Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Reproductive biology of the threatened and highly fragmented shrub Persoonia hirsuta (Proteaceae)

Nathan J. Emery https://orcid.org/0000-0002-3385-1675 A * and Catherine A. Offord A
+ Author Affiliations
- Author Affiliations

A The Australian PlantBank, Australian Institute of Botanical Science, Australian Botanic Garden, Mount Annan, NSW 2567, Australia.


Handling Editor: Andrew Denham

Australian Journal of Botany 70(1) 56-62 https://doi.org/10.1071/BT21068
Submitted: 1 June 2021  Accepted: 10 November 2021   Published: 7 December 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

The Australian Proteaceous genus Persoonia is known to be pollinated by bees and have variable breeding systems that range from strictly self-incompatible to differing levels of self-compatibility. The endangered Persoonia hirsuta (Hairy Geebung) is a species currently in decline throughout its distribution, with many populations occurring in fragmented habitats comprising fewer than 10 plants or a single isolated individual. Despite its threatened status and recent population decline, the reproductive biology of P. hirsuta is unknown. In this study, we surveyed floral visitors and their foraging behaviour, and investigated the breeding system of P. hirsuta by conducting experimental hand-pollinations at two of the largest known populations. P. hirsuta was almost exclusively visited by native bees, including Leioproctus, Megachile and Tetragonula species. This study was the first to report Xylocopa bees and Zizinia butterflies visiting Persoonia flowers. On average, both foraging time per flower and the number of flowers visited per plant varied significantly among insect genera. Notably, Xylocopa bees visited more flowers per plant than did any other pollinator (22.1 ± 10.8 flowers). P. hirsuta has a breeding system that displays partial self-incompatibility with significantly higher fruit set in the cross- and open-pollination treatments at both populations (19.4 ± 10.8 to 44.8 ± 8.2%) than in the autogamy and selfed treatments (0.6 ± 0.6 to 9.0 ± 5.1%). The results of this study are critical to the future management of P. hirsuta, and suggest that its small and isolated populations may produce very few viable fruits in the absence of outcrossing.

Keywords: bees, breeding system, habitat fragmentation, hairy geebung, Leioproctus, Megachile, pollination, self-incompatibility, Xylocopa.


References

Aguilar R, Ashworth L, Galetto L, Aizen MA (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9, 968–980.
Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 16913941PubMed |

Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Molecular Ecology 17, 5177–5188.
Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches.Crossref | GoogleScholarGoogle Scholar | 19120995PubMed |

Aizen MA, Ashworth L, Galetto L (2002) Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? Journal of Vegetation Science 13, 885–892.
Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter?Crossref | GoogleScholarGoogle Scholar |

Auld TD, Keith DA, Bradstock RA (2000) Patterns in longevity of soil seedbanks in fire-prone communities of south-eastern Australia. Australian Journal of Botany 48, 539–548.
Patterns in longevity of soil seedbanks in fire-prone communities of south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Auld T, Freestone M, Broadhurst L, Zimmer H, Swarts N, Gallagher R (2018) Deciding whether to translocate. In ‘Guidelines for the translocation of threatened plants in Australia’, 3rd edn. (Eds LE Commander, DJ Coates, L Broadhurst, CA Offord, RO Makinson, M Mattes) pp. 9–26. (Australian Network for Plant Conservation: Canberra, ACT, Australia)

Ayre D, Haynes A, Gregory D (2021) Low genetic differentiation despite fragmentation in an endangered fire-sensitive shrub. International Journal of Plant Sciences 182, 229–237.
Low genetic differentiation despite fragmentation in an endangered fire-sensitive shrub.Crossref | GoogleScholarGoogle Scholar |

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Benson D, McDougall L (2000) Ecology of Sydney plant species. Part 7b: dicotyledon family Proteaceae to Rubiaceae. Cunninghamia 6, 1016–1202.

Bernhardt P, Weston P (1996) The pollination ecology of Persoonia (Proteaceae) in eastern Australia. Telopea 6, 775–804.
The pollination ecology of Persoonia (Proteaceae) in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Cadzow B, Carthew SM (2000) Breeding system and fruit development in Persoonia juniperina (Proteaceae). Cunninghamia 6, 941–950.

Cane JH (2001) Habitat fragmentation and native bees: a premature verdict? Conservation Ecology 5, 3–10.
Habitat fragmentation and native bees: a premature verdict?Crossref | GoogleScholarGoogle Scholar |

Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18, 237–268.
Inbreeding depression and its evolutionary consequences.Crossref | GoogleScholarGoogle Scholar |

Chia KA, Koch JM, Sadler R, Turner SR (2015) Developmental phenology of Persoonia longifolia (Proteaceae, R.Br.) and the impact of fire on these events. Australian Journal of Botany 63, 415–425.
Developmental phenology of Persoonia longifolia (Proteaceae, R.Br.) and the impact of fire on these events.Crossref | GoogleScholarGoogle Scholar |

Collins BG, Rebelo T (1987) Pollination biology of the Proteaceae in Australia and southern Africa. Australian Journal of Ecology 12, 387–421.
Pollination biology of the Proteaceae in Australia and southern Africa.Crossref | GoogleScholarGoogle Scholar |

Dick CW, Hardy OJ, Jones FA, Petit RJ (2008) Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biology 1, 20–33.
Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees.Crossref | GoogleScholarGoogle Scholar |

Eckert CG (2002) Effect of geographical variation in pollinator fauna on the mating system of Decodon verticillatus (Lythraceae). International Journal of Plant Sciences 163, 123–132.
Effect of geographical variation in pollinator fauna on the mating system of Decodon verticillatus (Lythraceae).Crossref | GoogleScholarGoogle Scholar |

Emery NJ, Offord CA (2018) Managing Persoonia (Proteaceae) species in the landscape through a better understanding of their seed biology and ecology. Cunninghamia 18, 89–107.

