Sexual dimorphism in the dioecious monocot Lomandra leucocephala ssp. robusta and its potential ecosystem and conservation significance
Jenna T. Draper
A D , John G. Conran A , Nicholas Crouch B , Philip Weinstein A and Bradley S. Simpson C
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, Molecular Life Sciences Building, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia.
B Conservation and Horticulture, Technical and Further Education SA, Urrbrae Campus, 505 Fullarton Road, Netherby, SA 5062, Australia.
C University of South Australia, Clinical and Health Sciences, Health and Biomedical Innovation South Australia, GPO Box 2471, Adelaide, SA 5001, Australia.
D Corresponding author. Email: jenna.draper@adelaide.edu.au
Australian Journal of Botany 68(4) 275-287 https://doi.org/10.1071/BT20006
Submitted: 15 January 2020 Accepted: 31 May 2020 Published: 12 June 2020
Abstract
Dioecious plants constitute 7% of all angiosperm species, yet they occur in many habitat types, partially through the deployment of sexual dimorphisms that assist in reproduction. In the present work, the dioecious monocot Lomandra leucocephala ssp. robusta (Asparagaceae: Lomandroideae) was studied to understand how sexual dimorphisms can assist species conservation and inform us of a species’ potential significance in an ecosystem. Floral display was sexually dimorphic, as male inflorescences were displayed more prominently and more conspicuously in UV range. Male nectar analysed by thin-layer chromatography contained a higher glucose content than female nectar. However, both sexes contained hexose-rich nectar, a common indicator of generalist pollination, which was supported by observations of floral visitors. Floral extract comparison conducted via gas chromatography-mass spectrometry showed that male extracts contained more compounds that potentially convey greater resistance to biotic and abiotic threats. Chemical comparison of leaves by high performance liquid chromatography with peak area ratio analysis revealed this technique could be used as a tool for gender identification of individuals during non-flowering periods. Due to the generalist pollination mechanisms of L. leucocephala ssp. robusta, may have an important role in the conservation and support of local insect populations. The presence of chemical biotic and abiotic resistance may also make L. leucocephala ssp. robusta a significant contributor to the ongoing stabilisation of the sand dunes. Conservation efforts required for L. leucocephala ssp. robusta are likely to be minimal, as pollination services are provided by a diversity of pollinating taxa, including introduced species, which will be abundant regardless of variable flowering periods. Further observational study of L. leucocephala ssp. robusta pollinators and differences in pollinator visitation behaviours between sexes is recommended to better understand efficient pollination for the species, and potentially reveal a greater extent of ecosystem benefit for this species.
Additional keywords: coastal dune ecosystems, dioecy, leaf chemistry, nectar composition.
References
Abrahamczyk S, Kessler M, Hanley D, Karger DN, Müller MPJ, Knauer AC, Keller F, Schwerdtfeger M, Humphreys AM (2017) Pollinator adaptation and the evolution of floral nectar sugar composition. Journal of Evolutionary Biology 30, 112–127.| Pollinator adaptation and the evolution of floral nectar sugar composition.Crossref | GoogleScholarGoogle Scholar | 27747987PubMed |
Ahmad NM, Martin PM, Vella JM (2008) Floral structure and development in the dioecious Australian endemic Lomandra longifolia (Lomandraceae). Australian Journal of Botany 56, 666–683.
| Floral structure and development in the dioecious Australian endemic Lomandra longifolia (Lomandraceae).Crossref | GoogleScholarGoogle Scholar |
Ainsworth C (2000) Boys and girls come out to play: the molecular biology of dioecious plants. Annals of Botany 86, 211–221.
| Boys and girls come out to play: the molecular biology of dioecious plants.Crossref | GoogleScholarGoogle Scholar |
Ashman TL (2009) Sniffing out patterns of sexual dimorphism in floral scent. Functional Ecology 23, 852–862.
| Sniffing out patterns of sexual dimorphism in floral scent.Crossref | GoogleScholarGoogle Scholar |
Bader JC, Van Helden BE, Close PG, Speldewinde PC, Comer SJ (2019) Sheoak woodlands: a newly identified habitat for Western ringtailed possums. Journal of Wildlife Management 83, 1254–1260.
| Sheoak woodlands: a newly identified habitat for Western ringtailed possums.Crossref | GoogleScholarGoogle Scholar |
Bajpai V, Pandey R, Negi MPS, Bindu KH, Kumar N, Kumar B (2012) Characteristic differences in metabolite profile in male and female plants of dioecious Piper betle L. Journal of Biosciences 37, 1061–1066.
