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Keywords:

  • differential allocation;
  • paternity;
  • Promerops cafer;
  • sexual selection;
  • tail manipulation

Abstract

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

The differential allocation hypothesis predicts that females should invest more in reproduction when paired with attractive males. We measured egg volume in Cape sugarbirds (Promerops cafer), a sexually dimorphic passerine, in relation to paternity of the offspring and in response to an experimental tail length treatment. We manipulated tail length, after pair formation, but before egg laying: males had their tails either shortened or left unmanipulated. Our manipulation was designed to affect female allocation in a particular breeding attempt rather than long-term mate choice: males with shortened tails would appear to be signalling at a lower level than they should given their quality. We found that egg volume was smaller in the nests of males with experimentally shortened tails but larger when the offspring were the result of extra-pair matings. Both these findings are consistent with the differential allocation hypothesis. We suggest that tail length may be used by females as a cue for mate quality, eliciting reduced female investment when breeding with social mates; and with males with shortened tails.


Introduction

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

Females are expected to invest differentially in reproduction depending on the attractiveness of their mates: they should allocate more resources to offspring sired by attractive males, as such offspring are more likely to survive and breed, than offspring sired by less attractive males. This differential allocation hypothesis (Burley, 1986; Sheldon, 2000) has recently been modelled formally by Harris & Uller (2009), who found that the hypothesis applies when females mate with high quality mates, but that when mating with low quality mates, increased female investment was predicted only in cases where parental investment had a relatively low impact on offspring quality. In addition, they found that condition, the probability of achieving further matings, and the expected future prediction of male quality should all affect the pattern of female investment in relation to male quality.

Evidence consistent with the differential allocation hypothesis has been found in several studies of birds (De Lope & Møller, 1993; Petrie & Williams, 1993; Møller & de Lope, 1995; Cunningham & Russell, 2000; Kolm, 2001; Limbourg et al., 2004; Bonato et al., 2009). In contrast, other work has found either no relationship between male attractiveness and female investment (Sanz, 2001; Smiseth et al., 2001; Mazuc et al., 2003; Michl et al., 2005), or even, in one case, a negative relationship (Griffith et al., 1999). In birds, differential allocation can be detected unequivocally only at the egg stage, as patterns of offspring care can be the result of both differential allocation by the female and compensatory care by the female for poor male care (Wright & Cuthill, 1989; Witte, 1995). Offspring behaviour is an additional complication: maternal effects primarily serve the parent’s interests in cases in which offspring control provisioning, whereas when parents control provisioning the reverse is true – maternal effects primarily serve the interests of the offspring (Hinde et al., 2010).

In monogamous birds with biparental care, females sometimes choose males on the basis of display traits such as long tails (e.g. Andersson, 1982; Evans & Hatchwell, 1992; Møller, 1988), bright colours (e.g. Badyaev & Hill, 2002; Pryke et al., 2002), song (e.g. Hasselquist et al., 1996; Forstmeier & Leisler, 2004; Reid et al., 2004) and mechanical sound (e.g. Prum, 1998). These traits may signal the benefits, either direct or indirect, that a female would obtain by mating with a given male. Direct benefits might include contributions to offspring rearing, in the form of territory defence and/or provisioning (Heywood, 1989; Hill, 1991; Buchanan & Catchpole, 2000). Indirect benefits include heritable traits promoting offspring survival and reproductive success (Andersson, 1994; Borgia et al., 2004). However, males signalling high quality in terms of indirect benefits may not be the best providers of direct benefits (Buchanan & Catchpole, 2000; Qvarnström, 1997; Sanz, 2001; but see Senar et al., 2002), perhaps because of trade-offs with costly ornamentation (Balmford et al., 1993; Kokko, 1998; Olson & Owens, 1998; Buchanan et al., 2001). A female selecting a mate may be trading off direct benefits against indirect benefits and would have to consider her own condition when deciding on the appropriate trade-off (Badyaev & Hill, 2002). In birds, the results of the balance between direct and indirect benefits and overall parental provisioning can be reflected in measurable variables such as clutch size and volume, offspring growth rate and fledging mass.

