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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2010 Mar 10;277(1690):2083–2088. doi: 10.1098/rspb.2010.0109

An immunological cost of begging in house sparrow nestlings

Gregorio Moreno-Rueda 1,*,†
PMCID: PMC2880102  PMID: 20219741

Abstract

Parent–offspring conflict predicts that offspring should demand a greater parental investment than is optimal for their parents to deliver. This would escalate the level of offspring demand ad infinitum, but most of the models on the evolution of parent–offspring communication predict that begging must be costly, such costs limiting the escalation and defining an optimal level of begging. However, empirical evidence on this issue is mixed. A potential begging cost that remains to be accurately explored is a decrease in immunocompetence for offspring begging fiercely. This study experimentally analyses this cost in house sparrow (Passer domesticus) nestlings. A group of nestlings was forced to beg fiercely for a prolonged time while a control group begged at low levels, both groups receiving the same quantity of food. At the same time, the nestling response to an antigen (phytohaemagglutinin) was measured. Nestlings forced to beg fiercely showed a reduction in immunocompetence with respect to control chicks, but the two groups showed no difference in growth rate. The largest and the smallest nestlings in each brood showed a similar response to the treatment. These results strongly suggest a trade-off between begging and immunocompetence in this species. This trade-off may be a consequence either of resources from the immune system being reallocated to begging behaviour, or of adaptive immunosuppression in order to avoid oxidative stress. Steroid hormones are proposed as mediators of such a trade-off.

Keywords: growth costs, honest signalling, parent–offspring conflict, sibling competition, trade-offs

1. Introduction

The parent–offspring conflict determines that, given the genetic differences between siblings, and between parents and their offspring, each offspring will demand a greater parental investment than is optimal for their parents to deliver, elevating the level of offspring begging signals in species with parent–offspring communication (Trivers 1974; Lazarus & Inglis 1986; Clutton-Brock 1991; Mock & Parker 1997). This conflict may be resolved if offspring begging is costly, and thus there would be an optimal begging level for each offspring (according to its state) in which costs balance benefits (reviewed in Kilner & Johnstone 1997; Mock & Parker 1997; Godfray & Johnstone 2000; Johnstone & Godfray 2002; Harper & Maynard Smith 2003; Wells 2003). Such costs are therefore necessary for the stability of begging, according to these models, independent of whether begging is used in the honest communication of need or in sibling competition (Royle et al. 2002).

However, empirical evidence for the existence of begging costs is mixed (Roulin 2001; Wright & Leonard 2002; Moreno-Rueda 2007). It has been proposed that begging signals, by attracting predators, may increase the risk of predation, which would limit begging escalation; but evidence for such a cost is unclear (Haskell 2002; Moreno-Rueda 2007). Given that begging usually implies conspicuous movements and loud calls (e.g. Redondo & Castro 1992), it is assumed to be energetically costly. However, estimations of the energetic expenditure have proved difficult to interpret (Moreno-Rueda 2007). A trade-off between begging and growth has been shown in two bird species (canary, Serinus canaria, Kilner 2001; magpie, Pica pica, Rodríguez-Gironés et al. 2001). These studies suggest that energy allotted to begging is diverted from energy allocated for growth, implying fitness consequences, given that size at fledging frequently influences survival in birds (Ringsby et al. 1998; Schwagmeyer & Mock 2008). However, no growth cost associated with begging has been found in three other bird species (house sparrow, Passer domesticus, Kedar et al. 2000; ring dove, Streptopelia risoria, Rodríguez-Gironés et al. 2001; tree swallow, Tachicyneta bicolor, Leonard et al. 2003), nor in a burying beetle (Nicrophorus vespilloides, Smiseth & Parker 2008).

Such inconsistencies in results have led some researchers to suggest that the physiological costs of begging are relatively low (Chappell & Bachman 2002; Wells 2003; Searcy & Nowicki 2005), and the aforementioned models therefore lack support. Later models predicted relatively cheap begging (Bergstrom & Lachmann 1997, 1998), but cheap begging is probably uninformative with respect to offspring need (Brilot & Johnstone 2002). To ascertain the cost of begging is a central pillar in order to identify which models most accurately describe the resolution of the parent–offspring conflict. At this point, to claim that begging cost is relatively low is premature, as many types of costs have not yet been tested (Moreno-Rueda 2007). In fact, a possible explanation for the contrasting results for the trade-off between begging and growth is that, in some species (such as the house sparrow), resources used in begging may be diverted from resource-demanding functions other than growth.

