The risk of pollen-mediated gene flow from exotic Corymbia plantations into native Corymbia populations in Australia

Forest Ecology and Management 256 (2008) 1–19

Contents lists available at ScienceDirect

Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco

Review

The risk of pollen-mediated gene flow from exotic Corymbia plantations into native Corymbia populations in Australia R.C. Barbour a,*, A.C. Crawford b, M. Henson c, D.J. Lee d, B.M. Potts a, M. Shepherd b a

School of Plant Science and Cooperative Research Centre for Forestry, University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia Centre for Plant Conservation Genetics and Cooperative Research Centre for Forestry, Southern Cross University, P.O. Box 157, Lismore, New South Wales 2480, Australia c Forests New South Wales, P.O. Box J19, Coffs Harbour Jetty 2450, Australia d Queensland Department of Primary Industries & Fisheries and Sunshine Coast University, Locked Bag 16 Fraser Road, Gympie, Queensland 4570, Australia b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 7 December 2007 Received in revised form 21 February 2008 Accepted 10 March 2008

Sectors of the forest plantation industry in Australia are set to expand in the near future using species or hybrids of the spotted gums (Corymbia, Section Politaria). Plantations of these taxa have already been introduced across temperate and subtropical Australia, representing locally exotic introductions from native stands in Queensland and New South Wales. A literature review was undertaken to provide insights into the potential for pollen-mediated gene flow from these plantations into native populations. Three factors suggest that such gene flow is likely; (1) interspecific hybridisation within the genus has frequently been recorded, including between distantly related species from different sections, (2) apparent high levels of vertebrate pollinator activity may result in plantation pollen being moved over hundreds of kilometres, (3) much of the plantation estate is being established among closely related taxa and therefore few barriers to gene flow are expected. Across Australia, 20 of the 100 native Corymbia taxa were found to have regional level co-occurrence with plantations. These were located most notably within regions of north-east New South Wales and south-east Queensland, however, co-occurrence was also found in south-west Western Australia and eastern Victoria. The native species found to have cooccurrence were then assessed for the presence of reproductive barriers at each step in the process of gene flow that may reduce the number of species at risk even further. The available data suggest three risk categories exist for Corymbia. The highest risk was for gene flow from plantations of spotted gums to native populations of spotted gums. This was based on the expected limited existence of pre- and postzygotic barriers, substantial long-distance pollen dispersal and an apparent broad period of flowering in Corymbia citriodora subsp. variegata plantations. The following risk category focussed on gene flow from Corymbia torelliana  C. c. variegata hybrid plantations into native C. c. variegata, as the barriers associated with the production and establishment of F1 hybrids have been circumvented. For the lowest risk category, Corymbia plantations may present a risk to other non-spotted gum species, however, further investigation of the particular cross-combinations is required. A list of research directions is provided to better quantify these risks. Empirical data will need to be combined within a risk assessment framework that will not only estimate the likelihood of exotic gene flow, but also consider the conservation status/ value of the native populations. In addition, the potential impacts of pollen flow from plantations will need to be weighed up against their various economic and environmental benefits. ß 2008 Elsevier B.V. All rights reserved.

Keywords: Biological invasions Exotic species Plantation forestry Off-site impacts Genetic pollution Genetic contamination

Contents 1.

2. 3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Genetic impacts of pollen flow from exotic species . . . . . . . . . 1.2. Exotic gene flow from hardwood plantations in Australia . . . . Use of Corymbia for plantation forestry . . . . . . . . . . . . . . . . . . . . . . . . Definition of exotic gene flow in the context of Australian eucalypts

* Corresponding author. Tel.: +61 3 62262603; fax: +61 3 62262698. E-mail address: [email protected] (R.C. Barbour). 0378-1127/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2008.03.028

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

2 2 2 3 3

2

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

4.

5. 6. 7.

8. 9.

Taxonomy of Corymbia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Higher order taxonomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Taxonomy and natural distribution of the spotted gums (Section Politaria) and C. torelliana (Section Cadagaria) . . . . . . . . . . . . . . . . Patterns of hybridisation within the genus Corymbia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Geographical proximity of native populations to Corymbia plantations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Risk assessment framework for pollen-mediated gene flow . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Pollen production and release from plantations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Flowering phenology and interspecific synchrony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3. Distance of pollen dispersal from plantations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3.1. Patterns of pollen flow in eucalypts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3.2. Vectors of pollen flow in Corymbia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3.3. Techniques for assessing gene flow from Corymbia plantations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3.4. Seed dispersal from plantations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4. Crossing-incompatibilities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5. Hybrid survival and fitness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.1. F1 hybrid seedling establishment through to reproductive maturity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5.2. Second-generation hybridisation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Species at greatest apparent risk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Research directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . .

4 4 4 5 5 6 6 8 10 10 11 12 13 13 14 14 14 15 16 16 17

1. Introduction

1.2. Exotic gene flow from hardwood plantations in Australia

1.1. Genetic impacts of pollen flow from exotic species

In Australia, over 807,000 ha of hardwood plantations have been established for pulpwood and sawlog production (National Forest Inventory, 2007), the majority of which have been established across temperate regions of the country using Eucalyptus globulus and Eucalyptus nitens (National Forest Inventory, 2006). As the genus Eucalyptus dominates the majority of native non-arid woodland and forest communities throughout Australia (Wardell-Johnson et al., 1997), the potential for pollenmediated gene flow from locally exotic plantations into native eucalypt populations appears to exist (Strauss, 2001; Potts et al., 2003; Kanowski et al., 2005; Salt et al., 2005). Considerable research is being conducted into the extent to which gene flow from E. globulus and E. nitens may occur (Barbour et al., 2002, 2003, 2005a,b, 2006a,b, 2007, 2008), and results to date have shown that despite initial concerns of broad-scale genetic invasion, the number of species and populations at risk appear to be reducing as further biological information is gathered (Barbour et al., 2006b, 2008). Nevertheless, specific sites and species are being recognised to be of particular risk. These include the rare Eucalyptus perriniana, which now has E. nitens plantations near the largest of its three small populations in Tasmania. The E. nitens and E. perriniana appear to flower synchronously (Barbour et al., 2006b), be within pollen dispersal range (Barbour et al., 2005b) and are crosscompatible (Barbour et al., 2005a). In another example, assessments of the widely distributed Eucalyptus ovata, which is frequently found adjacent to plantations of both E. globulus and E. nitens, have found exotic F1 hybrids within native openpollinated seed lots and as seedlings in the wild (Barbour et al., 2003, 2008). Indeed, seed collections from fragmented populations of E. ovata growing adjacent to E. nitens have found levels of hybridisation as high as 56% for individual trees (Barbour et al., 2005b). However, early results from field trials have suggested that the E. ovata  E. nitens F1 hybrids may be less fit than local E. ovata, and in the long-term selected against (Barbour et al., 2006a). Consequently, despite the range of potential barriers that can exist to prevent gene flow from exotic plantations in Australia, detailed case-by-case analysis is required to identify the native populations for which such barriers are not effective. The large-scale expansion of hardwood plantations seen throughout the productive temperate regions of Australia is,

The movement of pollen from agricultural crops or introduced species can have significant genetic impacts on sympatric native populations through hybridisation and introgression (Ellstrand, 1992b; Rhymer and Simberloff, 1996; Vila et al., 2000; Wolf et al., 2001). Such gene movement has received considerable attention following concerns over the escape of genetically modified crops (Hoffman, 1990; Raybould and Gray, 1994; Chapman and Burke, 2006), as well as in regard to the evolution and invasion of weeds from short-rotation crop species (Small, 1984; Van Raamsdonk and Van Der Maesen, 1996; Snow et al., 2001). Increasingly, however, the potential impacts of pollen flow from exotic species into native populations are receiving attention (Shapcott, 1998; Figueroa et al., 2003; Brock, 2004; Vanden Broeck et al., 2005). Such movement can facilitate the invasion of exotic genes through F1 hybridisation and backcrossing (Rhymer and Simberloff, 1996; Arnold, 1997; Ellstrand et al., 1999). This process can result in the alteration of natural patterns of genetic diversity, reducing the genetic integrity of native populations and in some cases result in the extinction of ‘‘pure’’ native species (Levin et al., 1996; Rhymer and Simberloff, 1996; Ellstrand et al., 1999; Vila et al., 2000). Because the introgression of exotic genes can result in significant phenotypic alterations to recipient native species, gene flow can also have broader community level impacts particularly when foundation or keystone species are affected (Anttila et al., 1998; Whitham et al., 2006). The extent to which exotic gene flow can impact on native species is driven by a range of pre- and post-zygotic barriers (Levin, 1978). These barriers include reductions in the quantity of exotic pollen released, limitations in the distance over which it can be dispersed, flowering time asynchrony, crossing-incompatibilities, and reduced hybrid fitness (Levin, 1978; Potts et al., 2003). The source/sink ratio of exotic pollen to receptive native flowers can also strongly influence gene flow, resulting in rare or small populations being at a particular risk of extinction through pollen swamping (Ellstrand, 1992b; Levin et al., 1996). The converse of this, however, is that small-scale plantings may have little impact on large native populations.

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

3

Table 1 Area (ha) and regional location of Corymbia plantations established across Australia Region

Species

Area

Botanical regions

Source

South-east QLD and northern NSW

C. C. C. C. C. C. C.

18,000

Burnett, Darling Downs, Moreton, Port Curtis, Wide Bay/North Coast, Northern Tablelands Central Coast, Central Western Slopes South-west Victorian Volcanic Plain, Wannon East Gippsland

Lee (2007), H. Smith (personal communication) and M. Henson (personal communication) M. Henson (personal communication) R. Moore (personal communication) T. Jackson (personal communication) P. Noble (personal communication)

Central coastal NSW South-west Western Australia Western Victoria Eastern Victoria

henryi, C. maculata, torelliana F1 hybrid, c. variegata maculata, C. c. variegata maculata maculata maculata, C. c. variegata

Total

10 2,000 600 100 20,710

however, yet to occur within other regions, despite considerable interest (Commonwealth of Australia, 2002; Dickinson et al., 2004, 2005; Lee, 2007). Species of the genus Corymbia have displayed some of the greatest potential for broadening the national plantation estate into the humid and low rainfall regions of northern Australia (Dickinson et al., 2005; Lee et al., 2005; Lee, 2007). There is concern, however, that the planting of this genus may result in exotic gene flow to native Corymbia forests, for three reasons. Firstly, interspecific hybridisation within the Corymbia genus has frequently been documented, with unusually high levels noted for crosses between more distantly related species (i.e. intersectional crosses, Potts et al., 2003). Secondly, dispersal of seed and pollen by Corymbia species can potentially occur over large distances due to the specific vertebrate and invertebrate vectors involved (Wallace and Trueman, 1995; Southerton et al., 2004; Wallace et al., 2008). Thirdly, the majority of the estate has been established among native populations of the same species used for plantation establishment, or species that are closely related (Brooker and Kleinig, 1996; National Forest Inventory, 2006), which will likely result in the existence of few barriers to hybridisation. Consequently, investigation of the potential off-site genetic impacts of the fledgling Corymbia plantation industry may identify populations or species that are of particular concern prior to the expansion of the estate, and potentially allow pre-emptive management intervention if required. 2. Use of Corymbia for plantation forestry All Corymbia plantations that have currently been established have been done so for both pulp and solid wood production. The species used in plantations are restricted to the spotted gums (section Politaria), and in particular Corymbia maculata and Corymbia citriodora subsp. variegata (herein referred to as C. c. variegata, Lee, 2007; Smith et al., 2007). The majority of the industry is based on open-pollinated seed collected from native stands (currently established plantations) or seed orchards (increasingly used for establishments from 2009) rather than seed from artificial pollination (Lee, 2007; Smith et al., 2007). The seed sources most commonly used for C. c. variegata plantation seed orchard establishment are Woondum near Gympie and to a much lesser extent Grange and Richmond Range from northern New South Wales (Lee, 2007). The susceptibility of the spotted gums to Quambalaria Shoot Blight caused by the fungus Quambalaria pitereka has also resulted in increasing interest in crossing C. c. variegata with Corymbia torelliana (section Cadagaria), as the hybrids appear considerably more robust to fungal infection (Lee, 2007). Hybrids also show other beneficial traits including vigorous growth and frost resistance, and are easily propagated via cloning (Lee, 2007). While the majority of reproductively mature plantings of the hybrids are as research trials in southern Queensland and northern New South Wales, deployment into commercial plantations has recently begun in southern Queensland.