| Characteristic differences in metabolite profile in male and female plants of dioecious Piper betle L.Crossref | GoogleScholarGoogle Scholar | 23151795PubMed |
Baker HG, Baker I (1982) Chemical constituents of nectar in relation to pollination mechanisms and phenology. In ‘Biochemical aspects of evolutionary biology’. (Ed. M Nitecki) pp. 131–171. (University of Chicago: Chicago, IL, USA)
Bawa KS (1980) Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11, 15–39.
| Evolution of dioecy in flowering plants.Crossref | GoogleScholarGoogle Scholar |
Bawa KS (1982) Outcrossing and the incidence of dioecism in island floras. American Naturalist 119, 866–871.
| Outcrossing and the incidence of dioecism in island floras.Crossref | GoogleScholarGoogle Scholar |
Bawa KS (1994) Pollinators of tropical dioecious angiosperms: a reassessment? No, not yet. American Journal of Botany 81, 456–460.
| Pollinators of tropical dioecious angiosperms: a reassessment? No, not yet.Crossref | GoogleScholarGoogle Scholar |
Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution 29, 167–179.
| Dioecism in tropical forest trees.Crossref | GoogleScholarGoogle Scholar | 28563295PubMed |
Beach JH (1981) Pollinator foraging and the evolution of dioecy. American Naturalist 118, 572–577.
| Pollinator foraging and the evolution of dioecy.Crossref | GoogleScholarGoogle Scholar |
Bell G (1985) On the function of flowers. Proceedings of the Royal Society of London. Series B, Biological Sciences 224, 223–265.
| On the function of flowers.Crossref | GoogleScholarGoogle Scholar |
Bernardello G, Anderson G, Stuessy T, Crawford D (2001) A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernández Islands (Chile). Botanical Review 67, 255–308.
| A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernández Islands (Chile).Crossref | GoogleScholarGoogle Scholar |
Blüthgen N, Fiedler K (2004) Preferences for sugars and amino acids and their conditionality in a diverse nectar‐feeding ant community. Journal of Animal Ecology 73, 155–166.
| Preferences for sugars and amino acids and their conditionality in a diverse nectar‐feeding ant community.Crossref | GoogleScholarGoogle Scholar |
Borkent CJ, Harder LD (2007) Flies (Diptera) as pollinators of two dioecious plants: behaviour and implications for plant mating. Canadian Entomologist 139, 235–246.
| Flies (Diptera) as pollinators of two dioecious plants: behaviour and implications for plant mating.Crossref | GoogleScholarGoogle Scholar |
Calaça P, Schlindwein C, Bastos E (2018) Discriminating unifloral honey from a dioecious mass flowering tree of Brazilian seasonally dry tropical forest through pollen spectra: consequences of honeybee preference for staminate flowers. Apidologie 49, 705–720.
| Discriminating unifloral honey from a dioecious mass flowering tree of Brazilian seasonally dry tropical forest through pollen spectra: consequences of honeybee preference for staminate flowers.Crossref | GoogleScholarGoogle Scholar |
Cameron M (2006) Nesting habitat of the glossy black-cockatoo in central New South Wales. Biological Conservation 127, 402–410.
| Nesting habitat of the glossy black-cockatoo in central New South Wales.Crossref | GoogleScholarGoogle Scholar |
Caro TM, O’Doherty G (1999) On the use of surrogate species in conservation biology. Conservation Biology 13, 805–814.
| On the use of surrogate species in conservation biology.Crossref | GoogleScholarGoogle Scholar |
Case A, Barrett SCH (2004) Floral biology of gender monomorphism and dimorphism in Wurmbea dioica (Colchicaceae) in Western Australia. International Journal of Plant Sciences 165, 289–301.
| Floral biology of gender monomorphism and dimorphism in Wurmbea dioica (Colchicaceae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Casuga FP, Castillo AL, Corpuz MJT (2016) GC-MS analysis of bioactive compounds present in different extracts of an endemic plant Broussonetia luzonica (Blanco) (Moraceae) leaves. Asian Pacific Journal of Tropical Medicine 6, 957–961.
| GC-MS analysis of bioactive compounds present in different extracts of an endemic plant Broussonetia luzonica (Blanco) (Moraceae) leaves.Crossref | GoogleScholarGoogle Scholar |
Cayenne Engel E, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. American Journal of Botany 90, 1612–1618.