A good candidate might be the immune system (Roulin 2001; Goodship & Buchanan 2007; Moreno-Rueda 2007; Loiseau et al. 2008; Ros 2008). The immune system is costly (Lochmiller & Deerenberg 2000; Schmid-Hempel 2003; Ardia & Schat 2008), and it has been shown that it may take resources from other costly functions (Sheldon & Verhulst 1996; Norris & Evans 2000; Zuk & Stoehr 2002). In fact, several studies have shown a trade-off between offspring growth and the function of the immune system (Fair et al. 1999; Soler et al. 2003; Brommer 2004; Mauck et al. 2005). Therefore, there could be a three-way trade-off among begging, growth and the immune system, some species re-allocating resources for begging signals from growth while others re-allocate resources from the immune system.

Here, I test whether begging signals entail a cost in the form of lower immunocompetence. Given that less immunocompetent animals have a higher mortality risk (Møller & Saino 2004), there would be an optimal begging level, the marginal benefit of increased begging (more food delivered by parents) being balanced by an increase in mortality risk related to decreased immunocompetence. I empirically test this hypothesis with a species in which a growth cost has been looked for and not demonstrated: the house sparrow (Kedar et al. 2000), using similar methodologies to previous studies (Kilner 2001; Rodríguez-Gironés et al. 2001; Leonard et al. 2003).

2. Material and methods

The study was carried out in 2009 with house sparrow nestlings from 22 pairs breeding in captivity in an outdoor aviary in Moraleda de Zafayona (SE Spain). The birds were supplied with dipteran larvae for feeding the nestlings (Moreno-Rueda & Soler 2002). From each nest, I removed the largest and the smallest nestlings (brood sizes: 2–4, mean = 3 ± 0.87 (s.d.)), when they were 5 days old (0 = hatching), and I placed them in an adjacent laboratory. At least one nestling (alien when brood size was 2) was consistently left in the nest to avoid desertion. In an alternate routine, each brood was assigned to a high-begging (HB) or a low-begging (LB) treatment, the biggest and the smallest chicks in each brood receiving the same treatment. The experimental trials lasted 6 h, beginning at 08.15 (local time, ± 15 min) and ending at about 14.15. Nestlings were then returned to their nests. The experiment had no negative effects on nestlings, and none died during the experiment or the days after. During the experiment, nestlings were maintained at 28–32°C (peripheral temperature) in a cup simulating a nest. Nestlings were weighed with an electronic balance (accuracy of 0.01 g) at the start and the end of the trial, and I estimated the mass gained (MG) during the trial as final mass minus initial mass, as well as relative mass gain as a percentage of initial mass. I fed the nestlings each 30 min with a dipteran larva, the same food as they received in the aviary. The average mass of a larva was 0.087 g, and each nestling received 12 larvae during the trial (i.e. all nestlings were fed with 1.044 g during the complete trial). In this way, all nestlings received the same quantity of food (MI). I also weighed the faeces excreted by the chicks (MF). Mass ingested by the nestlings during the trials (MI, which was constant) could be excreted (MF), used in growth (MG), or expended in other metabolic activities implied in self-maintenance, begging or immune response (MM). Therefore, I estimated the metabolic expenditure as MM = MI − MG − MF (Kilner 2001; Leonard et al. 2003).

In the HB treatment, every 10 min I stimulated begging for 60 s by using three different stimuli: acoustic (a characteristic and standardized whistle), tactile (gently touching their gapes with a forceps) and visual (blocking the light of a lamp). All these stimuli successfully elicited begging in nestlings. Thus, nestlings in the HB treatment begged for a total of 2160 s. Each 30 min, the stimulation coincided with feeding, and then the nestling was fed at the end of the 60 s of begging. In the LB group, nestlings begged only when they were fed, and always for less than 5 s. Nestlings showed no begging in the absence of stimulus. Thus, the LB nestlings begged for a total of less than 90 s during the complete trial. In the aviary, parents visited the nests each 2–6 min (average: 3 min; n = 8 broods 4–6 days old), and therefore nestlings were probably stimulated to beg more frequently than in my HB treatment (10 min). In the aviary, each nestling was fed approximately every 10–40 min (average: 20 min). Therefore, the rhythm at which I fed the nestlings (30 min) was similar to that used by their parents in the aviary. This regularity of stimulation and feeding matches that used in other studies with this species (Grodzinski et al. 2009).

To test the effect of begging on the immune response, immediately before the start of the trials I injected, in the left patagium of the chicks, 0.1 mg of phytohaemagglutinin (PHA-P; Sigma Aldrich, L-8754) diluted in 0.02 ml of isotonic phosphate buffer (following Smits et al. 1999). PHA-P is an innocuous protein that provokes an immune response in birds mediated by T-cells (Kennedy & Nager 2006), although other components of the immune system are also involved in the response (Martin et al. 2006; Tella et al. 2008). Previously, I measured (three times) the patagium thickness with a pressure-sensitive micrometer (Mitutoyo Inc.; accuracy: 0.01 mm). At the end of the experiment (6 h), I again measured the patagium thickness, calculating the T-cell-mediated immune response as the difference between the second and first measurements. Previous studies have shown that 6 h is sufficient time to detect an immune response in the house sparrow (Navarro et al. 2003; Martin et al. 2006). The repeatability of measuring the patagium thickness was 0.98 (n = 8; Bailey & Byrnes 1990).

