Seed germination biology of the Albany pitcher plant, Cephalotus follicularis
Michael P. Just A , David J. Merritt B C , Shane R. Turner A B C , John G. Conran D and Adam T. Cross A E
+ Author Affiliations
- Author Affiliations
A Centre for Mine Site Restoration, Department of Environment and Agriculture, Curtin University, GPO Box U1987, Bentley, WA 684, Australia.
B Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, WA 6005, Australia.
C The University of Western Australia, School of Biological Sciences, Crawley, WA 6009, Australia.
D ACEBB and SGC, School of Biological Sciences, The University of Adelaide, SA 5005, Australia.
E Corresponding author. Email: adam.cross@curtin.edu.au
Australian Journal of Botany 67(7) 480-489 https://doi.org/10.1071/BT19053
Submitted: 22 March 2019 Accepted: 17 September 2019 Published: 8 November 2019
Abstract
Cephalotus follicularis is an ecologically unique, taxonomically isolated and range-restricted carnivorous plant that occurs exclusively within vulnerable wetland habitats in coastal south-western Australia. Very little is known about the reproductive biology of this iconic plant species, particularly in relation to seed dormancy and the specific requirements for germination. This knowledge gap must be filled to facilitate the establishment of conservation and management initiatives for the species, as Cephalotus is increasingly impacted by habitat loss, alteration to natural hydrological and fire regimes and, in recent times, climatic change. This study aimed to determine the type of seed dormancy that the seeds of Cephalotus possess, determine the optimum conditions required for seed germination, and examine the storage behaviour of seeds. The seeds of Cephalotus are small (1.0 × 0.5 mm), lightweight (0.1 mg) and remain indehiscent within a wind-dispersed hairy achene. Results suggest that the seeds may exhibit some sensitivity to desiccation and appear to be short lived (<12 months) when stored at 23°C. Maximum germination was achieved after 16 weeks incubation at 15°C for seeds removed from the protective outer layer of the achene, while seeds retained within the protective outer layer displayed lower germination success. The post-ripening morphological changes in the embryo, limited response to gibberellic acid, and the long time period required for germination suggests that the seeds exhibit morphophysiological dormancy, with a fraction of seeds remaining dormant for a period of time post-dispersal. These results highlight the importance of limiting hydrological alteration within the few remaining habitats that continue to support Cephalotus, but to ensure its long-term protection, further research focusing on phenology and in situ recruitment is required.
Additional keywords: morphophysiological seed dormancy, narrow-range endemic, Oxalidales, southwest Australia.
References
Auld TD, Bradstock RA (1996) Soil temperatures after the passage of a fire: do they influence the germination of buried seeds? Australian Journal of Ecology 21, 106–109.| Soil temperatures after the passage of a fire: do they influence the germination of buried seeds?Crossref | GoogleScholarGoogle Scholar |
Auld TD, Denham AJ (2006) How much seed remains in the soil after a fire? Plant Ecology 187, 15–24.
| How much seed remains in the soil after a fire?Crossref | GoogleScholarGoogle Scholar |
Baker KS, Steadman KJ, Plummer JA, Merritt DJ, Dixon KW (2005) Dormancy release in Australian fire ephemeral seeds during burial increases germination response to smoke water or heat. Seed Science Research 15, 339–348.
| Dormancy release in Australian fire ephemeral seeds during burial increases germination response to smoke water or heat.Crossref | GoogleScholarGoogle Scholar |
Baskin CC, Baskin JM (2004) A classification system for seed dormancy. Seed Science Research 14, 1–16.
| A classification system for seed dormancy.Crossref | GoogleScholarGoogle Scholar |
Baskin CC, Baskin JM (2014) ‘Seeds: ecology, biogeography, and evolution of dormancy and germination.’ (Academic Press: San Diego, CA, USA)
Bekker RM, Bakker JP, Grandin U, Kalamees R, Milberg P, Poschlod P, Thompson K, Willems JH (1998) Seed size, shape and vertical distribution in the soil: indicators of seed longevity. Functional Ecology 12, 834–842.