| Linking pollinator visitation rate and pollen receipt.Crossref | GoogleScholarGoogle Scholar | 21653336PubMed |
Chalcoff V, Gleiser G, Ezcurra C, Aizen M (2017) Pollinator type and secondarily climate are related to nectar sugar composition across the angiosperms. Evolutionary Ecology 31, 585–602.
| Pollinator type and secondarily climate are related to nectar sugar composition across the angiosperms.Crossref | GoogleScholarGoogle Scholar |
Chalwatzis N (2013) ‘Simulation of bee-colours II.’ Available at http://www.ultravioletphotography.com/content/index.php/topic/648-simulation-of-bee-colours-ii/ [Verified 24 February 2019]
Charlesworth D (1999) Theories on the evolution of dioecy. In ‘Gender and sexual dimorphism in flowering plants’. (Eds M Gerber, T Dawson, L Delph) pp. 33–60. (Springer: Berlin, Germany)
Choudhry N, Singh S, Siddiqui MB, Khatoon S (2014) Impact of seasons and dioecy on therapeutic phytoconstituents of Tinospora cordifolia, a Rasayana drug. BioMed Research International 2014, 1–11.
| Impact of seasons and dioecy on therapeutic phytoconstituents of Tinospora cordifolia, a Rasayana drug.Crossref | GoogleScholarGoogle Scholar |
Conran JG (1998) Lomandraceae. In 'The families and genera of vascular plants.' (Eds K Kubitzki, H Huber, P Rudall, P Stevens, T Stützel.) Vol. 3 pp. 354–365. (Springer-Verlag: New York, NY, USA)
Collier N (2007) Identifying potential evolutionary relationships within a facultative lycaenid–ant system: ant association, oviposition, and butterfly–ant conflict. Insect Science 14, 401–409.
| Identifying potential evolutionary relationships within a facultative lycaenid–ant system: ant association, oviposition, and butterfly–ant conflict.Crossref | GoogleScholarGoogle Scholar |
Conran JG (2005) Ultraviolet reflectance patterns in some Agapanthaceae, Alliaceae and Amaryllidaceae and their possible significance for pollination. Herbertia 58, 75–90.
Corlett RT (2016) Plant diversity in a changing world: status, trends, and conservation needs. Plant Diversity 38, 10–16.
| Plant diversity in a changing world: status, trends, and conservation needs.Crossref | GoogleScholarGoogle Scholar | 30159445PubMed |
Costich DE, Meagher TR (1992) Genetic variation in Ecballium elaterium (Cucurbitaceae): breeding system and geographic distribution. Journal of Evolutionary Biology 5, 589–601.
| Genetic variation in Ecballium elaterium (Cucurbitaceae): breeding system and geographic distribution.Crossref | GoogleScholarGoogle Scholar |
Cox PA (1981) Niche partitioning between sexes of dioecious plants. American Naturalist 117, 295–307.
| Niche partitioning between sexes of dioecious plants.Crossref | GoogleScholarGoogle Scholar |
Crawford DJ, Anderson GJ, Bernardello G (2011) ‘The reproductive biology of island plants.’ (Eds D Bramwell, J Caujapé-Castells) (Columbia University Press: New York, NY, USA)
Dahlgren RMT, Clifford HT, Yeo PF (1985) ‘The families of monocotyledons: structure, evolution, and taxonomy.’ (Springer-Verlag: Berlin, Germany)
Darbyshire I, Anderson S, Asatryan A, Byfield A, Cheek M, Clubbe C, Ghrabi Z, Harris T, Heatubun C, Kalema J, Magassouba S, McCarthy B, Milliken W, Montmollin B, Lughadha E, Onana J-M, Saïdou D, Sârbu A, Shrestha K, Radford E (2017) Important plant areas: revised selection criteria for a global approach to plant conservation. Biodiversity and Conservation 26, 1767–1800.
| Important plant areas: revised selection criteria for a global approach to plant conservation.Crossref | GoogleScholarGoogle Scholar |
Dawson W, Fischer M, Kleunen M (2012) Common and rare plant species respond differently to fertilisation and competition, whether they are alien or native. Ecology Letters 15, 873–880.
| Common and rare plant species respond differently to fertilisation and competition, whether they are alien or native.Crossref | GoogleScholarGoogle Scholar | 22676338PubMed |
de la Riva EG, Pérez‐Ramos IM, Tosto A, Navarro‐Fernández CM, Olmo M, Marañón T, Villar R (2016) Disentangling the relative importance of species occurrence, abundance and intraspecific variability in community assembly: a trait‐based approach at the whole‐plant level in Mediterranean forests. Oikos 125, 354–363.
