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Keywords:

  • asynchrony;
  • sex allocation;
  • sex-specific growth;
  • sexual size dimorphism;
  • sibling competition

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. Studies of sex allocation in birds have traditionally centred on Fisher's (1930) theory of equal parental investment in male and female offspring. They concentrate particularly on sexually dimorphic species, where costs of rearing offspring are assumed to vary between male and female young because of body size differences.

2. Higher mortality of the larger sex (males), particularly in poorer conditions, is expected to result in female-biased sex ratios in the great tit, Parus major. Several studies have found the contrary, reporting male-biased fledging and recruiting sex ratios when conditions are poor. One reason why this may be the case is that males can gain more food resources than their sisters because of the competitive advantage afforded by their larger size. They may thus suffer less mortality in the nest or fledge in better condition, thereby enhancing their survival prospects.

3. This study investigates the importance of size in competitive interactions between nestlings of different sexes. A cross-fostering design was employed to create broods of mixed size through swapping half a brood of 2-day-old ‘small’ and half a brood of 4-day-old ‘large’ nestlings. Nestling morphometrics and mortality were measured during the nestling period. Nestlings were sexed by PCR amplification of sex-linked genes. To test for a male advantage in competitive environments, size and mortality measures were compared between ‘small’ males and females, and ‘large’ males and females (i.e. the interaction term ‘size treatment’ and ‘sex’).

4. There was greater sexual dimorphism between small nestlings than large nestlings at fledging. This is interpreted as revealing enhanced competitive ability of male offspring under stressful conditions. Offspring from the ‘large’ group suffered lower mortality, but there was no difference in mortality according to sex, and no significant size*sex interaction. Similarly, no difference in recruitment was found, although this may be due to the small overall proportion of birds recruiting (3·1%).

5. The study suggests that male biased fledging/recruitment sex ratios in great tits may be explained by enhanced competitive ability of male nestlings in poor rearing environments.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

In sexually dimorphic animals, two non-exclusive hypotheses have been proposed to explain sex ratio biases towards the smaller sex at the end of the period of parental care. First, natural selection for equal allocation to male and female offspring will result in biased sex ratios when the cost of rearing each sex differs (as expected for dimorphic species; Fisher 1930). Secondly, sexual selection for larger size of one sex in adulthood may necessitate larger size of that sex during the period of parental investment. Consequent non-adaptive mortality of the larger sex due to higher energy demands which cannot be met by parents then results in sex-biased mortality (Clutton-Brock, Albon, & Guinness 1985). Both processes may result in the over-production of the smaller sex via the same mechanism, namely increased mortality of the larger sex.

Studies of altricial birds have tested for sex ratio biases in dimorphic species, considering both of the above theories as possible causes of sex ratio biases (e.g. Weatherhead & Teather 1991). However, although a few have documented sex ratio biases towards the smaller sex in stressful rearing conditions (Howe 1977; Cronmiller & Thompson 1981; Røskoft & Slagsvold 1985), most found no deviation from unity in sex ratios despite considerable sexual dimorphism of the study species (Selander 1960; Richter 1983; Weatherhead 1983; for reviews see Newton 1979; Clutton-Brock 1986). As it seems reasonable to expect that offspring size dimorphism results in different rearing costs of males and females, or unequal nutritional requirements, the mismatch of empirical results with theoretical predictions points to other processes in the nest counter-balancing sex-biased starvation. The greater size of one sex may enable it to reach higher towards the parent, occupy favoured feeding positions or push smaller nest-mates away from food deliveries. Through such competitive advantages, larger offspring may be able to gain additional food they require for growth and maintenance.

