Days before the start of the summer fishing season, when guides and outfitters on Canada’s west coast gamble their financial prospects for the year, fishing lodge owner Ryan Chamberland received devastating news.

The coastal waters of Vancouver Island, which he and four generations of his family had fished for salmon, would be out of bounds. The unexpected closure was part of a desperate effort by the Canadian government to save an endangered population of killer whales.

That same summer, Tahlequah, one of the threatened whales, nudged the lifeless body of her newborn calf for 17 days of mourning. Shortly after, the once-playful Scarlet, a three-year-old female orca, succumbed to a bacterial infection as scientists from the Canadian and US governments worked desperately to save her.

The unfolding tragedy of the southern resident killer whales – and the government response – has exposed a complex ecosystem in crisis. Chinook salmon, the whale’s main prey, are also disappearing. In an area heavily reliant on tourism and fishing, an impending collapse of the two species has led to feuding over how to stave off an ecological disaster.

“Shutting us down to create more prey for them is not going to do anything for their diet,” said Chamberland. After the news broke, he began receiving panicked calls from clients, looking to cancel trips planned months in advance. Shock quickly gave way to frustration for the young business owner. “I think it’s really scary that we are the target,” he said of the closures.

At the end of October, the federal government announced additional steps in its plan to save the whales, unveiling C$61.5m (£36m) in funding to establish protected zones, limit marine traffic and increase food sources for the whales. The funding comes in addition to a previously pledged C$167.4m for similar measures promised early in the year.

“We have an obligation both legally and from a moral perspective, from the context of sustaining biodiversity, to do what we can to protect and recover these whales,” the federal fisheries minister, Jonathan Wilkinson, told the Guardian. “The decline of biodiversity around the world we’re seeing is extremely sobering.”

The staggering body of evidence that marine waters are in trouble has prompted bitter finger pointing: fishermen blame the jarring noise of whale watching boat engines for the declining health of the whales. Whale watching companies in turn blame overfishing and agricultural waste dumped into the ocean. And First Nations face accusations they over-harvest salmon in some parts of the province.

In spite of the urgency, the crisis has been decades in the making: engine noise from commercial shipping, which has increased dramatically over the years, harms a whale’s ability to hunt. Toxic pollutants from agriculture and industry have built up in the whale’s blubber, and when they become stressed – often the result of hunger – the pollutants metabolise into their bodies, sickening them.

But many of the groups that spend time on the water agree: the largest and most troubling element of the whale’s trajectory to extinction is the disappearance of Chinook salmon – known by anglers as the “king salmon”.

For millennia, pods of orcas hunting along the rugged coast of British Columbia were a common sight. Held in high regard by First Nations communities, European settlers saw their voracious appetite for coveted Chinook salmon as a problem – going as far as lobbying for a cull of the whales they called the “blackfish”.

Today, there are only 74 of the salmon-eating killer whales left in the Salish Sea, known to researchers as “southern residents”. With a dwindling breeding population, the demographics aren’t promising: no successful births have been recorded over the last three years.

While the demise of the whales have captured the public’s sympathy, scientists worry that far less attention is given to the plight of salmon, a bellwether species for both the health of the whales and the ecosystem.

The remaining killer whales consume roughly half a million Chinook salmon per year, but years of overfishing, degradation of habitat and warming waters have crushed the once-healthy Chinook populations, along with other species of Pacific salmon. Even the sizes of salmon have decreased. Chinook once frequently exceeded 100 pounds (45kg). Now, they’re often less than half that weight.

The annual return of salmon on the mighty Fraser River, the largest source of salmon in the province and a feast for the whales, has become increasingly bleak. Millions of fish are disappearing, despite predictions they will return. Most of the known stocks of Chinook salmon around British Columbia are considered threatened or endangered, said Greg Taylor, a commercial fishing industry veteran-turned-conservationist.

