BEHAVIORAL BIOLOGY 17, 495-506 (1976), Abstract No. 5285
Open-Field Behavior in Muroid Rodents 1
RICHARD C. WILSON, THOMAS VACEK, DAVID L. LANIER, and DONALD A. DEWSBURY
Department of Psychology, University of Florida, Gainesville, Florida 32611
Open-field behavior was observed in 10-rain tests of 10 adult males of each of 12 species of muroid rodents and of the two reciprocal crosses of Peromyscus leucopus and P. gossypinus. Considerable variation was found in number of squares entered, number of fecal boli deposited, and patterns of behavior displayed in the open field. Animals generally showed decreasing ambulation as tests progressed and tended to seek walls. Most measures varied significantly as a function of the general ecology of these species.
This research was conducted in order to broaden the comparative base of available information on rodent open-field behavior. The open-field technique has become a widely-used method in studies o f rodent behavior. It permits quantification o f the amount o f activity, the amount of defecation, and of the patterns of behavior emitted in a standardized test situation in a fixed period of time. The open-field method has proven useful in both physiological and developmental analyses (e.g., Candland and Campbell, 1962; Glickman, Sroges, and Hunt, 1964). It has proven particularly sensitive to genotypic differences, b o t h within species (e.g., Bruell, 1964, 1967; DeFries and Hegmann, 1970; Harrington, 1972; Southwick and Clark, 1968; Thompson, 1953) and between species (e.g., Glickman and Hartz, 1964). While open-field behavior often has been treated as a measure of "emotionality" or "exploratory drive," an alternative approach would be to treat the open field simply as an analytical tool for assessing species-typical behavioral tendencies in a relatively unstructured situation. Cross-species comparative studies o f open-field behavior have utilized relatively domesticated forms of laboratory rodents. In the decade since 1Supported by Grant BMS75-08658 from the National Science Foundation. We thank the following individuals who contributed stock for the breeding of these animals: R. H. Baker. F. Elliot, A. A. Gerall, J. Helm. E. T. Hooper, J. A. King, D. Mat.lock, N. Negus, A. Pinter, G. A. Saeher, and D. D. Thiessen; and T. Kelley for statistical consultation. Reprint requests should be sent to D. A. Dewsbury. 495 Copyright © 1976 by Academic Press, Inc. All rights of reproduction in any form reserved.
496
WILSONETAL.
Glickman and Hartz (1964) pointed to the need for systematic comparisons of relatively nondomesticated species, no such studies have appeared. What data are available on nondomesticated forms (e.g., Poley and Mos, 1974; Summerlin and Wolfe, 1974) generally refer to but one species. The present study provides systematic comparative data. Despite the wide interest in the open field behavior of the Fa generations produced by crossing inbred strains, there have been no studies of cross-species hybrids, Such data are also presented.
METHODS The subjects for this research were 140 sexually mature, male muroid rodents. There were 10 animals from each of the following 12 species: Peromyscus gossypinus (cotton mice), Peromyseus leucopus (white-footed mice), Peromyscus eremieus (cactus mice), Microtus montanus (montane voles), Microtus ochrogaster (prairie voles), Microtus pennsylvanicus (meadow voles), Microtus californicus (California voles), Seotinomys teguina, (brown mice), Meriones tristrami (Israeli gerbils), Baiomys taylori (northern pygmy mice), Mesocricetus auratus (Syrian golden hamsters), and Ototylomys phyllotis (big-eared climbing rats). In addition there were 10 males from each of the two reciprocal crosses between P. gossypinus and P. leucopus. In referring to the hybrids the species of the dam will precede that of the sire. The customary abbreviations for genera (e.g., M. tristrami) will be used. Although several genera start with identical letters, species names permit unambiguous identification. All animals, except the hamsters, were born and raised in this laboratory. The hamsters were of the Lak:LVG (Syr.)strain purchased from the Lakeview Hamster Colony, Newfield, New Jersey. All animals had been individually housed for at least 2 weeks before testing and had continuous access to food and water. Additional details concerning the taxonomy and characteristics of these species can be found in Dewsbury (1974). The open field was constructed of plywood and measured 101.6 X 101.6 X 45.7 cm. It was painted flat gray. The floor was demarcated into 25 squares of equal dimensions by painted black lines. These squares could be treated as belonging to three classes: those bounded by two walls (2W), by one wall (1W), and by no walls (OW). During testing the field was illuminated by a sin~e 25-W red light bulb suspended approximately 1.3 m above the center square. One experimenter (T. V.) counted the number of squares entered during each test by activating a microswitch connected to a bank of print-out counters. Behavioral patterns were categorized by another experimenter (R. W.) using an Esterline-Angus operations recorder. In order to minimize effects
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
497
of operating noise on the test itself, the latter machine was placed outside the testing room. Background masking noise was provided as a by-product of the activity level of other animals housed in the testing room. Each animal received one 10-min test in the open field. For purposes of data collection the test was divided into five 2-min periods. All animals were tested in the early portion of the dark phase of their reversed light-dark cycles. The open field was thoroughly washed with pine-scented detergent before each test. Tests were initiated by placing an animal in a comer square of the open field. The criterion for scoring a square entry was that an animal's two forepaws had to enter that square. The number of fecal boli was counted at the end of each test. The frequency and duration of each of the following 10 categories of behavior were recorded: Rearing-adopting a posture in which the forepaws were lifted from the ground, but not placed against a wall. Rearing at wall-adopting a posture in which the forepaws were lifted from the ground and placed against a wall. Freezing-standing still or crouching without movement. Gnawing at the open field-gnawing at exposed screws or wooden portions of the field. Scratching at field-repetitive scratching at the floor or walls with the forepaws. Jumping-leaving the ground completely by jumping movements. Locomotor-exploratory behavior-walking and running about the field. Grooming-all grooming, preening, scratching, licking, and biting of the animal's own body. Head movement-crouching or standing immobile except for head movements. Climbing-climbing up the comers of the open field, usually by using protruding screws as footholds. Although provisions were made for scoring "foot-ttmmping" (pounding the hind feet with rhythmic staccato movements as is common in gerbils and woodrats) and "rolling" (spinning the body along the long axis, Glickman and Hartz, 1964), neither behavioral pattern ever was observed.
