Energy metabolism of oiled muskrats

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  • Energy metabolism of oiled muskrats

    E. H. MCEWAN, N. AITCHISON, AND P. E. WHITEHEAD Canadian Wildlye Service, University of British Columbia, Vancouver, British Columbia

    Received April 10, 1974

    MCEWAN, E. H., N. AITCHISON, and P. E. WHITEHEAD. 1974. Energy metabolism of oiled muskrats. Can. J. Zool. 52: 1057-1062.

    The heat production of muskrats (Ondatra zibethica), oiled with varying quantities of crude oil, was measured at three ambient temperatures, -5, 5, and 10C on days 0, 1, and 3 after oiling. On day 0, the heat production of muskrats oiled with 1.9 to 42.3 g of oil was from 14 to 119% higher, r e s ~ t i v e l y , than the non-oiled muskrats. Three days after oiling, the metabolic rate of oiled mus ats was about the same as the control values. A similar trend was determined for ambient temperatures of 5 and 10C. Heav oiling increased the thennal conduction of muskrats by as much as 12270. To compensate z r the loss of insulation and increased thermal conductivity of the fur, there was a 2.5-fold increase in dry-matter intake. In view of their dependence on water, both for feeding activities and a place for refuge, it is doubtful if muskrats exposed to moderate quantities of oil could survive under natural conditions.

    MCEWAN, E. H., N. AITCHLSON et P. E. WHITEHEAD. 1974. Energy metabolism of oiled muskrats. Can. J. Zool. 52: 1057-1062.

    On a mesure la prduction de cbaleur chez des rats musquCs (Otrdatra zibeihica) enduits d'lluile au moyen de quantitb variabls d'huile brute, it trols tempCratures ambiantes, -5, 5 el l K , 0,l et 3jour.s aprk le trairement. Au jour 0, la production dc chxleur des rats musquk enduirs de 1.9 h 42.3 g d'hhue est de 14 ilYc;, plus pande, respeciivemt, que celle des animaw non huilts. Trois joucs aprbs le tmitement, le rnetaholisme des rats musques huiles est B peu prks le m&me que celui des nnirn~ux temoins. 11 s'irablir une tendance sirnulaire aux temperatures arnbia~cs de 5 et 1 K . Une 6paisse couche d'huile augmente In conduction thermque des rats rnusquds jusqu'h 122Ls decc qu'elle est normalemenf. Afin de compenser la perte de son iwlation et l'augmentation de la conductivitk thermique de sa fourrurc, le rat musqu! augmeqte son ingestion d'un facteur de 2.5 [rnatikre dche). Les rats musqubs dependent du mlI~eu aquntique, el pour leur alimentntion, et comme heu de rcfuge; il est donc peu pro3ble clu'ils puissent survivre en milieu narurel ~prPls exposition .i des quan~itCs modCrCes d'hu~le.

    Fraduit par le journal]

    Introduction temperature was about 10C in winter and 15C in summer. A diet of medicated Purina rabbit chow was provided ad

    Oil pollution has become a serious hazard to libitum. Feed consumption was measured daily; body aquatic birds and mammals. Studies have shown weights were taken regularly. that oil contamination of the feathers of birds The apparatus used for metabolic rate measurements results in a breakdown in insulation and a was an open-circuit respirometer, described previously

    (McEwan and Koelink 1973). From July 1972 to April marked increase in rate (Hartung 1973, the metabolic rate of 29 muskrats was determined 1967; McEwan and Koelink 1973). The ingestion from 34c to -8C, lowered at 2-3C intemals. Four of refined oils associated with ~reenine: can be muskrats were starved for 24 and 48 h to determine fast- toxic to waterfowl (Hartung A d ~ u i t 1966). Little information is available on the effects of oil pollution on aquatic and semiaquatic mam- mals. The present study was undertaken to pro- vide basic information on the effects of measured quantities of crude oil on the energy metabolism of muskrats.

    Materials and Methods Throughout June to December 1972, adult muskrats

    were procured by live-trapping on Westham Island, Delta, British Columbia. The animals were penned indi- vidually, or in pairs, in wire cages, measuring 2 X 2 X 2 ft, suspended in about 12 in. of water. The water temper- ature of the tank remained at about 5C; the ambient air

    ing metabolic rate. Rectal temperatures were taken at the beginning and completion of each trial. Metabolic rate determinations of normal and oiled muskrats were taken at 10,5, and -5C, on days O,1, and 3 after oiling. Over a 10-min period, three readings of COz production and Oz consumption were made at 3, 6, and 9min. For each temperature setting, three sets of these readings were taken consecutively at 10, 20, and 30 min. Heat produc- tion was calculated from oxygen consumption and carbon dioxide production, according to the formula (Brouwer 1965): kcal = 3.866 (liters of 02) + 1.200 (liters of C02).

