‘ :‘ ‘ 3|‘I ‘ Tl _ TIITI I" I; ‘1‘ TM Hi'i a‘il ‘1 11 T T >\ \T If ‘ ET! I T‘ T .1 ’1 31‘ ’I 11; M | | l N ‘I l T W l {I H l .3 I T T‘ i‘ w (T I TM -1_‘_‘ ‘ Icon 1‘ (De—‘03 I II I THE FASTENG METABOLISM OF SUBADULT MALLARDS ACCLITMATIZED T0 LOW AMTBEENT TEMPERATURES Thesis for the Degree of M. S. MICHIGAN STATE UNIVERSTTY KTRTLAND GORDON SMITH 19 72 TTTTTT TTTTTTTTT ! 301005 Michigf' State Univc sity « TTT T 12 .A-T‘ ‘- ut J- U ~’\| \. ‘0 , u/ ‘ 1‘ ('0 {3135 t A 'K "'3 1 0 «dn o ‘5“ A H ‘V'vi 3 40“., lvsJ ABSTRACT THE FASTING METABOLISM OF SUBADULT MALLARDS ACCLIMATIZED T0 LOW AMBIENT TEMPERATURES Bv d Kirtland Gordon Smith The caloric requirements of 20 male and 20 female subadult Mallards were determined at low ambient temperatures. The fasted, acclimatized birds were eXposed to a ~10 C to 20 C range, and the time required to consume 50 cc of oxygen at each test temperature was determined manome- trically. The average weight of males was 154 gm greater than females. There was no relationship between weight loss and ambient temperature during an 18 hour fast prior to metabolic determinations. A significant linear relationship between increasing oxygen consumption and decreasing ambient temperature was observed for both sexes. Although there was no significant difference in the regression coefficients between sexes, there was a significant difference in the elevations of the regression lines, with metabolic intensity being greater for males than for females. When heat production was divided by the metabolic body size (WO°744), a sex difference in metabolism unrelated to body weight was still evident. The greater metabolic intensity and body weight of the males suggests that they can tolerate lower temperature extremes than the females. The lower critical temperature was near 20 C for a fasted bird. When the calorigenic effect of food was estimated, the lower critical temperature decreased to an estimated 10 C range; the temperature that commonly occurs when breeding is initiated in the spring. THE FASTING METABOLISM OF SUBADULT MALLARDS ACCLIMATIZED TO LOW AMBIENT TEMPERATURES BY Kirtland Gordon Smith A THESIS Submitted to Michigan State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Department of Fisheries and Wildlife 1972 1:3 DEDICATION To my most sincere and devoted teachers, Charles and Margaret Smith, whose wise guidance have produced a deeply appreciative student. ii ACKNOWLEDGEMENTS I wish to thank the members of my professorial committee, Dr. Harold H. Prince, Dr. Walter H. Conley and Dr. Robert K. Ringer, for the guidance, suggestions and valuable editorial comments. My thanks go to Dr. E. P. Reineke for his patience and crea- tivity in the field of calorimetry and Mr. Robert Freeman for his assistance in an attempt to understand the dynamics and techniques involved. Finally, to the many members of the faculty and staff at Michigan State University who were continually bombarded with my impatient inquiries, I extend my thanks. The study was supported in part by the Detroit Edison Company and the Institute of Water Research. Use of the Michigan State University computing facilities was made possible through support, in part, from the National Science Foundation. LIST OF TABLES LIST OF FIGURES INTRODUCTION . . MATERIALS AND METHODS RESULTS . . . . DISCUSSION . . . LITERATURE CITED TABLE OF CONTENTS iv Page vi 13 19 Table 1. 2. LIST OF TABLES Body weights (i’i S.E.) before and after an 18 hour faSt O I O O O C O O O O O O I I O O O O O O O O O O O O O 0 Thermal conductance of several avian species . . . . . . . . Figure 1. 2. 3. LIST OF FIGURES Page Respiratory chamber and Mallard in resting position . . . . 4 Metabolic rates of male and female Mallards under varied temperatures expressed in ccOZ/gm/hr . . . . . . . . . . . 