I investigate the importance of size and sex in competitive chick interactions in a large-brooded, synchronously hatching (within 2 days) species, the great tit Parus major, where competition for food is likely to be especially intense. Mean clutch size is 9·1 eggs (± 1·16, n = 273), and nestlings are provisioned for 17–22 days, with an average of 5·9 fledglings (± 3·2, n = 96) produced per nest. In this population, adult great tits exhibit 7% sexual dimorphism in mass and 3·5–4% skeletal size dimorphism (tarsus and wing lengths, males > females), with size differences statistically apparent amongst nestlings from 5 days of age (this study). Males are expected to have higher nutritional requirements for maintenance and growth, and thus female-biased sex ratios are predicted if these requirements cannot be met. Studies measuring energetic requirements of sexually size-dimorphic blackbirds (Icteridae) have shown that in these species males (larger) do, indeed, have higher energy demands than females (Fiala & Congdon 1983; Teather & Weatherhead 1988). Similarly, greater energetic demands of the larger sex (females) have been directly measured in marsh harriers (Riedstra, Dijkstra & Daan 1998). In great tits, contrary to the expectation that under poor rearing conditions males perform relatively worse then their sisters, several studies have demonstrated male-biased sex ratios amongst nestlings reared in poor environments. Dhondt (1970) found that both in areas and periods unfavourable for nesting great tits significantly more males fledged. In a brood size manipulation experiment, Smith, Kallander & Nilsson (1989) found proportionally more males surviving from enlarged than reduced broods. Lessells, Mateman & Visser (1996) found that the proportion of males hatching in a clutch increases with laying date (later hatching broods are less successful and are expected to experience less food abundance). Furthermore, they found more males recruiting from nests with higher nestling mortality. An earlier study of the same population of tits similarly found a male-biased sex ratio amongst fledglings when nestling mortality was higher (Drent 1984).

These studies demonstrate a biased sex ratio contrary to that predicted by theory and no study, to my knowledge, has reported the reverse pattern in great tits. Even if there is no difference in the cost of rearing male and female nestling great tits, as a recent study suggests (Lessells, Oddie & Mateman 1998), we would expect to observe neither a male nor female biased sex ratio. I suggest that the observed male biases are due to the enhanced competitive ability of males due to their larger size. Using a cross-fostering experimental design to establish an obvious size difference within a brood, growth and survival of different sized nestlings of different sexes was investigated. By comparing nestling growth between ‘small’ males and females competing with ‘large’ males and females in the same nest, I test whether males indeed fare better than their sisters in conditions of extreme sibling competition.

Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Cross-fostering manipulation

Nest-box breeding great tits on the Swedish island of Gotland (57°10′N, 18°20′E) were experimentally manipulated for this study in 1997 and 1998. Nest-boxes were monitored for nest establishment and egg-laying, and daily nest-box checks allowed exact hatching dates to be determined. Following hatching, a small amount of blood (1–5 µL) was collected from the brachial vein of each chick on day 1 (day of first egg hatching = day 0) for sex determination using PCR-based molecular techniques (Griffiths, Double, Orr & Dawson 1998). Blood was stored in 50 µL SET buffer at − 20°C (1997) or 98% alcohol (1998). Individual nestlings were matched to their blood samples by a unique identification code created by selective clipping of one or two of their six down tracts.

The size of nestlings within a brood was experimentally manipulated by moving chicks of different ages between nests. Nests with similar brood size (same or ± 1 nestling) at hatching were paired for cross-fostering generally when nestlings in one nest were 2 days old and in the other 4 days old. Half of the ‘large’ brood was then swapped with half of the ‘small’ brood, creating two nests each with half ‘large’ and half ‘small’ nestlings (see Fig. 1.) Sex of nestlings was not known at the time of swap, but the large brood size (mean = 8·33 at time of cross-fostering) in this species meant that in the majority of cases nestlings of both sexes would be present in each group. Chicks were selected for swapping on the basis of which down tract was clipped; for each manipulation I selected nestlings for moving starting with the next consecutive letter code to the last swap in order to randomise which nestlings were relocated. Brood sizes did not change except in two pairs of nests where brood size increased or decreased by one nestling in each nest. In total, 42 pairs of nests were created (17 in 1997 and 25 in 1998).

image

Figure 1. Representation of cross-fostering design to create broods (n = 84) of mixed size Parus major nestlings. Typically half a brood of 4-day-old nestlings were swapped with half a brood of 2-day-old nestlings. Sex of nestling was not known at swap, rather the proportion of one sex moved was determined by chance.

