Temporal responses to environmental scale in the lizard Anolis carolinensis (reptila, lacertilia, iguanidae)

Behavioural Processes, 13 (1986) 339-352 Elsevier TEMPORAL RESPONSES TO ENVIRONMENTAL SCALE IN THE LIZARD ANOLIS CAROLINENSIS (REPTILA, LACERTILIA, IGUANIDAE) Alton J . DE LONG *, Neil GREENBERG ** and Carl KEANEY *** University of Tennessee, Knoxville, 37916 (USA) * Department of Textiles, Merchandising, and Design ** Department of Zoology *** Life Sciences Graduate Program in Ethology (Accepted 10 July 1986) ABSTRACT Alton J . De Long, Neil Greenberg, and Carl Keaney, 1986, Temporal Responses To Environmental Scale In The Lizard Anolis Carolinensis Behav . Processes, 13 : 339-352 . An influence of spatial scale on temporal processing has been described in humans (De Long, 1981) . The hypothesis that a similar relationship exists in reptiles was tested by placing twelve lizards in volumetrically constant but large-scale or small-scale "home" environments and alternately exposing them to large and small scale novel environments in a counterbalanced design . Behavioral measures included latencies and frequencies for four types of behavior associated with behavioral arousal and exploration and for duration of behavioral states . Results indicate (1) behavioral latencies are significantly reduced in small-scale novel environments and (2) as predicted, the ratio of latencies in large-scale divided by smallscale novel environments is essentially identical to the ratio of the scales of the environments themselves . Linear regression analyses relating latencies to the ratio yield results remarkably similar to those previously reported for temporal experience and spatial scale in human subjects . This research suggests that an experiential temporal-spatial relativity may be phylogenetically primitive .

KEY WORDS

:

Time perception,

Environmental scale, Lizard, Reptile

INTRODUCTION Previous studies have reported the existence of a phenomenological space- time relationship in which spatial perception influences the experience of time (De Long, 1981, 1983a) . This relationship exhibits both neurological (De Long & Lubar, 1979) and behavioral correlates (De Long,

Correspondence

to : Neil Greenberg **

0376-6357/86/$03 .50

m 1986 Elsevier Science Publishers B .V . (Biomedical Division)

339



3 40

1983b),

including

an

improvement

in task

performance associated

with

relative decrease in spatial scale . The present experiment was designed to determine if vertebrates in other taxa exhibited similar behavior consistent with a theory of experiential space-time relativity . Specifically, this study tested the hypothesis that an animal's behavior in an environment of one scale should exhibit rather precise, measurable temporal differences compared to the same behavior in an environment of another scale . This hypothesis was predicated on the idea that the experience of temporal duration is a

relationship

which is a

function of spatial scale (De Long, 1981) .

The relationship between

temporal behavior and environmental scale is represented as the ratio TB/ES . A doubling or halving of the denominator requires an equivalent doubling or halving of the numerator to maintain a constant relationship . In this experiment animals were placed in a home environment and exposed to two volumetrically identical novel environments which differed only in scale of surface patterning . "small" .

Two spatial scales were used, "large" and

The large scale was precisely twice the linear dimensions of the

small . Thus, each animal was exposed to a novel environment which was either identical in scale to its home environment or of a different scale . It was hypothesized that if an animal's latency to initiating behavior in a novel environment was affected by environmental scale, that is, experienced as a relational and experiential constant,

animals would have a smaller

elapsed latency in the small-scale novel environment than in the large, regardless of the scale of their home environment .

The reasoning is based

on the previous formulation relating temporal experience, spatial scale and elapsed time :

E = x(T),

where "E" is experienced duration, "x" is the

reciprocal of spatial scale, and "T" is elapsed time (De Long, 1981) . This experiment assumes E is a subjective (animal-dependent) constant . The present report tests the prediction that an animal's latency period,

(T),

in a large-scale environment will be twice as long as that in a small-scale environment (E = 1/2(T)), if the large-scale environment is twice that of the small (x = 1/2) .

