The influence of nutrition and seasonal conditions on mineral status in the reindeer

Department of Biology, University of Joensuu, 80100 Joensuu 10, Finland

AND

Deportment ofZoology, University of Oulu, 90100 Oulu 10, Finland

Received July 15, 1976

HYVARINEN, H., T. HELLE, M. NIEMINEN, P. VAYRYNEN, and R. VAYRYNEN. 1977. The influence of nutrition and seasonal conditions on mineral status in the reindeer. Can. J. Zool. 55: 648-655.

Body weight, serum sodium, potassium, calcium, magnesium, copper, and zinc concentra- tions, and alkaline phosphatase (EC 3.1.3.1) activity were measured in freely grazing reindeer in Kuusamo, Finland (66"301N), at four different seasons in the year. The same parameters were also measured in late winter in a group of artificially fed reindeer in Kuusamo and a group in Enontekio, Finland (68"301N), which were grazing freely in very poor conditions. Some weeks after sampling about 40% of the reindeer in this latter area died of malnutrition. Bone densities were measured in some of these animals.

The reindeer in Enontekio had suffered from severe mineral deficiency. Serum calcium, magnesium, and copper concentrations were very low. It is assumed that the final death of the animals may have been caused by a disturbance in mineral metabolism. Serum calcium concent- ration was also low in the freely grazing group with near normal winter food conditions in Kuusamo. It is suggested that the reindeer compensate for the poor mineral content of the winter food by using the skeleton as a mineral bank even in normal winter. A seasonal cycle was found in serum copper concentration in the hinds, values being high in late pregnancy and after parturi- tion. Serum potassium and zinc concentrations were lowest in autumn and winter.

H Y V ~ N E N , H., T. HELLE, M. NIEMINEN, P. VAYRYNEN et R. VAYRYNEN. 1977. The influence of nutrition and seasonal conditions on mineral status in the reindeer. Can. J. Zool. 55: 648-655.

On a mesure le poids, les concentrations de sodium, de potassium, de calcium, de magnesium, de cuivre et de zinc skriques, ainsi que I'activite de laphosphatase alcaline (EC 3.1.3.1) chez des rennes broutant en liberte a Kuusamo, Finlande (66'30' N), a quatre moments de I'annee. On a de plus mesure les m&mes parametres a la fin de l'hiver, chez un groupe de rennes nounis artificiel- lement a Kuusamo et chez un groupe de rennes broutant librement dans des conditions tres mauvaises B Enontekio, Finlande (68"30' N). Quelques semaines apres I'echantillonnage, environ 40% des rennes de ce demier groupe sont morts de malnutrition. On a mesure la densite osseuse chez certains de ces animaux.

Les rennes d'Enontekio ont subi une carence minerale grave. Les concentlations de calcium, de magntsium et de cuivre seriques Ctaient tres faibles. On croit que la mort de ces animaux peut avoir CtC causee par un derangement du metabolisme des minCraux. Le calcium serique etait egalement en concentration faible chez le groupe libre de Kuusamo en hiver, dans des conditions alimentaires pres de la normale. On croit que le renne compense le contenu mineral faible de la nouniture d'hiver en se servant de son squelette comme source d'elements mineraux, meme lors d'un hiver normal. Chez les biches, les concentrations de cuivre serique suivent un cycle saisonnier, les valeurs etant elevees a la fin de la grossesse et apres la parturition. Les concentra- tions de potassium et de zinc seriques atteignent leurs valeurs minimales al'automne et kl'hiver.

[Traduit par le journal]

Introduction adapted to this during the process of evolution. The seasons exercise a far-reaching effect on Such is the case with the reindeer in Finland,

the availability and composition of the food of which live in almost the same manner as their animals living in the wild in boreal, subarctic, wild ancestors, roaming freely in the forests or and arctic areas. Very considerable seasonal subarctic and arctic mountain areas beyond lati- variation in environment is experienced in such tude 65". During late winter and early spring con- areas, and the animals have necessarily become ditions are very harsh in many cases as a result

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HYVARINEN ET AL.

