Costs and benefits of experimentally induced changes in the allocation of growth versus immune function under differential exposure to ectoparasites

Abstract

Background: Ecological immunology has focused on the costs of investment in immunocompetence. However, understanding optimal resource allocation to immune defence requires also identification of its benefits, which are likely to occur only when parasites are abundant.

Methodology: We manipulated the abundance of parasitic hen fleas in blue tit (Cyanistes caeruleus) nests, and supplemented their hosts, the nestlings, with methionine (a sulphur amino acid enhancing cell-mediated immunity) during day 3-6. We found a significant interaction between these two experimental factors on the development of immune defences and growth rates. Only in parasitized nests did methionine supplementation boost immune (PHA) response, and did nestling with experimentally increased immunocompetence show a relatively faster growth rate than control nestlings between days 6-9. Hence, the allocation of resources into immune defence and its growth-benefits are apparent only in presence of parasites. The main cost of methionine-induced increased allocation to the immune system was an increase in mortality, independently of ectoparasites. Nestlings in all treatments compensated initial growth reduction and all reached equal body size at day 16 (just prior to fledging), indicating a lack of long-term benefits. In addition, methionine treatment tended (P = 0.09) to lower circulating plasma immunoglobulin levels, possibly indicating a trade-off between the cell-mediated and humoral components of the immune system.

Conclusions: We found no strong benefits of an increased investment in immunocompetence in a parasite-rich environment. Any deviation from the growth trajectory (due to changes in allocation induced by methionine) is largely detrimental for survival. Hence, while costs are apparent identifying the benefits of investment in immunocompetence during ontogeny is challenging.

Figure 1. Physiological traits of control (C, open symbols) and methionine-supplemented (M, filled symbols) blue tit nestlings reared in deparasitized and parasitized nests; least square means ± SE.

Sample sizes (number of nestlings) are indicated on the graphs.

Figure 2. Survival of blue tit nestlings after the start of methionine supplementation (day 3 post-hatching).

During the supplementation period (between day 3 and 6) methionine-treated nestlings (M, filled symbols, N = 209) had higher mortality than control nestlings (C, open symbols, N = 212).

Figure 3. Mass gain of control (C, open symbols) and methionine-supplemented (M, filled symbols) blue tit nestlings in deparasitized and parasitized nests; least square means + SE.

(A) During the supplementation period (between day 3 and 6) methionine treated nestlings had suppressed growth, but in deparasitized nests not significantly so. (B) Immediately after supplementation ended (between day 6 and 9) methionine treated nestlings had higher mass gain than control nestlings in parasitized nests, but not in deparasitized nests. Sample sizes are indicated on the graphs. Statistics in Table 2.