MURDOCH RESEARCH REPOSITORY

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Moore, T.L., Ruthrof, K.X., Craig, M.D., Valentine, L.E., Hardy, G.E.St.J. and Fleming, P.A. (2016) Living (and reproducing) on the edge: Reproductive phenology is impacted by rainfall and

canopy decline in a Mediterranean eucalypt. Australian Journal of Botany, 64 (2). pp. 129-141.

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Living (and reproducing) on the edge: reproductive phenology is impacted by rainfall and canopy decline in a Mediterranean eucalypt Moore, T. L.1, Ruthrof, K. X. 1, Craig, M. D.1, 2, Valentine, L. E.1, 2, Hardy, G. E. St J.1, Fleming, P. A.1 5

1 State Centre of Excellence for Climate Change, Woodland and Forest Health, School of Veterinary and

Life Sciences, Murdoch University. 2 ARC Centre of Excellence for Environmental Decisions, School of Plant Biology, University of Western

Australia. 10

*Corresponding author: Tracey Moore

Email: t.moore@murdoch.edu.au or mooretraceylee@gmail.com 15

Address: School of Veterinary and Life Sciences,

Murdoch University,

90 South St, Murdoch, 6150,

Western Australia

Phone: 08 93607236 20

Mobile: + (614) 41789815

Abstract

Many of the worlds’ forests and woodlands are currently showing symptoms of declining condition due to a

range of factors, including changing climatic conditions, drought, and insect herbivory. Altered abiotic and 25

biotic conditions can influence the condition of trees which can, in turn, affect tree reproductive cycles.

However, the potential impact of tree decline on reproductive cycles has rarely been examined. This study

investigated the influence of canopy condition on the reproductive cycle of Eucalyptus wandoo in south-

western Australia. Canopy and seed trap monitoring were used to assess bud production, flowering, fruiting

and seed fall over 12 months at 24 sites across two locations (Dryandra Woodland and Wandoo 30

Conservation Park). Time since last fire, rainfall, ambient temperatures and the condition of individual trees

were recorded. We found that bud production, flowering and fruiting was correlated with tree condition:

healthier trees were generally associated with higher reproductive effort. Time since last fire was also

strongly related to the reproductive efforts at both locations. Declining annual rainfall and increased

temperatures also an impact on reproduction, made evident by the aborted flowering in Dryandra Woodland. 35

Decline in tree condition, coupled with changes in climate, have major implications for flowering phenology

of this species and have the potential to alter reproductive effort, recruitment, and future population

dynamics. Consideration of these issues should be incorporated into the conservation management of E.

wandoo and similar Eucalypt species.

40

Keywords: canopy condition, serotiny, weather, tree size, time since last fire, die-off, dieback, forest,

woodland, climate change, drought

Introduction

Declines in the condition of forests and woodlands have become apparent around the world (Reid and 45

Landsberg 2000; Close and Davidson 2004; Allen et al. 2010; Matusick et al. 2012; Brouwers et al. 2013).

These include Phytophthora ramorum-related oak death in Spain and Portugal (Brasier et al. 1993), drought-

induced pine forest death in the United States (Breshears et al. 2005), and drought-related Eucalyptus spp.

mortality in south-western Australia (Matusick et al. 2012; 2013). Canopy loss and death of branches are

symptoms of a decline in tree condition (Carnegie 2007; Matusick et al. 2012) and such symptoms can 50

affect the reproductive phenology of individual trees as well as the structure, functioning and composition of

an ecosystem (Allen et al. 2010). Furthermore, throughout the world, dramatic climatic changes (i.e.

increased ambient temperatures, changes in the amount of rainfall and its seasonality) are occurring

(Klausmeyer and Shaw 2009; Allen et al. 2010), potentially further altering the reproductive efforts of trees

(Ashton 1975; Pook 1986; House 1997; Law et al. 2000; Pau et al. 2011). 55

Eucalyptus wandoo ssp. wandoo (hereafter referred to as E. wandoo) is a smooth-barked serotinous species

endemic to south-west Western Australia (Yates and Hobbs 1997; Doughty 2000). Once covering most of

the Western Australian agricultural zone, much (60%) of the original 218 680 ha range of this tree species

has been cleared for agriculture. Most of the remaining extent occurs in small reserves, roadsides and as 60

isolated paddock trees (Doughty 2000; Wandoo Recovery Group 2006). Over the last few decades, patches

of E. wandoo have shown evidence of a decline in canopy condition (Whitford et al. 2008; Hooper 2009;

Dalmaris 2012; Brouwers et al. 2013). Eucalyptus wandoo canopy decline is patchy and cyclic, differing

from many other eucalypt declines in the south-west Western Australia, where large areas of canopy are lost

(Matusick et al. 2012; Matusick et al. 2013). Reproductive efforts of E. wandoo could be altered by this 65

decline in canopy condition, adding pressure to a species with an already restricted range (Mattiske & Havel

1998; Wandoo Recovery Group 2006). Furthermore, this may have effects on the wider ecosystem as

previous studies have noted that the decline in E. wandoo condition can affect woodland fauna and its

habitat (Moore et al. 2013a; Moore et al. 2013c; Moore et al. 2013b; Moore et al. 2014) and lack of

recruitment therefore can have long term effect on the overall biodiversity of an area. 70

Tree decline, weather and fire regimes have the ability to significantly affect the reproductive efforts of

eucalypts. Several studies have noted the effects of many climatic and environmental factors on the

production of flowers, fruits, and seeds over the long life spans of eucalypt species, which often exceed 200

years (Ashton 1975; House 1997; Brookshire et al. 1999). The biodiversity hotspot in south west Western 75

Australia, where E. wandoo is endemic (Klausmeyer et al. 2011), has recently been experiencing extreme

weather conditions including high temperatures and below average rainfall (Bureau of Meteorology 2010).

