ethology Ethology Mark C. Mainwaring*, David Lucy & Ian R. Hartley*

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1 international journal of behavioural biology ethology Ethology Hatching Asynchrony Decreases the Magnitude of Parental Care in Domesticated Zebra Finches: Empirical Support for the Peak Load Reduction Hypothesis Mark C. Mainwaring*, David Lucy & Ian R. Hartley* * Lancaster Environment Centre, Lancaster University, Lancaster, UK Department of Mathematics and Statistics, Lancaster University, Lancaster, UK Correspondence Mark C. Mainwaring, Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK. m.mainwaring@lancaster.ac.uk Received: February 2, 2014 Initial acceptance: February 3, 2014 Final acceptance: February 10, 2014 (T. Tregenza) doi: /eth Keywords: hatching asynchrony, parental care, offspring begging Abstract Parent offspring conflict over the supply of parental care results in offspring attempting to exert control using begging behaviours and parents attempting to exert control by manipulating brood sizes and hatching patterns. The peak load reduction hypothesis proposes that parents can exert control via hatching asynchrony, as the level of competition amongst siblings is determined by their age differences and not by their growth rates. Theoretically, this benefits the parents by reducing both the peak load of the offspring s demand and their overall demand for food and benefits the offspring by reducing the amplification of their competition. However, the peak load reduction hypothesis has only received mixed support. Here, we describe an experiment where we manipulated the hatching patterns of domesticated zebra finch Taeniopygia guttata broods and quantified patterns of nestling begging and parental feeding effort. There was no difference in the begging intensity of nestlings raised in asynchronous or experimentally synchronous broods, yet parental feeding effort was lower when provisioning asynchronous broods and particularly so when levels of nestling begging were low. Further, both parents acted in unison, as there was no evidence of parentally biased favouritism in relation to hatching pattern. Therefore, our study provided empirical support for the prediction that hatching asynchrony reduces the feeding effort of parents, thereby providing empirical support for the peak load reduction hypothesis. Introduction Hatching asynchrony, whereby offspring from a single reproductive event either hatch or are born asynchronously over an extended period of time, is a taxonomically widespread phenomenon. The causes and consequences of asynchronous hatching have largely been studied in birds (reviews in Magrath 1990; Stoleson & Beissinger 1995), yet offspring either hatch or are born asynchronously in taxa as diverse as reptiles (While et al. 2007; While & Wapstra 2009), insects (Smiseth & Morgan 2009), amphibians (Ryan & Plague 2004) and sharks (Gilmore 1993). Despite being ubiquitous across a range of taxa, the evolution of hatching asynchrony remains controversial as it results in size asymmetries amongst offspring that appear to be maladaptive as they often result in the reduced survival and/or condition of later hatched and smaller offspring (Stoleson & Beissinger 1995; Glassey & Forbes 2002a,b). However, given that parental incubation behaviours appear to determine the level of hatching asynchrony, at least within avian broods (Magrath 1990; Ricklefs 2002; Gilby et al. 2013), then hatching patterns should be an optimal strategy for parents. Further, hatching asynchrony is predicted to simultaneously benefit offspring as it reduces the extent of sibling competition, and specifically, the begging intensity of broods (Hahn 1981). Nevertheless, despite a considerable amount of empirical research seeking to explain the evolution of Ethology 120 (2014) Blackwell Verlag GmbH 577

2 Hatching Asynchrony and Parental Care M. C. Mainwaring, D. Lucy & I. R. Hartley hatching asynchrony (Magrath 1990; Stoleson & Beissinger 1995), there remains little consensus regarding the adaptive benefits. Many hypotheses have been proposed to explain the evolution of hatching asynchrony (Magrath 1990; Stoleson & Beissinger 1995). One of them, the peak load reduction hypothesis, suggests that parents can benefit from hatching asynchrony as it reduces the peak load of care that they provide to their offspring (Hussell 1972). Further, as hatching asynchrony results in offspring competitiveness being determined by the subsequent age hierarchies, and not by individual solicitation behaviours or growth rates, then hatching asynchrony can lead to a reduction in the overall demand for food (Hahn 1981; Ricklefs 2002). However, a theoretical model by Mock and Schwagmeyer (1990) provided only negligible support for the peak load