Securing Long-Term Floral Resources for the

Honeybee IndustryRIRDC Pub. No. 08/087

08-087covers.indd 2 14/05/2008 3:31:49 PM

Securing Long-Term Floral Resources for the

Honeybee Industry

by David C. Paton

May 2008

RIRDC Publication No08/087 RIRDC Project No UA-66A

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© 2007 Rural Industries Research and Development Corporation. All rights reserved. ISBN 1 74151 675 7 ISSN 1440-6845 Securing Long-Term Floral Resources for the Honeybee Industry Publication No. 08/087 Project No.UA-66A The information contained in this publication is intended for general use to assist public knowledge and discussion and to help improve the development of sustainable regions. You must not rely on any information contained in this publication without taking specialist advice relevant to your particular circumstances.

While reasonable care has been taken in preparing this publication to ensure that information is true and correct, the Commonwealth of Australia gives no assurance as to the accuracy of any information in this publication.

The Commonwealth of Australia, the Rural Industries Research and Development Corporation (RIRDC), the authors or contributors expressly disclaim, to the maximum extent permitted by law, all responsibility and liability to any person, arising directly or indirectly from any act or omission, or for any consequences of any such act or omission, made in reliance on the contents of this publication, whether or not caused by any negligence on the part of the Commonwealth of Australia, RIRDC, the authors or contributors.

The Commonwealth of Australia does not necessarily endorse the views in this publication.

This publication is copyright. Apart from any use as permitted under the Copyright Act 1968, all other rights are reserved. However, wide dissemination is encouraged. Requests and inquiries concerning reproduction and rights should be addressed to the RIRDC Publications Manager on phone 02 6271 4165

Researcher Contact Details David C. Paton School of Earth and Environmental Sciences University of Adelaide, ADELAIDE SA 5005 Phone: 08 8303 4742 Fax: 08 8303 6222 Email: david.paton@adelaide.edu.au

In submitting this report, the researcher has agreed to RIRDC publishing this material in its edited form. RIRDC Contact Details Rural Industries Research and Development Corporation Level 2, 15 National Circuit BARTON ACT 2600 PO Box 4776 KINGSTON ACT 2604 Phone: 02 6271 4100 Fax: 02 6271 4199 Email: rirdc@rirdc.gov.au. Web: http://www.rirdc.gov.au Published in May 2008

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Foreword The Australian honeybee industry depends on floral resources provided by a variety of native and exotic plants. These resources are changing as a consequence of vegetation clearance, dieback of rural trees, improved control of exotic plants, and intensification of agriculture. Climate change also has the potential to affect floral resources. Most Australian beekeepers move their apiaries around rural landscapes to exploit seasonal flushes of flowering. Many have a working knowledge of their resource base but changes in the quantities of flowers being produced from one year to the next, in the frequency of flowering, and impacts of droughts and fires on resources are poorly documented. This project aimed to develop simple methods for recording the flowering of key floral resources that the industry can use to further its understanding of the resources it depends on. An understanding of how resources change in time and space will allow the honeybee industry to identify potential threats and plan its future to minimize the impacts of these. A key component of this study was to establish a number of monitoring programs to document current floral resources used by apiarists to document how these change in the future. Key floral resources used by the honeybee industry in South Australia are sensitive to droughts, producing few flowers in drought years or the following year, in the case of many eucalypts. During years when key resources were flowering extensively, significant quantities of nectar remained unexploited in flowers even near apiaries, suggesting that honeybees are not threatening native flower-visiting fauna at these times. The abundance of nectar in flowers at these times was not caused by an increase in secretion rates but by low visitation rates from native fauna, particularly nectar-feeding birds. These findings should assist the industry in maintaining access to these resources in the future. This report, an addition to RIRDC’s diverse range of over 1800 research publications, forms part of the Honeybee R&D program, and documents the value of native floral resources in rural landscapes in parts of South Australia and how these resources vary from one year to the next and over longer periods of time, and in response to fire and drought. Most of our publications are available for viewing, downloading or purchasing online through our website: • downloads at www.rirdc.gov.au/fullreports/index.html • purchases at www.rirdc.gov.au/eshop Peter O’Brien Managing Director Rural Industries Research and Development Corporation

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Acknowledgments This project was funded by the Rural Industries Research and Development Corporation, with some additional financial support provided by the South Australian Department for Environment and Heritage, the South Australian Department of Water Land and Biodiversity Conservation, and the South Australian Apiarists Association. Joel Allan, Janet Newell, Cassandra Hlava, Caragh Heenan, Lydia Paton, Fiona Paton, Leanne Mladovan, Craig Gillespie and Colin Bailey assisted with field work. Laurie Haegi (DEH), Sean Kennedy (SA Water) and Barry Barrett provided access to Para Woodland, Mt Bold and Bingara respectively. Leigh Duffield and Peter Koch provided information on pollen sources used by their bees at Newland Head and Bingara, and Monarto respectively. Leigh Duffield provided further support by placing an additional apiary at Newland Head Conservation Park in 2006. Joel Allan assisted with producing maps and Joel Allan and Dan Rogers provided constructive comments on drafts of this report.

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Contents Foreword ............................................................................................................................................... iii Acknowledgments................................................................................................................................. iv Executive Summary ............................................................................................................................ vii Introduction ........................................................................................................................................... 1 Objectives............................................................................................................................................... 3 Methods .................................................................................................................................................. 4

Study sites ........................................................................................................................................... 4 Measuring standing crops and production of nectar............................................................................ 5 Flowering levels and phenologies of eucalypts................................................................................... 6 Flowering of other plants .................................................................................................................... 7 Visitation rates to flowers.................................................................................................................... 7 Long-term monitoring programs ......................................................................................................... 8 Assessing the potential for revegetation to provide floral resources for honeybees ........................... 9

Results & Discussion ........................................................................................................................... 11 Nectar production and standing crops ............................................................................................... 11

24 hour production ........................................................................................................................ 11 Standing crops ............................................................................................................................... 13

Flowering of key species of eucalypts............................................................................................... 13 Quantities of flowers produced ..................................................................................................... 13 Individual variation in the timing of flowering ............................................................................. 20

Use of floral resources by honeybees and other fauna ...................................................................... 22 Nectar sources ............................................................................................................................... 22 Pollen sources used by honeybees at study sites ........................................................................... 25

Long-term monitoring of Banksia ornata in Ngarkat Conservation Park.......................................... 28 Responses of plants to other extreme weather events: frosts ............................................................ 31 Baseline monitoring of plants and floral resources on farmland being set aside for restoration....... 31 Floral resources in the future............................................................................................................. 33

References ............................................................................................................................................ 40

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Tables Table 1. Quantities of nectar produced (mg sugar/flower/d) and standing crops of nectar (mg sugar/flower) .

for different species of eucalypts in different environments in South Australia during 2004-2007. 12 Table 2. Maximum floral production levels for a variety of eucalypt species in South Australia.. ............... 14 Table 3. Levels of flowering for eucalypts at three selected sites between 2004 and 2007........................... 18 Table 4. The levels of flowering for Eucalyptus camaldulensis and Eucalyptus leucoxylon are shown for a .. range of sites in South Australia between 2004 and 2007. .............................................................. 19 Table 5. Frequency to visits to flowers of various eucalypts by native birds and honeybees are provided for different settings and in different years in the Mt Lofty Region of South Australia........................ 25 Table 6. Major sources of pollen used by honeybees at selected study sites in the Mt Lofty region.. .......... 26 Table 7. Flowering levels for selected shrubs and herbs used by honeybees as sources of pollen and nectar .. while exploiting floral resources from various species of eucalypt varied between years............... 27 Table 8. Influence of tree density on the shape and surface areas of the canopies of various eucalypts. ...... 39

Figures Figure 1. Location of major study sites in the Mt Lofty region of South Australia. ......................................... 5 Figure 2. Flowering levels in 2004, 2005 and 2006 for three populations of Eucalyptus camaldulensis in ...... South Australia (Baan Hill Soak (top); Cromer CP (mid) and near Meadows (bottom).. ............... 16 Figure 3. Flowering levels for three populations of Eucalyptus in South Australia........................................ 17 Figure 4. Per cent through flowering for populations of Eucalyptus leucoxylon (top) and Eucalyptus

fasciculosa (bottom) in spring 2006 at Scott Conservation Park. .................................................... 21 Figure 5. Percent through the flowering season for a population of Eucalyptus goniocalyx at Para Wirra ....... Recreation Park in March 2005. ...................................................................................................... 22 Figure 6. Annual mortality of Banksia ornata at Ngarkat Conservation Park from 1994 to 2005 ................. 28 Figure 7. Production of inflorescences (cobs) by Banksia ornata .................................................................. 29 Figure 8. Rates of recovery of floral production for populations of Banksia ornata following three fires..... 30 Figure 9. Map showing the location of various eucalypts on the 70 ha Mt Bold site. .................................... 34 Figure 10. Baseline measures of the distribution and abundance (% cover) of Hypochoeris glabra, Echium .... plantagineum, Lissanthe strigosa and eucalypts.............................................................................. 35 Figure 12. Distribution of various species of eucalypts in circa 50 ha at Bingara showing the background ....... distribution of Hypochoeris glabra.................................................................................................. 36

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Executive Summary

What the report is about This report documents the floral resources used by the honeybee industry in rural landscapes of South Australia, particularly the Mt Lofty Ranges. Various species of eucalypt are important sources of nectar for honeybees in this region. A simple method is developed to document the flowering of these plants, allowing spatial and temporal variation in flowering to be documented. The research focussed on documenting nectar production and flowering of key eucalypts and comparing the performances of these plants in remnant native vegetation, with those of trees in paddocks and revegetation. The extent to which paddock trees, trees in revegetation and trees in intact native vegetation were used by honeybees and native fauna particularly native birds is assessed using visitation rates to flowers and from the quantities of nectar left unexploited in flowers at the end of the day. The influences of drought, frost and fire on floral production were assessed at several long-term monitoring sites and used as a basis for predicting likely changes in floral resources for the honeybee industry with climate change. Additional long-term monitoring programs were established on three farms that are being set aside for revegetation to document changes in floral resources through time. Some recommendations on planting densities and species compositions in revegetation programs are made to improve the likelihood that these revegetation programs will provide resources of value to the honeybee industry.

Who is the report targeted at? The report aims primarily to provide information on the use of different floral resources by the honeybee industry, and how the flowering levels of key plant species changes over time and following perturbations like fire and drought. Since fire and drought are more likely in southern Australia due to climate change, monitoring the performances of the plants during and following the current drought, and following recent fires, provides a strong basis for predicting future changes to floral resources.

Background The honeybee industry uses three types of floral resources: a diversity of native plants, a suite of introduced plants that are environmental weeds, and various annual and perennial crops. The value of native plants as floral resources has been eroded in recent years, and is likely to continue to decline, because of vegetation clearance, rural tree decline, and reduced access to crown land. Changes in agriculture practices and intensification may also reduce floral resources to honeybees by eliminating some of the important weed species. Climate change also has the potential to alter flowering levels and performances of these plants. To be able to plan for the future, the honeybee industry needs to better document the floral resources that are currently being used and to establish baselines from which to monitor changes in these resources over time.

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Aims/Objectives The objectives of this project were to:

1. Document the importance of scattered (paddock) trees, trees in natural areas and trees in revegetation areas to the honeybee industry in South Australia.

2. Determine if trees in different landscapes (paddock, woodland, revegetation) or in different condition differ in floral resource production.

3. Document the sources and location of pollen used when honeybees exploit floral resources from trees in rural landscapes.

4. Measure resource share between honeybees and other fauna. 5. Develop a simple method of scoring tree condition and flowering so that beekeepers can

objectively and quantitatively document changes in tree health and annual variation in flowering levels of key eucalypt species through time so they can better track long-term changes in their resource base.

A further key component of this study was to establish and maintain a number of monitoring programs to document current floral resources used by apiarists, and how these change through time particularly with anticipated changes in climate and rural land use.

Methods used Observations of the use of floral resources by honeybees were undertaken at six sites established in the Mt Lofty Ranges of South Australia. The sites included rural areas with scattered trees, areas of intact native vegetation, and areas of revegetation. Counts of honeybees and other insects visiting flowers on marked branches at hourly intervals throughout the day coupled with the time taken to process flowers were used to determine daily visitation rates to flowers. Visitation rates to flowers by birds were determined from the amount of time birds spent foraging on the flowers of marked branches during 30 minute observation periods spread evenly over the day, combined with the time the birds took to probe flowers. Nectar was measured using calibrated capillary tubes to extract and determine the volume of nectar in a flower and a hand-held sugar refractometer used to measure the sugar concentration. The quantities of nectar produced per day were determined by covering flowers with fine voile bags for 24 hours, measuring the accumulated nectar in these flowers, and subtracting the quantity present in samples of flowers taken at the time the flowers were bagged. A simple method of estimating the numbers of flowers produced per unit of canopy, the handspan method, was developed and used for documenting the quantities of flowers produced by plants. The quantities of flowers per handspan were estimated for 25 to 50 individual plants to represent the level of flowering for plant populations at different locations and different times. Abundances of flowers and responses to fire and drought were assessed for Banksia ornata in Ngarkat annually using a series of permanent 50 m x 4 m quadrats. Smaller sized quadrats were used to document floral abundances of other species. The establishment of baseline levels of floral resources in farming areas was done using a GPS to map all the trees. Line transects and 25m x 25m cells were used to document per cent cover or numbers of individuals for understorey species.