341

METHODS Twelve adult male Anolis carolinensis were used in the experiment . Subjects were commercially supplied by the Snake Farm, LaPlace, Louisiana . The size range of animals used was from 60 mm to 67 mm (snout-to-vent) with a mean length of 62 .1 mm (SD = 1 .9 mm) . Before experimentation, animals were placed in habitats under conditions known to initiate and maintain an activity cycle of 14h light/10h dark, and provided daily temperature fluctuations from 10 ° to 22 ° C . Lizards were fed commercially supplied 3week old crickets which were provided on a schedule that maintained alertness in the captive population . Handling was strictly minimized to eliminate potential extra-experimental stress (Meier et al ., 1973) . Six subjects were randomly assigned to large-scale "home" environments (HL) and six to small-scale home environments (HS) . The environments were 25cm X 25cm X 50cm all glass vivaria provided with water and a wooden perch and separated by sliding partitions from equivalent "novel" environments situated on either side . Because spatial scale is defined in terms of linear dimensionality (De Long, 1981) all environments were constant volumetrically, differing only in spatial scale . Spatial scale in home and novel vivaria was manipulated on the floor, back and side walls by means of and paper squares pasted on the surfaces . Squares in large-scale environments were twice the size and twice as coarse as those in the small scale environments . Thus, adjacent to each home environment (HL or HS), one novel large-scale environment (NL) and one novel small-scale environment (NS) was provided alternatively to the left or right to control for directional bias . After at least 24 hours of habituation to the home (HL or HS) environment, animals were exposed to a novel (NL or NS) environment on alternate days . Each animal had five ten-minute exposures to each of the alternative novel environments . This was accomplished by sliding the partition separating the home environment from an adjacent novel environment . Lizard movement was facilitated by the sight of the experimenter's hand placed at the opposite end of the home tank . Lizards were never touched and never gave evidence of behavioral "startle" responses or stress . Behavioral observations were conducted in a darkened room to minimize observer effects, and behavior was recorded using a multichannel event recorder . The behaviors selected were "Site-Change," (SC), "Posture-Change," (PC), "Tongue-Touch," (TT), and "Air- Lick," (AL), all components of spontaneous exploratory behavior (Greenberg, 1985) . The color of the animal during each observation period was also noted . The data collected and the manner of collection yielded records of frequency, latency, and duration of specific behaviors . Of the twelve animals involved, one lacked an appropriate amount of behavior under the H5 condition for comparison, and was dropped from the analysis although inclusion would not have altered the significance of the results as estimated by the Wilcoxon rank-sums test .



342

RESULTS Latencies for analyzed

per

each type

of behavior

in

novel environments

were

animal to derive a "scale-effect" index . Mean Novel Large

scale (NL) environment latencies were divided by the mean Novel Small scale (NS) environment latencies for each behavior . These indices were then averaged and treated as the individual animal's score, and an overall mean index value derived . Theoretically, with an NSINL ratio of 1/2 this value should be 2 .0 . The data yield a mean value of 2 .21 (SEM =

.35, N = 11) . A

more central but comparable "scale-effect" index was also derived for each animal based on the latencies for the first occurence of any type of behavior exhibited in novel environments . This index has a value of 1 .73 (SEM =

.15, N = il) .

To test for differences between latencies in NL and NS environments, the Wilcoxon-Mann-Whitney Rank-Sum test was performed for each type of behavior recorded . The results yielded significant differences for three of the four units of exploratory behavioral patterns recorded : sitechange, posture-change and tongue-touch . Air-lick, a behavioral pattern known to be facilitated by behavioral stress (Greenberg, 1985) was unaffected (see Table 1) . The same statistical test applied to latencies in NL and NS environments for the first behavior demonstrated a significant difference (z = 2 .66 ; p= .004, N = 11) .

TABLE 1 :

NL X NS Contrast for Latency

Z*

p =

Site-Change

(SC)

1 .61

.019

Posture-Change

(PC)

2 .27

.012

Tongue-Touch

(TT)

2 .07

.019

Air-Lick

(AL)

0 .75

.227

* Wilcoxon-Mann-Whitney Rank-Sum Test (N=11) .

34 3

To

examine the degree of relationship between latencies in NL and NS

environments, a linear regression was conducted with NS latencies as the independent variable . Results are : r = .67 (p <

.71 (p

.01, N = 11) for SC ; r =

.025, N = 11) for PC ; r = - .08 (ns, N = 11) far IT ; and r = - .01

(ns, N = 11) for AL . For the first behavior in novel environments the same linear regression is highly significant (r =

.74, p <

.005, N = 11) .

To determine if animal size was related to either an animal's scale index ratio or to the latencies in novel environments linear regressions were conducted, treating animal length as the independent variable . Results were r = - .22 (ns, N = 11) and r = - .05 (ns, N = 11) for the index ratio and latencies, respectively . In a previous study with human subjects (De Long, 1981) it was found that the longer subjects were exposed to scale-model environments in realizing a temporal relationship (the imagined experience of 30 minutes), the greater the index ratio--elapsed time in a 1/12 model divided by elapsed Lime in a 1/24 model (the larger environment also being twice the size of the smaller) . To examine this phenomenon in lizards, a linear regression was conducted with combined latencies (NL and NS environments) for the first behavior in novel environments as the independent variable, and the scale-index ratio for the first behavior as the dependent variable . The purpose of this analysis was to determine if the amount of time exposed to a novel environment prior to the first behavior emitted influenced the scale-index ratio . Results with this animal sample are essentially similar to those obtained with humans (r =

.60 ; p <

.05, N = 11) . The

comparability of results in both studies is shown in Table 2 .



34 4

TABLE

2:

Scale-Index Ratios (Large/Small) Associated With Elapsed Time or

Latencies (Exposure to Environments) Based on Linear Regression Lines .

Elapsed Time or Latencies Sub ect

(N)

-lsd

- .5sd

Mean

+ .5sd

+lsd

Mean

SEM

r

Lizards

(11)

1 .23

1 .48

1 .73

1 .98

2 .23

1 .73

.15

.60

.05

Humans*

(124)

1 .10

1 .44

1 .77

2 .10

2 .44

1 .77

.06

.30

.001

-

*from 11eLong (1981) . To compensate for differences in elapsed times in the two studies (minutes for humans and seconds in the current study), scaleindex ratios are shown in terms of means and standard deviations to either side of the mean .

