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Illumination preference and visual orientation of wild-reared mice, Peromyscus leucopus
Anim. Behav., 1982, 30, 339-344 ILLUMINATION PREFERENCE AND VISUAL ORIENTATION WILD-REARED MICE, PEROMYSCUS LEUCOPUS
OF
BY RONALD E. BARRY, Jr.* & EDWARD N. FRANCQ
Department of Zoology, The University of New Hampshire, Durham, NH 03824 Abstract. A two-phase study was conducted with Peromyscus leucopus noveboracensis.; In the field, frequency of captures was examined relative to nocturnal cloud co~,er and moon visibility. No relationships were apparent. In the laboratory, preferences of wild-reared mice for opposing visual cues under contrasting levels of illuminance were studied. Mice preferred an illumination equivalent to that striking a field on a clear, moonlit night (0.020 foot-candle) to the average of that striking the forest floor on a cloudy, moonlit night (0.005 foot-candle). At the lower intensity, mice showed no preference between two identical boxes placed vertically or horizontally. At the higher level of illuminance, there was a preference for the horizontal box, suggesting a tendency to orient toward horizontal objects over vertical ones at certain light levels. Higher natural nocturnal illuminance is not avoided (and may actually be preferred) by P. leucopus. Vision may be an important sensory modality in orientation and navigation under these conditions. moonlit night (Kavanau (1967), (1968), (1969a,b); Kavanau & Havenhill (1976) for P. maniculatus, P. crinitus, P, leucopus, and P . californicus). Based on these accounts, and reports that Peromyscus possesses the best visual acuity of any rodent tested thus far (Vestal 1970, 1973; King & Vestal 1974), we hypothesized that P. leucopus noveboracensis would be more active on brighter (clear, moonlit) nights than on darker (cloudy, moonlit) nights. We also hypothesized that mice preferred an illumination roughly equivalent to that striking the substrate on a clear, full-moonlit night to one perceptibly less intense. In addition, we hypothesized that the use of vision in habitat orientation and navigation requires high nocturnal illumination. Investigations of this sort are important in establishing bases for activity, movements, and habitat selection and utilization in small mammals. Methods Field Study The field study was p a r t of a larger project conducted in two woodlots, termed east and west sampling areas, in Stratford County, New Hampshire. The live-trapping period was June 7 through September 17, 1976. Traps were open a total of 5150 trap-nights and relevant data were gathered on 136 captures. Sampling and studysite details are described elsewhere (Barry & Francq 1980). Phases of the moon for evenings of the trapping period were recorded as new, first quarter, full, Or third quarter. Percentage 0f sky Cover, recorded at Pease Air Force Base about 5 miles from the study site, was obtained from the National Weather Service in Ashevi!le, North
The amount of available light may be a major factor in determining activity of Peromyscus. Although this genus is nocturnal (Johnson 1926; Svihla 1932; Behney 1936; Burt 1940; Getz 1959), species appear to be most active during relatively bright portions of the night. Both Svihla and Burt suggested an activity peak around dusk. Behney found peak exploration at about one hour after sunset. However, there are conflicting conclusions on the illumination preferences of various species of Peromyscus, and there are probably speciesspecific preferences related to the nature of the preferred habitat, predator-prey relationships, the capabilities of the sensory apparatus, and so on. Most conclusions have been drawn on the basis of observations or capture under various sky and moon conditions. Greater activity has been observed on cloudy and/or moonless nights by a number of investigators (Johnson 1926; Butt 1940; Provost 1940; Blair 1943, 1951; Gentry & Odum 1957; Hirth 1959; Owings & Lockard 1971). On the other hand, others have found either no relationship between activity of certain peromyscines and sky and/or moon condition (Hays 1958; Orr 1959), or enhancement of activity by the presence of lunar illumination (Owings & Lockard 1971; Marten 1973). Also, under controlled conditions, several species have been shown to either avoid darkness (Moody 1929 for P. maniculatus gracilis; Brant & Kavanau 1965 for P. crinitus) or exhibit decreased activities at light levels below that striking the earth's surface on a clear, full*Present address: Center of Environmental Science, Unity College, Unity, ME 04988. Address reprint requests to R.E.B. 339
340
ANIMAL
BEHAVIOUR,
Carolina. Sky conditions were classified as clear, partly cloudy, and cloudy. Sky cover was recorded from 1800 to 0600 hours EST according to the following criteria; dear: an average of less than 50 70 sky cover for the recording period, with at least one hourly recording o f zero cover and no recording of 10070 cover; cloudy: an average o f greater than 50 7o sky cover for the recording period with at least one hourly recording o f 100~o cover and no recording of zero cover, partly cloudy: anything intermediate to clear and cloudy conditions. Chi-square analysis was used to determine relationships between capture frequency and nocturnal cloud cover and moon visibility. Expected capture frequency was based on the relative frequencies of trap-nights during various sky and moon conditions.