TABLE 1. Animals used in the study and conditions at sampling

Hinds or Group calves Sampling time* Living conditions before sampling (at least 2 months)

Hinds

Hinds

In captivity out of doors. Fed on dry hay (ad libitum), dry leaves of Betula and lichens (Cladonia). Most hinds pregnant

Grazing freely in the forests at timbercutting sites. Good supply of Alectoria lichens from felled trees. Digging conditions for Cladonia lichens difficult. Most hinds pregnant

Hinds

Hinds

Calves aged about 1 month

Hinds

Calves aged about 4 months

Hinds

Calves aged about 8 months

Grazing freely. No Alectoria lichens on trees. Hard crust on the snow, and digging conditions for Cladonia lichens very difficult. Soon after sampling a large number of reindeer in this area died of malnutrition. Most hinds were pregnant in early winter

Freely grazing lactating hinds in the forests. Good supply of Betula and Salix leaves, and of green grasses for about 1 month before sampling. Earlier living conditions as group 1

Calves of the hinds in group 4A. Main food, milk from the hind

Grazing freely in the forests. Good supply of green grasses and mushrooms

Calves of the hinds in group 5A. Main food the same as for the hinds, but most were also still taking milk

Grazing freely in the forests at timber-cutting sites. Good supply of Alectoria lichens from felled trees. Snow con- ditions also favorable for digging for Cladonia lichens or Deschampsia flexuosa grass

Calves of the hinds in group 6A. Food the same as that of the hinds

*Day. month, year.

of the thick, hard snow and (or) ice cover on the ground (cf. Steen 1966; Hyvarinen et al. 1975). The main winter food, lichens (Cladonia spp. and Alectoria spp.), are poor in proteins and minerals as compared with the summer food, grasses, hay, leaves of trees, and mushrooms (see Ahti 1961; Scotter 1965, 1967; Kelsall 1968; Steen 1966; Isotalo 1971). Although some work has been published in recent years concerning the nutritional status or body water content of reindeer and caribou during the winter (Afanasev 1963 ; Luick et al. 1973; Cameron and Luick 1972; Hyvarinen et al. 1975) very little is known about the mineral status of reindeer under winter conditions, although some data are available on blood mineral concentrations (Manery et al. 1966; McEwan 1968; Dietrich and Luick 1971).

The aim of this study is to give information on the mineral status and mineral metabolism of freely grazing reindeer at different seasons and under extreme dietary conditions. The concen- trations of serum main cations (sodium, potas- sium, calcium, and magnesium) and of some trace elements (copper and zinc), serum alkaline phosphatase (EC 3.1.3.1) activity, and bone specific gravity are used as parameters in this study.

Material and Methods The animals used in the study (Table 1) are mainly the

same as described in our earlier work (Hyv2rinen et al. 1975). Only group 6 (Table 1) is new. Groups 1, 2, 4, 5, and 6 were living in Kuusamo (66"30f N) and group 3 in Enontekio (68"30' N). The animals in groups 2, 6A, and 6B were captured in winter by foot noose and those in

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CAN. J. ZOOL. VOL. 55, 1977

I 1 1 l l l l l 1 l l I l

Ill V VII IX XI I morith 11 12 3 2 2L 18 n adults

33 15 5 n calves FIG. 1. Changes in body weight of adult female reindeer and calves living wild in the forests of

Kuusamo. C, calving time. G-3, group 3 (see Table 1).

group 3 by lasso. The summer and autumn samples (groups 4 and 5) were taken at reindeer roundups. Since the duration of corralling at these roundups was found to have a clear effect on serum cslcium and sodium levels (Hyvarinen et a/ . 1976), only the results from animals corralled for less than 6 h are included here. The blood samples were taken within 5 min of capture, after which the animals were weighed. No immobilizing drug was used in handling the animals. The blood samples were taken into a centrifuge tube from the jugular vein. The samples were then cooled to 0°C and serum from coagu- lated blood was separated by centrifugation within 4 h of sampling. Samples were frozen and serum calcium, sodium, potassium, magnesium, copper, and zinc contents were measured later with an atomic absorption spectro- photometer (Perkin Elmer 290B) using the routine procedures (Perkin-Elmer Corporation 1972). Serum alkaline phosphatase activity was measured by the method of Bodansky and Schwarz (1961).