Across Australia, approximately 21,000 ha of Corymbia plantations have been established (Table 1). While this current estate is not large it provides insights into the likely locations of further expansion. In south-west Western Australia, approximately 2000 ha of C. c. maculata have been established, while in remaining areas of this state, the Northern Territory, South Australia and Tasmania plantations of Corymbia have not been established. In northern New South Wales and south-east Queensland, approximately 18,000 ha of C. c. variegata and the C. torelliana hybrid have been planted. Further south in the Central and North Coast regions of New South Wales small-scale plantings of ca. 10 ha of C. maculata have been conducted. In western Victoria, approximately 600 ha of C. maculata plantations have been established near Cavendish in the Green Triangle, while a small area of C. maculata and C. c. variegata has been established in east Gippsland, eastern Victoria. 3. Definition of exotic gene flow in the context of Australian eucalypts Exotic gene flow refers to hybridisation and the introgression of genetic material from domesticated or non-local populations into native populations. This process occurs through the establishment of F1 hybrids following pollen flow from plantations into native forests, survival and growth of these hybrids to reproductive maturity, and backcross hybridisation with native populations. Latter generation backcrossing finally results in the ‘‘mixing’’ or complete introgression of the introduced genes. This process can also occur through seed dispersal from plantations followed by maturation of seedling to allow subsequent crossing. Because seed movement from plantations is generally limited, the following review focuses primarily on the impacts of pollen movement. Other terms such as ‘‘genetic pollution’’, ‘‘genetic contamination’’ and pollen-mediated gene flow, all describe the same process but differ in the degree to which they place the process in a negative light. Gene flow is a natural process that continually occurs within and between native populations, however, in the current case involves the genes of any exotic species, population or improved germplasm planted outside its natural range. The extent to which an introduced population is ‘‘exotic’’ is driven by the degree to which it represents novelty in its new environment. This is firstly influenced by the geographical distance from its native origin, which affects the extent to which it would have been in reproductive contact with native species previously, during both recent and evolutionary time. Secondly, novelty is driven by the genetic relatedness of an introduced species compared to surrounding native populations. While Corymbia is native to Australia, the translocation of east coast species such as C. maculata into the range of West Australian C. calophylla populations, not only places two species into sympatry that have previously been isolated for approximately 9 million years (Hill, 1994; see also Hill and Johnson, 1995), but also two species that have substantial molecular and quantitative genetic differences (Section 4.1). The planting of C. c.

4

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

variegata adjacent to native Corymbia henryi populations in northern New South Wales, however, places two closely related species into reproductive contact that co-occur naturally to some degree. In such situations, while the genetic novelty of exotic gene flow ‘‘per pollen grain’’ may be less, the levels of hybridisation that occur may be greater due to their close relatedness resulting in fewer reproductive barriers, potentially resulting in equivalent genetic impact. 4. Taxonomy of Corymbia 4.1. Higher order taxonomy The taxonomy of the eucalypts has been controversial, with a number of classifications proposed (Pryor and Johnson, 1971; Hill and Johnson, 1995; Brooker, 2000; Ladiges and Udovicic, 2000). This review follows the eucalypt species taxonomy of EUCLID (CPBR, 2006; Supplementary data 1) which is based on Hill and Johnson (1995) with the Corymbia forming a separate genus to Eucalyptus and Angophora (Ladiges and Udovicic, 2000). The taxonomy of EUCLID, however, has been adjusted according to King (2004) (see also Section 4.2) in regard to section Politaria. This treatment of Corymbia as a separate genus differs from the previous classification by Pryor and Johnson (1971) and Brooker (2000) which recognised Corymbia as a subgenus within Eucalyptus. The genus Corymbia is comprised of seven sections; Fundoria, Apteria and Rufaria (red bloodwoods), Politaria (spotted gums), Cadagaria, Ochraria (yellow bloodwoods) and Blakearia (ghost gums). Phylogenetic studies by Hill and Johnson (1995) were not able to resolve the precise relationship among the Politaria, Cadagaria and Ochraria. These sections were distinct from the Blakearia, and collectively formed a separate clade to the Fundoria, Apteria and Rufaria (Fig. 1). Recent molecular phylogenetic analysis has provided strong evidence for the splitting of Angophora, Corymbia and Eucalyptus into separate genera. Initial molecular studies attempting to resolve the higher order taxonomy of the eucalypts were limited by the character sets of the ITS regions used and the number of taxa assessed (Udovicic et al., 1995; Steane et al., 1999; Udovicic and Ladiges, 2000). Several recent efforts addressing these issues and expanding the character set of the markers have corroborated the uniqueness of the Corymbia lineage (Steane et al., 2002; Ochieng et al., 2007a,b; Parra-O et al., 2007). 4.2. Taxonomy and natural distribution of the spotted gums (Section Politaria) and C. torelliana (Section Cadagaria) Spotted gums are a complex of closely related taxa that naturally occur along the eastern seaboard of Australia from

around latitude 168 in north Queensland to latitude 378 in eastern Victoria (Hill and Johnson, 1995). Their taxonomy remains controversial as classification often relies on subtle variation in morphology and leaf oils, and knowledge of the geographic origins of a specimen (McDonald and Bean, 2000; McDonald et al., 2000). Four taxa, three of which occur as a latitudinal replacement series, were recognised by Hill and Johnson (1995) in their revision of the genus. C. c. citriodora is distributed from south-west of Cooktown to south of Gladstone, and west to the Great Dividing Range west of Springsure (Qld), with a major disjunction of 300 km separating northern and southern populations (Hill and Johnson, 1995, Fig. 2). C. c. variegata has a wide range from the Carnarvon and Dawes Ranges north of Monto (Queensland), contracting southwards to sub-coastal regions south to Nymboida River and north-west of Coffs Harbour in NSW (Hill and Johnson, 1995). Intergrades and hybrids with C. c. citriodora are believed to occur in the north-east of C. c. variegata’s range. C. henryi tends to occur on less fertile low lying country from Brisbane (Queensland) in the north to near Glenreagh south of Grafton in NSW in the south. Hybrids or intergrades are expected with C. c. variegata where they co-occur. C. maculata occurs mainly along the coast of NSW from the Manning River valley in the north to near Bega in the south, with outlying occurrences near Nowa in eastern Victoria (Hill and Johnson, 1995). Isozyme analyses have shown distinct geographic structuring within spotted gums with two distinct genetic alliances suggested: C. c. citriodora–C. c. variegata and C. henryi–C. maculata (McDonald et al., 2000). Subsequent reanalysis of this data however, revealed that selection at one locus, PGM2, had inflated genetic distance estimates between C. henryi and the other northern taxa, with the effect of exaggerating the affinity between C. henryi and C. maculata (King, 2004). Analysis of the diversity and distribution of chloroplast DNA haplotypes confirmed low levels of differentiation among northern spotted gum taxa, the distinctness of C. maculata from northern taxa, and population subdivision within C. maculata (King, 2004). More recently, analysis based on microsatellite markers to revisit genetic structuring in spotted gums concluded there were at least four but probably five recognisable populations in spotted gums (Fig. 2, Shepherd et al., 2008). These delineations had poor alignment with current taxonomic groups, but rather, appeared more strongly driven by geographic barriers. C. maculata was resolved as a taxon and had the greatest genetic distance to any other population. Three clusters were evident within the northern taxa but alignment with taxonomic groupings was poor. C. citriodora material from north of the major disjunction in central Queensland formed a northern population. C. c. citriodora, C. c.

Fig. 1. Taxonomic relationships among Corymbia sections, with Angophora as the out-group taxon. The analysis was based on a general suite of morphological traits (from Hill and Johnson, 1995).

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

5

Fig. 2. Distribution of the spotted gums (section Politaria) and C. torelliana (&) in Australia (a) (from Hill and Johnson, 1995) and the genetic structuring of the spotted gum complex based on microsatellite genetic markers (b) (from Shepherd et al., 2008). The microsatellite analysis of the four spotted gum taxa, C. c. citriodora (*), C. c. variegata (~), C. henryi (^) and C. maculata (+), identified five populations that transgressed phenotypically defined taxonomic boundaries.

variegata and C. henryi material from below this disjunction but north of the Border Ranges, formed a central population, whereas a southern population was comprised of C. c. variegata and C. henryi from predominately south of the Border Ranges. An additional population, composed of north coast C. maculata, however, should also be evident based on evidence from isozymes and cpDNA studies (McDonald et al., 2000, 2003; King, 2004). C. torelliana is regarded as the closest relative of the spotted gums and belongs to a closely related Section, Cadageria (Fig. 1). It occurs in a restricted distribution in rainforest margins in North Queensland. C. torelliana is known to hybridise with spotted gums, both artificially, and naturally based on recorded spontaneous hybrids between cultivated and native plants (Hill and Johnson, 1995). 5. Patterns of hybridisation within the genus Corymbia Natural hybridisation in eucalypts is generally agreed to have played a major role in the evolution of the current day species (Pryor and Johnson, 1981; Potts and Reid, 1990; McKinnon et al., 2004). Assessments of contemporary patterns of interspecific hybridisation demonstrate numerous hybrid combinations, not only between closely related species, i.e. species within series, but also between more distantly related species of different sections (Griffin et al., 1988; Potts et al., 2003). Despite this propensity, strong barriers to hybridisation exist between genera of eucalypts, resulting in species of Corymbia being unable to cross with Eucalyptus and Angophora (Griffin et al., 1988; Ellis et al., 1991; Potts et al., 2003; Supplementary data 2). Intersectional hybridisation within Corymbia has been recorded with all sections, with the exception of Fundoria (Fig. 3a). The majority of naturally occurring hybrid combinations have occurred

with Politaria, however, artificial pollination involving Cadagaria and Rufaria has demonstrated the potential for a range of combinations to be produced involving other sections. Interseries hybridisation has only been recorded within Rufaria and Blakearia (Supplementary data 2), no doubt due to the higher number of species within these sections. Hybridisation between species within series has also been commonly recorded. Natural hybridisation within Politaria, for example, has been noted between C. c. variegata and C. c. citriodora, C. henryi and C. maculata (Fig. 3b). There does appear to be a taxonomic influence on the frequency of recorded natural hybrid combinations (Table 2), however, the degree to which this is a product of geographical proximity is uncertain (Griffin et al., 1988). Among manipulated crosses, however, there appears no such trend, with a number of combinations between the two major clades of Corymbia being recorded. It is important to note, however, that many of these crosses were conducted using ‘‘cut-style’’ techniques and therefore may circumvent natural barriers to hybridisation (see Section 7.4). Hybrids involving the plantation species C. maculata have been documented with C. bloxsomei, C. c. variegata, C. gummifera, C. intermedia, C. torelliana, and C. watsoniana (Supplementary data 2). Hybrids with C. c. variegata have been recorded with C. bloxsomei, C. c. citriodora, C. henryi, C. maculata, C. torelliana and C. watsoniana. 6. Geographical proximity of native populations to Corymbia plantations Native Corymbia populations are found broadly across Australia, with all continental states except the ACT having records. Using the botanical regions of each state, outlined in EUCLID (CPBR, 2006), the native species that were in regional proximity to Corymbia plantations were determined. Of the 100 species and

6

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19 Table 2 Patterns of natural and manipulated hybridisation within or involving the genus Corymbia Taxonomic distance between crosses

Manipulated

Natural

n successful

n tested

Intergenera Intersection Interseries Intraseries

0 14 1 0

4 15 1 0

0 13 40 48

Total

15

20

101

n reported

Successful crosses were those that produced viable seed. See Supplementary data 2 for source data. Records of manipulated hybrids include those produced using methods that involve inducing receptivity, such as cutting off the stigma, which may increase the likelihood of successful hybridisation.

for the botanical regions within each state found to have cooccurrence). The native species found within the same botanical regions as planted Corymbia represent the species most likely to be within pollen dispersal range of plantations. In both NSW and Queensland, all the native spotted gum species were found to regionally co-occur with plantations, highlighting the potential for exotic gene flow involving closely related species to those in plantations. All the regionally co-occurring native species will be more closely analysed for the existence of barriers to gene flow from plantations in the following sections. 7. Risk assessment framework for pollen-mediated gene flow