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Of importance when swapping was the size difference between nestlings, rather than age per se. Therefore, in six of the 42 pairs, nestlings of 3 and 5 days were swapped (especially at the beginning of the season when nestlings grew slowly) or 3- with 4-day-olds, etc. Nests with hatching asynchrony of more than 1 day were not used. In this population eggs sometimes hatch 1 or 2 days after the first hatching date. Size manipulations thus reflected possible natural variation in sibling size and competitive situations which may be naturally encountered by last-hatching nestlings. If it was obvious that the size difference between nestlings was too extreme for smaller nestlings to survive, the swap was not carried out. As all nestlings were bled on day 1, nestlings were not bled and transported on the same day.

Morphometric measures

The following morphological measurements were recorded at the time of cross-fostering: mass (using 10-g pesola spring balance accurate to 0·1 g), tarsus and gape length (using dial callipers to nearest 0·5 mm). Gape length measures from one end of the mouth crease to the point of the bill and increases with nestling age as the bill develops. Measures were repeated 5 days after experimental manipulation (n = 80, i.e. nestlings aged 7 and 9 days), 10 days after manipulation (n = 39, i.e. nestlings aged 12 and 14 days), and 12 days after manipulation (n = 72, nestlings aged 14 and 16 days). Nestling mass of great tits on day 15 after hatching is generally the same as that at fledging (Schifferli 1972; van Balen 1973), and the last set of measurements were taken to reflect condition at fledging. Originally, measurements were taken 10 days following manipulation, but it was soon recognized that nestlings could be safely measured 2 days later without causing premature fledging. Because of time constraints, nestling measures at day 12 were prioritized, explaining the small sample size for day 10 measures. Other sample sizes less than 84 represent whole brood failures or predation. On days 10 and 12 post-manipulation, wing development was substantial enough that wing length was additionally measured to the nearest 0·5 mm. Nestlings were banded with aluminium rings, matching down clipping identification marks to ring number. Where nestlings were not aged 2 and 4 days when swapped, measures were not always taken 5, 10 or 12 days after swapping, but on days when nestlings were 7/9, 12/14 or 14/16-day-old (or as near as possible).

After fledging, boxes were checked for individuals failing to fledge. Birds recruiting to this population in 1998 and 1999 were recorded by catching pairs breeding in any of the ∼1000 nestboxes in the surrounding woodlands using either nest-box traps or mist-nets. Between 170 and 240 pairs of great tits breed annually in the nest-boxes on Gotland. In 1998, 72·1 and 76·9% of all breeding males and females were caught, respectively, and in 1999, 83·5% males and 85·3% females were caught. Although it is possible that recruiting individuals may breed in natural holes, as well as nestboxes, there is no reason to believe why nestlings of either sex from either experimental category should preferentially nest in natural cavities. Thus, I expect no sampling bias in recruits from each treatment due to recruitment of individuals outside nestboxes, which could not be measured.

Sex identification

Nestling sex was determined by PCR amplification of two CHD genes located on the sex chromosomes. Two copies of the gene are present in females (CHD1W, present on the W chromosome and CHD1Z, present on the Z chromosome), whereas only one copy (CHD1Z) is present in homogametic males. After DNA extraction from blood samples (5% chelex extraction) these sex-specific fragments of the CHD gene were amplified using primers P2/P8 and PCR conditions as described in Griffiths et al. (1998). Products were run on 6% polyacrylamide gel and visualized using silver staining (Promega). I lacked samples for 25/699 (3·6%) nestlings and failed to determine sex in a further two (0·3%) cases. From 54 blood samples of adults (28 males, 26 females) and 20 recruits (12 males, eight females) where I determined phenotypic sex in the field, genetic sex determined by molecular methods matched in all 74 cases.