Laboratory Study Subjects. Mice trapped in the vicinity of Durham, N H were used in experiments. They were housed in pairs (of opposite sex whenever possible) in plastic cages with water and food provided ad libitum. A dark:light cycle of 15D :9L was maintained so that animals used for experimentation were subjected to trials during their normal dark period. Animals were exposed to this photoperiod for at least two weeks before being used for trials. Ceiling-mounted fluorescent lights provided lighting while dark periods consisted of total darkness. Only apparently healthy, mature animals, at least seven weeks old, were used. Females were not used when obviously gravid or nursing, or withi~t one week after the last pup o f a litter had been removed. Other than the age requirement indicated above, the use o f males was not restricted by reproductive conditions. Apparatus. Each of two small rooms housed a test apparatus. Temperature was maintained at 21 C, and the air was recycled. The rooms were buffered against light but not soundproof. ~ ^e~:vte~ C m ahreb~ c~ eh=be,
~ b
A~tivxty c~ambor
[r t ~ t
c~e c.nb*~
Fig. 1. Design of the test apparatus as viewed from above.
30,
2
Each of two test apparatuses (Fig. 1) consisted of two chambers separated by a central, neutral chamber. Walls were constructed of masonite and were 51 cm high for one apparatus and 61 cm high for the other; otherwise, the apparatuses were identical. The neutral chamber and apparatus cover was an 0.64cm ~ mesh hardware cloth. Sand covered the floors for a depth of 1 to 5 cm. A mouse introduced to the neutral chamber could enter either of the end chambers by passing through treadle boxes with attached mercury microswitches wired to an event recorder. Data collected consisted o f (1) the frequencies of visits, (2) the duration of each visit, and (3) total time spent in each chamber. The duration of any visit to a chamber was recorded to the nearest minute, and only visits lasting more than 30 s were recorded. The two variables considered most important in recognizing chamber preferences were total time spent and duration per visit. As the end chambers housed different cues, chamber preferences translate to cue preferences. A mouse was allowed free access to the entire apparatus during tests not employing a removable glass partition. During tests using contrasting visual cues, each end chamber was divided into activity and cue chambers by a glass partition to prevent other sensory cues from interacting with visual ones. Objects were placed in the cue chambers at the ends of the apparatus (Fig. 1). Water was provided ad libitum in each end. Although a variety of contrasting visual, olfactory, and tactile cues under differing levels of illumination were used in the entire study, this report deals only with two light levels and horizontally versus vertically oriented visual cues.
Experiments were run under two different light conditions: 0.005 foot-candle and 0.020 foot-candle. The mean values for illuminated forests and fields on cloudy and clear moonlit nights, respectively, were the bases for choosing the light levels for laboratory experiments. These were determined as follows. Using a Weston Model 1979 foot-candle meter with a spectral sensitivity of 380 to 760 nm, and a Weston selenium photovoltaic cell couplet, outdoor illuminance readings were made on two evenings in January 1976, when the ground was snowcovered. Ten measures of illumination were taken at ground level on a moonlit but overcast night. Five of these were in areas of no cover and five were under coniferous canopy and understory cover. These 10 measures together
BARRY & FRANCQ: VISUAL ORIENTATION BY PEROMYSCUS averaged roughly 0.003 foot-candle. Ten additional measures were taken another night in an open field under full moonlight and clear skies. These averaged 0.019 foot-candle. This latter value corresponds well with published values of illumination at the substrate (Blair 1943; Dice 1945; Kavanau 1968) with a full moon at zenith. In the laboratory a 15-W incandescent white light, placed approximately 1.8 m above the substrate over the centre of the apparatus, provided the desired illuminance in the activity chamber o f the test apparatus. A shade restricted diffusion o f light to the area below the light source. Light levels were adjusted by rheostats and by placing brown wrapping paper over the test chamber. Procedure. Experiments consisted of trials lasting 14 to 15.25 h each. For each experiment, mice (equal numbers of each sex) were tested in random sequence, with cage mates never run sequentially. After each trial, both treadle boxes were removed and blown free of faecal pellets and other extraneous materials. Visually evident faecal pellets were removed from the sand substrate, which was thoroughly raked and turned over in an attempt to bury any undetectable materials; this also dispersed residual urine odours. To eliminate any effect due to position preference by the mice, we switched the horizontal and vertical cue orientations randomly between the two cue chambers. Experiment 1, illuminance preference. This experiment was an examination of visual orientation in response to different levels of illumination. In one chamber, illumination measured 0.020 foot-candle, while in the other, it was roughly 0.002 foot-candle. No glass partitions in the chambers were employed in this experiment. Experiment 2, vertical versus horizontal cues at 0.005 foot-candle. This experiment was an examination of visual orientation in response to objects differentially oriented. The objects were boxes of 18 x 18 x 60 cm placed either vertically or horizontally. The boxes were wrapped with plain brown wrapping paper to eliminate any visual cues associated with surface peculiarities. The base of each box was centrally positioned 4 cm behind the glass partition. Experiment 3, vertical versus horizontal cues at 0.020 foot-candle. This experiment was identical to experiment 2, except for the difference in illumination.