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Results/Key findings The quantities of nectar produced over 24 hours were determined for eighteen species of eucalypts, including one natural hybrid. Of the species sampled, four consistently produced more nectar per flower per day than the other species. These species were Eucalyptus angulosa (7.4 – 10.6 mg sugar/flower/day), E. torquata (7.6 – 15.4 mg/fl/d), E. leucoxylon (7.3 – 15.6 mg/fl/d) and E. cosmophylla (9.7 - 18.8 mg/fl/d). Eucalyptus albopurpurea, E cladocalyx, E. diversifolia, E incrassata, a natural E. porosa -E. leucoxylon hybrid, and E. platypus typically produced 2-5 mg/fl/d, while E. baxteri, E. calycogona, E. fasciculosa, E. odorata, E. socialis and E. viminalis typically produced between 0.5 – 2 mg/fl/d. Eucalyptus remota and E. porosa produced <0.5mg/fl/d. The quantities of nectar produced by plants in revegetation, in remnant vegetation or by plants scattered across paddocks were similar. Plants in revegetation programs, therefore, are just as productive as those in intact native vegetation, so revegetation has the potential to replace losses in floral resources. The quantities of nectar remaining in flowers late in the day were often substantial, particularly for Eucalyptus cosmophylla, E. leucoxylon, E. angulosa, E incrassata and E. torquata where there was often more than 1 mg/fl left unexploited. For some species like E. leucoxylon and E. cosmophylla there was often over 5 mg/fl of nectar, even when a commercially-managed apiary was within a few hundred metres. At times these high volumes of nectar were such that nectar dripped from the flowers. This apparent over-production of nectar, however, was not caused by the plants producing more nectar in some years than others but reflected low visitation rates to flowers particularly by native birds. The high quantities of unexploited nectar in flowers indicate that honeybees are unlikely to be affecting the ability of native fauna to harvest nectar from these flowers. Beekeepers, therefore, should be allowed to have continued access to these resources. The rates at which flowers were visited by native fauna and honeybees were assessed for ten species of eucalypts on 33 occasions, across three different settings: remnant vegetation, paddock trees and revegetation. For most species and on most occasions honeybees were more frequent floral visitors than other invertebrates and birds, accounting for more than 100 visits per flower per day for at least three species of eucalypt (E. cosmophylla, E. odorata and E. torquata) on some occasions. For another four species of eucalypts, honeybees made at least five visits per flower per day on most occasions. The other major visitors to flowers were various species of honeyeaters, lorikeets, Silvereyes and Crimson Rosellas, the latter often removing flowers to harvest nectar from them. The rates at which birds visited flowers varied dramatically both within a species and between species, ranging from 0 - 23.4 visits/flower/day. On more than half of the occasions, birds made less than one visit/flower/day suggesting that floral resources often exceeded the numbers of birds available to exploit them consistent with measurements of nectar in flowers. In general, those eucalypts (e.g. E. calycogona, E. fasciculosa, E. odorata) with small flowers and producing low to moderate quantities of nectar (<2mg/fl/d) received 0 - 1.4 visits/flower/day from birds. Those species that had larger flowers and produced higher amounts of nectar (E. cosmophylla, E. leucoxylon, E. torquata) typically had visitation rates ranging from 0.1 - 10 visits/flower/day. For Eucalyptus leucoxylon visitation rates were generally higher in remnant vegetation than in paddock trees or revegetation, particularly in 2004 and 2006 when E. leucoxylon flowered more extensively. This suggests that any potential impact of honeybees on native flora and fauna will be lower for scattered paddock trees. This pattern of reduced use of paddock trees, however, was not seen for either Eucalyptus diversifolia or E. cosmophylla. On two occasions, both involving eucalypts in remnant vegetation, the rates at which birds visited flowers exceeded 20 times per flower per day. These both coincided with times when there were few other plants in flower. Sources of pollen used by honeybees when exploiting floral resources at the study sites were largely confined to one or two species at a site. Key pollen sources being used by the bees were Echium plantagineum, and Hypochoeris glabra, both environmental weeds. Eucalyptus camaldulensis,

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Gonocarpos elatus and Lissanthe strigosa were the native plants that provided some pollen but only at 1 – 2 study sites each. The numbers of flowers produced by different species of Eucalyptus varied dramatically. Some species produced moderately low maximum numbers of flowers (e.g. E. angulosa, E. astringens, E. cosmophylla, E. incrassata and E. torquata) and these tended to be species with larger flowers. Other species with smaller flowers had maximums in excess of 200 flowers per handspan of canopy (e.g. E. baxteri, E. calycogona, E. camaldulensis, E. cladocalyx, E. diversifolia, E. fasciculosa, E. obliqua, E. odorata, E. porosa, and E. socialis). One species, E. leptophylla had over 800 floral units per handspan of canopy. There were also substantial changes. Considerable variation was found in flowering levels (flowers/handspan) between individual plants within the same population and between populations of the same species. For example, the numbers of flowers produced by individual E. camaldulensis varied from <5 to >250 per handspan, an almost 50 fold spread. Despite the broad range in flowering levels there were differences in the spread of flowering levels between years within a site and also between sites in any one year. Eucalyptus leucoxylon flowered extensively in spring 2006 despite a severe drought but most populations did not flower or flowered poorly in 2007, suggesting that droughts may affect subsequent flowering rather than the flowering at the time of the drought. The complexity or variability in the flowering of these plants was increased further by the wide range in the timing of flowering of individual plants within a population. For all of the species of eucalypts that were monitored there were some individual plants within a population that had almost finished flowering while others had barely commenced flowering. This pattern suggests that the timing of flowering within these populations of plants is influenced at least to some extent by genetic differences rather than local environments, since plants a few metres apart should experience similar environments. One outcome of this variability is that moderate to large sample sizes are needed to document flowering seasons adequately. The handspan method that has been developed in this study provides a relatively simple way of estimating floral production for a range of eucalypts that is capable of documenting not just changes in the quantities of flowers being produced from one year to the next, but also the variability that exists within and between populations in floral production. Since the numbers of flowers and not the quantity of nectar produced by flowers is the major variable affecting resource production monitoring the quantities of flowers produced each year over extended periods is required to document changes in resources. South Australian beekeepers will commence monitoring some of their floral resources using this technique in 2008. Long-term monitoring of Banksia ornata at Ngarkat revealed that this species produced far fewer flowers following drought years. Recovery of floral production following a fire in January 1999 was much slower (~ 9 years) compared to recovery following earlier fires in December 1990 and November 1997, suggesting that recent droughts were also affecting post-fire recovery. Low seedling recruitment for Banksia ornata following the January 2006 fire suggests floral resources for this reserve will be even further reduced following this fire. The distributions and abundances of key floral resources being used by honeybees on three farms being set aside for re-establishment of native vegetation were mapped and provide a baseline from which to judge how floral resources change as the new vegetation is established. Trees planted densely (>250 trees/ha) may not be as productive as more widely spaced trees. More widely spaced trees have larger canopy dimensions and may produce more flowers per unit area of canopy, and so be a more valuable resource to the beekeeping industry. The weeds that currently provide significant quantities of pollen to the honeybee industry in these rural landscapes are likely to be eliminated as part of the revegetation works. Suitable native plants that can provide pollen still need to be identified and incorporated into the planting programs.

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Implications for relevant stakeholders The floral resources used by honeybees are sensitive to drought, fire and cold temperatures, and these can affect the quantities of flowers produced for more than just a single flowering season. Given that droughts, fires and extremes in temperature are all likely to increase with climate change, floral resource availability is likely to decline in the future. The honeybee industry is therefore likely to be significantly affected by predicted climate change. Given that significant quantities of nectar were left unexploited in the flowers of key eucalypts even close to apiaries, is consistent with honeybees not having a detrimental effect on native nectarivores. This was particularly true for scattered paddock trees that were used less frequently by nectar-feeding birds than trees in intact native vegetation. In general the low visitation rates by honeyeaters to flowers may indicate that these birds are also vulnerable to the impacts of climate change, and sounds a warning for wildlife managers.

Recommendations The honeybee industry needs to invest in understanding how the floral resources that they currently depend on will respond to climate change. The relatively simple method developed for scoring the flowering performances of native plants, particularly eucalypts should allow individual beekeepers to commence monitoring key assets and so provide a broader base on which changes to resource levels are assessed. There is considerable potential, and a commitment from a biodiversity perspective, at least in South Australia, to re-establish extensive areas of native vegetation that if planted at appropriate densities with an appropriate mix of plants may provide not only biodiversity outcomes but critical additional floral resources for the honeybee industry. Identification of potential pollen sources for honeybees from amongst the local native flora is still deficient.

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Introduction Extensive vegetation clearance throughout the arable areas of Australia has reduced floral resources for beekeepers. In South Australia typically 90% or more of the native vegetation in arable areas has been cleared for agriculture; the level of clearance greater in areas with higher rainfall and better quality soils (e.g. Paton et al. 1999, Paton et al. 2004a). In the more heavily cleared areas many key eucalypts exist primarily as scattered paddock trees or along roadside verges (e.g. Paton et al. 2005a; Carruthers & Paton 2005). Although broadscale vegetation clearance has largely stopped in most states, paddock trees can and are still being cleared to facilitate intensification of agriculture. Scattered trees in paddocks and along roadsides also appear more susceptible to loss of condition due to changed environmental conditions than those in intact bushland (e.g. Paton et al. 1999; Paton et al. 2005a). The prognosis for these trees continuing to provide significant floral resources to beekeepers in the long term is likely to be limited (e.g. Paton et al. 1999; 2004b; 2005a, b). In many areas, a significant number of the trees are in poor condition, suffer from various ailments (high mistletoe infestations, mundulla yellows, lerp, over-browsing by koalas) and produce few flowers that may not produce as much nectar or pollen (e.g. Paton et al. 2002; Paton et al. 2005a, b; Ward 2005). If these trees continue to deteriorate in condition then simply protecting rural trees from clearance will not secure floral resources for the beekeeping industry. Other more active programs of management may be required. Coupled with this exacerbated rate of tree loss is the lack of recruitment of young trees in agricultural settings to replace those mature trees that die. Based on measurements of tree sizes, there has been a long period (many decades) of little or no recruitment (e.g. Carruthers & Paton 2005; Paton et al. 2005a). As a consequence any losses in the current crop of rural trees or in their condition will not be immediately replaced or compensated for by new trees establishing. Even if young trees are allowed to establish now, there will still be a lag of several decades before another generation of mature plants will be present in the landscape and available for beekeepers to use. Revegetation is often promoted as a panacea to environmental degradation. However to date, most revegetation programs are small in area (often <1ha) and consist of planting a few tree species, often at high density (e.g. Paton et al. 2004a) that may not provide adequate flowers (or resources produced per flower) to compensate for the floral losses caused by ongoing rural tree decline. When planted at high densities, eucalypts rarely produce lateral branches, and their roots are equally restricted laterally because of competition with adjacent plants. Such plants may not produce many flowers. South Australian beekeepers have identified a number of factors that have influenced, and were likely to continue to influence, the availability of floral resources for beekeepers (Paton et al. 2004b). These factors included dieback of eucalypts, grazing of understorey, more frequent dry conditions in recent years, and a reduction of agricultural weeds associated with a shift from grazing to cropping. Shifts in the types of crops and shifts to more intensive agriculture were also issues, since these also potentially reduced the availability of important weed species such as Echium plantagineum and Hypochoeris glabra (Paton et al. 2004b). Although vegetation clearance was an issue in the past, its significance has declined following the introduction of native vegetation clearance legislation. However, fires in remnant vegetation have resulted in beekeepers being displaced from some key areas for periods of up to 10 years while the vegetation recovers. Predictions from anticipated climate change suggest increased risks of droughts, fire, extremes in weather conditions, and shifts in the timing, amount and pattern of rainfall. All of these have the potential to significantly influence the performances of plants and hence floral resources. The current drought conditions in south-eastern Australia provide an opportunity to assess the likely responses of native plants to

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droughts and hence longer-term impacts of climate change on the beekeeping industry. Changes in climate are also likely to lead to some adjustments to agriculture reducing the areas of water-dependent crops, and this may lead to reductions in some irrigated horticultural crops (e.g. oranges) further reducing floral resources to the beekeeping industry. Within the Mt Lofty Ranges and adjacent arable regions, where native vegetation clearance has been severe, there is an increasing realisation that to prevent further imminent losses of biodiversity, there is an urgent need to re-establish significant amounts of native habitat for wildlife (e.g. Paton et al. 2004a). This is reflected in the South Australian Government’s ‘No Species Loss’ and ‘Nature Links’ policies, and by the recognition of the Mt Lofty region as a biodiversity hotspot by the Federal Government. For the Mt Lofty region, the Adelaide and Mt Lofty Ranges Natural Resource Management Plan has set a long-term target of re-establishing native vegetation back to 30% of its original cover. This amounts to converting at least 100,000 hectares of farmland back to native vegetation in this region alone, and becomes one of the major potential changes to land use within the region, that both threatens existing floral resources used by the honeybee industry (various agricultural weeds) but also provides significant opportunities of growing natural floral resources of value to the beekeeping industry. A recently completed survey of South Australian beekeepers (Paton et al. 2004b) indicated that many of the beekeepers surveyed had poor knowledge of the floral resources that their bees were actually using, particularly key pollen sources used when honeybees were exploiting nectar from selected eucalypt species that provide little pollen (e.g. E. leucoxylon, E. fasciculosa). Furthermore, beekeepers differed greatly in their estimates of annual variations in floral production of key species and hence the reliability of certain species as nectar producers. Without knowledge of the full complement of plants being used and patterns to flowering and how these change through time it is not possible to predict potential longer-term changes in resource availability for the beekeeping industry. Without this information it is difficult to incorporate the needs of the SA apiary industry into future revegetation and restoration programs. This project aims to better document the use and importance of native plants (particularly woodland eucalypts) in different landscapes (natural bushland, paddock and revegetation plot) to commercial beekeepers, identifying deficiencies in the resource base where they exist. This information will then be used to assist in maintaining the health and productivity of current trees from a beekeeper perspective while growing the floral resource base through appropriate revegetation and restoration programs. If the honeybee industry is to respond to changing resource levels and take a proactive role in revegetation programs that may secure floral resources in the medium and long-term then three pieces of information are needed. First, more accurate information is needed on the suite of species used by the industry when key nectar-producing plants are flowering. Such information is critical to informing natural resource managers on plant species compositions for re-vegetation. Second, one needs information that will allow predictions as to how the current floral resources might change through time, due to loss of condition or numbers of rural trees and lack of replacement and or changes to the frequency, extent and timing of flowering of key species, the latter a likely response to climate change. Third, one needs information on how planting densities and arrangements of plants in revegetation programs may influence tree shape and eventual productivity of individual plants. Such information is also critical to providing advice to revegetation programs and is likely to have important biodiversity outcomes as well.

