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Environmental Factors Influencing Fruit Production and Seed Biology of the Critically Endangered Persoonia Pauciflora (Proteaceae)

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Environmental Factors Influencing Fruit Production and Seed Biology of the Critically Endangered Persoonia Pauciflora (Proteaceae) Folia Geobot https://doi.org/10.1007/s12224-019-09343-6 Environmental factors influencing fruit production and seed biology of the critically endangered Persoonia pauciflora (Proteaceae) Nathan J. Emery & Catherine A. Offord # The Author(s) 2019 Abstract The factors that influence seed production incubated seeds. Our study highlights the importance of and seed dormancy in rare plant species are crucial to ensuring appropriate biotic pollen vectors are present in their conservation yet are often poorly understood. In the local landscape for maximising viable fruit produc- this study, we examined the breeding system and seed tion for this species. In addition, our data indicate that biology of the critically endangered Australian endemic recruitment will most likely occur after the endocarp has species Persoonia pauciflora through a series of exper- suitably weakened, allowing physiological dormancy of iments. Pollinator visitation surveys and manipulative the embryo to be relaxed and germination to commence hand-pollination treatments were conducted to investi- following summer temperatures. gate the breeding system and subsequent seed produc- tion. We used an experimental seed burial to examine Keywords breeding system . endocarp . Leioproctus . the breakdown of the woody endocarp and changes to Persoonia pauciflora . pollination . seed germination germination over time. Seed germination response un- der simulated local seasonal conditions was also exam- ined. Persoonia pauciflora was found to be predomi- nantly pollinated by native bees, and cross-pollinated Introduction flowers produced significantly more mature fruit (18 ± 3%) than self-pollination treatments (2–3%). The aver- Numerous factors operating at a range of spatial scales can age strength of P. pauciflora pyrenes buried in soil affect plant abundance or rarity (Schemske et al. 1994). significantly decreased over two years, from 413.3 ± The most important ecological information for conserving 14.6 N to 130.8 ± 11.8 N. Post-burial seed germination rare species is their reproductive traits, as these are asso- was cyclical, with highest final germination percentage ciated with species persistence in the landscape. The occurring following late-summer exhumations (75 ± 2% regeneration niche, originally defined by Grubb (1977), and 74 ± 14%, respectively). When seeds were incubat- highlights the crucial role of plant reproductive factors for ed under different local seasonal conditions, germina- population persistence, with viable seed production noted tion at local summer temperatures was more likely when as a major component of this niche. Important consider- compared with autumn/spring and winter temperature- ations include both species and environmental factors that influence seed production, such as breeding system and : pollen vectors. The potential for flow-on effects from seed N. J. Emery (*) C. A. Offord production means that subsequent factors associated with The Australian PlantBank, The Australian Botanic Garden Mount successful seedling establishment, such as seed dormancy Annan, Royal Botanic Gardens and Domain Trust, Mount Annan, NSW 2567, Australia and germination, are also key traits that define the repro- e-mail: [email protected] ductive niche (Grubb 1977; Bykova et al. 2012;Jiménez- N. J. Emery and C. A. Offord Alfaro et al. 2016). Seed bank dynamics are a particularly partially removed (Bauer et al. 2004;Chiaetal.2016b). important inclusion in threatened species management, as Within the endocarp is one or two seeds, comprising an dormant seeds and adult plants are affected by different outer testa that holds an embryo and cotyledons. Some suites of external environmental stresses (Pavlik et al. Persoonia species have a physiologically dormant em- 1993; Donohue et al. 2010). If the requirements for seed bryo that requires specific environmental cues (i.e. tem- germination are ascribed to specific triggers, such as the perature and moisture) for germination (Bauer and chemical stimulants in smoke, for example, then popula- Johnston 1999). Furthermore, if physiological dormancy tions may become locally extinct in areas where those is alleviated, the embryo must then have enough growth triggers, such as fires, are not common in the landscape. potential to break through the endocarp (Nikolaeva 1969). Indeed, changes in any component of a species’ repro- In an ecological context, the window of conditions re- ductive niche could cause range-shifts through population quired for relaxing physiological dormancy in the embryo expansion or extinction, and rare species are likely to be