RESULTS
Species Comparisons The mean total number of squares entered in the 10-min tests for each of the 12 species can be found in Table 1. Analysis of variance revealed a significant difference among species with respect to the total number of squares crossed, (F(11,108) = 4.02, P < 0.01. Individual comparisons using
498
WILSON ETAL. TABLE 1 Means and Standard Errors for Number of Boli and Total Number of Squares Crossed and Results of Analyses of Variance for Changes as a Function of Period 12 Species and Two Hybrids Inferential statistics on square crossings Number of Boll Mean (SE)
Number of Squares Mean(SE)
F (Period)
S. teguina P. gossypin us P. leucopus P. eremicus M. tristrami M.. californicus B. taylori M. auratus O. phyllotis M. montanus M. ochrogaster M. pennsylvanicus
0.7(0.2) 1.5(0.6) 0.8(0.4) 3.7(1.1) 1.1 (0.8) 1.1(0.5) 0.0(0.0) 1.0(0.8) 5.2(2.0) 3.1(1.9) 8.0(2.3)
648.4(129.3) 584.2(81.1) 454.0(81.2) 433.8(73.9) 430.0(19.6) 377.9(178.4) 310.6(91.9) 297.1(15.4) 275.3(80.7) 181.5(27.6) 152.9(25.7) 94.2(14.6)
0;2>0 1>0;1>2;2>0 1>0;2>0 1>0;2>0 1>0 1>0;2>0 1>0;2>0 1>0;2>0
aNewman-Keuls technique (dr = 18). *P < 0.05. **P < 0.01. Considerable variability across species is apparent. For all species, except M. auratus and M. ochrogaster, l o c o m o t o r - e x p l o r a t o r y behavior was the most prevalent pattern. Climbing was observed in just two species, P. gossypinus and P. leucopus. Coefficients o f correlation between the number of square entries and number of boli and between the amount of time spent in locomotorexploratory behavior and number of boli were obtained from the within subject sums of squares and cross-products from a multivariate one way analysis o f variance. The correlation coefficients were 0.00 and 0.06, respectively, both nonsignificant. The correlation between number of squares entered and time spent in l o c o m o t o r - e x p l o r a t o r y behavior was 0.67
(e < 0.0001). Comparisons o f Hybrids
The behavior o f the reciprocal hybrids under study can be compared to the parental species using the same measures as discussed for comparisons across species. It can be seen in Table 1 that both hybrids scored slightly below the lower scoring parent species with respect to the total number of square entries. However, analysis of variance revealed no significant differences among the four groups, /7(3, 36) = 1.32. F r o m the data in Fig. 1 and the statistics in Table 1, it can be seen that b o t h hybrids showed significant
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
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WILSONETAL.
differences in number of square entries as a function of period, with maximal levels in the first period. The distribution of entries as a function square type falls within the general range of the species reported in this study (Table 2). The number of fecal boll deposited by hybrids is shown in Table 1. Analysis of variance revealed a significant difference among the two hybrids and two parental species in number of boli, F(3, 36) = 4.20, P < 0 . 0 5 ) . Newman-Keuls analyses revealed one significant difference-the P1 X Pg hybrids deposited significantly more boll than the P. leucopus mice. Neither hybrid showed a significant correlation within genotype between number of boli and either the number of squares entered or the amount of time spent in locomotor-exploratory behavior. Data on behavioral categorizations of the hybrids appear in Table 3. In general the patterns resemble those of the parental species. Hybrids tended to spend more time freezing and less time in locomotor-exploratory activity than did the parental species. Like the parental species, the hybrids showed climbing behavior.
DISCUSSION These data reveal clear species differences among muroid rodents with respect to square entries, defecation, and behavioral patterns as measured in the open field. Most species tended to seek walls and to show decreased ambulation over time. Behavior of the species hybrids generally resembled that of the parental species. The inclusion in the sample of a previously-studied species, golden hamsters, provides a partial standard, so that the results of the present study can be compared with those of others using the same species (e.g., Glickman and Hartz, 1964; Jowaisas, 1969). Insofar as they can be compared, the different studies appear to have generated similar data. The shapes of the curves portraying changes in the number of square entries over successive 2-rain intervals are virtually identical in the present study and that of Glickman and Hartz (1964). While there were fewer entries in the latter study, the squares in Glickman and Hartz's apparatus were 50% larger than in the open field in the present study. Results obtained with the relatively nondomesticated species in the present study generally parallel those gathered on laboratory rats and other relatively domesticated forms. For example, those species which showed significant changes over time all showed decreased ambulation similar to that commonly seen in more domesticated forms (e.g., Glickman and Hartz, 1964). Like domesticated forms (e.g., Fredericson, 1953; Ross, Nagy, Kessler, and Scott, 1966) these animals generally tended to enter squares bounded by walls relatively more frequently than those without walls. Domestication appears to have produced minimal alterations in open field behavior (cf. Lockard, 1968).
