Protein digestion in snowshoe hares

Institute of Animal Resource Ecolog~ and Department of Zoolog!,, Uni~lersity of British Columbia, 2075 Wesbrook Mall, Vctnc.ou~~er, B . C . , Cantrdtr V6T I W5

Received November 7. 1983

SINCLAIR, A. R. E., and J . N. M. SMl'rH. 1984. Protein digestion in snowshoe hares. Can. J . Zool. 62: 520-52 1 . Pehrson (A. Pehrson. 1984. Faecal nitrogen as an index of hare browse quality. Can. J . Zool. This issue) suggests that

energy, not protein, is the limiting resource for snowshoe hares in winter. We accept this as an alternative point of view. and we await the publication of evidence to support this view. Pehrson's experiments on protein content of food, faecal protein. and weight loss by mountain hares are difficult to interpret because levels of protein and secondary compounds are confounded. The outcome of Pehrson's laboratory tests does not agree with our field data on snowshoe hares.

SINCLAIR, A. R . E. , et J . N. M . SMITH. 1984. Protein digestion in snowshoe hares. Can. J . Zool. 62: 520-52 1 . Pehrson (A. Pehrson. 1984. Faecal nitrogen as an index of hare browse quality. Can. J . Zool. Ce numero.) considere que

c'est l'energie, et non les proteines. qui constitue la ressource limitante des lievres en hiver. 11 s'agit la d'une theorie nouvelle et nous attendons que soient publiees des preuves a l'appui. Les experiences de Pehrson sur le contenu en proteines de la nourriture, les proteines fecales et la perte de masse chez les licvres variables sont difficiles a interpreter, car il y a confusion entre les concentrations de proteines et les concentrations des composes secondaires. Les resultats des tests de Pehrson en laboratoire ne confirment pas les donnees que nous avons recueillies en nature sur les licvres.

[Traduit par le journal]

We welcome Pehrson's ( 1984) report because it raises three important issues. First, Pehrson considers energy, not protein. to be the critical limiting resource for snowshoe hares (Lepus americanus) in winter. Second, he criticizes the validity of the technique that we reported for monitoring protein use by wild hares (Sinclair et al. 1982). Third, he argues that our experi- ments with captive hares produced aberrant results because they did not allow the operation of the normal digestion process in hares. We consider each of these issues below.

Energy We accept Pehrson's suggestion that energy rather than pro-

tein may be the limiting resource. Our technique was develoepd to test Keith's (1974) hypothesis that declines in numbers of snowshoe hares in peak years are caused by food shortages. The limiting resources concerned could be energy, protein, both energy and protein, or other factors. To support Keith's hypothesis, we need only show that one or more limiting nutri- ents are in short supply. We chose protein because it is easier to monitor than energy in wild animals. Furthermore, as pointed out by Pehrson, there is usually a positive correlation between protein content and energy content in plant tissues. To test for undernutrition, we need a measure that unequivocally indicates weight loss as a result of food shortage. Our proposal that faecal protein levels are a good index of undernutrition is supported in other studies of wild herbivores (Bredon et al. 1962; Sinclair 1977; Mould and Robbins 198 I) .

Energy shortages have not yet been measured directly in wild hares. It might be possible to monitor levels of fatty acids or ketones in the blood (O'Kelly 1973; LeResche et al. 1974). but the relevant calibration experiments have yet to be done for hares. Furthermore, handling stress raises levels of fatty acids and ketones in the blood and hence masks the true energy state of the undisturbed hare. The criteria suggested by Pehrson as indicators of energy shortage are either confounded by protein and secondary compounds (urea) or are too indirect to confirm undernutrition (twig diameter, bark: wood ratios).

In short, energy is difficult to monitor, while protein is

relatively simple. Pehrson may be right that energy is the major factor limiting hares in winter, but until some evidence for this is published, we feel that trying to measure protein is a better point to begin.

Protein Pehrson feels that, because he found no relationship in

mountain hares (L. timidus) between weight loss and faecal protein content, the latter cannot be a valid indicator of protein intake. There are three objections to this argument. First, if Pehrson's experimental evidence truly reflects events in the field, there should be no regular seasonal fluctuations in faecal protein in parallel with weight changes in wild snowshoe hares. Figure 8 in Sinclair et al. ( 1 982) shows a regular drop in faecal protein in four consecutive winters. We know from trapping studies (Keith and Windberg 1978; C. J . Krebs, J . N . M. Smith, and A . R. E. Sinclair, in preparation), that hares lose weight in winter. We therefore question the application of Pehrson's results to the snowshoe hare in the field.

