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A female Xenopsylla ramesis. Photo credit: Michael W. Hastriter.

Most fleas have it made. Riding around on their hapless hosts, the parasites are safe and warm with an almost limitless supply of food on tap. But not all parasites are quite so lucky. Cynthia Downs from Hamilton College, USA, explains that the surroundings may be less wholesome for fleas that hitch a ride on species that live in burrows where the carbon dioxide levels can rocket. ‘I was interested in how environmental conditions affect host–parasite interactions’, explains Downs, remembering how her interest in the effects of carbon dioxide was triggered while working in Berry Pinshow's lab in Ben-Gurion University of the Negev, Israel. ‘They were investigating how burrow geometry affects concentrations of CO₂ in burrows and the physiology of rodents’, says Downs. Learning that high concentrations of CO₂ in air can affect the immune response of mammals, Downs wondered how parasitic hitchhikers may be affected by the stale subterranean air produced by their hosts.

‘I wanted to determine how concentrations of CO₂ that mimic those found in some burrows where fleas reside affected how fleas interacted with their hosts,’ says Downs. Working with Irina Khokhlova, Downs carefully mixed CO₂ with air to reproduce the atmospheric conditions that have been measured in the tunnels of some burrowing species and then pumped the modified air into the airtight plastic cages of burrowing Sundevall's jirds to simulate the atmosphere below ground. ‘Overall, the jirds are fairly docile and very easy to work with’, recalls Downs, but she admits that she had to overcome her natural squeamishness about plunging her hand into a box of Xenopsylla ramesis fleas before transferring them to the rodents – even though the fleas do not bite humans.

Explaining that the fleas spend only a fraction of their lives riding on their hosts – only hopping onto a passing rodent for 3- to 6-day periods when they need to feed and reproduce – Downs and Khojhlova replaced the rodents’ population of 150 fleas every 3–6 days, counting the survivors to calculate the survival rate. And when they compared the fleas’ death rate with that of fleas from jirds in a normal atmosphere, they found that it rocketed, with 27% more fleas dying in the stale air. The simulated-burrow fleas also produced 0.3 eggs per female less than the fleas that were basking in fresh air. And when the duo tested how well the fleas coped after abandoning the host and hunkering down in the improvised burrow's sand for several days, they found a similar increase in the death rate. The high-CO₂ fleas were also less keen on escaping. ‘Fleas don't tolerate living in a high fractional concentration of CO₂ used in this experiment very well,’ says Downs. ‘I expected to see a small decrease in survival…but I didn't expect to see a decrease in reproductive success’, she adds.

So instead of being prepared for their subterranean existence, Xenopsylla ramesis fleas are significantly compromised by their high-CO₂ lifestyle. Downs suggests that the burrow fleas may hold their breathing tubes (spiracles) open for longer than fleas in a normal atmosphere, causing them to dry out faster and die. She also says, ‘They probably experience many CO₂ conditions in their natural environment’, explaining that the fleas are happy to infest many other rodent species, which has probably prevented them from adapting to the burrow's stale atmosphere, while possibly providing a little relief for the burrowing rodents from scratching at their uninvited guests.

• © 2015. Published by The Company of Biologists Ltd