OPEN-FIELD BEHAVIORIN MUROID RODENTS
503
Data on body length, excluding tail, from Hall and Kelson (1959) and from measurements of M. tristrami and M. auratus in our laboratory were examined to search for a possible relationship between body length and square entries. No consistent relationship was found. For example, the smallest species, B. taylori and the four largest, M. tristrami, 34. californicus, M. auratus, and O. phyllotis, all were clustered at the middle of the distribution of square entries. The species with the most entries, S. teguina, was the second smallest. In his classical work on open field behavior, Hall (1934; 1936) proposed: (a) that there is an inverse correlation between amount of defecation and ambulation and (b)that both are indicants of "emotionality." The questions of the reliability of the proposed inverse relationship and the validity of these measures as indicants of "emotionality" have caused much controversy (see Tobach and Schneirla, 1962; Pare, 1964; DeFries and Hegmann, 1970; Archer, 1973). While the present data do not bear on the issue of "emotionality," they can be related to the proposed inverse correlation; no such relationship was found. While any generalizations must be limited by the recognition of the many factors that can act to produce negative results, these data do not indicate any significant relationship between the number of square entries and number of boli deposited when examined across species under the present conditions. A primary advantage to work with a variety of relatively nondomesticated species lies in the potential for uncovering ecological correlates of open-field behavior (Glickman and Hartz, 1964; Dewsbury, 1973). The species studied in the present research can be considered as falling into three general ecological groups which vary with respect to characteristics such as food and habitat preferences (e.g., Baker, 1971). P. leucopus, t 9. gossypinus, and O. phyllotis all are semiarboreal species whose diets consist primarily of seeds, fruit, and plants. M. tristrami, M. auratus, and P. eremicus are primarily desert dewellers. The four Microtus species and probably B. taylori are field dwellers which eat mainly green vegetable matter, such as grasses, and tend to build runways under tall grass. S. teguina is difficult to classify. While it tends to dwell in fields and make runways, it is quite insectivorous and primarily diurnal (Hooper, 1972). Analyses of variance for nested designs were used on data from the 11 classified species to examine possible effects of ecological grouping on open-field behavior. Data analyzed included the total number of square entries, the number of boli, the percentage of entries that were into the OW squares, and the amount of time spent in each of the 10 behavioral categories shown in Table 3. The results are presented in Table 4. Each of the 13 variables showed significant variation as a function of ecological grouping. Many individual comparisons, evaluated with t tests, were significant. Field-dwelling species displayed the fewest square entries. This result appears consistent with observations of activity in the natural habitat.
504
WILSON E T A L . TABLE 4 Means and Inferential Statistics for Various Behavioral Measures as a Function of Ecological Groupings Mean
Measure
Arboreal (A)a
Total square entries Boli Entries OW squares (%) Reard Rear at walld Freezed Gnaw fieldd Scratch fieldd Jumpd Loco.--explored Groomd Head moved Climbb
437.8 1.9 30.2 19.2 104.2 29.8 5.8 0.0 23.4 343.0 59.3 70.6 2.7
Desert (B)b
Field (C)c
F
A vs. B A vs. C
387.0 223.4 8.23*** 0.88 1.5 3.7 3.66* 0.68 18.1 21.0 10.59"** 4.56*** 38.3 6.1 19.02"** 2.34* 156.0 62.5 47.58*** 2.63* 17.1 49.9 3.42* 1.18 25.0 8.8 24.24*** 5.39*** 0.5 0.0 6.19"* 2.19" 2.2 0.3 17.09"** 3.13"* 3 1 0 . 1 248.5 8.94*** 1.13 49.8 145.4 27.42*** 0.96 4.7 52.6 13.38"** 3.24** 0.0 0.0 5.27** 1.85
3.20** 1.62 2.98* 2.54* 3.72*** 1.36 1.16 0.00 4.41"** 3.27** 4.43*** 0.97 2.40**
B vs. C 2.80*** 1.99 1.01 7.64*** 6.32*** 2.42* 5.38*** 2.84* 3.09** 2.26* 5.11"** 4.75*** 0.00
alncludes 1'. gossypinus, P. leucopus, and O. phyllotis. bIncludes M. auratus, M. tristrami, and P. eremicus. CIncludes M. californicus, M. montanus, M. ochrogaster, M. pennsylvanicus, and B. taylori.
