Climatic and photoperiodic effects on flowering phenology of select eucalypts from south-eastern Australia

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Highlights

Abstract

Flowering phenology plays an important role in the plant life cycle as it is sensitive to climate. The timing and intensity of flowering is important for the reproductive success, fitness, survival and diversity of plants. Its study in relation to the environment can therefore aid in understanding the response of species to climate change. Long-term studies examining the relationship between flowering phenology and climate are limited in Australia. This study explores the effect of photoperiod length, temperature and rainfall on flowering duration and intensity of Eucalyptus tricarpa, Eucalyptus microcarpa and Eucalyptus polyanthemos using long term data sets from two locations and the statistical model: generalised additive model for location, scale and shape (GAMLSS). The study further incorporates the phenological response to calibrate the flowering sub-module of the mechanistic model TACA-GEM to investigate the effect of predicted climate change on flowering phenology. Flowering intensity of E. microcarpa increased as temperatures warmed in the months prior to flowering but declined when warmer temperatures occurred in the early stages of bud development. For E. polyanthemos flowering decreased with increases in temperature combined with decreased rainfall and shorter days. Increased rainfall, cooler temperatures and shorter days increased flowering in E. tricarpa. Modelling of species response to climate change showed that decreases in flowering intensity and duration for all three species are likely. The temperature thresholds required for flowering of E. polyanthemos were exceeded under climate change while the requirement for longer days prevented flowering phenology shifting to cooler months. E. tricarpa exhibited a decline in flowering intensity and duration under climate change; however, its requirements for shorter days allowed the species to continue to flower during winter. E. microcarpa displayed no consistent relationship to photoperiod and a decline in flowering intensity and duration under climate change was modelled. The species’ specific responses to photoperiod suggests that flowering asynchrony between the coexisting species may be linked to day length and that the asynchrony will be strengthened under climate change as flowering duration and intensity contract under a warmer and drier climate.

Introduction

Reproductive success of plants is reliant on the timing and intensity of flowering (Griffin, 1980) which in turn is sensitive to climate (Sparks and Carey, 1995). Small changes in climate can alter reproductive events which in turn may affect recruitment success, fitness and survival (Fenner, 1998, Hudson et al., 2009), as well as ecological processes and communities (Dunlop and Brown, 2008, Peñuelas and Filella, 2001). For example, the onset of spring has advanced while the arrival of winter has been delayed due to recent climate warming (IPCC, 2013). This has had an impact on plant phenology (Bradley et al., 1999, Chmielewski and Rötzer, 2001) by causing an advance or delay in spring phenological events (Amano et al., 2014, Menzel, 2002, Menzel et al., 2006, Schwartz, 2003). The impact of changes in the timing of flowering can affect not only individual species but disrupt synchrony with other species (Chuine, 2010, Stenseth and Mysterud, 2002). Flowering synchrony among individuals aids in pollination, gene transfer, and production of strong progenies (Bassett, 2002, Griffin, 1980). Changes in phenology and the development of asynchronies can therefore also lead to negative socio-economic impacts (Peñuelas and Filella, 2001, Prieto et al., 2008). Phenological studies that provide a greater understanding of species’ phenological responses to environmental change are therefore useful for informing conservation, forestry and farming practices (Baumgärtner and Hartmann, 2000, Khurana and Singh, 2001, van Vliet, 2010).