Data analysis

Comparison of male and female sizes (mass, tarsus length, wing length, gape length) among both small and large nestlings were made using paired t-tests of sib-group means. Analyses were carried out to look for effects of nestling sex and size (‘large’ vs. ‘small’ nestlings, according to box of origin) on survival and morphological measures. To determine whether there was a different effect of being large or small for each sex of individual on growth, the interaction term size*sex was entered in a general linear model with morphological measurements (tarsus, mass, gape length, wing) as dependent variables and size and sex as factors. The unit of analysis was each nestling, but because nestlings are reared non-independently in a common environment, box of rearing was included as a factor in the model to control for differences between nests due to parental/territory quality and year. Because sizes of nestlings at swapping would influence subsequent measures, initial mass and tarsus measures were included as covariates. Timing of breeding was found to have a significant effect on growth measures and this variation was removed from the model by including clutch initiation date as a covariate. Analyses were carried out separately for each set of chick measures (on days 5, 10 and 12 following manipulation) using procedure manova in the statistical package JMP Statistical Discovery Software Version 3·1.

Logistic regression was used to assess whether survival of nestlings to day 5, 10 and 12 following brood manipulation was a function of their sex, size and the interaction of the two. The same analysis was used to examine effects of an individual's size and sex on survival to fledging. From 75 nests (excluding four predated nests and five total nest failures, total number of nestlings = 633), 79% of nestlings fledged. As survival differs greatly between nest-boxes, the environmental factor ‘box of rearing’ was added to the model as a random effect. Likelihood ratio tests were used to determine the significance of a variable, entering variables ‘sex’, ‘size’, “size*sex' and ‘box of rearing’ in the model simultaneously. Since controlling for timing of breeding (lay date) and cross-fostering had no effect on the outcome of tests, these variables were not included in results presented here in order to keep the model as simple as possible. The number of birds recruiting from experimental nests in 1998 and 1999 in relation to their size and sex was analysed similarly.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The 699 nestlings involved in the study fell into the following categories: 161 small males, 175 small females, 156 large males and 182 large females (25 unsexed).

Nestling growth

Development of sexual dimorphism

For all measurements post-cross-fostering where sexual dimorphism was detected, males were larger than females (Tables 1a and 1b). At the time of manipulation, there was no difference in any size measure between small (2-day-old) male and female nestlings. Amongst small nestlings, by day 5 post-manipulation, males had larger tarsi (t= − 2·06, d.f. = 46, P = 0·045). By day 10 post-manipulation sexual differences in tarsus length remained (t= − 3·61, d.f. = 20, P = 0·002) and a difference in body mass was also apparent (t= − 2·23, d.f. = 20, P = 0·038). Wing length was marginally non-significantly different in males and females (t= − 2·02, d.f. = 20, P = 0·057). Near fledging (12 days post- manipulation) male nestlings were larger than females for all measures (mass: t= − 3·29, d.f. = 35, P = 0·002; tarsus: t= − 5·77, d.f. = 35, P = 0·000; gape length: t= − 2·32, d.f. = 35, P = 0·026; wing length: t= − 2·20, d.f. = 35, P = 0·034).

Table 1.  (a) and (b) Size dimorphism (%) between male and female great tit nestlings following cross-fostering manipulation of half a brood of small nestlings with half a brood of large nestlings. Values for small nestlings in Table 1a, large nestlings in Table 1b. Both nestlings which were moved and those which stayed in their natal nest are included. Positive values indicate males larger than females, negative values females larger than males (*  P < 0·05, **  P < 0·01, ***  P < 0·001; for statistical tests see text). Sample sizes on day 0 deviate from the original 84 manipulated nests because not every nest was composed of nestlings from each category. Sample sizes on days 5, 10 and 12 differ as nestlings died, leaving some categories empty, and because not all nests were visited on each measurement day to record nestling sizes (see Methods: morphometric measures)(a) Small nestlings: (b) Large nestlings
Day post- manipulationAge n Mass Tarsus lengthGape (days)Wing
0265− 0·10− 0·10− 0·72 
5747+ 6·04+ 2·60*− 0·25 
101221+ 8·03*+ 5·78**+ 0·01+ 4·15
121436+ 5·80**+ 3·69***+ 0·92*+ 2·66*
Day post- manipulationAge n Mass Tarsus length Gape (days)Wing
0469− 1·32− 1·33− 2·28** 
5964+ 3·82*+ 1·14− 0·77 
101428+ 4·00***+ 2·24***+ 0·04+ 1·82
121656+ 4·64***+ 2·19***+ 0·44+ 1·50