Fig. 3. Intersectional hybridisation within Corymbia and intrasectional hybridisation within section Politaria. (a) Shows the frequency of intersectional hybrid combinations found in Corymbia as a percentage of the total number of recorded natural intersectional hybrid combinations ( ) and as a fraction of the number of manipulated combinations tested ( ). The hash-line divides the species belonging to the two major clades within Corymbia (see Section 4.1). The area of the circle indicates the number of taxa in each section (also in brackets). The majority of the manipulated hybrid combinations are produced using the cut-style procedure. (b) Shows the number of published records for hybrids between all possible cross-combinations within section Politaria. No manipulated examples of hybrids between species of Politaria have been published, however, the figure does included hybrids between cultivated plants and native populations. See Supplementary data 2 for source literature.

subspecies of Corymbia (Supplementary data 1), only 20 were found within the same botanical regions as plantations (Table 3). None of these species are listed as vulnerable or threatened under the Environment Protection and Biodiversity Conservation Act 1999 (http://www.deh.gov.au). It is important to note, however, that C. petalophylla and C. watsoniana subsp. capillata all have restricted ranges and may be vulnerable to pollen swamping and have higher risk of exotic gene flow. In Western Australia plantings have occurred in the south-west region where C. calophylla, C. ficifolia and C. haematoxylon are found (Table 3). In Victoria, no native Corymbia are found in the east where C. maculata plantations have been established at Wannon in the Victorian Volcanic Plain regions, while in the East Gippsland region, native populations of C. gummifera and C. maculata are found where both C. c. variegata and C. maculata plantations are established. In NSW, plantations in the North Coast, Central Coast and North Tableland regions, results in regional co-occurrence with C. c. variegata, C. eximia, C. gummifera, C. henryi, C. intermedia, C. maculata, C. trachyphloia and C. tessellaris, while in Queensland 16 native species co-occurred with plantations (see Supplementary data 3–6

A framework for assessing the risk of exotic pollen-mediated gene flow from eucalypt plantations has been developed by Potts et al. (2003), based upon key biological factors that can act as barriers to hybridisation (Fig. 4). The potential for gene flow into native Corymbia populations from forestry plantations is considered and knowledge gaps are identified. 7.1. Pollen production and release from plantations The quantity of pollen produced from plantations will influence the levels at which hybridisation with sympatric native populations can occur. Flower abundance and hence pollen release from eucalypt plantations can be influenced by environmental conditions such as temperature, rainfall and nutrient availability (Eldridge et al., 1993; House, 1997). Flower abundance in plantations is also known to increase with age (Eldridge et al., 1993; Barbour et al., 2008) and spacing (Williams et al., 2006) of individual trees, and may also vary according to provenance (Eldridge et al., 1993; Chambers et al., 1997). The age of first flowering (flowering precocity) in plantation eucalypts normally varies from 2 to 10 years (depending on the species), however, rare precocious flowering may occur in seedlings as young as 2 months (Eldridge et al., 1993). There is limited data on the age of first flowering in Corymbia plantations, although there are anecdotal reports of spotted gum plantations flowering at 3–4 years for C. c. variegata plantations (Nikles et al., 2000). Individuals from a seedling plantation of the same species, however, have also been observed flowering at 18 months in the Kingaroy region (D. Kleinig, personal communication), in a clonal plantation at approximately 3.5 years in the Woolgoolga region (S. Boyton, personal communication), and as a general pattern of heavy flowering at around 2 years of age (D. Lee, personal communication). The patterns of flowering in older plantations are also poorly understood, however, a survey conducted by the authors on 15 C. c. variegata plantations (Fig. 5a) confirms the existence of reproduc-

Table 3 Co-occurrence of plantations and native populations of Corymbia within the botanical regions of Australia Section

Series

Species

Regional co-occurrence States with regional co-occurrence

Botanical regions with co-occurrence

Hybrids recorded with plantation species

Flower size

Flowering phenologya

Bud width (mm)

Bud height (mm)

J

F

M

A

*

*

M

J

Trachyphloiae

trachyphloia

QLD, NSW

Burnett, Darling Downs, Moreton, Port Curtis, Wide Bay, North Coast

2–3

3–5

*

*

Blakearia

Grandifoliae Tessellares

dallachiana tessellaris

QLD QLD, NSW

Port Curtis Burnett, Darling Downs, Moreton, Port Curtis, Wide Bay, North Coast

4–5 3–5

5–7 5–6

*

*

Cadagaria

Torellianae

torelliana torelliana (northern NSW)

. .

. .

M M

5–8 na

10–12 na

Ochraria

Eximiae

bloxsomei eximia petalophyllab watsoniana subsp. watsoniana

QLD NSW QLD QLD

Burnett North Coast, Central Coast Burnett Burnett, Darling Downs

M, V

M, V

5–6 5–7 4–5 12–16

8–9 9–14 6–8 15–20

citriodora subsp. citriodora citriodora subsp. variegata henryi maculata

QLD

Burnett, Port Curtis, Wide Bay

M, V

4–5

7–9

*

*

*

*

*

*

QLD, NSW

Burnett, Darling Downs, Moreton, North Coast Moreton, North Coast East Gippsland, North Coast, Central Coast

M

5–7

8–11

*

*

*

*

*

V V

6–8 5–7

9–13 8–11

*

erythrophloia ficifolia calophylla gummifera

QLD WA WA VIC, QLD, NSW

M

4–6 6–8 7–10 5–8

5–8 9–13 7–14 8–11

* * * *

* * * *

Intermediae

haematoxylon intermedia

WA QLD, NSW

M

5–7 5–7

7–10 7–12

* *

* *

Polycarpae

clarksoniana

QLD

4–7

7–13

Rhodopes

hendersonii xanthope

QLD QLD

4–6 5–6

8–11 7–8

Politaria

Rufaria

Maculatae

Dichromophloiae Ficifoliae Gummiferae

QLD, NSW VIC, NSW

Burnett, Port Curtis, Wide Bay South-west South-west East Gippsland, Burnett, Moreton, Port Curtis, Wide Bay, North Coast, Central Coast, Northern Tablelands South-west Burnett, Darling Downs, Moreton, Port Curtis, Wide Bay, North Coast Burnett, Darling Downs, Moreton, Port Curtis, Wide Bay Burnett Port Curtis

*

* *

*

*

*

*

O

N

D

*

*

*

*

* *

* *

*

* *

* *

* *

* *

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

* *

* na

S

* * *

*

* *

A

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

Apteria

J

*

*

*

*

Provided for each native species found in regional co-occurrence with plantations is their taxonomy and the states and botanical regions in which co-occurrence was identified (using CPBR, 2006). In addition, recorded hybrid combinations involving each native species with those used in plantations have been provided (M, with C. maculata; V, with C. c. variegata, see Supplementary data 2 for source literature), as well as the range in flower bud size (from Hill and Johnson, 1995) and flowering phenology for each species. The phenological data includes flowering observations for planted C. torelliana in northern New South Wales (M. Shepherd, personal communication; C. Chaffey personal communication) and for natural populations, despite no co-occurrence between plantation and native populations identified for this species. a Source literature: Hill and Johnson (1995), Brooker and Kleinig (1996), Law et al. (2000), Jackson (2001) and Dale and Hawkins (1983). b Listed as ‘‘2K’’ under the ROTAP (Rare or Threatened Australian Plants) coding system, meaning that this species occurs over a range of less than 100 km but its conservation status is poorly known. No species listed are currently listed under the Environment Protection and Biodiversity Conservation Act 1999.

7

8

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

Fig. 4. Risk assessment framework for pollen-mediated gene flow from exotic eucalypt plantations in Australia (from Potts et al., 2003). The framework outlines the biological steps in the process of pollen-mediated gene flow. Incompatibility between sympatric species at any one step will act as a barrier to gene flow.

tive activity, with a general pattern of increasing flower abundance with age and considerable variability between sites. It is apparent, therefore, that spotted gum plantations are likely to flower, and often from a young age, however, more detailed studies are required to determine the extent to which environmental and genetic factors influence site-to-site variation. This would need to include factors such as tree spacing (Williams et al., 2006) as stocking and/or thinning regimes resulting in 250–1100 trees per ha are being maintained in response to varying soil moisture levels and end-use requirements (i.e. sawlog or pulp). The use of the spotted gum hybrid with C. torelliana raises particular concern in regard to the quantity of exotic pollen released from plantations. The results of a 6-year-old genetic trial containing C. c. variegata, C. torelliana and the F1 hybrid between the two species indicated the hybrid produces substantially greater flower bud abundance compared to C. c. variegata (Fig. 6). This abundance appears to be due to the intermediate inheritance of this trait, as the pure species C. torelliana displays even greater abundance. In addition, these hybrids appear to produce pollen and viable seed, demonstrating their ability to contribute to the next generation (Fig. 6). 7.2. Flowering phenology and interspecific synchrony The annual season (phenology) of flowering in eucalypts can have substantial influence on the potential for exotic gene flow, as it dictates the degree to which interspecific flowering synchrony occurs, and the degree to which plantation pollen can reach receptive native stigma (Levin, 1978; Vanden Broeck et al., 2003;

Barbour et al., 2006b). Eucalypt species tend to have characteristic flowering seasons, although variation is also typical when assessing individual trees or populations, and patterns from year to year (Griffin, 1980; Pook et al., 1997; Law et al., 2000; Keatley et al., 2004). The most pronounced environmental influence on flowering phenology appears to be temperature, or more precisely the seasonal heat sum for a site (Moncur et al., 1994; Barbour et al., 2006b). In addition to environmental influences, genetic variation can also exists (Apiolaza et al., 2001; Barbour et al., 2006b). While reliable data on flowering phenology for specific sites and species is often difficult to obtain, the use of generalised flowering data has been show to provide a valuable and conservative assessment of risk, from which point more specific analyses can be conducted (Barbour et al., 2006b). Table 3 documents the available generalised flowering data for all native Corymbia species found to regionally co-occur with plantations. Considerable variation exists in the time of year and duration of flowering. Most species appear to flower for 2–6 months, during spring, summer and autumn. Corymbia tessellaris and more notably C. c. variegata appear to have much longer periods of flowering, with C. c. variegata having records for every month of the year. This apparent variability in C. c. variegata has also been noted by seed orchard practitioners (D. Lee, personal communication), and raises the likelihood that considerable flowering synchrony will exist between C. c. variegata plantations and native Corymbia populations. Fig. 5b describes the predicted time of flowering of plantations in northern New South Wales and southern Queensland based on the stages of bud development of individual trees in the months prior to flowering. This work does

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

9

Fig. 6. Inheritance of flower bud abundance in the F1 hybrid between C. torelliana (,) and C. c. variegata (<). Approximately 20 trees of each cross-type were assessed within a 6-year-old randomised common garden trial at Coolabunia, southern Queensland. Abundance was assessed on a log categorical scale in August 2007. All cross-types were significantly different from each other (F2,60 = 56.7, P < 0.001) following an analysis fitting cross-type as a fixed effect (Proc Mixed of SAS, version 9.1, Cary NC, USA). The F1 hybrid is the result of placing C. c. variegata pollen on C. torelliana flowers. The photos show a cross-section of a seed capsule with viable seed and pollen produced from a flower of an F1 hybrid, demonstrating the potential for second-generation crossing.