Additionally, prescribed burning, a biodiversity management tool, is frequently used to reduce the risk of

large scale wildfires (Burrows and Abbott 2003). The frequency or season of prescribed burns have the

potential to alter the reproductive effort of E. wandoo, as fire is a stimulant of seed germination and 80

flowering in many tree species (Pyke 1983; Burrows et al. 1990; Burrows and Abbott 2003; Lamont and

Downes 2011). Together fire and climate may influence reproductive efforts in these trees.

Current published work on the flowering phenology of E. wandoo is limited to the pollen-mediated gene

flow of the species (Byrne et al. 2008). Given the lack of information on the reproductive effort of E. 85

wandoo and how it is influenced by climatic and environmental factors, a greater understanding E. wandoo

flowering phenology is needed if remaining populations are to be effectively managed. In this study we

asked:

a. is the reproductive effort of E. wandoo related to rainfall and ambient temperature?

b. if the reproductive effort (i.e. budding, flowering, fruiting and seed fall) of E. wandoo is influenced 90

by canopy condition?

c. does time since last fire influence reproductive effort in E. wandoo?

Methods

Site description 95

Study sites were located in two locations, Dryandra Woodland (DW) (32° 48′ S, 116° 53′ E) and Wandoo

Conservation Park (WCP) (31° 54′ S, 116° 27′ E), 160km south-east and 75km east of Perth, Western

Australia, respectively. At each location, 12 sites were located in pure E. wandoo stands (total n = 24 sites).

Eucalyptus wandoo stands are generally open with an understorey comprised of Gastrolobium spp.,

Macrozamia riedlei, Xanthorrhoea preissii and a grassy herb layer (Yates and Hobbs 1997). Land clearing, 100

stock grazing, timber harvesting (logging) and prescribed burns have occurred in both locations (Department

of Conservation and Land Management 1980). Sites were initially selected using Landsat data (1999-2009)

and VegMachine (Commonwealth Scientific and Industrial Research Organisation 2010), a program that

calculates changes in vegetation reflectance over time and which can quantitatively identify healthy and

declining stands of trees. Following initial site selection, on-ground measures of tree condition were used to 105

classify sites as either healthy or declining. A healthy site was defined as one with predominately healthy

trees (trees with <50% canopy decline), whilst declining sites were composed predominately of trees in

decline (trees with >50% canopy decline). It must be noted that both healthy and declining trees were

evident at all sites, due to the spatially patchy nature of E. wandoo decline. Final site selection resulted in a

50:50 mix of healthy and declining sites. 110

Weather conditions

For comparison with the tree reproductive effort variables in this study, monthly rainfall (mm), and

minimum and maximum monthly temperature (°C) averages were downloaded from the Bureau of

Meteorology (Bureau of Meteorology 2009) database for Narrogin and York weather stations (Narrogin 115

station: 010614, 40 km from DW; York station: 010311, 40km from WCP) for the duration of this study and

to obtain long term averages (Narrogin/DW: 1913-2013, York/WCP: 1996-2013). Available total annual

rainfall and monthly minimum and maximum temperature (°C) data were also downloaded for 13 years

(1997-2010) for Narrogin/DW and 19 years (1991-2010) for York/WCP. Mean, 95% confidence intervals

(CI), and minimum and maximum values were calculated for each weather variable (Table 1). Independent 120

t-tests were performed to compare monthly rainfall, and minimum and maximum monthly temperature

between long term averages and averages during this study (IBM 2012). Statistical analysis was not

performed for summer rainfall averages as data were too sparse.

Reproductive effort 125

Two methods, canopy monitoring and seed trapping, were used to record the reproductive efforts of E.

wandoo trees over a 12-month period. Canopy monitoring involved recording the reproductive effort of 144

trees (six trees at each site, each >20cm diameter at breast height, DBH) over ten sampling events at near

monthly intervals (May 2010 - April 2011, excluding August and December), by estimating the percentage

of canopy that was: a) budding, b) flowering, and c) fruiting. Values were estimated from the same location 130

on the ground (by Tracey Moore) by visual assessment using binoculars (10 x 42, Nikon Monarch

Binoculars). Reproductive effort values measured over the year were summed to create a single value for

each of the 144 trees which was then arcsine square root-transformed to meet the assumptions of parametric

statistics (Zar 1998).

135

Seed trapping was commenced in June 2010 at each of the 24 sites when two seed traps were placed

randomly underneath the same E. wandoo tree, a tree that were also being canopy-monitored, making a total

of 48 seed traps. Seed traps were not placed under a tree if that tree had started to flower (this study

commenced just as E. wandoo was observed flowering in the area) or if its canopy overlapped with an

adjacent tree, to ensure samples were from one tree and the start of the flowering event was captured. Seed 140

traps were made from a steel ring (0.44m-diameter, 0.15m2 opening) and canvas cone (0.30m-deep) held

approximately 0.4m from the ground through attachment to three metal fence dropper posts (Yates et al.