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Objectives The objectives of this project were to: 1. Document the importance of scattered (paddock) trees, trees in natural areas and trees in

revegetation areas to the honeybee industry in South Australia. 2. Determine if trees in different landscapes (paddock, woodland, revegetation) or in

different condition differ in floral resource production. 3. Document the sources and location of pollen used when honeybees exploit floral

resources from trees in rural landscapes. 4. Measure resource share between honeybees and other fauna. 5. Develop a simple method of scoring tree condition and flowering so that beekeepers can

objectively (quantitatively) document changes in tree health and annual variation in flowering levels of key eucalypt species through time so they can better track long-term changes in their resource base.

A further key component of this study was to establish and maintain a number of monitoring programs to document current floral resources used by apiarists, and how these change through time particularly with anticipated changes in climate and rural land use.

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Methods

Study sites This project concentrated primarily in the Mt Lofty region of South Australia. Over 90% of the region has been cleared of native vegetation, disproportionately from land with better quality soils that was most suited to agriculture (e.g. Paton et al. 2004a). The region’s native vegetation consists of a range of woodland and forest systems, heathlands and coastal scrubs all of which are used by beekeepers to some extent, primarily from late autumn to early summer (Paton et al. 1999; Paton et al. 2004b). As a consequence of the high levels of vegetation clearance, native fauna have declined and continue to decline within the region, but programs established by the State Government and the Natural Resource Management Board aim to re-establish significant amounts of native vegetation to the region. Some initial revegetation took place in the 1970s when 1680ha of land in the Monarto region was revegetated with both endemic and non-endemic eucalypts, the latter primarily from Western Australia. A small range of other trees (Allocasuarina, Callitris) and large shrubs (Melaleuca, Hakea) were also included in the plantings. However, no understorey was planted in these amenity plantings, because the proposal for the new satellite city at Monarto was dropped by the State Government before any of the understorey plantings commenced. This revegetation is now sufficiently mature to be used by native fauna and by beekeepers with several apiary sites placed to exploit the floral resources provided by the plantings. Within the Mt Lofty region six sites were established to assess floral resource production and use by beekeepers over a series of 2-3 years. These sites covered areas of native vegetation set aside for conservation (Newland Head Conservation Park, Scott Conservation Park), areas of established revegetation (Monarto), and agricultural areas used primarily for grazing where a moderate density of scattered trees had been retained (Para Woodland, Bingara and Mt Bold; Figure 1). These three agricultural areas were selected because they were sites that had been earmarked for the re-establishment of native vegetation, providing an opportunity to influence the planting programs and to assess floral resource values of the reconstructed systems relative to the current systems, as revegetation programs become established. Additional information on flowering phenologies, floral resource production and performances of key plants used by South Australian apiarists was collected from a range of other sites within the Mt Lofty Ranges, on Kangaroo Island, and from two areas of mallee-heath (Ngarkat, Messent) that are used annually by beekeepers during winter. Ngarkat and Messent Conservation Parks, both in the Upper South East of South Australia, are important sites for the South Australian honeybee industry because they enable beeekepers to maintain hive strength during winter prior to providing pollination services to horticultural crops (e.g. almonds). The key plant species exploited is Desert Banksia Banksia ornata (Paton 1999). At these two mallee-heath sites, long-term monitoring programs for Banksia ornata were established in 1990 and 2002 respectively as part of studies documenting the recovery of both flora and fauna following fire. Both areas, but Ngarkat in particular, experience frequent and extensive fires. During the seventeen year period of monitoring at Ngarkat there have been six extensive fires (1990-1; 1997-8; 1998-9; 2002-3; 2004-5 and 2005-6). The smallest of these burnt 9,750 ha and the largest 65,900 ha. In 2007, 182,300 ha (68% of the park) was less than 10 years post-fire. In addition to the fires there were five periods of drought (1990-91; 1994-5; 1997-8; 2002-3 and 2006-7). Monitoring at

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Messent Conservation Park commenced in July 2002 following a managed burn in May that got out of control and burnt over a third of the park.

Figure 1. Location of major study sites in the Mt Lofty region of South Australia.

Measuring standing crops and production of nectar The volume and concentrations of nectar in flowers were measured using 10 or 20 µl calibrated glass capillary tubes and a 0-90% Atago hand sugar refractometer. Volumes were determined by measuring the length of the capillary tube that contained fluid to the nearest millimetre and converting this to microlitres (µl) knowing the length of the tube and its volume. When the volumes were small and of high concentrations a small quantity of water (~5-10 µl) was added to the flowers to more efficiently extract the nectar. Since the sugar refractometer measured concentrations as %wt/wt sucrose equivalents, all concentrations

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were converted to %wt/volume using the equation 8.197 (%wt/wt)1.108. Volumes and concentrations were then multiplied to estimate the quantity of sugar (µg) present in each sampled flower. Two types of measurements were collected: the standing crop of nectar remaining in flowers and the quantity of nectar produced over a 24 hour period. Standing crops of nectar were estimated by sampling 15 flowers from each of five trees. Measurements of standing crops were made in late afternoon after honeybees had stopped foraging. Nectar production was determined by bagging separate samples of flowers in fine voile bags at the same time as samples of flowers were collected for measuring standing crops. The voile bags (11 threads/cm) prevented floral visitors from accessing the flowers, but allowed air passage, and so did not allow water to condense inside the enclosure. Samples of 15 bagged flowers were collected 24 hours later from each of five plants and the accumulated volume and its concentration measured. The average production of nectar was calculated by subtracting the standing crop at the time the flowers were bagged from the accumulated nectar and expressing this as mg sugar/flower/day for each of the five plants, separately. The mean of the five trees was then used as an estimate of 24h nectar production. In the case of eucalypt flowers only fresh, fully open, flowers were sampled. Flowers where any of the filaments were still curled (young flowers) or were being shed (old flowers) were excluded.

Flowering levels and phenologies of eucalypts At best, beekeepers keep qualitative records of flowering of key plant species. Given the reluctance of beekeepers to record detailed information of the flowering of key plants, including eucalypts, a simple technique needed to be developed that would allow comparisons between years and sites with respect to the quantities of flowers being produced. The method also needed to be able to account for the wide variation in the quantities of flowers produced by different species of eucalypts. The technique that was adopted involved estimating the numbers of floral units (buds, open flowers and recently finished flowers) that were present (on average) within an area of canopy that could be covered with an outstretched hand (handspan). The floral units in this case represented the flowers that would be produced during that flowering event and did not include any small buds that were for a future flowering event in a subsequent year. The area covered by an outstretched hand is approximately 0.04 m2, and observers simply estimated the total number of floral units into one of the following categories: 0, 1, 2, 3, 4, 5, 6-10, 11-15, 16-20, 21-25, 26-30, 31-40, 41-50, 51-75, 76-100, 101-125, 126-150, 151-175, 176-200, 201-250, 251-300, 301-400, 401-500, 501-600, 601-700, 701-800, 801-900, 901-1000. Initially this involved counting the floral units present under several ‘handspans’ and then using these to estimate the average quantity of flowers over the canopy as a whole. Using this technique, independent observers scored the flowering levels in the same category in over 95% of occasions, with the remaining <5% of records being recorded in an adjacent flowering category. In addition to recording the number of floral units, observers also recorded the % of these flowers that were buds, flowers, and recently finished flowers, to estimate both the level of flowering at the time of the observations and the extent to which the tree had progressed its flowering for that year. The level of flowering at the time was simply the % of the floral units that were flowers at the time of observation, while the extent through that season’s flowering was simply estimated by adding half the % of open flowers to the % of the floral units that had finished flowering. For example, if the plant had 20% of the floral units as buds, 30% as flowers and 50% had finished flowering then the percent through flowering for this plant was estimated as 65%. To assess the levels of flowering of various eucalypt species at any location or time between 25 and 50 individual plants were scored. For our surveys this also included recording the position of each tree with a Global Positioning System (GPS), estimating the height and dbh

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(diameter at breast height) of the trees, and recording their condition by estimating the percentage of the canopy that was still intact and had not suffered any dieback (loss of foliage). The percentage of the canopy that was still intact was estimated by eye using the proportion of outer branches with and without foliage. A range of statistics can then be generated from these data to compare flowering levels between samples of trees in different locations and through time.

Flowering of other plants The abundances of flowers produced by a range of herbaceous plants, including Echium plantagineum, Hypochoeris glabra, Banksia ornata, and other heaths, were determined by counting all the flowers present in quadrats that varied in size from 1m x 1m (E. plantagineum),10 m x 2 m (H. glabra) to 50 m x 4 m (Banksia ornata). For a range of other plants that were at low densities the numbers of flowers present on samples of 10-20 individual plants were counted.

Visitation rates to flowers The frequency with which honeybees and other insects visited the flowers of eucalypts was determined by selecting 1-5 flowering branches on up to ten individual plants and counting all of the open flowers present on each branch. To determine daily rates of visitation, the numbers of honeybees and other insects at the flowers on each branch was counted hourly from dawn until dusk. Records were also kept on whether the insects were collecting nectar or pollen. Between these counts the time taken by individual honeybees and other insects to visit five flowers was timed with a stop watch. These data were combined to estimate daily visitation rates. For example, if the total numbers of honeybees counted at a branch during the hourly counts was 15, and the bees visited six flowers per minute while foraging, then those bees made a total of 5,400 visits to the flowers on that branch during the day (15 x 6 x 60 (minutes in an hour)). If there was a total of 1,800 flowers on the branch, then on average the flowers received three visits per flower per day. Similar methods were used for shrubs and herbs, with either the numbers of flowers on whole plants, or the numbers of flowers in marked quadrats being used as the sampling unit rather than branches. The frequency with which birds visited flowers was assessed by selecting 2-4 individual trees or portions of the canopies of 2-4 trees and recording bird use of the flowers on these branches during five or six 30 minute observation periods spread evenly over the day. During these observations the times when birds alighted in the sampling area, the times they commenced and ceased foraging, and the times when they left the sampling area were recorded to the nearest second. During the intervening periods the numbers of flowers on each tree or observation branch was counted, and the speed with which birds probed 10 flowers timed with a stopwatch. These data were then combined to estimate the average rate at which birds visited flowers. For example if there was a total of 990 seconds of foraging by a particular bird species during six 30 minute observation periods then that species averaged 330 seconds of foraging per hour. If the birds visited flowers at a rate of 40 per minute and there were 2000 flowers on the branch, then, on average, birds would visit 220 flowers in an hour and a flower would receive 0.11 visits per hour. Over a 14 hour day the average number of visits by birds per flower per day would be 1.54.

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Long-term monitoring programs Baseline measures of resources and long–term monitoring programs have been established at five locations. Three monitoring sites have been established in the Mt Lofty Ranges where native vegetation is to be re-established over the next 5-10 years: Mt Bold, Para Woodland and Bingara. The other two monitoring programs were in Messent Conservation Park and Ngarkat Conservation Park and were built on programs that had already been established, that focused on documenting the flowering and post-fire recovery of Banksia ornata and other prominent shrubs within these mallee-heath systems. The Mt Bold property was grazed by cattle until 2004, when cattle were removed prior to re-planting the heavily cleared parts of the property with a range of native plants. At Mt Bold, four techniques of restoring natural habitats are being used: natural regeneration following hand removal of weeds, natural regeneration without weed control, direct seeding and planting of tube-stock seedlings. These latter two methods were done in conjunction with use of weedicides that targeted some of the broad-leaved weeds such as Echium plantagineum. Both Bingara and Para Woodland are still being grazed by stock but at reduced densities since 2005. Bingara is lightly grazed by cattle while Para Woodland is grazed by sheep. Active revegetation on these two sites is yet to commence, although some eucalypt seedlings have appeared on Para Woodland. Western Grey Kangaroos and European Rabbits are also present on all three properties. At each of the sites in the Mt Lofty Ranges a 40-70 ha area was selected and all the remaining trees mapped using a GPS. The size (dbh, height), condition (% canopy intact), minimum and maximum heights of their canopies, and the lateral spread of canopies estimated from pacing the distance of the canopy out from the trunk on each of the four major compass bearings were measured for each of these trees. Heights were estimated using a clinometer or by simple extrapolation of a known height (2 m). Trunk diameters were measured with a tape measure. In addition to scoring these physical attributes of trees, annual floral production was also estimated using the handspan technique (described above) for up to 50 individuals of each tree species if present. The numbers of mistletoes in each tree were also scored as well as the locations of any remnant tree stumps. The distribution of understorey plants within each of these areas was assessed in one of two ways; At Bingara and ParaWoodland the distributions of Echium plantagineum and Hypochoeris glabra were assessed by mapping the patches of each plant species along a series of parallel transects that ran 25-40 m apart across each site during late spring. Each transect was walked and a GPS used to record the edges of each patch of plants or when the densities of the plants changed dramatically. For the Mt Bold site, the distribution of all shrubs and herbs was determined by dividing the site into over a thousand 25 m x 25 m cells and then recording the percent of each cell covered by Echium plantagineum, Hypochoeris glabra, as well as all other herbs, small shrubs and grasses. For larger shrubs (e.g. Blackberry (Rubus sp.), Lissanthe strigosa, Acacia spp., Xanthorrhoea semiplana) the actual number of individual plants or clumps was recorded as well as an estimate of the cover. Monitoring of Banksia ornata in Ngarkat was based on counting the numbers of cobs (inflorescences) produced in four 50 m x 4 m transects established at each of 45 sites in July (middle of the flowering season, Paton 1999). Each site was at least 3km from another. For 29 of the sites, observations on floral production commenced in 1990-1991 as part of a project aimed at assessing impacts of honeybees on the flora and fauna of this reserve (Paton 1996, 1997, 1999). Additional sites were added in 1995 (1), 1999 (3) and 2004-5 (12) to increase the spread of sites across the reserve and to increase the levels of replication for assessing recovery after different fires.