Fig. 5. Flowering characteristics of C. c. variegata plantations in northern New South Wales and southern Queensland (a) percentage of trees with current seasons flower buds versus plantation age. Summarised data are for trees in the buffer (edge) row (n = 10) and an inside row (5 rows in from edge, n = 10) of plantations. Significant variation was found testing the fixed effect of plantation age (F5,22 = 4.39, P = 0.006), however, the fixed effect of buffer compared to inside trees was not significant (F1,22 = 0.09, P = 0.77, Proc Mixed of SAS, version 9.1, Cary NC, USA). (b) Estimated flowering time of plantations, based on the stage of development of the current season’s flower buds at the time of survey. Data were collected by the authors at the beginning of August 2007 across 15 plantations (20 trees per plantation).

predict a more restricted time of flowering compared to the native forest assessments described above, however, further verification of this pattern is required. Indeed, areas of co-occurrence between plantation and any native Corymbia species will need specific siteby-site assessment due to the expected genetic and environmental variation in phenology. Observations from native populations of C. torelliana in north Queensland compared to plantings in northern NSW, however, show similar results despite considerable differences in latitude (Table 3). The factors influencing the flowering of plantation and native Corymbia should represent a major focal point for future research, and include the production of predictive models. Such models will be particularly important for the plantation species given the wide range of conditions in which they are established and the likely genetic manipulations of the species (i.e. through selection and breeding). While C. c. variegata may display an unusually broad period of flowering, native populations of the plantation species C. maculata,

were recorded flowering for just 4 months of the year, between June and October. C. maculata plantations have been established in eastern Victoria and in north and central coastal regions of NSW. Based on the phenology of the native C. maculata populations, substantial flowering asynchrony between C. maculata plantations and native C. gummifera may well exist in Victoria, representing a major barrier to gene flow. In addition, four of the seven native species in NSW found to have regional co-occurrence with plantations also appear to flower asynchronously with C. maculata (C. intermedia, C. gummifera, C. henryi, and C. trachyphloia). In situations where C. maculata plantations are established adjacent to native populations of the same species, genetic variation in flowering may prevent synchrony. The native source population for genetic material for stocking of C. maculata plantations tends to be the northern populations of the species. The extent to which flowering synchrony would occur between plantations and native populations of C. maculata in Victoria, therefore, needs further investigation. While patterns in flowering phenology in eucalypt species can initially be estimated using generalised flowering data, such data is typically not available for F1 hybrids, such as C. c. variegata  C. torelliana. Nevertheless assessments of the inheritance of flowering phenology in a select few cross-combinations have typically demonstrated intermediate inheritance in this trait (Gore and Potts, 1995; Lopez et al., 2000a; see Lopez et al., 2000b for exception), which includes an assessment of the C. c. variegata  C. torelliana hybrid combination in India (Verma and Sharma, 1999). This may prove a beneficial rule of thumb, however, given the apparent vast amount of variation in flowering phenology seen for C. c. variegata, such predictions would only be possible once the

10

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

Fig. 7. Floral visitors of C. c. variegata and C. torelliana  C. c. variegata F1 hybrids grown in genetic trials in south-east Queensland and north-east New South Wales. Photo of the Rainbow Lorikeet (Trichoglossus haematodus) provided by J. Currie.

flowering of this parent is better understood. Nevertheless, assessments of the hybrids themselves is now possible given the number of research trials that have been established to assess their performance. 7.3. Distance of pollen dispersal from plantations 7.3.1. Patterns of pollen flow in eucalypts Pollen dispersal generally appears to be the primary mode by which gene flow occurs within tree species (Hamrick and Nason, 2000). Given the potential for flowering time to overlap between

native and plantation Corymbia species, the pattern of pollen movement from plantations needs to be considered to identify native species at risk and attempt to establish minimum safe distances between plantation and native populations. Pollen is sticky and forms irregular granular aggregates in the majority of eucalypt species, which indicates pollination occurs via animal vectors (House, 1997). A leptokurtic distribution is described for the majority of studies on pollen movement in flowering plants, i.e. a curve showing a steep initial decline followed by a tail of low level but often long-distance dispersal (Ellstrand, 1992a; Hamrick and Nason, 2000). This pattern appears to be the case in eucalypts,

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

based initially on limited studies and observations of hybrid frequencies in relation to sources of naturally occurring interspecific pollen (Potts et al., 2003), and more recently on a study assessing pollen flow from exotic E. nitens plantations (Barbour et al., 2005b). This study assessed pollen dispersal into native E. ovata populations by examining F1 hybrid seed frequency. Levels of F1 hybridisation averaged 13% at the boundary of plantations, dropped to 1% by 200 m and then stayed at this mean level to the extent of the sampled range at 1600 m. It is important to note, however, that E. nitens is pollinated by small insects less than 1 cm in length (Hingston et al., 2004) and therefore pollen dispersal distances in vertebrate pollinated species such as Corymbia are probably much greater (Southerton et al., 2004). A tendency for hybridisation to be higher at sites where adjacent native forest is more fragmented, suggests greater buffer distances between plantations and native forests are required in such landscapes. A gene flow model developed for eucalypts by Linacre and Ades (2004) indicates a minimum isolation distance of 100 m is required to limit gene introgression from plantations. As recognised by the authors, however, pollinator behaviour is an important but difficult parameter to accurately quantify, and is unlikely to have been adequately captured by their model. Isolation distances of 200 m have been recommended for seed orchards of eucalypts and other tree species (van Wyk, 1981), however, it has been suggested that the key isolating factor in this case is not distance from the contaminating source but the presence of buffer zones with nonhybridising species (Griffin, 1989). It is unclear as to the width required for a buffer zone to act effectively in reducing pollen dispersal from plantations, however, the size of the flowering crop and the degree of flowering synchrony in the buffer trees, with the plantations, will no doubt also play a significant role. 7.3.2. Vectors of pollen flow in Corymbia Corymbia flowers attract a wide range of generalist pollinators, from small (<1 cm) native bees, flies and beetles to bats, honey eaters, lorikeets and parrots (Bacles et al., 2007; House, 1997;

11

Southerton et al., 2004, Fig. 7). The often larger flower size of Corymbia compared to those of Eucalyptus, the aggregation of flowers into bunches, and its typically northern Australian distribution, results in Corymbia being frequently visited by a diversity of vertebrate pollinators (Southerton et al., 2004). Dispersal of pollen by nectar feeding bats and birds is expected to result in pollen flow over much greater distances from plantations compared to insect pollination. Pollen and nectar feeding bats and birds, for example, may travel in excess of 50 km in a day to access food resources (Southerton et al., 2004). Rainbow lorikeets, are capable of moving up to 35 km from roosting to feeding sites, and migratory honeyeater species may potentially transfer pollen between trees more than 100 km apart (Southerton et al., 2004). Bats in particular appear to have substantial ability to carry viable pollen over long distances. The primary pollen and nectar feeding bats of eucalypts in the northern New South Wales region, include the little red flying fox (Pteropus scapulatus), the black flying fox (Pteropus alecto), the grey-headed flying fox (Pteropus poliocephalus), and the Queensland blossom bat (Syconycteris australis, Strahan, 1991). P. poliocephalus has been observed feeding on the flowers of several Corymbia species, such as C. eximia, C. gummifera, C. henryi, C. intermedia, C. maculata and C. tessellaris (Eby, 1991). P. alecto is also known to visit introduced C. torelliana in suburban Brisbane when in flower (Markus and Hall, 2004). The similarity in flower size and morphology between species of Corymbia is likely to result in vertebrate activity within plantation grown species, assuming the time of flowering is compatible with migration and feeding patterns, and the abundance of flowers is large enough to attract visitation. Studies of P. poliocephalus in relation to patterns of flowering have shown that this species is capable of locating flowering resources from a distance of hundreds of kilometres. Radiotracking studies of this species in northern New South Wales have revealed that individuals may regularly undertake long-distance seasonal migrations up to 800 km (Eby, 1991, 1996). These movements appear to be highly correlated with the flowering

Fig. 8. Spatial analysis of the potential scale of vertebrate pollen dispersal from Corymbia plantations in north-east New South Wales, Ten and fifty km radii have been placed around the publicly owned Spotted gum plantations (Corymbia, section Politaria) in the region (black shading). The distribution of native Corymbia forests is also provided (shades of grey). These radii demonstrate the area over which species of birds and bats may potentially travel as pollen vectors, following feeding activity within a flowering Corymbia plantation. The area of native Corymbia forest within the dispersal radii is provided in Table 4. Spatial analysis conducted by R. Kirwood (Forests New South Wales).

12

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

Table 4 Area (ha) of forest containing species of Bloodwood (Corymbia, sections Apteria and Rufaria) and Spotted gums (section Politaria) within potential vertebrate pollen dispersal range from Corymbia plantations in northern New South Wales Forest type

Total area

Area within 10 km of current C. torelliana  C. c. variegata trials

Area within 50 km of current C. torelliana  C. c. variegata trials

Area within 10 km of current spotted gum plantations

Area within 50 km of current spotted gum plantations

Spotted gums (dominant/co-dominant) Spotted gums (possible associate) Red bloodwoods (dominant/co-dominant) Red bloodwoods (possible associate) Spotted gum plantations printed on map

378,099 168,507 63,209 281,457 8,196

3576 2483 2177 3032

240,209 58,604 61,343 191,760

160,443 54,182 28,885 84,781

378,099 168,507 63,209 281,457

Data provided by R. Kirwood (Forests New South Wales). This table is an adjunct to Fig. 8.

pattern of spotted gums, which occurs sequentially from north to south. P. poliocephalus have also been tracked from northern NSW coastal areas to riverine forests west of the dividing range (240 km), believed to be associated with flowering Eucalyptus albens (Eby, 1991). Importantly, this species is known to travel more than 45 km to feeding areas during a single night (Eby, 1996). Flying foxes therefore appear to be capable of traversing much of the plantation range in a relatively short period of time, and may carry large amounts of pollen with them. Pollen carried by bats has been shown to be viable. In a study by McCoy (1990) it was revealed that flying foxes (P. alecto and P. scapulatus) carry large volumes of viable pollen grains on their fur, which when transferred to receptive stigmas of the eucalypt species E. porrecta and E. confertiflora resulted in fertilisation. It has been suggested that sporadic, long-distance pollination events by birds or bats may correspond with outcrossing breeding strategies typically described for eucalypts (Bacles et al., 2007; Potts and Wiltshire, 1997; McDonald, 2004; Southerton et al., 2004). In this regard, various eucalypt species are known to produce large volumes of nectar during the night, possibly to attract nocturnal pollinators such as bats (McCoy, 1990). There are no published studies of eucalypt pollen viability in the field, however, it has been suggested that pollen may remain viable for at least 8 days while being transported by insect vectors (unpublished data cited by Griffin, 1989). Pollination of eucalypt species (by flying foxes) may therefore occur over hundreds of kilometres, the probability of which may only depend upon flowering synchrony and intensity. The combined influence of long-distance pollen dispersal, with a Corymbia plantation estate that has been established throughout a landscape, on the area over which plantation pollen may be dispersed is demonstrated in a spatial analysis of north-east New South Wales (Fig. 8 and Table 4). By delineating 10 and 50 km radii around the publicly owned estate in the region, it is clear that the use of isolation zones to prevent exotic gene flow would not be feasible. Indeed, the figure also places into question the use of the botanical regions employed in the current work, to determine the native species potentially at risk of exotic gene flow based on regional co-occurrence. Nevertheless, in the face of apparent landscape-level dispersal of Corymbia pollen and substantial propensity for hybridisation within the genus, a large number of native Corymbia species co-occur whilst maintaining distinct species-specific characteristics (North Coast region of NNSW [Supplementary data 5] has 8 species, Cook region of Queensland [Supplementary data 6] has 33 species, from EUCLID, CPBR, 2006). This suggests that reproductive barriers exist that will limit the influence of expected broad-scale dispersal of plantation pollen (Asante et al., 2001). Within the spotted gum complex, however, weak genetic structuring across species ranges (Fig. 2) is consistent with extensive levels of pollen-mediated gene flow.

7.3.3. Techniques for assessing gene flow from Corymbia plantations Due to the uncertainty associated with inferring patterns of gene flow from studies of vector behaviour or pollen movement (Pacheco et al., 1986), describing patterns of realised gene flow in terms of hybridisation events provides a more accurate depiction of the spatial risks of exotic gene flow. The identification of exotic hybrids among open-pollinated seed lots of native trees, sampled at varying distances from a plantation pollen source, can be conducted using both quantitative and molecular genetic techniques (Ellstrand, 1992a; Hamrick and Nason, 2000). As mentioned above, pollen flow from E. nitens plantations has been assessed by determining the frequency of F1 hybrids in open-pollinated seed lots of native E. ovata (Barbour et al., 2005b). The introduction of E. nitens onto the island of Tasmania has not only introduced a species that is genetically distinct from native populations (Barbour et al., 2003; McKinnon et al., 2008), but is exceptionally different in its seedling morphology (Barbour et al., 2003, 2005a). The leaves of E. nitens at node 10 are sessile, opposite, glaucous and have distinct basal lobing of the lamina. In comparison, the seedling leaves of E. ovata are petiolate, alternate, green and display no basal lobing. The generally intermediate nature of F1 hybrid eucalypts (Pryor, 1976; Wiltshire and Reid, 1987; Delaporte et al., 2001; Barbour et al., 2005a), therefore results in F1 hybrids between these two species being easily identifiable within E. ovata seed lots. To assist in determining whether such quantitative variation exists in Corymbia, an assessment of seedling leaf morphology was conducted for the 20 native taxa that regionally co-occur with plantations (including those used in plantations, in EUCLID, CPBR, 2006). Very little leaf variation was found that could

Fig. 9. Seedling morphological variation in the spotted gums (Section Politaria). From left to right; C. maculata, C. henryi, C. citriodora subsp. variegata and C. citriodora subsp. citriodora.

