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.

Prey choice, provisioning behaviour, and effects of early nutrition on nestling phenotype of titmice

“…We believe that this type of basic information is needed before we can answer more sophisticated questions, such as, would global warming lead to diet shifts in these species (Both, 2010)? Lastly, as in previous studies (Arnold et al, 2007), the relationship between spider intake and nestling size shown here highlights the importance of considering not only the composition of nestling food, but also the quality of the diet (its nutritional value) and the influence of this factor on offspring growth and development.…”

“…More recent studies (Ramsay & Houston, 2003) have shown that spiders are nutritionally similar to caterpillars, except that spiders contain high levels of taurine, an amino acid essential for the proper development and function of the central nervous system (Ramsay & Houston, 2003;Arnold et al, 2007 and references therein). Taurine is also reported to have effects on personality (e.g., risk-taking behaviour) and cognition in offspring (Arnold et al, 2007). To our knowledge, no studies have shown a direct link between taurine levels and body size in wild birds, despite there being some evidence from poultry that taurine is a growth factor directly associated with bone growth (Martin & Patrick, 1961).…”

“…Some authors have reported that the 2 variables are quadratically related ; this study), whereas others have found that such a relationship is asymptotic (Tremblay et al, 2005;Burger et al, 2012). Spiders are also an important food for many forest passerines (Gajdoš & Krištín, 1997); however, there is little information on their influence on nestling phenotype (Arnold et al, 2007). In general terms, studies dealing with nestling diet and provisioning behaviour from an ecological perspective are scarce (see, e.g., Cowie & Hinsley, 1988;Grundel, 1990;Grundel & Dahlsten, 1991;Naef-Daenzer, Naef-Daenzer & Nager, 2000;Mägi et al, 2009, Burger et al, 2012.…”

Environmental and genetic determinants of innovativeness in a natural population of birds

“…Fledging mass was also not linked to PSP, suggesting that food availability during the nestling stage as such was not the driving factor. Arnold et al [128] reported a link between the availability of an important amino acid found in spiders and cognitive development in the blue tit (Cyanistes caeruleus). Given that invertebrate density in general is higher in oak-rich habitats and is also likely to be higher where competition is less pronounced in low population density, our results on individual differences in PSP could instead be best explained by dietary composition during early nestling development.…”

The effect of food quality during growth on spatial memory consolidation in adult pigeons

“…It is not only the amount of food, but the type of diet that matters. For example, blue tit (Cyanistes caeruleus) nestlings supplemented with taurine (an amino acid important for early development) performed better as adults in a spatial memory task compared with taurine-deprived blue tits (Arnold et al, 2007). However, other studies in rats (Rattus norvegicus) have found the opposite result.…”