10 Metabolic rates of male and female mallards under varied temperatures expressed in ccOz/gm/hr . . . , , , , , , . , 11 vi INTRODUCTION The physiological stress imposed upon a wild animal during the winter months is among the most critical in the organism's life (West, 1960; Sturkie, 1965; Brocke, 1968; Gordon, 1968). Kendeigh (1944) stated that temperature is one of the most important environmental fac- tors controlling distribution, migration, abundance and time and extent of breeding of wild birds under normal outdoor conditions. Lefebvre and Raveling (1967) have related the distribution of two races of Canada Geese in winter to body size and corresponding estimates of heat loss. Temperature, as well as other abiotic factors, has been correlated to seasonal and daily behavior among avian species by Salt (1952), West (1960), Cox (1961), and Reed (1971). If ambient temperatures upset the equilibrium.between heat production and loss, the animal's behavior must be altered to maintain homeostasis. Fundamentals of energy exchange in endotherms and the literature dealting with avian bioenergetics have been reviewed from.many points of view by Irving (1955), Hart (1957), Klieber (1961), King and Farner (1961), and West (1962). Caloric requirements under varied temperatures have been determined for many avian species (Steen, 1957;.Dawson and Tordoff, 1964; Lasiewski and Dawson, 1964; King, 1964; Brush, 1965). Most bioenergetic investi- gations of birds have been restricted to the laboratory or have dealt only with the energy requirements of a few normal activities under free- living conditions. Until reliable techniques are perfected to obtain the total picture of metabolic intensity in the field, laboratory studies 2 are more important from a comparative rather than an ecological view (Owen, 1969). The study was designed to quantify the resting metabolic require- ments of the Mallard, Anas platyrhynchos, as a function of temperature. The Mallard has a circumpolar distribution in the Northern Hemisphere and among waterfowl is probably the most abundant species (Delacour, 1964). There has been no previous attempt to determine the existence energy of a Mallard during winter's extreme conditions, however, there is some empirical data concerning lower lethal temperatures, winter behavior and basal metabolic rates (Kendeigh, 1945; Streicher gt al., 1950; Jordan, 1953; Madson, 1960; Reed, 1971). To attest to its abil- ity to tolerate extreme conditions, Giaja _£._l. (1928, in Brody, 1945) found that a Mallard in a post-absorptive state was able to maintain body temperature for one hour at -100 C. MATERIALS AND METHODS Forty, seven—month—old Mallards were used in the experiment. The birds were progeny of "game farm” Mallards obtained from the Max MCGraw Wildlife Foundation, Dundee, Illinois. The birds were fed a ration of two parts corn and one part Purina Flight Conditioner ad libitum, and maintained in 7 x 3 x 3 M outdoor pens containing a heated water supply from October through February. Ambient temperature in the pens was recorded daily. Prosser and Brown (1950) define 002 as milliliters of oxygen (S.T.P.D.) consumed per gram dry weight per hour. In my study, Q02 refers to milliliters of oxygen (S.T.P.D.) consumed per gram wet weight per hour. Q02 values were obtained manometrically based on a constant pressure changing volume respirometer as discussed by Reineke (1961). A 20 x 35 x 40 cm plexi-glass chamber with five ports was constructed (Figure 1). A 50 cc gas syringe, manometer, c0pper-constantan thermo- couple, air inlet tube, and exhaust were arranged in the five openings of the respirometer. A copper screen bed of indicating Ascarite (sodium hydrate asbestos) was attached to the door of the chamber. A pilot study revealed that at the thermal condition of maximum C02 production, 150 cm: of Ascarite were saturated in four hours. An air pump was used to ventilate the system during the acclimation period and between each Q02 determination. It was found that an adult male Mallard could sur- vive in the chamber without the air pump for four hours before chronic anoxia became fatal. A mercurial barometer was used to determine Figure I. Respiratory chamber and Mallard in resting position. ‘ . . . a 0. O... s-.._ . . _ atmOSpheric pressure and the copper-constantan thermocouple with a millivolt recorder monitored ambient temperature (TA). TA was control- led by an environmental chamber with a temperature range of -30 C to 50 C i.1 C. Metabolic rates of the birds were determined between 