We examined patterns of investment, at the egg stage, in Cape sugarbirds (Promerops cafer), passerines endemic to the fynbos biome of South Africa (Fry et al., 2000). Tail length is extremely sexually dimorphic: males have graduated tails up to 380 mm long, whereas female tails are around 160 mm long (body mass of both sexes c. 37 g) (Cheke et al., 2001). They are socially monogamous and territorial (Cheke et al., 2001). Females are responsible for nest construction and incubation of the clutch, which consists of two eggs, but males contribute to offspring provisioning, although typically at a lower rate than females (Broekhuysen, 1959). Male tail length is likely to have a signal function and be under sexual selection as it shows high between individual variability (coefficient of variation 21.7%: Grégoire et al., 2007), and female Cape sugarbirds appear to favour long-tailed males as extra-pair mates (McFarlane et al., 2010). If tail length signals heritable benefits in males, one would predict that long-tailed males should provide greater indirect benefits than short-tailed males (although they may be unable to provision at a high rate as they are handicapped by the possession of a long tail ornament; or unwilling to do so as seeking extra-pair mates is a more optimal strategy). Therefore, we would predict that experimental shortening of male tail length would lead females to reduce their investment in offspring as the apparent quality of their mate has been reduced.

In this paper, we test the hypothesis that male tail length influences the volume of eggs laid by their pair female using a manipulation experiment where male tail length was reduced after social mate choice but prior to breeding. Reducing male tail length should reduce male quality, as perceived by the female. If females are allocating resources differentially, based on perceived male quality, then females would be predicted to allocate fewer resources to their offspring if the tail length of their social mate is reduced, resulting in smaller eggs.

Methods

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

Cape sugarbirds were studied in Swartboskloof, Jonkershoek Nature Reserve outside Stellenbosch, South Africa (33°60′S18°58′E), during the breeding seasons of 2004 and 2005 (February–August). The vegetation is classified as mountain fynbos (Fraser, 1989). The study site is dominated by Protea nerifolia, with some Protea nitida and Protea repens, and indigenous riparian forest patches.

Adults were captured using mist nets throughout the study period under license from the Western Cape Nature Conservation Board (permit no. 177/2003). Each individual was provided with a numbered aluminium leg ring and three plastic colour rings, producing a colour permutation unique to each bird. We measured right and left tarsus, bill length and head plus bill length to the nearest 0.1 mm using callipers. Right and left wing length (flattened chord), palette width and right and left central tail feathers were measured to the nearest millimetre using metal rulers (Svensson, 1992; Grégoire et al., 2007). Right and left measurements were averaged to give a single measure of each trait. Males which were paired socially with a female, but had not started breeding, were alternately assigned to one of two treatment groups –control, where the bird was handled and measured, and manipulated, where the bird was handled, measured and 65 mm was cut from the six central tail feathers (one standard deviation of male tail length, calculated from 34 males with fully grown tails captured in 2003). The cut tips were shaped to resemble the natural tail tip. Sham controls (cut and re-glued) and elongations were not conducted because of the difficulties in creating a join, which was robust enough to last the entire 5–6 month breeding season. The manipulation was conducted after social mate choice but before breeding commenced, to manipulate sexual rather than social mate choice, following McFarlane et al. (2010).

Nests were located by observing adult behaviour. The identity of the putative parents was noted through observations of territorial behaviour and nest construction. Eggs were photographed using a Fujifilm Finepix 6900 zoom digital camera (Fujifilm Global, Tokyo, Japan) on a background of 1 mm squared paper. Egg length and width were measured using SigmaScan Pro 5 (SPSS, Chicago, IL, USA), then volume was calculated using the formula 0.515 × length × (width)2 (Hoyt, 1979). This method reduced both the time spent at the nest and egg handling by the observer compared to taking physical measurements of each egg. Hatching date was converted to a code standardized for the two seasons i.e. day one was 7 April, and the earliest date of hatching was 11 April.

Data analysis

Adult morphological variables were significantly intercorrelated (Pearson correlation matrix P < 0.05). Principal components analysis (PCA) was therefore carried out using spss v13 (SPSS, Chicago, IL, USA) in order to eliminate the correlated terms, replacing them with orthogonal variables (Cuthill et al., 1999). Separate analyses were conducted for males and females. Tail length and palette width were excluded, as these features vary between seasons and also to investigate the effects of these ornamental traits on reproductive investment. Two principal components were extracted, explaining 78.8% of the variation in the data in males and 83.1% in females. These factors were difficult to explain in biological terms, therefore a varimax rotation (Quinn & Keough, 2002) was applied to clarify their structure (Table 1 in McFarlane et al., 2010). Egg volume was log10 transformed prior to analysis.