Therefore, during the trials, all nestlings received the same input of resources, but HB nestlings begged 24 times more than LB nestlings. If there is a three-way trade-off between growth, immune response and begging, the house sparrow nestlings begging more fiercely should decrease their investment in growth, or immune response, or both. However, given that previous studies found no evidence that house sparrow nestling, reduce growth rate in response to increased begging (Kedar et al. 2000), I predict that the trade-off is translated to the immune response, which should be lower in HB nestlings.

In the statistical analyses, the variable ‘immune response’ was log-transformed to follow the requisites of parametric statistics (normality, homoscedasticity; Quinn & Keough 2002). The analyses were performed with a repeated measures analysis for variance (RM-ANOVA). This test was used to analyse the difference in the dependent variables between the smallest and the largest nestlings in a paired way (within-subjects component), as well as the interaction with the treatment, in order to examine whether the effect of the treatment varied with nestling rank. Moreover, in the between-subjects component, the test analysed the effect of the treatment on the dependent variables, considering the brood as a statistical unit, thereby avoiding pseudoreplication (von Ende 2001). In a final analysis I used general linear models (GLM), in which I introduced date, brood size and initial nestling body mass as covariates, given that these factors affect (directly or indirectly) the immune response in the house sparrow (Westneat et al. 2004). In this last analysis, RM-ANOVA was not possible, and the largest and the smallest nestlings were analysed separately.

3. Results

No significant differences appeared in initial body mass between LB (low-begging) and HB (high-begging) nestlings (RM-ANOVA, between-subjects component, F1,20 = 0.10; p = 0.75; table 1). In an initial analysis, as predicted, the higher begging effort expended by HB nestlings depressed their immune response (between-subjects component, F1,20 = 5.87; p = 0.02; table 1). No significant difference was found in the immune response between largest and smallest nestlings (within-subjects component, F1,20 = 3.15; p = 0.09), and the interaction with the treatment was not significant (F1,20 = 1.80; p = 0.20). When the effect of the treatment was analysed separately for the largest and smallest nestlings, the begging level was found to have a significant influence on the immune response in the largest nestlings (ANOVA, F1,21 = 8.04; p = 0.01), but a non-significant influence in the smallest nestlings (F1,21 = 2.77; p = 0.11; table 1). Therefore, there was evidence of a trade-off between begging and immune response in the house sparrow, at least for the largest nestlings.

Table 1.

Means ± standard deviations of the dependent variables used in the study, for largest and smallest nestlings in the high-begging (HB) and low-begging (LB) treatments. Immune response was measured as patagium swelling in response to PHA inoculation. Raw data are shown, although analyses were performed with transformed data when necessary.

largest nestlings
 smallest nestlings
high-begging (n = 11) low-begging (n = 11) high-begging (n = 11) low-begging (n = 11)
immune response (mm) 20.64 ± 12.61 49.30 ± 31.82 21.79 ± 15.45 28.61 ± 10.11
initial body mass (g) 8.80 ± 1.25 8.97 ± 1.11 6.50 ± 0.97 6.61 ± 1.32
mass gain (g) 0.45 ± 0.21 0.36 ± 0.18 0.48 ± 0.22 0.50 ± 0.19
relative mass gain (%) 5.28 ± 3.18 4.21 ± 2.19 7.93 ± 5.22 8.17 ± 3.67
faecal mass (g) 0.32 ± 0.10 0.34 ± 0.08 0.28 ± 0.13 0.22 ± 0.13
estimated metabolic expenditure (g) 0.26 ± 0.15 0.34 ± 0.13 0.26 ± 0.14 0.29 ± 0.13
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Consistent with the findings of Kedar et al. (2000), the treatment had no impact on mass gained in house sparrow nestlings (RM-ANOVA, between-subjects component, F1,20 = 0.18; p = 0.68; table 1). The smallest nestlings tended to gain more mass than largest ones (within-subjects component, F1,20 = 4.03; p = 0.06; table 1), but there was no significant interaction with treatment (F1,20 = 1.63; p = 0.22). Measured as a percentage of initial mass, relative mass gain was also unaffected by the treatment (between-subjects component, F1,20 = 0.10; p = 0.76; table 1) and the interaction with rank was not significant (F1,20 = 1.43; p = 0.25). No effect of the treatment on faeces mass was found (between-subjects component, F1,20 = 0.33; p = 0.57; table 1). The largest nestlings excreted significantly heavier faeces than did the smallest nestlings (within-subjects component, F1,20 = 8.35; p < 0.01; table 1), but there was no interaction with treatment (F1,20 = 1.98; p = 0.18). The estimated metabolic expenditure was not affected by the treatment (between-subjects component, F1,20 = 1.45; p = 0.24), did not vary with nestling rank (within-subjects component, F1,20 = 0.78; p = 0.39; table 1) nor showed a significant interaction (F1,20 = 0.56; p = 0.46).