| Disentangling the relative importance of species occurrence, abundance and intraspecific variability in community assembly: a trait‐based approach at the whole‐plant level in Mediterranean forests.Crossref | GoogleScholarGoogle Scholar |
Delph LF (2009) Sex allocation: evolution to and from dioecy. Current Biology 19, R249–R251.
| Sex allocation: evolution to and from dioecy.Crossref | GoogleScholarGoogle Scholar | 19321140PubMed |
Dötterl S, Glück U, Jürgens A, Woodring J, Aas G (2014) Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS One 9, e93421
| Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea.Crossref | GoogleScholarGoogle Scholar | 24676333PubMed |
Ecroyd CE (1996) The ecology of Dactylanthus taylorii and threats to its survival. New Zealand Journal of Ecology 20, 81–100.
Edivani VF, Roselaini MDC, Mendes do Carmo R, Neto JNM (2015) Functional dioecy and moth pollination in Cabralea canjerana subsp. canjerana (Meliaceae). Darwiniana 3, 96–107.
Elisens WJ, Freeman CE (1988) Floral nectar sugar composition and pollinator type among New World genera in tribe Antirrhineae (Scrophulariaceae). American Journal of Botany 75, 971–978.
| Floral nectar sugar composition and pollinator type among New World genera in tribe Antirrhineae (Scrophulariaceae).Crossref | GoogleScholarGoogle Scholar |
Ervik F, Tollsten L, Knudsen J (1999) Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae). Plant Systematics and Evolution 217, 279–297.
| Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae).Crossref | GoogleScholarGoogle Scholar |
Faegri K, Van der Pijl L (1979) ‘The principles of pollination ecology.’ (Pergamon Press: Oxford, UK)
Farwig N, Randrianirina EF, Voigt FA, Kraemer M, Bhning-Gaese K (2004) Pollination ecology of the dioecious tree Commiphora guillauminii in Madagascar. Journal of Tropical Ecology 20, 307–316.
| Pollination ecology of the dioecious tree Commiphora guillauminii in Madagascar.Crossref | GoogleScholarGoogle Scholar |
Fromhage L, Kokko H (2010) Spatial seed and pollen games: dispersal, sex allocation, and the evolution of dioecy. Journal of Evolutionary Biology 23, 1947–1956.
| Spatial seed and pollen games: dispersal, sex allocation, and the evolution of dioecy.Crossref | GoogleScholarGoogle Scholar | 20695970PubMed |
Garnock-Jones PJ, Gemmill CEC, Prebble J, Ryan K (2014) New Zealand flowers: what do the birds and the bees see? In ‘Next generation systematics. ASBS Conference’. (Ed. Organising Committee) p. 37. (Australasian Systematic Botany Society: Palmerston North, NZ)
Gerber M (1999) Theories of the evolution of sexual dimorphism. In ‘Gender and sexual dimorphism in flowering plants.’ (Eds M Gerber, T Dawson, L Delph) pp. 97–122. (Springer: Berlin, Germany)
Givnish TJ (1982) Outcrossing versus ecological constraints in the evolution of dioecy. American Naturalist 119, 849–865.
| Outcrossing versus ecological constraints in the evolution of dioecy.Crossref | GoogleScholarGoogle Scholar |
Godley EJ (1979) Flower biology in New Zealand. New Zealand Journal of Botany 17, 441–466.
| Flower biology in New Zealand.Crossref | GoogleScholarGoogle Scholar |
Habib MR, Karim MR (2016) Chemical characterization and insecticidal activity of Calotropis gigantea L. flower extract against Tribolium castaneum (Herbst). Asian Pacific Journal of Tropical Disease 6, 996–999.
| Chemical characterization and insecticidal activity of Calotropis gigantea L. flower extract against Tribolium castaneum (Herbst).Crossref | GoogleScholarGoogle Scholar |
Higham RK, McQuillan PB (2000) Cyathodes divaricata (Epacridaceae) – the first record of a bird-pollinated dioecious plant in the Australian flora. Australian Journal of Botany 48, 93–99.
| Cyathodes divaricata (Epacridaceae) – the first record of a bird-pollinated dioecious plant in the Australian flora.Crossref | GoogleScholarGoogle Scholar |
Hultine KR, Grady KC, Wood TE, Shuster SM, Stella JC, Whitham TG (2016) Climate change perils for dioecious plant species. Nature Plants 2, 16109
| Climate change perils for dioecious plant species.Crossref | GoogleScholarGoogle Scholar | 28221374PubMed |
Kato M, Kawakita A (2004) Plant-pollinator interactions in New Caledonia influenced by introduced honey bees. American Journal of Botany 91, 1814–1827.