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In determining the numbers of cobs produced by Banksia ornata, the numbers of budded, flowering and finished cobs were counted separately in each quadrat and added to determine the production of cobs for that year. Cobs that had been aborted before flowering were also counted but not used in estimating floral production. However, flowering inflorescences that had been removed by Yellow-tailed Black Cockatoos were included. The numbers of flowers present on other species of plant were also counted. During these July counts, the numbers of live Banksia ornata plants and plants that had died in the last year were also counted. If quadrats had been burnt then the numbers of seedlings and dead seedlings were counted each year. These counts were then used to record the responses of the plants to drought and to document the speed of recovery following fire. In addition to these quadrats, five additional 50 m x 4 m quadrats were established in September 2005 where more detailed information on individual plants was collected. This included mapping the locations of individuals of the prominent heath land plants to an accuracy of 0.1 m within each quadrat so that the fate of individual plants could be followed more closely through time. For each mapped plant we measured the size of the plant (height and the area of basal root mass for species that re-sprout following fire), and recorded the percentage of the canopy that was intact. For Banksia ornata we also counted the numbers of infructescences on each plant and the number of follicles in each infructescence to determine the accumulated seed bank for this species in each quadrat. These five quadrats were burnt in the January 2006 fire (by chance), allowing more detailed information on the initial recovery of these plant populations to be collected. At Messent Conservation Park, six sites were established in July 2002, each 3 km apart. Three of the sites were established in areas that had been burnt when a control burn escaped from control lines, the other three sites were in mature heaths. Four 50 m x 4 m quadrats were established at each site and the production of Banksia ornata cobs, numbers of seedlings establishing post fire and annual mortality rates determined from annual counts in July as outlined above.

Assessing the potential for revegetation to provide floral resources for honeybees The quantities of nectar produced by individual flowers and the numbers of flowers per handspan on their own are not sufficient to estimate the quantities of nectar produced by different eucalypts on a per hectare basis. The surface area (m2) of the canopy and the density of trees (trees/ha) is also needed. The handspan method (above) estimates the floral abundance over about 0.04 m2 of canopy surface so to convert flowers per handspan to flowers per tree, the canopy surface area of the tree is needed. Without that information and a measure of the density of trees, the quantities of nectar produced by different eucalypts in various woodland, forest, mallee-heath or agricultural systems can not be calculated and the productivity of different systems cannot be compared. To estimate the surface area of the canopy of a tree, the shape of the tree and the percent of the perimeter of the tree that has canopy are needed. In addition, it is necessary to obtain the height of the tree (H), the average canopy radius (r), and average minimum height of the canopy (L). Although the horizontal area that the canopy of a tree covers is easily calculated as πr2, this does not represent the surface area of the canopy, because the surface area of the canopy is not just the area in the horizontal plane, but a more complex area over three dimensions. The surface area of the canopy then depends on the shape of the tree. Furthermore the canopies of most eucalypts are not continuous over the whole surface area and so the per cent of the canopy surface with foliage needs to be estimated to correct for this.

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To estimate the per cent canopy surface (P) that had foliage, a point on the outer lowest edge of the canopy was selected, and an imaginary line was drawn from this point to the top of the tree and down to the opposite bottom edge of the canopy. The per cent of this line that had canopy against it was then estimated. To estimate the shape of the tree, the canopy was divided into three equal layers (top(t), middle(m), bottom(b)) in the vertical plane, and the average horizontal width of each layer estimated on a 1, 2, 3 basis, relative to the measured radius (diameter). This was done by assigning 3 to the layer that had the widest diameter and the other two layers were assigned either a value of 1, 2 or 3 based on the width of the canopy for that layer relative to the layer with the widest canopy. Thus a tree with a pyramid shape would have a score of 1, 2 and 3 for the top, middle and bottom layers respectively, a tree with a reverse pyramid shape 3, 2, 1 and a tree where the width of the canopy of the tree was the same for all three layers 3, 3 ,3. The tree shape and per cent of canopy perimeter with foliage were combined with the canopy radius and vertical spread of the canopy to estimate the canopy surface area of the tree. The methods used to estimate the average radius and the minimum and maximum heights of canopies have been described in earlier sections. To calculate the surface area of canopy the tree was considered to consist of three cylinders each with a height of (H-L)/3 stacked on top of each other and the radius corrected for the relative width of each cylinder. The tree’s surface area was then calculated as the lateral surface area of each cylinder plus the horizontal surface area (πr2) and corrected for the per cent canopy perimeter (P) with foliage. Tree surface area (m2) = (P/100)(πr2 + π2r(b/3)((H-L)/3) + π2r(m/3)((H-L)/3) + π2r (t/3)((H-L)/3))

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Results & Discussion

Nectar production and standing crops

24 hour production The quantities of nectar produced over 24 hours were determined for eighteen species of eucalypts, including one natural hybrid (Table 1). For most species nectar production was determined on more than one occasion and from one or more study sites or environmental settings. Of these eucalypts, there were four species that consistently produced more nectar per flower per day than the other species. These species were Eucalyptus angulosa (7.4 – 10.6 mg/fl/d), E. torquata (7.6 – 15.4 mg/fl/d), E. leucoxylon (7.3 – 15.6 mg/fl/d) and E. cosmophylla (9.7 - 18.8 mg/fl/d; Table 1). Eucalyptus albopurpurea, E cladocalyx, E. diversifolia, E incrassata, a natural E. porosa -E. leucoxylon hybrid, and E. platypus typically produced 2-5 mg/fl/d, while E. baxteri, E. calycogona, E. fasciculosa, E. odorata, E. socialis and E. viminalis typically produced between 0.5 – 2 mg/fl/d (Table 1). Eucalyptus remota and E. porosa produced < 0.5 mg/fl/d. The quantities of nectar produced by plants in revegetation, in remnant vegetation or by plants scattered across paddocks were similar (Table 1). For example, Eucalyptus cosmophylla produced between 9.7 and 18.8 mg/fl/d in remnant vegetation, 13.0 – 14.4 mg/fl/d in paddocks and 12.3 – 12.8 mg/fl/d in re-vegetation. Eucalyptus leucoxylon produced between 8.3 and 15.3 mg/fl/d in remnant vegetation, 7.3 – 15.1 mg/fl/d in paddocks, and 8.3 – 15.6 mg/fl/d in re-vegetation. The quantities of nectar produced by E. fasciculosa and E. odorata were also similar for trees in remnant vegetation and in revegetation (Table 1). These data suggest that the quantity of sugar produced per flower is a characteristic of the species and is relatively constant irrespective of the environment of the tree. Even in the drought year of 2006, nectar production was comparable to previous years. For example, measures of nectar production of E. leucoxylon ranged from 9.1 – 14.1 mg/fl/d in 2004 – 2005 and from 7.3 – 15.6 mg/fl/d during the drought year of 2006. Eucalyptus calycogona, E. incrassata and the natural E. porosa – E. leucoxylon hybrid also produced similar quantities of nectar in the drought year compared to other years (Table 1). There were, however, some localised effects of environmental conditions on nectar secretion. Severe frosts affected the production of nectar by E. cosmophylla on one occasion at Newland Head Conservation Park with the flowers remaining frozen for more than half the day and 24 hour nectar production reduced to 2.6 mg/fl/d. Similarly production of nectar by E. diversifolia at the same site may have also been affected by frosts. At other sites a severe winter frost(s) resulted in all of the buds of E. diversifolia for the 2006 flowering season being dropped prior to flowering and the outer foliage being severely burnt (see below).

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Table 1. Quantities of nectar produced (mg sugar/flower/d) and standing crops of nectar (mg sugar/flower) for different species of eucalypts in different environments in South Australia during 2004-2007. Key for locations: BING Bingara nr Mt Compass; FCNP Flinders Chase National Park; FRFM Frahn’s Farm area; GEMD Gemini Downs nr Salt Creek; MPHR Monarto Princes Hwy Reserve; MRV1 Monarto Revegetation Site 1 MRV4 Monarto Revegetation Site 4; MRVB Monarto Revegetation Browns Rd; MTBO Mt Bold; MZOO Monarto Zoo; NGCP Ngarkat Conservation Park; NHCP Newland Head Conservation Park; PAWD Parawoodland; SCCP Scott Conservation Park. Data show means ± s.e. for five plants on almost all occasions. * indicates plants likely to be affected by a severe frost.

Plant species Month Year Location Environment Standing

Crop 24h

production Eucalyptus albopurpurea Feb 2007 FCNP remnant 0.41 ± 0.22 3.18 ± 0.35 Eucalyptus angulosa Jun 2005 NHCP paddock 1.78 ± 0.47 10.64 ± 2.69 Eucalyptus angulosa Jun 2007 NHCP paddock 1.22 ± 0.28 7.39 ± 2.03 Eucalyptus angulosa May 2007 NHCP mixture 0.37 ± 0.24 8.31 ± 1.25 Eucalyptus baxteri Feb 2007 FCNP remnant 0.19 ± 0.03 0.76 ± 0.15 Eucalyptus baxteri Jun 2007 NHCP remnant 0.05 ± 0.02 0.56 ± 0.07 Eucalyptus calycogona Oct 2004 MRV4 reveg 0.20 ± 0.06 0.75 ± 0.15 Eucalyptus calycogona Oct 2006 MRV4 reveg 0.15 ± 0.01 0.86 ± 0.26 Eucalyptus calycogona Sep 2006 MRV4 reveg 0.36 ± 0.06 1.31 ± 0.21 Eucalyptus cladocalyx Feb 2007 FCNP remnant 0.09 3.62 Eucalyptus cosmophylla Jun 2006 FCNP remnant 0.003 ± 0.003 12.95 ± 1.40 Eucalyptus cosmophylla Jun 2006 NHCP paddock 1.41 ± 0.33 12.98 ± 3.81 Eucalyptus cosmophylla Jun 2006 NHCP remnant 0.43 ± 0.29 2.62 ± 1.03* Eucalyptus cosmophylla Jun 2006 NHCP reveg 0.004 ± 0.004 12.84 ± 1.38 Eucalyptus cosmophylla May 2006 NHCP remnant 2.99 ± 0.57 18.76 ± 1.81 Eucalyptus cosmophylla May 2006 NHCP paddock 3.25 ± 0.70 14.43 ± 1.77 Eucalyptus cosmophylla May 2006 NHCP paddock 5.92 ± 0.67 12.97 ± 3.81 Eucalyptus cosmophylla May 2006 NHCP reveg 7.78 ± 0.85 12.28 ± 1.83 Eucalyptus cosmophylla May 2006 NHCP remnant 9.22 ± 0.44 9.71 ± 2.19 Eucalyptus diversifolia Jul 2006 GEMD paddock 0.50 ± 0.08 5.12 ± 0.95 Eucalyptus diversifolia Jul 2007 GEMD paddock 0.50 ± 0.12 1.90 ± 0.45 Eucalyptus diversifolia Sep 2006 NHCP paddock 0.65 ± 0.28 0.09 ± 0.16* Eucalyptus diversifolia Sep 2006 NHCP remnant 0.69 ± 0.18 0.30 ± 0.36* Eucalyptus fasciculosa Oct 2006 SCCP remnant 0.26 ± 0.07 0.78 ± 0.14 Eucalyptus fasciculosa Sep 2006 NHCP remnant 0.38 ± 0.05 1.34 ± 0.14 Eucalyptus fasciculosa Sep 2006 NHCP remnant 0.36 ± 0.07 0.80 ± 0.09 Eucalyptus fasciculosa Sep 2006 NHCP reveg 0.17 ± 0.03 0.86 ± 0.14 Eucalyptus incrassata Dec 2004 NGCP remnant 3.24 ± 0.74 2.68 ± 0.95 Eucalyptus incrassata Dec 2006 MRV4 remnant 3.94 ± 1.75 3.73 ± 1.55 Eucalyptus leucoxylon Dec 2004 BING paddock 10.3 ± 0.86 12.66 ± 2.14 Eucalyptus leucoxylon Dec 2004 INVA remnant 0.77 ± 0.24 10.76 ± 1.48 Eucalyptus leucoxylon Dec 2006 INVA remnant 14.55 ± 3.94 15.30 ± 2.28 Eucalyptus leucoxylon Nov 2005 MRVB reveg 3.37 ± 0.77 14.12 ± 3.31 Eucalyptus leucoxylon Nov 2006 BING paddock 19.17 ± 2.75 15.10 ± 3.60 Eucalyptus leucoxylon Nov 2006 SCCP remnant 3.98 ± 1.32 8.94 ± 2.30 Eucalyptus leucoxylon Nov 2006 MRVB reveg 20.65 ± 3.09 15.59 ± 5.69 Eucalyptus leucoxylon Oct 2004 MRV4 reveg 5.68 ± 1.15 9.10 ± 1.15 Eucalyptus leucoxylon Oct 2006 SCCP remnant 6.22 ± 1.19 10.91 ± 6.79 Eucalyptus leucoxylon Oct 2006 MRV4 reveg 8.21 ± 0.84 10.22 ± 3.13 Eucalyptus leucoxylon Sep 2006 MTBO paddock 6.55 ± 0.82 7.26 ± 1.62 Eucalyptus leucoxylon Sep 2006 PAWD paddock 2.54 ±1.02 10.32 ± 1.45 Eucalyptus leucoxylon Sep 2006 MPHR remnant 3.00 ±0.90 8.32 ± 2.41 Eucalyptus odorata Mar 2006 MPHR remnant 0.06 ± 0.02 1.03 ± 0.44

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Eucalyptus odorata Mar 2006 MZOO reveg 0.07 ± 0.03 1.03 ± 0.15 Eucalyptus odorata Mar 2007 MPHR remnant 0.001 ± 0.001 0.68 ± 0.20 Eucalyptus odorata Mar 2007 MZOO reveg 0.028 ± 0.01 0.65 ± 0.22 Eucalyptus ovata Jun 2007 FCNP reveg 0.02 ± 0.008 0.51 ± 0.15 Eucalyptus platypus (ssp 1) Apr 2005 MRVB reveg 0.16 ± 0.07 0.42 ± 0.24 Eucalyptus platypus (ssp 2) Dec 2006 MRV4 reveg 0.53 ± 0.05 7.75 ± 2.01 Eucalyptus por x leu Nov 2005 PAWD paddock 0.88 ± 0.41 3.26 ± 0.59 Eucalyptus por x leu Oct 2006 PAWD roadside 0.89 ± 0.18 4.79 ± 0.59 Eucalyptus porosa Nov 2006 FRFM remnant 0.15 ±0.05 0.16 ± 0.05 Eucalyptus porosa Nov 2006 FRFM reveg 0.34 ± 0.10 0.31 ± 0.18 Eucalyptus remota Jun 2006 FCNP remnant 0.03 ± 0.01 0.22 ± 0.08 Eucalyptus socialis Dec 2004 NGCP remnant 0.47 ± 0.07 1.26 ± 0.20 Eucalyptus torquata Apr 2005 MRVB reveg 1.34 ± 0.28 7.63 ± 1.12 Eucalyptus torquata May 2005 MRV4 reveg 1.26 ± 0.21 7.74 ± 1.11 Eucalyptus torquata May 2007 MRV1 reveg 1.77 ± 0.41 15.35 ± 2.83 Eucalyptus viminalis Mar 2007 MTBO remnant 0.06 ± 0.01 0.62 ± 0.15

Standing crops The quantities of nectar remaining in flowers late in the day (standing crops; Table 1) were often substantial, particularly for Eucalyptus cosmophylla, E. leucoxylon, E. angulosa, E incrassata and E. torquata where there was often more than 1mg/fl left unexploited. For some species like E. leucoxylon and E. cosmophylla there was often over 5mg/fl of nectar, even when a commercially-managed apiary was within a few hundred metres. At times these high volumes of nectar were such that nectar dripped from the flowers. This apparent over-production of nectar, however, is not caused by the plants producing more nectar in some years than others but reflects low visitation rates to flowers (see below).

