Northbourne Avenue's median strip will be bare of trees by late 2016 or early 2017 as construction of the light rail line gets under way.
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Growing of about 700 brittle gum saplings will begin two years before the semi-mature replacement trees are planted along the completed light rail line, with the Territory and Municipal Services directorate expected to choose Yarralumla Nursery for the commission.
The trees will be grown to about 2.5 metres before they are planted on the roadway, with trunks grown to about 50 millimetres.
Announcing plans for Eucalyptus mannifera to be planted above an "urban meadow" along the 12--kilometre route, Capital Metro Minister Simon Corbell said there were already about 100,000 of the trees around Canberra's suburbs.
The consortium chosen to build and operate the line will decide the final timeline for removal and replanting, with the Northbourne section expected to be planted in staggered formation.
"We'd be looking within the first six to 12 months of construction commencing," Mr Corbell said on Thursday.
"Most likely it will need to be removal largely in one go, but I am also aware the National Capital Authority are keen to see other staging options at least considered."
Mr Corbell was interested in considering an exotic tree planting on Northbourne Avenue but the NCA's guidelines required Australian natives in the area.
The policy was developed in the 1970s and has seen natives used in Canberra's town centres.
The men responsible for planning and growing the city's original urban landscape both favoured a mix or native and exotic trees for the city.
Horticulturalist Charles Weston, Canberra's foundation afforestation officer, used native Australian plants and trees alongside exotics, including species from Europe and North America. Responsible for planting two million trees and shrubs between 1913 and 1926, Mr Weston also planted eucalypts and wattles.
His successor, Lindsay Pryor, believed species should be chosen for their capacity to grow well irrespective of their origin. Appointed director of Parks and Gardens in 1944 and after extensive travel overseas, he said in a 1990 interview that some species were "elegant in their own right".
Mr Pryor followed the Weston approach and is credited with the foundation of the Australian National Botanic Gardens.
"I adopted the idea and I've stuck with it ever since, that one should use species which grow well, irrespective of whether they're indigenous Australian or exotic," he said.
"I've always believed that a mix of plant material to be used, as between exotic and indigenous, is appropriate."
The Barr government and Capital Metro Agency believe many of the Northbourne Avenue trees are failing and will need to be replaced regardless of the planned construction.
Mr Pryor and members of an expert committee were responsible for the original red gum plantings, also known as Eucalyptus blakelyi.
He considered the plantings to have achieved only an "indifferent result" due to lerp insect damage, causing discolouration and shed of limbs.
In an early 1980s report, the Capital Territory Department acknowledged it did not know how to save spotted white gum trees and the remaining red gums along the avenue as drought and persistent insect attack took their toll.
City Parks Administration director Ron Murray said in October 1981 that there were no proposals to replace the trees, despite spraying providing only a temporary relief.
A 2010 assessment found some of the current crop of Northbourne trees would have remained viable for as long as 20 years.