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

13

Fig. 10. Performance of E. ovata  E. nitens F1 hybrids (^) relative to pure parental E. ovata (^) and E. nitens (b only, ~) under the conditions of a naturally regenerating E. ovata forest (from Barbour et al., 2006a). (a) Shows the relative performance in seed establishment. (b) and (c) describe performance of seedlings planted in triangles consisting of F1 hybrids, their E. ovata half-sibs and E. nitens, and in pairs consisting of just the hybrids and their half-sibs.

be use in isolation to confidently identify F1 hybrids (Fig. 9, see also Larmour et al., 2000). All species displayed petiolate to tapering bases with no basal lobing, and obovate to lanceolate laminas with little glaucousness. Variation in other quantitative seedling traits may exist, and would need further investigation, i.e. in leaf chemistry (Atkinson et al., 1997; Espejo et al., 2004) and cotyledon morphology (Meddings et al., 2003). In comparison to quantitative markers, molecular markers appear to present more opportunity for studying patterns of gene flow from Corymbia plantations (Larmour et al., 2000). Microsatellite markers have been developed for the spotted gum complex which may present substantial opportunity for identifying hybrid progeny (Jones et al., 2001). These markers have been successfully used to distinguish F1 and second-generation hybrids involving C. torelliana and C. c. variegata (M. Shepherd, unpublished data). Due to the cost of genotyping progeny using molecular techniques, a combined approach using morphological variation to identify putative hybrids, followed by molecular verification for a selection of the putative hybrids, may prove the best strategy. Despite the similarity in morphology of the Corymbia species, crossing between C. c. variegata plantations and C. maculata for example, may result in the production of hybrids that can be tentatively identified. In addition to the use of molecular markers for hybrid identification, alternative molecular techniques are arising that may provide novel opportunities for assessing pollen movement. This includes particularly, the correlated paternity analyses such as the two-generation approach (Austerlitz and Smouse, 2001a,b, 2002; Smouse et al., 2001; Dyer et al., 2004). 7.3.4. Seed dispersal from plantations Seed dispersal in eucalypts is likely to be less problematic than pollen dispersal in the containment of plantation genes. Eucalypts are generally regarded as having no special adaptations for the dispersal of their seed, which typically occurs to within two tree heights from the base of the tree (Cremer, 1966; Barbour et al., 2003). Exceptions to this are seen in species of Corymbia in section Rufaria, which often possess a membranous wing (Brooker and Kleinig, 1996) that may assist to some degree in dispersal. More notably, however, C. torelliana produces seed that is transported more than 300 m away by native Trigona bees (Wallace and Trueman, 1995; Wallace et al., 2008). Bees collect resin from the mature capsules of C. torelliana for nest construction, with the seeds becoming attached to the resin. This attribute of C. torelliana has resulted in the species being placed on the environmental weed list in a number of shires of NSW as early road-side amenity

plantings have resulted in broad-scale invasion in a number of areas (Anon., 2002, 2007). While plantations of pure species C. torelliana are not being established, the capsule and seed morphology of the F1 hybrid between C. torelliana and C. c. citriodora, has been found to be unsuitable for resin foraging by bees and the seeds not associated with the resin (Wallace et al., 2005). Furthermore, native bees appeared to forage only on hybrid seed capsules that had been chewed and discarded onto the ground by black cockatoos. This suggests native bees may not be effective dispersers of plantation grown C. torelliana hybrid seed. Nevertheless, accurate quantification of seed movement from discarded capsules is necessary as capsule foraging by birds within eucalypt plantations is frequently recorded. In addition, with the scaling up of hybrid breeding programs involving C. torelliana to include a range of spotted gum species (Lee, 2007), further study may also need to include new hybrid combinations, including the C. torelliana  C. c. variegata combination being deployed currently. 7.4. Crossing-incompatibilities Studies of natural hybridisation between species of eucalypts have recorded only 15% of possible combinations expected on geographic or taxonomic grounds (Griffin et al., 1988). This suggests that barriers to gene flow have evolved for many closely related sympatric species, improving the fitness of the population by reducing the frequency of inferior matings. While in a number of cases flowering asynchrony may be one such barrier preventing hybridisation, a range of post-mating (pre-zygotic) and postzygotic barriers also exist. While strong barriers prevent hybridisation between Corymbia and other genera of Myrtaceae such as Eucalyptus (Griffin et al., 1988), partial or complete barriers within Corymbia may also exist. These barriers may occur due to pollen tubes being unable to germinate and grow the length of the style and reach the ovules, to penetrate ovules and allow fertilisation or due to abnormalities in zygote and seed development (Gore et al., 1990; Ellis et al., 1991; Sedgley and Granger, 1996; Delaporte et al., 2001). Few studies have been conducted to assess the existence of crossing-incompatibilities within Corymbia. Recent work has assessed seed output following hybridisation using C. torelliana as the maternal parent and pollen from 16 species (Dickinson et al., 2007). The species assessed were from 6 of the 7 sections of Corymbia, and from Eucalyptus and Angophora. Some barriers appeared to exist for a number of cross-combinations, which appeared independent of taxonomic affinities. While the closely

14

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

related species C. c. variegata and C. c. citriodora displayed the highest levels of interspecific cross-compatibility, no seed was produced from crosses with the closely related C. leichardtii (section Ochraria), but, successful hybridisation did occur with the most distantly related species of section Rufaria. Although a valuable first insight into crossability of C. torelliana across the genus, the lack of replication in the pollen parents precludes strong conclusions. The ‘‘one-stop’’ crossing technique used in the study, involving decapitation of the style to facilitate immediate receptivity, also bypasses a number of potential barriers such as style-length incompatibility, pollen–pistil incongruity and pollen competition with native intraspecific pollen. These findings are likely, therefore, to be an underestimate of the levels of incompatibility. In addition, the partial incompatibilities identified in this work suggest that further genetic incompatibilities may develop in the form of reduced seedling germination and growth abnormalities. Clearly, crossing-incompatibilities are likely to exist to prevent or limit hybridisation between plantation and native Corymbia species in many cases. In assessments placing pollen from the plantation species E. nitens on the stigma of open-pollinated flowers of 13 native species, Barbour et al. (2005a) found that only seven species produced hybrids. In addition, using controlledpollination techniques, significant differences were found in the number of seed produced per flower when compared to outcross pollination. Without the existence of clear patterns of crossability within the genus Corymbia, further studies will need to be assessed on a cases-by-case basis. As only 20 native Corymbia taxa have been found in regional co-occurrence with plantations across Australia, crossing programs can be developed that focus on these species as the females in the crosses, using techniques that do not involve artificially inducing receptivity (i.e. through cutting off the stigma). This will be particularly effective in areas such as eastern Victoria and south-west Western Australia where only two to three native species exist. In north-east NSW, C. watsoniana subsp. watsoniana may be one example where crossing-incompatibilities exist, as the considerably larger flower size (Table 3) may restrict the ability of plantation pollen to grow the full length of its style and facilitate successful fertilisation (Gore et al., 1990).

but in the case of establishing exotic hybrids, the lack of adaptation to the local environments and the genetic incompatibilities associated with F1 hybridisation. This is demonstrated in a study conducted by Barbour et al. (2006a), assessing the relative ability of exotic E. ovata  E. nitens F1 hybrid seed to establish in the regenerating habitat of the native E. ovata forest. Fig. 10a demonstrates that compared to glasshouse conditions, only 3% of the seed sown under wild conditions, established and survives as small seedlings. In addition, the proportion of hybrids that established in the wild was significantly lower compared to that in the glasshouse, demonstrating stronger selection against the hybrids under such conditions. Similarly, the exotic hybrids demonstrated poorer survival within seedling-based trials (Fig. 10b and c). Assessments of E. nitens seedlings also found poorer performance relative to the E. ovata, demonstrating the difficulties that exotic species may have in establishing. As described, F1 hybrids are expected to display poorer average performance relative to their parental species, or at least to be poorer than mid-parent values. Despite this, however, a proportion of F1 hybrid seedlings are often successful to the point that they may contribute to the next generation. This may particularly be the case for the C. torelliana  C. c. variegata F1 hybrids being tested for commercial deployment into plantations. These hybrids are reported as displaying significantly greater growth, as well as disease, insect and frost tolerance compared to open-pollinated pure parental species (Lee, 2007). Nevertheless, as Potts and Dungey (2004) point out, such results are often a response to a release from inbreeding depression. If hybrid genotypes were compared to outcrossed pure species controls generated through controlled-pollinations, rather than bulk open-pollinated seed lots which typically have a high proportion of selfed progeny (McDonald, 2004), relative hybrid performance may be considerably reduced. Nevertheless, individual hybrid plants are likely to be successful (Lee, 2007), and given their unusual propensity for vegetative propagation (Lee, 2007; Trueman and Richardson, 2007), further development of the C. torelliana  C. c. variegata hybrid is likely to continue. The use of such hybrids in plantation forestry circumvents the F1 hybrid stepping-stone and its associated barriers to exotic gene flow, as hybridisation involving these plantations will represent second-generation hybridisation.

7.5. Hybrid survival and fitness 7.5.1. F1 hybrid seedling establishment through to reproductive maturity F1 hybrid eucalypts typically display poorer average survival and growth compared to outcrossed parental controls, representing a major partial barrier to gene flow (Potts and Dungey, 2004). F1 hybrid inviability can frequently appear at germination but typically becomes noticeable at the seedling stage. In the cross between E. camaldulensis and E. globulus, Meddings et al. (2003) found that 72% of hybrids displayed abnormal seedling characteristics, where as the proportion of seedlings from intraspecific pollination displaying such characters was less than 1%. This trend also typically continues to later ages. Eucalyptus ovata  E. globulus F1 hybrids, for example, were assessed in a 10-year-old field trial and found to display 74% poorer survival than pure E. ovata produced from open-pollination (Lopez et al., 2000b). Virtually all studies of the performance of F1 hybrids in eucalypts have been conducted under the conditions of plant nurseries or managed silvicultural systems. The ability of the F1 hybrids to survive and reproduce within naturally regenerating forests, therefore, is an important consideration when assessing the impacts of pollen flow from plantations. Such conditions typically result in strong selection against weaker genotypes. This selection may not only be due to the harsher conditions of the wild,

7.5.2. Second-generation hybridisation The second-generation of hybrids can also demonstrate reduced performance and survival relative to pure species grandparents. Such advanced generation breakdown can result from chromosomal differences, genomic incompatibility and disruption of gene complexes (Potts et al., 2003). Pilipenka (1969) noted that for some advanced generation hybrids, as many as 90–95% of seedling may display abnormal or dwarf phenotypes, which would act as a major barrier to gene flow. Second-generation hybridisation can result from a number of different cross-pollination events involving F1 hybrids, these being self-pollination or outcross pollination with hybrids of the same cross-type to produce an F2 generation, pollination with a third species producing three-way hybrids and pollination with a parental species to produce backcross hybrids. These three cross-combinations result in very different genomic interactions which inturn can result in considerable variation in survival and fitness. Understanding the nature of second-generation hybridisation in Corymbia will be important for assessing the risk of gene flow from C. torelliana  C. c. variegata F1 hybrid plantations as well as the likely impacts of exotic F1 hybrids that reach reproductive maturity. F2 hybrids, whether they are selfed or outcrossed, typically display a large proportion of abnormal seedlings, with reduced survival and poorer performance (Potts and Dungey, 2004).

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

15

parental populations will make detection of gene flow from plantations established with F1 hybrids difficult at both morphological and molecular levels and efforts to do so should expect to underestimate levels of hybridisation. Evidence of spontaneous second-generation hybridisation in Corymbia has been documented. Putative backcross hybrids were identified among open-pollinated seed lots of C. torelliana growing within amenity plantings (M. Shepherd, unpublished data). F1 hybrids with C. c. variegata were also identified at the site. This apparent backcross hybridisation event demonstrates the ability of F1 hybrids in Corymbia to contribute to latter-generations. 8. Species at greatest apparent risk

Fig. 11. Influence of second-generation hybridisation on eucalypt growth (from Potts et al., 2000). Mean basal area per planted seedling (treating deaths as zero) for E. nitens  globulus hybrids and pure species controls at age 4 years. Cross-types correspond to E. globulus (g  g) or E. nitens (n  n) outcrosses, backcrosses of the F1 hybrids to E. globulus (BCg) or E. nitens (BCn), F1 and outcrossed F2 hybrids. Common letters indicate means that are not significantly different at the P < 0.05 level.

