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Alberts_huddling1978

Alberts_huddling1978 - i 1 Journal of Comparative and...

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Unformatted text preview: i 1 Journal of Comparative and Physiological Psychology 1978, Vol. 92, No. 2, 231e245 Huddling by Rat Pups: Group Behavioral Mechanisms of Temperature Regulation and Energy Conservation Jeffrey R. Alberts Indiana University Body heat loss was attenuated and oxygen consumption was reduced by hud— dling in litters of developing rats. Rat pups derive physiological benefits from huddling similar to those enjoyed by adult mammals; these findings contrast with previous characterizations of the altricial rat as poikilothermic. Huddling insulates by lessening the exposed body surface area of the participants, thus retarding heat loss and enhancing the efficiency of thermogenesis. These physical mechanisms of the clump are actively regulated by the pups. A novel quantitative measure of huddle size revealed a form of group regulatory be— havior in rat pups whereby the surface expanded and contracted with in- creases and decreases in ambient temperature. The individual basis of this group regulatory activity was investigated by marking individual pups and ob- serving them in huddles by means of time—lapse videography. It was found that individual animals circulate through the huddle, frequently exchanging locations in the group. By studying the huddle positions of an anesthetized pup and a marked control sibling, dynamics of the pup flow were clarified. Or— dinarily. the direction of movement was actively downward, into the pile; im— mobile pups “floated” on the surface. When the nest temperature was raised to thermoneutral, the direction of pup flow reversed and an immobile animal sank to the depths of the huddle. Through individual competitive adjustments the huddle behaves as a selflregulating unit which provides warmth and insu- lation to all its active members. From birth. the rat is a member of a so— cial group. viz., the litter and mother. In— teraction between rat pups initially consists of huddling behavior. Broadly defined, Most of this research was supported by Grant MH28355AOI from the National Institute of Mental Health to the author, Experiment 1 and portions of Experiment 3 were submitted as part ot‘a doctoral dis- sertation to the faculty of Princeton University and were supported by a grant from the National Institute of Mental Health to Byron A. Campbell and a predoctoral fellowship from that agency to the author. The oxygen analyzer and laboratory space for Experiment 2 were generously made available by Henry D. Prange and David Robertshaw. Department of Physiology, Indiana University. The careful and creative assistance o1 Brad May made the metabolic experiments possible. 1 would particularly like to thank B. A. (‘ampbelf J. C. Craig. M. l, Friedman. l). -i, Howell. B. (i. lialet'. (i. l i. Mueller. l). K. Randall. and C. S. Sher-rick for their support during various phases of the research. Requests tor reprints should be \(‘Jlli to Jetirev it. Alberts. Department of Psvchoiogy. lnriiana l'niuersitv. Bloomington. lndiana 174M, purignt .o‘. ~ :. '» 'fm butternut 1: i. ,_.v;._ .i. kmw .a um. im, All name ti reproutn ‘ior. ‘:i .m huddling is the behavior that leads to the formation and maintenance of the litter ag~ gregate (Alberts, 1978) and, similarly, pro— duces the social clumps of adult rats ob— served under group—living conditions (Bar— nett, 1963; Calhoun, 1962; Steineger, 1950). Huddling is the major behavioral activity of the infant rat. Pups exhibit vigorous and persistent huddling behavior with a variety of animate and inanimate stimuli. Thermal. olfactory, photic, and several kinds of tactile cues all play a demonstrable role in the ex- pression of huddling by rat pups (Alberts, 1978; Cosnier, 196:3). There are many functions clumping might serve during early life. In the wild. rat pups are born and reared in special burrows that are defended by the mother against rats and other intruders (Calhoun. 1962). Clumping, or any behavior that confines the pups to the maternal nest. would therefore aid in pro— tection from predation and permit the dam 'i rm rewruw: i-vr , i [O to leave the nest to forage. By keeping the pups together and easy to localize during the mother’s periodic visitations, huddling may also increase the efficiency of parental in— vestments, such as nursing. In adult animals at least. huddling is widely considered to be an important behavioral adjustment to cold temperatures (Whittow, 1971). Despite the prominence of huddling in the life history of the rat and its broad phyloge— netic representation (see Whittow, 1971, 1 73). little is known about the development or the significance of the behavior. Cosnier (1965) concluded that gregariousness in in— fant rats is primarily a thermotactile re— sponse. Welker (1959) and Jeddi (1970) reached similar conclusions from their ob servations of neonatal dogs. Cosnier recog- nized