| Seed size, shape and vertical distribution in the soil: indicators of seed longevity.Crossref | GoogleScholarGoogle Scholar |
Bradshaw SD, Dixon KW, Lambers H, Cross AT, Bailey J, Hopper SD (2018) Understanding the long-term impact of prescribed burning in mediterranean-climate biodiversity hotspots, with a focus on south-western Australia. International Journal of Wildland Fire 27, 643–657.
| Understanding the long-term impact of prescribed burning in mediterranean-climate biodiversity hotspots, with a focus on south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Carta A, Bedini G, Müller JV, Probert RJ (2013) Comparative seed dormancy and germination of eight annual species of ephemeral wetland vegetation in a Mediterranean climate. Plant Ecology 214, 339–349.
| Comparative seed dormancy and germination of eight annual species of ephemeral wetland vegetation in a Mediterranean climate.Crossref | GoogleScholarGoogle Scholar |
Clarke C, Cross AT, Rice B (2018) Conservation of carnivorous plants. In ‘Carnivorous plants: physiology, ecology and evolution’. (Eds L Adamec, A Ellison) pp. 377–388. (Oxford University Press: London)
Cochrane A, Yates CJ, Hoyle GL, Nicotra AB (2015) Will among-population variation in seed traits improve the chance of species persistence under climate change? Global Ecology and Biogeography 24, 12–24.
| Will among-population variation in seed traits improve the chance of species persistence under climate change?Crossref | GoogleScholarGoogle Scholar |
Conran JG (2004) Cephalotaceae. In ‘The families and genera of vascular plants. Vol. 6. Flowering plants. Dicotyledons: Celastrales, Oxalidales, Rosales, Cornales, Ericales’. (Ed. K Kubitzki) pp. 65–68. (Springer Verlag: Berlin)
Conran JG, Denton MD (1996) Germination in the Western Australian Pitcher Plant Cephalotus follicularis and its unusual early seedling development. Western Australian Naturalist 21, 37–42.
Cronquist A (1981) ‘An integrated system of classification of flowering plants.’ (Columbia University Press: New York)
Cross AT, Merritt DJ, Turner S, Dixon KW (2013) Seed germination of the carnivorous plant Byblis gigantea (Byblidaceae) is cued by warm stratification and karrikinolide. Botanical Journal of the Linnean Society 173, 143–152.
| Seed germination of the carnivorous plant Byblis gigantea (Byblidaceae) is cued by warm stratification and karrikinolide.Crossref | GoogleScholarGoogle Scholar |
Cross AT, Cawthray GR, Merritt DJ, Turner SR, Renton M, Dixon KW (2014) Biogenic ethylene promotes seedling emergence from the sediment seed bank in an ephemeral tropical rock pool habitat. Plant and Soil 380, 73–87.
| Biogenic ethylene promotes seedling emergence from the sediment seed bank in an ephemeral tropical rock pool habitat.Crossref | GoogleScholarGoogle Scholar |
Cross AT, Turner SR, Renton M, Baskin JM, Dixon KW, Merritt DJ (2015) Seed dormancy and persistent sediment seed banks of ephemeral freshwater rock pools in the Australian monsoon tropics. Annals of Botany 115, 847–859.
| Seed dormancy and persistent sediment seed banks of ephemeral freshwater rock pools in the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar | 25660345PubMed |
Cross AT, Paniw M, Ojeda F, Turner SR, Dixon KW, Merritt DJ (2017) Defining the role of fire in alleviating seed dormancy in a rare Mediterranean endemic subshrub. AoB Plants 9, plx036
| Defining the role of fire in alleviating seed dormancy in a rare Mediterranean endemic subshrub.Crossref | GoogleScholarGoogle Scholar | 28948008PubMed |
Cross AT, Barrett MD, Turner SR, Dixon KW, Merritt DJ (2018a) Seed-dormancy depth is partitioned more strongly among habitats than among species in tropical ephemerals. Australian Journal of Botany 66, 230–242.