341
Statistical Analysis of Laboratory Results For each experiment, data consisting of frequencies of visits, duration per visit, and total time spent in the opposing chambers were analysed by split-plot analysis of variance (following a completely randomized design). This analysis permitted the recognition of cue preferences, sex differences, and sex/cue interactions. Results Field Study Results o f the field work are summarized in Table L Although there were more captures of P. leucopus under a full moon than under other phases in the west sampling area, and more during the third quarter in the east area, in neither case did the numbers of captures differ significantly (P>0.05) from expected values. When numbers of captures during all visible phases of the moon were pooled and compared to captures during new moon, no significant departure from expected captures for either sampling area was revealed (P>0.05). In the west area there were more captures under cloudy than under clear or partly cloudy skies, while in the east there were more under clear skies. However, actual captures for neither area differed significantly (P>0.05) from the expected during the several conditions of cloud cover. Capture frequency was examined under various combinations o f sky condition and moon visibility. For both areas, more mice were captured under clear skies and a visible moon. However, captures under clear and partly cloudy skies were no more frequent than expected (P>0.05) when the moon was visible. In the west area, under cloudy skies, capture frequency was not related to moon visibility (P>O.05). In the east, under cloudy skies, there were insufficient captures for analysis. Laboratory Study None of the experiments revealed sex differences or sex[cue interactions in the preferences of the mice for various cues. For this reason, the data for both sexes are pooled for all experiments. In experiment 1, mice spent more time in the more illuminated habitat (F = 91.23; d f = 1,4; P < 0 . 0 1 ) (Table II), indicating a clear preference for the greater light level. Several individuals were found clinging upside down to the hardware cloth cover of the more illuminated chamber at the end of the trials, possibly demonstrat-
342
ANIMAL
BEHAVIOUR,
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2
Table I. Captures of P. leueopus in West and East Sampling Areas Under Various Moon Phases, Sky Conditions and Combinations of Sky Condition and Moon Visibility*
Sampling area
Moon phase New First quarter Full Third quarter Sky condition Clear Partly cloudy Cloudy Sky condition Clear Partly cloudy Cloudy
West
East
Total
18 26 35 19
6 6 10 16
24 32 45 35
32 29 37
19 10 9
51 39 46
Moon Moon visible not visible 28 4 25 4 27 10
Moon Moon visible not visible 18 1 8 2 6 3
*Moon visible = first quarter, full, or third quarter; moon not visible = new moon. ing an orientation to the light source. This was not seen in the darker side. In experiment 2, at an illuminance of 0.005 foot-candle, mice showed no visual preference for either the vertical or the horizontal box (Table III). However, in experiment 3, identical to experiment 2 except for the higher light level, both sexes spent more time in the chamber with the horizontally-positioned box ( F = 15.36; d f = 1,6; P < 0 . 0 1 ) (Table IV). Also, mice spent considerably more time per visit in the 'horizontal' chamber (F = 8.25; d f = 1,6; P<0.05). On several occasions, a mouse was found lying next to the glass partition in the preferred chamber at the end of the trial, and digging next to the glass was evident in both chamber in an apparent attempt by the mouse to reach the box. Discussion
On the basis of our field results, moon phase is not a factor in capture frequency (activity) of white-footed mice. That the mice did not refrain from surface activity on moonlit nights is not surprising considering that peromyscines have good visual acuity (Rahmann et al. 1968; Vestal 1970; Vestal & Hill 1972; King & Vestal 1974) and presumably rely heavily on vision in their travels (King 1974). The laboratory study (experiment 1) shows that wild-reared white-footed mice can discriminate between two naturally occurring, nocturnal levels of illuminance. Mice prefer the level offered by a full moon on a clear night in
the open (approximately 0.020 foot-candle) to one roughly tenfold darker, corresponding more to the natural levels found in sheltered spots in a forest on a cloudy, but moonlit night. Similarly, Brant & Kavanau (1965) found that darkness was a 'mildly aversive stimulus' for the canyon mouse (Peromyscus crinitus). Middle to late dusk and the early phase of dawn were found to have a great activity-stimulating effect on Peromyscus (Kavanau 1967). In addition, Peromyscus orient to an artificial m o o n and use celestial objects (e.g. twilight sun and moon) and landmarks as navigational aids (Kavanau 1968; 1969a, b). The results of experiment 1 suggest that orientation to or by the moon in the wild is possible; the apparent attraction of the mice to the light source argues strongly in favour of this thesis. Table II. Experiment 1. Summary of Visits by Peromyscus leucopus to Opposing Levels of Illuminationt
0.002 foot-candle 0.020 foot-candle Frequency of visits Duration per visit (minutes) Total time (minutes)
27.7 (6.7)
36.7 (6.7)
11.4 (6.7)
20.3 (4.2)
151.8 (21.2)
**
616.0 (37.6)
?Means and standard errors of means (in parentheses). N = 6: **Significant treatment effect (P<0.01).
BARRY & FRANCQ: VISUAL ORIENTATION BY PERO'MYSCUS Table HI. Experiment 2. Summary of Visits by Peromyscns leucopus to Vertical versus Horizontal Cues at an Illum[nance of 0.005 foot-candler
Vertical
Horizontal
cue
Frequency of visits Duration per visit (minutes) Total time (minutes)
cue
30.1 (5.2)
25.7 (3.1)
11.9 (2.3)
14.1 (2.6)
301.7 (53.1)
323.0 (42.6)
t Means
and standard errors of means (in parentheses). N = 10.
