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Cloacal erection promotes vent apposition during forced copulation in the New Zealand stitchbird (hihi): implications for copulation efficiency in other species

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Abstract

Cloacal protuberances (CP) in male birds result from spermatic engorgement of storage tubules around the cloaca during the breeding season. We examined seasonal changes in the volume and orientation of the CP in the New Zealand stitchbird Notiomystis cincta. The male stitchbird has one of the largest recorded CPs for any species (max = 1,570 mm3), with CP volume increasing by almost 400% between the non-breeding and breeding seasons. While sperm competition has been positively correlated with the magnitude of CP storage in other species, no evidence previously existed for the CP improving copulation efficiency. By measuring the relative orientation of the CP throughout the year, we show that not only does the CP increase in size as males become sexually active, it also changes its orientation by approximately 60°. This results in it shifting from facing posteriorly to becoming almost perpendicular to the abdomen. This cloacal “erection” improves the apposition of the male and female cloacal openings during face-to-face forced copulation in this species. This provides the first reported evidence supporting the copulation efficiency hypothesis of the avian CP. While the magnitude of seasonal changes in female cloacal volume was similar to males, female cloacal orientation remained virtually unchanged across seasons. This difference between the sexes is likely to reflect differing selection pressures for optimizing sperm transfer. In females, a posterior-facing cloaca is ideal for both waste evacuation and sperm reception, whereas, for the male, a posterior-facing cloaca is well suited for waste evacuation, but possibly hinders sperm delivery. Changes in male cloacal orientation from the non-breeding to the breeding season are a likely reflection of conflict in this dual function. Evidence of changes in CP orientation in another passerine species suggests this phenomenon is widespread and also important for understanding related fields such as sperm competition, forced copulation and constraints on the evolution of the avian intromittent organ.

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Acknowledgments

We thank Clare Miller, Kirsty Chalmers, Troy Makan and Sandra Jack for help in the field and Barbara Walter, Ray Walter, Ian Price, Thomas-Helmig Christensen, Rachel Curtis, Rosalie Stamp, Richard Griffiths, the Supporters of Tiritiri Matangi Inc and the New Zealand Department of Conservation for logistical support. We also thank Marty Leonard, Staffan Roos and two anonymous referees for their helpful comments on a previous version of this manuscript. This study was supported by a Massey University doctoral scholarship to M.L. and partly funded by the New Zealand Lotteries Commission and the Supporters of Tiritiri Matangi. All work was carried out under a research permit from the New Zealand Department of Conservation, had Massey University animal ethics approval and complied with the current laws of New Zealand

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Correspondence to Matthew Low.

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Communicated by M. Leonard

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Low, M., Castro, I. & Berggren, Å. Cloacal erection promotes vent apposition during forced copulation in the New Zealand stitchbird (hihi): implications for copulation efficiency in other species. Behav Ecol Sociobiol 58, 247–255 (2005). https://doi.org/10.1007/s00265-005-0935-5

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