| Seed-dormancy depth is partitioned more strongly among habitats than among species in tropical ephemerals.Crossref | GoogleScholarGoogle Scholar |
Cross AT, Davis AR, Fleischmann A, Horner JD, Jürgens A, Merritt DJ, Murza GL, Turner SR (2018b) Reproductive biology and prey-pollinator conflicts. In ‘Carnivorous plants: physiology, ecology and evolution’. (Eds L Adamec, A Ellison) (Oxford University Press: London)
Cross AT, Paniw M, Scatigna AV, Kalfas N, Anderson B, Givnish TJ, Fleischmann A (2018c) Systematics and evolution of small carnivorous genera. In ‘Carnivorous plants: physiology, ecology and evolution’. (Eds L Adamec, A Ellison) pp. 120–134. (Oxford University Press: London)
Cross AT, Kalfas N, Nunn R, Conran JG (2019) ‘Cephalotus, the Albany pitcher plant.’ (Redfern Natural History Productions: Poole, UK)
Downes KS, Light ME, Posta M, Kohout L, Van Staden J (2013) Comparison of germination responses of Anigozanthos flavidus (Haemodoraceae), Gyrostemon racemiger and Gyrostemon ramulosus (Gyrostemonaceae) to smoke-water and the smoke-derived compounds karrikinolide (KAR1) and glyceronitrile. Annals of Botany 111, 489–497.
| Comparison of germination responses of Anigozanthos flavidus (Haemodoraceae), Gyrostemon racemiger and Gyrostemon ramulosus (Gyrostemonaceae) to smoke-water and the smoke-derived compounds karrikinolide (KAR1) and glyceronitrile.Crossref | GoogleScholarGoogle Scholar | 23299994PubMed |
Erickson TE, Shackelford N, Dixon KW, Turner SR, Merritt DJ (2016) Overcoming physiological dormancy in seeds of Triodia (Poaceae) to improve restoration in the arid zone. Restoration Ecology 24, S64–S76.
| Overcoming physiological dormancy in seeds of Triodia (Poaceae) to improve restoration in the arid zone.Crossref | GoogleScholarGoogle Scholar |
FAO (2014) ‘Genebank standards for plant genetic resources for food and agriculture.’ Rev. edn. (FAO: Rome)
Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305, 977
| A compound from smoke that promotes seed germination.Crossref | GoogleScholarGoogle Scholar | 15247439PubMed |
Hay FR, Adams J, Manger K, Probert R (2008) The use of non-saturated lithium chloride solutions for experimental control of seed water content. Seed Science and Technology 36, 737–746.
| The use of non-saturated lithium chloride solutions for experimental control of seed water content.Crossref | GoogleScholarGoogle Scholar |
Heibl C, Renner SS (2012) Distribution models and a dated phylogeny for Chilean Oxalis species reveal occupation of new habitats by different lineages, not rapid adaptive radiation. Systematic Biology 61, 823–834.
| Distribution models and a dated phylogeny for Chilean Oxalis species reveal occupation of new habitats by different lineages, not rapid adaptive radiation.Crossref | GoogleScholarGoogle Scholar | 22357726PubMed |
Hong TD, Ellis RH (1996) ‘A protocol to determine seed storage behaviour.’ (International Plant Genetic Resources Institute: Rome)
Jennings DE, Rohr JR (2011) A review of the conservation threats to carnivorous plants. Biological Conservation 144, 1356–1363.
| A review of the conservation threats to carnivorous plants.Crossref | GoogleScholarGoogle Scholar |
Joley DB, Maddox DM, Schoenig SE, Mackey BE (2003) Parameters affecting germinability and seed bank dynamics in dimorphic follicles of Centaurea solstitialis in California. Canadian Journal of Botany 81, 993–1007.
| Parameters affecting germinability and seed bank dynamics in dimorphic follicles of Centaurea solstitialis in California.Crossref | GoogleScholarGoogle Scholar |
Lamont BB, Downes KS (2011) Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa. Plant Ecology 212, 2111–2125.