A linear mixed-effects model was constructed using residual maximum likelihood (REML) in R (2008), using egg volume as the dependent variable, and year and male as random terms to control for pseudoreplication. Independent terms were factors one and two from the PCA, hatch date, male palette width, natural tail length; tail treatment and the interaction between these last two terms (representing tail length at laying), and a final term relating to the number of extra-pair chicks in the clutch: none, one, or two. With the exception of hatch date, which was retained in all models as breeding season in Cape sugarbirds lasts for 6 months, and we expected females to lay larger eggs as the season progressed as future mating opportunities declined (Harris & Uller, 2009), stepwise backward selection was employed: nonsignificant terms were dropped sequentially until a fully significant model was obtained.

Results

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

Fifty-five nests were found in 2004, 44 of which provided egg volume data. Fifty-two nests were found in 2005, 37 of which provided egg volume data. Several pairs in each year produced two broods, while a few produced three. All nests which were found before hatching contained two eggs.

PCA

In males, factor one was most closely related to head plus bill, bill and tarsus length (skeletal body size), and factor two referred mainly to wing length (a feather-based measure of body size). In females, factor one also reflected skeletal body size but excluded tarsus length, whereas factor two referred to wing and tarsus length (both skeletal and feather-based body size) (McFarlane et al., 2010).

Experimental manipulation

Treatment significantly reduced tail length (independent samples T-test: 2004 and 2005 combined T = 2.714, d.f. = 32, P = 0.005). The two groups did not differ in any of the traits we measured prior to treatment (independent T-tests, 2004 and 2005 combined: factor one: T = 0.424, d.f. = 32, P = 0.674, factor two: T = 0.0278, d.f. = 32, P = 0.978, tail length: T = −0.555, d.f. = 32, P = 0.583, palette width: T = −0.503, d.f. = 32, P = 0.618). Although we assigned equal numbers of males to the control and experimental groups in each season, only 56% (45 of 81) of broods yielded nestlings old enough to take blood samples, on account of predation and chicks dying of exposure. In three broods, paternity could not be unambiguously assigned (see McFarlane et al., 2010), leaving 42 broods for analysis. Of the social males providing care for these broods, in 2004, 11 males were assigned to the control group and 7 to the treatment group. In 2005, nine were controls and three were manipulated.

Egg volume

Two factors had a negative effect on egg volume: experimental shortening of tail length (t = −2.20, d.f. = 35, P = 0.035, Fig. 1); and the number of chicks sired by the social male (t = 3.03, d.f. = 35, P = 0.005, Fig. 1). The interaction between natural tail length and treatment (in other words, tail length at the point of mating) was also significant (t = 2.25, d.f. = 35, P = 0.030), which means that the effect of natural tail length on egg volume was dependent on whether the male’s tail had or had not been manipulated. This appears to be because of the fact that in broods in which the social male was unmanipulated, egg volume declined with tail length significantly more than when the social male’s tail length had been reduced.

image

Figure 1.  Cape sugarbird (Promerops cafer) egg volume in relation to experimental shortening of male tail length; and whether at least one chick in each brood of two chicks resulted from extra-pair copulation. Mean egg volumes (standard errors indicated) are fitted values derived from a linear mixed-effects model using residual maximum likelihood (see text for details).

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Discussion

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

Female Cape sugarbirds decrease their investment in egg volume in response to a reduction in male tail length: both experimental treatment alone (Fig. 1); and the interaction between treatment and natural tail length (i.e. the tail length of the social male prior to manipulation) explain significant variation in egg volume. In addition, female Cape sugarbirds increase egg volume when they secure extra-pair matings (Fig. 1), which is consistent with our earlier finding that females prefer long-tailed males for extra-pair copulations (McFarlane et al., 2010). These results support the differential allocation hypothesis (Burley, 1988): with females investing more in their eggs when paired with more attractive males. But interestingly, despite the predictions of Harris & Uller (2009), the opportunity for future matings that season (as reflected by the variable ‘hatching date’) appeared to have no effect on egg volume. Differential allocation in egg volume has been shown in both mallards (Anas platyrhynchos) (Cunningham & Russell, 2000) and ostriches Struthio camelus (Bonato et al., 2009): females laid larger (and heavier) eggs when paired with attractive males. In contrast, egg size, clutch size and yolk volume were unaffected by male badge size in house sparrows (Passer domesticus) (Mazuc et al., 2003). To our knowledge, ours is the first experimental study showing that egg volume is adjusted in response to manipulation of a male trait.