dmeasured in sec. *P < 0.05. **P < 0.01. ***P < 0.001. "Grass-eaters have smaller home r a n g e s . . , and may take less risk (that is, less exposure outside of grassy, overhead cover) in obtaining food along their runways than seed-eaters of similar size that need to move over larger areas in search of scattered, seed-bearing plants" (Baker, 1971, p. 802). Rearing and rearing at the walls were especially frequent in desert dwellers and infrequent in field dwellers. The reason for these presumed evolutionary divergences may lie in the utility of the rearing response in increasing the field of view in the natural habitat. While rearing would improve the field of view in the desert, it would provide no such advantage for species inhabiting runways in a thick cover of tall grass. Arboreal species showed the greatest amounts of jumping, locomotorexploratory behavior, standing still with head movements, and climbing, and the highest percentage of entries into OW squares. Desert dwellers displayed the most gnawing and scratching of the field; field dwellers showed the most boli, freezing, and grooming. Seven of the species from the present research also were included in a
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
505
comparative study of food hoarding reported by Lanier, Estep, and Dewsbury (1974). M. auratus and the three Microtus species studied were the best hoarders under the conditions of the Lanier et al. study. A cross-species correlation coefficient for these seven species between number of pellets hoarded in the predeprivation condition (Lanier et al., 1974) and percentage of time in locomotor-exploratory behavior in the present study revealed a significant inverse relationship, r ( 5 ) = - 0 . 8 5 , P < 0.05, 2-tailed. Perhaps the same ecological factors that facilitate the evolution of food hoarding patterns, such as predator pressure (see Ewer, 1968), are responsible for the evolution of tendencies for restricted locomotor-exploratory activity. The correlations between amount hoarded and the number of square entries (-0.57) and the number of boli (-0.06) were not significant, r(5) 0.05 = 0.75. The relationships found between open field patterns and characteristics such as food preferences and hoarding behavior suggest that species-typical activity patterns may be partially a function of the type of food eaten and the foraging pattern appropriate to that food type. Behavioral patterns of the cross-species reciprocal hybrids generally resembled those of the parental species. Interestingly, P. leucopus, P. gossypinus, and their two hybrids were the only animals to show climbing in the open field. REFERENCES Archer, J. (1973). Tests for emotionality in rats and mice: A review. Anita. Behav. 21, 205-235. Baker, R. H. (1971). Nutritional strategies of myomorph rodents in North American grasslands. J. Mammal. 52, 800-805. Bruell, J. H. (1964). Inheritance of behavioral and physiological characters of mice and the problem of heterosis. Amer. Zool. 4, 125-138. Bruell, J. H. (1967). Behavioral heterosis. In J. Hirsch (Ed.), "Behavior-Genetic Analysis." New York: McGraw-Hill. Candland, D. K., and Campbell, B. A. (1962). Development of fear in the rat as measured by behavior in the open field. J. Comp. Physiol. Psychol. 55,593-596. DeFiles, J. C., and Hegmann, J. P. (1970). Genetic analysis of open field behavior. In G. Lindzey, D. D. Thiessen (Eds.), "Contributions to Behavior-Genetic Analysis-The Mouse as a Prototype," New York: Appleton-Century-Crofts. Dewsbury, D. A. (1973). Comparative psychologists and their quest for uniformity. Ann. iV. Y. Acad. ScL 223, 147-167. Dewsbury, D. A. (1974). The use of muroid rodents in the psychology laboratory. Behav. Res. Meth. Instr. 6, 301-308. Ewer, R. F. (1968). "Ethology of Mammals," New York: Plenum. Frederieson, E. (1953). The wall-seeking tendency in three inbred mouse strains (Mus musculus). J. Genet. Psychol. 82, 143-146. Glickman, S. E., and Hartz, K. E. (1964). Exploratory behavior in several species of rodents. J. Comp. Physiol. Psychol. 58, 101-104. Glickman, S. E., Sroges, R. W., and Hunt, J. (1964). Brain lesions and locomotor exploration in the albino rat. J. Comp. Physiol. Psychol. 58, 93-100.
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Hall, C. S. (1934). Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Cornp. Psychol. 18, 385-403. Hall, C. S. (1936). Emotional behavior in the rat. III. The relationship between emotionality and ambulatory behavior. J. Comp. Psychol. 22, 345-352. Hall, E. R., and Kelson, K. R. (1959). "The Mammals of North America." New York: Ronald Press. Harrington, G. M. (1972). Strain differences in open-field behavior of the rat. Psychon. ScL 27, 51-53. Hooper, E. T. (1972). A synopsis of the rodent genus Scotinomys. Occ. Pap. Mus. Zool. Univ. Mich. 665, 32 pp. Jowaisas, D. (1969). Changes in the open field behavior of female golden hamsters. Psychon. Sci. 14, 126-127. Lanier, D. L., Estep, D. Q., and Dewsbury, D. A. (1974). Food hoarding in muroid rodents. Behav. Biol. 11, 177-187. Lockard, R. B. (1968). The albino rat: A defensible choice or a bad habit? Amer. Psychol. 23, 734-742. Pare, W. P. (1964). Relationship of various behaviors in the open-field test of emotionality. Psychol. Rep. 14, 19-22. Poley, W. and Mos, L. (1974). Emotionality and alcohol selection in deer mice (Peromyscus maniculatus). Quart. J. Stud. Alc. 35, 59-65. Ross, S., Nagy, Z. M., Kessler, C., and Scott, J. P. (1966). Effects of illumination on wall-leaving behavior and activity in three inbred mouse strains. J. Comp. Physiol. Psychol. 62, 338-340. Southwick, C. H., and Clark, L. (1968). Interstrain differences in aggressive behavior and exploratory activity of inbred mice. Commun. Behav. Biol. 1, 49-59. Summerlin, C. T., and Wolfe, J. L. (1971). Social influences on exploratory behavior in the cotton rat, Sigmodon hispidus. Cornmun. Behav. Biol. 6, 105-109. Thompson, W. R. (1953). The inheritance of'behavior: Behavioral differences in fifteen mouse strains. Canad. J. Psychol. 7, 145-155. Tobach, E., and Schneirla, T. C. (1962). Eliminative responses in mice and rats and the problem of "emotionality." In E. L. Bliss (Ed.), "Roots of Behavior." New York: Harper & Brothers. Wirier, B. J. (1962). "Statistical Principles in Experimental Design." New York: McGrawHill.