1994). Petroleum jelly was applied to the three droppers as a deterrent to terrestrial invertebrates entering

the traps and removing seeds. Seed traps collected all leaves, sticks, buds, opercula, flowers, and fruits of E.

wandoo and were emptied nine times between July 2010 and April 2011 into labeled paper bags. The 145

biomass of each collection was dried at 40°C for 24h before being sieved and weighed. We classified the

range of reproductive tissue types collected from the seed traps into the following categories: a) failed

flowering effort; b) flowering effort; and c) aborted fruit, listed below;

a. Failed flowering effort - determined by the total mass (g) of unopened and aborted buds with 150

opercula still attached;

b. Flowering effort - represented by the total mass (g) of opercula collected (eucalyptus buds are

capped by an operculum, which is dropped as the flower opens; (opercula production is a good

indicator of the amount of flowering that occured; Semple et al. 2007); and

c. Aborted fruit - determined by the total mass (g) of unopened fruit (generally very desiccated, and 155

unlikely to hold viable seeds).

Values for each of the above reproductive effort variables were summed across the entire seed trap

monitoring period and across both seed traps to create a single value for each tree (24 trees), and arcsine

square root-transformed to meet the assumptions of parametric statistics (Zar 1998).

160 Time since last fire

Year since last fire for each site was taken from Department of Parks and Wildlife (DPaW) databases

(available from the staff at the Perth Hills and Great Southern Districts, DPaW, Western Australia). Details

on the types of fires that occurred in these areas are limited, but the majority were low, cool fires designed

reduce the fuel load in the understorey layer (prescribed burns). 165

Tree condition

A range of tree condition characteristics were estimated once for each of the 144 trees prior to the

reproductive effort monitoring (and again in 2011 on a selection of trees; Stuart 2011). USDA tree

condition assessment is a measure of tree condition characteristics originally designed and used in the USA 170

for Pinus spp. (Schomaker et al. 2007) but a range of measures can be adapted to the assessment of

eucalypts, including crown density and crown dieback. Crown density was the percent crown that contained

foliage, branches, and reproductive structures. Crown dieback was the percent crown that has undergone

recent dieback, or lost foliage. Canopy cover was estimated by taking four canopy cover measurements

1.5m from the base of each tree at north, south, east and west directions using a spherical densitometer and 175

averaged for the tree to give a single value (Lemmon 1956). Lastly, we estimated the percent of dead

branches, or the percentage of all major branches with a diameter >20 cm that are senescent, as these

characteristics have been used in other studies to investigate the relationships between tree condition and

wildlife species richness and abundance (Wentzel 2010). All these percentage values were expressed as

proportions and arcsine-square-root transformed (Zar 1998). These condition values remained constant 180

throughout the study and were also unchanged the following year (condition values on the same trees in the

following year were unchanged; Stuart 2011).

Analyses 185

Relationships between the reproductive effort of each of the 144 trees (six trees in each of the 24 sites), and

tree condition and time since last fire were analysed using generalised additive mixed models (GAMMs;

REML-restricted maximum likelihood). Dependent reproductive effort variables for canopy monitoring

were the arcsine square root-transformed values for the proportion of the canopy budding, flowering, or

fruiting. Initial analyses found location (Dryandra Woodland or Wandoo National Park) was a significant 190

variable so the two locations were analysed separately. Site (1-24) and tree (1-6) variables were nested in

each model. Fixed variables in each model included time since last fire, crown density, crown dieback,

proportion of dead branches, and canopy cover. None of these fixed independent variables were highly

correlated (r ≥ 0.40) so all variables were retained (Pearson’s r; Microsoft Excel; Appendix 1). The number

of independent variables varied between 1 and 5 in each model, but a maximum of five independent 195

variables were used in each model so as not to exceed the ratio of independent factors to replicates, to avoid

over-fitting, and strive for parsimony in terms of numbers of parameters (Burnham and Anderson 2002). A

total of 30 models were created for each dependent variable, capturing combinations of all parameters.

Seed trap monitoring was similarly analysed using GAMMs to explore the relationships between the 200

reproductive effort for each of the 24 trees, and tree condition and time since last fire. Dependent variables

were the total mass of flowering effort, failed flowering effort or aborted fruit. The two locations, Dryandra

Woodland and Wandoo National Park were again analysed separately and the five fixed variables were the

same as for the previous analysis. Data were not nested for this analysis as there was only one tree at each

of the 24 sites that underwent seed trap monitoring. The number of independent factors varied between 1 205

and 3 in each model, but a maximum of 3 independent variables were used in each model so as not to exceed

the ratio of independent factors to replicates, to avoid over-fitting, and strive for parsimony in terms of

numbers of parameters (Burnham and Anderson 2002). A total of 24 models were created for each

dependent variable, capturing combinations of all parameters.

210

An adjusted R2-value was calculated for each model as well as standardised β and P-values for each

parameter within those models. The standardised β coefficients are the regression coefficients when first

standardising all of the variables to a mean of 0 and a standard deviation of 1, and indicate the relative

contribution of each independent variable (e.g. crown density) in the prediction of the dependent variable

(e.g. proportion of canopy budding) (Statistica 9, Statsoft, Melbourne, Vic., Australia). When a 215

standardised β value was insignificant in a model, the model was compared against the same model, but

excluding that parameter. Only models with a ∆AICc of <4, models with considerable empirical support,

were considered further. The AICc model weight (ωi) was calculated for each of the models; ωi values

therefore indicate the likelihood that each model is the best model to describe the data. Model-averaged β

values (Ʃ β *wi; Burnham and Anderson 2002) were calculated to determine the importance of each habitat 220

variable in the prediction of the dependent variable. Only the most significant relationship was graphed as

scatterplots for each reproductive effort variable, using the transformed values.