As with almost all other aspects of plant phenology, the flowering behaviour of plants is influenced by a range of environmental signals, including climate (Ashton, 1975, Keatley and Hudson, 2007a), light (Thomas, 2006), phylogeny (Fenner, 1998), competition (Stephenson, 1981), geography (Ashton, 1975, Law et al., 2000), and inflorescence architecture (Primack, 1987, Stephenson, 1981). Of all these signals, light is typically the most influential (Thomas, 2006). Day length or photoperiodic length (sun hours or daylight duration that plants receive in a day; Garner and Allard, 1920) is a major regulator of flowering time which allows a plant to maximise reproduction (Mattson and Erwin, 2005, Richardson et al., 2013). Salisbury (1961) defined this mechanism as photoperiodism which describes the ability of a plant to measure the duration of the photoperiod (i.e. day length) which in turn allows a plant to meet the requirements of natural selection and aid in niche specialisation. Thomas and Vince-Prue (1997) classified plants into five photoperiodic flowering response classes: short-day plants (SDP); long-day plants (LDP); day-neutral plants (DNP); intermediate day plants (IDP); and ambiphotoperiodic-day plants (ADP). For SDP, flowering occurs when night length exceeds a critical length while for LDP flowering is triggered when day length is longer than a critical length. DNP flower irrespective of day/night length while IDP flower only when the day length is neither too long nor short. ADP require a sequence of short and long days to enhance flowering. SDP and LDP's can be either facultative (flowering is stimulated by changes in photoperiod length) or obligate (flowering requires a photoperiodic threshold to be attained) (Thomas and Vince-Prue, 1997). Despite the global importance of light in flowering, a paucity of studies exist on the effect of photoperiod on flowering in the genus Eucalyptus. In the one glasshouse study by Bolotin (1975), (61)% of Eucalyptus occidentalis seedlings raised under 16 h days initiated floral buds by the age of six months while floral buds were absent in control seedlings raised under natural day lengths. These results suggest E. occidentalis falls into the LDP flowering response class and highlight that photoperiod may be an important mechanism in the flowering of some eucalypts.

Heatsum has a major influence on the timing of flowering commencement; flowering will not typically commence until a certain threshold of accumulated temperature or growing degree days has been reached (Wielgolaski, 1999). Keatley et al. (2004a) emphasised the need to identify the appropriate lower and upper threshold temperatures in order to improve our ability for predicting changes in flowering pattern and intensity as temperatures changes with climate change. For the Box-Ironbark species: E. microcarpa, Eucalyptus melliodora, Eucalyptus leucoxylon, Eucalyptus polyanthemos and Eucalyptus tricarpa, flowering typically commences and peaks earlier at sites with warmer temperatures (Keatley and Hudson, 2007b). Moreover, Keatley and Hudson (2000) demonstrated that flowering commencement in E. leucoxylon, E. polyanthemos and E. tricarpa was influenced by the accumulation of minimum and maximum temperature for two months prior to flowering commencement so that warmer locations would reach the required threshold earlier. For E. microcarpa, E. polyanthemos, E. tricarpa and E. leucoxylon, rainfall had a negative influence on flowering when the temperature influence was positive (Hudson et al., 2011a). Hudson and Keatley (2010) identified a positive influence of rainfall on flowering for E. leucoxylon and E. tricarpa. In some cases a rainfall threshold is required before flowering commences (Crimmins et al., 2013, Friedel et al., 1994, Kim et al., 2009, Peñuelas et al., 2004, Prieto et al., 2008). Keatley and Hudson (2007a) showed that temperature and/or rainfall influenced the flowering of 65 plant species of south-eastern Australia.

Eucalypts are widely distributed and economically important species in Australia (Boland et al., 2006, Keatley and Hudson, 2007a). Flowering of eucalypts is generally irregular (Griffin, 1980, Keatley and Hudson, 1998) while regeneration is reliant on the timing and synchrony of species phenological cycles (Semple et al., 2007). Australia contains a large area of temperate forest (Boland et al., 2006) where plant growth patterns and reproduction correlate with the seasonal changes in temperature (Fenner, 1998). In the temperate regions, winter frost and severe summer droughts pose a risk for the growth of some species (Davidson and Reid, 1980, Paton, 1982, Pook et al., 1965) though the effect on flowering phenology is relatively unknown. In south-eastern Australia the average mean temperatures have increased by 0.5 to 1.0 °C since 1901 and between 0.4 and 0.7 °C since the 1950s (Reisinger et al., 2014). Rainfall in the region has also declined since the 1950s by 5 to 25 mm per year with some regions of Victoria showing statistically significant trends in rainfall decline (Reisinger et al., 2014). By the 2080s, climate change in south-eastern Australia may cause up to a 3.0–4.0 °C increase in temperature and a decline in rainfall (Reisinger et al., 2014). The potential for significant changes in flowering phenology in south-eastern Australia exists due to changes in temperature and rainfall. Assessment of species phenological response and its sensitivity to climate may help in identifying species that may be at risk to severe future climatic events (Mazer et al., 2013). However, knowledge gaps in plant phenology in Australia are large compared to the northern hemisphere which has been driven by a lack of extensive research and a long-term datasets which makes it difficult to determine the influence of climate and climate change on species phenology (Chambers, 2006).