reduction hypothesis as it showed that any energy savings for parents due to hatching asynchrony would be minimal, except in species with very large clutch sizes and extreme cases of asynchrony. This view was supported by an empirical study of European bee-eaters Merops apiaster which showed that the benefits accrued by parents through asynchronous hatching were negligible (Lessells & Avery 1989). Further, a study of burying beetles Nicrophorus vespilloides found that hatching asynchrony reduced the peak level of offspring demand, but as there were no differences in parental provisioning behaviours between asynchronous and synchronous broods (Smiseth & Morgan 2009), then this was interpreted to provide no empirical support for the peak load reduction hypothesis. However, other empirical studies of birds have provided support for the peak load reduction hypothesis by reporting that experimentally synchronous broods begged or competed harder for food than asynchronous broods (Fujioka 1985; Vi~nuela 1999; Cook et al. 2000; Gilby et al. 2011a). For example, the total demand of house martin Delichon urbica broods was reduced by 7 8% through asynchronous hatching (Bryant & Gardiner 1979), and hatching asynchrony reduced the energy expenditure of parents by reducing the duration, but not the magnitude, of the peak load of offspring demand within green-rumped parrotlet Forpus passerinus broods (Siegel et al. 1999). Consequently, empirical support for the peak load reduction hypothesis is mixed. Parents may control the level and distribution of parental care through provisioning rules, yet the evolutionary interests of one parent may not match the interests of the other parent (Clutton-Brock 1991). Each parent will prefer the other to invest more than they do themselves (Trivers 1974), which may result in differences in how the two parents allocate the same form of parental care to individual offspring. Such parentally biased favouritism occurs when the two parents deviate from one another by preferentially feeding offspring in relation to their size, begging behaviours or other attributes (Lessells 1998, 2002a,b). As hatching asynchrony is controlled by the onset of incubation, then the sex that incubates will have better control over the subsequent hatching regime than the other parent (Slagsvold & Lifjeld 1989). It is possible, therefore, that hatching asynchrony may play a role in sexual conflict as well as in parent offspring conflict (Forbes 1993), especially where the parents differ in their response to begging from offspring of different sizes. Several studies of birds report that late hatched nestlings within asynchronously hatched broods are preferentially fed by females (Stamps 1990; Leonard & Horn 1996; Krebs et al. 1999; Dickens & Hartley 2007; Wiebe & Slagsvold 2009) and males (Westneat et al. 1995; but see Shiao et al. 2009). Meanwhile, whilst female canaries Serinus canaria paid decreasing attention to the begging behaviours of growing nestlings, the males responsiveness remained constant (Kilner 2002a). In this study, we aim to further our understanding of the evolution of hatching asynchrony by empirically testing the peak load reduction hypothesis. We simultaneously controlled brood sizes and manipulated hatching patterns in domesticated zebra finches Taeniopygia guttata and having previously shown that nestling begging intensity did not differ between asynchronous and synchronous broods (Mainwaring et al. 2011); here, we quantified patterns of parental feeding effort. Our study replicates another study on wild zebra finches which found that nestlings in asynchronous broods begged less intensely than nestlings in experimentally synchronous broods, which led to parents providing less food in total to asynchronous broods (Gilby et al. 2011a). Consequently, by replicating that study in domesticated zebra finches, we have the opportunity to provide an intraspecific comparison of the peak load reduction hypothesis in zebra finches. Domesticated zebra finches lay one egg per day and begin incubation as soon as the first egg is laid, so that broods hatch asynchronously over approximately 5 d (Skagen 1988; Gilby et al. 2013). Zebra finch parents respond passively to sibling competition within broods for food, and so early hatched nestlings receive a greater share of the food (Gilby et al. 2011b; Mainwaring et al. 2011) and are larger throughout the nestling period (Zann 1996; Mainwaring et al. 2010, 2012). In this study, we test the 578 Ethology 120 (2014) Blackwell Verlag GmbH