Results 225

Weather conditions

Over the year-long monitoring period, average monthly maximum temperatures ranged from 15 to 35°C,

while average monthly minimum temperatures ranged from 1 to 16 °C. Maximum monthly temperatures

were recorded at both locations in January 2011 (Figure 1). The majority of rainfall (>80mm) fell in June

2010 in WCP, and March and July 2010 in DW. Summer rainfall is a common occurrence in both locations 230

(12 of the last 16 years at WCP and 13 of the last 21 years at DW have recorded >20mm summer rainfall)

and there was summer rainfall in both locations in January 2011 (WCP: 49.3mm, DW: 70.0mm; Figure 1).

The study year showed marked differences from previous weather conditions for south-west Western

Australia. The summer of 2009/10 was the driest summer on record with December 2009, January and 235

February 2010 reaching abnormally high temperatures (Bureau of Meterology 2011). Minimal summer

rainfall was noted for January 2010 (DW: 1.60mm WCP: 0.00 mm; Figure 1) and this hot dry spell

(constituting drought conditions; Bureau of Meteorology 2010) continued into 2010, with lower than

average winter rainfall for DW. Both sites recorded hotter maximum temperatures than averages recorded

over the last 15- 20 years (2010 values were above the average 95% CI; Appendix 1), though minimum 240

temperatures for 2010/11 did not differ from the long-term averages. Dryandra Woodland also had

significantly less annual rainfall over 2010/11 compared with the previous 15-20 years, yet WCP received

>100mm rainfall in September 2010 which DW missed out on (Figure 1) and both sites received summer

rainfall. Statistical analysis revealed significant differences in rainfall at DW and temperature averages at

both locations between this study and the long term averages (by t-tests; Appendix 1). 245

250

Dryandra Woodland Wandoo CP

Fig. 1. Monthly rainfall (mm; bar graph) at Dryandra Woodland (DW; a) and Wandoo Conservation Park

(WCP; b), and maximum and minimum monthly average temperatures (°C; line graph) at Dryandra 255

Woodland (c) and Wandoo Conservation Park (d) from January 2010 to April 2011 (monitoring period was

from May 2010 to April 2011) and the respective long term averages (DW: 1913-2013, WCP: 1996-2013)

(Bureau of Meteorology 2009). All values are mean ± SE.

Reproductive effort and weather conditions 260

Our analyses indicated that the reproductive effort of E. wandoo trees was related to weather conditions in

the preceding months with the flowering of E. wandoo trees seemingly following rainfall events. Peak

flowering in WCP occurred in June and November 2010, after significant rainfall events in March (86.3mm)

and September (103.3mm), as well as the usual winter rainfall (Figure 1). Following that, trees went on to

fruit in January-April 2011. Significant flowering in DW was not observed until January 2011 after 16.8 265

mm of summer rainfall occurred in the fortnight prior (70mm of rainfall was recorded for January 2011, an

above average rainfall; Figure 1). Some trees in DW went on to fruit after the summer flowering event but

not with the same intensity as trees in WCP (Figure 2).

Monitoring period Monitoring period

270

Fig. 2. The percentage of canopy that was budding, flowering or fruiting as measured by the monthly

canopy monitoring of E. wandoo trees in 24 sites at Dryandra Woodland (a) and Wandoo Conservation 275

Park (b) from May 2010 to April 2011 (ten monitoring events). The mass (g) of failed flowering effort

indicated by aborted or unopened bud, flowering effort indicated by opened bud and aborted fruit as

measured by the seed trap monitoring of 24 trees in Dryandra Woodland (c) and Wandoo Conservation

Park (d), from July 2010 to April 2011 (nine monitoring events). Values are mean ± SE.

280

Eucalyptus wandoo reproductive effort

Budding differed between locations. Although an average 50% of E. wandoo canopies budded between May

and December 2010, the proportion was greater in DW than WCP. The proportion of canopy flowering also

varied markedly between locations (Figure 2a and b). There was minimal flowering at DW until a peak in

January 2011 (Figure 2a) whereas, in contrast, at WPC, 6-12% of E. wandoo canopies flowered between 285

June and November 2010 (Figure 2b). The percentage of canopy fruiting varied between the two locations

(Figure 2). From February 2011 till the completion of this study (March 2011), only 5-10% of canopies in

DW showed fruiting compared to 25 -30% of the WCP canopies (Figure 2a and b).

Canopy monitoring data was supported by seed trap data, with significant effects of time of year on 290

flowering effort, failed flowering effort, and aborted fruit (Figure 2c and d). Flowering effort decreased

from the commencement of the study, followed by an increase after January 2011 in WCP (Figure 2b).

Dryandra Woodland Wandoo CP

Failed flowering efforts peaked at the commencement of the monitoring period with a continual decrease at

DW but a second peak in April 2011 at WCP (Figure 2c and d). Trees in both locations aborted fruit,

although the mass of aborted fruit was consistently < 0.2 g (Figure 2c and d). Trees aborted fruit at different 295

times (Figure 2c and d). No seeds were collected from seed traps during this study.