Tibia bones were taken about 2 weeks after death from four hinds which had died of malnutrition in Enontekio in the spring of 1973 and from four hinds in Kuusamo slaughtered at the autumn roundup in 1974. Dry weight of the bones was determined by drying for about 48 h at 105°C. The volume of the bones was measured by immersing them in water in a volumetric syringe. The dry weight versus volume of the tibia gave its specific gravity (grams per cubic centimetre). The t-test was used to test the significance of differences between group mean values.

Results Changes in Body Weight

The body weight of the hinds living wild in the forests of Kuusamo decreased by about 5 kg between March and the end of June, during which period parturition had taken place (Fig. 1).

The most common calving time is the end of May, but the first calves are born at the beginning of May and the last in mid-June. The weight of a newborn calf is about 5 kg (cf. Varo 1973), so that the loss in body weight between the March and June-July measurements is approximately equivalent to the weight of a calf.

The weight of the hinds living outdoors in captivity in Kuusamo was only slightly higher than that of the freely grazing hinds in March.

The weight of the hinds in the Enontekio area, where very little food was available, was highly significantly lower than the figures for the two Kuusamo groups (Table 2). Between summer and autumn the weight of the freely grazing hinds in Kuusamo increased by about 10 kg and that of the calves by about 20 kg. The weight continued to increase on the autumn and early winter and that of the hinds was about 25% higher at the beginning of February 1974 than it had been early summer 1973.

Serum Alkaline Phosphatase Activity and the SpeciJic Gravity of the Tibia

Serum alkaline phosphatase activity was high- est in the young growing calves in groups 4B and 5B, and was similarly at its highest in the hinds during the summer (Fig. 2, Table 2). The lowest figures were reached in the midwinter group (6A) 1974 and in the group of the hinds feeding in captivity in March 1973 (group 1 ; serum alk-

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HYVARINEN ET AL.

FIG. 2. Seasonal changes in serum alkaline phosphatase activity of adult female reindeer (A) and their calves (C) living wild in the forests of Kuusarno. At the beginning of the curves the calves are about 1 month old (group 4B). At the end of the curves the calves are about 8 months old (group 6B). The curve of the adults consists of the groups 2,4A, 5A, and 6A. G-1, group 1 , G-3, group 3 (malnutri- tion group, Enontekio). For further information see Table 1 .

aline phosphatase (SAP) activity 9,39 + 0,92 Bodansky units). Activity was significantly higher in the group living wild in the forests of Kuusamo (group 2; SAP activity 14,41 Bodansky units) and in the group living under poor feeding con- ditions in Enontekio (group 3; SAP activity 12,88 + 1,44 Bodansky units) than in the feeding group in March 1973.

The specific gravity of the whole tibia bones of the hinds which had died in Enontekio in spring 1973 (1.01 + 0.086 g/cm3, n = 4) was very low (p < 0.01) compared with those measured in Kuusamo in autumn 1974 (1.47 + 0.089, n = 4).

Changes in Serum Mineral Content No significant changes were noted in serum

sodium content in the material studied. Serum potassium content was higher in the group that were fed (group 1) in Kuusamo in late winter 1973 than in the freely grazing group (2), and much lower in the hinds (group 3) living under difficult conditions in Enontekio. Serum potas- sium content was at about the same level in both summer and winter in the hinds in Kuusamo, though it was considerably lower in autumn, when it also fell below the corresponding value for the calves (Table 2).

