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Novel mating modes on wave-swept shores: aerial copulation and sperm release in an intertidal stalked barnacle

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Abstract

Mating behavior of the intertidal stalked barnacle, Pollicipes polymerus, is unusual. Spermcast mating is unexpectedly common, but its prevalence and mechanisms of sperm release and capture are unknown. Moreover, copulation has never been observed in P. polymerus, despite possessing a well-developed penis and despite numerous attempts to observe it. This raises questions about whether spermcasting is a primary or secondary mode of mating in P. polymerus. Through field observations at sites in Barkley Sound, British Columbia (48°N, 125°W) in the northern hemisphere summers of 2012–2014, (a) the incidence of sperm leakage at low tide and (b) the type and prevalence of copulatory behaviors were quantified. Sperm leakage was an infrequent event: ~0.1 % of P. polymerus released a milky, viscous liquid between their opercular plates at low tide. Microscopic examination confirmed that this liquid contained abundant sperm, although sperm viability could not be verified. Some leaker individuals (31 % of 13 examined) contained newly released egg sacks, so sperm leakage in these may have been a post-mating response. However, the remaining leakers contained either fully mature egg masses (egg lamellae), or no eggs or sperm at all, suggesting that sperm leakage was an active process. Transects of P. polymerus beds revealed that sperm leakage at low tide was independent of most weather and tidal conditions. However, sperm leakage was more common lower in the intertidal at more wave-exposed sites. Rates of copulation in the field were about four times those of sperm leakage, suggesting that leakage may be a secondary mode of fertilization. Unique among barnacles, copulation occurred mostly when barnacles were partially emersed, shortly after contact with breaking waves on an incoming tide. Aerial copulation may allow P. polymerus to mate more reliably on shores with high wave exposure. Also unlike other barnacles, reciprocal copulation was occasionally observed in P. polymerus.

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Acknowledgments

This work was supported by NSERC Discovery Grants to A.R.P. (A7245). We thank J. Sykes, C. Keates, N. Webster, and S. Anthony for field assistance, the director and staff of the Bamfield Marine Sciences Centre for logistical support, and C. Cameron, J. Healy, S. Leys, E. Lovas and A. Oatway for advice regarding sperm imaging.

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Correspondence to Marjan Barazandeh.

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Communicated by J. Grassle.

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Barazandeh, M., Palmer, A.R. Novel mating modes on wave-swept shores: aerial copulation and sperm release in an intertidal stalked barnacle. Mar Biol 162, 881–888 (2015). https://doi.org/10.1007/s00227-015-2631-y

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