The fact that eggs are smaller when both are within pair suggests that females lay larger eggs for extra-pair males which they are choosing to sire their chicks. This result is consistent with differential allocation. A previous study of Cape sugarbirds has shown that long-tailed males appear to focus on extra-pair copulations, whereas short-tailed males concentrate on mate guarding: both naturally short-tailed males and experimentally shortened males have a reduced probability of being cuckolded compared to long-tailed males (McFarlane et al., 2010). Whether it is females which somehow appear to escape the attention of their social males and find extra-pair mates, or males which abandon their social females in favour of seeking extra-pair copulations, is worthy of further detailed study. The fact that egg volume in control broods declined with tail length irrespective of whether the brood contained extra-pair young or not is consistent with an earlier finding that tail length had an negative effect on within-pair paternity, the effect of which was reduced when tail length was shortened (McFarlane et al., 2010). In broods in which the tail of the social male had been shortened, egg volume actually increased with tail length in broods containing only within pair chicks, but declined in those containing at least one extra-pair chick.

Although females use tail length as a measure of male attractiveness (McFarlane et al., 2010) and adjust their investment accordingly, an alternative explanation of our results could be that direct benefits could be more important than indirect ones, with females using male tail length as a direct predictor of male provisioning rate. Cape sugarbirds do not display courtship feeding, so egg investment could not be directly affected by this behaviour. But a recent study by Russell et al. (2007) showed that female superb fairy-wrens (Malurus cyaneus) reduced their investment in eggs when nesting in the presence of helpers relative to nesting without helpers. When controlling for egg volume, it was shown that chick mass was significantly increased in the presence of helpers (Russell et al., 2007). This suggests that females reduce their investment when high provisioning rates are likely. Female Cape sugarbirds may use male tail length as a predictor of provisioning rate, with long-tailed males being expected to provision less than short-tailed males (Balmford et al., 1993; Sanz, 2001). Females could then reduce their investment in eggs when male tail length is reduced, to save their own resources for future reproduction.

The role of egg volume on offspring growth and survival is difficult to quantify and variable among species. Mean egg mass was positively related to mean nestling mass in starlings (Smith & Bruun, 1998). In common (Sterna hirundo) and roseate (Sterna dougallii) terns, Nisbet (1978) showed that chicks from large eggs survived better than those from small ones, although chicks from small eggs grew faster in common terns. In roseate terns, chicks from large eggs grew faster after they were 4 days old. Egg volume was also a positive predictor of chick survival in herring gulls (Larus argentatus) (Parsons, 1970) and thin-billed prions, Pachyptila belcheri (Silva et al., 2007). Cape sugarbirds disperse at the end of the breeding season, and offspring are not highly philopatric. We were therefore unable to relate egg volume to survival beyond the nestling stage. In addition, starvation was extremely rare during the nestling stage in our study population (i.e. present in < 5% of broods), so if there are any detectable effects of egg volume and growth rate on survival, they most likely occur after fledging.

In summary, we have tested the differential allocation hypothesis in Cape sugarbirds by experimentally manipulating male tail length prior to egg laying. Females differentially allocate resources to their eggs in relation to male tail treatment, as egg size was reduced in the nests of males with shortened tails; and increased in nests with extra-pair offspring. This is the first experimental study showing that egg volume is adjusted in response to manipulation of a male trait.

Acknowledgments

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

Thanks to Rene Gaigher, Hanneline Smit and Mike Thorsen for field assistance. Bruno Faivre, Arnaud Grégoire, Marina Préault and Brent Sinclair are thanked for statistical advice, useful discussions and assistance in the field; and Thais Martins for making helpful comments on the manuscript. Birds were captured under permit no. 177/2003 from Cape Nature, who also allowed us to work in Jonkershoek. MLM was supported by a Leverhulme Study Abroad Studentship, and running costs were funded through a grant to MIC from Stellenbosch University. Ethical clearance for this work was granted by the Stellenbosch University research committee.

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  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
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