    Muskrats were oiled by placing them in a small tank, 25 X 50cm, partially filled with water upon which a measured quantity of crude oil varying from 2 to 49 g had been added. Before the muskrats were placed in the oily water, the volatile parts of the oil were allowed to evaporate. After a 5-min immersion in the oily water, the

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  • 1058 CAN. J. ZOOL. VOL. 52, 1974

    muskrat was transferred to the respirometer. The amount of oil remaining in the tank was determined by extracting it with petroleum ether, distilling off the ether layer, and weighing the remaining quantity of oil. A control musk- rat was removed from its cage and placed in the metabo- lism chamber. For oil treatments above 10 g of oil, a second muskrat was placed for 5 min in a tank filled with water only, to compare the activity of oiled and non-oiled muskrats. Muskrats were oiled once, except for muskrat No. 1564, which was oiled twice (Table 1). For practical purposes, light-oil treatments were considered below 10 g of oil, and heavy-oil treatments above 10 g.

    Results and Discussion Figure 1 gives a summary of the pooled data

    (n = 190) representing the relation between heat production and decreasing ambient temperature. Although metabolic rate measurements were made from July to April, no seasonal changes were observed. In the present study, the thermo- neutral zone of fed muskrats ranged from 10 to about 25C. These animals were unable to tolerate temperatures above 32C. Hart (1962) reported that muskrats tested at various air temperatures for 1 h showed an increased heat production be- low a critical temperature value of about 10C. In air, the thermoneutral zone of muskrats ranged from 10 to about 25C, while in water the range was reduced to 25-30C (Hart 1962). In the present study, the mean resting metabolic rate in the thermoneutral zone was 83 kcal/kg-day, which is similar to the basal heat production of mink, 84.3 kcal/kg- day (Farrell and Wood 1968). In the recalculation of Hart's (1971) data, an energy equivalent of 4.73 kcal/liter of oxygen at standard temperature and pressure (STP) was

    FIG. 1. The relationship between heat production and ambient temperature for muskrats fed (X), fasted 24 h (a), and fasted 48 h (0). Each curve is drawn through points which are the average of 3C intervals.

    used (Brody 1945). His value of 0.97 ml O2/g. h corresponded to 110 kcal/kg.day, which ex- ceeded the present value by 32%. The mean heat production of muskrats, fasted for 24 and 48 h, amounted to 60 and 50 kcal/kg. day, respectively (Fig. 1). During the 2-day fast, the decrease in body weight amounted to 9.5%. The lower metabolic rate may be due in part to a lowered body temperature. The mean body temperature of 48-h-fasted muskrats dropped from 38 to 37C.

    The amount of crude oil on the water surface of the tank ranged from 1.6 to 39.2 mg/cm2, or 2 to 49 g of oil (Table 1). The uptake of oil by muskrats was a function of the amount of oil present (jj = 0.13 f 0.78x), where y represents the amount of oil on muskrats and x equals the amount of oil added to the tank (Fig. 2). The mean percentage of oil adhering to the fur of muskrats amounted to 80% of the oil present. The rate of oil uptake per muskrat would be expected to gradually level off as the quantity of oil was increased. During the 5-min period in clean water, most of the muskrats floated or swam leisurely in the tank. The behavior mani- fested by muskrats placed in the oily water consisted of trying to escape from the tank, preening, and shivering. The fur of muskrats treated with 25.6-42.3 g of oil became wet, re- sulting in a loss of buoyancy. Wragg (1954) measured the sinking rate of muskrats in water and fuel oil. He found that muskrats exposed to

    I / " , 1 1 I I Oo I0 20 XI 40 5a

    OIL ADDED Ql

    FIG. 2. The relationship between the amount of crude oil added to tank and amount retained by muskrats.

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  • MCEWAN ET AL.: ENERGY METABOLISM OF OILED MUSKRATS 1059

    4 ml of fuel oil were almost completely sub- merged in 40 min. During the first 3 days after oiling, six of eight muskrats oiled with 2-9 g of oil lost 4% of their body weight; this may have been due to handling and confinement in the respirometer chamber and a reduction in feed intake. The mean weight loss of muskrats oiled with 18.5-42.3 g of oil was I1 % (Table 1) in 3 days and from 17 to 26y0 in 3 weeks after oiling.

    The heat production of oiled and control muskrats in relation to the degree of oiling and ambient temperature is tabulated in Table 2. On day 0, at - 5C, the heat production of muskrats oiled with amounts varying from 2.8 to 42.3 g of oil increased from 20 to 119% above the control values. At ambient temperatures of -5, 5, and 10C, the mean temperatures in the chambers containing the five heavily oiled muskrats were

    2.9, 2.0, and 2.4C higher, respectively, than the chambers containing the non-oiled animals. For the heaviest oiled muskrat, the ratio of resting to maximum oxygen consumption, 0.637 and 2.138 liters/h. ~ t . ~ . ' ~ , was 3.4, slightly less than Hart's (1962) ratio of 3.5. By day 3, the mean difference in the metabolic rates of heavily oiled and control muskrats was about 20y0. The metabolic rates of oiled muskrats maintained at 5 and 10C were similar and decreased gradually from day 0 to day 3, except for those treated with 18.5 g of oil (Table 2).