Amongst large nestlings, females had longer gapes than males at swap (4-day-old; t= 2·93, d.f. = 68, P = 0·005), but other measures did not differ (mass: t= 0·58, d.f. = 68, P = 0·561, tarsus: t= 1·17, d.f. = 68, P = 0·248). By day 5 after manipulation, males were heavier (t= − 2·6, d.f. = 63, P = 0·012) than females and gape length differences were no longer apparent. The sex-specific mass difference remained 10 days post-manipulation (t= − 4·39, d.f. = 27, P = 0·000) when males also had longer tarsi (t= − 4·56, d.f. = 27, P = 0·000). There was non-significant tendency for males to have longer wings than females at this time (t= − 1·87, d.f. = 27, P = 0·072). Near fledging males were heavier (t= − 5·54, d.f. = 55, P = 0·000) and had longer tarsi (t= − 5·53, d.f. = 55, P = 0·000). There was still a tendency for males to have longer wings than females, but this was not statistically significant (t= − 1·91, d.f. = 55, P = 0·061), and there was no apparent sexual size dimorphism in gape length (t= − 1·28, d.f. = 55, P = 0·206).

Comparison of size differences in large and small nestlings

In order to compare sexual size differences between large and small nestlings, the interaction term of the effects ‘size category’ and ‘sex’ was determined in a multiple analysis of variance of nestling measures. After 5 days of growth with size-manipulated nest-mates, the size difference between males and females was the same amongst small nestlings as that for large nestlings (size*sex, F1,432 = 1·505, P = 0·221). However, 12 days following manipulation, there was a significant difference between the sexual dimorphism amongst the large nestlings compared to the small nestlings (size*sex, F1,354 = 5·434, P = 0·020). Ten days following manipulation the size*sex term was marginally non-significant (F1,354 = 2·822, P = 0·095), perhaps due to smaller sample sizes. The significant effect on day 12 post-manipulation was mainly due to an effect on wing length (dropping wing length from analysis: size*sex, F1,354 = 3·586, P = 0·059). Significance remained when any other dependent variables were removed from the model (mass: F1,354 = 5·900, P = 0·016, tarsus: F1,354 = 5·085, P = 0·025, gape length: F1,354 = 5·018, P = 0·026).

Nestling measures both 10 and 12 days following manipulation reveal a greater sexual size difference amongst small nestlings compared to the size difference in large nestlings. Amongst small nestlings, females are smaller than males to a greater degree than amongst large nestlings (Fig. 2).

image

Figure 2. Size differences between male and female great tit nestlings in cross-fostered groups of ‘small’ and ‘large’ offspring, 12 days following experimental manipulation. Small nestlings are thus typically 14-day-old, large nestlings 16-day-old. Graphs illustrate mean nestling (a) mass (g) (b) tarsus length (mm) (c) gape length (mm) and (d) wing length (mm) with standard errors.

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Nestling mortality

Parental and/or territory quality was a strong influence on nestling survival, with nest of rearing a significant effect on survival of nestlings to all ages. The size category of nestlings ‘large’ or ‘small’ was also a predictor of survival, with larger nestlings clearly suffering less mortality (Table 2). Nestling survival was not affected by nestling sex, and there was no different effect of nestling sex among large and small young (non-significant size*sex interaction; Table 2).