Table IV. Experiment 3. Summary of Visits by Peromyscus leucopus to Vertical versus Horizontal Cues at an Illuminance of 0.020 foot-candle~
Vertical
Horizontal
cue
Frequency of visits Duration per visit (minutes) Total time (minutes)
cue
18.8 (3.0)
18.9 (3.4)
15.3 (4.4)
*
28.7 (4.9)
222.8 (29.8)
**
457.8 (53.7)
t Means and standard errors of means (in parentheses). N=8. *Significant treatment effect (/'<0.05). **Highly significant treatment effect (P<0.01). How important is vision in the navigation of these mice ? The results o f experiments 2 and 3, which differed only in illuminance, support the contention that illumination level is critical to the use of vision and visual cues in navigation. Mice that did not discriminate visually between two objects (cues) at lower natural, nocturnal light levels did so at full-moonlight illumination. The evidence that white-footed mice are able to navigate by vision at higher nocturnal illuminance, that they prefer such levels to much lower ones, and that they are attracted to a light source in the laboratory would lead to the expectation that they would be more active on nights when the full moon was visible. However, energy needs obviously prohibit restriction of activity to such periods alone. What is significant is that activity is not adversely affected during well-illuminated nocturnal periods. During such times mice may realize an advantage through an increased reliance on vision in orientation, navigation and escape. Barry & Francq (1980) have demonstrated the use of landmarks during escapes in daylight. The increased efficiency of flight afforded by illumination in familiar
343
territory, which permits the use of landmarks as visual references, may help to offset disadvantages associated with predation. Our study presents evidence of preference for horizontal objects over vertical ones at certain light levels. This is in contrast to Joslin's study (1977), which suggested a primary requirement for verticality and only a secondary orientation to horizontal cues at similar illumination. However, the P. leucopus Joslin studied were conceived of laboratory-reared parents which likely differ from wild:reared individuals in their preferences for visual cues (including vertical and horizontal ones), as shown by Barry (1978) in his comparison of wild-reared and first generation laboratory-reared individuals. Our work suggests that landmarks with major horizontal components, such as logs and rocks, are important to the white-footed mouse in visual orientation and navigation. This is consistent with the preference of this mouse f o r wooded or shrubby habitat (Dice 1922; Choate 1973; Kaufman & Fleharty 1974) in which such objects are common. Additionally, M'Closkey (1975, 1976) has shown that fallen branches, logs, and horizontal and low-angle branches are extensively utilized by P. leucopus, and that logs and branches are important structural characteristics of the preferred habitat. While visual orientation of Peromyscus is facilitated by greater illumination, the chance of predation is also increased. Objects with major horizontal components such as logs and branches are important avenues of escape (Brand 1955; Smith & Speller 1970; Barry & Francq 1980), and temporary refuge may be found more readily beneath horizontal ones than under or by climbing vertical ones. Therefore a tendency to orient preferentially to horizontal cues as illumination and vulnerability increase would be selectively advantageous. Acknowledgments
This paper is based on a dissertation by R. E. Barry, Jr., accepted by the Zoology Department o f the University of New Hampshire in partial fulfilment of the requirements for the Ph.D. degree. We acknowledge the financial support of the Zoology Department of the University of New Hampshire. REFERENCES
Barry, R. E., Jr. 1978. Orientation to the habitat in the white-footed mouse, Peromyscus leucopus noveboracensis. Ph.D. thesis, University of New Hampshire, Durham.
344
ANIMAL
BEHAVIOUR,
Barry, R. E., Jr. & Francq, E. N. 1980. Orientation to landmarks within the preferred habitat by Peromyscus leucopus. J. Mamenal., 61, 292-303. Behney, W. H. 1936. Nocturnal explorations of the forest deermouse. J. MammaL, 17, 225-230. Blair, W. F. 1943. Activities of the Chihuahua deermouse in relation to light intensity. J. Wildl. Mangmt, 7, 92-97. Blair, W. F. 1951. Population structure, social behavior, and environmental relations in a natural population of beach mice (Peromyscus polionotus leucocephalus). Contrib. Lab. Vert. Biol., University of Michigan, 48, 1-47. Brand, R. H. 1955. Abundance and activity of the wood mouse (Peromyscus leucopus noveboracensis) in relation to the character of its habitat. Ph.D. thesis, University of Michigan, Ann Arbor. Brant, D. H. & Kavanau, J. L. 1965. Exploration and movement patterns of the canyon mouse Peromyscys crinitus in an extensive laboratory enclosure. Ecology, 46, 452-461. Burt, W. H. 1940. Territorial behavior and populations of some small mammals in southern Michigan. Misc. Publ. Mus. Zool., University of Michigan, 45, 1-58. Choate, J. R. 1973. Identification and recent distribution of white-footed mice (Peromyscus) in New England. J. MammaL, 54, 41-49. Dice, L. R. 1922. Some factors affecting the distribution of the prairie vole, forest deer mouse, and prairie deer mouse. Ecology, 3, 29-47. Dice, L. R. 1945. Minimum intensities of illumination under which owls can find dead prey by sight. Am. Nat., 79, 385-416. Gentry, J. B. & Odum, E. P. 1957. The effect of weather on the winter activity of old-field rodents. J. Mammal., 38, 72-77. Getz, L. L. 1959. Activity of Peromyscus leucopus. J. Mammal., 40, 449-450. Hays, H. A. 1958. The effect of mieroclimate on the distribution of small mammals in a tall-grass prairie plot. Trans. Karts. Acad. Sci., 61, 40-63. Hirth, H. F. 1959. Small mammals in old-field succession. Ecology, 40, 417-425. Johnson, M. S. 1926. Activity and distribution of certain wild mice in relation to biotic communities. J. MammaL, 7, 245-277. Joslin, J. K. 1977. Visual cues used in orientation by white-footed mice, Peromyscus leucopus: a laboratory study. Am. Midl. Nat., 98, 308-318. Kaufman, D. W. & Fleharty, E. D. 1974. Habitat selection by nine species of rodents in north-central Kansas. Southwest. Nat., 18, 443-452. Kavanau, J. L. 1967. Behavior of captive white-footed mice. Science, N.Y., 155, 1623-1639. Kavanan, J. L. 1968. Activity and orientational responses of white-footed mice to light. Nature, Lond., 218, 245-252.