Second, Pehrson's experiments do not control for the pres- ence of secondary chemicals in the food offered to his mountain hares, although these compounds are known to interfere with hare digestion (Sinclair et al. 1982, Table I). Because the effects of protein and secondary compounds are confounded in Pehrson's study, his results fail to separate the effects of these two factors.

Third, Pehrson interprets his Fig. I to show that there is no relationship between protein ingested and weight change and that mountain hares can maintain weight on a diet of 6% pro- tein. This level is below the minimum maintenance level that we estimated for the smaller snowshoe hare. In addition to the complication of secondary chemicals, Pehrson did not measure the actual protein content of the twigs eaten or rejected by his mountain hares, only the average amount offered in a 1000-g ration. Sinclair et al. ( 1982) point out that it is invalid to measure dietary protein from clippings made by humans because hares may not select by the same criteria. The exam- ples in Pehrson's Table 1 do not, therefore, represent the pro-

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tein intake of hares from each plant species, unless hares feed unselectively, which we know to be false (e.g., Sinclair and Smith 1984).

Digestibility Pehrson makes a third objection to our experiment; he sug-

gests that the pelleted food that we used (Sinclair et al. 1982) contained such small particles that it interfered with the hares' digestive mechanism for sorting food particles by size. If this hypothesis is correct, our hares should have been less efficient at digesting pellets containing 13% crude protein than at di- gesting pellets containing 9 or 20% protein, because only the 13% pellets contained powdered particles of even size. Our Fig. 7 (Sinclair et al. 1982) shows that the points for the 1370 pellets lie on the straight line relating dietary protein to faecal protein. and not off the line, as would be predicted by Pehrson's hypothesis.

Although we find fault with Pehrson's experiments, we do feel that our results could be improved upon. We calculated (Sinclair et al. 1982) that wild adult snowshoe hares in winter need 7 g crude protein/day, which they obtain from an esti- mated 150 g dry matter, with a 9.9% (not 11.396, as stated by Pehrson) mean protein content: this is the threshold value for body weight maintenance. This 150 g may be underestimated; if it were 200 g, for example, the mean protein level required for body maintenance would be only 8.75%. We need better information on the amounts of natural foods eaten by hares and their digestibilities. Detailed data on weight change and faecal protein output of individual hares in winter could help to dis- tinguish these alternate viewpoints.

Our initial experiments deliberately controlled for secondary compounds. In the field, these compounds inhibit protein digestion and thus must raise the minimum threshold intake required to maintain body weight. While the role of secondary chemicals in food selection by hares is less clear than claimed by Pehrson (Sinclair and Smith 1984). we clearly need to know more about this, and further experiments are in progress.

These gaps in our knowledge do not alter our earlier conclusion (Sinclair et al. 1982) that hares producing faeces with less than 7.5% protein are suffering from a protein shortage and perhaps also an energy shortage. The presence of secondary chemical compounds merely results in our being conservative when we conclude that hares are short of food.

In conclusion, Pehrson's energy hypothesis is a useful one but it remains to be substantiated. We disagree, however, that his experiments invalidate our approach. Experiments that fail to control for the presence of secondary compounds and that do not measure actual protein intake. as opposed to average protein content in a ration. cannot be used to reject either field observations or experiments that do control for these factors.

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KEITH. L. B. 1974. Some features of population dynamics in mam- mals. Proc. Int. Congr. Game Biol. 11: 17-58.

KEITH, L. B.. and L. A. WINDBERG. 1978. A demographic analysis of the snowshoe hare cycle. Wildl. Monogr. No. 58.

LERESCHE, R. E., U . S . SEAL. P. D. KARNS. and A. W. FRANZMANN. 1974. A review of blood chemistry of moose and other cervidae, with emphasis on nutritional assessment. Nat. Can. 101: 263-290.

MOULD, E. D., and C . T. ROBBINS. 1981 . Nitrogen metabolism in elk. J . Wildl. Manage. 45: 323-334.

O'KELLY, J . C . 1973. Seasonal variations in the plasma lipids of genetically diffcrcnt types of cattle: steers on different diets. Comp. Biochem. Physiol. 44: 303 -3 12.

PEHRSON. A. 1984. Faecal nitrogen as an index o f hare browse qual- ity. Can. J . Zool. 62. This issue.

SINCLAIR. A. R. E. 1977. The African buffalo. University of Chicago Prcss. Chicago.

SIN( 'LAIK, A . R. E.. C . J . KREBS. and J . N. M . SMITH. 1982. Diet quality and food limitation in herbivores: the case of the snowshoe hare. Can. J . Zool. 60: 889-897.

S INCLAIR. A. R. E.. and J . N. M. SMITH. 1984. Do plant secondary compounds determine feeding preferences of snowshoe hares? Oecologia (Berlin). In press.

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