Serum calcium content was very low in the hinds living under very poor nutritional con- ditions (group 3: Table 2, Fig. 3), and also com- paratively low in the freely grazing hinds at Kuusamo in late winter 1973, when compared

m ~ 3 - * w m r - - N o l - b w m l l ' n m hi,,,,,,,,

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652 CAN. J . ZOOL. VOL. 55, 1977

' ' ' v ' lvlll ' I X ' ' X I ' ' 1 ' k o n t h 1 1 21 9 20 n A

8 7 5 n C FIG. 3. Seasonal changes in the serum calcium of adult

female reindeer and calves. See the legend of Fig. 2.

I l l t l l l t i l l l t l

Ill V VII IX XI I m o n t h 11 22 17 20 n A

8 7 5 n C FIG. 4. Seasonal changes in the concentration of serum

magnesium. See the legend of Fig. 2.

0'21 ' 111 I V 'MI ' lX ' X I ' I ' k o n t h 1L 22 18 2 0 n A

8 6 5 n C FIG. 5. Seasonal changes in the concentration of serum

copper. See the legend of Fig. 2.

with the values during the summer and autumn (groups 4 and 5). Serum magnesium content was also very low in Enontekio hinds (group 3), and lower in the freely grazing hinds in Kuusamo (group 2) in March than in the summer (group 4). The winter feeding group (group 1) did not differ significantly from the summer group.

The serum magnesium content was slightly lower in the calves than the hinds in summer and autumn while the serum calcium concentration was correspondingly slightly higher (Table 2, Fig. 4).

Serum copper content was very low in the malnutrition group (3) in winter compared with all the other groups. In the freely grazing Kuusamo groups serum copper reached a high level in March and at the end of June (1 month after parturition), decreasing thereafter to assume a significantly lower level in autumn. In the calves serum copper continued to decrease towards the winter, but in the hinds it increased slightly (Fig. 5), and by the beginning of February the concentration was significantly higher in the latter than in the former.

Seasonal changes in serum zinc concentrations were similar to those in serum copper, though the zinc content in the serum of the group 3 suffering from malnutrition was about the same as that of the summer groups (Table 2).

Discussion The very hard conditions endured by group 3

living freely in the forests of Enontekio had had a pronounced effect on the mineral status of the animals. Serum calcium and magnesium were very low, and a comparison of the values for the different groups clearly shows that the reindeer in Enontekio were suffering from marked calcium deficiency and at least moderate magnesium deficiency. Bone resorption had caused a notice- able reduction in the specific gravity of the tibia and, in general, the animals which died in the same area 2 or 3 weeks after our blood samples were taken had very thin and porous bones.

Serum calcium concentration was also low in group 2 in Kuusamo in the late winter 1973. In groups 2 and 3, both of which had low serum calcium content, serum alkaline phosphatase activity was elevated as compared with the feeding group 1 and with group 6 in February 1974. It is supposed that elevated serum alkaline phosphatase activity is connected with increased secretion in the parathyroids for the mobilization of bone calcium. It is well known that serum alkaline phosphatase activity is elevated in con- nection with strong parathormone-induced bone resorption (Fourman and Royer 1968).

It is very likely that even in normal winters reindeer suffer from lack of minerals. The cal-

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HYVARINEN ET AL. 653

TABLE 3. Mineral content (% dry weight) of the most important food sources of the reindeer in different seasons

Food Ash K Mg Ca P Ca :P Reference

Winter Cladonia 1 .l-2.6 0.194.50 0.03-0.10 0.08-0.16 0.04-0.09 1.8-2.0 SITRA*

2.0-3.1 0.19-0.25 0.03-0.08 0.06-0.14 0.04-0.08 1.4-2.0 Isotalot Alectoria spp. 1.1-2.9 0.134.66 0.03-0.04 0.07-0.33 0.04-0.17 1.8-1.9 SITRA