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Kavanau, J. L. 1969a. Influences of light on activity of small mammals. Ecology, 50, 548-557. Kavanau, J. L. 1969b. Influences of light on activity of the small mammals, Peromyscus sp., Tamias striatus, and Mustela rixosa. Experientia, 25, 208-209. Kavanau, J. L. & Havenhill, R. M. 1976. Compulsory regime and control of environment in animal behavior. III. Light level preferences of small nocturnal malrmaals. Behaviour, 59, 203-225. King, J. A. 1974. Visual orientation to food in Peromyscus. Am. Zool., 14, 1279. King, J. A. & Vestal, B. M. 1974. Visual acuity of Peromyscus. J. MammaL, 55, 238-243. Marten, G. G. 1973. Time patterns of Peromyscus activity and their correlations with weather. J. Mammal., 54, 169-188. M'Closkey, R. T. 1975. Habitat dimensions of whitefooted mice, Peromyscus leucopus. Am. Midl. Nat., 93, 158-167. M'Closkey, R. T. 1976. Use of artificial microhabitats by white-footed mice, Peromyscus leucopus. Am. Midl. Nat., 96, 467-470. Moody, P. A. 1929. Brightness vision in the deer-mouse,
Peromyscus maniculatus graeilis. Exper. Zool., 52, 367-405. Orr, H. D. 1959. Activity of white-footed mice in relation to environment. J. Mammal., 40, 213-221. Owings, D. H. & Loekard, R. B. 1971. Different nocturnal activity patterns of Peromyscus californicus and Peromyseus eremieus in lunar lighting. Psychon. Sei., 22, 63-64. Provost, M. W. 1940. Dynamics of Peromyscus populations. M.S. thesis, University of New l.lampshire. Rahmann, H., Rahmann, M. & King, J. A. 1968. Comparative visual acuity (minimum separable) in five species and subspecies of deer-mice (Peromyscus). PhysioL Zool., 41, 298-312. Smith, D. A. & Speller, S. W. 1970. The distribution and behaviour of Peromyscus maniculatus gracilis and Peromyscus leucopus noveboracensis (Rodentia: Cricetidae) in a southeastern Ontario woodlot. Can. J. Zool., 48, 1187-1199. Svihla, A. 1932. A comparative life-history study of the mice of the genus Peromyscus. Misc. PubL Mus. Zool., University of Michigan, 24, 1-39. Vestal, B. M. 1970. Development of visual acuity in two species of Peromyscus (Rodentia). Ph.D. thesis, Michigan State University. Vestal, B. M. 1973. Ontogeny of visual acuity in two species of deer-mice (Peromyscus). Anita. Behav., 21, 711-719. Vestal, B. M. & Hill, J. L. 1972. Pattern vision of deermice (Peromyscas) under red light. J. MammaL, 53, 374-376.
(Received 3 April 1981 ; revised 16 July 1981 ; MS. number A2634)
OF
BY RONALD E. BARRY, Jr.* & EDWARD N. FRANCQ
Department of Zoology, The University of New Hampshire, Durham, NH 03824 Abstract. A two-phase study was conducted with Peromyscus leucopus noveboracensis.; In the field, frequency of captures was examined relative to nocturnal cloud co~,er and moon visibility. No relationships were apparent. In the laboratory, preferences of wild-reared mice for opposing visual cues under contrasting levels of illuminance were studied. Mice preferred an illumination equivalent to that striking a field on a clear, moonlit night (0.020 foot-candle) to the average of that striking the forest floor on a cloudy, moonlit night (0.005 foot-candle). At the lower intensity, mice showed no preference between two identical boxes placed vertically or horizontally. At the higher level of illuminance, there was a preference for the horizontal box, suggesting a tendency to orient toward horizontal objects over vertical ones at certain light levels. Higher natural nocturnal illuminance is not avoided (and may actually be preferred) by P. leucopus. Vision may be an important sensory modality in orientation and navigation under these conditions. moonlit night (Kavanau (1967), (1968), (1969a,b); Kavanau & Havenhill (1976) for P. maniculatus, P. crinitus, P, leucopus, and P . californicus). Based on these accounts, and reports that Peromyscus possesses the best visual acuity of any rodent tested thus far (Vestal 1970, 1973; King & Vestal 1974), we hypothesized that P. leucopus noveboracensis would be more active on brighter (clear, moonlit) nights than on darker (cloudy, moonlit) nights. We also hypothesized that mice preferred an illumination roughly equivalent to that striking the substrate on a clear, full-moonlit night to one perceptibly less intense. In addition, we hypothesized that the use of vision in habitat orientation and navigation requires high nocturnal illumination. Investigations of this sort are important in establishing bases for activity, movements, and habitat selection and utilization in small mammals. Methods Field Study The field study was p a r t of a larger project conducted in two woodlots, termed east and west sampling areas, in Stratford County, New Hampshire. The live-trapping period was June 7 through September 17, 1976. Traps were open a total of 5150 trap-nights and relevant data were gathered on 136 captures. Sampling and studysite details are described elsewhere (Barry & Francq 1980). Phases of the moon for evenings of the trapping period were recorded as new, first quarter, full, Or third quarter. Percentage 0f sky Cover, recorded at Pease Air Force Base about 5 miles from the study site, was obtained from the National Weather Service in Ashevi!le, North