Open-Field Behavior in Muroid Rodents 1
RICHARD C. WILSON, THOMAS VACEK, DAVID L. LANIER, and DONALD A. DEWSBURY
Department of Psychology, University of Florida, Gainesville, Florida 32611
Open-field behavior was observed in 10-rain tests of 10 adult males of each of 12 species of muroid rodents and of the two reciprocal crosses of Peromyscus leucopus and P. gossypinus. Considerable variation was found in number of squares entered, number of fecal boli deposited, and patterns of behavior displayed in the open field. Animals generally showed decreasing ambulation as tests progressed and tended to seek walls. Most measures varied significantly as a function of the general ecology of these species.
This research was conducted in order to broaden the comparative base of available information on rodent open-field behavior. The open-field technique has become a widely-used method in studies o f rodent behavior. It permits quantification o f the amount o f activity, the amount of defecation, and of the patterns of behavior emitted in a standardized test situation in a fixed period of time. The open-field method has proven useful in both physiological and developmental analyses (e.g., Candland and Campbell, 1962; Glickman, Sroges, and Hunt, 1964). It has proven particularly sensitive to genotypic differences, b o t h within species (e.g., Bruell, 1964, 1967; DeFries and Hegmann, 1970; Harrington, 1972; Southwick and Clark, 1968; Thompson, 1953) and between species (e.g., Glickman and Hartz, 1964). While open-field behavior often has been treated as a measure of "emotionality" or "exploratory drive," an alternative approach would be to treat the open field simply as an analytical tool for assessing species-typical behavioral tendencies in a relatively unstructured situation. Cross-species comparative studies o f open-field behavior have utilized relatively domesticated forms of laboratory rodents. In the decade since 1Supported by Grant BMS75-08658 from the National Science Foundation. We thank the following individuals who contributed stock for the breeding of these animals: R. H. Baker. F. Elliot, A. A. Gerall, J. Helm. E. T. Hooper, J. A. King, D. Mat.lock, N. Negus, A. Pinter, G. A. Saeher, and D. D. Thiessen; and T. Kelley for statistical consultation. Reprint requests should be sent to D. A. Dewsbury. 495 Copyright © 1976 by Academic Press, Inc. All rights of reproduction in any form reserved.
496
WILSONETAL.
Glickman and Hartz (1964) pointed to the need for systematic comparisons of relatively nondomesticated species, no such studies have appeared. What data are available on nondomesticated forms (e.g., Poley and Mos, 1974; Summerlin and Wolfe, 1974) generally refer to but one species. The present study provides systematic comparative data. Despite the wide interest in the open field behavior of the Fa generations produced by crossing inbred strains, there have been no studies of cross-species hybrids, Such data are also presented.
METHODS The subjects for this research were 140 sexually mature, male muroid rodents. There were 10 animals from each of the following 12 species: Peromyscus gossypinus (cotton mice), Peromyseus leucopus (white-footed mice), Peromyscus eremieus (cactus mice), Microtus montanus (montane voles), Microtus ochrogaster (prairie voles), Microtus pennsylvanicus (meadow voles), Microtus californicus (California voles), Seotinomys teguina, (brown mice), Meriones tristrami (Israeli gerbils), Baiomys taylori (northern pygmy mice), Mesocricetus auratus (Syrian golden hamsters), and Ototylomys phyllotis (big-eared climbing rats). In addition there were 10 males from each of the two reciprocal crosses between P. gossypinus and P. leucopus. In referring to the hybrids the species of the dam will precede that of the sire. The customary abbreviations for genera (e.g., M. tristrami) will be used. Although several genera start with identical letters, species names permit unambiguous identification. All animals, except the hamsters, were born and raised in this laboratory. The hamsters were of the Lak:LVG (Syr.)strain purchased from the Lakeview Hamster Colony, Newfield, New Jersey. All animals had been individually housed for at least 2 weeks before testing and had continuous access to food and water. Additional details concerning the taxonomy and characteristics of these species can be found in Dewsbury (1974). The open field was constructed of plywood and measured 101.6 X 101.6 X 45.7 cm. It was painted flat gray. The floor was demarcated into 25 squares of equal dimensions by painted black lines. These squares could be treated as belonging to three classes: those bounded by two walls (2W), by one wall (1W), and by no walls (OW). During testing the field was illuminated by a sin~e 25-W red light bulb suspended approximately 1.3 m above the center square. One experimenter (T. V.) counted the number of squares entered during each test by activating a microswitch connected to a bank of print-out counters. Behavioral patterns were categorized by another experimenter (R. W.) using an Esterline-Angus operations recorder. In order to minimize effects
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
497
of operating noise on the test itself, the latter machine was placed outside the testing room. Background masking noise was provided as a by-product of the activity level of other animals housed in the testing room. Each animal received one 10-min test in the open field. For purposes of data collection the test was divided into five 2-min periods. All animals were tested in the early portion of the dark phase of their reversed light-dark cycles. The open field was thoroughly washed with pine-scented detergent before each test. Tests were initiated by placing an animal in a comer square of the open field. The criterion for scoring a square entry was that an animal's two forepaws had to enter that square. The number of fecal boli was counted at the end of each test. The frequency and duration of each of the following 10 categories of behavior were recorded: Rearing-adopting a posture in which the forepaws were lifted from the ground, but not placed against a wall. Rearing at wall-adopting a posture in which the forepaws were lifted from the ground and placed against a wall. Freezing-standing still or crouching without movement. Gnawing at the open field-gnawing at exposed screws or wooden portions of the field. Scratching at field-repetitive scratching at the floor or walls with the forepaws. Jumping-leaving the ground completely by jumping movements. Locomotor-exploratory behavior-walking and running about the field. Grooming-all grooming, preening, scratching, licking, and biting of the animal's own body. Head movement-crouching or standing immobile except for head movements. Climbing-climbing up the comers of the open field, usually by using protruding screws as footholds. Although provisions were made for scoring "foot-ttmmping" (pounding the hind feet with rhythmic staccato movements as is common in gerbils and woodrats) and "rolling" (spinning the body along the long axis, Glickman and Hartz, 1964), neither behavioral pattern ever was observed.