| Plant-pollinator interactions in New Caledonia influenced by introduced honey bees.Crossref | GoogleScholarGoogle Scholar | 21652329PubMed |
Kay Q, Lack AJ, Bamber FC, Davies CR (1984) Difference between sexes in floral morphology, nectar production and insect visits in a dioecious species, Silene diocia. New Phytologist 98, 515–529.
| Difference between sexes in floral morphology, nectar production and insect visits in a dioecious species, Silene diocia.Crossref | GoogleScholarGoogle Scholar |
Keiper P, Johnson CN (2004) Diet and habitat preference of the Cape York short-nosed bandicoot (Isoodon obesulus peninsulae) in north-east Queensland. Wildlife Research 31, 259–265.
| Diet and habitat preference of the Cape York short-nosed bandicoot (Isoodon obesulus peninsulae) in north-east Queensland.Crossref | GoogleScholarGoogle Scholar |
Law B, Gonsalves L, Chidel M, Brassil T (2016) Subtle use of a disturbance mosaic by the south-eastern long-eared bat (Nyctophilus corbeni): an extinction-prone, narrow-space bat. Wildlife Research 43, 153–168.
| Subtle use of a disturbance mosaic by the south-eastern long-eared bat (Nyctophilus corbeni): an extinction-prone, narrow-space bat.Crossref | GoogleScholarGoogle Scholar |
Lawton J, Brown V (1994) Redundancy in ecosystems. In ‘Biodiversity and ecosystem function. Vol. 99’. (Eds E Schulze, HA Mooney) pp. 255–270. (Springer: Berlin, Germany)
Lebot V, Lawac F (2017) Quantitative comparison of individual sugars in cultivars and hybrids of taro [Colocasia esculenta (L.) Schott]: implications for breeding programs. Euphytica 213, 147
| Quantitative comparison of individual sugars in cultivars and hybrids of taro [Colocasia esculenta (L.) Schott]: implications for breeding programs.Crossref | GoogleScholarGoogle Scholar |
Lee AT, Macfarlane TD (1986) Lomandra. In ‘Flora of Australia. Vol. 46: Iridaceae to Dioscoreaceae’. (Ed. AS George) pp. 100–141. (Australian Government Publishing Service: Canberra, ACT, Australia)
Lee AT, Macfarlane TD (2017) Lomandra. In ‘Flora of Australia’. (Australian Biological Resources Study, Department of the Environment and Energy: Canberra, ACT, Australia) Available at https://profiles.ala.org.au/opus/foa/profile/Lomandra [Verified 15 August 2019]
Lokvam J, Braddock JF (1999) Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae). Oecologia 119, 534–540.
| Anti-bacterial function in the sexually dimorphic pollinator rewards of Clusia grandiflora (Clusiaceae).Crossref | GoogleScholarGoogle Scholar | 28307711PubMed |
Lord JM, Westoby M (2006) Accessory costs of seed production. Oecologia 150, 310–317.
| Accessory costs of seed production.Crossref | GoogleScholarGoogle Scholar | 16947043PubMed |
Macfarlane TD (1984) Taxonomic classification of the Lomandra odora group (Xanthorrhoeaceae or Dasypogonaceae). Nuytsia 5, 13–24.
Macfarlane TD, Conran JG (2014) Lomandra marginata (Asparagaceae), a shy-flowering new species from south-western Australia. Australian Systematic Botany 27, 421–426.
| Lomandra marginata (Asparagaceae), a shy-flowering new species from south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Main A (1981) Ecosystem theory and function. Journal of the Royal Society of Western Australia 64, 1–4.
Main A (1982) Rare species: precious or dross? In ‘Species at risk: research in Australia’. (Eds R Groves, W Ride) pp. 163–174. (Australian Academy of Science: Canberra, ACT, Australia)
Maron M, Dunn PK, McAlpine CA, Apan A (2010) Can offsets really compensate for habitat removal? The case of the endangered red‐tailed black‐cockatoo. Journal of Applied Ecology 47, 348–355.
| Can offsets really compensate for habitat removal? The case of the endangered red‐tailed black‐cockatoo.Crossref | GoogleScholarGoogle Scholar |
Menzel R, Shmida A (1993) The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a study case. Biological Reviews of the Cambridge Philosophical Society 68, 81–120.