The amount of available light may be a major factor in determining activity of Peromyscus. Although this genus is nocturnal (Johnson 1926; Svihla 1932; Behney 1936; Burt 1940; Getz 1959), species appear to be most active during relatively bright portions of the night. Both Svihla and Burt suggested an activity peak around dusk. Behney found peak exploration at about one hour after sunset. However, there are conflicting conclusions on the illumination preferences of various species of Peromyscus, and there are probably speciesspecific preferences related to the nature of the preferred habitat, predator-prey relationships, the capabilities of the sensory apparatus, and so on. Most conclusions have been drawn on the basis of observations or capture under various sky and moon conditions. Greater activity has been observed on cloudy and/or moonless nights by a number of investigators (Johnson 1926; Butt 1940; Provost 1940; Blair 1943, 1951; Gentry & Odum 1957; Hirth 1959; Owings & Lockard 1971). On the other hand, others have found either no relationship between activity of certain peromyscines and sky and/or moon condition (Hays 1958; Orr 1959), or enhancement of activity by the presence of lunar illumination (Owings & Lockard 1971; Marten 1973). Also, under controlled conditions, several species have been shown to either avoid darkness (Moody 1929 for P. maniculatus gracilis; Brant & Kavanau 1965 for P. crinitus) or exhibit decreased activities at light levels below that striking the earth's surface on a clear, full*Present address: Center of Environmental Science, Unity College, Unity, ME 04988. Address reprint requests to R.E.B. 339
340
ANIMAL
BEHAVIOUR,
Carolina. Sky conditions were classified as clear, partly cloudy, and cloudy. Sky cover was recorded from 1800 to 0600 hours EST according to the following criteria; dear: an average of less than 50 70 sky cover for the recording period, with at least one hourly recording o f zero cover and no recording of 10070 cover; cloudy: an average o f greater than 50 7o sky cover for the recording period with at least one hourly recording o f 100~o cover and no recording of zero cover, partly cloudy: anything intermediate to clear and cloudy conditions. Chi-square analysis was used to determine relationships between capture frequency and nocturnal cloud cover and moon visibility. Expected capture frequency was based on the relative frequencies of trap-nights during various sky and moon conditions.
Laboratory Study Subjects. Mice trapped in the vicinity of Durham, N H were used in experiments. They were housed in pairs (of opposite sex whenever possible) in plastic cages with water and food provided ad libitum. A dark:light cycle of 15D :9L was maintained so that animals used for experimentation were subjected to trials during their normal dark period. Animals were exposed to this photoperiod for at least two weeks before being used for trials. Ceiling-mounted fluorescent lights provided lighting while dark periods consisted of total darkness. Only apparently healthy, mature animals, at least seven weeks old, were used. Females were not used when obviously gravid or nursing, or withi~t one week after the last pup o f a litter had been removed. Other than the age requirement indicated above, the use o f males was not restricted by reproductive conditions. Apparatus. Each of two small rooms housed a test apparatus. Temperature was maintained at 21 C, and the air was recycled. The rooms were buffered against light but not soundproof. ~ ^e~:vte~ C m ahreb~ c~ eh=be,
~ b
A~tivxty c~ambor
[r t ~ t
c~e c.nb*~
Fig. 1. Design of the test apparatus as viewed from above.
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Each of two test apparatuses (Fig. 1) consisted of two chambers separated by a central, neutral chamber. Walls were constructed of masonite and were 51 cm high for one apparatus and 61 cm high for the other; otherwise, the apparatuses were identical. The neutral chamber and apparatus cover was an 0.64cm ~ mesh hardware cloth. Sand covered the floors for a depth of 1 to 5 cm. A mouse introduced to the neutral chamber could enter either of the end chambers by passing through treadle boxes with attached mercury microswitches wired to an event recorder. Data collected consisted o f (1) the frequencies of visits, (2) the duration of each visit, and (3) total time spent in each chamber. The duration of any visit to a chamber was recorded to the nearest minute, and only visits lasting more than 30 s were recorded. The two variables considered most important in recognizing chamber preferences were total time spent and duration per visit. As the end chambers housed different cues, chamber preferences translate to cue preferences. A mouse was allowed free access to the entire apparatus during tests not employing a removable glass partition. During tests using contrasting visual cues, each end chamber was divided into activity and cue chambers by a glass partition to prevent other sensory cues from interacting with visual ones. Objects were placed in the cue chambers at the ends of the apparatus (Fig. 1). Water was provided ad libitum in each end. Although a variety of contrasting visual, olfactory, and tactile cues under differing levels of illumination were used in the entire study, this report deals only with two light levels and horizontally versus vertically oriented visual cues.
