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Behavioral Plasticity Is Not Significantly Associated with Head Volume in a Wild Chestnut Thrush (Turdus Rubrocanus) Population Qingshan Zhao1,2 and Yuehua Sun1*

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Behavioral Plasticity Is Not Significantly Associated with Head Volume in a Wild Chestnut Thrush (Turdus Rubrocanus) Population Qingshan Zhao1,2 and Yuehua Sun1* Zhao and Sun Avian Res (2016) 7:12 DOI 10.1186/s40657-016-0048-z Avian Research RESEARCH Open Access Behavioral plasticity is not significantly associated with head volume in a wild Chestnut Thrush (Turdus rubrocanus) population Qingshan Zhao1,2 and Yuehua Sun1* Abstract Background: The drivers of intraspecific variation in behavioral plasticity are poorly known. A widely held hypothesis is that brain size is positively correlated with behavioral plasticity. Methods: A total of 71 Chestnut Thrushes (Turdus rubrocanus) were caught in the wild population. We quantified behavior plasticity of activity of individuals measured in the same cage across two contexts (common and with a novel object stimulation), using a random regression analysis. We then investigated whether head volume (a proxy for brain size) was associated with behavioral plasticity in activity level using Spearman rank-order correlation. Results: We found no significant evidence that activity plasticity was associated with relative head volume. There was no sex difference in head volume or in variance in head volume. Conclusions: We speculate that the absence of an association between brain volume and activity behavior plasticity may result from the inaccuracy of using external skull measurements to estimate brain size, or from a particular part of the brain being responsible for plasticity in activity level. Keywords: Activity, Behavioral plasticity, Chestnut Thrush, Head volume Background behaviors based on current different contexts or environ- Behavioral plasticity is the ability of an animal to alter its ments, regardless of the past environment (Dingemanse behavior in response to changes in the environment, and and Wolf 2013; Snell-Rood 2013). Differential activation the evolutionary causes and consequences of behavioral of an underlying neural network may result in plasticity plasticity has received much attention in the past four (Snell-Rood 2013). An increase in behavioral plasticity decades (Dingemanse et al. 2010; Betini and Norris 2012). should correspond to an increase in sensory input and Snell-Rood (2013) defined two major forms of behavioral neuron number and ultimately overall brain size (Snell- plasticity: developmental and activational. Developmen- Rood 2013). tal behavioral plasticity is analogous to the traditional The relative brain size of birds is comparable to that definition of phenotypic plasticity: environmental con- of mammals, but varies greatly among taxa (Winkler ditions at a specific life history phase drive individual et al. 2004; Day et al. 2005). Studies have revealed that behavior into an irreversible developmental trajectory, brain size of bird is correlated with measures of behav- and result in a fixed behavioral phenotype in adulthood ioral flexibility such as invasion success (Sol and Lefeb- (Piersma and Drent 2003; Dingemanse and Wolf 2013). vre 2000; Sol et al. 2002; Møller and Erritzøe 2015), life Activational behavioral plasticity is short-term environ- history traits (Iwaniuk and Nelson 2003), feeding inno- mental effects on behavior: individuals express different vation (Lefebvre et al. 2004), food hoarding (Garamszegi and Eens 2004), migration (Shultz et al. 2005), and escape *Correspondence: [email protected] strategy (Samia et al. 2015). Compared with a large body 1 Key Laboratory of Animal Ecology and Conservation Biology, Institute of studies that addressed interspecific variation in brain of Zoology, Chinese Academy of Sciences, Beijing 100101, China Full list of author information is available at the end of the article size, studies of brain size at the intraspecific level, even © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhao and Sun Avian Res (2016) 7:12 Page 2 of 6 intra-population level, have only recently started (Gonda Simple cage test et al. 2013). Although intraspecific variation in brain Each bird was tested individually in a standard cage size is smaller than interspecific variation (Gonda et al. (50 cm × 36 cm and 60 cm high) similar to that described 2013), there also exists an association between brain size by Kluen et al. (2012) between 0900 and 1600 hours. and behavioral flexibility at the within-population level, After a habituation period of 10 min, the experimenter including migratory behavior (Møller 2010; Fuchs et al. briefly entered his hand in the cage, as if something was 2015), food hoarding (Roth and Pravosudov 2009), anti- hanged from the roof of the cage. After that, we vid- predator behavior (Öst and Jaatinen 2015) and breeding eoed the bird for 5 min, and this is the baseline session. strategies (Jaatinen and Öst 2016). Thus