| The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a study case.Crossref | GoogleScholarGoogle Scholar |
Milet-Pinheiro P, Navarro DMDAF, Dötterl S, Carvalho AT, Pinto CE, Ayasse M, Schlindwein C (2015) Pollination biology in the dioecious orchid Catasetum uncatum: how does floral scent influence the behaviour of pollinators? Phytochemistry 116, 149–161.
| Pollination biology in the dioecious orchid Catasetum uncatum: how does floral scent influence the behaviour of pollinators?Crossref | GoogleScholarGoogle Scholar | 25771507PubMed |
Monks A, Burrows L (2014) Are threatened plant species specialists, or just more vulnerable to disturbance? Journal of Applied Ecology 51, 1228–1235.
| Are threatened plant species specialists, or just more vulnerable to disturbance?Crossref | GoogleScholarGoogle Scholar |
Mouillot D, Bellwood DR, Baraloto C, Chave J, Galzin R, Harmelin-Vivien M, Kulbicki M, Lavergne S, Lavorel S, Mouquet N, Paine CET, Renaud J, Thuiller W (2013) Rare species support vulnerable functions in high-diversity ecosystems. PLoS One 11, e1001569
| Rare species support vulnerable functions in high-diversity ecosystems.Crossref | GoogleScholarGoogle Scholar |
Müller H (1873) Ground ivy. Nature 8, 161–162.
| Ground ivy.Crossref | GoogleScholarGoogle Scholar |
Ohya I, Nanami S, Itoh A (2017) Dioecious plants are more precocious than cosexual plants: a comparative study of relative sizes at the onset of sexual reproduction in woody species. Ecology and Evolution 7, 5660–5668.
| Dioecious plants are more precocious than cosexual plants: a comparative study of relative sizes at the onset of sexual reproduction in woody species.Crossref | GoogleScholarGoogle Scholar | 28808545PubMed |
Parsons PA (1958) Evolution of sex in flowering plants of South Australia. Nature 181, 1673–1674.
| Evolution of sex in flowering plants of South Australia.Crossref | GoogleScholarGoogle Scholar |
Pate J, Kopper S (1994) Rare and common plants in ecosystems, with special reference to the south-west Australian flora. In ‘Biodiversity and ecosystem function. Vol. 99’. (Eds E Schulze, HA Mooney) pp. 293–325. (Springer: Berlin, Germany)
Pemberton RW (2010) Biotic resource needs of specialist orchid pollinators. Botanical Review 76, 275–292.
| Biotic resource needs of specialist orchid pollinators.Crossref | GoogleScholarGoogle Scholar |
Petanidou T (2005) Sugars in Mediterranean floral nectars: an ecological and evolutionary approach. Journal of Chemical Ecology 31, 1065–1088.
| Sugars in Mediterranean floral nectars: an ecological and evolutionary approach.Crossref | GoogleScholarGoogle Scholar | 16124233PubMed |
Pickering CM (2001) Size and sex of floral displays affect insect visitation rates in the dioecious Australian alpine herb, Aciphylla glacialis. Nordic Journal of Botany 21, 401–409.
| Size and sex of floral displays affect insect visitation rates in the dioecious Australian alpine herb, Aciphylla glacialis.Crossref | GoogleScholarGoogle Scholar |
Pickering CM, Jordan M, Hill W (2003) Sexual dimorphism and sex ratios of two Australian dioecious species of alpine pineapple grass, Astelia alpina var. novaehollandiae and Astelia psychrocharis (Asteliaceae). Nordic Journal of Botany 23, 225–236.
| Sexual dimorphism and sex ratios of two Australian dioecious species of alpine pineapple grass, Astelia alpina var. novaehollandiae and Astelia psychrocharis (Asteliaceae).Crossref | GoogleScholarGoogle Scholar |
Ramírez N (2003) Floral specialization and pollination: a quantitative analysis and comparison of the Leppik and the Faegri and van der Pijl classification systems. Taxon 52, 687–700.
| Floral specialization and pollination: a quantitative analysis and comparison of the Leppik and the Faegri and van der Pijl classification systems.Crossref | GoogleScholarGoogle Scholar |
Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DFB, Eisenhauer N (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science 336, 589–592.
| Impacts of biodiversity loss escalate through time as redundancy fades.Crossref | GoogleScholarGoogle Scholar | 22556253PubMed |
Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101, 1588–1596.
| The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database.Crossref | GoogleScholarGoogle Scholar | 25326608PubMed |
Richmond CE, Breitburg DL, Rose KA (2005) The role of environmental generalist species in ecosystem function. Ecological Modelling 188, 279–295.