the contribution of huddling to ho- meostatic functions in the fragile neonate and suggested that grouping is an important condition for survival and early development in the altricial rat. Two of the experiments reported below were designed to examine the effect of hud— dling behavior on two measures of physio- logical function in rat pups: body tempera— ture and oxygen consumption. In addition. three experiments are described which studied the behavioral dynamics of the group itself and of the individuals in the group during huddling. Experiment 1 As noted before. huddling among adult animals is frequently considered to be an adaptive social defense to cold (Whittow, 1971). Many species of animals abandon solitary habits and live in close association with conspecifics during the colder months (Hart, 1971). Huddling attenuates convec— tive heat loss by reducing the exposed sur~ face area of an animal. Moreover. in furred or feathered forms. the behavior provides each participant with a localized area of thicker insulation. In addition. huddling with other warm bodies reduces heat loss by conduction to colder surfaces. The parameters of body temperature regulation differ between immature rats and adults. For its size. the infant rat produces less and loses more body heat than does the 32 JEFFREY R. ALBERTS adult (Taylor, 1960). Thermogenesis by shivering is absent in the infant, and the limits of metabolic heat production are below that of the adult. Heat loss is rapid in pups because they lack insulative fur and subcutaneous fat and cannot exert control over vascular flow (Hull, 1973). Moreover, juveniles have a relatively greater heat—losing surface area than adults. Together, these morphological and phys— iological attributes leave the rat pup with thermoregulatory capabilities so narrow that its body temperature tends to approximate that of the environment (Hahn & Kold— ovsky, 1966). As a result, many writers have termed the infant rat “poikilothermic,” thereby likening the process of body tem- perature regulation in this small mammal to that of a reptile. The question can be raised, then, whether huddling can make a quanti— tatively significant contribution to body temperature defense to the rat pups when they lack the thermogenic and heat—con— serving capabilities of homeotherrnic adults. Experiment 1 was performed to evaluate the effect of huddling on rectal temperature in rat pups of various ages. Method Subjects. A total of 96 rat pups were tested. Pups were tested only once each. at 5, 10. 1.3. or 20 days of age. All pups were born in the Princeton [Iniversity colony, descendants of SpragueeDawley rats from the breeding population. or were derived from adult rats purchased from Camm Research, Inc. Three days after birth (Day (J), litters were uniformly reduced to eight pups each and otherwise left, undisturbed with the mother in standard plastic maternity cages. Purina Laboratory Chow and water were continuously available. Twenty'four pups were used in each age group. Procedure. Colonic temperatures were measured to the nearest .11) °(‘ with a Shulteis mercury thermomtn ter. The bulb of the thermometer was sufficiently small to be accommodated by the youngest pups and was ins serted to a depth of 10 min. The thermometer‘s rapid rise time (hence short insertion period) was advanta geous in minimizing stress~induced hyperthermic re— actions. Litters were removed from the home cage and initial rectal temperatures were recorded, l’ups were marked tor individual identification and then placed in Plexiglas compartments carpeted with home cage shavings and topped With hardware cloth. Four pups from each litter xvere noused singly ‘isoiatesi and four pups were kept together in a single compartment (huddlers a. Temper- iture measurements were made hourly on each pup for 'he next ihr. GROUP HECIJLA’I‘ORY BEHAVIOR IN DEVELOPING RATS 36L 5-DAYS-OLD — IO-DAYS—OLD " l’ 34~ L .— )— h 32* a o L r r LII 30L _ I a t :> _ a 2 I (I 28f" r to I I 0—0 Single pups a *- l- 2 I v H Huddles of 4 pups m 26>- ~ I— I ' I a l l i l l J _I — l5'DAYS‘OLD — 20-DAYS-OLD 4 I W +- _ , 0 36 ‘1— LL) 0; l I t a: g <;:; _ ‘ I 34‘- — 32?- I— 30— l I I 1“' I l l I 2 3 4 O l 2 3 4 HOURS OUT OF NEST Ot‘ Figure I. Rectal temperatures of rat pups at 24 °C in huddles of four siblings (closed circles) or alone (open circles). (The n = 1‘2 for each condition at each age.) The ambient temperature ranged from iii to 24 °C. Relative humidity was not controlled but was monitored with a hygrometer and ranged from 40% to 60%. Results and Discussion The initial colonic temperatures of the pups did not differ, but after 4 hr out of the nest, the rectal temperatures of the isolated 5-,10—, and 15—day—old pups were signifi— cantly below those of the littermates left in clumps of four (Mann-Whitney U test. two-tailed, ps = .000, .038, .006, respective— ly). The colonic temperatures of 20—day-old isolates, on the other hand. did not differ significantly from their huddling siblings after 4 hr l'p = .253). Figure 