The potential for gene flow from exotic eucalypt plantations into Australia's rare native eucalypts
Research highlights
▶ The potential for genetic contamination of Australia's rare native eucalypts from hybridisation with non-local eucalypt plantations was assessed. ▶ 70% of the 74 nationally listed rare eucalypt taxa were at negligible risk. ▶ Rare taxa most at risk of hybridisation with plantation species were identified. ▶ A case study aimed at testing the risk assessment and adaptive management strategies for a rare taxa in a high risk landscape was undertaken. ▶ Hybrids between the rare and plantation species comprised 0.2% of the open-pollinated seed collected from the rare species, but this rate is expected to increase as flowering increases in the plantation.
Introduction
Hybridisation between species or between naturally allopatric populations is now recognised as being an important contributor to the evolution (Abbott et al., 2003, Ellstrand and Schierenbeck, 2000) and invasion (Ellstrand et al., 2010, Gaskin and Schaal, 2002, Vila et al., 2000) of many exotic plant species. Movement of pollen and its potential genetic and ecological consequences became a public concern following the deployment of genetically modified (GM) crops, as escapes of transgenes into non-transgenic populations were reported (Stewart et al., 2003). These studies highlighted the importance of considering pollen movement and its impacts more generally (Ellstrand, 1992, Ellstrand and Elam, 1993). Gene flow from non-GM crops or exotic species into native populations through hybridisation and introgression has been recognised as posing a risk to the genetic integrity and survival of “pure” species populations (Ellstrand, 1992, Rhymer and Simberloff, 1996, Wolf et al., 2001). These risks have the potential to be higher in the case of rare species and small populations, due to their vulnerability to reproductive swamping (i.e. source/sink effects, Ellstrand and Elam, 1993, Field et al., 2009, Levin et al., 1996, Wolf et al., 2001) and sensitivity to compounding adverse environmental conditions (Rhymer, 2008).
Eucalypts represent a central component of the Australian biota, being the dominant tree in the majority of non-arid woodland and forest communities (Williams and Woinarski, 1997). There are nearly 900 eucalypt taxa (CPBR, 2006), which are endemic to Australia and its surrounding islands. Within these, 74 taxa are currently listed as endangered or vulnerable at the national level in Australia and require special attention. A notable characteristic of eucalypts is their propensity for interspecific hybridisation (Potts and Wiltshire, 1997). Under natural circumstances eucalypts are often observed to hybridise (Griffin et al., 1988, Potts and Wiltshire, 1997), however, the degree to which this occurs is limited by pre-mating barriers such as spatial isolation and flowering asynchrony (Keatley et al., 2004, Potts and Wiltshire, 1997), and post-mating crossing-incompatibilities. The latter prevents successful hybridisation between the three genera of eucalypts (Angophora, Corymbia, and Eucalyptus) and also between the major subgenera within Eucalyptus (Griffin et al., 1988, Potts et al., 2003).
At least eight eucalypt species and a few artificial hybrids are being deployed in industrial hardwood plantations in Australia (National Forest Inventory, 2006). This plantation estate has expanded dramatically over the last two decades, and now covers nearly 1 million ha in Australia (950,000 ha, Gavran and Parsons, 2009). Its expansion is likely to continue due to increasing public pressure to reduce native forest harvesting, reduce the Australian trade deficit in forest products and to develop carbon off-set industries (National Forest Inventory, 2006). Due to the often weak barriers to hybridisation within eucalypts, there is concern over the potential for pollen-mediated gene flow from plantations into native eucalypt populations (Kanowski et al., 2005, Potts et al., 2003, Salt et al., 2005, Strauss, 2001, Wardell-Johnson et al., 1997). This concern is based on the fact that genetic material used for stocking plantations is typically established well out of its native range, as locally exotic species, hybrids, provenances or genotypes (Barbour et al., 2008a, Potts et al., 2003).
Considerable work has been conducted to assess the potential for exotic gene flow from the major temperate plantation eucalypts in Australia, Eucalyptus globulus and Eucalyptus nitens. This work has demonstrated that F1 hybridisation involving plantations and their adjacent native species can occur (Barbour et al., 2008b, Barbour et al., 2003, Barbour et al., 2005a, Barbour et al., 2005b, Barbour et al., 2006b, Barbour et al., 2002) and that F1 hybrid seedlings are establishing in the wild at some locations (Barbour et al., 2008b, Barbour et al., 2003). In addition, work in the subtropical and tropical regions of Australia has identified a potential for such gene flow (Barbour et al., 2008a, Kanowski et al., 2005). An important aspect of assessing the off-site risks from planting Eucalyptus that has not been addressed is the likelihood of exotic gene flow to the rare eucalypt species of Australia.
The aim of this study was to assess the likelihood of pollen-mediated gene flow from eucalypt plantations into all nationally listed endangered or vulnerable (herein referred to as rare) eucalypt species of Australia to better focus resources to the protection of species most at risk. This assessment was conducted through the integration of spatial analyses of the proximity of plantations to each native species, and the knowledge of the reproductive barriers that exist amongst them. Following this, a detailed case study was conducted into the likelihood of exotic gene flow into a rare Tasmanian species, Eucalyptus perriniana, from surrounding E. nitens plantations, by assessing levels of F1 hybridisation between the two species and their reproductive biology.