Following the production of 400 outcrossed F2 C. torelliana  C. c. variegata hybrid seed in Shepherd et al. (2006), only 39% germinated and survived to 6-month-old seedling under glasshouse conditions, however no parental controls or F1s were grown. Producing this F2 was also hampered by low seed set (D. Lee, personal communication). Similarly, despite limited assessments (de Assis, 2000; Barbour, 2004), three-way hybridisation is also expected to produce poor performing progeny (Barbour et al., 2007). In comparison to F2 and three-way hybrids, backcross generations tend to display improved performance and may indeed contribute substantially to introgression (Arnold, 1997; Arnold et al., 1999; Potts et al., 2003). This has been best studied in eucalypts in a cross between E. nitens and E. globulus in which dramatically lower growth was found for F1 and F2 generations compared to parental species, however, first generation backcross hybrids displayed considerable improvement with no significant difference being detected between backcross and parental E. globulus by age four (Potts et al., 2000, Fig. 11). Such similarity between parental and BC1 hybrid characteristics has also been noted for crosses involving E. nitens and E. cordata in which backcrosses were increasingly indistinguishable from parental species in their morphological characteristics (Barbour et al., 2007, Fig. 12). The uncertainty in identifying backcross hybrids from

Regional level spatial analysis of the co-occurrence of plantations and native populations isolated 20 of the 100 species and subspecies of Corymbia in Australia, to be at potential risk of exotic pollen-mediated gene flow. Further barriers also appear to exist, such as asynchrony in flowering phenology, crossing-incompatibilities and reduced hybrid fitness, however, without the availability of specific biological information on co-occurring plantation and native species in situ, the species or populations at risk are difficult to isolate. Nevertheless, three distinct categories of risk can be identified and are listed below. These categories are listed in order of greatest expected likelihood of hybridisation. 1. Spotted gum plantations against native spotted gum populations. Because the majority of Corymbia plantations, using species of spotted gums, have been established within the range of native populations of these species, the centre of diversity for this industrially significant group is potentially vulnerable to exotic gene flow. The close relatedness of taxa within this complex may result in few barriers to cross-fertilisation, as demonstrated by natural patterns of hybridisation and controlled-pollination studies (Table 2 and Fig. 3). In addition, the expected longdistance pollen movement may mean large areas of native forest are vulnerable to such pollination. The species being planted most commonly within the range of native spotted gum populations is C. c. variegata which may potentially have a very broad period of flowering, further supporting a very high likelihood of exotic pollination. Nevertheless, asynchrony in flowering does exist (Table 3) between other members of the spotted gum complex, which has been suggested as preventing hybridisation between C. henryi, C. maculata and C. c. variegata at one site (McDonald, 2004). Gene flow resulting from such pollinations could impact on the genetic architecture that exists

Fig. 12. Influence of second-generation hybridisation on eucalypt seedling morphology (from Barbour et al., 2007). Plot describes the frequency distribution of E. cordata  (E. nitens  E. cordata) backcross hybrids (grey) relative to the pure parental species (E. nitens = black, E. cordata = white) along the single discriminant function separating the pure species based on seedling morphological traits.

16

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

within native populations (Fig. 2), not only having significant biological impacts, but could potentially compromise genetic resources available for future breeding programs. It should be remembered, however, that much of the risk will depend on the scale at which future plantings occur. The size of the current plantation estate is comparably small relative to the size of native populations of spotted gums. 2. C. torelliana hybrid plantations against native spotted gum populations. The fact that the production of F1 hybrids for deployment into plantations circumvents a number of first generation pre- and post-zygotic barriers to gene flow, these plantations pose a unique risk to native populations. While the viability of crosses involving plantation pollen and a third species are likely to be poor and contribute little to further gene flow, backcrossing with parental populations of the hybrids may pose a greater risk. The hybrid combination currently receiving most attention is C. torelliana  C. c. variegata. Due to hybrid plantations not planned for establishment within proximity to parental C. torelliana populations, only C. c. variegata populations appear at risk of backcrossing. The success of three-way crosses with spotted gums that are closely related to C. c. variegata, or indeed the success of crossing involving different populations to the source population of parental C. c. variegata is unknown (see Section 2). 3. Spotted gum plantations against populations of other species of Corymbia. Further assessment of the species other than spotted gums, found in regional co-occurrence with plantations is necessary to determine the potential for gene flow. A number of potential crossing-incompatibilities and flowering asynchronies have been identified within the genus Corymbia, however, the degree to which they will act as barriers for these species is uncertain. Hybrid combinations have been identified involving the species used for plantations and native species (Section 5) suggesting that they are reproductively compatible in a number of cases. Nevertheless, only research specifically focussed on key biological steps in the process will elucidate these concerns. Species such as C. petalophylla appear at particular risk based on their restricted distribution (Table 3) and the frequency of hybrid combinations recorded between section Ochraria and Politaria (Fig. 3). The apparently limited period of flowering of C. petalophylla, however, may act to successfully prevent hybridisation (Table 3).

9. Research directions The following list of research directions are placed in order of priority, but also in order of logical progression, as quantification of factors involved with one step will frequently allow more precise analysis of following steps. 1. Reproductive attributes of the plantation species. Quantify the genetic and environmentally induced variation in flowering precocity, abundance and phenology for the major plantation species and hybrids. This should include the development of predictive models for each trait. 2. Flowering phenology of the native species. This should focus on the native species found in regional co-occurrence with the plantations and be conducted at specific sites of co-occurrence, assessing both the plantation and native species. 3. Pollen dispersal and vector behaviour. Confirmation of vertebrate pollinator visitation of flowers of plantation grown Corymbia is required. This should include assessments of nocturnal activity and plantations in southern latitudes, i.e. in Victoria where vertebrate pollinator activity is expected to be less prevalent.

4. Cross-compatibility of regionally co-occurring native species. This should be conducted using (i) controlled isolation techniques, without artificial induction of receptivity through style cutting, to determine whether cross-combinations are possible, and (ii) supplementary pollination to determine crossability under competition with naturally occurring intraspecific pollen. Studies should be structured to address the three risk categories defined above and compared to seed set following intraspecific control crosses. 5. Levels of hybridisation at plantation boundaries. This would involve open-pollinated seed collections from native populations adjacent to plantations, to assess levels of hybridisation, and surveys for establishing F1 hybrids in areas of seedling recruitment. This would preferably be conducted using morphological screening techniques, however, molecular markers or a combination of both may be necessary to identify hybrids. The development of a morphological approach can be initiated using artificially produced hybrids. A subset of collections should be conducted at sites most likely to have hybridisation occurring, based on synchrony in flowering phenology and the taxonomic relatedness of co-occurring species. 6. Pattern of pollen dispersal from plantations. This will use the above approach (point 5) to detect hybrids, but focus on a select few plantations, detailing the variation in the frequency of hybridisation with distance from the pollen sources. The sampling strategy could be tailored accordingly to the community of vectors found to be present (i.e. vertebrates compared to invertebrates). Forest structure (i.e. degree of fragmentation) and composition (area and scale of flowering in related and unrelated plant species) should be integrated into such studies where possible. Correlated paternity approaches could also be used as an alternative molecular approach if quantitative markers specific to the plantation species are difficult to identify. 7. Seed dispersal from C. torelliana F1 hybrids. Confirmation of the lack of bee dispersal of seed of hybrid combinations planned for commercial deployment compared to the pure species C. torelliana is required. This should include from discarded capsules following feeding by birds. 8. Hybrid establishment and fitness. The establishment of seed sowing and seedling-based trials within disturbed and regenerating areas of forest is necessary. This would be concentrated on species at greatest apparent risk of gene flow based on spatial proximity, flowering synchrony and observed hybridisation and be established with plants generated from artificial pollination studies or hybrids that have been detected among openpollinated seed lots. Monitoring of any exotic hybrids found selfestablished, along with suitable control plants, would represent the most appropriate ‘‘trial’’. All trials should be assessed through to reproductive age or until all hybrids have died. 9. Risk assessment of the potential for gene flow. As empirical data is collected on each step in the process of gene flow, it should be fed into an analytical framework to allow better quantification of risk. Data included in such analyses would include regional co-occurrence, flowering synchrony, pollen dispersal patterns, cross-compatibility, hybrid survival and fitness, as well as the conservation status/value of the native species or populations.

Acknowledgements This research was supported under an Australian Research Council’s Linkage Project (grant no. LP0455522) awarded to Professor Brad Potts and Associate Professor Rene´ Vaillancourt, University of Tasmania. Many thanks go to R. Kirwood for GIS map

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

construction and compilation of associated data, G. Luker for assistance with the construction of Fig. 2 of the manuscript, D. Lee and G. Dickenson for sharing pre-publication results. H. Wallace, S. Boyton, D. Kleinig, J. Ochieng, C. Chaffey also provided helpful discussions on the topic.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.foreco.2008.03.028. References Anon., 2002. Council Business Paper. Meeting February 12. Proposed Amendments to DCP 17. QPO (Online). City Council, Lismore, New South Wales. Anon., 2007. Kendron Brook catchment remnant vegetation prioritisation assessmentand weed mapping project final report. Kendron Brook Catchment Branch, WPSQ & Water Resources Branch, City Policy & Strategy, Brisbane City Council, Brsbane, Queensland. Anttila, C.K., Daehler, C.C., Rank, N.E., Strong, D.R., 1998. Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. American Journal of Botany 85, 1597–1601. Apiolaza, L.A., Potts, B.M., Gore, P.L., 2001. Genetic control of peak flowering time of Eucalyptus globulus. In: Barros, S. (Ed.), IUFRO International Symposium on Developing the Eucalypt of the Future. Chile, INFOR, Valdivia, p. 155. Arnold, M.L., 1997. Natural Hybridization and Evolution. Oxford University Press, Oxford. Arnold, M.L., Bulger, M.R., Burke, J.M., Hempel, A.L., Williams, J.H., 1999. Natural hybridization: how low can you go and still be important? Ecology 80, 371– 381. Asante, K., Brophy, J., Doran, J., Goldsack, R., Hibbert, D., Larmour, J., 2001. A comparative study of the seedling leaf oils of the spotted gums: species of the Corymbia (Myrtaceae), section Politaria. Australian Journal of Botany 49, 55– 56. Atkinson, M.D., Jervis, A.P., Sangha, R.S., 1997. Discrimination between Betula pendula, Betula pubescens, and their hybrids using near-infrared reflectance spectroscopy. Canadian Journal of Forest Research 27, 1896–1900. Austerlitz, F., Smouse, P.E., 2001a. Two-generation analysis of pollen flow across a landscape. III. Impact of adult population structure. Genetical Research 78, 271– 280. Austerlitz, F., Smouse, P.E., 2001b. Two-generation analysis of pollen flow across a landscape. II. Relation between 0 ft, pollen dispersal and interfemale distance. Genetics 157, 851–857. Austerlitz, F., Smouse, P.E., 2002. Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161, 355–363. Bacles, C.F.E., Brooks, J., Lee, D.L., Schenk, P., Lowe, A., Kremer, A., 2007. Reproductive biology of Corymbia citriodora subsp. variegata and effective pollen-mediated gene flow across its native range. In: Proceedings IUFRO Working Group 2.08.03, Eucalypts and Diversity: Balancing Productivity and Sustainabilty. IUFRO, Durban, South Africa, pp. 1–11. Barbour, E.L., 2004. Eucalypt Hybrids in South-Western Western Australia. Rural Industries and Development Corporation, CAL-5A. Cambera, Australia. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., Tibbits, W.N., Wiltshire, R.J.E., 2002. Gene flow between introduced and native Eucalyptus species. New Forests 23, 177–191. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., 2003. Gene flow between introduced and native Eucalyptus species: exotic hybrids are establishing in the wild. Australian Journal of Botany 51, 429–439. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., 2005a. Gene flow between introduced and native Eucalyptus species: crossability of native Tasmanian species with exotic E. nitens. Australian Journal of Botany 53, 465–477. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., 2005b. Pollen dispersal from exotic eucalypt plantations. Conservation Genetics 6, 253–257. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., 2006a. Gene flow between introduced and native Eucalyptus species: early-age selection limits invasive capacity of exotic E. ovata  nitens F1 hybrids. Forest Ecology and Management 228, 206– 214. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., Tibbits, W.N., 2006b. Gene flow between introduced and native Eucalyptus species: flowering asynchrony as a barrier to F1 hybridisation between exotic E. nitens and native Tasmanian Symphyomyrtus species. Forest Ecology and Management 226, 9–21. Barbour, R.C., Potts, B.M., Vaillancourt, R.E., 2007. Gene flow between introduced and native Eucalyptus species: morphological analysis of tri-species and backcross hybrids involving E. nitens. Silvae Genetica 56, 127–133. Barbour, R.C., Otahal, Y., Vaillancourt, R.E., Potts, B.M., 2008. Assessing the risk of pollen-mediated gene flow from exotic Eucalyptus globulus plantations into native eucalypt populations of Australia. Biological Conservation 141, 896–907. Brock, M.T., 2004. The potential for genetic assimilation of a native dandelion species, Taraxacum ceratophorum (Asteraceae), by the exotic congener T. officinale. American Journal of Botany 91, 656–663.