Reproductive effort and tree condition

Reproductive effort in terms of budding was correlated to the condition of E. wandoo trees (Table 1 and 2)

as estimated by canopy monitoring. In DW, greater percentages of budding were seen on E. wandoo trees 300

with less canopy cover (Figure 3a), fewer dead branches and higher crown density (Table 1 and 2). In WCP,

budding was more common on trees with sparser canopies and fewer dead branches (Table 1).

Eucalyptus wandoo trees showing generally fewer signs of decline flower more often and had fewer failed

flowering events. Based on canopy monitoring, a greater proportion of flowering in the canopy in DW 305

occurred in sites with less canopy cover (Figure 3c) and fewer dead branches (Table 1). Based on seed trap

monitoring, a larger mass of flowering effort was recorded on E. wandoo trees in DW with fewer signs of

canopy loss or dead branches (Figure 4a) and full crowns (Table 2). At WCP E. wandoo trees with fewer

dead branches, or signs of crown loss, and fuller canopies showed greater flowering events (Table 1).

Similarly, as measured by the seed trap monitoring, a larger mass of flowering effort occurred in WCP in E. 310

wandoo trees with fuller canopies (Table 2). Failure to flower in DW occurred on E. wandoo trees with less

canopy cover and more crown retraction (Table 2). Results were similar in WCP with more failed attempts

to flower in E. wandoo trees with sparser canopies (Figure 4f) and more crown dieback and canopy loss

(Table 2).

315

In both locations E. wandoo trees in good condition fruited more often. Eucalyptus wandoo trees with denser

crowns (Figure 3e) and fewer signs of tree decline showed the highest fruiting values in DW (Table 1). In

WCP, trees with few dead branches (Figure 3f) and minimal crown dieback also showed the greatest

percentages of fruiting in the canopy (Table 1). For both locations, fruiting occurred primarily in trees with a

canopy cover of 40-60% which is considered of average canopy condition (Table 1). In terms of aborted 320

fruit, at DW E. wandoo trees with full canopies containing few dead branches (Figure 4c) had higher masses

of aborted fruit. Whereas in WCP E. wandoo trees with signs of canopy loss and larger percentages of dead

branches (Figure 4d; Table 2), had larger masses of aborted fruit. Summarizing that in DW fruit aborted

more often on E. wandoo trees with a full canopy but with some dead branches, whereas in WCP fruit was

aborted more commonly on E. wandoo trees in poor condition with more dead branches and crown loss. 325

Table 1: Generalised additive mixed models investigating the relationship between reproductive effort from canopy

monitoring, and tree condition, and time since last fire variables

Only those models with an Akaike information criterion adjusted for small sample size (AICc) of <∆4 of the best model are 330 shown (these models have the greatest likelihood of all model-sets to best describe the dataset). Models are ranked according to

their ∆AICc and the AICc model weight (wi); variables are listed in order of terms of decreasing absolute standardised β values.

Models for the percentage of the canopy budding, flowering or fruiting of Eucalyptus wandoo at 24 sites in Dryandra Woodland

and Wandoo Conservation Park, and tree condition, and time since last fire (fixed variables). Abbreviations for independent

variables: canopy cover (CC), time since last fire (TSLF), proportion of dead branches (PDB), crown dieback (DB) and crown 335 density (CD). Values for nested variables, site and tree (six trees per site, 144 trees in total) are not presented.

Reserve Canopy measure Model Adjusted

R2 ΔAICc w i

Dryandra Woodland

Bud CC + TSLF 0.11 0.00 0.23

CC 0.08 0.26 0.20

CC + PDB 0.11 1.23 0.12

CC + TSLF + PDB 0.13 1.91 0.09

CD + CC 0.10 2.10 0.08 Flower CC + PDB 0.12 0.00 0.31

CC 0.08 0.40 0.26

PDB 0.06 1.48 0.15

CC + PDB+ TSLF 0.12 3.47 0.06 Fruit CD 0.06 0.00 0.41

CD+ DB 0.06 3.03 0.09

CD+ CC 0.06 3.44 0.07

Wandoo Conservation Park

Bud TSLF + PDB 0.12 0.00 0.24

TSLF + CC 0.11 1.04 0.15

TSLF + PDB + CD 0.12 2.23 0.08

TSLF + CD 0.10 2.23 0.08

TSLF + PDB + CC 0.13 2.81 0.06 Flower TSLF + PDB 0.18 0.00 0.21

TSLF + CC 0.17 0.91 0.13

TSLF + DB 0.17 0.92 0.13

TSLF + CD 0.16 1.29 0.11

TSLF + PDB + DB 0.17 2.25 0.07

TSLF + PDB + CD 0.17 2.30 0.07

TSLF + CC + DB 0.18 2.73 0.05

TSLF + PDB + CC 0.18 3.03 0.05 Fruit PDB + DB 0.22 0.00 0.15

CC + PDB + DB 0.25 0.10 0.14

Table 2: Generalised additive mixed models investigating the relationship between reproductive effort from seed trap

monitoring, and tree condition, and time since last fire variables 340 Only those models with an Akaike information criterion adjusted for small sample size (AICc) of <∆4 from the best model are

shown (these models have the greatest likelihood of all model-sets to best describe the dataset). Models are ranked according to

their ∆AICc and the AICc model weight (wi); variables are ordered in terms of decreasing absolute standardised β values. The

mass of the flowering, failed flowering and aborted fruit of Eucalyptus wandoo at 24 sites in Dryandra Woodland and Wandoo

Conservation Park, and tree condition, and time since last fire. Abbreviations for independent variables: canopy cover (CC), time 345 since last fire (TSLF), proportion of dead branches (PDB), crown dieback (DB) and crown density (CD).