Section snippets
Spatial assessment
All 74 eucalypt species or subspecies classified as endangered or vulnerable in 2009 by the Australian Government (Department of the Environment, Water, Heritage and the Arts, www.deh.gov.au/cgi-bin/sprat/public/sprat.pl) were assessed for their spatial distribution relative to eucalypt plantations. Three species on the list, Eucalyptus aquatica, Eucalyptus olivacea and “Eucalyptus sp. Howes Swamp Creek” were not included in the analyses as they were no longer regarded as legitimate taxa and
Spatial assessment of plantations across Australia
Of the 74 nationally listed rare eucalypt taxa of Australia, 22 were found to have point locations (representing an individual or population) within 10 km of a eucalypt plantation of the same genus (Table 1). Looking specifically at each genus, no point locations for the four rare Corymbia species were found within this distance of Corymbia plantations. No known Angophora species are established as plantations, so neither of the two rare Angophora were found to be at risk. All 22 rare eucalypt
Discussion
Despite the broad overlap of the geographic distribution of both Australia's rare eucalypt taxa, and the current eucalypt plantation estate (Fig. 1), only 22 of the 74 endangered or vulnerable taxa were found within 10 km of a plantation. The four species predicted to have highest likelihood of exotic gene flow are E. alligatrix subsp. limaensis, E. conglomerata, E. kabiana, and E. strzeleckii; either because they had more than 10% of their distribution within 1 km of plantations, or due to
Acknowledgements
The authors wish to thank the CRC for Forestry for financial support, Gunns Ltd. and the Department of Primary Industries and Water (Threatened Species Unit) for permission to conduct seed collections and field observations, and Scott Nichols, Anthony Mann, Jnthony Bloomfield and Matthew Lacombe for their assistance. We also thank the National Plantation Inventory for providing the GIS shape files for the distribution of eucalypt plantations, and the following agencies for the point location
References (56)
- et al.
The risk of pollen-mediated gene flow from exotic Corymbia plantations into native Corymbia populations in Australia
Forest Ecol. Manage.
(2008) - et al.
Assessing the risk of pollen-mediated gene flow from exotic Eucalyptus globulus plantations into native eucalypt populations of Australia
Biol. Conserv.
(2008) - et al.
Gene flow between introduced and native Eucalyptus species: early-age selection limits invasive capacity of exotic E. ovata × nitens F1 hybrids
Forest Ecol. Manage.
(2006) - et al.
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 Ecol. Manage.
(2006) - et al.
Consequences of broadscale timber plantations for biodiversity in cleared rainforest landscapes of tropical and subtropical Australia
Forest Ecol. Manage.
(2005) - et al.
Plant conservation genetics in a changing world
Trends Plant Sci.
(2009) - et al.
Estimating isolation distances for genetically modified trees in plantation forestry
Ecol. Model.
(2004) - et al.
Association mapping in structured populations
Am. J. Hum. Genet.
(2000) - et al.
Natural inter-subgeneric hybridization between Eucalyptus acmenoides Schauer and Eucalyptus cloeziana F. Muell (Myrtaceae) in southeast Queensland
Ann. Bot.
(2001) - et al.
The potential for genetic contamination vs. augmentation by native plants in urban gardens
Biol. Conserv.
(2006)
Plant introductions, hybridization and gene flow
Philos. Trans. R. Soc. Lond., Ser. B: Biol. Sci.
Adaptation, migration or extirpation: climate change outcomes for tree populations
Evol. Appl.
Gene flow between introduced and native Eucalyptus species: exotic hybrids are establishing in the wild
Aust. J. Bot.
Gene flow between introduced and native Eucalyptus species: crossability of native Tasmanian species with exotic E. nitens
Aust. J. Bot.
Pollen dispersal from exotic eucalypt plantations
Conserv. Genet.
Gene flow between introduced and native Eucalyptus species
New Forest
A new classification of the genus Eucalyptus L’Her. (Myrtaceae)
Aust. Syst. Bot.
Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia
Conserv. Genet.
Conservation Biology: Evolution in Action
EUCLID: Eucalypts of Australia
Gene flow by pollen: implications for plant conservation genetics
Oikos
Got hybridization? A multidisciplinary approach for informing science policy
BioScience
Population genetic consequences of small population size: implications for plant conservation
Annu. Rev. Ecol. Evol. Syst.
Hybridization as a stimulus for the evolution of invasiveness in plants?
Proc. Natl. Acad. Sci. U.S.A.
Molecular and morphological evidence of natural interspecific hybridization between the uncommon Eucalyptus aggregata and the widespread E. rubida and E. viminalis
Conserv. Genet.
Hybrid Tamarix widespread in US invasion and undetected in native Asian range
Proc. Natl. Acad. Sci. U.S.A.
National Plantation Inventory 2009 Update
Sexual reproduction and tree improvement strategy—with particular reference to Eucalyptus
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