3 M. C. Mainwaring, D. Lucy & I. R. Hartley Hatching Asynchrony and Parental Care following two predictions of the peak load reduction hypothesis: first, that parental feeding effort will be higher in experimentally synchronous than in asynchronous broods (Stoleson & Beissinger 1997); and second, that parentally biased favouritism will lead to male and female parents differing in their provisioning towards asynchronous and synchronous broods. Materials and Methods General Methods and Manipulation of Hatching Synchrony A population of domesticated zebra finches was maintained at Lancaster University in a temperature controlled room at approximately 20 C, under full spectrum, artificial light (Bennett et al. 1996) on a 16 8 light dark regime. All of the birds were ringed and, before breeding, were housed in one of two single-sex aviaries where the other aviary was visible, although no physical contact was possible. Birds were randomly chosen for breeding and were, for an introductory period of 7 d, placed into breeding cages ( cm) with another bird of the same sex and given a diet of ad libitum rearing food (Nectarblend Rearing Softfood; Haiths Ltd., Cleethorpes, UK) and seed. Individual breeding females were then placed into one half of a partitioned breeding cage ( cm), and a randomly selected, unrelated male was placed into the other half of the breeding cage, but behind an opaque partition, which meant that the birds were visually isolated (Mainwaring et al. 2012). Then, following a period of 7 d, the partitions were removed and the breeding pairs were kept in these breeding cages throughout the course of the experiment. Each pair had access to a nestbox (15 cm 3 ) that was externally attached to the breeding cage. Breeding pairs were provided daily with ad libitum seed, cuttlebone, grit and drinking water and provided weekly with vitamin supplements, charcoal and bathing water. Pairs were randomly assigned to either the asynchronous (n = 16) or synchronous (n = 12) hatching regime. Nestboxes were checked each morning, when fresh eggs were individually numbered with a non-toxic indelible marker pen. In broods assigned to the synchronous treatment, eggs were removed on the day that they were laid and replaced with an artificial egg, and then, all of the eggs in the clutch were returned on the day following clutch completion, to establish hatching synchrony. The eggs were placed in small bowls, which were lined with tissue, to replicate the conditions that they would have experienced within the nest as closely as possible, and all of the eggs were turned daily to prevent the yolk from settling. The hatching success of eggs was high (94.5%), and the manipulation of hatching patterns had no effect on the hatching success of eggs (Mainwaring et al. 2011). Further, there were no differences in the changes in body condition, as indicated by a composite index of mass in relation to head-bill length, of either males or females between pairing and clutch completion in either asynchronous or synchronous treatments (Mainwaring et al. 2011). All of the synchronous broods hatched within a 24-h interval, and the variation in hatching mass within broods was never >0.5 grams. In all nests, brood sizes were maintained at four, either by the addition of extra foster nestlings from other broods or through fostering nestlings to other broods as necessary (Mainwaring et al. 2010, 2012; Mainwaring & Hartley 2013). The presence of unrelated foster nestlings within broods has the potential to introduce bias as they increase the begging intensity of broods (Boncoraglio & Saino 2008), but we are confident that bias was not introduced into our study as only four nestlings (of a total of 112) were fostered into broods and were distributed evenly with respect to treatment. Note that the extra foster nestlings hatched from corresponding eggs so that, for example, a last hatched nestling was replaced with a last hatched nestling (Mainwaring et al. 2012). All pairs were encouraged to breed twice and therefore raise one asynchronous and one synchronous brood (Mainwaring et al. 2012), but whilst many pairs included in this study achieved this aim, some did not and bred only once. Quantifying Parental Care and Nestling Begging Behaviours Patterns of parental care and nestling begging were quantified using video cameras recording through a hole in the back of each nestbox, which was covered when not filming. Birds were familiarised with the camera and tripod over a 24-h period before recording (Royle et al. 2006), and the nests were all filmed for 3 h, in the mornings, beginning between 0900 and Videos were recorded when nestlings were 8 13 d old and not either side of this period because parents usually stood over their nestlings whilst feeding at a younger age, which obscured them from view, and after this period due to the risk of premature fledging (Royle et al. 2006; Mainwaring et al. 2011). Nestlings were weighed immediately prior to filming, and there were no differences in the mean mass of Ethology 120 (2014) Blackwell Verlag GmbH 579