15 January to 15 February. Ducks were fasted for 18 hours before oxygen consumption was determined. Even though a post—absorptive state was relatively assured after 18 hours (Benedict and Lee, 1937; Sleeth and Van Liere, 1937), a mixed caloric conversion for both fat and protein catabolism of 4.825 Kcal/liter 02 was used. Weights of both sexes were recorded before and after the fasting period. The pre-cooled respiratory chamber was darkened during the 2.5 hour acclimation period and during the Q02 determinations. At the end of this period, the air pump was stopped and the chamber was sealed. Fifty milliliters of air were injected from the gas syringe into the chamber; the length of time required to consume the volume of air, as determined by the manometer, was used to calculate oxygen consumption per gram per hour. One measurement was taken every five minutes and the measurements were rejected if TA fluctuated j; 1 C during the thirty minute test period. If a fluctuation of 1:1 C occurred, no measurement was attempted until the TA returned to its previous value. Five birds of each sex were randomly chosen and subjected to one of four temperature zones centering around -8 C, 0 C, 10 C and 20 C. No bird was used twice. Any movement by the bird in the chamber was readily detected by fluctuations in the manometer fluid level, and measurements were accepted only if the animal was quiet. Condensation or ice was present in the chamber after the three hours at all of the test temperatures, indicating that the atmosphere was saturated with 6 water vapor and thus simplifying the conversion of the volume of oxygen from ambient temperature-pressure-saturated (A.T.P.S.) to standard temperature—pressure-dry (S.T.P.D.). In a saturated system, P equals 1120 the aqueous vapor pressure; therefore, aqueous vapor pressure at the specific TA was subtracted from the barometric pressure to standardize the volume of air. 002 was determined from 10:30 to 11:00 for females and 14:00 to 14:30 for males. Body weight data were analyzed with a two—way analysis of variance (Steel and Torrie, 1960) using the model Xij = u + oi + Bj +(a B>ij+i:ij where Xij equals the individual duck weight, u equals the parametric mean, ai equals the ith treatment effect (1 = 1...a) with the treatments representing the weight before and after the 18 hour fast, Bj equals the jth block effect (j = 1...b) with the blocks representing sex, a Bij represents the interaction of sex and weight loss, ands:ij equals the random, experimental error (independently and normally distributed about zero mean and with a common variance). The effects of temperature on 002 and caloric values were determined using the polynomial regression routine discussed in Cooley and Lohnes (1971). Standard linear and quadratic models were sufficient to explain these effects. Treatment separations without the added effects of temperature for differences between sexes were accomplished with an analysis of covariance (Steel and Torrie, 1960) using the model Yij - B(Xij - Q..) = u + ai +Elij where Yi equals the oxygen consumption of an individual duck, 8(Xij - j E..) equals the adjustment for regression of oxygen consumption on . .th temperature, u equals the parametric mean, oi equals the 1 treatment effect (i = 1...a) with the treatments representing male and female oxygen consumption, ande ij equals the random, experimental error 7 (independently and normally distributed about zero mean and with a common variance). This model provides for the known relationship with temperature, allowing an analysis of variance on adjusted treatment means. It is assumed that temperature is a fixed variable and measured without error, that the regression of oxygen consumption on temperature is linear, and that the error is random and in an independent, normal distribution about zero mean with a common variance. Unless otherwise stated, in all cases where statistical significance is indicated P< 0.001. Analyses were conducted on the CDC 6500 computer at the Michigan State University computer center. RESULTS Average body weights of seven—month-old male and female Mallards were significantly different before and