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Unexpectedly low paternal diversity is associated with infrequent pollinator visitation for a bird-pollinated plant

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Abstract

The behaviour of pollinators has important consequences for plant mating. Nectar-feeding birds often display behaviour that results in more pollen carryover than insect pollinators, which is predicted to result in frequent outcrossing and high paternal diversity for bird-pollinated plants. We tested this prediction by quantifying mating system parameters and bird visitation in three populations of an understory bird-pollinated herb, Anigozanthos humilis (Haemodoraceae). Microsatellite markers were used to genotype 131 adult plants, and 211 seeds from 23 maternal plants, from three populations. While outcrossing rates were high, estimates of paternal diversity were surprisingly low compared with other bird-pollinated plants. Despite nectar-feeding birds being common at the study sites, visits to A. humilis flowers were infrequent (62 visits over 21,552 recording hours from motion-triggered cameras, or equivalent to one visit per flower every 10 days), and the majority (76%) were by a single species, the western spinebill Acanthorhynchus superciliosus (Meliphagidae). Pollen counts from 30 captured honeyeaters revealed that A. humilis comprised just 0.3% of the total pollen load. For 10 western spinebills, A. humilis pollen comprised only 4.1% of the pollen load, which equated to an average of 3.9 A. humilis pollen grains per bird. Taken together, our findings suggest that low visitation rates and low pollen loads of floral visitors have led to the low paternal diversity observed in this understory bird-pollinated herb. As such, we shed new light on the conditions that can lead to departures from high paternal diversity for plants competing for the pollination services of generalist nectar-feeding birds.

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Acknowledgements

This project was funded by an Australian Research Council grant to SLK and RDP (DP140103357). Approval for the use of motion-triggered cameras to observe birds visiting A. humilis plants in Ioppolo Nature Reserve was granted by the University of Western Australia Animal Ethics Committee. Ethics approval for mist-netting and bird banding/ringing was granted by Edith-Cowan University (Davis 14087) and cross-institutional approval was granted by the University of Western Australia (Edith-Cowan University Project number 14087). Bob Huston (Department of Biodiversity, Conservation and Attractions) provided logistical support, Mike Lohr and Floyd Holmes assisted with bird banding, Alison Ritchie and Carole Elliott assisted with the analysis, and Bronwyn Ayre, Jo-Anne Kestel, Terry Kestel, William Thomas, and Kelly Irving assisted with fieldwork.

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All authors conceived of the concepts and ideas. JHK conducted the field and lab work, with assistance from SLK, JA and RAD. JHK and SLK analysed the data. JHK, RDP and SLK led the the writing with significant contributions from all others.

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Correspondence to Joshua H. Kestel.

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The authors declare that they have no conflict of interest.

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Communicated by Monica Geber.

We examined the mating system of a bird-pollinated herb to test the prediction that bird pollination leads to high paternal diversity. Field and camera observations used to estimate visitation rates revealed that while nectar-feeding birds were common in the area, visits to Anigozanthos humilis were infrequent. Microsatellite markers demonstrated that outcrossing rates were high but, contrary to expectations, paternal diversity was very low. Our findings give insight into the circumstances that can lead to departures from high paternal diversity for plants competing for the pollination services of generalist nectar-feeding birds.

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Kestel, J.H., Phillips, R.D., Anthony, J. et al. Unexpectedly low paternal diversity is associated with infrequent pollinator visitation for a bird-pollinated plant. Oecologia 196, 937–950 (2021). https://doi.org/10.1007/s00442-021-04906-x

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  • DOI: https://doi.org/10.1007/s00442-021-04906-x

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