1.9-2.1 0.23-0.24 0.02-0.03 0.16-0.20 0.06-0.07 2.2-3.0 Isotalo Deschampsia 4.1-5.3 1.28-1.55 0.07-0.08 0.16-0.23 0.15-0.26 0.9-1.1 SITRA

flexuosa 8.5 1.56 0.10 0.25 0.17 1.5 Isotalo

Spring Betula spp. 1.4-7.7 0.25-1.04 0.054.32 0.16-0.76 0.114.39 1.5-2.0 SITRA

2.8-9.6 0.36-0.81 0.07-0.28 0.374.57 0.22-0.28 1.4-3.9 Isotalo Salix spp. 2.1-9.4 0.38-1.66 0.09-0.28 0.33-0.95 O.l(M.51 1.9-3.3 SITRA

4.5-6.1 0.96-1.48 0.16-0.29 0.53-0.63 0.16-0.61 1 .O-2.0 Isotalo Carex 3.7-8.0 0.86-2.24 0.09-0.21 0.20-0.41 0.134.23 1.5-1.8 Isotalo

Summer, Autumn Equisetumspp. 12.3-19.5 1.80-2.76 0.21-0.34 0.90-1.13 0.154.27 4.2-6.0 SITRA

13.2-15.9 1.70-3.91 0.21-0.46 0.66-0.92 0.20-0.30 3.1-3.3 Isotalo Menyanthes 8.4-10.3 1.95-2.61 0.16-0.29 0.61-0.93 0.154.28 3.34.1 SITRA

rrifoliata 8.2 1.03 0.25 0.49 0.11 4.5 Isotalo Chamaenerium 5.4-10.3 1.32-2.79 0.29-0.35 0.67-0.90 0.23-0.52 1.7-2.9 SITRA

angustifolium 6.7 1.21 0.35 0.82 0.26 3.2 Isotalo Boletus spp. 6.3-7.8 2.20-2.53 0.05-0.09 0.06-0.09 O.S(M.56 0.1-0.2 SITRA

8.1 2.88 0.88 0.24 0.48 0.5 Isotalo

'Unpublished results of SITRA investigation team, Finland. tIsotalo 1971 (see the references).

cium, phosphorus, and magnesium content of the main winter food, lichens, is low (Table 3), so that if any shortage of food occurs this mineral deficiency may very soon develop into a severe case. The need for minerals, as also for other nutrients, is especially urgent in late winter and spring as a result of the increased require- ments of the developing calf.

Cameron and Luick (1972) and Luick et al. (1974) have shown that the flux of water through the total body water pool diminishes markedly during the winter, a phenomenon which is con- nected primarily with a low-nitrogen lichen diet. In view of the low concentrations of most minerals in lichens they suggest that minerals must be recycled between the body fluid and tissue pool and the alimentary tract. This must be true, but it is clear that even in normal winters reindeer must use bone minerals to compensate for the mineral insufficiency in their diet, especi- ally in late winter in the presence of increased fetal requirements as parturition approaches. The role of the skeleton as a mineral bank must be of great importance at this time. Marked bone resorption during the winter is also reported in the Finnish white-tailed deer (Paatsama et al. 1973).

In the case of group 3 in Enontekio the animals had also suffered from an obvious protein defi- ciency (Hyvarinen et al. 1975), but their serum protein levels were not lower than those reported by Afanasev (1963) for late winter in the U.S.S.R. or by McEwan (1968) in freely grazing animals in Canada.

The reindeer in Enontekio mostly died at the beginning of May, in places where the snow had melted. About 40% of the adult reindeer in this area died (Huttu-Hiltunen 1973) and only a few calves were found alive that summer. According to the herdsmen many of the animals suffered convulsions before death, and their death at places where food was more readily available together with these convulsions and the low serum calcium and magnesium levels indicate a possible disturbance in mineral metabolism of the grass tetany type. The most characteristic biochemical abnormality in grass tetany is a subnormal level of magnesium in the blood. Low serum calcium levels have been found to accompany low magnesium levels (Smith et al. (1972). The classical effect of hypocalcemia is tetany. Tetany is induced in most animals when the serum calcium level falls below 7 mg/100 ml (Smith et al. 1972). Many of the animals in

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654 CAN. J. ZOOL. VOL. 55, 1977

Enontekio had calcium levels below this, about 6.5-6.6. No clear signs of tetany could be seen, but some animals had difficulty in moving. It is difficult to say how the low energy intake is related to mineral deficiences.

