Plasma ghrelin concentrations change with physiological state in a sciurid hibernator (Spermophilus lateralis)

Abstract

Ghrelin is a recently discovered hormone which has profound effects on food intake and lipogenesis in mammals. In all mammals studied thus far, plasma ghrelin concentrations are increased before a meal and decrease immediately following a meal; ghrelin levels increase with fasting. The golden-mantled ground squirrel Spermophilus lateralis (also known as Callospermophilus lateralis (see Helgen et al., 2009) is a diurnal hibernator which has a robust annual cycle of body mass gain and loss that is primarily controlled by food intake. We hypothesized that in spring, summer, and autumn, the endogenous ghrelin concentrations of hibernators would be similar to those of non-hibernators, but that during the winter hibernation season, plasma ghrelin concentrations would be low or undetectable. We found that peripherally injected ghrelin significantly increased food intake in June. Plasma ghrelin concentrations were significantly increased through 5 days of fasting during a short-term fast in summer. Over a 24h period, ghrelin concentrations increased at night and decreased during the day with drops corresponding to times when squirrels were eating. In January, ghrelin concentrations are low but measurable even while animals are at low body temperature (Tb). This is the first report of ghrelin concentrations in a non-photoperiodic hibernator. We suggest that ghrelin may be important for the regulation of food intake and the body mass cycle in mammals that hibernate.

Figure 1

Validation of total ghrelin EIA assay: dilution curve for GMGS (sample diluted at 5:0, 3:2, 2:3, and 1:4 with assay buffer)

Figure 2

Mean cumulative food intake (in grams) for the six hours after peripheral saline and ghrelin injections in June (control N=4, ghrelin N=4)

Figure 3

Figure 3A. Mean change in body mass with fasting ± SEM during short term fast in July (control N=4, 1-day N=5, 3-day N=5, 5-day N=4). Different letters are statistically different (p<0.05); 3B: Mean ghrelin concentrations ± SEM in short-term fast in July. Letters a & b are statistically different (p<0.05)

Figure 4

Figure 4A. Each point represents mean food intake ± SEM per day from September to January 2008–2009 (N=5), including times of 24-hour ghrelin secretion experiment and January ghrelin experiment; *=animals catheterized for 24 hour ghrelin experiment; ↓=animals sacrificed for January ghrelin experiment; 4B: 24-hour plasma ghrelin secretory pattern and times observed feeding/hour in GMGS—shaded area denotes dark hours (lights out); each point on ghrelin line represents the mean ± SEM for each time period; each point on feeding line represents the total number of times animals were observed feeding for each time period (N=5)

Figure 5

Mean ghrelin concentrations ± SEM in animals at low tissue temperature in January (LTT) (N=5) and in animals euthermic in January (N=4). Letters a & b are statistically different (p<0.05).