Nothing in nature is constant, from the grand seasonal cycles that sweep the higher latitudes to the daily solar rhythm of tides that leaves exposed coastal residents roasting in the sun before they are plunged again beneath the waves. ‘Aerial exposure and the unpredictable nature of the thermal stress during low tides may be critical factors in defining the thermal physiology of intertidal organisms’, says Anne Todgham, from the University of California, Davis, USA. However, Todgham points out that few lab-based studies take into account the random thermal fluctuations that shore dwellers experience in their natural environment: lab-based animals are generally exposed to a single heat wave after a period of stable preparation in the lab. Wondering how shoreline residents cope with the natural variation in their thermal regime, Todgham and her colleagues recreated the unpredictable climate that fingered limpets (Lottia digitalis) clinging to the Northern California shore experienced during the summer months between April 2011 and March 2013 to find out how daily temperature fluctuations affect their thermal tolerance.

Working with Madeline Drake and Nathan Miller, Todgham recreated the low-tide conditions at Fort Ross with a heating block while washing fresh seawater over the gastropods to simulate high tide twice a day for a fortnight. In addition, the team exposed limpets to: a reliable tidal cycle (where they were always warmed to 24°C); a second scenario where they were warmed repeatedly to 32°C (the highest temperature recorded at the Fort Ross site); a third scenario where the tide washed back and forth, but the limpets experienced no warming during low tide; and a final scenario where the limpets were continually submerged at 13°C. After completing the 14 d tidal simulations, Drake and Miller measured the heart rates of a selection of the limpets as they were warmed gently (6°C h−1) until the temperature threatened their survival and their heart rates dropped suddenly. The team also collected portions of the limpets' bodies and analysed them for evidence of stress.

Impressively, the limpets that had experienced the Northern California simulated tide were best prepared as the temperature began to rise, with their hearts holding out until the temperature reached ∼40.5°C. Meanwhile, the limpets that experienced reliable tidal cycles (where the low tide temperature never varied) held out to ∼38°C. In contrast, the hearts of the limpets that had been immersed for the entire fortnight began to fail at ∼36°C. Todgham says, ‘Repeated aerial exposure alone (the most predictable aspect of the tidal cycle), regardless of the magnitude of temperature increase, had the largest effect on maintaining a high upper temperature tolerance in limpets’, adding, ‘the heating during low tide is less important’.

However, when Drake analysed how the limpets managed their energy budget and resistance to stress, she and Todgham were surprised to find that the limpets that had experienced the most variation in their conditions were no better prepared than the limpets that had been submerged for the entire period.

So it seems that repeated exposure to the air at low tide is critical for the limpets’ high temperature preparations, and Todgham says, ‘If aerial exposure is the predominant factor driving thermal tolerance of intertidal limpets, and perhaps intertidal organisms more broadly, this suggests that organisms inhabiting the low intertidal are likely sensitive to warming not only as a result of a thermal history of lower temperatures but also as a result of not being predictably exposed to air during low-tide periods’.

M. K.
N. A.
A. E.
The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis
J. Exp. Biol.