RESULTS
Species Comparisons The mean total number of squares entered in the 10-min tests for each of the 12 species can be found in Table 1. Analysis of variance revealed a significant difference among species with respect to the total number of squares crossed, (F(11,108) = 4.02, P < 0.01. Individual comparisons using
498
WILSON ETAL. TABLE 1 Means and Standard Errors for Number of Boli and Total Number of Squares Crossed and Results of Analyses of Variance for Changes as a Function of Period 12 Species and Two Hybrids Inferential statistics on square crossings Number of Boll Mean (SE)
Number of Squares Mean(SE)
F (Period)
S. teguina P. gossypin us P. leucopus P. eremicus M. tristrami M.. californicus B. taylori M. auratus O. phyllotis M. montanus M. ochrogaster M. pennsylvanicus
0.7(0.2) 1.5(0.6) 0.8(0.4) 3.7(1.1) 1.1 (0.8) 1.1(0.5) 0.0(0.0) 1.0(0.8) 5.2(2.0) 3.1(1.9) 8.0(2.3)
648.4(129.3) 584.2(81.1) 454.0(81.2) 433.8(73.9) 430.0(19.6) 377.9(178.4) 310.6(91.9) 297.1(15.4) 275.3(80.7) 181.5(27.6) 152.9(25.7) 94.2(14.6)
0;2>0 1>0;1>2;2>0 1>0;2>0 1>0;2>0 1>0 1>0;2>0 1>0;2>0 1>0;2>0
aNewman-Keuls technique (dr = 18). *P < 0.05. **P < 0.01. Considerable variability across species is apparent. For all species, except M. auratus and M. ochrogaster, l o c o m o t o r - e x p l o r a t o r y behavior was the most prevalent pattern. Climbing was observed in just two species, P. gossypinus and P. leucopus. Coefficients o f correlation between the number of square entries and number of boli and between the amount of time spent in locomotorexploratory behavior and number of boli were obtained from the within subject sums of squares and cross-products from a multivariate one way analysis o f variance. The correlation coefficients were 0.00 and 0.06, respectively, both nonsignificant. The correlation between number of squares entered and time spent in l o c o m o t o r - e x p l o r a t o r y behavior was 0.67
(e < 0.0001). Comparisons o f Hybrids
The behavior o f the reciprocal hybrids under study can be compared to the parental species using the same measures as discussed for comparisons across species. It can be seen in Table 1 that both hybrids scored slightly below the lower scoring parent species with respect to the total number of square entries. However, analysis of variance revealed no significant differences among the four groups, /7(3, 36) = 1.32. F r o m the data in Fig. 1 and the statistics in Table 1, it can be seen that b o t h hybrids showed significant
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
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differences in number of square entries as a function of period, with maximal levels in the first period. The distribution of entries as a function square type falls within the general range of the species reported in this study (Table 2). The number of fecal boll deposited by hybrids is shown in Table 1. Analysis of variance revealed a significant difference among the two hybrids and two parental species in number of boli, F(3, 36) = 4.20, P < 0 . 0 5 ) . Newman-Keuls analyses revealed one significant difference-the P1 X Pg hybrids deposited significantly more boll than the P. leucopus mice. Neither hybrid showed a significant correlation within genotype between number of boli and either the number of squares entered or the amount of time spent in locomotor-exploratory behavior. Data on behavioral categorizations of the hybrids appear in Table 3. In general the patterns resemble those of the parental species. Hybrids tended to spend more time freezing and less time in locomotor-exploratory activity than did the parental species. Like the parental species, the hybrids showed climbing behavior.
DISCUSSION These data reveal clear species differences among muroid rodents with respect to square entries, defecation, and behavioral patterns as measured in the open field. Most species tended to seek walls and to show decreased ambulation over time. Behavior of the species hybrids generally resembled that of the parental species. The inclusion in the sample of a previously-studied species, golden hamsters, provides a partial standard, so that the results of the present study can be compared with those of others using the same species (e.g., Glickman and Hartz, 1964; Jowaisas, 1969). Insofar as they can be compared, the different studies appear to have generated similar data. The shapes of the curves portraying changes in the number of square entries over successive 2-rain intervals are virtually identical in the present study and that of Glickman and Hartz (1964). While there were fewer entries in the latter study, the squares in Glickman and Hartz's apparatus were 50% larger than in the open field in the present study. Results obtained with the relatively nondomesticated species in the present study generally parallel those gathered on laboratory rats and other relatively domesticated forms. For example, those species which showed significant changes over time all showed decreased ambulation similar to that commonly seen in more domesticated forms (e.g., Glickman and Hartz, 1964). Like domesticated forms (e.g., Fredericson, 1953; Ross, Nagy, Kessler, and Scott, 1966) these animals generally tended to enter squares bounded by walls relatively more frequently than those without walls. Domestication appears to have produced minimal alterations in open field behavior (cf. Lockard, 1968).