The changes in serum copper content in the grazing hinds in Kuusamo suggest a possible seasonal change in serum copper concentration under normal conditions. The copper content is high in late winter before and after parturition, and is lowest in autumn and early winter. It is known that the serum copper concentration in sheep decreases during pregnancy (Underwood 1971), but it increases again during the time of parturition to reach the highest levels recorded 1 week after lambing (Howell et al. 1968). In women copper almost doubles during pregnancy, these changes being connected mainly with fluctuations in serum ceruloplasmin levels (Underwood 1971). The reindeer in Enontekio (group 3) had very low serum copper concentra- tions as compared with the other groups. It is very difficult to say what is the significance of this copper deficiency in the case of the reindeer deaths in the Enontekio area. The reindeer may have had deficiencies in some other trace elements or vitamins as well, although their serum zinc concentration was normal.

The high level of serum alkaline phosphatase activity in young calves is connected with rapid bone growth. It is known that alkaline phos- phatase participates in bone formation (Robison 1923). During bone formation activity is atso markedly elevated in the serum or plasma (see Fourman and Royer 1968). In February 1974 the serum alkaline phosphatase activity of the calves was already about the same as that in the adults, which clearly indicates a cessation of growth during the winter months. The compara- tively high serum alkaline phosphatase activity in the hinds in summer is probably connected with bone regeneration after the winter and with antler formation. Plasma alkaline phosphatase activity is extremely high in white-tailed deer stags during antler growth (Graham et al. 1962). Our later measurements (unpublished data) indicate that the serum phosphate concentration is rather high during autumn and winter and low during the time of the growth in June and July.

Feeding conditions had a clear effect on serum potassium content during the winter. The potas- sium concentration was high in the feeding group

and lowest in group 3, those experiencing poor nutritional conditions. The potassium content of winter food is very low (Table 3). In the autumn the serum potassium concentration of the hinds was also low, however, although this time the reindeer could get good quality food with a high potassium content in nature. This may be connected with the rut, which occurred just at the sampling time. The reproductive cycle may also be responsible for the changes in serum zinc concentrations (cf. Underwood 1971; Henkin 1971), though nutritional aspects and general changes in metabolism (cf. McEwan and Whitehead 1970; Luick et al. 1974) may also be important factors occasioning the low autumn and winter zinc values.

AFANASEV, W. P. 1963. Eiweissmorphologisches Bild des Blutes bei den Renntieren hangt von der Jahreszeit ab. Tr. Mosk. Vet. Akad. 47: 329.

AHTI, T. 1961. Poron ravinnosta ja laitumista. Lapin tut- kimus seuran wosiki j a , 2: 18-28.

BODANSKY, O., and M. K. SCHWARZ. 1961. Alkaline and acid phosphatases. In Methods in medical research. Vol. 9: Edired by J. H . Quastel. Yearbook Medical Pub- lishers, Chicago. pp. 7%98.

CAMERON, R. D., and J. R. LUICK. 1972. Seasonal changes in total body water, extracellular fluid, and blood volume in grazing reindeer. Can. J. 2001.50: 107-1 16.

DIETRICH, R. A., and J. R. LUICK. 1971. Reindeer in biomedical research. Lab. Anim. Sci. 21: 817-824.

FOURMAN, P., and P. ROYER. 1968. Calcium and the bone. Blackwell, Oxford.

GRAHAM, E. A., R. RAINEY, R. E. KUHLMAN, E. H. HOUGHTON, and C. A. MOYER. 1962. Biochemical in- vestigations of deer antler growth. Part I. J. Bone Jt. Surg. 44-A: 482-488.

HENKIN, R. J. 1971. Newer aspects of copper and zinc metabolism. In Newer trace elements in nutrition. Edited by W. Mertz and W. E. Comatzer. Academic Press, New York. pp. 255-312.