1 depicts the median rectal temperatures of the pups for each hour of the experiment. It can be seen in Figure 1 that huddling attenuated the rate of temperature loss in an age-related manner. Significant (p < .051 differences in rectal temperature between grouped and singly housed pups were found after the first hour out of the nest in the '2 and 10—day-olds. Fifteemdaywold isolates. however. did not have significantly iower 233 colonic temperatures until the third hour of the experiment. The 20—day—old pups (both the singles and huddlers) successfully de- fended their initial rectal temperatures for the entire 4—hr duration of the test period. The 15— and 20—day—old pups did not show the same dramatic body temperature de» creases as did the younger subjects. These data are entirely consistent with general descriptions of the ontogeny of thermo- regulation in altricial mammals (Barnett & Mount, 1971; Hart, 1971; McCance, 1959) and with Cosnier’s (1965) findings on surface temperature changes in isolated and grouped pups. During development, heat production ability increases, heat loss decreases with increasing size, and the insulation value of the pelage improves. The temperature challenge used here was probably not suffi— ciently severe to see a robust huddling effect in the older pups. In a pilot study (Alberts, 1973, unpublished), however, huddling in a very cold (10 °C) environment enabled 15— and 20—day—olds to defend their colonic temperatures more effectively than singleton littermates. Huddling appears to provide the rat pup with an effective behavioral means of re- ducing loss of body heat and thus combating cold challenge. It is not possible to extend interpretation of these data to more natural conditions or even to estimate the extent to which huddling can augment temperature regulation in the litter situation. The con— ditions used in this experiment were less than optimal for the pups; very small clumps were used and the insulation of the nest was eliminated. Nevertheless, even the neonates derived marked thermoregulatory benefits from huddling with small numbers of other furless, rapidly cooling siblings. Experiment 2 Rectal temperature is a useful but limited measure of temperature regulation. Al— though rectal temperature is often inter— preted as an “average" body temperature. it is not representative of the organism as a whole and remains a regional temperature measurement. Moreover. while rectal temv perature may yield information on the con— sequences of an organism‘s thermal re~ 234 sponse, it does not reflect the strategy used. Body temperature is the difference between the amounts of heat produced and heat dis— sipated. Two animals may manifest equiv— alent body temperatures, but one may be losing heat more rapidly and therefore exert a greater metabolic effort to maintain the same colonic temperature. A more direct measure of thermogenic effort is found in metabolic rate. Oxygen consumption (V02: volume of oxygen con- sumed/body weight/time) is a standard technique for determination of metabolic rate and can be used to quantify thermoge— nesis. Homeotherms increase their metabolic rate in cold temperatures; thus, their rate of VOg is lower in warm temperatures, reaching its minimum in the range defined as the zone of thermoneutrality. In true poikilotherms, however, metabolism varies directly with ambient temperature and there is no zone of thermoneutrality. Because the rectal temperature of a juve~ nile rodent is likely to decrease precipitously in a cold environment, the pup is often termed “poikilothermic” (Fairfield, 1948; Fowler & Kellogg, 1975). Taylor (1960) showed, however, that neonatal rats increase their metabolic heat production by 100% if the temperature challenge is not too severe to combat. Classifying the neonatal rat as “poikilothermic” is not accurate and can be seriously misleading (Hull, 1973). Huddling behavior has been implicated as a behavioral means of reducing metabolic expenditure in adult homeotherms. Adult mice permitted to huddle in cold environ- ments survive longer than singly housed mice (King & Connon, 1955; Sealander, 1952), presumably because huddling reduces metabolic expenditures (Howard, 1951; Pearson, 1960). Prychodko (1958) calculated that at —3 °C, the nutritive energy require— ment of a mouse in a huddle of five is re— duced by almost 3094). a metabolic response equivalent to that of raising the ambient temperature 11 °C. The present experiment investigated whether huddling could conserve metabolic energy in rat pups. It was possible that the results of the previous rectal temperature experiment told only part or the story: even the "poikilothermic" neonates. whose body JEFFREY R. ALBERTS temperatures dropped dramatically, may have been making metabolic responses not apparent from their colonic temperatures. Past research, using various measures of metabolic rate, has been inconclusive. Taylor (1960) found only meager differences in oxygen consumption by grouped and iso— lated pups, but