OPEN-FIELD BEHAVIORIN MUROID RODENTS
503
Data on body length, excluding tail, from Hall and Kelson (1959) and from measurements of M. tristrami and M. auratus in our laboratory were examined to search for a possible relationship between body length and square entries. No consistent relationship was found. For example, the smallest species, B. taylori and the four largest, M. tristrami, 34. californicus, M. auratus, and O. phyllotis, all were clustered at the middle of the distribution of square entries. The species with the most entries, S. teguina, was the second smallest. In his classical work on open field behavior, Hall (1934; 1936) proposed: (a) that there is an inverse correlation between amount of defecation and ambulation and (b)that both are indicants of "emotionality." The questions of the reliability of the proposed inverse relationship and the validity of these measures as indicants of "emotionality" have caused much controversy (see Tobach and Schneirla, 1962; Pare, 1964; DeFries and Hegmann, 1970; Archer, 1973). While the present data do not bear on the issue of "emotionality," they can be related to the proposed inverse correlation; no such relationship was found. While any generalizations must be limited by the recognition of the many factors that can act to produce negative results, these data do not indicate any significant relationship between the number of square entries and number of boli deposited when examined across species under the present conditions. A primary advantage to work with a variety of relatively nondomesticated species lies in the potential for uncovering ecological correlates of open-field behavior (Glickman and Hartz, 1964; Dewsbury, 1973). The species studied in the present research can be considered as falling into three general ecological groups which vary with respect to characteristics such as food and habitat preferences (e.g., Baker, 1971). P. leucopus, t 9. gossypinus, and O. phyllotis all are semiarboreal species whose diets consist primarily of seeds, fruit, and plants. M. tristrami, M. auratus, and P. eremicus are primarily desert dewellers. The four Microtus species and probably B. taylori are field dwellers which eat mainly green vegetable matter, such as grasses, and tend to build runways under tall grass. S. teguina is difficult to classify. While it tends to dwell in fields and make runways, it is quite insectivorous and primarily diurnal (Hooper, 1972). Analyses of variance for nested designs were used on data from the 11 classified species to examine possible effects of ecological grouping on open-field behavior. Data analyzed included the total number of square entries, the number of boli, the percentage of entries that were into the OW squares, and the amount of time spent in each of the 10 behavioral categories shown in Table 3. The results are presented in Table 4. Each of the 13 variables showed significant variation as a function of ecological grouping. Many individual comparisons, evaluated with t tests, were significant. Field-dwelling species displayed the fewest square entries. This result appears consistent with observations of activity in the natural habitat.
504
WILSON E T A L . TABLE 4 Means and Inferential Statistics for Various Behavioral Measures as a Function of Ecological Groupings Mean
Measure
Arboreal (A)a
Total square entries Boli Entries OW squares (%) Reard Rear at walld Freezed Gnaw fieldd Scratch fieldd Jumpd Loco.--explored Groomd Head moved Climbb
437.8 1.9 30.2 19.2 104.2 29.8 5.8 0.0 23.4 343.0 59.3 70.6 2.7
Desert (B)b
Field (C)c
F
A vs. B A vs. C
387.0 223.4 8.23*** 0.88 1.5 3.7 3.66* 0.68 18.1 21.0 10.59"** 4.56*** 38.3 6.1 19.02"** 2.34* 156.0 62.5 47.58*** 2.63* 17.1 49.9 3.42* 1.18 25.0 8.8 24.24*** 5.39*** 0.5 0.0 6.19"* 2.19" 2.2 0.3 17.09"** 3.13"* 3 1 0 . 1 248.5 8.94*** 1.13 49.8 145.4 27.42*** 0.96 4.7 52.6 13.38"** 3.24** 0.0 0.0 5.27** 1.85
3.20** 1.62 2.98* 2.54* 3.72*** 1.36 1.16 0.00 4.41"** 3.27** 4.43*** 0.97 2.40**
B vs. C 2.80*** 1.99 1.01 7.64*** 6.32*** 2.42* 5.38*** 2.84* 3.09** 2.26* 5.11"** 4.75*** 0.00
alncludes 1'. gossypinus, P. leucopus, and O. phyllotis. bIncludes M. auratus, M. tristrami, and P. eremicus. CIncludes M. californicus, M. montanus, M. ochrogaster, M. pennsylvanicus, and B. taylori.