The federal Department of Fisheries and Oceans (DFO) has attempted to stem the decline of the Chinook, but its own staff complain of funding shortages. An internal memo, provided to the Guardian, detailed how the department couldn’t afford to continue a number of its salmon monitoring programmes. Following public scrutiny of the memo, funding was redirected to the programmes, but critics contend it represents a disregard for the health salmon stocks.

“People make the mistake that DFO’s mandate is conservation of fish. That’s not their mandate. Their mandate is sustainable fishing … Their clients are not the fish, their clients are the industries, the recreational and the commercial fishing industries,” said Taylor.

First Nations communities living along rivers in British Columbia have long relied on the predictable return of salmon for food and ceremonial purposes, and their collapse has hit them particularly hard.

For Gerald Michel of the Xwisten Nation in central British Columbia, the legacy of Canada’s folly in the Atlantic Ocean resonates deeply. Decades of overfishing and short-sighted mismanagement by federal government and the commercial industry resulted in the collapse of the cod fishery, with the fish only recently making a comeback following a strict moratorium.

“In some rivers, we’ve seen the numbers drop from the millions to the thousands,” said Michel. Having worked over the years as a fishery manager, Michel has witnessed the destruction of critical spawning streams through poor logging practices and dam construction – and says he has little faith in the government to be an effective steward.

In Canada, First Nations are constitutionally guaranteed the right to harvest salmon from the rivers, with a certain allocation for food, societal and ceremonial purposes, trumped by conservation measures. But numerous communities along the massive Fraser and Skeena Rivers have volunteered to dramatically scale back, if not halt, their annual harvest.

“Some of the First Nations say, ‘We’re bearing the brunt of first conservation,’ by limiting their fisheries,” said Gord Sterritt of the Upper Fraser Conservation Alliance. “I think we haven’t done enough to limit fisheries and curtail fisheries in the marine waters. The harvest … is huge and this year was no exception.”

Salmon spend much of their lives in cooler waters near Alaska. When fishing ships haul in large catches, they’re often grabbing salmon from rivers along the west coast, said Taylor, with no ability to determine the origin of the fish. The result is often an over-harvest of vulnerable river populations.

As the federal government eyes limiting the catch of Chinook in certain areas to help the killer whales, the closure of recreational fishing along a 70km corridor of the rugged coast of Vancouver Island has sent a chill throughout nearby small towns.

“Closures would crush us. At the gas pumps, restaurants, liquor stores, boat launches,” said Dan Drover, manager of an outfitter in Campbell River, a city dubbed the “Salmon Capital of the World” for its plentiful stock of Pacific salmon. “Our community grew up with fishing rods in our hands.”

The fisheries minister told the Guardian he wouldn’t rule out more closures for the region in the future. Earlier this summer, the US government closed salmon fishing along the mouth of the Columbia River for the first time in recent memory.

Along the thickly forested banks of the Quinsam River on Vancouver Island, the government released four million Chinook into the wild last year from its hatchery. Few return; most will fall victim to seals, fishermen, whales and temperature fluctuations. Those that manage to struggle back become an insurance policy for bad years. While scientists worry about an over-reliance on hatchery fish, which potentially forces competition between wild and hatchery salmon, they remain a key strategy for the government.

Other solutions have been proposed to help recover both salmon and killer whale numbers: the government has begun limiting marine traffic through areas in close proximity to the whales, forcing ships to slow down and quiet their engines. They’ve shut down fishing and have invested in stream rehabilitation.

The battle is winnable, say Taylor and Dr Deborah Giles, a whale researcher at the University of Washington. But progress requires a willingness to change behaviour and a recognition that past harvest quotas and government oversight have failed.

The Pacific Salmon Commission, an multinational oversight body, has called for an immediate reduction to the Chinook harvest to stave off impending collapse. Conservation groups have taken it further, calling for the complete closure of Chinook fishing.

“It is hard to ask people to look at themselves and see how they play into it. People fall in love with these whales, but aren’t necessarily yet willing to make change in their own life to help them,” said Giles. “We’re going to have to continue to ask ourselves what more we can do.”