NUTRITIONAL DEFICITS DURING POST-HATCHING DEVELOPMENT, CORTICOSTERONE, SPATIAL MEMORY AND THE HIPPOCAMPUS

Most avian species demonstrate significant individual variation in development rates within populations and among siblings within family broods, but the fitness consequences of such variation are unclear (O’Connor 1984; Ricklefs 1983). Whereas genetic factors might explain some of the variation, most differences in growth rates appear to be due to food availability (O’Connor 1984; Ricklefs 1983). Altricial birds grow very rapidly and depend entirely on their parents for food until they learn to forage independently (O’Connor 1984; Ricklefs 1983). Young birds suffer high mortality after they become independent, and the slower growing ones often show the lowest survival rates (O’Connor 1984; Ricklefs 1983; Merilla & Wiggins 1995). The causes of high mortality in first-year animals are not well understood, but it has been suggested that learning abilities of young play a critical role in their survival and thus selection pressure on learning could be high (Weathers & Sullivan 1989; Dukas 1998). It has been well documented that song learning in birds is negatively affected by nutritional deprivation during early post-hatching development (Nowicki et al. 2002; Buchanan et al. 2003; Spenser et al. 2003). It is less known, however, whether other learning abilities are also dependent on nutritional condition and development rates during early post-hatching period, and whether slower growing individuals might suffer higher mortality specifically because nutritional deficits cause learning impairments later in life.

 In mammals, the effects of malnutrition on the development of the brain and cognitive abilities have received considerable attention (Dauncey & Bicknell 1999; Bedi 2003). It has been suggested that malnutrition during early postnatal development might have a negative impact on the maturation of the brain, and the hippocampus in particular (Dauncey & Bicknell 1999; Bedi 2003). Because the hippocampus has been implicated in mediating spatial memory in both mammals and birds (Sherry et al. 1992), it is logical to predict that malnutrition during development might negatively impact spatial memory later in life (Bedi 1992; Dauncey & Bicknell 1999; Bedi 2003).

In food-caching birds hippocampal development continues even after fledging (Clauton 1995) and thus it might be sensitive to malnutrition during post-hatching period. Using western scrub-jays (Aphelocoma californica) we evaluated experimentally whether poor nutrition during early post-hatching development has a long-term effect on hippocampal structure and spatial memory. Compared to controls, one-year-old jays that experienced nutritional deficits had smaller hippocampi with fewer neurons, and performed worse in a cache recovery task and in a spatial version of an associative learning task. In contrast, performance of nutritionally deprived birds was similar to that of controls in two color versions of an associative learning task. These findings suggest that nutritional deficits during early development have long-term consequences for hippocampal structure and spatial memory function which, in turn, are likely to have a strong impact on animal’s future fitness.

Previously, several studies indicated that song learning in male birds might be impaired by nutritional stress during development and suggested that impaired song learning abilities provide an indirect signal of inferior quality of these males to their potential mates (Nowicki et al. 2002; Buchanan et al. 2003; Spencer et al. 2003). These studies suggested that song learning is an indicator that may correlate with some other phenotypic and/or genotypic variables that could directly affect fitness. It has also been shown that food deprivations during early post-hatching development could result in smaller body size (Searcy et al. 2004) and in reduced parasite resistance (Buchanan 2003), which could lead to higher mortality. Our study further supports the idea that nutrition during early post-hatching development may have serious implications for future fitness by showing that nutritional deficits similar to what could be observed between siblings within natural broods during early post-hatching development have long-term negative effects on the hippocampus and spatial memory, which could have a direct impact on future survival and fitness (Pravosudov & Lucas 2001).

The differences in hippocampus structure and spatial memory performance between nutritionally deprived and control scrub-jays were observed more than seven months after achieving nutritional independence despite the fact that there were no differences in telencephalon volume or brain mass.  These results indicate that nutritional rehabilitation (after the jays became independent and had unlimited access to food) did not alleviate the deleterious effects of malnutrition during the early post-hatching period.  These findings are particularly important with respect to the effects of malnutrition during development on the brain, cognitive abilities and general fitness later in life. From an evolutionary biology perspective, these memory impairments provide the critical link that might explain why slower growing individuals may suffer lower fitness and increased mortality later in life. Food caching animals in particular should be strongly affected by memory impairments because their survival critically depends on their ability to locate previously hidden caches (Pravosudov & Lucas 2001) and it is well known that they use spatial memory to do so (Shettleworth 1995).

We also investigated the effect on nutritional deficits on adrenocortical function and showed that compared to birds fed ad libitum, western scrub-jays that experienced nutritional deficits during post-hatching development also (a) had significantly elevated baseline corticosterone levels, (b) tended to have stronger adrenocortical stress response later in life whereas their baseline corticosterone levels were similar to those of controls and (c) had higher degree of fluctuating asymmetry in bone and feather measurements.

            Adrenocortical response to food shortages appears to be highly adaptive as it facilitates more begging which, it turn, should stimulate parents to increase their provisioning rates (Kitaysky et al. 2001). If parents are incapable of adjusting their foraging behavior, nestlings might maintain elevated corticosterone levels which appears to be responsible for numerous developmental disorders relating to fluctuating asymmetry and impaired cognition (Pravosudov et al. 2005; Kitaysky et al. 2003; Clinchy et al. 2004; Buchanan et al. 2003, 2004; Spencer et al. 2003).  Scrub-jays that experienced nutritional deficits during post-hatching development in this study suffered impaired spatial memory and had significantly reduced hippocampal volume with fewer neurons compared to birds raised on ad libitum food (Pravosudov et al. 2005). Studies that directly manipulated corticosterone levels in growing songbird chicks also suggested that elevated corticosterone levela are likely to be a key factor in developing brain disorders related to song nuclei later in life (Buchanan et al. 2003, 2004).

            Second important finding of our study concerns the fact that scrub-jays that experienced nutritional deficits during post-hatching development tended to have a stronger adrenocortical response to stress later in life even though they had ad libitum food since the time they learned to eat on their own. Much avian research has been focused on the relationship between ecological conditions and adrenocortical stress response (Wingfield et al. 1995, 1997, 1998). It has been suggested that stress response reflects ecological conditions preceding the time of sampling and thus the magnitude of stress response has been used as an indicator of past conditions (Wingfield et al. 1997, 1998; Clinchy et al. 2004). Our findings suggest that conditions during early development might also be responsible for at least some variation in adrenocortical stress responses in adult birds, in addition to environmental conditions preceding sampling. Our data indicated that in identical favorable conditions, birds that experienced malnutrition during post-hatching development tended to have stronger adrenocortical response to acute stress. It is not well known, however, how developmental history would affect stress response in animals which live in less favorable environments after becoming nutritionally independent, assuming that individuals survive. It is clear, however, that environment during early development need to be taken into consideration.