4 Hatching Asynchrony and Parental Care M. C. Mainwaring, D. Lucy & I. R. Hartley nestlings in asynchronous and synchronous broods, although nestling masses were more variable in asynchronous broods (Mainwaring et al. 2011). All of the parental feeding visits and associated nestling begging activities recorded during the 3 h of filming were included in this study. Prior to filming, all nestlings were individually marked with white correction fluid on their head, which remained visible for the full duration of the videos and meant that the nestlings were individually identifiable throughout. Zebra finches regurgitate food for their nestlings several times during each feeding visit (Royle et al. 2006; Mainwaring et al. 2011), and for each feeding visit, the following data were recorded, which nestling received the feed, the duration of the regurgitated feed and the maximum begging intensity score of each nestling. Parents were scored as having fed a nestling when they inserted their bill into the nestling s gaping mouth, and they could be seen regurgitating, with characteristic heaves of their bodies. Regurgitate duration (feed load size) was measured frame by frame (accurate to 0.04 s), from the point at which parents inserted their bill until it was withdrawn from the nestling s mouth. Nestling begging intensity was scored on a four point scale (Kilner 1995; Royle et al. 2006) as follows: 0: no begging; 1: mouth open and slight movements of the tongue; 2: mouth open, more regular tongue movements and rolling of the head and neck; 3: mouth open, rapid tongue movements, exaggerated head rolling and body squirming (following Royle et al. 2006; Mainwaring et al. 2011). Statistical Analyses In this study, we expand on a previous study (Mainwaring et al. 2011) and use the same dataset to examine patterns of parental care. Models were fitted with the lm (R Development Core Team 2012) and the lme4 (Bates et al. 2008) packages. The total time spent feeding the nestlings at each parental feeding visit was considered to be a response to the total begging intensity of all nestlings within a nest, with potential covariates being the brood hatching pattern (asynchronous or synchronous) and the sex of the feeding parent (male or female). Logarithmic transformation to remove negative skew was employed for both feeding time and begging intensity. The total feed time for each parental feeding visit was considered a continuous response, and the models were fitted using hatching pattern, begging intensity and parent sex as fixed effects. Random effects allowed the models to account for repeated measures for related data, and parental pair was fitted as a random term in all of the models. The Akaike information criterion (AIC) was employed as the main criterion for model selection (Burnham & Anderson 2002), and a significance level of a = 0.05 was adopted throughout. All tests are 2-tailed. Results Model 2 showed that parental feeding effort was lower at asynchronous broods than at experimentally synchronous broods, although the absolute differences in effort were very small (Table 1; Fig. 1). We then tested for evidence of parentally biased favouritism by including parent sex as a fixed effect. Model 9 examines parental feed time in relation to begging intensity, hatching pattern and their interaction term, whereas model 10 includes parent sex as a fixed effect and model 11 includes parent sex and the interaction term between parental sex and hatching pattern as fixed effects (Table 1). Models 9, 10 and 11 were not significantly different from each other. However, model 9 had the lower AIC value and was the more parsimonious, meaning that the inclusion of a parent sex term made no difference to the total feeding time per visit (Table 1). Further, the interaction term between parent sex and hatching pattern was not significant, meaning that both parents provisioned the nestlings in both asynchronous and synchronous broods in a consistent way (Table 1). A visual inspection of the residuals from model 9 suggested that nest-specific random effects might be usefully used to improve the models. Therefore, parental pair, nestling identity, nestling weight, and the interaction between nestling weight and parental pair were all fitted as nested random terms into models 13 and 14. Note that nestling weight was nested within nestling identity, both of which were nested within parental pair, and those three effects were nested within the interaction between nestling weight and parental pair. The inclusion of the random gradients term in model 14 did not significantly improve the fit and so model 13 is considered the optimum model for these particular observations (Table 1). The significant interaction term in model 13 (Fig. 2) indicates that the rate of increase in parental feeding effort with begging intensity differed with hatching pattern. In synchronous broods, parental feeding effort did not vary in relation to begging intensity, whereas in asynchronous broods, higher levels of begging intensity resulted in higher levels of parental feeding effort. 580 Ethology 120 (2014) Blackwell Verlag GmbH