should reflect the local climate, meaning that variation in sensitive to even small changes in the reproduction niche germination may be apparent at fine scales (Jiménez- (Grubb 1977; Bykova et al. 2012). Alfaro et al. 2016). This intricate relationship between The reproductive niche is an especially important con- the endocarp and embryo suggests that Persoonia germi- sideration for Proteaceae, as species from this expansive nation traits – and the seed biology more generally – plant family often exhibit a very low fruit-to-flower ratio, should be examined in both laboratory and field environ- sometimesaslowas0.01%(Carolin1961;Lamontand ments (Baskin et al. 2006;EmeryandOfford2018). Barrett 1988). Although numerous contributing factors Seed burial trialling is a common method to examine have been documented (Groom and Lamont 1998), key the effects of dormancy over time. This is because the knowledge gaps remain. The genus Persoonia is endemic initial age and viability of the seeds are known, allowing to Australia and is a good model in which to study key the effects of the environment on dormancy release and reproductive traits in Proteaceae, as numerous species germination to be interrogated. For example, following have received considerable attention focussed on the a two-year soil burial, Norman and Koch (2008)found mechanisms that affect seed production and germination P. longifolia endocarps did not significantly decline in (Bernhardt and Weston 1996;Weston2003; Rymer et al. hardness, and still required chipping to stimulate 2005;Chiaetal.2016b;EmeryandOfford2018). Several germination. More recently, Chia et al. (2016b)reported species are known to have breeding systems that prefer- the germination of exhumed P. longifolia seeds was entially select outcrossed pollen (Krauss 1994; Cadzow cyclical, and highest following 30 months of burial. It and Carthew 2000; Wallace et al. 2002; Rymer et al. was determined that the combination of endocarp weak- 2005). For example, Krauss (1994) reported 20% of ening caused by significant wet/dry cycles, coupled with outcrossed flowers from P. mollis plants produced mature warm summer temperatures breaking physiological dor- fruit, compared with only 1% of self-pollinated flowers. mancy, allowed seeds to subsequently germinate (Chia Fruit set was also very high in P. rigida when flowers et al. 2016b). Temperature, in particular, has a pivotal were left open to outcrossing (67.4%; Trueman and Wal- role in controlling physiological dormancy, as many lace 1999). This could not be matched by manual cross- species require a period of constant temperatures within pollination, suggesting that manual hand-pollination does a threshold, or the correct alternating temperature pat- not effectively mimic natural pollinator behaviour to tern for relaxing dormancy (Offord and Meagher 2001). achieve similar pollination success (Trueman and Additionally, this temperature window varies according Wallace 1999). Leioproctus (sub-genus Cladocerapis) to the species and the geographic distribution of its bees are widely reported to be frequent visitors to eastern populations. Thompson et al. (1977) illustrated this by Australian Persoonia species (Bernhardt and Weston screening 292 plants for the alternating temperature and 1996; Wallace et al. 2002; Rymer et al. 2005). When light regimes in which germination was promoted. The foraging on Persoonia flowers, Leioproctus bees contact authors noted that the response of species to ex situ the stigma as they collect pollen and nectar, making them conditions reflected the conditions experienced in situ. effective pollinators of the genus (M. Batley pers. comm.). In this way, species could be grouped according to Persoonia fruits contain a woody endocarp, which is habitat (Thompson et al. 1977). In a comprehensive noted as a mechanical dormancy mechanism in the genus, study on 43 species in Western Australia, Bell et al. and germination only occurs if the endocarp is at least (1995) demonstrated that the relationship between Environmental factors influencing fruit production and seed biology of the critically endangered Persoonia... germination and temperature was dependent on a spe- Ironbark (Eucalyptus fibrosa) and Spotted Gum cies’ life history, and suggested that understorey species (Corymbia maculata) woodlands around North were likely to have more specific germination require- Rothbury in the lower Hunter Valley region of NSW ments compared to overstorey species. (Fig. 1). Spatially, the species encompasses a linear With nine species currently threatened, endangered range of 4.3 km, a total area of occupancy of 29 ha, or critically endangered, there are important conserva- and around two-thirds of the plants occur on a single tion outcomes for understanding the link between the private property (Office of Environment and Heritage environment and seed traits in Persoonia (Rymer et al. 2012). Persoonia
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