Reserve Canopy measure Model Adjusted R2 ΔAICc wi

Dryandra Woodland

Flower PDB + DB + CD 0.83 <0.01 0.66 Failed Flowering TSLF + DB + CC 0.97 <0.01 0.95

Aborted Fruit

PDB + CC 0.13 <0.01 0.18 PDB 0.02 0.11 0.17

Wandoo Conservation

Park

Flower TSLF +CC 0.47 <0.01 0.36

TSLF 0.40 0.08 0.34 Failed Flowering CC + TSLF + DB 0.05 <0.01 0.56

Aborted Fruit

PDB + DB 0.38 <0.01 0.56 PDB 0.25 0.91 0.14

350

Fig. 3. Relationships between reproductive efforts of Eucalyptus wandoo trees, as estimated by canopy 355

monitoring, and tree condition measures and time since last fire. Factors that were significantly correlated

with reproductive effort in Dryandra Woodland were: budding and canopy cover (a), flowering and canopy

cover (c), fruiting and crown density (e). Variables that were significantly correlated with reproductive

effort in Wandoo Conservation Park were: budding and time since last fire (b), flowering and time since last

fire (d) and fruiting and the proportion of dead branches (f). All dots represent the transformed reproductive 360

effort per tree (n = 144) in each location. Note that only the most significant relationships for each measure

of reproductive effort in each location are graphed.

Dryandra Woodland Wandoo CP

365

Fig. 4. Relationships between reproductive effort of Eucalyptus wandoo trees, as measured by seed trap

monitoring, and tree condition and time since last fire. Only the variables showing the most significant

relationships to reproductive effort at each location are graphed. Factors that were significantly correlated 370

with reproductive effort observed in Dryandra Woodland were flowering (a) and aborted fruit (c) and

proportion of dead branches and failed flowering and time since last fire (e). Variables that were

significantly correlated with reproductive efforts in Wandoo Conservation Park were flowering and time

since last fire (b), aborted fruit and proportion of dead branches (d) and failed flowering and canopy cover

(f). All dots represent the average transformed reproductive effort per tree (n = 24). 375

Dryandra Woodland Wandoo CP

Reproductive effort and time since last fire

Time since last fire was correlated to reproductive efforts at both locations (Table 1 and 2; Figures 3b and d,

and 4b and e). In WCP, sites with older fuel loads had higher percentages of canopy with bud and flowers

(Figure 3b and d), and a larger flowering effort as measured by the seed trap monitoring (Figure 4b). The 380

correlations between time since last fire and reproductive efforts at DW were weaker than at WCP, but less

flowering and budding in the canopy was related to older fuel loads (Table 1).

Time since last fire also influenced the failed flowering events in both locations (Table 2). In DW, sites of

older fire ages had fewer failed flowering events (Figure 4e). The inverse was true for WCP, where a larger 385

mass of failed flowering events occurred at sites of older fire age (Table 2). Fruiting or aborted fruit of E.

wandoo canopies in both locations showed no relationships with time since last fire (Tables 1 and 2).

Discussion

Budding, flowering and fruiting was variable over the months, location and sites in this study. There is 390

evidence that tree condition, climate and time since last fire affect the reproductive efforts of E. wandoo.

Reproductive effort and weather conditions

Flowering intensity and frequency in eucalypts varies from year to year (Semple et al. 2007) with rainfall

and temperature variations likely influencing reproductive efforts in many eucalypts as they do in many 395

flowering shrub species (Nagy et al. 2012). The intensity of flowering events in many trees has been shown

to be related to temperature and rainfall (Pfeifer et al. 2006; Hudson et al. 2011), such as drought during the

wet season in the Wet Tropics of Australia (Law et al. 2000). A study on temperate shrubs in Germany

noted that drought and temperature changes extended the occurrence and frequency of flowering in some

shrubs species, although this did depend on shrub or plant size (Nagy et al. 2012). Our results indicated that 400

rainfall and temperature variations likely influencing reproductive efforts in E. wandoo. Rainfall events, in

particular, appeared to be related to flowering attempts in E. wandoo, with trees from both locations

flowering after rainfall. Flowering after rainfall in 2010 was successful at WCP, as fruiting was evident

from January 2011 onwards. However, in DW, flowering was not successful over the 2010 year (with more

aborted flowers, no flowering, and little subsequent fruit), after the lower than average rainfall recorded at 405

DW in winter 2010 (May-June). However, after a summer rainfall event in DW, trees flowered in January.

A number of these trees in DW also went onto fruit after the summer flowering event but not to the same

intensity as trees in WCP; most likely due to the higher than average summer temperatures observed in DW.