Table 2.  Proportion of great tit nestlings dying and predictors of survival. Logistic regression relating nestling mortality to nestling size and sex and size * sex interaction, following brood composition manipulation (see Methods). Original number of nestlings in each treatment group in nests without total nest failure/predation: large males 143, large females 169, small males 156, small females 165
Time post-manipulationProportion of nestlings dyingnPredictors of nestling survivald.f.Likelihood ratio χ2P (>χ2)
5 daysLarge 312Nest of rearing73184.04<0.001
 Males0.0913Size150.006<0.001
 Females0.0712Sex10.4120.52
Small 321Size*Sex10.4150.70
 Males0.2945   
 Females0.2745   
10 daysLarge 312Nest of rearing73190.30<0.001
 Males0.0913Size160.581<0.001
 Females0.0712Sex10.4620.50
Small 321Size*Sex10.0730.79
 Males0.3250   
 Females0.2948   
12 daysLarge 312Nest of rearing73208.32<0.001
 Males0.1014Size156.271<0.001
 Females0.1018Sex10.1080.74
Small 321Size*Sex10.1770.67
 Males0.3453   
 Females0.3456  
FledgingLarge 312Nest of rearing73201.63<0.001
 Males0.1014Size161.012<0.001
 Females0.1118Sex10.0370.85
Small 321Size*Sex11.0160.31
 Males0.3555  
 Females0.3456   

Recruitment

Twenty birds recruited to the breeding population (3·1%), 15 from 1997 and five from 1998. The size category of a nestling in the experimental manipulation did not affect its chances of recruiting (χ2 = 0·00, P = 0·99, d.f. = 1), nor did any morphological measure at fledging predict recruitment probability (mass: χ2 = 2·250, P = 0·134, d.f. = 1; tarsus: χ2 = 2·642, P = 0·104, d.f. = 1; wing: χ2 = 0·627, P = 0·429, d.f. = 1; gape length: χ2 = 1·143, P = 0·285, d.f. = 1). Body condition, measured as residual mass at fledging for a given body size (tarsus length) was almost a significant predictor of nestling recruitment (χ2 = 3·038, P = 0·081, d.f. = 1). Comparing the masses of individuals recruiting to those not, recruiting nestlings had higher mean absolute body weights (recruits: 17·28 ± 0·40 g; non-recruits 16·94 ± 0·08 g) and higher weights relative to body size (recruits: 0·50 ± 0·29 g; non-recruits: − 0·02 ± 0·06 g), although these differences are not statistically significant (day 12 mass: F1,444 = 0·688, P = 0·407, residual day 12 mass: F1,444 = 3·008, P = 0·083). The recruits consisted of 12 males and eight females; this difference was not statistically significant (χ2 = 1·322, P = 0·245, d.f. = 1). Finally, the interaction effect size*sex on recruitment was not significant (χ2 = 0·020, P = 0·881, d.f. = 1).

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

For a species where males are larger than females, one would expect a female sex ratio bias at the end of the period of investment, assuming the smaller sex to be less costly to rear (Fisher 1930; Maynard-Smith 1980). Several studies of great tits have reported the opposite (Dhondt 1970; Drent 1984; Smith et al. 1989; Lessells et al. 1996) and this study highlights the importance of size dominance of larger offspring which could account for this observed discrepancy. In experimentally manipulated broods of great tits comprising half ‘large’ and half ‘small’ nestlings, sexual size dimorphism was less marked for large individuals than for small individuals. When competition for food is relaxed, i.e. amongst large nestlings, males and females attain more similar growth measures than when competition is pronounced (small nestlings). The advantage of ‘being male’– attaining higher weights and larger biometric sizes than sisters – is particularly important for small nestlings who face an extremely competitive nest environment. Larger individuals may be more successful at obtaining food by reaching closer to parents when begging, pushing smaller competitors away from access to parents, and occupying preferred feeding positions in the nest (Rydén & Bengtsson 1980; Bengtsson & Rydén 1983; Kolliker et al. 1998).

The idea that females are at a competitive disadvantage with larger nest mates is supported by the sexual size differences observed between nestlings (Tables 1a and 1b). By fledging, small males and females differed significantly in every dimension measured (mass, tarsus length, wing length, gape length), but amongst large nestlings only in mass and tarsus length. Moreover, the degree of dimorphism is greater amongst small nestlings. Small females must compete with three classes of nestling, all larger than themselves: large males, large females and small males. Large females, on the other hand, must compete only with one class of nestling larger than themselves (large males).