behavioral plas- Then, we hung a novel object (a pink plastic pig measur- ticity should be linked with brain size at the intra-popula- ing 6 cm × 5 cm × 10 cm, presumably unknown in this tion level (Mery and Burns 2010). natural environment) from the roof of the cage, and then The aim of this study was to test whether variation in video-recorded for 5 min (the test session). To quantify behavioral plasticity correlate with brain size in a wild behavioral plasticity, we quantified the activity (5-min Chestnut Thrush (Turdus rubrocanus) population. Quan- records of the number of hops and short flights within tification of behavioral plasticity under natural condi- and between perches) in these two sessions, respectively. tions could be a challenge. First, environmental variables Twenty-three recaptured birds were tested twice in dif- may show little variation, and it may be difficult to quan- ferent days (with at least 7-day interval). tify a given condition experienced by the subject (Lefeb- vre et al. 2004). Second, conspecifics and heterospecifics Statistical analyses in the surroundings can affect the measurement of an The repeatability of head volume measured on different individual’s behavior (Kluen et al. 2012). Thus it may be days was calculated using a linear mixed model (LMM) better to evaluate individual behaviors in an artificial, with individual identity (ID) as a random effect. Fol- standard environment. Therefore, we used a modi- lowing recommendations of Nakagawa and Schielzeth fied simple cage test developed by Kluen et al. (2012) to (2010), information on individuals with only one meas- quantify individual behavioral plasticity of activity. Activ- ure was retained. We used the function rpt.remlLMM ity level may be a key trait that links behavior to feeding of R package ‘rptR’ to calculate repeatability and p val- rate and predation risk (Sih et al. 2004). The response to ues for repeatability derived from log likelihood ratio novel stimuli has been described as a simple mechanism test (LRT) (Nakagawa and Schielzeth 2010). To calculate to regulate ecological plasticity (Brown et al. 2013). So relative head volume, the allometric effect needs to be we use the change of activity in the presence and absence accounted for (Iwaniuk and Nelson 2003). We first ran a of the novel object to quantify the behavioral plasticity. linear regression to test whether sex, wing length, tarsus Brain size is tightly correlated with head volume, so we length and body mass were significantly associated with use head volume as a proxy for brain size (Møller 2010; head volume. We found that tarsus length was positively Öst and Jaatinen 2015). For reasons discussed above, we correlated with head volume. Therefore, we calculated predicted that behavioral plasticity is positively corre- the residuals (relative head volume) of a log–log least- lated with head volume. squares linear regression of brain volume against tarsus length (Iwaniuk and Nelson 2003; Sol et al. 2005). Methods We calculated behavior plasticity of activity of indi- Study area and subjects viduals measured in the same cage across two contexts We conducted this study in April‒July 2014 in a farm- (common and with a novel object stimulation), using a land landscape at the northern edge of the Lianhuashan random regression analysis (Nussey et al. 2007; Kluen Nature Reserve, Gansu Province, Central China (34.67°N, and Brommer 2013). We used the square-root transfor- 103.50°E). In our study area, Chestnut Thrushes start to mation of activity (to make error distribution approxi- build nests in late April and clutches are initiated from mate normality) as the response variable. As we were early May to late June. We used mist nets to catch birds. mainly interested in the random effects, we consid- All birds trapped were weighed (to the nearest 0.1 g), ered the slope of the regression line as behavior plas- measured for tarsus length (to the nearest 0.1 mm), wing ticity when the interaction between ID and context is length (to the nearest 0.1 mm), and head size (width, fitted as a random effect. As fixed effects, sex (female breadth, and height to the nearest 0.01 mm), and banded. and male), date (where April 17 = 1, April 18 = 2, etc.), We estimate head volume as the product of head length context, and test time (where 12 o’clock noon = 0, (minus beak length), head width, and head height to the 1 p.m. = 1, 11 a.m. = −1, etc.) were included in this nearest 0.01 ml according to Møller (2010). We captured model. Given that individuals were tested at different 71 adult birds. And 23 individuals were recaptured. times in their reproductive cycle, and hormone levels Zhao and Sun Avian Res (2016) 7:12 Page 3 of 6 and the resultant behavior change during the breeding Table 1 Summary of the linear model of head volume cycle, nest age (day 1 is the day of clutch initiation) was (mL) in relation to sex, body mass, wing length and tarsus length of Chestnut Thrush (n 71) also included as a fixed effect.
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