Flowering of key species of eucalypts

Quantities of flowers produced The numbers of flowers produced by different species of Eucalyptus vary dramatically. Table 2 provides a summary of the maximum numbers of flowers produced per unit area of canopy (handspan) by individuals of a range of species. Some species produced moderately low numbers of flowers (e.g. E. angulosa, E. astringens, E. cosmophylla, E. incrassata and E. torquata) and these tended to be species with larger flowers. Other species with smaller flowers had maximums in excess of 200 flowers per handspan of canopy (e.g. E. baxteri, E. calycogona, E. camaldulensis, E. cladocalyx, E. diversifolia, E. fasciculosa, E. obliqua, E. odorata, E. porosa, and E. socialis). One species, E. leptophylla had over 800 floral units per handspan of canopy (Table 2).

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Table 2. Maximum floral production levels for a variety of eucalypt species in South Australia. The table shows the maximum number of floral units (buds, flowers and finished flowers combined) present in the canopy that can be covered by an average handspan (=0.04 m2). Where data exist, the maximum level of flower production is provided for each year from 2004-2007. Note where no data are provided, flowering was either not scored or the species did not flower in that year. * indicates species introduced to South Australia in revegetation programs. Species Maximum Maximum in any one year 2004 2005 2006 2007 Eucalyptus albopurpurea 126-150 21-25 76-100 126-150 Eucalyptus angulosa 51-75 26-30 21-25 51-76 Eucalyptus astringens* 31-40 31-40 Eucalyptus baxteri 251-300 251-300 Eucalyptus calycogona 301-350 251-300 126-150 301-350 Eucalyptus camaldulensis 251-300 251-300 251-300 151-175 151-175 Eucalyptus cladocalyx 351-400 76-100 76-100 351-400 Eucalyptus cosmophylla 31-40 31-40 Eucalyptus diversifolia 251-300 151-175 251-300 Eucalyptus fasciculosa 201-250 76-100 201-250 31-40 Eucalyptus goniocalyx 101-125 101-125 26-30 Eucalyptus incrassata 51-75 51-75 26-30 41-50 Eucalyptus leptophylla 801-850 801-850 Eucalyptus leucoxylon 101-125 41-50 21-25 101-125 1-5 Eucalyptus microcarpa 126-150 126-150 Eucalyptus obliqua 401-450 401-450 Eucalyptus odorata 201-250 201-250 201-250 Eucalyptus ovata 176-200 176-200 26-30 51-75 Eucalyptus platypus* 76-100 51-75 51-75 76-100 Eucalyptus porosa 201-250 76-100 201-250 Eucalyptus remota 151-175 151-175 Eucalyptus socialis 301-350 301-350 151-175 301-350 Eucalyptus torquata* 51-75 51-75 41-50 31-40 Eucalyptus viminalis 101-125 76-100 76-100 101-125 Table 2 provides an indication of the maximum potential production of flowers for selected species, and some of the variability in this measure from one year to the next, but within each species there is enormous variability between individuals in the quantity of flowers being produced in any one year. Figures 2 and 3 provide some examples illustrating the variation between individual plants within the same population and between populations of the same species. For example, the numbers of flowers produced by individual E. camaldulensis varied from <5 to > 250 per handspan, almost 50 fold even within the same flowering season (Fig. 2). This is equivalent to levels of floral production spanning up to 10 flowering categories (Fig 2). Despite the broad range in flowering levels there were differences in the spread of flowering levels between years within a site and also between sites in any one year (e.g. Figs 2, 3). For example, E. camaldulensis produced more flowers at Baan Hill in 2004 than the three subsequent years with no flowers produced by trees at this site in 2007. At Cromer and Meadows the flowering levels were much higher in 2005 than either 2004 or 2006 (Fig. 2). The Meadows sites however had moderate flowering in 2007 while Cromer had light levels of flowering in 2007 (see Table 4). Figure 3 shows similar data for populations of three other species of eucalypt. For each of these species there was a range of flowering levels amongst individual plants in any one year, but also substantial differences between years. Eucalyptus angulosa flowered moderately in 2005, had light flowering in 2006 and produced large numbers of flowers in

15

2007. For E. goniocalyx at Para Wirra flowering was higher in 2005 than 2006 or 2007 while for E. leucoxylon at Bingara flowering was highest in 2006. The handspan method that has been developed in this study provides a relatively simple way of estimating floral production for a range of eucalypts that is capable of documenting not just changes in the quantities of flowers being produced from one year to the next, but also the variability that exists within and between populations in floral production. A range of statistics can be generated from the handspan data. Two simple statistics are the percent of plants that produce flowers in a year and the median flower level. The use of these two statistics in indicating the extent of flowering in any one year is shown in Tables 3 and 4. The percent of plants producing flowers in any one year, although easily collected, does not reflect the actual levels of flowers produced and so the median flower level is potentially a better statistic to indicate the extent of flowering in any one year. Two important patterns can be discerned from the information provided in Tables 3 and 4. First, within a site, different species of eucalypts are not in synchrony with respect to the quantities of flowers they produce in one year relative to other years. For example at Newland Head, Eucalyptus angulosa flowered well in the years in which other key species (E. cosmophylla, E. fasciculosa and E. diversifolia) either did not flower or flowered poorly. There were also some species that flowered in each of three consecutive years, versus some that flowered in only one of three years or in alternate years, and one species (E. fasciculosa) that although flowering at one site did not flower at another site for the three years from 2005-2007. This variability within a species is illustrated for two additional species, E. camaldulensis and E. leucoxylon in Table 4. Different populations of E. camaldulensis flowered well in years when other populations did not flower or flowered poorly, and vice versa. Populations of E. leucoxylon, however, were more synchronous with all populations flowering well in 2006 and all flowering poorly, if at all, in 2007.

16

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Figure 2. Flowering levels in 2004, 2005 and 2006 for three populations of Eucalyptus camaldulensis in South Australia (Baan Hill Soak (top); Cromer CP (mid) and near Meadows (bottom). The figure illustrates the variability in the production of flowers within each of the populations, between years and between populations in each year.

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Eucalyptus angulosa (Newland Head)

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Figure 3. Flowering levels for three populations of Eucalyptus in South Australia over four years (2004-07) illustrating the variability in the production of flowers within the populations within and between years.

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Table 3. The levels of flowering for various eucalypts are shown for three selected sites between 2004 and 2007. The table shows the percentage of plants that were in flower and the median flowering level for those plant species for each year in which flowering was scored. Location and species % plants to flower Median flower level 2004 2005 2006 2007 2004 2005 2006 2007 Newland Head Cons Park Eucalyptus angulosa 100 64 94 16-20 1-5 26-30 Eucalyptus cosmophylla 0 93 0 0 16-20 0 Eucalyptus diversifolia 0 98 0 0 101-125 0 Eucalyptus fasciculosa 21 99 0 0 41-50 0 Flinders Chase National Park Eucalyptus albopurpurea 100 82 100 16-20 6-10 76-100 Eucalyptus cladocalyx 100 78 100 41-50 26-30 151-175 Eucalyptus cosmophylla 0 50 0 0 1-5 0 Eucalyptus diversifolia 0 100 0 0 51-75 0 Eucalyptus fasciculosa 0 0 0 0 0 0 Eucalyptus ovata 100 94 94 101-125 1-5 26-30 Eucalyptus remota 100 0 76-100 0 Monarto Eucalyptus calycogona 100 87 100 0 76-100 11-15 101-125 0 Eucalyptus leucoxylon 100 69 100 0 26-30 1-5 16-20 0 Eucalyptus platypus 100 89 100 31-40 16-20 151-176 Eucalyptus torquata 99 100 100 21-25 26-30 76-100 Eucalyptus odorata 98 96 41-50 41-50 The quantities of flowers produced by various species of eucalypts are likely to be influenced by many external and internal factors. Resource allocation to other functions may reduce flower production in some years. For example, committing resources to the production of fruits following extensive flowering may reduce the plant’s ability to allocate resources to bud production for the following year and this may account for some species not producing flowers in every year. Rainfall, particularly at the time of bud initiation, is likely to be a key external environmental variable. Extensive rains in the Mt Lofty Ranges in November 2005 coincided with the timing of foliage production for Eucalyptus leucoxylon and may have stimulated extensive bud production for this species. As a consequence, flowering was extensive during winter and spring 2006, despite the severe drought conditions at that time. With limited rainfall during 2006 there was negligible foliage production in that year. Most populations of E. leucoxylon produced no buds and did not flower in 2007. The only populations of E. leucoxylon where some plants produced a few flowers in 2007 were at Mt Bold and a site near Inman Valley, two of the wettest parts of the Mt Lofty Ranges. For some species, rainfall events 2-3 years prior to flowering might influence the quantities of flowers produced in a particular year, since some eucalypts will hold two or more cohorts of buds in their canopies at any one time.

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Table 4. The levels of flowering for Eucalyptus camaldulensis and Eucalyptus leucoxylon are shown for a range of sites in South Australia between 2004 and 2007. The table shows the percentage of plants that were in flower and the median flowering level for those plant species for each year in which flowering was scored. Species & location % plants to flower Median flowering level 2004 2005 2006 2007 2004 2005 2006 2007 Eucalyptus camaldulensis Cygnet Park KI 100 92 41-50 6-10 Baan Hill 70 36 100 0 76-100 0 31-40 0 Inman VH 100 10 100 36 + 0 51-75 0 Inman Sawpit 88 100 4 6-10 41-50 0 Inman Glacier Rock 88 92 0 6-10 41-50 0 Hindmarsh Tiers 76 88 0 1-5 31-40 0 Currency Creek 2 100 0 0 76-100 0 2k W Meadows 8 100 40 100 0 151-175 0 41-50 2k N Meadows 8 100 28 100 0 101-125 0 41-50 Gilberton 94 94 76 31-40 31-40 6-10 Athelstone 84 92 68 6-10 76-100 6-10 Kangaroo Ck 80 48 20 6-10 0 0 Gorge 80 92 92 41-50 26-30 31-40 Birdwood 48 60 84 0 1-5 31-40 Cromer 0 100 57 76 0 41-50 1-5 6-10 Gumeracha WH 92 4 92 76-100 0 21-25 South Para River 88 76 0 26-30 6-10 0 ParaWoodland 97 88 18 101-125 21-25 0 Eucalyptus leucoxylon Ngarkat 95 - - 21-25 burnt burnt Gemini Downs 96 26-30 Messent CP 84 96 0 11-15 11-15 0 Monarto 100 69 100 0 26-30 1-5 16-20 0 Inman Valley 100 5 100 4 16-20 0 31-40 0 Bingara 100 14 100 0 6-10 0 41-50 0 Scott CP 8 100 0 0 26-30 0 Mt Bold 98 52 41-50 1-5 ParaWoodland 83 100 0 1-5 41-50 0 Our knowledge of the flowering biology of most of our native plants remains poor. The semi-quantitative methods developed in this study provide a basis for documenting flowering biology but measures of flowering performance need to be conducted over a much longer time period than 3-4 years to allow the key factors influencing the frequency and extent of flowering to be identified and then experimentally tested. Rainfall and temperature are likely to change in the future as a result of climate change, and understanding how those changes will influence the frequency and extent of flowering will be important from both a wildlife management perspective and a honey production perspective. The predictions are that there will be an increase in the frequency of severe weather conditions including droughts, coupled with changes in diurnal and nocturnal temperatures including risks of frosts, but also potential changes in the seasonal timing of rainfall and amounts of rainfall (fewer days of rain, but greater amounts of rainfall on those days). All of these have the potential to disrupt the flowering patterns of native perennial plants. By maintaining annual monitoring of the flowering outputs of a suite of eucalypt species over time, but particularly during and following droughts as well as during more benign

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conditions, should allow predictions of how key floral resources for the beekeeping industry are likely to change with climate change over the next 50-100 years. Previous studies have collected information on the flowering of native and introduced plants retrospectively from beekeepers (e.g. Paton et al. 2004b). Although these provide some background to flowering, few beekeepers kept any written records, let alone detailed records of flowering of any of the plant species that they exploited, and so these assessments were based almost entirely on qualitative expert opinions and memory. Given the variability in floral production within individual plants within the one flowering season (e.g. Figs 2 & 3) basing flowering patterns on these data was probably naïve. The flowering of these plants is much more complex than was likely to be detected from answers to a questionnaire and hence that information is unlikely to be adequate for predicting changes to the flowering of plants in the future. The simple method of scoring flowering levels of plants developed here provides a simple mechanism for the industry to semi-quantitatively document flowering performances in the future.

Individual variation in the timing of flowering The complexity or variability in the flowering of these plants is increased further by the wide range in the timing of flowering of individual plants within a population. For all of the species of eucalypts that were monitored during this study there were some individual plants within a population that had almost finished flowering while others had barely commenced flowering. In none of the populations was there an obvious gradient in flowering times across a population with some topographical feature, more often plants that were well advanced with their flowering were next to plants that had barely started to flower (e.g. Fig. 4 & 5). This pattern suggests that the timing of flowering within these populations of plants is influenced at least to some extent by genetic differences rather than local environments, since plants a few metres apart often differed in the timing of their flowering. This spread of individual flowering times within a population has important implications for gene flow and also extends the period of time that plants will be flowering in an area, potentially increasing the time that apiaries can be based at a site.

