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A book of condolences and a photograph of former Finance Minister Jim Flaherty is placed on a table in the lobby of House of Commons on April 11, 2014.FRED CHARTRAND/The Canadian Press

Stephen Harper not only lost a friend and a party mentor when Jim Flaherty passed away suddenly last week, he gained another hole in the federal political landscape.

It is a hole that the diminutive former finance minister filled in a very big way – one that presents strategic challenges for Mr. Harper as he tries to create the most advantageous narrative for his party going into the 2015 general election.

There are now five empty seats to be filled with by-elections across the country: Two in Alberta and three – including one in Mr. Flaherty's riding of Whitby-Oshawa in the Greater Toronto Area. The race in the MacLeod riding south of Calgary, which became open last fall with the retirement of Ted Menzies, must be called by mid-May and it is customary for all vacancies to be filled at the same time.

That means Mr. Harper could call five by-elections to take place in June. But is it best to go all at once? Or would it be better to divide the races into two lots, holding the Alberta by-elections this spring and waiting for fall to call the votes in Ontario?

Splitting the votes is more expensive for the parties, robbing them of an economy of scale. The Conservatives, who have a much healthier bank account than either the Liberals or the New Democrats, may want to hold two sets of by-elections to drain the other parties' resources.

If they believe they are going to do very well, at least in the ridings that were Conservative before they became vacant, two well-spaced nights of victories might a good thing.

On the other hand, the Conservatives already had one scare last fall in the Manitoba riding of Brandon-Souris, a former Tory stronghold that became a head-to-head battle between themselves and the Liberals.

No party wants to lose ground during by-elections because it suggests their rivals have momentum. Perceived momentum – so political wisdom says – sometimes translates into real momentum. And another strong showing by the Liberals could provide tangible proof of the sustained popularity that Justin Trudeau has enjoyed in opinion polls.

So, if the Conservatives are worried about any of the seats that are currently open, they may not want to have bad news this spring followed by more bad news a few months from now when the the general vote in 2015 is closer on the horizon.

Trinity-Spadina, which was vacated when New Democrat MP Olivia Chow decided to enter municipal politics, is not a Conservative seat and there is no expectation that the Tory candidate will do well in that riding. With the current disarray of the Liberals in that constituency, the NDP believes it has a clear advantage.

Scarborough-Agincourt, which was opened by the recent resignation by Jim Karygiannis, is more of a crapshoot. Although Mr. Karygiannis held the riding for the Liberals since 1988, it may have been his ability to engage the immigrant groups that make up two-thirds of its populous that kept it in the Liberal fold. Any party could do well if it attracted the right candidate.

No one expects the Liberals or the New Democrats to win in MacLeod. It is solid Conservative territory.

Fort McMurray-Athabaska in northern Alberta, which became open in January with the resignation of Conservative MP Brian Jean, may be more difficult. Mr. Jean trounced his opposition in 2011, taking 71 per cent of the popular vote.

But the Liberals and the New Democrats are running strong candidates. The nature of the electorate is changing because of the large influx of oil field workers from other provinces. And one Conservative source familiar with the race in Fort McMurray warned it was not being treated as a slam-dunk. "Not taking anything for granted. We learned a lesson in Brandon," he said.

Sources for the New Democrats say "it could get interesting." And, even if the race was tight, it could suggest Conservative support is weakening.

Then there is Mr. Flaherty's riding, where he took nearly 60 per cent of the popular vote in 2011. The question is, how much of that was committed Conservative support and how much was due to Mr. Flaherty's own personal popularity?

Although the Liberals are leading in opinion polls across the country, recent polls suggest the Conservatives maintain the advantage in the GTA which includes Whitby-Oshawa. But the seat went Liberal as recently as 2004. It is also home to strong union elements that could be helpful to the New Democrats.

The GTA is critical to the Conservatives winning a second majority. They do not want to look like that support is seeping.

All of which may factor into Mr. Harper's decision about by-election timing – a decision with a fast-approaching deadline.

Gloria Galloway is a parliamentary reporter in Ottawa.

With a report from Josh Wingrove