The effects of aestivation and re-feeding on the structure and function of the gut in the green-striped burrowing frog, Cyclorana alboguttata

Cramp, Rebecca L. (2005). The effects of aestivation and re-feeding on the structure and function of the gut in the green-striped burrowing frog, Cyclorana alboguttata PhD Thesis, School of Integrative Biology, The University of Queensland.

       
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Author Cramp, Rebecca L.
Thesis Title The effects of aestivation and re-feeding on the structure and function of the gut in the green-striped burrowing frog, Cyclorana alboguttata
Formatted title
The effects of aestivation and re-feeding on the structure and function of the gut in the green-striped burrowing frog, Cyclorana alboguttata
School, Centre or Institute School of Integrative Biology
Institution The University of Queensland
Publication date 2005-01-01
Thesis type PhD Thesis
Supervisor Craig E. Franklin
Total pages 200
Total colour pages 2
Total black and white pages 198
Language eng
Subjects 060604 Comparative Physiology
0608 Zoology
060203 Ecological Physiology
Formatted abstract
Burrowing frogs can spend up to several years ensconced in underground burrows during which time they do not feed; they only return to the surface for short periods following heavy rain where they must reproduce and feed to replenish endogenous energy reserves before returning underground. Burrowing frogs provide an ideal model to examine the impact of prolonged food deprivation on the gut and the impacts these changes might have on the re-feeding ability of these animals. In the present study, I examined the response of the gut of the burrowing frog, Cyclorana alboguttata to natural periods of food deprivation occurring with 3 and 9 months of aestivation and assess the impact of such changes on the subsequent ability of the animal to re-feed following aestivation.

Prolonged fasting during aestivation had a marked impact on the morphology of the gastrointestinal tract of C. alboguttata. Following 3 months of aestivation, the stomach, small intestine and large intestine were reduced by 25, 70 and 55 %, respectively. Nine months of aestivation resulted in a further 20 % and 6 % reduction in stomach and small intestinal masses. Intestinal longitudinal folds were reduced by 80 % in height, while enterocyte crosssectional areas were also markedly reduced following 3 months of aestivation. There were numerous cellular and sub-cellular changes to the absorptive epithelium following 3 and 9 months of aestivation. Despite the large number of morphological changes in the absorptive epithelium, there were few changes in the pattern of innervation by nerves in the gastrointestinal tract following 3 and 9 months of aestivation. Enterocyte turnover kinetics were examined in control and aestivating C. alboguttata using the incorporation of a tritiated thymidine marker nucleotide. Total enterocyte turnover time was estimated to have increased by approximately 1-fold in 3-month aestivating animals when compared with fed control animals. Moreover, there were fewer enterocytes undergoing mitosis in 3-month aestivating animals.

Prolonged fasting during aestivation had a clear influence on several functional properties of the small intestine. The mass specific metabolic rate of the isolated small intestine was elevated in 3-month burrowing frogs when compared to inter digestive control animals and equivalent to that of fed control animals. When changes in the overall mass of the small intestine with aestivation were accounted for, the overall metabolic cost of the small intestine to the aestivating animal was approximately equivalent to that of interdigestive control animals, but significantly less than that of fed control animals. The metabolic rate of aestivating C. alboguttata was observed to decline by almost 70 % in 3-month aestivating animals, thereby resulting in an increased contribution of the small intestine to the overall metabolic rate of the animal (20 % c.f. 5 – 8 % in control animals). The nutrient uptake capacity of the small intestine was examined by measuring the uptake kinetics of the amino acid proline in control and aestivating animals. Proline transporter activity was markedly elevated (40%) in aestivating tissues when compared with both fed and interdigestive control animals, although total proline uptake capacity (total uptake over the entire intestine) was equivalent to interdigestive control animals but less than fed control animals. The proportion of proline transport occurring via Na+-independent pathways (diffusion, non-Na+- dependant carriers) was much greater in 3-month aestivating animals (~95%) when compared to both fed and interdigestive control animals (~60%).

Given the extent of morphological and functional changes occurring to the gut during aestivation, I examined the influence of 3-months aestivation on the rate of food passage through the gut and assimilation efficiency of C. alboguttata. Passage rates were significantly longer in animals that had recently experienced 3-months of aestivation, but there were no differences in the abilities of animals to digest and assimilate energy, carbon and nitrogen from their meals. Hence, it was expected that the morphological and functional changes to the small intestine which occurred during aestivation were rectified either by arousal from aestivation or with the consumption of the first meal. When the same morphological parameters described for aestivation were examined in animals aroused from 3-months of aestivation and at two stages during the digestion of the first meal, it was evident that botharousal from aestivation and the consumption of the first meal had a significant impact on gut morphology, with almost all morphological parameters returning to within control values within 36 h of the consumption of the first meal. Intestinal metabolic rates and nutrient transport capacity peaked initially with arousal from aestivation and within the first 36 h of digestion, but returned to within active levels by the end of the digestion of the first meal. I also examined the total metabolic costs associated with re-feeding (i.e. specific dynamic action, SDA) following aestivation. It was found that while metabolic rates reached maximum (over 400 % increase in metabolic rate) 36 h following the ingestion of the first meal, the overall energy expended to completely restore gut morphology and function did not differ greatly from that observed in animals the do not down-regulate their guts between meals as documented by Secor (2001).

It is concluded then that while the energetic costs associated with the maintenance of a functional gut during aestivation are high, these costs are outweighed by the ability of the animal to capitalise on the first meal following aestivation. Morphological changes to the gut are transitory, and probably reflect changes in enterocyte size and age. The ability of the small intestine to retain its capacity to transport amino acids may reflect an acceptable energetic cost carried by burrowing frogs which allows them to reclaim nutrients lost to the gut during aestivation and rapidly begin assimilating nutrients at the completion of aestivation. The reduced energetic costs associated with the consumption of the first meal following aestivation suggests that the small intestine does not require extensive up-regulation and what up-regulation in required is not energetically expensive. Burrowing frogs therefore represent an organism that is appears to be well suited to prolonged periods of food deprivation.
Keyword Aestivation
Starvation
Small Intestine
Frog
Digestive physiology

 
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Created: Fri, 24 Aug 2012, 21:39:34 EST by Dr Rebecca Cramp on behalf of School of Biological Sciences