Reproductive phenology has not been considered explicitly in the majority of species distribution models although it is clear that species presence is dependent on survival and production of viable seeds in a given area (Chuine and Beaubien, 2001). Statistical modelling approaches are commonly used to model species distributions and can relate the timing of phenological events to climatic factors but are limited in considering phenological constraints on the breadth of a species niche (Chuine et al., 2013). Mechanistic models on the other hand are based on cause-effect relationships between biological processes and some environmental factors and have been used to examine leaf phenology in northern hemisphere species (Caffarra et al., 2011, Chuine et al., 2013, Morin et al., 2009). Mechanistic models have been developed for assessing the impact of climate change on regeneration and distribution of eucalypts in south-eastern Australia but they do not consider flowering phenology (Mok et al., 2012, Rawal et al., 2015).

This study explores the flowering behaviour of three Eucalyptus species of south-eastern Australia in relation to environmental factors using statistical modelling of long term (20, 39 years) flowering datasets across two locations in south-eastern Australia. This study will extend on the previous work for these eucalypts (Hudson et al., 2009, Hudson et al., 2011a) by investigating the influence of photoperiod length in combination with lagged temperature and rainfall effects on flowering intensity and duration, a combination of climatic factors not previously examined. A further extension to the previous studies includes modelling of flowering phenological response to climate change predicted for Australia by the 2080s using a mechanistic model TACA-GEM (Mok et al., 2012, Rawal et al., 2015). The study incorporates a non-linear statistical component to this mechanistic model and attempts to define the flowering phenological response of E. microcarpa, E. polyanthemos and E. tricarpa under a range of climate scenarios. Using this combined approach, this study seeks to predict the possible vulnerability of selected Eucalyptus species to climate change in south-eastern Australia. This study aims to address the following questions: (1) How do lagged temperature and rainfall affect flowering abundance and duration? (2) Is photoperiod an important factor in the flowering phenology of selected species? (3) Does climate change affect flowering phenology and synchrony of the study species?

Section snippets

Species selection

Three Eucalyptus species were selected from dry sclerophyll forest located in the temperate region of south-eastern Australia (Victoria). Two long term (20, 39 years) flowering datasets were available for three co-occurring species E. microcarpa (grey box), E. polyanthemos (red box) and E. tricarpa (red ironbark) which represent the dry open ‘Box-Ironbark forests’ of the warm temperate region of Victoria (Newman, 1961, Orscheg et al., 2011). Annual rainfall in this region ranges from 400 to 1000

Climatic conditions and flowering pattern

Havelock and Rushworth share a similar climate (Fig. 1). Havelock is generally cooler in most months although significant differences were limited to Tmax in November (Kruskal Wallis, P  0.05; Fig. 1). Peak flowering abundance in E. polyanthemos and E. tricarpa were earlier at Rushworth, however, there were no significant differences in flowering duration between locations for any of the species (ANOVA, P > 0.05, Table 1, Fig. 2). Flowering intensity differed significantly between locations

Discussion

Temperature (Chmielewski and Rötzer, 2001, Dai et al., 2013, Wielgolaski, 1999), together with rainfall (Semple and Koen, 2010) and photoperiod length (Fenner, 1998, Vitasse and Basler, 2013) are major contributing factors that drive phenophases of plants. Previous studies on these Box-Ironbark eucalyptus have demonstrated that temperature has the most influential effect on flowering, either alone (Hudson et al., 2009, Keatley and Hudson, 2000) or in combination with rainfall (Hudson and

Conclusion

This study identified photoperiod length and lagged temperature and rainfall as key variables that drive reproductive phenology in three co-occurring eucalypt species. A key finding is the photoperiodic response identified for the first time in the flowering phenology of eucalypts in Australia. Species sensitivity in response to small differences in climate also suggests that flowering phenology is very sensitive to climate in the bud development stage and overall to climatic change. The effect

Acknowledgements

We thank the Department of Environment, Land, Water and Planning, Victoria and AusAID for funding and ongoing support. We also thank the University of Melbourne for logistic support. We thank two reviewers for comments that improved the manuscript

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