HOWELL, J., MAC., N. EDINGTON, and R. EWBANK. 1968. Observations on copper caeruloplasmin levels in the blood of pregnant ewes and lambs. Res. Vet. Sci. 9: 160-164.

HUTTU-HILTUNEN, V. 1973. Kato. Poromies, 2: 38. HYVARINEN, H., and T. HELLE. 1974. Poroerotukset ja

porojen lihan maku. Poromies, 1: 8-9. HYVARINEN, H., T. HELLE, R. VAYRYNEN, and P. VAY-

RYNEN. 1975. Seasonal and nutritional effects on serum proteins and urea concentration in the reindeer (Ran- gifer tarandus tarandus L.). Br. J. Nutr. 33: 63-72.

HYVARINEN, H., T. HELLE, M. NIEMINEN, P. VAYRY- NEN, and R. VAYRYNEN. 1976. Some effects of handling reindeer during gatherings on the composition of their blood. Anim. Prod. 22: 105-114.

ISOTALO, A. 1971. Poron luonnonvaraisten rehukasvien ravintoarvosta. Lapin tutkimusseuran vuosikirja, 28: 28-45.

KELSALL, J . P. 1968. The migratory barren-ground caribou

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

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YO

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UN

IV o

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14Fo

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of Canada. Can. Wildl. Serv. Monogr. 3. Queen'sPrinter, Ottawa. pp. 79-82.

LENT, P. C. 1965. Rutting behaviour in barren-ground caribou population. Anim. Behav. 13: 259-264.

LUICK, J. R., R. A. DIETRICH, D. HOLLEMAN, and R. G. WHITE. 1974. Studies on the nutrition and metabolism of reindeer-caribou in Alaska with special interest in nutri- tional and environmental adaptation. Progr. Rep., Univ. Alaska, Fairbanks.

LUICK, J. R., S. J. PERSON, R. D. CAMERON, and R. G. WHITE. 1973. Seasonal variations in glucose metabolism of reindeer (Rnngifer tnrnndus L.) estimated with (U- 14C) glucose and (3-)H) glucose. Br. J. Nutr. 29: 345.

MANERY, J. F., J. S. BARLOW, and J. M. FORBES. 1966. Electrolytes in tissues, red cells and plasma of the polar bear and caribou. Can. J. Zool. 44: 235-240.

o MCEWAN, E. H. 1968. Hematological studies of barren- ground caribou. Can. J. Zool. 46: 1031-1036.

MCEWAN, E. H., and P. E. WHITEHEAD. 1970. Seasonal changes in the energy and nitrogen intake in reindeer and caribou. Can. J. Zool. 48: 905-913.

PAATSAMA, S., H. SUOMUS, and E. TANHUAPAA. 1973.

Valkohantapeura tutkimuksen valokeilassa. Kasvu ja lisaruokinta. Metsataja, 4: 6-7.

PERKIN-ELMER CORPORATION. 1972. Analytical methods for atomic absorption spectrophotornetry. Nonvalk, Connecticut, U.S.A.

ROBISON, R. 1923. The probable significance of hexosephosphoric esters in ossification. Biochem. J. 17: 286-293.

SCOTTER, G. W. 1965. Chemical composition of forage lichens from northern Saskatchewan as related to use by barren-ground Caribou. Can. J. Plant Sci. 45: 246-250.

1967. The winter diet of barren-ground caribou in northern Canada. Can. Field-Nat. 81: 33-39.

SMITH, H. A., T. C. JONES, and R. 0. HUNT. 1972. Veteri- nary pathology. Lea & Febiger, Philadelphia.

STEEN, E. 1%6. Investigations into reindeer grazing in north Scandinavia. Int. Grassl. Congr. Helsinki, Sect. 4. 10: 998-1003.

UNDERWOOD, E. J. 1971. Trace elements in huhan and animal nutrition. Academic Press, New York.

VARO, M. 1973. Tutkimuksia poron jalostusmahdollisuuk- sista. Poromies, 1: 1S28.

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