It has been noted by apiarists that flowering, and therefore nectar and honey production, in E. wandoo varies

from year to year (Gaynor 2008; Law and Chidel 2008), and these annual variations could reflect rainfall 410

and, perhaps, also temperature. In particular, the flowering attempt at DW coincided with some of the

hottest summer maximum temperatures recorded for the area (up to a maximum 42.2ºC recorded), perhaps

resulting in the lower percentage of fruit seen in canopies at DW compared to WCP. Understanding the

effects of hotter summer temperatures and lower rainfall on E. wandoo flowering is therefore important to

help predict how they may respond to future climate change. 415

Drought and extreme temperatures can interfere with the reproductive cycle of eucalypts, as they do for

many tree species worldwide (Ashton 1975; Pook 1986; House 1997; Law et al. 2000; Pau et al. 2011; Nagy

et al. 2012). Furthermore, phenology is known to be influenced by weather conditions and climate change

(Cleland et al. 2007; Pau et al. 2011; Nagy et al. 2012). Continual changes in weather conditions (and 420

longer term climate change) may alter the reproductive efforts of E. wandoo in the long term (i.e. altering

the flowering time and length, changing the life cycle of pollinators, seed set and the reproduction of the

individual tree; Law and Chidel 2008; Nagy et al. 2012). Apiarists working in our locations observed that

eucalypt flowering events in recent years were diminished compared to the 1930-40s (Gaynor 2008).

Overall, it seems that E. wandoo recover and reproduce poorly from a state of decline if extreme heat and 425

drought occur regularly, leading to E. wandoo mortality and a lack of seed production in surviving trees.

Reproductive effort and tree condition

As previously mentioned, there are many factors that can influence the reproductive efforts of a eucalypt, for

example, rainfall and ambient temperatures (Ashton 1975; House 1997; Brookshire et al. 1999). This study 430

indicated that tree decline is another factor capable of altering the reproduction of eucalypts. Our study

found that reduced reproductive effort (e.g. budding, flowering, failed flowering, fruiting and aborted fruit)

in E. wandoo was strongly linked with decline symptoms (e.g. loss of canopy and more dead branches).

Decline in condition, or the loss of canopy, can reduce the reproductive capacity of eucalypts, often making

them reproductively dormant (Ferretti 1997). Generally, E. wandoo trees with few or no decline symptoms 435

(fewer dead branches and trees with healthy canopy cover) had higher percentages of budding, flowering

and fruiting, and a lower mass of aborted fruit.

Many eucalypts are serotinous, storing their seeds within the canopy for many months, seasons or even years

after a flowering event until suitable conditions for seedling establishment, such as a fire event (Burrows and 440

Abbott 2003), occur (Midgley and Enright 2000; Ruthrof et al. 2002; Cramer and Midgley 2009). No seeds

were recorded in seed traps during this study. The absence of seed fall could indicate that seed was not

formed over the previous year, which is unsurprising given the hot and dry conditions experienced over

summer 2009/10, or that the conditions were not suitable for seed release. Additionally, the lack of fire to

release the serotinous seeds could explain the lack of seeds observed (Gill and McMahon 1986; Lamont 445

1991; Burrows 2008; Lamont and Downes 2011), however, the ability of a tree to produce seeds is also

likely dependent on the canopy condition (Midgley and Enright 2000). Studies in other eucalypt species

have similarly noted that seed fall is highly variable (Semple et al. 2007) and seed fall monitoring over a

longer time frame may be required to better explore relationships between seed fall and canopy condition.

450

Failed reproductive efforts

As observed in this study, high levels of aborted buds and fruit are considered normal in many flowering

species (Stephenson 1981) as long lived plants, such as many eucalypts, have many opportunities to set seed

over the lifespan over 100 years. In many plant species not all buds go on to produce flowers and not all 455

flowers go on to produce fruit (Stephenson 1981), as some plant species reabsorb nutrients and resources

before aborting buds or fruit (Stephenson 1981; Cramer and Midgley 2009). This suggests that premature

abortion of reproductive efforts may be a survival mechanism employed when essential resources are scarce

in the environment (e.g. minimal water or nutrients in times of drought).

460

Reproductive effort and time since last fire

Fire is typically an agent of change that alters the structure of woodlands (Penn et al. 2003; Greenberg and

Waldrop 2008; Close et al. 2009), assists with the regeneration of trees and shrubs by enhancing seed

release and establishment (Burrows et al. 1990; Mercer 1994), and can stimulate flowering in many tree

species (Pyke 1983; Lamont and Downes 2011; Shepherd et al. 2011). Mass recruitment of eucalypts can 465

occur after fire events (Wellington and Noble 1985; Ruthrof et al. 2003). This study produced similar

results to the literature although the results differed between the two locations studied. Wandoo

Conservation Park generally had more budding and flowering in sites with older fire ages whereas sites in

DW with older fire ages had fewer budding and flowering events. The buildup of buds varies between E.

wandoo trees of different post-fire ages until a fire event can stimulate dehiscence of the opercula and 470

flowering. On average the post-fire age at DW is 19 years (range 9-23 years) and at WCP 11 years (range 5-

18 years), indicating that most WCP sites have undergone fires more recently than DW. As previously

stated, regular fire events can stimulate the reproduction and recruitment of many eucalypts (Burrows et al.

1990; Ruthrof et al. 2003), including E. wandoo, resulting in more budding and flowering events as is likely

occurring in WCP. In contrast, less regular fire events, like the situation at DW, may result in less regular 475

reproductive efforts. The same scenario may be relevant for the estimation of failed flowering events in

both locations as our study suggests that failed reproductive efforts may be related to certain fuel ages.