5 M. C. Mainwaring, D. Lucy & I. R. Hartley Hatching Asynchrony and Parental Care Table 1: Summary of linear mixed models examining parental feed time in relation to hatching pattern, parental sex and nestling begging intensity. The fixed and nest-specific random terms of those models selected as the best fit are shown and all terms in the models are significant at a = Note that logarithmic transformation to remove negative skew was employed for both feeding time and begging intensity. Note also in the explanatory terms, we used Wilkinson Rogers modelling notation, with 1 indicating an intercept term Model Response Effect Estimate Standard deviation F value p value AIC 1 Feed time ~ Feed time ~ Hatching pattern Feed time ~ Parent sex (male) Feed time ~ Begging intensity < Feed time ~ Hatching pattern Parent sex (male) Feed time ~ Begging intensity < Hatching pattern < Feed time ~ Begging intensity < Parent sex (male) Feed time ~ Begging intensity < Hatching pattern < Parent sex (male) Feed time ~ Begging intensity < Hatching pattern < Begging intensity: hatching pattern Feed time ~ Begging intensity < Hatching pattern < Parent sex (male) Begging intensity: hatching pattern Feed time ~ Begging intensity < Hatching pattern < Parent sex (male) Begging intensity: hatching pattern Begging intensity: parent sex (male) Feed time ~ Begging intensity < Begging intensity: hatching pattern Feed time ~ Begging intensity < Hatching pattern Begging intensity: hatching pattern (1 nest) (random effect) (r 2 ) 14 Feed time ~ Begging intensity < Hatching pattern Begging intensity: hatching pattern (1 nest) (random effect) (r 2 ) (0 + begging intensity nest) (random effect) < (r 2 ) Ethology 120 (2014) Blackwell Verlag GmbH 581

6 Hatching Asynchrony and Parental Care M. C. Mainwaring, D. Lucy & I. R. Hartley 150 total feed time per nestling synchronous hatching pattern asynchronous Fig. 1: The total feed time (seconds) per nestling per parental feeding visit in experimentally synchronous and asynchronous broods. Note that three outlying values, defined as being outside 1.5 times the interquartile range above the upper quartiles, from nestlings within one asynchronous brood are omitted from the figure. total feed time per visit (seconds) synchronous asynchronous total begging per visit Fig. 2: Scatter plot showing the relationship between the summed begging intensity of nestlings in asynchronous and synchronous broods per feeding visit and the summed feed time for the corresponding feeding visit. Each point represents an individual parental feeding visit and is the sum of all the begging intensity in the nest per parental feeding visit and the sum of all the feeding time per parental feeding visit. The two lines are geometric representations of the difference in the relationship between asynchronous and synchronous broods. See methods for full details. Discussion The main finding of this study was that parental feeding effort was significantly lower for parents provisioning asynchronously hatched broods, and particularly, so when levels of nestling begging intensity were low. In this study, we have presented data relating to overall provisioning feeding effort, and whilst it may have be preferable to examine the peak level of parental feeding effort, we found that an appropriate measure of maximal provisioning effort was difficult to quantify. Nevertheless, this supports our first hypothesis, which predicted that parental feeding effort would be lower when provisioning asynchronous broods. Further, this means that our study provides empirical support for the peak load reduction hypothesis (Mock & Ploger 1987; Stoleson & Beissinger 1997), thereby adding to previous empirical studies that show that asynchronous hatching reduces parental workloads (Bryant & Gardiner 1979; Fujioka 1985; Siegel et al. 1999; Vi~nuela 1999; Cook et al. 2000; Gilby et al. 2011a). However, it is important to remember that other studies have found that hatching asynchrony either does not alter parental feeding effort or actually increases it (Lessells & Avery 1989; Smiseth & Morgan 2009). Parents provisioning asynchronously hatched broods benefitted through a reduction in the level of care they provided, yet it may also be expected that the advantages of hatching asynchrony were accrued by the nestlings as well, through increased levels of growth (Stoleson & Beissinger 1995, 1997). However, the mean mass of nestlings at pre-fledging did not differ with respect to hatching pattern (Mainwaring et al. 2012). This means that whilst hatching asynchrony reduced parental workloads, there were no apparent benefits accrued by the nestlings in asynchronous broods through increased growth. Having also shown that the begging intensity of nestlings did not differ between the two hatching patterns (Mainwaring et al. 2011), then our study also provides no support for the sibling rivalry reduction hypothesis. 582 Ethology 120 (2014) Blackwell Verlag GmbH