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Figure 4. Per cent through flowering for populations of Eucalyptus leucoxylon (top) and Eucalyptus fasciculosa (bottom) in spring 2006 at Scott Conservation Park. Each point represents an individual plant, the darker the spot the more advanced through the flowering season. Percent through the flowering season is calculated as the percent of flowers that had finished plus half of the per cent of flowers that were flowering (i.e. not buds or recently finished).

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Figure 5. Percent through the flowering season for a population of Eucalyptus goniocalyx at Para Wirra Recreation Park in March 2005. Each point represents the position of an individual plant. The darker the spot the more advanced through the flowering season. Percent through the flowering season is calculated as the per cent of flowers that had finished plus half of the per cent of flowers that were flowering (i.e. not buds or recently finished).

Use of floral resources by honeybees and other fauna

Nectar sources The rates at which flowers were visited by native fauna and honeybees were assessed for ten species of eucalypts on 33 separate occasions, across three different settings: remnant vegetation, paddock trees and revegetation (Table 5). For most species and on most occasions, honeybees were more frequent floral visitors than other invertebrates and birds, accounting for more than 100 visits per flower per day for at least three species of eucalypt (E. cosmophylla, E. odorata and E. torquata) on some occasions. For another four species of eucalypts, honeybees made at least five visits per flower per day on most occasions (Table 5). The other major visitors to flowers were various species of honeyeaters, lorikeets, Silvereyes and Crimson Rosellas, the latter often removing flowers to harvest nectar from them. Non-honeybee invertebrates (mainly ants, flies, wasps, native bees), smaller in size than honeybees, were sometimes abundant at flowers but because they moved between flowers infrequently they usually accounted for less than 5% of the invertebrate visits to flowers (details not provided) and so were considered unimportant floral visitors with respect to resource consumption.

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The rates at which birds visited flowers varied dramatically both within a species and between species, ranging from 0 - 23.4 visits/flower/day. On more than half of the occasions birds made less than 1 visit/flower/day suggesting that floral resources often exceeded the numbers of birds available to exploit them. In general, those eucalypts (e.g. E. calycogona, E. fasciculosa, E. odorata) with small flowers and producing low to moderate quantities of nectar (<2 mg/fl/d) received 0 - 1.4 visits/flower/day from birds. Those species that had larger flowers and produced higher amounts of nectar (E. cosmophylla, E. leucoxylon, E. torquata, Table 1) typically had visitation rates ranging from 0.1 - 10 visits/flower/day (Table 5). On two occasions, both involving eucalypts in remnant vegetation, the rates at which birds visited flowers exceeded 20 times per flower per day. These both coincided with times when there were few other plants in flower. There are limited data on the rates at which individual flowers of eucalypts are visited by birds or honeybees. However, honeyeaters have been reported visiting the flowers of eucalypts as frequently as 10-40 times per flower per day for E. cosmophylla and 15-29 times per flower per day for E. leucoxylon (Paton 1982a, 1985, 1986a, 1990). At these times the birds were defending individual feeding territories, suggesting that food resources were limited (Ford 1979, 1981, Ford and Paton1982, Paton 1985). Rates of visitation to individual flowers by honeyeaters for these two species were generally much lower during the current study with territorial behaviour being observed on only one occasion when Red Wattlebirds and New Holland Honeyeaters defended parts of the canopies of E. leucoxylon in remnant vegetation at Inman Valley in December 2004. At this time visitation rates to flowers by birds were over 20 visits per flower per day. These were by far the highest rates of visits to flowers for this species during the current study. Standing crops of nectar were also the lowest for this species at this time (Table 1). For Eucalyptus leucoxylon visitation rates were generally higher in remnant vegetation than in paddock trees or revegetation, particularly in 2004 and 2006 when E. leucoxylon flowered more extensively (Table 5). In 2006 visitation rates to flowers by birds ranged from 0.17 - 0.81 visits/flower/day for paddock trees, from 0.61 - 3.05 visits/flower/day for re-vegetation and from 1.38 - 6.86 visits/flower/day for remnant vegetation. In 2004, a year of moderate flowering, paddock trees received 0.13 visits/flower/day and re-vegetation 0.33 visits/flower/day, while trees in remnant vegetation received 23.4 visits/flower/day. In 2005, a year with limited flowering, E. leucoxylon received 10-12 visits/flower/day for trees in both paddock and re-vegetation settings (Table 5). Populations of E. leucoxylon in remnant vegetation did not flower adequately in 2005 (only 5-18% of plants produced flowers, Table 4) to assess visitation rates in these areas in this year. These data indicate that Eucalyptus leucoxylon in paddock settings are not as heavily exploited by native birds as trees in remnant vegetation, particularly in those years when this species flowers extensively. An inability to access paddock trees does not account for the reduced bird activity at these trees, since paddock trees are accessed in years of poor flowering. Low visitation by birds to paddock trees in years when E. leucoxylon flowers extensively suggests a preference for the birds to forage at trees in remnant native vegetation. Two factors may account for this preference. First, some honeyeaters like the abundant New Holland Honeyeater nest in shrubs and so remnant vegetation provides opportunities to breed while scattered trees in paddocks do not. Second, on the approach of an aerial predator (e.g. sparrowhawk, goshawk) many honeyeaters, but particularly New Holland Honeyeaters, will retreat to the shrub layer where the vegetation is often denser. Trees in paddocks without a shrub layer do not afford the birds with the same opportunities to avoid potential predators. This pattern of reduced use of paddock trees was not seen for either Eucalyptus diversifolia or E. cosmophylla, where the frequency of bird visits to flowers were the same or marginally higher at paddock trees (Table 5). For both species, the paddock trees were small (<5m in height) and had dense canopies that often reached the ground. These dense canopies were

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such that honeyeaters, when challenged by an aerial predator, did not seek protection in other plants. The plants that were observed were also within 200 m of dense native vegetation and so the risks of predation for birds even accessing these plants let alone exploiting them were minimal compared to exploiting E. leucoxylon where paddock trees were up to 20 m tall, had much lower foliage densities and had canopies that rarely came within 3m of the ground. For these trees there was also no nearby remnant vegetation. Given that scattered paddock trees of E. leucoxylon provide lower quality habitat for honeyeaters and receive less attention from them, ongoing use of paddock trees by honeybees is less likely to be detrimental to native fauna than ongoing use of remnant vegetation. Even the use of E. leucoxylon in remnant vegetation by honeybees may not be detrimental to native fauna in years when this species flowers extensively. In both 2004 and 2006 there were substantial quantities of nectar still present in flowers at the end of the day (Table 1). For example, standing crops of nectar in flowers of E. leucoxylon in remnant vegetation varied from 3-15 mg sucrose equivalents per flower in 2006. A 20 g honeyeater the size of a New Holland Honeyeater needs to harvest about 5 g of sugar per day to meet its daily energy requirements (Paton 1982b). Given that New Holland Honeyeaters visit about 40 flowers per minute when foraging on E. leucoxylon, they can harvest their daily energy requirements in just 8 - 40 minutes of foraging (depending on standing crops) even at the end of the day. Since nectar levels are generally lowest at the end of the day (e.g. Paton 1982b, Paton 1985), honeyeaters and other native nectar-feeding fauna should have no difficulty harvesting their requirements under these conditions. Even in 2004 and 2005 when nectar resources were less abundant and visitation rates to flowers much higher, the lowest standing crops of nectar (0.8 mg/flower) for E. leucoxylon were still sufficient to allow even the largest honeyeaters to harvest their daily requirements. For example, the largest honeyeater in South Australia, the Red Wattlebird (average mass 110 g) requires about 12.5 g of sugar from nectar to meet its daily energy requirements. Given that these larger honeyeaters can visit around 50 flowers per minute (the faster rate reflecting their larger body size and greater reach), wattlebirds should harvest the nectar they need in about five hours, equivalent to foraging for less than 50% of daylight hours. Only when standing crops of nectar approach 0.2 mg sugar/flower do the flowers become uneconomic for honeyeaters to exploit. This threshold was only reached (by the end of the day) on 13 of 59 occasions and this primarily involved species of eucalypts with small flowers that produced little nectar, and were not used as extensively by birds.

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Table 5. Frequency to visits to flowers of various eucalypts by native birds and honeybees are provided for different settings and in different years in the Mt Lofty Region of South Australia. The presence of an apiary stationed within 700m of the observation trees is indicated by an asterisk. ns = not scored. Plant species Location Type Month Year Visits/flower/day Bird Honeybee Eucalyptus angulosa* Newland Hd Remn June 2005 29.58 10.33 Eucalyptus calycogona Monarto RV4 Reveg Oct 2004 0.001 9.01 Eucalyptus calycogona Monarto RV4 Reveg Aug 2006 0.51 9.02 Eucalyptus calycogona Monarto RV4 Reveg Oct 2006 0.01 2.24 Eucalyptus cosmophylla* Newland Hd Remn May 2006 1.84 106.84 Eucalyptus cosmophylla* Newland Hd Padd May 2006 3.27 103.49 Eucalyptus diversifolia* Newland Hd Remn Sep 2006 0.15 2.01 Eucalyptus diversifolia* Newland Hd Padd Sep 2006 1.52 0.97 Eucalyptus diversifolia* Newland Hd Remn Oct 2006 0.46 0.47 Eucalyptus fasciculosa* Newland Hd Remn Sep 2006 1.37 16.6 Eucalyptus fasciculosa* Newland Hd Remn Oct 2006 0.33 20.5 Eucalyptus fasciculosa* Scott CP Remn Oct 2006 0.73 1.7 Eucalyptus kruseana Monarto RV4 Reveg Oct 2004 0.05 0 Eucalyptus leucoxylon Monarto RV4 Reveg Oct 2004 0.33 4.45 Eucalyptus leucoxylon* Bingara Padd Dec 2004 0.13 7.02 Eucalyptus leucoxylon Inman Valley Remn Dec 2004 23.4 20.52 Eucalyptus leucoxylon* Para Woodland Padd Nov 2005 10.45 20.37 Eucalyptus leucoxylon Monarto RVB Reveg Nov 2005 11.86 0.96 Eucalyptus leucoxylon Monarto RV4 Reveg Aug 2006 3.05 0 Eucalyptus leucoxylon Monarto PHR Remn Sep 2006 6.86 8.99 Eucalyptus leucoxylon* Para Woodland Padd Sep 2006 0.79 8.99 Eucalyptus leucoxylon* Scott CP Remn Oct 2006 1.38 7.32 Eucalyptus leucoxylon Monarto RV4 Reveg Oct 2006 0.61 1.36 Eucalyptus leucoxylon* Scott CP Remn Nov 2006 4.34 8.11 Eucalyptus leucoxylon* Bingara Padd Nov 2006 0.81 7.74 Eucalyptus leucoxylon* Bingara Padd Nov 2006 0.17 7.24 Eucalyptus leucoxylon Inman Valley Remn Dec 2006 0.79 1.61 Eucalyptus odorata Monarto PHR Remn Mar 2006 0.39 107.88 Eucalyptus platypus* Monarto RVB Reveg Mar 2005 1.73 20.88 Eucalyptus platypus* Monarto RVB Reveg Apr 2005 ns 5.68 Eucalyptus torquata* Monarto RVB Reveg Mar 2005 ns 72.46 Eucalyptus torquata* Monarto RVB Reveg Apr 2005 6.31 100.05 Eucalyptus torquata Monarto RV4 Reveg May 2005 1.8 11.18

* managed hives known to be present within 700m at time of assessment of floral visitation.

Pollen sources used by honeybees at study sites Only a small number of plants provided significant sources of pollen to honeybees during the periods when key eucalypt species were in flower (Table 6). In areas with scattered trees, the primary pollen sources in spring when Eucalyptus leucoxylon and Eucalyptus fasciculosa (at some sites) were flowering were introduced weeds of pastures (Echium plantagineum, Hypochoeris glabra, Arctotheca calendula and Plantago sp.) and one species of native herb

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Gonocarpos elatus. Honeybees in these settings also harvested pollen from remnant Eucalyptus camaldulensis and Bursaria spinosa if these were sufficiently close to be accessible. At Mt Bold, where some native understorey shrubs still existed in the paddocks, the epacrid Lissanthe strigosa was exploited. In nearby woodland remnants (e.g. Scott Conservation Park) introduced plants in adjacent pastures were also prominent pollen sources for honeybees exploiting flowering E. leucoxylon and E. fasciculosa. This in part reflected the lack of native understorey plants that were in flower in natural areas during this study, perhaps reflecting the unusually dry conditions. However, most of the understorey plants in these woodlands flower in late winter or early spring prior to the sites being stocked with honeybees. However honeybees did use native Bursaria spinosa when it flowered in December. In areas of mallee-heath, Banksia ornata, Eucalyptus cosmophylla, E. diversifolia, Styphelia exarrhena and Brachyloma ericoides provided pollen from late autumn to early spring when honeybees were harvesting nectar from Eucalyptus cosmophylla, Banksia ornata and to a lesser extent E. fasciculosa and E. diversifolia. For the revegetation site at Monarto where there was no understorey and where the adjacent pasture was heavily grazed, the only pollen sources available were Eucalyptus torquata and E. platypus during the period of time when the bees were present, with both species providing the bees with nectar and pollen. Table 6. Major sources of pollen used by honeybees at selected study sites in the Mt Lofty region. Introduced plants are indicated with an asterisk. Site Period of

use Nectar sources Pollen sources

Bingara Sep-Jan Eucalyptus leucoxylon *Hypochoeris glabra Eucalyptus fasciculosa *Plantago sp. Eucalyptus camaldulensis Bursaria spinosa Scott Sep-Dec Eucalyptus leucoxylon *Echium plantagineum Eucalyptus fasciculosa *Arctotheca calendula *Echium plantagineum Bursaria spinosa Monarto Apr-Oct Eucalyptus torquata Eucalyptus torquata Eucalyptus platypus Eucalyptus platypus ParaWoodland Sep-Dec Eucalyptus leucoxylon *Echium plantagineum *Echium plantagineum *Arctotheca calendula Eucalyptus camaldulensis Gonocarpos elatus Eucalyptus camaldulensis Newland Head Mar-Jul Eucalyptus cosmophylla Banksia ornata Eucalyptus fasciculosa Eucalyptus cosmophylla Banksia ornata Eucalyptus diversifolia Eucalyptus diversifolia Styphelia exarrhena Brachyloma ericoides MtBold Aug-Nov Eucalyptus leucoxylon *Echium plantagineum *Echium plantagineum *Hypochoeris glabra Lissanthe strigosa The flowering of the major plant species providing pollen to honeybees also varied from year to year (Tables 3, 4, 7). Perennial native shrubs in particular produced few if any flowers in