Finally, given that the immune response is (directly or indirectly) affected by date, brood size and body mass (Westneat et al. 2004), I repeated the models controlling for these variables. For the largest nestlings, the immune response significantly diminished with date, and it remained significantly affected by treatment, so that nestlings begging more fiercely showed a depressed immune response (table 2a). Similar results were found for the smallest nestlings (table 2b). In this case, when controlling for date, the difference in immune response between HB and LB treatments proved significant. When the same model was applied to mass gain, relative mass gain and estimated metabolic expenditure, the effect of the treatment on these variables remained non-significant (see the electronic supplementary material).

Table 2.

Effect of date, brood size, initial body mass and treatment on the strength of immune response in the (a) largest and (b) smallest nestlings.

d.f. F p β s.e.
(a) intercept 1 4.84 0.04
 date 1 4.82 0.04 −0.40 0.18
 body mass 1 2.02 0.17 0.24 0.17
 brood size 1 0.31 0.59 0.11 0.20
 treatment 1 12.01 0.003
 error 17
(b) intercept 1 7.76 0.01
 date 1 7.74 0.01 −0.51 0.18
 body mass 1 1.53 0.23 0.23 0.18
 brood size 1 1.81 0.20 0.28 0.21
 treatment 1 7.98 0.01
 error 17
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4. Discussion

This is the first study showing that offspring begging at high levels undergo depressed immunocompetence when challenged by an antigen (PHA), implying a trade-off between begging signalling and the immune system. At the same time, this study confirms an absence of trade-off, between growth and begging in the house sparrow, as previously reported by Kedar et al. (2000). Therefore, a cost of nestling begging is a reduction of their immune capacity, which may jeopardize their resistance to infections and their survival (Møller & Saino 2004).

Immune response is energetically costly (Demas 2004), and begging is presumably also energetically costly. Canary and magpie chicks forced to beg for a prolonged time divert growth energy to begging, thereby reducing growth rates (Kilner 2001; Rodríguez-Gironés et al. 2001). This effect, nevertheless, has not been detected in house sparrow nestlings (Kedar et al. 2000; this study), in which the energy needed for begging may have been diverted from the immune system, thereby weakening it. This could explain also why in other species (ring dove, tree swallow and a burying beetle) intense begging does not decrease the growth rate, either. Growth rate and immune response are also compromised (Fair et al. 1999; Soler et al. 2003; Brommer 2004), suggesting a three-way trade-off between growth, immune response and begging in nestlings, with the optimal strategy of energy allocation varying between species. Intraspecific variation in the optimal energy allocation according to the risk of parasitism is also possible. For example, great tit (Parus major) parents exposed to nest ectoparasites reduce yolk-androgen deposition, presumably to increase nestling immunocompetence (Tschirren et al. 2004), and by varying yolk-androgen deposition birds also modify nestling begging (e.g. Hinde et al. 2009).

On the other hand, physical effort provoked by the begging behaviour, with loud calls and many movements, probably increases the level of reactive oxygen species, disturbing the balance between pro-oxidative and anti-oxidative molecules (Costantini 2008). The immune response also increases the release of reactive oxygen species (Costantini & Møller 2009; Sorci & Faivre 2009). Both processes functioning simultaneously could increase oxidative stress over the levels that the nestling physiology may endure, and immune response could be adaptively reduced in order to diminish the risk of oxidative stress (Råberg et al. 1998; Monaghan et al. 2009). This could explain why great tit nestlings supplemented with carotenoids (an antioxidant; McGraw & Ardia 2003, 2004), beg more fiercely than do control chicks (Helfenstein et al. 2008), because these nestlings would have more resources to reduce the oxidative stress generated by begging.

