Summary
The dear enemy effect arises when territorial animals respond more intensely to unfamiliar strangers than to familiar neighbours. This widespread behavioural phenomenon occurs because strangers represent a threat to both an animal's territory and parentage whereas neighbours represent a threat only to parentage. Recent research in birds demonstrates some flexibility in the dear enemy effect across the breeding season. Given that neighbours often sire extrapair young, male animals may benefit by responding more aggressively to neighbours during periods of female fertility. Here we investigate the hypothesis that the dear enemy effect varies with female fertility by testing the prediction that male birds will respond more strongly to neighbours when their own mates are fertile than when they are not fertile. We conducted a playback experiment with wild song sparrows, Melospiza melodia, repeating playback sessions to paired territorial males over the course of a breeding season, including periods when females were fertile and periods when they were not. Male song sparrows displayed a dear enemy effect only when their social mate was not fertile. We conclude that male song sparrows adjust behaviour towards neighbours based on their own mate's fertility status, presumably because neighbours threaten a territorial male's parentage during his breeding partner's fertile period. When paternity is not at stake, reduced aggression towards neighbours may enhance fitness, but when paternity is at stake, normal levels of aggression towards neighbours may be favoured as a mate-guarding tactic.
Methodology
Study Site and Study Species
We conducted this experiment at the Queen's University Biological Station (44°34′N, 76°19′W) north of Kingston, Ontario, Canada. Our playback experiments took place between 18 April and 22 May 2015 and between 8 April and 15 May 2016; these periods correspond roughly to pair formation through nest building, egg laying and incubation in our study population. Our subjects were 29 focal male song sparrows (19 in 2015 and 10 in 2016) living in fields and marshes in the vicinity of the research station. Of our 29 subjects, 25 were banded with unique combinations of coloured leg bands and a Canadian Wildlife Services numbered band to facilitate individual identification. For the remaining four unbanded males, we distinguished between individuals based on recordings of their individually distinctive song types, as well as their territorial position. Sharing of complete song types between neighbours is rare for song sparrows in eastern North America (Hughes, Anderson, Searcy, Bottensek, & Nowicki, 2007; although see Foote & Barber, 2007), including in our study population (Stewart & MacDougall-Shackleton, 2008) and therefore distinguishing between individuals based on unique song types is not difficult. From the original 29 playback subjects, we excluded two individuals that did not respond to any playback trials, three individuals that never paired with a female, and two individuals that moved their breeding territory part-way through the study period. After these exclusions we were left with 22 males for our analyses.
Playback Experiment
We mapped the territories of our focal birds during their arrival from migration in early April. An observer followed focal birds around their territories for at least 90 min, taking careful note of locations where each bird sang, and logging these points into a GPS (Garmin GPS60). We set up our playback loudspeaker 10 m inside the subject's territory, nearest to the boundary with the neighbour that we were simulating with playback. We chose to place the loudspeaker slightly inside the territory in order to minimize the chance of interference from the neighbour. The loudspeaker occupied the same position for both neighbour and stranger trials. For most birds, we broadcast playback from the same location within each bird's territory across the entire season. In three instances, however, territory borders changed over the course of the experiment. In these instances we moved the speaker to maintain a position 10 m from the edge of the focal bird's territory (average distance moved in these three cases: 5 m). We placed the loudspeaker in a sound baffle made of a 20-inch (51 cm) diameter plastic parabola lined with 2-inch (5 cm) thick foam and a camouflage-coloured fabric. This baffle diminished the noise behind the loudspeaker, in order to further reduce interference from the neighbour. We did not conduct playback to neighbouring birds on the same day; subjects had to be at least one territory apart, and have different neighbours used for playback stimuli to receive playback on the same day.
We carried out playback experiments between 0630 hours and 1300 hours. An observer sat at a position 20 m away from the loudspeaker and dictated the focal bird's behaviour into a microphone, to serve as a record of the birds' response to playback. Playback trials began once both the focal bird and the neighbouring bird were not singing and when the focal bird was greater than 15 m away from the loudspeaker. The playback period lasted 3 min and was followed by a 5 min post-playback observation period. We focused our analysis solely on the 3 min playback period because most birds began countersinging with their neighbours during the post-playback period. After 20 min had elapsed from the end of the first playback trial, the subject received the second treatment (i.e. neighbour or stranger). We alternated the order of presentation of the neighbour and stranger stimuli, such that each bird received the neighbour or stranger playback first an equal number of times.