Fruiting, the precursor to seed fall (which did not occur in this study) was unrelated to time since last fire in

this study, indicating that other variables are influencing the fruiting of E. wandoo trees. Future studies

should examine factors that influence seed release from the canopy and seedling recruitment to better 480

understand the role fire can play in the management of the species.

Conclusion

Tree condition, as well as many other weather and habitat variables, can alter Eucalyptus reproduction

(Setterfield and Williams 1996; Law et al. 2000; Birtchnell and Gibson 2006; Semple et al. 2007). We have 485

shown that rainfall is a precursor to flowering events and time since last fire is related to reproductive effort.

While this study is a good starting point, its short sampling period of one year makes it difficult to

understand all the factors that influence reproductive efforts of E. wandoo in DW and WCP. Given the

dearth of studies on E. wandoo, this study, whilst only short-term, provides important insights into the

relationships between E. wandoo condition and reproductive effort. A decline in E. wandoo tree condition 490

influences reproduction and could affect future recruitment, and thus needs to be considered as part of the

conservation management of this species.

495

Acknowledgements

We thank the Holsworth Research Endowment, Wildlife Preservation Society Australia, State Centre for

Excellence of Climate Change, Woodland and Forest Health and Murdoch University for funding this

research. TLM was the recipient of a Murdoch University Research Scholarship for the duration of this

research. Field assistance was gratefully received from many volunteers, particularly Matthew Moore, 500

Bryony Palmer, Tegan Douglas and Kathryn Napier. Thanks is also given to Mike Calver and his advice on

the statistical analyses. This work was carried out with Department of Parks and Wildlife permits

(Regulation 17: SF007629).

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Appendices

Appendix 1: Weather conditions (rainfall and temperature) in Wandoo Conservation Park (WCP) and Dryandra 735 Woodland (DW) from previous years and this study period.

Means, 95% confidence intervals (CI, + and -), maximum and minimum values for the previous 20 years (1991 to 2011) and this

study period (May 2010 to April 2011) for the following weather conditions are described below; annual rainfall (mm), summer

rainfall (mm), maximum and minimum temperaures (°C). Results from an independent t-test comparing the long term and this

studies values for the weather variables except summer rainfall) were insignifcant. Wandoo Conservation Park weather data only 740 dates back to 1997 and is incomplete for some years. Bold indicates where the 2010/11 values fall outside the 95% CI. Summer

rainfall is for January, February and December of the same summer accumulated.

Previous 20 years (1991-2011) Study period

T-test, P value Mean CI -

95% Cl +95% Maximum Minimum

Annual rainfall (mm) WCP 382.41 328.61 508.35 459.90 221.20 427.80 0.22, 0.82 DW 448.61 383.28 325.29 619.50 291.30 239.60 -0.88, 0.38

Summer rainfall (mm) WCP 52.33 10.41 140.16 212.10 3.50 63.90 NA

DW 48.14 11.16 117.95 203.70 4.00 78.00 NA

Monthly maximum temperature (°C)

WCP 25.46 25.16 26.12 26.50 24.80 26.69 0.49, 0.62

DW 22.82 22.42 23.6 23.60 21.60 24.31 0.75, 0.45

Monthly minimum temperature (°C)

WCP 8.53 8.16 9.34 10.80 8.70 9.36 -0.17, 0.86 DW 9.75 9.5 10.3 10.80 9.20 9.85 0.48, 0.63

Appendix 2: Averaged standardised β values of the top models (with a ΔAICc <4) adjusted for small sample size, 745 explaining the percentage of the canopy budding, flowering or fruiting (from the canopy monitoring) at Dryandra

Woodland and Wandoo Conservation Park.

Abbreviations for all variables are as follows: canopy cover (CC), time since last fire (TSLF), proportion of dead branches (PDB),

crown dieback (DB) and crown density (CD).

Reserve Canopy measure CC CD DB PDB TSLF

Dryandra Woodland Bud -0.08 0.02 <0.01 -0.06 <0.01

Flower -0.14 <0.01 <0.01 -0.16 -0.02 Fruit 0.01 0.15 -0.01 <0.01 <0.01

Wandoo Conservation Park Bud -0.05 -0.02 <0.01 -0.02 0.20

Flower 0.03 0.01 -0.02 -0.08 0.25 Fruit <0.01 <0.01 -0.05 -0.07 <0.01

750

Appendix 3: Averaged standardised β values of the top models (with a ΔAICc <4) adjusted for small sample size,

explaining the mass flowering, failed flowering and aborted fruit (from the seed trap monitoring) at Dryandra Woodland

and Wandoo Conservation Park.

Abbreviations for all variables are as follows: canopy cover (CC), time since last fire (TSLF), proportion of dead branches (PDB), 755 crown dieback (DB) and crown density (CD).

Reserve Canopy measure CC CD DB PDB TSLF

Dryandra Woodland

Flower <0.01 0.01 -0.01 -0.17 <0.01 Failed Flowering -0.01 <0.01 0.10 <0.01 -0.10

Aborted Fruit 0.04 <0.01 <0.01 -0.01 <0.01

Wandoo Conservation

Park Flower 0.03 <0.01 <0.01 <0.01 0.22

Failed Flowering -0.09 <0.01 0.04 <0.01 0.08

Aborted Fruit <0.01 <0.01 0.01 0.05 <0.01