The trade-off between begging and immunocompetence is probably mediated by steroids (Ricklefs & Wikelski 2002; Adkins-Regans 2005; French et al. 2009). In house sparrow nestlings, food deprivation raises the plasma level of corticosterone, and the exogenous administration of this hormone heightens the level of begging at the same time as it lowers the immune response (Loiseau et al. 2008). Testosterone increases begging intensity in chicks of a number of species (reviewed in Schwabl & Lipar 2002; Gil 2008; Ros 2008) at the same time as inducing immunosuppression (Navara & Mendonça 2008). Also, intense nestmate competition elevates the levels of both steroids (Naguib et al. 2004). Testosterone, in fact, mediates the trade-off between growth and begging in canary nestlings (Buchanan et al. 2007). Therefore, begging effort by nestlings probably stimulates the secretion of these hormones, which in turn would reduce immunocompetence.

In conclusion, this study reveals physiological costs related to begging behaviour in house sparrow nestlings, depressing the immune response. These costs may limit the evolutionary escalation of begging, allowing an offspring to signal its feeding needs or its disposition to compete honestly by means of begging, as predicted by the models based on costly begging (e.g. Godfray 1991; Johnstone 1998; Rodríguez-Gironés 1999; Parker et al. 2002). Moreover, this cost implies that an infected offspring cannot afford the costs of begging while combating disease. In the barn swallow (Hirundo rustica), nestlings injected with sheep red-blood cells (SRBC), which elicit an immune response, begged at the same rate as control nestlings (Saino et al. 2000a), but showed reduced mouth redness (Saino et al. 2000b), and parents preferentially feed chicks with redder mouths (Saino et al. 2003). Furthermore, the findings suggest that, in some species, the cost of begging may be reflected in a reduction of the growth rate (e.g. the canary; Kilner 2001), while in others (such as the house sparrow) it may be expressed in lower immunocompetence.

Acknowledgements

This work was supported by a postdoctoral fellowship awarded to G.M.-R. by the Spanish government (Ministerio de Ciencia e Innovación). Comments by Trevor Price, Tomás Redondo and two anonymous referees greatly improved the manuscript. David Nesbitt improved the English. All work was performed with the permission of the Andalusian government.