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2007 and only the introduced annual species (Echium plantagineum) flowered moderately well in 2007 (Table 7). In contrast other annual herbs (e.g. Arctotheca calendula) produced few flowers in 2007, while the perennial Hypochoeris glabra produced less than half the flowers of the previous three years in 2007 (Table 7). These differences in the performances of annual and perennial plants are consistent with the annual cycles of the plants and rainfall. There was limited rainfall between early September 2006 and late April 2007 throughout most of the Mt Lofty Ranges (~100mm in total). Since this is the period when most of the perennial native shrubs initiate and develop buds for the next flowering season, limited, if any flowering of perennial shrubs should be expected in the following winter and spring. The same response probably applies to the perennial Hypochoeris. For annual plants like Echium plantagineum that germinate following rains in autumn and winter, the extent of flowering is more likely to reflect the conditions immediately prior to and during flowering. Since rainfall was close to average during late winter and spring in 2007, higher quantities of flowers would have been expected in 2007 than in the dry spring of 2006, as was observed (Table 7). Table 7. Flowering levels for selected shrubs and herbs used by honeybees as sources of pollen and nectar while exploiting floral resources from various species of eucalypt varied between years. Data for Banksia ornata are the mean number of inflorescences produced per m2 in each year. Data for other species are mean numbers of open flowers per m2 counted around peak flowering in each year, except for Styphelia exarrhena and Brachyloma ericoides which are mean number of open flowers per plant. (Information on the flowering of Arctotheca calendula was not assessed in areas where this plant was prominent. Information on the flowering levels of this plant were collected in plots established to monitor flowering of Hypochoeris and Echium, where Arctotheca was not abundant. Site Plant species 2004 2005 2006 2007 Newland Hd Banksia ornata 1.25 1.37 0 Styphelia exarrhena* 749 0 Brachyloma ericoides* 707 0 Bingara Hypochoeris glabra 12.9 10.4 13.2 4.9 Arctotheca calendula (0.85) (0.02) ParaWoodland Echium plantagineum 145 32 151 Arctotheca calendula (4.56) Ngarkat Banksia ornata 0.87 0.81 1.15 0.01 Messent Banksia ornata 0.30 0.23 0.32 0.02

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Long-term monitoring of Banksia ornata in Ngarkat Conservation Park. Figure 6 shows that there was increased mortality of Banksia ornata in drought years, with the mortality rate being greater for regenerating heaths that were less than 10 years post-fire than for mature heaths. In drought years, as much 10-25% of extant plants died, while in intervening years annual mortality was typically 5% or less. Background annual mortality in non drought years also appeared to be lower in the early 1990s than in later years, suggesting some cumulative effect of drier conditions on background rates of mortality. Floral production was also significantly reduced in drought years with negligible floral production in 2007 (Figure 7). The recovery of floral production by Banksia ornata following fires in December 1990, November 1997 and January 1999 is shown in Figure 8. Following the December 1990 fire, Banksia ornata took approximately five years to re-establish and produce a comparable number of inflorescences as mature heaths. However, a longer period of time, 6-7 years post-fire was required to recover floral production following the November 1997 fire, although floral production in these areas fell below mature heaths in the following year (Fig. 8). Comparable floral production on heaths burnt in January 1999, however, was yet to be attained nine years post fire. These data strongly suggest that recent post-fire recovery has been disrupted probably because of drought, increasing the period of time before beekeepers can return to use sites following fire.

0

5

10

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1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005

Ann

ual m

orta

lity (%

)

matureburnt 90-1

Figure 6. Annual mortality of Banksia ornata at Ngarkat Conservation Park from 1994 to 2005 is shown for mature heaths and heaths regenerating after being burnt in December 1990. Mature heaths were last burnt in 1978-9 and were at least 15 years post fire in 1994. Droughts occurred in 1995, 1997-8 and 2002-3. The period from 2000-01 was a less severe dry period.

29

0

100

200

300

400

500

600

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800

90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 05 06 07

cobs

Figure 7. Production of inflorescences (cobs) by Banksia ornata in mature heaths that were at least 10 years post-fire in 1990, with data representing the mean number of cobs produced per 50 m x 4 m quadrat. Drought years with an annual rainfall of <300 mm are shown with arrows along the x-axis. Recovery of vegetation and floral production from more recent fires is being monitored and initial indications are that the density of Banksia ornata plants will be markedly reduced following the 2006 fire. For example, in five 50 m x 4 m quadrats established in September 2005 that were burnt in January 2006, there were 788 mature Banksia ornata plants and an estimated 17,266 seeds present in infructescences on these plants. By December 2007, only 638 seedlings had established (3.7% germination rate) within these quadrats. Since Banksia ornata only establishes via seed in the year following fire, these data already indicate that the density of Banksia ornata plants will be lower following the 2006 fire. Given that many of these seedlings are likely to die before reaching maturity and producing inflorescences (e.g. Fig. 6), the density of mature Banksia ornata will be much lower post the 2006 fire than before. The productivity and post-fire recovery of other prominent plants that re-sprout following fire in these heath-lands was also low. For Allocasuarina pusilla, Leptospermum coriaceum, Leptospermum myrsinoides, and Phyllota pleurandroides only 16, 53, 68 and 26% of plants mapped prior to the 2006 fire survived to re-sprout post fire, respectively. Many of these plants were already showing signs of stress from recent droughts prior to the fire, with 92, 53, 61 and 60% of individual A. pusilla, L. coriaceum, L. myrsinoides and P. pleurandroides (respectively) showing at least 25% canopy dieback prior to the fire. Although these plants are not used extensively by honeybees, except A. pusilla that can be an important pollen

30

Figure 8. Rates of recovery of floral production for populations of Banksia ornata following three fires during the 1990s. The data show the number of inflorescences (cobs) produced by Banksia ornata per 50 m x 4 m quadrat in each year following each of the three fires. Stippled bars indicate the production of infloresences was lower on the regenerating heaths than in intact mature heaths, while solid bars indicate that inflorescence production was comparable to mature heaths that had not been burnt (Figure 7). The timing of fires is indicated by arrows above the x-axis. All areas regenerating after the December 1990 fire and November 1997 fire were re-burnt in January 2006.

burnt 1990-1

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90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 05 06 07

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burnt 1997-8

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90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 05 06 07

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burnt 1998-9

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90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 05 06 07

cobs

31

source in some years, the loss of canopy vigour during drought and poor recovery further illustrates likely changes to these heath-lands following recent droughts and fires. Given that predictions from climate change suggest an increase in the frequency and or severity of droughts and fires, key areas like Ngarkat are likely to continue to deteriorate as a significant resource base for beekeepers. Given the likely deterioration in floral resources in Ngarkat there is an increased premium on protecting remaining areas of comparable heathlands to the west and south-west of Ngarkat and closer to the coast, where rainfall is higher and droughts likely to be less severe. Although Banksia ornata still produced few flowers in these wetter areas in 2007 (e.g. Messent, Newland Head, Table 7), the better rainfall in these areas should result in reduced levels of dieback and mortality and so sustain plant population densities more effectively. If Banksia ornata is a key resource for the South Australian beekeeping industry then any attempts to re-establish these mallee heath systems should shy away from inland areas near Ngarkat and focus on re-constructing these systems in areas of higher rainfall within their former range.

Responses of plants to other extreme weather events: frosts Other environmental factors such as frosts that can affect plants may also change in frequency and intensity with climate change. In 2006 a severe frost in August in Messent resulted in all the large buds of Eucalyptus diversifolia being dropped over extensive areas of the park immediately prior to flowering. Much of the foliage was also burnt and the plants were still to recover and produce new shoots and buds 12 months later, with no flowering taking place in 2007. Eucalyptus incrassata was similarly affected while E. leucoxylon and E. fasciculosa were not affected. In nearby coastal scrubs along the Coorong, a suite of shrub species were also affected by this frost, including Leucopogon parviflorus, Acacia longifolia, Rhagodia candolleana, and Myoporum insulare. Of these plants, Leucopogon parviflorus is used frequently by apiarists in South Australia (Paton et al. 2004b). For this species, over 40% of the plants lost at least half their canopies in the frost, and a further 7% were killed. For the other three species 26-28% of the plants lost at least half their canopies in the frost, while mortality associated with the frost was as high as 33% for Acacia longifolia but only 1-3% for the other two species. For all of these plants, flowering was severely reduced in spring 2006 and the plants were still in poor condition 12 months later, indicating that the 2006 frost affected floral production in more than the year of the severe frost for these species as well. Elsewhere, nectar production in Eucalyptus cosmophylla was affected by a severe frost at Newland Head in June 2006.

Baseline monitoring of plants and floral resources on farmland being set aside for restoration The primary aim of this section of the project was to document the current distributions of key plant species on three properties that had been largely cleared and used for grazing but were being set aside for ecological restoration and the re-establishment of native vegetation. Figures 9-12 show the distribution of eucalypts and one or more key understorey plant species (from a beekeeper perspective) for the Mt Bold, Para Woodland and Bingara properties prior to the establishment of revegetation and restoration works.

32

Each of these properties supported populations of at least four species of eucalypts, but usually only one or two species were sufficiently abundant to be of value to the honeybee industry (Table 6). There were no saplings or young trees present on any of the properties indicating that there had been no recent recruitment. Eucalyptus leucoxylon and to a lesser extent E. fasciculosa and/or E. camaldulensis were the tree species being used by beekeepers, as well as the introduced Echium plantagineum. Another introduced herb Hypochoeris glabra provided important quantities of pollen at two of the sites (Table 6, Figs. 11-12). Other sources of pollen (e.g. Lissanthe strigosa) were more limited in distribution and abundance (e.g. Fig. 10) The intention is to re-assess the distributions and abundances of plants and floral resources about every five years and so determine how floral resources from a beekeeper perspective change as these areas are restored. The likely changes will include a substantial reduction in the distribution and abundance of introduced plant species that are currently important sources of pollen (i.e. Echium and Hypochoeris) and an increase in the cover of various eucalypts, eventually. In the case of the introduced plants, changes will be determined largely by a reduction in the distribution of the plant species and in the level of cover within the areas in which the species still occur. For the various eucalypts, changes will be measured by changes in the abundance and canopy areas of trees over the property. For Para Woodland and Mt Bold, the removal of Echium plantagineum will reduce the quantities of nectar as well as pollen available for use by honeybees. The loss of nectar should be eventually compensated for by an increase in the abundances of E. leucoxylon. The flowers of Echium plantagineum are open for approximately one day and produce an average of 0.38mg sugar/fl/day (± 0.8, s.e., n= 3 days). At 400 flowers per m2 this amounts to 0.15g sugar/m2 or 1.5 kg sugar/ha being produced per day for the areas with a high density of Echium. If Echium is removed and replaced by E. leucoxylon, will E .leucoxylon produce a comparable amount of sugar? Estimates of the quantity of nectar produced by E. leucoxylon can be made from measures of nectar production per flower (Table 1), average floral densities from handspan estimates, the surface area (m2) of the canopy of a typical tree and a measure of the per cent of flowers that are open. At our study sites a typical E. leucoxylon produced 11.4 mg sugar/fl/day (s.e. = 0.8 mg, n = 13 days; Table 1). The median floral abundance was typically around 21-25 flowers per handspan of which 25% were typically open and functioning as flowers at any one time. Assuming an average of five open flowers per handspan (=0.04 m2) or 125 flowers per m2, the average E. leucoxylon produces 1.4 g sugar/m2 of canopy surface. This is about 10 times the maximum amount of nectar that can be produced per m2 by Echium plantagineum when present at high density. Paddock trees for E. leucoxylon were on average 11.8 m high, had an average minimum canopy height of 4.5 m and an average radius of 7.8 m. The typical shape of the trees was t = 2, m = 3 and b = 2, and on average the per cent canopy perimeter with foliage was 56%, giving an average surface area of canopy of 263 m2. Thus an average E. leucoxylon tree produces 0.38 kg sugar per day. At a low density of 10 trees per hectare (equivalent to 20% horizontal cover), E. leucoxylon would produce 3.8 kg sugar/ha/day. Although honeybees will share this resource with native birds, the quantity of nectar produced is more than double the amount produced by Echium plantagineum when present at high density. Thus replacing Echium with E. leucoxylon should result in a substantially higher quantity of nectar being produced. The concern from a honeybee perspective, however, will be in establishing alternative pollen sources for honeybees if Echium plantagineum is removed. There were relatively few native plant species that provided pollen in quantity to honeybees when E. leucoxylon was flowering even in intact systems, and at least some of these (e.g. various epacrids) are not easily re-established. Further work is required to identify a range of native understorey plants to consider in these re-vegetation programs to provide pollen. However, Echium, Hypochoeris,

33

and Artotheca may still be present in sufficient abundance in adjacent agricultural areas that will not be re-vegetated, to meet pollen needs.

Floral resources in the future Based on this study, the availability of floral resources for honeybees is likely to change in the future. Those changes are likely to be caused by changes in climate, particularly changes to the frequency and intensity of extreme events (drought, frost, fire) but also potentially to changes in the timing of rainfall. Changes in land use, due both to changes in agricultural systems and restoration programs, will also affect the distribution of future resources for beekeepers. In South Australia, the honeybee industry is particularly vulnerable to these changes because of the extent to which native vegetation has been cleared. In the heavily cleared Mt Lofty region, scattered paddock trees are used widely by apiarists and are an important resource for them. Assessments of the extent to which key floral resources (e.g. E. leucoxylon) were used near apiaries even within intact woodlands and mallee-heaths as well as revegetated systems indicated, at least for the period 2004-7, that there were often substantial quantities of nectar left unexploited in flowers at the end of the day. Those quantities were sufficient to meet the needs of native birds, the largest and most-energy demanding nectarivores in this system. On occasions, nectar even dripped from the flowers. Under these conditions continued access for beekeepers to these floral resources should be permitted. This is particularly true for scattered paddock trees that typically do not receive the same level of visitation as trees in intact systems. Whether the period from 2004-07 is atypical is not known. However, New Holland Honeyeaters bred poorly in the Mt Lofty Ranges during two of the last four years (2005, 2007) due to a lack of winter flowering by key understorey species (various epacrids, Banksia). In fact, 2005 and 2007 were the only two years since 1984 where the species has bred poorly (Paton 2006, unpubl.). Low numbers of this common honeyeater, therefore, may have contributed to the general lack of resource use during this period.

