During reproduction, seabirds need to balance the demands of self- and offspring-provisioning within the constraints imposed by central place foraging. To assess behavioral adjustments and tolerances to these constraints, we studied the feeding tactics and reproductive success of common murres (also known as common guillemots) Uria aalge, at their largest and most offshore colony (Funk Island) where parents travel long distances to deliver a single capelin Mallotus villosus to their chicks. We assessed changes in the distance murres traveled from the colony, their proximate foraging locations and prey size choice during two successive years in which capelin exhibited an order of magnitude decrease in density and a shift from aggregated (2004) to dispersed (2005) distributions. When capelin availability was low (2005), parental murres increased their maximum foraging distances by 35% (60 to 81 km) and delivered significantly larger capelin to chicks, as predicted by central place foraging theory. Murres preferred large (>140 mm) relative to small capelin (100–140 mm) in both years, but unexpectedly this preference increased as the relative density of large capelin decreased. We conclude that single prey-loading murres target larger capelin during long foraging trips as parents are ‘forced’ to select the best prey for their offspring. Low fledgling masses suggest also that increased foraging time when capelin is scarce may come at a cost to the chicks (i.e. fewer meals per day). Murres at this colony may be functioning near physiological limits above which further or sustained adjustments in foraging effort could compromise the life-time reproductive success of this long-lived seabird.