It could be argued that size treatment in this experiment is confounded with age and that sexual size dimorphism initially increases to a certain nestling age, but then declines. In this way, it would be possible to generate the observed results of size dimorphism more apparent amongst smaller nestlings simply as a function of their age. However, it is biologically unlikely that sexual size differences would develop and then diminish, and the significant size*sex interaction recorded 12 days post-manipulation was also detected 10 days post-manipulation, although not statistically significant. Size dimorphism could initially increase then decrease if males were to reach their asymptotic size before females. However, in a review of sexually size dimorphic species, Richner (1991) found no evidence for this, but that there is no difference between time for each sex to reach its asymptote or the smaller sex reaches asymptotic body mass quicker.

The effect reported here of males faring better than their sisters is opposite to that expected from a simple nutritional dependence. It is also contrary to studies of sexually dimorphic mammals demonstrating higher mortality of the larger sex (Clutton-Brock et al. 1985; Clutton-Brock 1991). Studies revealing sex-biased mortality of sexually dimorphic mammals typically deal with organisms with a litter size of one (ungulates, primates, man), where there is no sibling competition. In multiparous, sexually size dimorphic organisms, sibling competition may represent a considerable influence on the sex ratio at the end of the period of care.

It is possible that hormonal differences between the sexes, their effects on behaviour (e.g. increased aggression) and immune responses of nestlings could account for male dominance in the feeding arena, rather than size as I have argued. The experimental design allows the effect of size to be teased apart from the effect of sex and other traits which co-vary with sex such as hormonal levels. If sex-specific hormone levels alone were responsible for increased male growth we would expect the same sexual dimorphism to be equally apparent in small and large nestlings. However, this study reveals that that size per se, and not other traits specific to sex, is an important determinant of offspring growth.

There is one possible explanation for depressed growth in small females which cannot, however, be excluded on the basis of this study. In birds, females are the heterogametic sex, and environmentally dependent expression of deleterious recessive alleles on the unguarded W chromosome could result in decreased female performance. However, investigations of sex-specific growth combined with brood size manipulations in the sexually monomorphic collared flycatcher, Ficedula albicollis, provide no evidence for this phenomenon in birds (Sheldon et al. 1998).

Although this study demonstrates that both size and sex of offspring affect fledging measures, the results showed nestling mortality to be a function of size category only and not predicted by nestling sex. Increased mortality amongst small nestlings was not surprising given that they had to compete with half a brood of considerably larger sibs. In naturally hatching clutches, the longest interval between hatching of the first and last egg is commonly 2 days, in one case 4 (personal observation; also true for other great tit populations). In nests with such extreme hatching asynchrony, it is usual that most eggs hatch on day 0 and only one, or two at most, hatch up to 2 days later. Often these last-hatched nestlings die within a day or two, unable to compete with such large sibs. In such asynchronously hatching nests, this mortality could be interpreted as an adaptive parental strategy to increase chances of survival in remaining offspring (e.g. Lack 1954). Although in great tits synchronous broods produce slightly more (but not significantly so) offspring, fledglings from asynchronous broods are heavier (see Amundsen & Slagsvold 1998). Given the discrepancy in competitive ability of male and female offspring, non-random allocation of sex between eggs may present a mechanism by which female birds could exert some control in breeding decisions, according to environmental conditions at time of rearing (see Slagsvold, Husby & Sandvik 1992). For example, if male nestlings are at a competitive advantage, females on high quality territories may produce larger broods by laying and hatching ‘male eggs’ last; females on low quality territories could follow a bet-hedging strategy more likely to result in brood reduction by laying ‘female eggs’ last. While there are numerous studies reporting associations between laying or hatching order, and the sex ratio (e.g. Ankney 1982; Cooke & Harmsen 1983; Ryder 1983; Weatherhead 1985; Bortolotti 1986; Clotfelter 1996; Dzus, Bortolotti & Gerrard 1996; Kilner 1998), at present there is no clear understanding of what explains such patterns.

