The mayor and Mr Lee each said Auckland should not repeat the mistake of underestimating demand for infrastructure such as the Harbour Bridge, which opened in 1959 with four lanes, only for four more lanes to be added later.
But Dr Cayford said in his blog that the most important part of the rail project would be the extra network capacity to be gained from connecting Britomart - which is now constrained by being a dead-end station - to the western line at Mt Eden.
"This will lead to much higher frequencies and greater carrying capacity per hour, even if there are no stations along the tunnel," he said.
Once the tunnels were operating from the western end of Britomart, a strong case would emerge for properly-funded stations to be built at strategic points along the new corridor.
"Landowners and public alike will call for stations, and the argument for private contributions to the cost and amenity of those stations will be huge," Dr Cayford said.
"Build the tunnel infrastructure and development will follow. Auckland Council must build the network, and that will be the trigger for next stages of development."
Dr Cayford described Manukau's new 2km spur railway as "a bleak reminder of what happens when what is built is a politically-motivated whole project".
"There it was all or nothing. It was all built and it is still nothing in regional terms, because the fundamental need to build a network was not respected."
He said the project, which has cost KiwiRail and Auckland Transport and its predecessors $81 million, was built contrary to advice from planners of Perth's successful rail network to develop loops rather than spur lines.
His comments followed an informal survey on Monday last week by three Auckland Council members who counted only 30 passengers catching a total of six trains from Manukau over two hours from 6am.
Patronage picked up later in the day, which had a wet start, and Auckland Transport is confident of meeting an annual patronage target of 600,000 trips through the line's new station once the Manukau Institute of Technology opens a satellite campus above it next year.
But councillor George Wood, a critic of the station's location, said of the target: "It's got a long way to go."
The project was first championed by former Manukau Mayor Sir Barry Curtis, and then Mr Brown as his successor, but opposed by Dr Cayford as regional transport chairman.