after the 18 hour fast (Table 1). Table 1. Body weights (i i S.E.) before and after an 18 hour fast. Ave. wt. (gm) Ave. wt. (gm) Ave. wt. (gm) Sex n before fast after fast lost female 20 10841213 1012:20C 71t5e male 20 1248t25b 1166:22d 72:6e Any two values in a row of column having the same superscript (a, b, c, d, e) are not significantly different. The males and females responded similarly to fasting and experienced a weight loss of 6.5 percent and 5.7 percent of the total body weight, respectively. The temperature during the period of fast in the outdoor pens varied from -30 C to 10 C. No mortality was observed. There was no relationship between maximum, minimum, or average daily temperatures during the period of fast and weight loss. Several times the black cover-over the respiratory chamber was lifted briefly to observe behavior. At lower temperatures, the birds would exhibit gross muscular activity, but eventually settle into the resting position shown in Figure 1. Once at rest, shivering was observed. There was a significant linear relationship between increasing oxygen consumption and decreasing ambient temperature for both sexes 9 (Figure 2). Although there is no significant difference between the regression coefficients, covariance analysis of the regression lines showed a significant difference in the elevation of the lines. The males consumed larger quantities of oxygen per gram body weight over the temperature range than females. The coefficient of variation for Q02 values of five males at -8 C, O C, 10 C, and 20 C was 15, 6, 6, and 7 percent, respectively and 14, 17, 9, and 16 percent for five females at each of the respective temperature zones. The high coefficients of determination (r2) imply that a large percentage of the variation in 002 can be explained by the independent variable, temperature. During a pilot study, oxygen consumption for an additional four males and two females was determined at temperatures ranging from 28 C to 38 C (Figure 2). A mean of 0.77 i 0.02 cc02/gm/hr was similar to the 002 at 22.1 C for the males and 19.4 C for females, suggesting that the lower critical temperature is in the vicinity of 20 C. A caloric value of 4,825 Kcal/liter 0 was used to convert oxygen 2 consumption to Reel of heat produced. Energy produced per day was then divided by the metabolic body size (W0°744 — King and Farner, 1961) so comparisons of metabolic rate could be made independent of body weight (Figure 3). For both sexes the theoretical, inverse linear relation between the amount of energy produced and decreasing tempera— ture was observed. The r2 values remained high, and the sexual dimor- phism in metabolism at all of the test temperatures remained evident. Using the body weights of my Mallards, a predicted basal metabolic rate 0.744 of 74.3 Kcal/wt /day was calculated (Figure 3) according to King and Farner's formula (1961) which assumes no sex difference in basal metab- olism. The conversion of oxygen consumption from the data above 25 C 0.7 to energy gave a value of 91.1 Kcal/wt 44/day. When energy production cc02/gm./ hr. 10 3.00 — 2.50 Male 0 y = 1.970 - 0.054 x r2: 0.932 2.00 O l.50-— LOO— O 8 o .0 Female 0 o _ 9: l.780—0.052x 0'50 r2 = 0.882 I J l l j A 0 IO 20 30 40 Temperature °C Figure 2. Metabolic rates of male and female Mallards under varied temperatures expressed in ccozlnghr. Six 002 values (above 25°C) are shown, but are not included in the regression analysis. 350 300 250 Kcal /wt.°'744/day m o 0 E7: 0 |00 50 11 o M018 y = 237.037—6.492x r2 = 0.932 Predicted """""""""" e' .inTEz" Female “ y = 206.986-6.055x r2 = 0.909 I .- l l 0 IO 20 Temperature °C Figure 3. Metabolic rates of mole and female Mallards under varied temperatures expressed in Kcal/wt.°-744/day. Predicted B.M. R. from King and Farner (l96l), assuming K(M=KWt.°'744) is similar for both sexes. 