Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring

Abstract

Early nutrition shapes life history. Parents should, therefore, provide a diet that will optimize the nutrient intake of their offspring. In a number of passerines, there is an often observed, but unexplained, peak in spider provisioning during chick development. We show that the proportion of spiders in the diet of nestling blue tits, Cyanistes caeruleus, varies significantly with the age of chicks but is unrelated to the timing of breeding or spider availability. Moreover, this parental prey selection supplies nestlings with high levels of taurine particularly at younger ages. This amino acid is known to be both vital and limiting for mammalian development and consequently found in high concentrations in placenta and milk. Based on the known roles of taurine in mammalian brain development and function, we then asked whether by supplying taurine-rich spiders, avian parents influence the stress responsiveness and cognitive function of their offspring. To test this, we provided wild blue tit nestlings with either a taurine supplement or control treatment once daily from the ages of 2-14 days. Then pairs of size- and sex-matched siblings were brought into captivity for behavioural testing. We found that juveniles that had received additional taurine as neonates took significantly greater risks when investigating novel objects than controls. Taurine birds were also more successful at a spatial learning task than controls. Additionally, those individuals that succeeded at a spatial learning task had shown intermediate levels of risk taking. Non-learners were generally very risk-averse controls. Early diet therefore has downstream impacts on behavioural characteristics that could affect fitness via foraging and competitive performance. Fine-scale prey selection is a mechanism by which parents can manipulate the behavioural phenotype of offspring.

Figure 1

Age-specific diet of nestlings. (a) The proportions of spiders fed to broods (total number of spiders/total number of spiders, caterpillars and other invertebrates) from 06.00 to 10.00 did not vary significantly with date at the ages of 5 (filled triangles, solid line) or 11 days (open squares, dashed line). The proportion of spiders sampled from oak trees in the study site did not vary with date (grey stars, dotted line). See text for further details. Day 1 (when the first brood reached the age of 5 days) was 13 May 2005. Displayed here are actual proportions rather than the arcsine square-root transformed proportions used in the statistical analysis. (b) Estimated hourly taurine intake per chick adjusted for age-specific mean body mass (mg h⁻¹ g⁻¹) was significantly higher for 5-day-old chicks than 11-day-old chicks (N=18 nests). Figure shows mean±s.e.m.

Figure 2

Risk taking in juvenile blue tits depended upon body mass (age, 39 days), sex and taurine supplementation. Risk taking was measured on the y-axis from risk prone (short mean time to approach the novel objects) to risk averse (long time to approach). (a) males: heavier birds in both treatment groups were significantly more risk prone than lighter birds; however, (b) females: the negative relationship between body mass and risk taking was broken in the taurine group (filled squares, dashed line) but not in the control group (stars, solid line). This interaction remained significant even when a potential outlier (see arrow in b), a particularly heavy, shy female was removed (GLMM: F=4.41, d.f.=3,17.7, p=0.017). Family identity, entered as a random factor, contributed significantly to the full model (z=2.12, N=41, p=0.02), indicating that the variance in risk taking was greater between families than within families.

Figure 3

Propensity to take risks (mean time to approach a novel object) and nestling diet (taurine (filled circles) or control (crosses) treatment) interacted to affect (a) general (not found/found food) and (b) spatial learning abilities (not learnt/learnt location of food) of juvenile blue tits. The dashed line indicates the mean time to approach the novel objects of all birds in the colony (N=41). Relatively bold, risk-prone birds that had received a taurine supplement had poor general learning abilities and never found food under flaps, and shy, risk-averse controls failed the spatial learning tasks. Taurine birds with intermediate risk-taking propensities and relatively bold controls were significantly more likely to learn to successfully use spatial cues to find food. Family identity was entered into the GLMM as a random factor but was non-significant. Means±s.e.m. are shown.