Emery NJ, Offord CA (2019) Environmental factors influencing fruit production and seed biology of the critically endangered Persoonia pauciflora (Proteaceae). Folia Geobotanica 54, 99–113.
Environmental factors influencing fruit production and seed biology of the critically endangered Persoonia pauciflora (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Field DL, Ayre DJ, Whelan RJ (2005) The effect of local plant density on pollinator behavior and the breeding system of Persoonia bargoensis (Proteaceae). International Journal of Plant Sciences 166, 969–977.
The effect of local plant density on pollinator behavior and the breeding system of Persoonia bargoensis (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Grobler BA, Campbell EE (2020) Pollinator activity and the fecundity of a rare and highly threatened honeybush species along a highway in the Cape Floristic Region. International Journal of Plant Sciences 181, 581–593.
Pollinator activity and the fecundity of a rare and highly threatened honeybush species along a highway in the Cape Floristic Region.Crossref | GoogleScholarGoogle Scholar |

Krauss SL (1994) Preferential outcrossing in the complex species Persoonia mollis R.Br. (Proteaceae). Oecologia 97, 256–264.
Preferential outcrossing in the complex species Persoonia mollis R.Br. (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 28313937PubMed |

Kunin WE (1997) Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber. Journal of Ecology 85, 225–234.
Population size and density effects in pollination: pollinator foraging and plant reproductive success in experimental arrays of Brassica kaber.Crossref | GoogleScholarGoogle Scholar |

Lamont BB, Klinkhamer PGL, Witkowski ETF (1993) Population fragmentation may reduce fertility to zero in Banksia goodii – a demonstration of the Allee effect. Oecologia 94, 446–450.
Population fragmentation may reduce fertility to zero in Banksia goodii – a demonstration of the Allee effect.Crossref | GoogleScholarGoogle Scholar | 28313684PubMed |

Maynard GV (1995) Pollinators of Australian Proteaceae. Flora of Australia 16, 30–36.

McKenna DJ (2007) Demographic and ecological indicators of rarity in a suite of obligate-seeding Persoonia (Proteaceae) shrubs. PhD thesis, Biological Sciences, University of Wollongong.

Mustajärvi K, Siikamäki P, Rytkönen S, Lammi A (2001) Consequences of plant population size and density for plant–pollinator interactions and plant performance. Journal of Ecology 89, 80–87.
Consequences of plant population size and density for plant–pollinator interactions and plant performance.Crossref | GoogleScholarGoogle Scholar |

Nield AP, Monaco S, Birnbaum C, Enright NJ (2015) Regeneration failure threatens persistence of Persoonia elliptica (Proteaceae) in Western Australian jarrah forests. Plant Ecology 216, 189–198.
Regeneration failure threatens persistence of Persoonia elliptica (Proteaceae) in Western Australian jarrah forests.Crossref | GoogleScholarGoogle Scholar |

Paton DC (1997) Honey bees Apis mellifera and the disruption of plant–pollinator systems in Australia. Victorian Naturalist 114, 23–29.

Rymer PD, Whelan RJ, Ayre DJ, Weston PH, Russell KG (2005) Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae). Biological Conservation 123, 521–532.
Reproductive success and pollinator effectiveness differ in common and rare Persoonia species (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Schurr L, Affre L, Flacher F, Tatoni T, Le Mire Pecheux L, Geslin B (2019) Pollination insights for the conservation of a rare threatened plant species, Astragalus tragacantha (Fabaceae). Biodiversity and Conservation 28, 1389–1409.
Pollination insights for the conservation of a rare threatened plant species, Astragalus tragacantha (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Tierney DA, Ahrens C, Rymer P, Auld TD (2020) The interaction of clonality, breeding system and genomics for a highly threatened plant species and the management implications. Biodiversity and Conservation 29, 3009–3029.
The interaction of clonality, breeding system and genomics for a highly threatened plant species and the management implications.Crossref | GoogleScholarGoogle Scholar |

Trueman S, Wallace H (1999) Pollination and resource constraints on fruit set and fruit size of Persoonia rigida (Proteaceae). Annals of Botany 83, 145–155.
Pollination and resource constraints on fruit set and fruit size of Persoonia rigida (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Wallace HM, Maynard GV, Trueman SJ (2002) Insect flower visitors, foraging behaviour and their effectiveness as pollinators of Persoonia virgata R.Br. (Proteaceae). Australian Journal of Entomology 41, 55–59.
Insect flower visitors, foraging behaviour and their effectiveness as pollinators of Persoonia virgata R.Br. (Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Wilcock C, Neiland R (2002) Pollination failure in plants: why it happens and when it matters. Trends in Plant Science 7, 270–277.
Pollination failure in plants: why it happens and when it matters.Crossref | GoogleScholarGoogle Scholar | 12049924PubMed |