| The role of environmental generalist species in ecosystem function.Crossref | GoogleScholarGoogle Scholar |
RStudio Team (2018) ‘RStudio ver. 1.2.1335 (RStudio: Integrated Development for R, RStudio, Inc.: Boston, MA, USA)
Sakai AK, Weller SG (1999) Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In ‘Gender and sexual dimorphism in flowering plants’. (Eds M Gerber, T Dawson, L Delph) pp. 1–31. (Springer: Berlin, Germany)
Sakai AK, Wagner WL, Ferguson DM, Herbst DR (1995) Origins of dioecy in the Hawaiian Flora. Ecology 76, 2517–2529.
| Origins of dioecy in the Hawaiian Flora.Crossref | GoogleScholarGoogle Scholar |
Samuel de Avila R, Freitas L (2011) Frequency of visits and efficiency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia itatiaiae (Rubiaceae). Australian Journal of Botany 59, 176–184.
| Frequency of visits and efficiency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia itatiaiae (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
Sharma D, Pramanik A, Agrawal P (2016) Evaluation of bioactive secondary metabolites from endophytic fungus Pestalotiopsis neglecta BAB-5510 isolated from leaves of Cupressus torulosa D.Don. 3 Biotech 6, 210
| Evaluation of bioactive secondary metabolites from endophytic fungus Pestalotiopsis neglecta BAB-5510 isolated from leaves of Cupressus torulosa D.Don.Crossref | GoogleScholarGoogle Scholar | 28330281PubMed |
Shmida A, Dafni A (1989) Blooming strategies, flower size and advertising in the ‘lily-group’ geophytes in Israel. Herbertia 45, 111–123.
Short J, Hide A, Stone M (2011) Habitat requirements of the endangered red-tailed phascogale. Wildlife Research 38, 359–369.
| Habitat requirements of the endangered red-tailed phascogale.Crossref | GoogleScholarGoogle Scholar |
Simpson BS, Luo X, Wang J, Song Y, Claudie D, Garg S, Smith N, McKinnon R, Semple S (2015) Development and evaluation of a topical anti-inflammatory preparation containing Dodonaea polyandra extract. Journal of Pharmacy & Pharmaceutical Sciences 18, 578
| Development and evaluation of a topical anti-inflammatory preparation containing Dodonaea polyandra extract.Crossref | GoogleScholarGoogle Scholar |
Smets E, Ronse Decraene L-P, Caris P, Rudall P (2000) Floral nectaries in monocotyledons: distribution and evolution. In ‘Monocots: systematics and evolution.’ (Eds K Wilson, D Morrison) pp. 230–240. (CSIRO: Melbourne, Vic., Australia)
Srivastav A (2019) Nature’s reaction to anthropogenic activities. In ‘The science and impact of climate change’. (Ed. RB Singh) pp. 79–109. (Springer Nature: Singapore, Singapore)
Steudel B, Hector A, Friedl T, Löfke C, Lorenz M, Wesche M, Kessler M (2012) Biodiversity effects on ecosystem functioning change along environmental stress gradients. Ecology Letters 15, 1397–1405.
| Biodiversity effects on ecosystem functioning change along environmental stress gradients.Crossref | GoogleScholarGoogle Scholar | 22943183PubMed |
Sugawara T, Kobayakawa M, Nishide M, Watanabe K, Tabata M, Yasuda K, Shimizu A (2010) Dioecy and pollination of Morinda umbellata subsp. umbellata (Rubiaceae) in the Ryukyu Islands. Acta Phytotaxonomica et Geobotanica 61, 65–74.
Telfer S (2015) ‘Tennyson Dunes Reserve biodiversity action plan.’ (Ecological Evaluation Pty Ltd: Adelaide, SA, Australia)
Tetetla-Rangel E, Dupuy J, Hernández-Stefanoni J (2017) Patterns and correlates of plant diversity differ between common and rare plant species in neotropical dry forest. Biodiversity and Conservation 26, 1705–1721.
| Patterns and correlates of plant diversity differ between common and rare plant species in neotropical dry forest.Crossref | GoogleScholarGoogle Scholar |
Thomson JD (1981) Selection for outcrossing, sexual selection, and the evolution of dioecy in plants. American Naturalist 118, 443–449.
| Selection for outcrossing, sexual selection, and the evolution of dioecy in plants.Crossref | GoogleScholarGoogle Scholar |
Thomson JD, Brunet J (1990) Hypothesis for the evolution of dioecy in seed plants. Trends in Ecology & Evolution 5, 11–16.
| Hypothesis for the evolution of dioecy in seed plants.Crossref | GoogleScholarGoogle Scholar |
Tollsten L, Knudsen J (1992) Floral scent in dioecious Salix (Salicaceae) —a cue determining the pollination system? Entwicklungsgeschichte und Systematik der Pflanzen 182, 229–237.