In this study, the unequal competition experienced in the nest can be interpreted as a sublethal fitness effect, resulting in nestlings of unequal quality. Increased size and mass at fledging has often been found to have important fitness consequences for great tits. Mass of fledglings correlates positively with post-fledging survival in several great tit populations (Perrins 1965; Dhondt 1971; Garnett 1981; Tinbergen & Boerlijst 1990; however, see Lindén, Gustafsson & Pärt 1992) and a previous study (Verboven & Visser 1998) found fledglings of higher mass to have higher recruitment probability. Skeletally larger individuals at fledging may be able to monopolize parental feeds outside the nest cavity and obtain higher dominance rank in hierarchical winter flocks (see Hinde 1952; Garnett 1981). Kluijver (1957) found female great tits to be subdominant to males in competition for food and roosting places. Larger body size at fledging could therefore promote mass gain in large individuals, in turn enhancing overwinter survival prospects.

The reproductive value of offspring (Williams 1966) is a more important measure of offspring fitness than overwinter survival and therefore it is more critical to consider offspring recruitment to the breeding population. It would seem reasonable to assume that the positive relationship between fledging mass and survival demonstrated for tits would result in greater recruitment probability of heavier nestlings. Indeed, Verboven & Visser (1998) demonstrated such a relationship in two different populations of great tits. Although the present study found no significant effect of fledging mass or size on recruitment, the trend was in the expected direction, but tests lacked power due to small numbers of birds recruiting (only 20 nestlings from 635; cf. Verboven & Visser 1998). Individuals which recruited weighed more than non-recruits in both absolute terms and relative to body size, although differences were not statistically significant (see Results). There was no evidence of sex-biased recruitment based on these small samples.

Thus, although no effects of nestling size and sex on mortality and recruitment were detected in this study, it is possible that the significant size differences observed at fledging could have important consequences for these two fitness parameters. This result is consistent with the explanation that a size advantage of male nestling great tits can account for observations of male-biased sex ratios. All previous reports of unbalanced sex ratios in great tits have recorded male-biased fledging and recruitment sex ratios when young were reared in poor environments (Dhondt 1970; Drent 1984; Smith et al. 1989; Lessells et al. 1996). Similarly, Heeb et al. (1999) found a greater proportion of male nestlings recruiting from experimentally flea-infested broods. These observed male-biased ratios could even be enhanced by parents altering sex ratio themselves to account for lower fitness values of daughters in some conditions. If this indeed occurs, it could amplify the sex bias effects recorded in unmanipulated brood studies (Dhondt 1970; Drent 1984; Lessells et al. 1996). Regardless, the present study points to competition as an important selective force in the nest affecting quality of males and females raised. It cannot offer a proximate explanation for correlations involving hatching sex ratios (e.g. Lessells et al. 1996), but may offer an explanation for the evolution of such patterns.

Fisher's (1930) theory of equal parental investment in the sexes has been the motivation for most avian studies of sex-specific growth and mortality. Most of these studies have concentrated on the differential cost to parents of rearing offspring to fledging, searching for adaptive explanations for biased sex ratios. Less attention has been paid to proximate explanations for biased fledging/recruitment sex ratios (although see Schifferli 1980; Teather 1992). Such mechanistic explanations of sex biases at fledging may be important, and not in conflict with ultimate explanations. This and previous studies of great tits highlight the importance of considering both approaches in sex ratio studies. Although natural selection is the ultimate cause of sex ratios biases, constraints due to an organism's life-history (i.e. sexual size dimorphism driven by sexual selection) should not be ignored. Recent molecular technology allowing sexing of young birds should facilitate further studies of sex-allocation and sex-biased parental care. However, the outstanding problem in avian sex allocation studies remains that of quantifying fitness returns of sons vs. daughters, and even in delimiting the period of parental care.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

This work was carried out under Swedish ringing license no. 576 with NERC funding. The author would like to thank local land-owners of Burgsvik, field-workers on Gotland for help with routine field-work and Michele Incagli for particular help with this experiment. Thanks are due to Simon Griffith and Richard Griffiths for laboratory advice, and Ben Sheldon and Loeske Kruuk for comments on the manuscript.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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Received 15 November 1999;revisionreceived 13 March 2000