Experiments were run under two different light conditions: 0.005 foot-candle and 0.020 foot-candle. The mean values for illuminated forests and fields on cloudy and clear moonlit nights, respectively, were the bases for choosing the light levels for laboratory experiments. These were determined as follows. Using a Weston Model 1979 foot-candle meter with a spectral sensitivity of 380 to 760 nm, and a Weston selenium photovoltaic cell couplet, outdoor illuminance readings were made on two evenings in January 1976, when the ground was snowcovered. Ten measures of illumination were taken at ground level on a moonlit but overcast night. Five of these were in areas of no cover and five were under coniferous canopy and understory cover. These 10 measures together
BARRY & FRANCQ: VISUAL ORIENTATION BY PEROMYSCUS averaged roughly 0.003 foot-candle. Ten additional measures were taken another night in an open field under full moonlight and clear skies. These averaged 0.019 foot-candle. This latter value corresponds well with published values of illumination at the substrate (Blair 1943; Dice 1945; Kavanau 1968) with a full moon at zenith. In the laboratory a 15-W incandescent white light, placed approximately 1.8 m above the substrate over the centre of the apparatus, provided the desired illuminance in the activity chamber o f the test apparatus. A shade restricted diffusion o f light to the area below the light source. Light levels were adjusted by rheostats and by placing brown wrapping paper over the test chamber. Procedure. Experiments consisted of trials lasting 14 to 15.25 h each. For each experiment, mice (equal numbers of each sex) were tested in random sequence, with cage mates never run sequentially. After each trial, both treadle boxes were removed and blown free of faecal pellets and other extraneous materials. Visually evident faecal pellets were removed from the sand substrate, which was thoroughly raked and turned over in an attempt to bury any undetectable materials; this also dispersed residual urine odours. To eliminate any effect due to position preference by the mice, we switched the horizontal and vertical cue orientations randomly between the two cue chambers. Experiment 1, illuminance preference. This experiment was an examination of visual orientation in response to different levels of illumination. In one chamber, illumination measured 0.020 foot-candle, while in the other, it was roughly 0.002 foot-candle. No glass partitions in the chambers were employed in this experiment. Experiment 2, vertical versus horizontal cues at 0.005 foot-candle. This experiment was an examination of visual orientation in response to objects differentially oriented. The objects were boxes of 18 x 18 x 60 cm placed either vertically or horizontally. The boxes were wrapped with plain brown wrapping paper to eliminate any visual cues associated with surface peculiarities. The base of each box was centrally positioned 4 cm behind the glass partition. Experiment 3, vertical versus horizontal cues at 0.020 foot-candle. This experiment was identical to experiment 2, except for the difference in illumination.
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Statistical Analysis of Laboratory Results For each experiment, data consisting of frequencies of visits, duration per visit, and total time spent in the opposing chambers were analysed by split-plot analysis of variance (following a completely randomized design). This analysis permitted the recognition of cue preferences, sex differences, and sex/cue interactions. Results Field Study Results o f the field work are summarized in Table L Although there were more captures of P. leucopus under a full moon than under other phases in the west sampling area, and more during the third quarter in the east area, in neither case did the numbers of captures differ significantly (P>0.05) from expected values. When numbers of captures during all visible phases of the moon were pooled and compared to captures during new moon, no significant departure from expected captures for either sampling area was revealed (P>0.05). In the west area there were more captures under cloudy than under clear or partly cloudy skies, while in the east there were more under clear skies. However, actual captures for neither area differed significantly (P>0.05) from the expected during the several conditions of cloud cover. Capture frequency was examined under various combinations o f sky condition and moon visibility. For both areas, more mice were captured under clear skies and a visible moon. However, captures under clear and partly cloudy skies were no more frequent than expected (P>0.05) when the moon was visible. In the west area, under cloudy skies, capture frequency was not related to moon visibility (P>O.05). In the east, under cloudy skies, there were insufficient captures for analysis. Laboratory Study None of the experiments revealed sex differences or sex[cue interactions in the preferences of the mice for various cues. For this reason, the data for both sexes are pooled for all experiments. In experiment 1, mice spent more time in the more illuminated habitat (F = 91.23; d f = 1,4; P < 0 . 0 1 ) (Table II), indicating a clear preference for the greater light level. Several individuals were found clinging upside down to the hardware cloth cover of the more illuminated chamber at the end of the trials, possibly demonstrat-
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BEHAVIOUR,
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Table I. Captures of P. leueopus in West and East Sampling Areas Under Various Moon Phases, Sky Conditions and Combinations of Sky Condition and Moon Visibility*
Sampling area
Moon phase New First quarter Full Third quarter Sky condition Clear Partly cloudy Cloudy Sky condition Clear Partly cloudy Cloudy
West
East
Total
18 26 35 19
6 6 10 16
24 32 45 35
32 29 37
19 10 9
51 39 46
Moon Moon visible not visible 28 4 25 4 27 10
Moon Moon visible not visible 18 1 8 2 6 3
*Moon visible = first quarter, full, or third quarter; moon not visible = new moon. ing an orientation to the light source. This was not seen in the darker side. In experiment 2, at an illuminance of 0.005 foot-candle, mice showed no visual preference for either the vertical or the horizontal box (Table III). However, in experiment 3, identical to experiment 2 except for the higher light level, both sexes spent more time in the chamber with the horizontally-positioned box ( F = 15.36; d f = 1,6; P < 0 . 0 1 ) (Table IV). Also, mice spent considerably more time per visit in the 'horizontal' chamber (F = 8.25; d f = 1,6; P<0.05). On several occasions, a mouse was found lying next to the glass partition in the preferred chamber at the end of the trial, and digging next to the glass was evident in both chamber in an apparent attempt by the mouse to reach the box. Discussion
On the basis of our field results, moon phase is not a factor in capture frequency (activity) of white-footed mice. That the mice did not refrain from surface activity on moonlit nights is not surprising considering that peromyscines have good visual acuity (Rahmann et al. 1968; Vestal 1970; Vestal & Hill 1972; King & Vestal 1974) and presumably rely heavily on vision in their travels (King 1974). The laboratory study (experiment 1) shows that wild-reared white-footed mice can discriminate between two naturally occurring, nocturnal levels of illuminance. Mice prefer the level offered by a full moon on a clear night in
the open (approximately 0.020 foot-candle) to one roughly tenfold darker, corresponding more to the natural levels found in sheltered spots in a forest on a cloudy, but moonlit night. Similarly, Brant & Kavanau (1965) found that darkness was a 'mildly aversive stimulus' for the canyon mouse (Peromyscus crinitus). Middle to late dusk and the early phase of dawn were found to have a great activity-stimulating effect on Peromyscus (Kavanau 1967). In addition, Peromyscus orient to an artificial m o o n and use celestial objects (e.g. twilight sun and moon) and landmarks as navigational aids (Kavanau 1968; 1969a, b). The results of experiment 1 suggest that orientation to or by the moon in the wild is possible; the apparent attraction of the mice to the light source argues strongly in favour of this thesis. Table II. Experiment 1. Summary of Visits by Peromyscus leucopus to Opposing Levels of Illuminationt
0.002 foot-candle 0.020 foot-candle Frequency of visits Duration per visit (minutes) Total time (minutes)
27.7 (6.7)
36.7 (6.7)
11.4 (6.7)
20.3 (4.2)
151.8 (21.2)
**
616.0 (37.6)
?Means and standard errors of means (in parentheses). N = 6: **Significant treatment effect (P<0.01).