12 was expressed as Kcal/day, a significant (0.01 < P < 0.025) quadratic effect of temperature was observed for the females [y = 203.42 - 8.153 ($0.839) x + 0.134 (i0.054)x2, r2 = 0.932], while the relationship remained linear for the males [y = 267.705 - 7.529 (i1.323)x, r2 = 0.933]. Because no quadratic effect was observed for the females when the data was expressed as Kcal/wt0°744 /day, it is assumed that random experimental differences in female body weight were responsible for the curvilinear relationship. DISCUSSION The problems involved attempting to evaluate metabolism are reviewed by Adams and Poulton (1932), Brody (1945), King (1957), Klieber (1961), Jellinck (1963), and Gordon (1968). There seems to be no single method capable of giving a complete picture of intermediary metabolism. The following assumptions were made using the manometric technique. The metabolic rates of the Mallards were normal for a particular test temp- erature after 2.5 hours. Steen (1957) found that Pigeons (Columba livia) sit quietly once a reSpirometer is darkened. West (1962) observed that metabolic rates remain elevated for approximately one hour after birds are placed in a darkened chamber. I assumed that the Mallards maintained a constant core temperature throughout the -8 C to 20 C range, based on observations of avian body temperatures by Simpson and Galbraith (1905), t a1° (1928), Kendeigh (1944), and Veghte (1964). Diurnal fluc- Giaja __ __ tuations corresponding with normal daily activity periods were reduced by the minimum size of the darkened metabolic chamber and by conducting 002 determinations at constant times for each sex. It was assumed that glycogen stores in the fasted ducks were minimal, and therefore heat production from anaerobic metabolism could be disregarded. With the assumption of a 100 percent saturated atmosphere surrounding the duck, heat loss due to evaporation would be negligible. Although evaporative heat loss in an atmosphere of low humidity is a factor, in a winter environment low temperatures (lower aqueous vapor pressure) also reduce evaporative heat loss (Birkebak g; g1,, 1966). It was also assumed that 13 14 the maintenance of the captive flock in an outdoor pen acclimatized the Mallards to the test temperatures (Dhar, 1922; Adolph, 1950; Sellers gt _at., 1951; Potter, 1958; Hart, 1957, 1962). Both male and female Mallards appeared to maintain homeostasis at low ambient temperatures in the same manner (Figure 2). The importance of metabolic determinations of wintering Mallards above 25 C is question- able. This, plus acute thermal polypnea causing pressure differentials in a constant pressure apparatus, precluded more than six 002 determina— tions above 25 C. Although the values were comparable to those at 20 C, more information is needed to confidently mark a zone of thermoneutrality. Individual variation in heat production below 0 C suggests a differential ability to adapt as lower temperature extremes are approached. Physical thermoregulatory mechanisms create the maximum effective- ness of insulation at the lower critical temperature of the theoretical zone of thermoneutrality. Below the lower critical temperature, the rate of heat loss (thermal conductance) remains constant (Gordon, 1968). Although thermal conductivity is inversely related to thickness of subcutaneous fat and density and insulative prOperties of the plumage, it may vary with severla other factors such as blood circulation, and evaporation rates (Gordon, 1968). A comparison of weight and weight specific conductance is made for several avian species in Table 2. A curvilinear relation appears to exist between increasing body weight and decreasing thermal conductance. The relatively low thermal con— ductivity of 0.053 cc02/gm/hr/° C for the Mallard suggests that it is capable of surviving in a variety of thermal extremes. High thermal conductance values greatly increase the cost of thermoregulation 15 Table 2. Thermal conductance of several avian species. Weight Thermal Cond. Species (gm) ccOZ/gm/hr/°C Reference Black Chinned Hummingbird 3.3 0.500 Lasiewski, 1963 (Archilochus alexandri) Black Capped Chickadee 10.6 0.283 Herreid and (Parus atricapillus) Kessel, 1967 White Crowned Sparrow 25.8 0.183 Herreid and (Zonotrichia leucophrys) Kessel, 1967 Cardinal 40.0 0.100 Dawson, 1958 (Richmondena cardinalis) Evening Grosbeak 58.0 0.100 Dawson and (Hesperiphona vesperitina) Tordoff, 1959 Northern Blue-Jay 81.0 0.045 Misch, 1960 (Cyanocitta