| Fire-stimulated flowering among resprouters and geophytes in Australia and South Africa.Crossref | GoogleScholarGoogle Scholar |
Lecoufle M (1990) ‘Carnivorous plants care and cultivation.’ (Cassell Publishers Ltd: London)
Long RL, Gorecki MJ, Renton M, Scott JK, Colville L, Goggin DE, Commander LE, Westcott DA, Cherry H, Finch‐Savage WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews of the Cambridge Philosophical Society 90, 31–59.
| The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise.Crossref | GoogleScholarGoogle Scholar | 24618017PubMed |
Lowrie A (2014) ‘Carnivorous plants of Australia – magnum opus.’ (Redfern Natural History Productions: Poole, UK)
Merritt DJ, Kristiansen M, Flematti GR, Turner SR, Ghisalberti EL, Trengove RD, Dixon KW (2006) Effects of a butenolide present in smoke on light-mediated germination of Australian Asteraceae. Seed Science Research 16, 29–35.
| Effects of a butenolide present in smoke on light-mediated germination of Australian Asteraceae.Crossref | GoogleScholarGoogle Scholar |
Merritt DJ, Turner SR, Clarke S, Dixon KW (2007) Seed dormancy and germination stimulation syndromes for Australian temperate species. Australian Journal of Botany 55, 336–344.
| Seed dormancy and germination stimulation syndromes for Australian temperate species.Crossref | GoogleScholarGoogle Scholar |
Metzner K, Gachet S, Rocarpin P, Saatkamp A (2017) Seed bank, seed size and dispersal in moisture gradients of temporary pools in Southern France. Basic and Applied Ecology 21, 13–22.
| Seed bank, seed size and dispersal in moisture gradients of temporary pools in Southern France.Crossref | GoogleScholarGoogle Scholar |
Miller BP, Dixon KW (2014) Plants and fire in kwongan vegetation. In ‘Plant life on the sandplains in Southwest Australia: a global biodiversity hotspot’. (Ed. H Lambers) pp. 147–169. (UWA Press: Perth)
Moore RP (1985) ‘Handbook on tetrazolium testing.’ (International Seed Testing Association: Zurich, Germany)
Pietropaulo J, Pietropaulo P (1986) ‘Carnivorous plants of the world.’ (Timber Press: Portland, OR, USA)
Sandiford EM, Barrett S (2010) ‘Albany regional vegetation survey: extent, type and status.’ (Department of Environment and Conservation: Albany, WA)
Sheldon JC (1974) The behaviour of seeds in soil: III. The influence of seed morphology and the behaviour of seedlings on the establishment of plants from surface-lying seeds. Journal of Ecology 62, 47–66.
| The behaviour of seeds in soil: III. The influence of seed morphology and the behaviour of seedlings on the establishment of plants from surface-lying seeds.Crossref | GoogleScholarGoogle Scholar |
Silberstein RP, Aryal SK, Durrant J, Pearcey M, Braccia M, Charles SP, Boniecka L, Hodgson GA, Bari MA, Viney NR, McFarlane DJ (2012) Climate change and runoff in south-western Australia. Journal of Hydrology 475, 441–455.
| Climate change and runoff in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Turner SR, Commander LE, Baskin JM, Baskin CC, Dixon KW (2009) Germination behaviour of Astroloma xerophyllum (Ericaceae), a species with woody indehiscent endocarps. Botanical Journal of the Linnean Society 160, 299–311.
| Germination behaviour of Astroloma xerophyllum (Ericaceae), a species with woody indehiscent endocarps.Crossref | GoogleScholarGoogle Scholar |
Yeates D (1992) Immature stages of the apterous fly Badisis ambulans McAlpine (Diptera: Micropezidae). Journal of Natural History 26, 417–424.
| Immature stages of the apterous fly Badisis ambulans McAlpine (Diptera: Micropezidae).Crossref | GoogleScholarGoogle Scholar |