BARRY & FRANCQ: VISUAL ORIENTATION BY PERO'MYSCUS Table HI. Experiment 2. Summary of Visits by Peromyscns leucopus to Vertical versus Horizontal Cues at an Illum[nance of 0.005 foot-candler
Vertical
Horizontal
cue
Frequency of visits Duration per visit (minutes) Total time (minutes)
cue
30.1 (5.2)
25.7 (3.1)
11.9 (2.3)
14.1 (2.6)
301.7 (53.1)
323.0 (42.6)
t Means
and standard errors of means (in parentheses). N = 10.
Table IV. Experiment 3. Summary of Visits by Peromyscus leucopus to Vertical versus Horizontal Cues at an Illuminance of 0.020 foot-candle~
Vertical
Horizontal
cue
Frequency of visits Duration per visit (minutes) Total time (minutes)
cue
18.8 (3.0)
18.9 (3.4)
15.3 (4.4)
*
28.7 (4.9)
222.8 (29.8)
**
457.8 (53.7)
t Means and standard errors of means (in parentheses). N=8. *Significant treatment effect (/'<0.05). **Highly significant treatment effect (P<0.01). How important is vision in the navigation of these mice ? The results o f experiments 2 and 3, which differed only in illuminance, support the contention that illumination level is critical to the use of vision and visual cues in navigation. Mice that did not discriminate visually between two objects (cues) at lower natural, nocturnal light levels did so at full-moonlight illumination. The evidence that white-footed mice are able to navigate by vision at higher nocturnal illuminance, that they prefer such levels to much lower ones, and that they are attracted to a light source in the laboratory would lead to the expectation that they would be more active on nights when the full moon was visible. However, energy needs obviously prohibit restriction of activity to such periods alone. What is significant is that activity is not adversely affected during well-illuminated nocturnal periods. During such times mice may realize an advantage through an increased reliance on vision in orientation, navigation and escape. Barry & Francq (1980) have demonstrated the use of landmarks during escapes in daylight. The increased efficiency of flight afforded by illumination in familiar
343
territory, which permits the use of landmarks as visual references, may help to offset disadvantages associated with predation. Our study presents evidence of preference for horizontal objects over vertical ones at certain light levels. This is in contrast to Joslin's study (1977), which suggested a primary requirement for verticality and only a secondary orientation to horizontal cues at similar illumination. However, the P. leucopus Joslin studied were conceived of laboratory-reared parents which likely differ from wild:reared individuals in their preferences for visual cues (including vertical and horizontal ones), as shown by Barry (1978) in his comparison of wild-reared and first generation laboratory-reared individuals. Our work suggests that landmarks with major horizontal components, such as logs and rocks, are important to the white-footed mouse in visual orientation and navigation. This is consistent with the preference of this mouse f o r wooded or shrubby habitat (Dice 1922; Choate 1973; Kaufman & Fleharty 1974) in which such objects are common. Additionally, M'Closkey (1975, 1976) has shown that fallen branches, logs, and horizontal and low-angle branches are extensively utilized by P. leucopus, and that logs and branches are important structural characteristics of the preferred habitat. While visual orientation of Peromyscus is facilitated by greater illumination, the chance of predation is also increased. Objects with major horizontal components such as logs and branches are important avenues of escape (Brand 1955; Smith & Speller 1970; Barry & Francq 1980), and temporary refuge may be found more readily beneath horizontal ones than under or by climbing vertical ones. Therefore a tendency to orient preferentially to horizontal cues as illumination and vulnerability increase would be selectively advantageous. Acknowledgments
This paper is based on a dissertation by R. E. Barry, Jr., accepted by the Zoology Department o f the University of New Hampshire in partial fulfilment of the requirements for the Ph.D. degree. We acknowledge the financial support of the Zoology Department of the University of New Hampshire. REFERENCES
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(Received 3 April 1981 ; revised 16 July 1981 ; MS. number A2634)