34

Figure 9. Map showing the location of various eucalypts on the 70 ha Mt Bold site.

35

Figure 10. Baseline measures of the distribution and abundance (% cover) of Hypochoeris glabra, Echium plantagineum, Lissanthe strigosa and eucalypts (all species combined) on the 70 ha study site at Mt Bold, prior to implementing restoration programs. The maps show % cover for each species or group of plants at the scale of 25 m x 25 m.

36

Figure 11. Baseline distribution of scattered trees and Echium plantagineum on circa 40 hectares of Para Woodland prior to any re-vegetation works. Densities of Echium reflect the abundances of plants and flowers with negligible < 1 flower/m2, low 1-10 flowers.m2, medium 11-50 flowers/m2, high 51-200 flowers/m2, very high 201-400 flowers/m2 and extreme >400 flowers/m2

Figure 12. Distribution of various species of eucalypts in circa 50 ha at Bingara showing the background distribution of Hypochoeris glabra.

37

The poor breeding performances of New Holland Honeyeaters in recent years indicate that the plant-pollinator systems of the Mt Lofty Ranges, already disrupted by extensive vegetation clearance (Paton 2000), are vulnerable to droughts and hence climate change. Since many of the plants used by these birds are also used by honeybees (e.g. Paton 1985, 1986b, 1996, Celebrezze & Paton 2004) the honeybee industry is equally vulnerable. The numbers of flowers produced by plants appears much more susceptible to droughts and extreme weather events than other aspects of flowering like nectar secretion. For most eucalypts the variation in the quantities of nectar produced were at most 2-fold across years and sites. Even in drought conditions, nectar production for key species like E. leucoxylon was similar to nectar production in years of better rainfall. Some reduction in nectar production, however, was detected for E. cosmophylla during a severe frost. In comparison the numbers of flowers produced by plants varied by as much as 10-fold, if not more within and between years, with many eucalypt populations failing to flower in some years. In some species there was synchrony between populations with respect to years of high versus low levels of flowering (E. leucoxylon) but for other species (E. camaldulensis) this was not the case. Both internal and external factors are likely to be involved in determining flowering levels in any one year. However, the flowering of many of the key plant species used by beekeepers is sensitive to droughts, although the effect of droughts may be reflected in the subsequent season and not necessarily in the year of the drought. For some species, the effect of a severe drought or severe frost may be expressed for several subsequent years (e.g. E. diversifolia, Banksia ornata). Given that droughts and extreme weather events, like frosts, are more likely in the future for southern Australia due to climate change, many of the more reliable sources of nectar exploited almost annually by beekeepers now are likely to much less reliable in the future. The frequency of fires is also likely to increase, and post-fire recovery of some systems may be greatly reduced and slowed by drought – with reductions in both the density of key plant species post-fire and increases in the time before these diminished populations flower. For example, for Ngarkat Conservation Park where currently more than 66% of the park (180,000 ha) is less than 10 years post-fire, low seedling recruitment, increased annual mortality and longer post-fire recovery times before flowering for Banksia ornata, coupled with negligible floral production during droughts suggest this park will be much less productive from a beekeeper perspective in the future. Climate change, therefore, is a significant threat to the maintenance of floral resources of value to the honeybee industry and the industry needs to develop strategies to overcome the likely reduced availability of key floral resources in the near future. Revegetation including forestry and carbon sequestration plantings may provide opportunities to grow floral resources for the honeybee industry depending on the species that are planted and the planting densities. Planted trees, once mature, produce comparable amounts of nectar on a per flower basis, but high planting densities may affect the production of flowers. For example, only 20% of regenerating E. camaldulensis growing at high densities (ca 2500 plants/ha) produced flowers and those that did flower produced no more than 11-15 flowers/handspan while nearby remnant trees (<50 plants/ha) all flowered with a median of 41-50 flowers/handspan. Whether new plantings have the potential to provide significant quantities of floral resources for beekeepers will also depend on the total areas of the plantings. In South Australia, but particularly the Mt Lofty region, the re-establishment of large areas of native vegetation is being promoted and implemented across agricultural areas to address imminent losses of biodiversity. The long-term target for this region is to re-establish native vegetation to 30% of

38

its original cover, with an initial emphasis on the disproportionately cleared systems (NRM Plan). The disproportionately cleared systems include grassy woodlands and coastal mallee-heaths that contain species of importance to the local honeybee industry, such as Eucalyptus leucoxylon, E. fasciculosa, E. camaldulensis, E. odorata, E. microcarpa, E. porosa, E. cosmophylla, E. diversifolia and E. angulosa as well as Banksia ornata. For this region at least there is an opportunity to secure significant additional floral resources for the honeybee industry within those plantings. Many of the revegetation programs to date have resulted in a few species being planted in plots at high densities (e.g. Paton et al. 2004a). At high densities, the widths of the canopies of the trees are relatively narrow being constrained by the canopies of adjacent trees (Table 8). For example, at densities of ≥1600 trees per hectare the average distance between trees is 2.5m or less, and the average canopy radius is 1.5m or less, even for trees taller than 10m. At lower densities of around 250 trees per hectare (about 6-7m between the trunks of trees), the average canopy radius was 3-4m with the canopies of adjacent trees also abutting. In contrast, when tree densities were below 50 trees/ha (>14m between tree trunks) adjacent canopies did not abut, and the average canopy radius varied from 5-8m for both E. leucoxylon and E. camaldulensis (Table 8). From a floral production perspective, planting at lower densities does not necessarily reduce the quantities of floral resources that can be produced on a site since trees at low density, because of their broader canopies, have canopy surface areas that are as much as ten times those of trees in the densest plantings (Table 8). In fact planting at lower densities may lead to greater overall floral production because trees in dense plantings produce far fewer flowers per unit area of canopy than widely spaced trees (see above). A range of tree species should also be planted in each area, particularly complementary species that flower in years when other species do not flower and vice versa (e.g. E. angulosa, E. cosmophylla). The woodland systems currently being targeted for revegetation typically consist of 4-6 species of eucalypts (e.g. Fig 9, 11,12) with the different eucalypts presumably responding to local heterogeneity in soils, topography and aspect. Given this, future plantings should include at least four or five species of eucalypts. In addition, a range of understorey species should also be considered. From a beekeeping perspective, these need to include shrubs capable of providing pollen for honeybees. At present honeybees tend to harvest the bulk of their pollen from introduced plants while exploiting the nectar produced by scattered paddock eucalypts. Relatively little pollen was harvested from native shrubs and more work is required to identify a range of native plants that can provide pollen at the time when some key eucalypts are flowering. To some extent, the dry conditions prevented many native shrubs from flowering particularly in 2007, and observations in years when more of these native plants are flowering may provide some additional species that could be included in plantings. Gonocarpos elatus, Lissanthe strigosa, Bursaria spinosa, and Banksia ornata all provide pollen to honeybees. These should be included in planting programs, provided the soils, topography and aspects are appropriate for them. Clearly more work is required to identify additional native plant species that provide significant quantities of pollen to honeybees so that they can be incorporated into future plantings as well.

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Table 8. Influence of tree density on the shape and surface areas of the canopies of various eucalypts. The table shows the average height, canopy radius, minimum height of the canopy above the ground, and the per cent of the canopy perimeter with foliage for E. leucoxylon and E. camaldulensis from the Mt Lofty Ranges (MLR) and Kangaroo Island (KI) and for a suite of eucalypt species planted at Monarto. The horizontal area occupied by the average tree and the canopy surface area have been calculated from the average tree dimensions. All except two populations of trees were in areas of natural regeneration in paddocks (KI) or in re-vegetated areas (MLR, Mon), except for two populations of remnant trees identified with an asterisk. Species Region

or Site

Density (trees/ha)

Tree height

(m)

Canopy radius

(m)

Min Canopy Height

(m)

% perimeter

with foliage

Hor. area

(m2)

Canopy surface

area (m2)

E. leucoxylon MLR ~ 1600 10.5 1.3 3.7 46 6 28 E. leucoxylon MLR ~ 250 10.4 3.8 4.3 61 46 99 E. leucoxylon* MLR ~ 25* 11.8 7.8 4.5 56 191 263 E. camaldulensis MLR ~ 1600 11.4 1.5 4.0 29 8 14 E. camaldulensis MLR ~ 250 11.3 4.0 4.6 38 52 78 E. camaldulensis KI ~ 2500 10.1 0.9 3.5 39 3 14 E. camaldulensis KI ~ 50 9.6 5.1 4.4 55 105 125 E. camaldulensis* KI ~ 50* 15.3 6.0 6.1 48 122 215 Eucalyptus spp Mon ~ 250 9.0 3.0 4.6 54 28 45 Revegetation guidelines generally promote the use of local genetic provenances when re-establishing habitat. However, given climate change, there may be merit in broadening the range of plants planted to include species of native plants not found locally, since these may be less sensitive to the anticipated changes in climate. Including such plants helps minimise the risk that the plantings fail altogether. Within the Monarto plantations, a wide range of eucalypts, including species endemic to parts of Western Australia, have been planted. These plantings now provide an opportunity to assess the performances of these plants under different conditions relative to local species. Two species of Western Australian eucalypt (E. platypus and E. torquata) currently used by beekeepers flowered more consistently than two endemic eucalypts (E. calycogona, E. leucoxylon) in these plantings (Table 3). Importantly the two Western Australian species appeared far less sensitive to drought, flowering extensively in 2007, while the two local species failed to flower in 2007. Most of the monitoring programs that have been established have only been operating for 3-4 years and a much longer period is required to properly assess the influence of droughts, fires, and frosts, as well as changes in the timing and extent of rainfall on the flowering performances of native plants and whether there are any lasting effects. The monitoring programs also need to be broadened to include other plant species and other regions. The simple handspan technique provides a relatively simple way for others, including beekeepers, to be involved in documenting changes in floral resources, particularly those on which their industry depends.

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Conservation Park. RIRDC, Canberra

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banding data. (Final report to DEH, Adelaide) Paton,D.C. Crossfield, E.L., Hurrell, B & Rogers, D.J. 2004b. Floral resources used by the

South Australian Apiary Industry. RIRDC, Canberra Paton, D.C., Gates, J.A. & Pedler, L.P. 2002. Birds. In M.Davies, C.R. Twidale, & M.J. Tyler

(eds). Natural History of Kangaroo Isalnd. 2nd edition. pp 88-110. Royal Soc. S.Aust., Adelaide

Paton, D.C., Prescott, A.M, Davies, R. J-P. and Heard, L.M. 1999. The distribution, status and

threats to temperate woodlands in South Australia. pp 57-85. In R.J. Hobbs & C.J.Yates (eds). Temperate Eucalypt Woodlands in Australia. Biology, Conservation, Management and Restoration. Surrey Beatty & Sons, Chipping Norton

Paton, D.C., Rogers, D.J. & Cutten, J. 2005b. Spatial and temporal aspects to the distribution

and spread of Mundulla Yellows. (Final report to DEH, Adelaide) Paton, D.C., Rogers, D.J. & Harris, W. 2004a. Birdscaping the environment: restoring the

woodland system of the Mt Lofty region, South Australia. Pp 331-358. In D. Lunney (ed.) Conservation of Australia's forest fauna (second edition). (Royal Zool. Soc. NSW, Mosman)

Paton, D.C., Rogers, D.J. & McInerney J. 2005a. Health and status of eucalypts in the South-

East of South Australia (Final report to the Native Vegetation Council, DWLBC) Ward, M.J. 2005. Patterns of box mistletoe Amyema miquelii infection and pink gum

Eucalyptus fasciculosa condition in the Mount Lofty Ranges, South Australia. Forest Ecol. & Management 213: 1-14

Securing Long-Term Floral Resources for the Honeybee Industry

by David PatonRIRDC Pub. No. 08/087

Contact RIRDC:Level 2

15 National CircuitBarton ACT 2600

PO Box 4776Kingston ACT 2604

Ph: 02 6271 4100Fax: 02 6271 4199

Email: rirdc@rirdc.gov.auweb: www.rirdc.gov.au

This publication can be viewed and purchased from our webstie:

www.rirdc.gov.au

Photos: Top­ – Foraging on Eucalyptus cosmophylla; bottom left – Eucalyptus fasciculosa; bottom right – Eucalyptus leucoxylon

The Australian honeybee industry dep­ends on floral resources p­rovided by a variety of native and exotic p­lants. These resources are changing as a consequence of vegetation clearance, dieback of rural trees, imp­roved control of exotic p­lants, and intensification of agriculture. Climate change also has the p­otential to affect floral resources.

This rep­ort documents the floral resources used by the honeybee industry in rural landscap­es of South Australia, p­articularly the Mt Lofty Ranges. Various sp­ecies of eucalyp­t are imp­ortant sources of nectar for honeybees in this region.

The rep­ort p­rovides information on the use of different floral resources by the honeybee industry, and how the flowering levels of key p­lant sp­ecies changes over time and following p­erturbations like fire and drought. Since fire and drought

are more likely in southern Australia due to climate change, monitoring the p­erformances of the p­lants during and following the current drought, and following recent fires, p­rovides a strong basis for p­redicting future changes to floral resources.

The Rural Industries Research and Develop­ment Corp­oration (RIRDC) manages and funds p­riority research and translates results into p­ractical outcomes for industry. Our business is about new p­roducts and services and better ways of p­roducing them. Most of the information we p­roduce can be downloaded for free from our website: www.rirdc.gov.au.

RIRDC books can be p­urchased by p­honing 02 6271 4160 or online at: www.rirdc.gov.au/eshop­.

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