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First published online November 17, 2005
Journal of Experimental Biology 208, 4467-4477 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01892

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Comparative overwintering physiology of Alaska and Indiana populations of the beetle Cucujus clavipes (Fabricius): roles of antifreeze proteins, polyols, dehydration and diapause

Valerie A. Bennett^1,*, Todd Sformo², Kent Walters¹, Oivind Toien², Kennan Jeannet², Ronald Hochstrasser^1,3, Qingfeng Pan⁴, Anthony S. Serianni⁴, Brian M. Barnes² and John G. Duman^1,

¹ Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA
² Institute of Arctic Biology, University of Alaska, Fairbanks, AK 49775, USA
³ Sycamore Community High School, 7400 Cornell Road, Cincinnati, OH 45242, USA
⁴ Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN, 46556, USA

View larger version (29K): [in a new window]   Fig. 1. Representative microhabitat (red) and air (black) temperatures experienced by C. clavipes in Alaska and Indiana over the three years of the study. Examples were chosen to illustrate the extremes of insulated and uninsulated microhabitats. Note how microhabitat temperatures in poorly insulated sites (in logs above snow levels) closely track air temperatures, while those in well-insulated sites (in logs below snow level) generally remain warmer than air temperatures after snow arrives in winter. (A) Temperatures in a poorly insulated log (off the ground) near Fairbanks, Alaska. (B) Temperatures at a well-insulated site near Wiseman, Alaska. (C) Temperatures in a poorly insulated log near South Bend, Indiana.

View larger version (14K): [in a new window]   Fig. 2. Temperatures experienced by C. clavipes larvae in two box enclosures near Fairbanks, one near the ground and therefore well insulated by snow (red line) and the other above snow level (black line).

View larger version (18K): [in a new window]   Fig. 3. Supercooling points (SCPs) of Alaska C. clavipes larvae from summer 2002 to spring 2004. Most are from the vicinity of Fairbanks, except those collection times identified by an asterisk, which are from near Wiseman. Black diamonds represent individual SCPs; however, there are numerous overlapping values. Green squares identify mean SCPs for a given date. Red squares identify larvae that were cooled to –60°C or –80°C without expression of a freezing exotherm. Numbers below the red squares indicate the number of individuals that did not freeze in that particular run. The red circles show the mean SCP when those individuals that did not freeze at –80°C were included in the mean calculation, using –80°C as the SCP of these individuals (9 January and 10 March 2004).

View larger version (19K): [in a new window]   Fig. 4. Comparisons of supercooling points (SCPs) of Alaska C. clavipes larvae cooled in contact with ice (red) with those of larvae not in contact with ice (black). Green squares indicate means. Red or black squares indicate larvae that did not freeze at –80°C or –60°C. Green circles indicate means calculated with the inclusion of individuals that did not freeze at –80°C (using –80°C as their SCP).

View larger version (12K): [in a new window]   Fig. 5. Representative supercooling points (SCPs) of C. clavipes larvae from the vicinity of South Bend, Indiana collected between Autumn 2001 and Summer 2004. Black diamonds indicate individual SCPs; however, there are numerous overlapping values. Green squares identify mean SCPs for a given date.

View larger version (22K): [in a new window]   Fig. 6. Water content of C. clavipes larvae collected near Fairbanks between 29 September 2002 and 9 March 2004. Horizontal axis identifies collection dates. Vertical axes show percent body water (blue line) and absolute body water (red line).

View larger version (25K): [in a new window]   Fig. 7. Correlation between supercooling points and absolute body water of C. clavipes larvae. There was a moderate, but highly significant, association between absolute body water and SCP (r=0.6079, P<0.001, N=384), based on the Spearman rank correlation.

View larger version (17K): [in a new window]   Fig. 8. The 13C{1H} NMR spectrum (150 MHz) of cold-acclimated C. clavipes hemolymph. (A) Expansion of the 22–98 p.p.m. region of the spectrum. Assignments of the major signals are as follows: a, ,-trehalose; b, glycerol; c, proline; d, betaine. The signal at 55.5 p.p.m. is a triplet and that at 68 p.p.m. is a complex multiplet; assignment of these signals to betaine is tentative [other species bearing a –N(CH3)3+ group may be responsible for these signals]. The signal marked with `x' was unassigned. (B) Expanded carboxyl region of the spectrum showing assignment c of the carboxyl carbon of proline; x was unassigned. (C) Expanded aromatic region of the spectrum, showing two broad multiplets due to presently unknown species. Signals in B and C were very weak compared with those observed in A (note the reduced S/N in B and C relative to A).

View larger version (31K): [in a new window]   Fig. 9. Seasonal changes in metabolic rate (CO2 production in µl h–1 g–1 dry mass) of C. clavipes larvae (N=6–11) from near South Bend, Indiana and Fairbanks, Alaska. Indiana larvae (IN) were collected on 8 November 2002 (autumn), 1 February 2003 and 3 June 2003. Alaska (AK) larvae were collected between 20 September and 3 October 2002 and either cold acclimated to –4.5°C for one month (AK autumn 2002; see text for details) or held in a box enclosure at ground level under Fairbanks field conditions until 16 January 2003 (AK January 2003 ground box). Alaska larvae were also collected on 19–22 March 2003 and 28–30 June 2003 and run immediately. Metabolic rates were determined at 20, 10 and 0°C. Body water content (% body water) is also shown for these larvae. Values are means ± S.E.M. See text for statements on statistical significance.