7 M. C. Mainwaring, D. Lucy & I. R. Hartley Hatching Asynchrony and Parental Care That hypothesis predicts that hatching asynchrony reduces the extent of sibling competition and, in particular, the begging intensity of broods (Hahn 1981; Glassey & Forbes 2002a,b; Kilner 2002b). Our results contradict our second hypothesis, which predicted that parentally biased favouritism would occur with respect to hatching pattern. We found that both parents acted in unison, which is contrary to general expectations as theoretical models suggest that parentally biased favouritism towards different types of offspring is the universally predicted outcome of evolutionary conflict of interest (Lessells 1998, 2002a,b). Furthermore, previous empirical studies of birds have demonstrated that parentally biased favouritism occurs with respect to offspring size, with smaller nestlings being preferentially provisioned by female (Stamps 1990; Leonard & Horn 1996, 1998; Krebs et al. 1999; Dickens & Hartley 2007; Wiebe & Slagsvold 2009) and male parents (Westneat et al. 1995; but see Shiao et al. 2009). However, when interpreting the findings of our study, it is important to remember that we studied domesticated zebra finches that were provided with ad libitum quantities of food and lived in a predatorfree environment. Consequently, the level of conflict between the parents and their offspring may have been less than when food was scarce. It is therefore interesting to note that our findings generally supported the results presented in a similar experiment involving wild zebra finches (Gilby et al. 2011a). That study showed reduced levels of both nestling begging and parental feeding effort in asynchronously hatched broods. Therefore, whilst both studies showed that hatching asynchrony resulted in reduced parental workloads, only nestlings in the wild showed reduced levels of begging activity. The disparity between that study and our own study suggests that whilst hatching asynchrony is adaptive for both domesticated and wild zebra finch parents, it has no apparent, or fewer, advantages for domesticated nestlings. The reduced levels of begging intensity within wild asynchronous broods may have occurred for two reasons. First, parental feeding visits to wild broods are much less frequent than visits to domesticated broods and food is likely to be in shorter supply in the wild, meaning that the nestlings may not have the energy for excessive begging activities (Parker et al. 2002). Second, the nestlings in wild broods were begging in an environment where predators may well hear them, meaning that selection may have acted against loud and excessive begging behaviours (Gilby et al. 2011a). Either way, the differences between domesticated and wild broods are interesting, yet it is probably not surprising that the domestication process has influenced the time budgets and life-history decisions of zebra finches. Our results also have broader implications for our understanding of the evolution of hatching asynchrony in birds. We have shown that parents derive benefits through hatching asynchrony, which should be expected within avian broods at least, as parents determine the extent of hatching asynchrony by initiating incubation prior to laying the last egg within clutches (Magrath 1990). Therefore, whilst our study adds support to those studies that have found support for the peak load reduction hypothesis (Bryant & Gardiner 1979; Fujioka 1985; Siegel et al. 1999; Gilby et al. 2011a), it is prudent to consider that other studies have found no apparent support for the peak load reduction hypothesis (Lessells & Avery 1989; Smiseth & Morgan 2009). This implies that the benefits accrued by parents and/or offspring through hatching asynchrony may vary both between and within species. Illustratively, our study involving domesticated zebra finches contrasts with the results of a similar experiment involving wild zebra finches (Gilby et al. 2011a), thereby suggesting that food availability or the risk of predation may influence family dynamics and the benefits of hatching asynchrony at the intraspecific level (Mainwaring & Hartley 2013). 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