dmeasured in sec. *P < 0.05. **P < 0.01. ***P < 0.001. "Grass-eaters have smaller home r a n g e s . . , and may take less risk (that is, less exposure outside of grassy, overhead cover) in obtaining food along their runways than seed-eaters of similar size that need to move over larger areas in search of scattered, seed-bearing plants" (Baker, 1971, p. 802). Rearing and rearing at the walls were especially frequent in desert dwellers and infrequent in field dwellers. The reason for these presumed evolutionary divergences may lie in the utility of the rearing response in increasing the field of view in the natural habitat. While rearing would improve the field of view in the desert, it would provide no such advantage for species inhabiting runways in a thick cover of tall grass. Arboreal species showed the greatest amounts of jumping, locomotorexploratory behavior, standing still with head movements, and climbing, and the highest percentage of entries into OW squares. Desert dwellers displayed the most gnawing and scratching of the field; field dwellers showed the most boli, freezing, and grooming. Seven of the species from the present research also were included in a
OPEN-FIELD BEHAVIOR IN MUROID RODENTS
505
comparative study of food hoarding reported by Lanier, Estep, and Dewsbury (1974). M. auratus and the three Microtus species studied were the best hoarders under the conditions of the Lanier et al. study. A cross-species correlation coefficient for these seven species between number of pellets hoarded in the predeprivation condition (Lanier et al., 1974) and percentage of time in locomotor-exploratory behavior in the present study revealed a significant inverse relationship, r ( 5 ) = - 0 . 8 5 , P < 0.05, 2-tailed. Perhaps the same ecological factors that facilitate the evolution of food hoarding patterns, such as predator pressure (see Ewer, 1968), are responsible for the evolution of tendencies for restricted locomotor-exploratory activity. The correlations between amount hoarded and the number of square entries (-0.57) and the number of boli (-0.06) were not significant, r(5) 0.05 = 0.75. The relationships found between open field patterns and characteristics such as food preferences and hoarding behavior suggest that species-typical activity patterns may be partially a function of the type of food eaten and the foraging pattern appropriate to that food type. Behavioral patterns of the cross-species reciprocal hybrids generally resembled those of the parental species. Interestingly, P. leucopus, P. gossypinus, and their two hybrids were the only animals to show climbing in the open field. REFERENCES Archer, J. (1973). Tests for emotionality in rats and mice: A review. Anita. Behav. 21, 205-235. Baker, R. H. (1971). Nutritional strategies of myomorph rodents in North American grasslands. J. Mammal. 52, 800-805. Bruell, J. H. (1964). Inheritance of behavioral and physiological characters of mice and the problem of heterosis. Amer. Zool. 4, 125-138. Bruell, J. H. (1967). Behavioral heterosis. In J. Hirsch (Ed.), "Behavior-Genetic Analysis." New York: McGraw-Hill. Candland, D. K., and Campbell, B. A. (1962). Development of fear in the rat as measured by behavior in the open field. J. Comp. Physiol. Psychol. 55,593-596. DeFiles, J. C., and Hegmann, J. P. (1970). Genetic analysis of open field behavior. In G. Lindzey, D. D. Thiessen (Eds.), "Contributions to Behavior-Genetic Analysis-The Mouse as a Prototype," New York: Appleton-Century-Crofts. Dewsbury, D. A. (1973). Comparative psychologists and their quest for uniformity. Ann. iV. Y. Acad. ScL 223, 147-167. Dewsbury, D. A. (1974). The use of muroid rodents in the psychology laboratory. Behav. Res. Meth. Instr. 6, 301-308. Ewer, R. F. (1968). "Ethology of Mammals," New York: Plenum. Frederieson, E. (1953). The wall-seeking tendency in three inbred mouse strains (Mus musculus). J. Genet. Psychol. 82, 143-146. Glickman, S. E., and Hartz, K. E. (1964). Exploratory behavior in several species of rodents. J. Comp. Physiol. Psychol. 58, 101-104. Glickman, S. E., Sroges, R. W., and Hunt, J. (1964). Brain lesions and locomotor exploration in the albino rat. J. Comp. Physiol. Psychol. 58, 93-100.
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Hall, C. S. (1934). Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Cornp. Psychol. 18, 385-403. Hall, C. S. (1936). Emotional behavior in the rat. III. The relationship between emotionality and ambulatory behavior. J. Comp. Psychol. 22, 345-352. Hall, E. R., and Kelson, K. R. (1959). "The Mammals of North America." New York: Ronald Press. Harrington, G. M. (1972). Strain differences in open-field behavior of the rat. Psychon. ScL 27, 51-53. Hooper, E. T. (1972). A synopsis of the rodent genus Scotinomys. Occ. Pap. Mus. Zool. Univ. Mich. 665, 32 pp. Jowaisas, D. (1969). Changes in the open field behavior of female golden hamsters. Psychon. Sci. 14, 126-127. Lanier, D. L., Estep, D. Q., and Dewsbury, D. A. (1974). Food hoarding in muroid rodents. Behav. Biol. 11, 177-187. Lockard, R. B. (1968). The albino rat: A defensible choice or a bad habit? Amer. Psychol. 23, 734-742. Pare, W. P. (1964). Relationship of various behaviors in the open-field test of emotionality. Psychol. Rep. 14, 19-22. Poley, W. and Mos, L. (1974). Emotionality and alcohol selection in deer mice (Peromyscus maniculatus). Quart. J. Stud. Alc. 35, 59-65. Ross, S., Nagy, Z. M., Kessler, C., and Scott, J. P. (1966). Effects of illumination on wall-leaving behavior and activity in three inbred mouse strains. J. Comp. Physiol. Psychol. 62, 338-340. Southwick, C. H., and Clark, L. (1968). Interstrain differences in aggressive behavior and exploratory activity of inbred mice. Commun. Behav. Biol. 1, 49-59. Summerlin, C. T., and Wolfe, J. L. (1971). Social influences on exploratory behavior in the cotton rat, Sigmodon hispidus. Cornmun. Behav. Biol. 6, 105-109. Thompson, W. R. (1953). The inheritance of'behavior: Behavioral differences in fifteen mouse strains. Canad. J. Psychol. 7, 145-155. Tobach, E., and Schneirla, T. C. (1962). Eliminative responses in mice and rats and the problem of "emotionality." In E. L. Bliss (Ed.), "Roots of Behavior." New York: Harper & Brothers. Wirier, B. J. (1962). "Statistical Principles in Experimental Design." New York: McGrawHill.