    The heat production of oiled muskrats minus the heat production of the respective controls on day 0 (- 5C), increased from 13 to 134 kcal/ kg. day as the degree of oiling increased (Fig. 3). By day 3, the metabolic rates of heavily oiled muskrats were reduced to values ranging from 14

    TABLE 1 Amount of crude oil retained by muskrats and the percentage

    body weight loss associated with oiling

    Oil retained Body wt., Wt. loss, Amount of oil,

    Date Animal No. f: % mg/cm2 g %

    'Part of oil added directly to muskrat.

    TABLE 2 Summary of metabolic rates (kcal/kg per day) of oiled and control muskrats

    measured on days 0, 1, and 3 and at -5, 5, and 10C

    Ta = -5C Ta = 5C Ta = lOC Oil,

    g 0 1 0 1 3 0 1 3

    42.3(1) 232 140 137 197 112 92 187 106 96 31.3(11 174 121 154 131 - 116 133 85 140

    "Number of muskrats per treatment in parentheses. tMean value of 18 control muskrats.

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  • 1060 CAN. I. ZOOL. VOL. 52, 1974

    to 33 kcal/kg- day above the controls. As shown in Fig. 4, there was a 7-fold difference between the metabolic rate of heavily oiled and lightly oiled muskrats on day 0 (5C). Three days later, the heat production of the oiled muskrats, except for those treated with 18.5 g of oil, was similar to the control values. The differences in the heat production of oiled and control muskrats measured at 1OC were similar to those at 5C (Fig. 5). On days 1 and 3, five determinations

    were from 0.6 to 12.0 kcal/kg- day less than the control values. The depressed metabolic rate of some of the oiled muskrats may be due to re- duced feed intake.

    The slope of the temperature-metabolism curve below the thermoneutral range provides a measure of the thermal conductance of muskrats and is inversely proportional to its insulation. The regression coefficients of muskrats oiled with 2-3.5, 6-9, 18-25, 3 1, and 42 g of oil were 2.84,

    FIG. 3. The difference between the heat roduction of oiled and control muskrats, measured on days O,1, and 3, at - 5C. Scale equals 150 kcal/kg

    FIG. 4. The difference between the heat production of oiled and control muskrats, measured on days 0, 1, and 3, at 5C. Scale equals 150 kcal/kg.day.

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  • McEWAN ET AL.: ENERGY METABOLISM OF OILED MUSKRATS 1061

    2.78,3.33,3.54, and 5.04, respectively, compared with the control value of 2.27 kcal/kg.24 h-C. For most species, there is a direct correlation between conductance and fur conductivity (Hart 1971). For muskrats, the pelt conductivity was 2 and 2.15 kcal/m2. h. C (Hart 197 1 ; W. H. Cottle, personal communication), respectively. In the present studies, heavy oiling increased the thermal conductance of muskrats by as much as 122%, compared with increases of 74 and 98% for oiled mallards and scaup, respectively (Mc- Ewan and Koelink 1973).

    The dry-matter intake of two heavily oiled muskrats, Nos. 1538 and 1590, and the mean intake of four control muskrats are shown in Fig. 6. During the first 3 days, feed consumption of both normal and oiled animals decreased, which was probably due to confinement and handling stresses associated with metabolic rate determinations. The dry-matter intake of a muskrat, oiled with 25 g of oil, increased from 60 to 100 g/day, then gradually returned to normal. On the other hand, the feed intake of a muskrat, oiled with 42 g of oil, increased to 200 g/day. Although water consumption was not measured, these animals consumed large volumes of water daily.

    Heavily oiled muskrats were observed to preen more than lightly oiled animals. This resulted in the loss of large amounts of underfur, and in causing the guard hair to remain erect. Muskrats are protected from the cooling effect of water by

    a layer of air trapped next to the skin, equivalent to 25% of the volume of the animal (Johansen 1962). Johansen found that animals depleted of the insulative air layer lose heat at a faster rate than normal muskrats. In the present study, heavily oiled muskrats remained out of the water for up to 30 days. Muskrats oiled with more than 10 g of oil tended to compensate for the loss of insulation by increasing their energy intake. The

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    FIG. 6. Mean dry-matter consumption of muskrats oiled with 25 and 42 g of crude oil compared with non- oiled muskrats: 0, control; X, 25 g of crude oil; 0 .42 g of crude oil.

    FIG. 5. The difference between the heat production of oiled and control muskrats, measured on days O,1, and 3, at 10C...