his animals were tested at thermoneutral or very cold (10 °C) temper— atures. Cosnier (1965) reported that hud- dling reduced oxygen consumption by rat pups aged L20 days, at either 21 or 32 °C. More recently, Bryant and Hails (1975) suggested that “before homeothermy is fully developed” in mice (Mus musculus), hud— dling may actually increase oxygen con— sumption. Their measures, however, ap— peared to be confounded by movement ar- tifacts in the respirometer. The question of the metabolic role of huddling in juveniles therefore remains open. The study reported below utilized a procedure and an apparatus well suited to accurate measures of metabolic responses in neonatal rats. Method Subjects. A total of 96 Sprag’ue-Dawley pups (12 litters) were used in this experiment. The litters were born in the Indiana University colony and were derived from a line ofrats initially purchased from Laboratory Supply Inc, Indianapolis. The breeding and rearing procedures were as described in the previous experi— ment. Apparatus. The respiratory chambers were con— structed from clean commercial paint cans. These inv expensive containers are sturdy but maleable, are water tight. and with the use of stopcock grease, can be re— peatedly opened and resealed. Hardware cloth baskets (1 cm mesh) approximately 2 cm smaller than the in- ternal dimensions of the cans were constructed to pre~ vent the animals from directly contacting the walls of the chamber. Legs, .5 cm in length, prevented contact with the floor. There were four such chambers made from 1~qt. (.95-l) cans and one chamber made from a l-gal. (.004‘m3) can. Each lid was fit with two pipes (3.5 mm ID) which served for air inlet and exhaust. Air en< tered near the base of the chamber through the longer pipe and was exhausted from the shorter effluent near the ceiling. A mercury thermometer was also sealed into each chamber lid. The small. 1-qt. chambers were used to test single pups and huddles or two. Huddles 01 four and eight were run in the larger. lvgal. can. Another respiratory chamber. adapted from a 54,131. (.0‘1Am'ii commercial aquarium was fit with a Plexiglas lid and arranged in— ternally in a manner similar to the cans described above. This chamber permitted subiects to be rlirectlv ob- served. l’he results of this experiment Using the two GROUP REGULATORY BEHAVIOR IN DEVELOPING RATS Air flow Regulator Oxygen Analyzer Chart Recorder Compressed Air 235 rate measuring system Telethermometer Pump Drierite 8 Soda Lime 1 ==EOverf|ow valve Damping ] [ Chamber Water bath containing respiratory chamber(s) Figure 2. System for analysis of oxygen consumption. types of chambers were the same, so no distinction is made between them in the discussion below. The testing chambers were submerged to within 5 cm of their top in a temperaturescontrolled water bath. Air tempera- ture in the chambers was either 28 or 30 °C, as described below. The system used to measure oxygen consumption is depicted in Figure 2. A Neptune Dyna-pump drew at- mospheric air through the respiratory chambers and into a damping chamber which also served as a manifold and water trap. Total flow rate, divided among the five respiratory chambers or through the larger glass chamber, was maintained at 1.200 ml/min. Still under negative pressure, the air passed through a column of dessicant (Drierite) and C02 absorbant (soda lime). The air flow rate-measuring system consisted of a 250-ml displacement flowmeter (VoleU—Meter, Brooks Instrument Div., Emerson Electronics), a water ma- nometer, needle valves, and a source of compressed air. The calibration apparatus was connectedto the gas- analyzing system by a T valve, as shown in Figure 3. Air left the pump under positive pressure. An ad- justable overflow valve was open on-line so that a con— stant flow of air. regulated at 5 in. (12.7 cm) of water (Matheson regulator) entered an Applied Electronics Oxygen analyzer (Model S-fiA. Sunnyvale. California). accurate to 001%. In addition to a digital display of percentage of O»; entering the analyzer, the output was transcribed continuously onto a Linear instruments (lrvine, California) stereo chart recorder. The full pen excursion or" 26 cm. corresponding to 1.0% oxygen. yielded a high degree of sensitivity. A second channel on the chart recorder monitored the bath temperature by means of a Yellow Springs Lelethermometer. Procedure The entire system was calibrated at the beginning of each experimental session. Air pressure and flow rate were adjusted with the displacement tlowmeter and water manometer. After flushing the entire system with atmospheric air for 15 min, the oxygen analyzer and chart recorder were calibrated. Rat pups were weighed individually and then placed in a single. large chamber as an intact litter (n = 8). When 5—day-old huddles were tested, the pups were placed in a glass finger bowl (11 X 5 cm). Pilot data and direct observation indicated that these neonates had difficulty maintaining ...
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