17

Brooker, M.I.H., Kleinig, D., 1996. Eucalyptus: An Illustrated Guide to Identification. Reed Books, Melbourne, Australia. Brooker, M.I.H., 2000. A new classification of the genus Eucalyptus L’Her. (Myrtaceae). Australian Systematic Botany 13, 79–148. Chambers, P.G.S., Potts, B.M., Tilyard, P., 1997. The genetic control of flowering precocity in Eucalyptus globulus ssp. globulus. Silvae Genetica 46, 207–214. Chapman, M.A., Burke, J.M., 2006. Letting the gene out of the bottle: the population genetics of genetically modified crops. New Phytologist 170, 429–443. Commonwealth of Australia, 2002. Plantations of Australia: the 2020 Vision. Canberra. CPBR, 2006. EUCLID: Eucalypts of Australia. CSIRO Publishing, Collingwood, Victoria. Cremer, K.W., 1966. Dissemination of seed from Eucalyptus regnans. Australian Forestry 30, 33–37. Dale, J.A., Hawkins, P.J., 1983. Phenological studies of spotted gum in southern inland Queensland. Department of Forestry Queensland, Technical paper no. 35, Brisbane. de Assis, T.F., 2000. Production and use of Eucalyptus hybrids for industrial purposes. In: Dungey, H.S., Dieters, M.J., Nikles, D.G. (Eds.), Hybrid Breeding and Genetics of Forest Trees. Proceedings of QFRI/CRC-SPF Symposium. Noosa, Australia, Department of Primary Industries, Brisbane, pp. 63–74. Delaporte, K.L., Conran, J.G., Sedgley, M., 2001. Interspecific hybridization within Eucalyptus (Myrtaceae): subgenus Symphyomyrtus, sections Bisectae and Adnataria. International Journal of Plant Sciences 162, 1317–1326. Dickinson, G., Bristow, M., Kelly, N., 2004. Promising high-value hardwood plantation tree species for the dry tropics of Queensland. In: Bevege, D.I., Bristow, M., Nikles, D.G., Skelton, D.J. (Eds.), Prospects for High-Value Hardwood Timber Plantations in the ‘Dry’ Tropics of Northern Australia. Private Forestry North Queensland Association, Inc, Mareeba, pp. 1–8. Dickinson, G., Lewty, M., Nester, M., Huth, J., Smith, T., Lee, D., Raddatz, C., 2005. Silviculture Research to Assist Large-scale Commercial Farm Forestry in Queensland. A report for the Joint Venture Agroforestry Program and the Natural Heritage Trust. Rural Industries Research and Development Corporation, Publication No. 04/185, Canberra. Dickinson, G.R., Wallace, H.M., Kelly, N.I., Lee, D.J., 2007. Inter-specific Corymbia hybrid research; providing new opportunities for plantation expansion in northern Australia. In: Nichols, D. (Ed.), ANZIF 2007 Growing Forest Values Conference, Coffs Harbour, NSW, Australia. Dyer, R.J., Westfall, R.D., Sork, V.L., Smouse, P.E., 2004. Two-generation analysis of pollen flow across a landscape V: a stepwise approach for extracting factors contributing to pollen structure. Heredity 92, 204–211. Eby, P., 1991. Seasonal movements of grey-headed flying-foxes, Pteropus poliocephalus (Ciroptera: Pteropodidae), from two maternity camps in northern New South Wales. Wildlife Research 18, 547–559. Eby, P., 1996. Interactions Between the Grey-headed Flying Fox Pteropus poliocephalis (Chiroptera: Pteropodidae) and its diet plants—seasonal movements and seed dispersal. University of New England. Eldridge, K., Davidson, J., Harwood, C., van Wyk, G., 1993. Eucalypt Domestication and Breeding. Clarendon Press, Oxford. Ellis, M.F., Sedgley, M., Gardner, J.A., 1991. Interspecific pollen–pistil interaction in Eucalyptus L’Her. (Myrtaceae): the effect of taxonomic distance. Annals of Botany 68, 185–194. Ellstrand, N.C., 1992a. Gene flow among seed plant populations. New Forests 6, 241–256. Ellstrand, N.C., 1992b. Gene flow by pollen: implications for plant conservation genetics. Oikos 63, 77–86. Ellstrand, N.C., Prentice, H.C., Hancock, J.F., 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annual Review of Ecology and Systematics 30, 539–563. Espejo, J., Herna´ndez, V., Sierra, V., Bacerra, J., Lo´pez, R., 2004. Determination of terpenes through Gas Chromatography–Mass Spectrometry (GC–MS) a new tool in the early determination of hybrid progenies of Eucalyptus nitens  E. globulus. In: Pereira, J., Marques, C., Coutinho, J., Madeira, M., Tome´, M., Borralho, N. (Eds.), Proceedings of the International IUFRO Conference ‘‘Eucalyptus in a changing world’’ on Silviculture and Improvement of Eucalypts, Aveiro, Portugal, RAIZ - Instituto de Investigac¸a˜o da Floresta e Papel, Eixo. Figueroa, M.E., Castillo, J.M., Redondo, S., Luque, T., Castellanos, E.M., Nieva, F.J., Luque, C.J., Rubio-Casal, A.E., Davy, A.J., 2003. Facilitated invasion by hybridization of Sarcocornia species in a salt-marsh succession. Journal of Ecology 91, 616–626. Gore, P.L., Potts, B.M., Volker, P.W., Megalos, J., 1990. Unilateral cross-incompatibility in Eucalyptus: the case of hybridisation between E. globulus and E. nitens. Australian Journal of Botany 38, 383–394. Gore, P.L., Potts, B.M., 1995. The genetic control of flowering time in Eucalyptus globules, E. nitens and their F1 hybrids. In: Potts, B.M., Borralho, N.M.G., Reid, J.B. (Eds.), Tibbits, W.N., Raymond, C.A. (Eds.), Proceeding of the CRC-THF IUFRO Conference on Eucalypt Plantations: Improving Fibre Yield and Quality, Hobart, Australia, CRC for Temperate Hardwood Forestry, pp. 241–242. Griffin, A.R., 1980. Floral phenology of a stand of mountain ash (Eucalyptus regnans F. Muell.) in Gippsland, Victoria. Australian Journal of Botany 28, 393–404. Griffin, A.R., Burgess, I.P., Wolf, L., 1988. Patterns of natural and manipulated hybridisation in the genus Eucalyptus L’Herit.—a review. Australian Journal of Botany 36, 41–66. Griffin, A.R., 1989. Sexual reproduction and tree improvement strategy—with particular reference to Eucalyptus. In: Gibson, G.I., Griffin, A.R., Matheson,

18

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19

A.C. (Eds.), Proceedings of the IUFRO Conference. Breeding Tropical Trees: Population Structure and Genetic Improvement Strategies in Clonal and Seedling Forestry, Pattaya, Thailand/Oxford Forestry Institute, Oxford, United Kingdom/Winrock International, Arlington, Virginia, USA, pp. 52–67. Hamrick, J.L., Nason, J.D., 2000. Gene flow in forest trees. In: Young, A., Boshier , D., Boyle, T. (Eds.), Forest Conservation Genetics: Principles and Practice. CABI Publishing, Wallingford, UK, pp. 81–90. Hill, K.D., Johnson, L.A.S., 1995. Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6, 185–504. Hill, R.S. (Ed.), 1994. History of the Australian vegetation: Cretaceous to recent. Cambridge University Press, Melbourne. Hingston, A.B., McQuillan, P.B., Potts, B.M., 2004. Pollinators in seed orchards of Eucalyptus nitens. Australian Journal of Botany 52, 209–222. Hoffman, C.A., 1990. Ecological risks of genetic engineering of crop plants. Bioscience 40, 434–437. House, S.M., 1997. Reproductive biology of eucalypts. In: Williams, J., Woinarski, J. (Eds.), Eucalypt Ecology: Individuals To Ecosystems. Cambridge University Press, Cambridge, pp. 30–56. Jackson, S.M., 2001. Foraging behaviour and food availability of the mahogany glider Petaurus gracilis (Petauridae: Marsupialia). Journal of Zoology 253, 1–13. Jones, M., Stokoe, R., Cross, M., Scott, L., Maguire, T., Shepherd, M., 2001. Isolation of microsatellite loci from spotted gum (Corymbia variegata), and cross-species amplification in Corymbia and Eucalyptus. Molecular Ecology Notes 1, 276–278. Kanowski, J., Catterall, C.P., Wardell-Johnson, G.W., 2005. Consequences of broadscale timber plantations for biodiversity in cleared rainforest landscapes of tropical and subtropical Australia. Forest Ecology and Management 208, 359– 372. Keatley, M.R., Hudson, I.L., Fletcher, T.D., 2004. Long-term flowering synchrony of box-ironbark eucalypts. Australian Journal of Botany 52, 47–54. King, R., 2004. Spatial structure and population genetic variation in a eucalypt species complex. PhD Thesis. Griffith University. Ladiges, P.Y., Udovicic, F., 2000. Comment on a new classification of the eucalypts. Australian Systematic Botany 13, 149–152. Larmour, J.S., Whitfeld, S.J., Harwood, C.E., Owen, J.V., 2000. Variation in frost tolerance and seedling morphology of the spotted gums Corymbia maculata, C. variegata, C. henryi and C. citriodora. Australian Journal of Botany 48, 445–453. Law, B., Mackowski, C., Schoer, L., Tweedie, T., 2000. Flowering phenology of myrtaceous trees and their relation to climatic, environmental and disturbance variables in northern New South Wales. Austral Ecology 25, 160–178. Lee, D.J., Debuse, V.J., Pomroy, P.C., Robson, K.J., Nikles, D.G., 2005. Developing Genetically Adapted Tree Varieties for Marginal Areas of Northern Australia. Rural Industries Research and Development Corporation, 04/186, Project No DAQ-261A, Canberra. Lee, D.J., 2007. Achievements in forest tree genetic improvement in Australia and New Zealand 2: development of Corymbia species and hybrids for plantations in eastern Australia. Australian Forestry 70, 11–16. Levin, D.A., 1978. The origin of isolating mechanisms in flowering plants. Evolutionary Biology 11, 185–317. Levin, D.A., Francisco-ortega, J., Jansen, R.K., 1996. Hybridization and the extinction of rare plant species. Conservation Biology 10, 10–16. Linacre, N.A., Ades, P.K., 2004. Estimating isolation distances for genetically modified trees in plantation forestry. Ecological Modelling 179, 247–257. Lopez, G.A., Potts, B.M., Gore, P.L., 2000a. The inheritance of flowering time in interspecific F1 hybrids of Eucalyptus. In: Dungey, H.S., Dieters, M.J., Nikles, D.G. (Eds.), Hybrid Breeding and Genetics of Forest Trees. Proceedings of QFRI/CRCSPF Symposium, Noosa, Australia, Queensland Department of Primary Industries, Brisbane, pp. 453–456. Lopez, G.A., Potts, B.M., Tilyard, P.A., 2000b. F1 hybrid inviability in Eucalyptus: the case of E. ovata  E. globulus. Heredity 85, 242–250. Markus, N., Hall, L., 2004. Foraging behaviour of the black flying-fox (Pteropus alecto) in the urban landscape of Brisbane, Queensland. Wildlife Research 31, 345–355. McCoy, M., 1990. Pollination of eucalypts by flying foxes in northern Australia. In: Slack, J.M. (Ed.), Flying Fox Workshop. NSW Agriculture and Fisheries, Wollongbar, pp. 33–37. McDonald, M., 2004. Outcrossing rates in a seedling seed orchard of Corymbia maculata (Spotted Gum). CSIRO Forestry and Forest Products, 1401, Canberra. McDonald, M.W., Bean, A.R., 2000. A new combination in Corymbia section Politaria: C. citriodora var. variegata (Myrtaceae). Austrobaileya 5, 735–736. McDonald, M.W., Butcher, P.A., Bell, J.C., Larmour, J.S., 2000. Intra- and interspecific allozyme variation in eucalypts from the spotted gum group, Corymbia, section Politaria (Myrtaceae). Australian Systematic Botany 13, 491–507. McDonald, M.W., Butcher, P.A., Larmour, J.S., Bell, J.C., 2003. Corrigendum. Intraand interspecific allozyme variation in eucalypts from the spotted gum group, Corymbia, section Politaria (Myrtaceae). Australian Systematic Botany 16, 643– 717. McKinnon, G.E., Jordan, G.J., Vaillancourt, R.E., Steane, D.A., Potts, B.M., 2004. Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London—Series B: Biological Sciences 359, 275–284. McKinnon, G.E., Vaillancourt, R.E., Steane, D.A., Potts, B.M., 2008. An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae). American Journal of Botany 95, 368–380. Meddings, R.A., McComb, J.A., Calver, M.C., Thomas, S.R., Mazanec, R.A., 2003. Eucalyptus camaldulensis  globulus hybrids. Australian Journal of Botany 51, 319–331.