References

  1. Adkins-Regans E.2005Hormones and social behavior Princeton, NJ: Princeton University Press [Google Scholar]
  2. Ardia D. R., Schat K. A.2008Ecoimmunology. In Avian immunology (eds Davidson F., Kaspers B., Schat K. A.), pp. 421–442 London, UK: Elsevier [Google Scholar]
  3. Bailey R. C., Byrnes J.1990A new, old method for assessing measurement error in both univariate and multivariate morphometric studies. Syst. Biol. 39, 24–130 [Google Scholar]
  4. Bergstrom C. T., Lachmann M.1997Signalling among relatives. I. Is costly signalling too costly? Phil. Trans. R. Soc. Lond. B 352, 609–617 (doi:10.1098/rstb.1997.0041) [Google Scholar]
  5. Bergstrom C. T., Lachmann M.1998Signaling among relatives. III. Talk is cheap. Proc. Natl Acad. Sci. USA 95, 5100–5105 (doi:10.1073/pnas.95.9.5100) [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brilot B. O., Johnstone R. A.2002Cost, competition and information in communication between relatives. J. Theor. Biol. 217, 331–340 (doi:10.1006/jtbi.2002.3035) [DOI] [PubMed] [Google Scholar]
  7. Brommer J. E.2004Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc. R. Soc. Lond. B 271, S110–S113 (doi:10.1098/rsbl.2003.0103) [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buchanan K. L., Goldsmith A. R., Hinde C. A., Griffith S. C., Kilner R. M.2007Does testosterone mediate the trade-off between nestling begging and growth in the canary (Serinus canaria)? Horm. Behav. 52, 664–671 (doi:10.1016/j.yhbeh.2007.08.009) [DOI] [PubMed] [Google Scholar]
  9. Chappell M. A., Bachman G. C.2002Energetic costs of begging behaviour. In The evolution of begging (eds Wright J., Leonard M. L.), pp. 143–162 Dordrecht, The Netherlands: Kluwer Academic Publishers [Google Scholar]
  10. Clutton-Brock T. H.1991The evolution of parental care Princeton, NJ: Princeton University Press [Google Scholar]
  11. Costantini D.2008Oxidative stress in ecology and evolution: lessons from avian studies. Ecol. Lett. 11, 1238–1251 [DOI] [PubMed] [Google Scholar]
  12. Costantini D., Møller A. P.2009Does immune response cause oxidative stress in birds? A meta-analysis. Comp. Biochem. Phys. A 153, 339–344 [DOI] [PubMed] [Google Scholar]
  13. Demas G. E.2004The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm. Behav. 45, 173–180 (doi:10.1016/j.yhbeh.2003.11.002) [DOI] [PubMed] [Google Scholar]
  14. Fair J. M., Hansen E. S., Ricklefs R. E.1999Growth, developmental stability and immune response in juvenile Japanese quails (Coturnix coturnix japonica). Proc. R. Soc. Lond. B 266, 1735–1742 (doi:10.1098/rspb.1999.0840) [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. French S. S., Moore M. C., Demas G. E.2009Ecological immunology: the organism in context. Integr. Comp. Biol. 49, 246–253 (doi:10.1093/icb/icp032) [DOI] [PubMed] [Google Scholar]
  16. Gil D.2008Hormones in avian eggs: physiology, ecology and behavior. Adv. Stud. Behav. 38, 337–398 (doi:10.1016/S0065-3454(08)00007-7) [Google Scholar]
  17. Godfray H. C. J.1991Signalling of need by offspring to their parents. Nature 352, 328–330 (doi:10.1038/352328a0) [Google Scholar]
  18. Godfray H. C. J., Johnstone R. A.2000Begging and bleating: the evolution of parent–offspring signalling. Phil. Trans. R. Soc. Lond. B 355, 1581–1591 (doi:10.1098/rstb.2000.0719) [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Goodship N. M., Buchanan K. L.2007Nestling testosterone controls begging behaviour in the pied flycatcher Ficedula hypoleuca. Horm. Behav. 52, 454–460 (doi:10.1016/j.yhbeh.2007.06.008) [DOI] [PubMed] [Google Scholar]
  20. Grodzinski U., Hauber M. E., Lotem A.2009The role of feeding regularity and nestling digestive efficiency in parent–offspring communication: an experimental test. Funct. Ecol. 23, 569–577 (doi:10.1111/j.1365-2435.2008.01536.x) [Google Scholar]
  21. Harper D., Maynard Smith J.2003Animal signals New York, NY: Oxford University Press [Google Scholar]
  22. Haskell D.2002Begging behaviour and nest predation. In The evolution of begging (eds Wright J., Leonard M. L.), pp. 163–172 Dordrecht, The Netherlands: Kluwer Academic Publishers [Google Scholar]
  23. Helfenstein F., Berthouly A., Tanner M., Karadas F., Richner H.2008Nestling begging intensity and parental effort in relation to prelaying carotenoid availability. Behav. Ecol. 19, 108–115 (doi:10.1093/beheco/arm103) [Google Scholar]
  24. Hinde C. A., Buchanan K. L., Kilner R. M.2009Prenatal environmental effects match offspring begging to parental provisioning. Proc. R. Soc. B 276, 2787–2794 (doi:10.1098/rspb.2009.0375) [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Johnstone R. A.1998Efficacy and honesty in communication between relatives. Am. Nat. 152, 45–58 (doi:10.1086/286148) [DOI] [PubMed] [Google Scholar]
  26. Johnstone R. A., Godfray H. C. J.2002Models of begging as a signal of need. In The evolution of begging (eds Wright J., Leonard M. L.), pp. 1–20 Dordrecht, The Netherlands: Kluwer Academic Publishers [Google Scholar]