cristata) Northwestern Crow 306 0.060 Irving, g£_§1,, (Corvus caurinus) 1955 Blue-Winged Teal (female) 362 0.052 Owen, 1970 (Anas discors) Willow Ptarmigan 708 0.029 Herreid and (Lagopus laggpus) Kessel, 1967 Mallard (female) 1166 0.054 Present study (Anas platyrhynchos Mallard (male) 1166 0.054 Present study (Anas platyrhynchos) Brant 1130 0.019 Irving, g£_§1,, (Branta berricola) 1955 Sandhill.Crane 2755 0.019 Herreid and (Grus canadensis) Kessel, 1967 16 at low ambient temperatures and may be an important factor in limiting the distribution of endotherms (Lasiewski, 1963). Fasting metabolic rates at low ambient temperatures are applicable to the activities of wintering populations of Mallards. Reed (1971) observed that a wintering flock of Mallards may feed only once a day, during the afternoon. He also noted a relationship between decreasing mean temperature for the three previous days and a decrease in activity on an open body of water. Energy spent on frequent feeding flights and warm weather activities must be used for chemical thermoregulation by wintering populations. The lack of a relationship between tempera- ture and weight loss in an 18 hour interval could also be related to Reed's (1971) field observations. Although he observed no relationship between temperature and activity on the same day, there was a relation- ship between decreasing activity and decreasing mean temperature on the previous day and the previous three-day period. This suggests that more than an 18 hour period at low ambient temperatures is needed to observe a weight loss as a function of temperature in a bird the size of the Mallard. A difference in metabolic intensity between sexes has been shown previously for several avian species (Herzog, 1930; Benedict, 1938; Quirring and Bade, 1943). Sturkie (1965) notes that a sex difference in heat production may depend upon the age of the birds and is not always evident when heat production is related to body weight. In this study, the metabolic differences between sexes cannot be explained by a weight difference alone. When heat production is expressed as a ratio with met- abolic body size (Figure 3), the regression lines are still significantly different. If there is a sex difference unrelated to body weight below the lower critical temperature, it is reasonable to expect an initial 17 difference in male and female basal metabolic rates. The prediction equation for the basal metabolic rate is M = 71.2 x W3/4L for human males and M = 65.8 x W3/4 for females, where M = Kcal/day and W = kilograms of body weight (Kleiber, 1961). The equation given by King and Farner (1961) for birds weighing more than 0.1 kg(M = 74.3 x WO°744) does not consider a difference in the constant K (74.3) for each sex. The sex difference in metabolic rate suggests that males can produce more energy in the form of heat per gram body weight than the females. Thus, with a similar food supply, males should be able to withstand lower am- bient temperatures before homeostasis is jeopardized. This difference in metabolism plus the males' larger size provides an explanation for the greater percentage of males in wintering populations in the northern part of the Mallard's winter range as reported by Bellrose g£_gl. (1961) and Reed (1971). Sudgin (1971) determined metabolizable energy (M.E.) expressed as Kcal/day for 12 male and 12 female five-month-old Mallards at 20 C. M.E. values include the heat increment of feeding above the post-absorptive level (S.D.A.). Once the S.D.A. is subtracted from M.E. and adjusted to the body weight of the Mallards used in this study, net energy values are comparable with the values obtained manometrically. For example, based on a proximate analysis of Manitou Wheat, the S.D.A. was estimated to be 14.5 percent of the total diet for both males and females (Brody, 1945; Kleiber, 1961). The net energy (M.E. - S.D.A) from the wheat diet was 145.07 kcal/day for males and 101.93 Kcal/day for females. I esti- mated the average net energy of my Mallards at 20 C to be 121.50 Kcal/day and 97.89 Kcal/day for males and females, respectively. 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