Moncur, M.W., Hand, F.C., Ramsden, N.G., 1994. Environmental and Cultural Effects on Flowering and Seed Production of Plantation Grown Eucalyptus nitens. Report for the Tasmanian Forest Research Council, Inc. Division of Forestry, CSIRO, Canberra. National Forest Inventory, 2006. Australia’s Plantations. Bureau of Rural Sciences, Canberra. National Forest Inventory, 2007. Australia’s Plantations—Inventory Update. Bureau of Rural Sciences, Canberra. Nikles, D.G., Lee, D.J., Robson, K.J., Pomroy, P.C., Walker, S.W., 2000. Progress on species selection trials and genetic improvement for hardwoods for commercial plantings in Queensland. In: Snell, A., Vize, S. (Eds.), Opportunities for the New Millenium. Proceedings of the 2000 Australian Forest Growers Conference. Cairns, Australia, pp. 23–31. Ochieng, J.W., Steane, D.A., Ladiges, P., Baverstock, P.R., Henry, R.J., Shepherd, M., 2007a. Microsatellites retain phylogenetic signals across genera in Eucalypts (Myrtaceae). General and Molecular Biology 30, 1125–1134. Ochieng, J.W., Steane, D.A., Baverstock, P., Henry, R.J., Shepherd, M., 2007b. Nuclear Ribosomal Pseudogenes resolve a corroborated Monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs. Molecular Phylogenetics and Evolution 44, 752–764. Pacheco, I.A., Kageyama, P.Y., Wiendl, F.M., Filho, E.B., 1986. Study of the dispersion of pollen of Eucalyptus saligna Smith by Apis mellifera L. bees using 32P radioactive phosphorous. IPEF Piracicaba 34, 47–52. Parra-O, C., Bayly, M., Udovicic, F., Ladiges, P., 2007. ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae). Taxon 55, 653–663. Pilipenka, F.S., 1969. Hybridisation of Eucalypts in the USSR. Botanicheski Institut, Akademiya Nauk SSSR. Pook, E.W., Gill, A.M., Moore, P.H.R., 1997. Long-term variation of litter fall, canopy leaf area and flowering in a Eucalyptus maculata forest on the south coast of New South Wales. Australian Journal of Botany 45, 737–755. Potts, B.M., Reid, J.B., 1990. The evolutionary significance of hybridisation in Eucalyptus. Evolution 44, 2151–2152. Potts, B.M., Wiltshire, R.J.E., 1997. Eucalypt genetics and genecology. In: Wiliams, J., Woinarski, J. (Eds.), Eucalypt Ecology: Individuals to Ecosystems. Cambridge University Press, Cambridge, pp. 56–91. Potts, B.M., Volker, P.W., Tilyard, P.A., Joyce, K., 2000. The genetics of hybridisation in the temperate Eucalyptus. In: Dungey, H.S., Dieters, M.J., Nikles, D.G. (Eds.), Hybrid Breeding and Genetics of Forest Trees. Proceedings of QFRI/CRC-SPF Symposium. Noosa, Australia, Department of Primary Industries, Brisbane, pp. 200–211. Potts, B.M., Barbour, R.C., Hingston, A.B., Vaillancourt, R.E., 2003. TURNER REVIEW No 6—genetic pollution of native eucalypt gene pools—identifying the risks. Australian Journal of Botany 51, 333–427. Potts, B.M., Dungey, H.D., 2004. Hybridisation of Eucalyptus: key issues for breeders and geneticists. New Forests 27, 115–138. Pryor, L.D., Johnson, L.A.S., 1971. A Classification of the Eucalypts. Australian National University Press, Canberra. Pryor, L.D., 1976. Biology of Eucalypts. Edward Arnold, London. Pryor, L.D., Johnson, L.A.S., 1981. Eucalyptus, the universal Australian. In: Keast, A. (Ed.), Ecological Biogeography of Australia. W. Junk, The Hague, pp. 499–536. Raybould, A.F., Gray, A.J., 1994. Will hybrids of genetically modified crops invade natural communities? Trends in Ecology and Evolution 9, 85–89. Rhymer, J.M., Simberloff, D., 1996. Extinction by hybridisation and introgression. Annual Review of Ecology and Systematics 27, 83–109. Salt, D., Lindenmayer, D., Hobbs, R., 2005. Trees and Biodiversity: A Guide for Australian Farm Forestry. Rural Industries and Development Corporation/Land & Water Australia/FWPRDC/MDBC Joint Venture Agroforestry Program, RIRDC publication number: 03/047, Kingston, ACT, Australia. Sedgley, M., Granger, L., 1996. Embryology of Eucalyptus spathulata and E. platypus (Myrtaceae) following selfing, crossing and reciprocal interspecific pollination. Australian Journal of Botany 44, 661–671. Shapcott, A., 1998. The genetics of Ptychosperma bleeseri, a rare palm from the Northern Territory. Australia. Biological Conservation 85, 203–209. Shepherd, M., Kasem, S., Lee, D., Henry, R., 2006. Construction of microsatellite linkage maps for Corymbia. Silvae Genetica 55, 228–238. Shepherd, M., Kasem, S., Ablett, G., Ochieng, J., Crawford, A., 2008. Genetic structuring in the spotted gum complex (Genus Corymbia Section Politaria). Australian Systematic Botany 21, 15–25. Small, E., 1984. Hybridisation in the domesticated-weed-wild complex. In: Grant, W.F. (Ed.), Plant Biosystematics. Academic Press, San Diego, CA, pp. 195– 210. Smith, H.J., Henson, M., Boyton, S., 2007. Forests NSW’ spotted gum (Corymbia spp.) tree improvement and deployment strategy. In: Wu, H., Williams, D., Harwood, C. (Eds.), Australasian Forest Genetics Conference – Breeding for Wood Quality. Australasian forestry research group 1 (Genetics), the IUFRO southern pine working (2.02.20), Hobart, Tasmania, Australia. Smouse, P.E., Dyer, R.J., Westfall, R.D., Sork, V.L., 2001. Two-generation analysis of pollen flow across a landscape. I. Male gamete heterogeneity among females. Evolution 55, 260–271. Snow, A.A., Uthus, K.L., Culley, T.M., 2001. Fitness of hybrids between weedy and cultivated radish: implications for weed evolution. Ecological Applications 11, 934–943. Southerton, S.G., Birt, P., Porter, J., Ford, H.A., 2004. Review of gene movement by bats and birds and its potential significance for eucalypt plantation forestry. Australian Forestry 67, 44–53.

R.C. Barbour et al. / Forest Ecology and Management 256 (2008) 1–19 Steane, D.A., McKinnon, G.E., Vaillancourt, R.E., Potts, B.M., 1999. ITS sequence data resolve higher level relationships among the eucalypts. Molecular Phylogenetics and Evolution 12, 215–223. Steane, D.A., Nicolle, D., McKinnon, G., Vaillancourt, R., Potts, B., 2002. Higher-level relationships among the eucalypts are resolved by ITS-sequence data. Australian Systematic Botany 15, 49–62. Strahan, R., 1991. Complete Book of Australian Mammals: the National Photographic Index of Australian Wildlife. Australian Museum, Cornstalk. Strauss, S.Y., 2001. Benefits and risks of biotic exchange between Eucalyptus plantations and native Australian forests. Austral Ecology 26, 447–457. Trueman, S.J., Richardson, D.M., 2007. In vitro propagation of Corymbia torelliana  C. citriodora (Myrtaceae) via cytokinin-free node culture. Australian Journal of Botany 55, 471–481. Udovicic, F., McFadden, G.I., Ladiges, P.Y., 1995. Phylogeny of Eucalyptus and Angophora based on 5S rDNA spacer sequence data. Molecular phylogenetics and evolution 4, 247–256. Udovicic, F., Ladiges, P.Y., 2000. Informativeness of nuclear and chloroplast DNA regions and the phylogeny of the eucalypts and related genera (Myrtaceae). Kew Bulletin 55, 633–645. Van Raamsdonk, L.W.D., Van Der Maesen, L.G.G., 1996. Crop-weed complexes: the complex relationship between crop plants and their wild relatives. Acta Botanica Neerlandica 45, 135–155. van Wyk, G., 1981. Pollen management for eucalypts. In: Pollen Management Handbook. Agriculture Handbook No. 587., USDA Forest Service. Vanden Broeck, A., Cox, K., Quataert, P., Van Bockstaele, E., Van Slycken, J., 2003. Flowering phenology of Populus nigra L., P. nigra cv. italica and P.  canadensis Moench. and the potential for natural hybridisation in Belgium. Silvae Genetica 52, 280–283. Vanden Broeck, A., Villar, M., Van Bockstaele, E., Van Slycken, J., 2005. Natural hybridization between cultivated poplars and their wild relatives: evidence and

19

consequences for native poplar populations. Annals of Forest Science 62, 601– 613. Verma, S.K., Sharma, V.K., 1999. The phenology of flowering of reciprocal F1 hybrids Eucalyptus citriodora Hook  Eucalyptus torelliana F.v. Muell., F2 segregates and parent species of new forest, Dehra Dun. Annals of Forestry 7, 120–124. Vila, M., Weber, E., Antonio, C.M.D., 2000. Conservation implications of invasion by plant hybridization. Biological Invasions 2, 207–217. Wallace, H., Trueman, S.J., 1995. Dispersal of seeds of Eucalyptus torelliana by the stingless bee, Trigona carbonaria. Oecologia 104, 12–16. Wallace, H., Stokoe, R., Trueman, S.J., Lee, D., 2005. Corymbia torelliana hybrids for hardwood forestry—without the weediness. In: Lee, D. (Ed.), Corymbia Research Meeting: Underpinning Development of a Profitable Hardwood Plantation Industry in Northern Australia by Research into Corymbia Species and Hybrids, Gympie, Queensland, Queensland Government, Department of Primary Industries and Fisheries, pp. 7–8. Wallace, H.M., Howell, M.G., Lee, D.J., 2008. Standard yet unusual mechanisms of long-distance dispersal: Seed dispersal of Corymbia torelliana by bees. Diversity and Distributions 14, 87–94. Wardell-Johnson, G., Williams, J.E., Hill, K., Cumming, R., 1997. Evolutionary biogeography and contemporary distribution of Eucalyptus. In: Williams, J., Woinarski, J. (Eds.), Eucalypt Ecology: Individuals to Ecosystems. Cambridge University Press, Cambridge, pp. 92–128. Whitham, T.G., Bailey, J.K., et al., 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics 7, 510–523. Williams, D.R., Potts, B.M., Neilsen, W., Joyce, K., 2006. The effect of tree spacing on the production of flowers in Eucalyptus nitens. Australian Forestry 69, 299–304. Wiltshire, R.J.E., Reid, J.B., 1987. Genetic variation in the Spinning Gum, Eucalyptus perriniana F. Muell. ex Rodway. Australian Journal of Botany 35, 33–47. Wolf, D.E., Takebayashi, N., Rieseberg, L.H., 2001. Predicting the risk of extinction through hybridization. Conservation Biology 15, 1039–1053.