  27. Kedar H., Rodríguez-Gironés M. A., Yedvab S., Winkler D. W., Lotem A.2000Experimental evidence for offspring learning in parent–offspring communication. Proc. R. Soc. Lond. B 267, 1723–1727 (doi:10.1098/rspb.2000.1201) [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kennedy M. W., Nager R. G.2006The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol. Evol. 21, 653–655 (doi:10.1016/j.tree.2006.09.017) [DOI] [PubMed] [Google Scholar]
  29. Kilner R. M.2001A growth cost of begging in captive canary chicks. Proc. Natl Acad. Sci. USA 98, 11 394–11 398 (doi:10.1073/pnas.191221798) [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kilner R., Johnstone R. A.1997Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol. Evol. 12, 11–15 (doi:10.1016/S0169-5347(96)10061-6) [DOI] [PubMed] [Google Scholar]
  31. Lazarus J., Inglis I.1986Shared and unshared parental investment, parent–offspring conflict, and brood size. Anim. Behav. 34, 1791–1804 (doi:10.1016/S0003-3472(86)80265-2) [Google Scholar]
  32. Leonard M. L., Horn A. G., Porter J.2003Does begging effort affect growth in nestling tree swallows, Tachycineta bicolor? Behav. Ecol. Sociobiol. 54, 573–577 (doi:10.1007/s00265-003-0668-2) [Google Scholar]
  33. Lochmiller R. L., Deerenberg C.2000Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87–98 (doi:10.1034/j.1600-0706.2000.880110.x) [Google Scholar]
  34. Loiseau C., Sorci G., Dano S., Chastel O.2008Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows. Gen. Comp. Endocrinol. 155, 101–108 (doi:10.1016/j.ygcen.2007.03.004) [DOI] [PubMed] [Google Scholar]
  35. Martin L. B., II, Han P., Lewittes J., Kuhlman J. R., Klasing K. C., Wikelski M.2006Phytohemagglutinin-induced skin swelling in birds: histiological support for a classic immunoecological technique. Funct. Ecol. 20, 290–299 (doi:10.1111/j.1365-2435.2006.01094.x) [Google Scholar]
  36. Mauck R. A., Matson K. D., Philipsborn J., Ricklefs R. E.2005Increase in the constitutive innate humoral immune system in Leach's Storm-Petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct. Ecol 19, 1001–1007 (doi:10.1111/j.1365-2435.2005.01060.x) [Google Scholar]
  37. McGraw K. J., Ardia D. R.2003Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am. Nat. 162, 704–712 (doi:10.1086/378904) [DOI] [PubMed] [Google Scholar]
  38. McGraw K. J., Ardia D. R.2004Immunoregulatory activity of different dietary carotenoids in male zebra finches. Chemoecology 14, 25–29 [Google Scholar]
  39. Mock D. W., Parker G. A.1997The evolution of sibling rivalry Oxford, UK: Oxford University Press [Google Scholar]
  40. Møller A. P., Saino N.2004Immune response and survival. Oikos 104, 299–304 (doi:10.1111/j.0030-1299.2004.12844.x) [Google Scholar]
  41. Monaghan P., Metcalfe N. B., Torres R.2009Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett. 12, 75–92 (doi:10.1111/j.1461-0248.2008.01258.x) [DOI] [PubMed] [Google Scholar]
  42. Moreno-Rueda G.2007Is there empirical evidence for the cost of begging? J. Ethol. 25, 215–222 (doi:10.1007/s10164-006-0020-1) [Google Scholar]
  43. Moreno-Rueda G., Soler M.2002Cría en cautividad del Gorrión Común Passer domesticus. Ardeola 49, 11–17 [Google Scholar]
  44. Naguib M., Riebel K., Marzal A., Gil D.2004Nestling immunocompetence and testosterone covary with brood size in a songbird. Proc. R. Soc. Lond. B 271, 833–838 (doi:10.1098/rspb.2003.2673) [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Navara K. J., Mendonça M. T.2008Yolk androgens as pleitropic mediators of physiological processes: A mechanistic review. Comp. Biochem. Physiol. A 150, 378–386 [DOI] [PubMed] [Google Scholar]
  46. Navarro C., Marzal A., de Lope F., Møller A. P.2003Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101, 291–298 (doi:10.1034/j.1600-0706.2003.11663.x) [Google Scholar]
  47. Norris K., Evans M. R.2000Ecological immunology: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19–26 (doi:10.1093/beheco/11.1.19) [Google Scholar]
  48. Parker G. A., Royle N. J., Hartley I. R.2002Begging scrambles with unequal chicks: interactions between need and competitive ability. Ecol. Lett. 5, 206–215 (doi:10.1046/j.1461-0248.2002.00301.x) [Google Scholar]
  49. Quinn G. P., Keough M. J.2002Experimental design and data analysis for biologists Cambridge, UK: Cambridge University Press [Google Scholar]
  50. Råberg L., Grahn M., Hasselquist D., Svensson E.1998On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. Lond. B 265, 1637–1641 (doi:10.1098/rspb.1998.0482) [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Redondo T., Castro F.1992Signalling of nutritional need by magpie nestlings. Ethology 92, 193–204 [Google Scholar]
  52. Ricklefs R. E., Wikelski M.2002The physiology/life-history nexus. Trends Ecol. Evol. 17, 462–468 (doi:10.1016/S0169-5347(02)02578-8) [Google Scholar]
  53. Ringsby T. H., Sæther B.-E., Solberg E. J.1998Factors affecting juvenile survival in House Sparrow Passer domesticus. J. Avian Biol. 29, 241–247 (doi:10.2307/3677106) [Google Scholar]
