Elevated extracellular magnesium in overwintering sandhoppers Talitrus saltator: Disentangling the effects of torpor and temperature

Abstract

Sandhoppers (amphipods) have long been thought to overwinter in the supratidal zone at high temperate latitudes, buried in a torpid or dormant state described as ‘hibernation’. Early correlative studies suggested an association between invertebrate activity and extracellular Mg²⁺, a well known narcotizing agent. More recently large temperature-related increases in extracellular Mg²⁺ were recorded in a Scottish population of the sandhopper Talitrus saltator associated with overwintering. Our study tests the idea that at low environmental temperatures large T. saltator enter a deep torpor, distinct from temperature-related reduced activity, and associated with an increase in extracellular Mg²⁺ related to, but different from, any effect of low temperature on Mg^2+.. Haemolymph from buried individuals was sampled in situ Sept 2017 - Feb 2018. Extracellular ions, including Mg²⁺ were quantified and correlated most strongly with burrow temperature. While there was a statistically significant and predictable increase in [Mg²⁺]_h with temperature reduction (0.19 mmol.L⁻¹.°C) the [Mg²⁺]_h of torpid individuals (3.91 mmol.L⁻¹) was greater than resting individuals ((6.39 mmol.L⁻¹) at equivalent low temperatures (< 4.2 °C). There was no difference in the concentrations of Na⁺, Ca²⁺ or Cu²⁺ as a result of temperature change or torpor. This was confirmed in laboratory experiments where there was a difference in [Mg²⁺]_h between torpid and resting individuals at the same comparatively high temperature (Δ 0.87 mmol.L⁻¹, T = 10 °C). There was a larger difference as a result of temperature reduction from 10 to 2 °C (Δ + 4.78 mmol.L⁻¹). This associates Mg²⁺ with torpor in T. saltator, as does experimentally blocking the antennal gland, which results in an elevated extracellular Mg²⁺ (but not Na⁺) and a cessation of activity even at high temperatures (15 °C). It is clear from the present study that elevated [Mg²⁺]_h in overwintering sandhoppers is associated with torpor and, to a lesser extent, exposure to low temperature, and these responses are different from individuals from a Scottish Talitrus saltator population examined previously.