Utteridge TMA, Saunders RMK (2001) Sexual dimorphism and functional dioecy in Maesa perlarius and M. japonica (Maesaceae/Myrsinaceae). Biotropica 33, 368–374.
| Sexual dimorphism and functional dioecy in Maesa perlarius and M. japonica (Maesaceae/Myrsinaceae).Crossref | GoogleScholarGoogle Scholar |
Vamosi JC, Otto SP (2002) When looks can kill: the evolution of sexually dimorphic floral display and the extinction of dioecious plants. Proceedings. Biological Sciences 269, 1187–1194.
| When looks can kill: the evolution of sexually dimorphic floral display and the extinction of dioecious plants.Crossref | GoogleScholarGoogle Scholar | 12061964PubMed |
Vamosi JC, Vamosi SM, Barrett SCH (2006) Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae). Proceedings. Biological Sciences 273, 2401–2407.
| Sex in advertising: dioecy alters the net benefits of attractiveness in Sagittaria latifolia (Alismataceae).Crossref | GoogleScholarGoogle Scholar | 16928645PubMed |
Vlasáková B, Jarau S (2011) Dioecious Clusia nemorosa achieves pollination by combining specialized and generalized floral rewards. Plant Ecology 212, 1327–1337.
| Dioecious Clusia nemorosa achieves pollination by combining specialized and generalized floral rewards.Crossref | GoogleScholarGoogle Scholar |
Watanabe K, Shimizu A, Sugawara T (2014) Dioecy derived from distyly and pollination in Psychotria rubra (Rubiaceae) occurring in the Ryukyu Islands, Japan. Plant Species Biology 29, 181–191.
| Dioecy derived from distyly and pollination in Psychotria rubra (Rubiaceae) occurring in the Ryukyu Islands, Japan.Crossref | GoogleScholarGoogle Scholar |
Watson DM, Mac Nally R, Bennett AF (2000) The avifauna of severely fragmented, buloke Allocasuarina leuhmanni woodland in western Victoria, Australia. Pacific Conservation Biology 6, 46–60.
| The avifauna of severely fragmented, buloke Allocasuarina leuhmanni woodland in western Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Welsford MR, Hobbhahn N, Midgley JJ, Johnson SD (2016) Floral trait evolution associated with shifts between insect and wind pollination in the dioecious genus Leucadendron (Proteaceae). Evolution 70, 126–139.
| Floral trait evolution associated with shifts between insect and wind pollination in the dioecious genus Leucadendron (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 26593965PubMed |
Wilson SK (2012) ‘Australian lizards: a natural history.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Yu L, Lu J (2011) Does landscape fragmentation influence sex ratio of dioecious plants? A case study of Pistacia chinensis in the Thousand-Island Lake region of China. PLoS One 6, e22903
| Does landscape fragmentation influence sex ratio of dioecious plants? A case study of Pistacia chinensis in the Thousand-Island Lake region of China.Crossref | GoogleScholarGoogle Scholar | 22163011PubMed |
Zhang J, Nielsen SE, Grainger TN, Kohler M, Chipchar T, Farr DR (2014) Sampling plant diversity and rarity at landscape scales: importance of sampling time in species detectability. PLoS One 9, e95334
| Sampling plant diversity and rarity at landscape scales: importance of sampling time in species detectability.Crossref | GoogleScholarGoogle Scholar | 25551824PubMed |
Zhao C, Zayed O, Zeng F, Liu C, Zhang L, Zhu P, Hsu CC, Tuncil YE, Tao WA, Carpita NC, Zhu JK (2019) Arabinose biosynthesis is critical for salt stress tolerance in Arabidopsis. New Phytologist 224, 274–290.
| Arabinose biosynthesis is critical for salt stress tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 31009077PubMed |
Zipkin EF, Andrew Royle J, Dawson DK, Bates S (2010) Multi-species occurrence models to evaluate the effects of conservation and management actions. Biological Conservation 143, 479–484.
| Multi-species occurrence models to evaluate the effects of conservation and management actions.Crossref | GoogleScholarGoogle Scholar |