  54. Rodríguez-Gironés M. A.1999Sibling competition stabilizes signalling resolution models of parent–offspring conflict. Proc. R. Soc. Lond. B 266, 2399–2402 (doi:10.1098/rspb.1999.0937) [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rodríguez-Gironés M. A., Zúñiga J. M., Redondo T.2001Effects of begging on growth rates of nestling chicks. Behav. Ecol. 12, 269–274 (doi:10.1093/beheco/12.3.269) [Google Scholar]
  56. Ros A. F. H.2008Patterns of testosterone responsiveness and immunity in relation to competitive behavior in chicks. Horm. Behav. 54, 234–237 (doi:10.1016/j.yhbeh.2008.02.022) [DOI] [PubMed] [Google Scholar]
  57. Roulin A.2001On the cost of begging vocalization: implications of vigilance. Behav. Ecol. 12, 506–510 (doi:10.1093/beheco/12.4.506) [Google Scholar]
  58. Royle N. J., Hartley I. R., Parker G. A.2002Begging for control: when are offspring solicitation behaviours honest? Trends Ecol. Evol. 17, 434–440 (doi:10.1016/S0169-5347(02)02565-X) [Google Scholar]
  59. Saino N., Ninni P., Incagli M., Calza S., Sacchi R., Møller A. P.2000aBegging and parental care in relation to offspring need and condition in the barn swallow (Hirundo rustica). Am. Nat. 156, 637–649 (doi:10.1086/316996) [DOI] [PubMed] [Google Scholar]
  60. Saino N., Ninni P., Calza S., Martinelli R., De Bernardi F., Møller A. P.2000bBetter red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. Proc. R. Soc. Lond. B 267, 57–61 (doi:10.1098/rspb.2000.0966) [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Saino N., Ambrosini R., Martinelli R., Ninni P., Møller A. P.2003Gape coloration reliably reflects immunocompetence of barn swallow (Hirundo rustica) nestlings. Behav. Ecol. 14, 16–22 (doi:10.1093/beheco/14.1.16) [Google Scholar]
  62. Schmid-Hempel P.2003Variation in immune defence as a question of evolutionary ecology. Proc. R. Soc. Lond. B 270, 357–366 (doi:10.1098/rspb.2002.2265) [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schwabl H., Lipar J. L.2002Hormonal regulation of begging behaviour. In The evolution of begging (eds Wright J., Leonard M. L.), pp. 221–244 Dordrecht, The Netherlands: Kluwer Academic Publishers [Google Scholar]
  64. Schwagmeyer P. L., Mock D. W.2008Parental provisioning and offspring fitness: size matters. Anim. Behav. 75, 291–298 (doi:10.1016/j.anbehav.2007.05.023) [Google Scholar]
  65. Searcy W. A., Nowicki S.2005The evolution of animal communication Princeton, NJ: Princeton University Press [Google Scholar]
  66. Sheldon B. C., Verhulst S.1996Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317–321 (doi:10.1016/0169-5347(96)10039-2) [DOI] [PubMed] [Google Scholar]
  67. Smiseth P. T., Parker H. J.2008Is there a cost to larval begging in the burying beetle Nicrophorus vespilloides? Behav. Ecol. 19, 1111–1115 (doi:10.1093/beheco/arn101) [Google Scholar]
  68. Smits S. E., Bortolotti G. R., Tella J. L.1999Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct. Ecol. 13, 567–572 (doi:10.1046/j.1365-2435.1999.00338.x) [Google Scholar]
  69. Soler J. J., De Neve L., Pérez-Contreras T., Soler M., Sorci G.2003Trade-off between immunocompetence and growth in the magpies: an experimental study. Proc. R. Soc. Lond. B 270, 241–248 (doi:10.1098/rspb.2002.2217) [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Sorci G., Faivre B.2009Inflammation and oxidative stress in vertebrate host–parasite systems. Phil. Trans. R. Soc. B 364, 71–83 (doi:10.1098/rstb.2008.0151) [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tella J. L., Lemus J. A., Carrete M., Blanco G.2008The PHA test reflects acquired T-Cell mediated immunocompetence in birds. PLoS ONE 3, e3295 (doi:10.1371/journal.pone.0003295) [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Trivers R. L.1974Parent–offspring conflict. Am. Zool. 14, 249–264 [Google Scholar]
  73. Tschirren B., Richner H., Schwabl H.2004Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc. R. Soc. Lond. B 271, 1371–1375 (doi:10.1098/rspb.2004.2730) [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. von Ende C.2001Repeated-measures analysis: growth and other time-dependent measures. In Design and analysis of ecological experiments. (eds Scheiner S. M., Gurevitch J.), pp. 134–157 New York, NY: Oxford University Press [Google Scholar]
  75. Wells J. C. K.2003Parent–offspring conflict theory, signalling of need, and weight gain in early life. Q. Rev. Biol. 78, 169–202 [DOI] [PubMed] [Google Scholar]
  76. Westneat D. F., Weiskittle J., Edenfield R., Kinnard T. B., Poston J. P.2004Correlates of cell-mediated immunity in nestling house sparrows. Oecologia 141, 17–23 [DOI] [PubMed] [Google Scholar]
  77. Wright J., Leonard M. L.2002The evolution of begging Dordrecht, The Netherlands: Kluwer Academic Publishers [Google Scholar]
  78. Zuk M., Stoehr A. M.2002Immune defense and host life history. Am. Nat. 160, S9–S22 (doi:10.1086/342131) [DOI] [PubMed] [Google Scholar]

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