Forced copulations and intra-specific parasitism: Two costs of social living in the white-fronted bee-eater.

White-fronted bee-eaters are colonially breeding birds that exhibit highly developed helping-at-the-nest. Through long-term studies of an individually-marked population, we have documented two costs of social living: 1) harassment of mated females by extra-pair males, and 2) intra-specific parasitism by females who lay eggs in the nests of others. Breeding females are sexually chased and, occasionally, forceably mated by males other than their mates. Focal-sampling of females throughout their period of receptivity revealed that the average female is involved in 5 to 8 sexual chases and is forceably copulated 0.15 to 0.23 times per breeding season. This risk to females would be much greater were it not for the behavior of male mates who remain close to, and actively defend, their partners. Such mate-guarding is highly effective — females entering and leaving the colony in consort with their mates are sexually harassed only 1/10 as often as females travelling alone. Although sexual harassment of females is common at bee-eater colonies, the risk of paternity uncertainty arising from forced copulations is thought to be low. The reason is that females copulate repeatedly with their male mates on all days immediately prior to as well as during egg laying. This point has been overlooked in previous reports and has led to an exaggeration of the paternity risks associated with forced sexual chases. We conclude that sexual chasing of extra-pair females is a low yield reproductive tactic employed primarily by monogamously mated males whose presence at the colony is required to allofeed and mateguard their own egg-laying females. Female white-fronted bee-eaters lay eggs in nests other than their own. This intraspecific parasitism constitutes a greater threat to certainty of parentage than does forced copulation. Over four years of study, 16% of nests were parasitized and 7 % of all eggs were laid by a female other than the breeder (Table 2). Parasitizing females come primarily from two sources: (1) members of mated pairs whose own breeding attempt is disrupted at the time of egg laying, and (2) single females who opportunistically add an egg at the nest of their parents (or parent plus step-parent). In each case of kin-parasitism, the “parasitic” female remained socially integrated with the host group and helped in the rearing of the young. In contrast, 9 of 10 females that parasitized the nests of non-relatives had no other interactions with the hosts (Table 3). Parasitizing females exhibited two specialized behaviors that enhanced their reproductive effectiveness: (1) they spent many hours observing, investigating, and testing the defenses of potential host nests, and (2) they preferentially laid in hosts' nests at the appropriate chronological stage of development. Breeding females also exhibited counterbehaviors against being parasitized. These included: (1) remaining sequestered in their nest chambers for 64%-65% of the daylight hours and 94 % of the pre-roost hours during their days of egg laying, (2) aggressively defending their nest entrances against all investigating (potentially parasitic) females, and (3) actively removing any eggs laid in their nests prior to the initiation of their own clutch. These tactics and countertactics suggest a long evolutionary history of parasitic opportunities and risks among white-fronted bee-eaters.