaas, & Groothuis, 2005; Dingemanse & de Goede, 2004; A. D. M. Wilson & Godin, 2009). Thus, it is possible that nest defence behaviour and nest vigilance or attentiveness are correlated at the pair level in eastern bluebirds, but future studies would need to discover links between other correlated suites of behaviours to uncover the behavioural syndrome. We did not specifically measure the coordination of parental care within pairs. It is possible that aggressive pairs staggered their visits to the nestbox or the female remained inside the nestbox while the male provisioned both her and the nestlings. We did not find support for the individual personality hypothesis or the pair intensity hypothesis. The only significant effect we detected for measures of individual parental care was a negative relationship between the number of fledglings and male visit rate. There is support for a positive relationship between increased activity at the nest and nest predation in some species of birds (Martin, Scott, & Menge, 2000; Muchai & du Plessis, 2005; Skutch, 1949) and high predation risk may favour low parental activity levels (Massaro, Starling-Windhof, Briskie, & Martin, 2008; Peluc, Sillett, Rotenberry, & Ghalambor, 2008). Thus, more experienced or

J. L. Burtka, J. L. Grindstaff / Animal Behaviour 100 (2015) 174e182

higher-quality parents may provision nestlings with higher-quality food items in fewer visits to the nest (Wright, Both, Cotton, & Bryant, 1998). This study demonstrates that reproductive effects should be examined at both the pair and individual levels in species that show biparental care in light of the pair coordination hypothesis. In species that experience high levels of competition for limited nesting sites, coordination of defensive behaviours within mated pairs or assortative mating on the basis of personality may be under strong selection and pairs with similar behaviour may be most effective at repelling competitors. The ability either to adjust behaviour to match that of a mate, or to mate assortatively may be an important defence for native species competing with aggressive invasive species.

Acknowledgments We acknowledge the support of numerous field assistants that assisted with nestbox monitoring throughout the study. Funding was provided by research grants from Bob and Julia Bollinger, the Oklahoma Ornithological Society, the Department of Zoology at Oklahoma State University and the Payne County Audubon Society. We also thank Ken Yasukawa and two anonymous referees for insightful comments on the manuscript.

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