Analysis of the latencies as well as the number of behaviors emitted per unit of time in large-scale and small-scale home and novel environments indicates patterns which are essentially identical, and suggests that the structure and relationships between the types of behavior recorded do not substantially vary across the scale of the novel environments . For example, rank-ordering of the behaviors based on mean latencies of the four different types of behavior is identical in NL and NS environments . The order from first to last behavior exhibited is, PC, SC, IT and AL . Actual mean latencies in NL and NS environments are contrasted in Figure 1 . Further, analysis of the "scale-effect" indices across the four types of behavior results in a similar pattern when computed either on the basis of mean latency across all animals or when computed on the basis of the ratio (NL/NS) for each individual animal before taking a mean index value . The difference in these two approaches is that in treating actual latencies as an animal's score and then deriving a scale-effect index (NL/NS) inordinately small or large latencies are given more weight in computing the mean .

When an animal's ratio is computed the effect of extreme



3 45

latencies

is nullified, but extreme ratios are given more weight . The

latter approach was used in this study, however, because of the results from earlier work with humans (De Long, 1981) which revealed that despite extremely short or long elapsed times when large and small scale environments were compared the scale-index ratio (large-scale elapsed time/small-scale elapsed time) was quite stable . Figure 1, however, illustrates that despite the particular form of analysis, the scale-index values do reveal a similar pattern for the four types of behavior . As was mentioned earlier, the overall mean "scale-effect" index based on using an animal's NL/NS latency ratio as its score was 2 .21 (n=ll) . 3 MEAN LATENCIES

∎ MEAN RATIOS

5 r U W 4 4 W

5

PC

SC

TT

AL

Fig . 1 . Scale-effect index computed from a mean latency across all animals and from the ratio (NL/NS) for individual animals before taking a mean index value .

Based on mean latencies shown in Figure 2, the overall average "scaleeffect" index is 1 .65 (n=ll) . Should one form of computation be spuriously inflated, the other must be spuriously deflated . If it is assumed both are equally inflated or deflated, and we accept a midpoint between them, we end up with a scale-effect index of

.93 1

(n=ll) .

Of the four types of



346

behavior,

only

AL remained unaffected by treatment differences . It also

shows the most variation in the "scale-effect" index between methods of computation, and is likely to be the least reliable in either case . If AL is dropped from the analysis, the midpoint value between both forms of computation is 2 .03 (n=11) (mean latencies, 1 .81 (n=ll) ; mean ratios, 2 .26 (n=11) .

150 140 0 130 120 110 100 W 90 80 a 70 N

a

d

60 50 40 30 20 10 0 PC

SC

IT

AL

Fig . 2 . Mean latencies for specific behaviors in small scale and large scale environments are contrasted . It was predicted that an animal's latency in the large scale environment would be twice as long as that in the small scale environment, because the large scale is twice that of the small .

With respect to the four experimental conditions used in the study, the scale-index ratios appear to be very stable . Table 3 shows the mean scale-index values for each condition based on the behaviors, SC, PC and TT . AL was dropped for this analysis because it was the only behavior which did not achieve a statistically significant difference between NL and NS environments ; and because, unlike the other behavioral units it is unaffected by prior environmental conditions (Greenberg, 1985) . It is apparent from Table 3 that experimental conditions do not appear to seriously affect the values of the scale-index ratios .



347

TABLE 3 : Nean Scale-index Ratios For Each Experimental Condition (SC, PC, and TT Combined)

First Novel Environment Larg e (NL) Small (NS)

Large (HL)

2 .32

2 .32

Small (HS)

2 .16

2 .25

Home Environment



34 8

DISCUSSION This study has attempted to test the hypothesis, derived from previous work with human subjects, that temporal experience is related to spatial scale in a phylogenetically conservative animal, the lizard, carolinensis .

Anolis

Results are consistent with the hypothesis that the spatial

scale of an environment is related to the temporal aspects of an animal's behavior .

Furthermore, certain relationships between the length of

exposure to an environment and the effects of scale on behavior appear similar to findings reported for human subjects . Specifically, the hypothesis that latency times will increase in the larger scale environment is clearly supported in three of the four behaviors examined ; and is even more pronounced when the first behavior in novel environments is examined . The only behavior for which latencies are not affected is "Air-Lick ." Interestingly, this behavior, which does not involve tactile contact with the environment, is the only reported component of exploratory behavior not reduced by stress in this species (Greenberg, 1985) . This study (1) reveals that latencies to exhibit exploratory behavior in small-scale novel environments are significantly less than those in large-scale environments, (2) demonstrates a significant correlation between latencies in the two types of environments, and (3) confirms the scale-effect index ratio of 2 .0, predicted from research on humans, in a reptile . Further, the linear regression analysis relating elapsed time prior to emitting the first behavior in a novel environment with the scaleindex ratio is similar to results with human subjects : the longer the animal is in the environment before testing, the stronger the effect of spatiall scale . It is possible that visual complexity as well as what we

refer to as

"spatial scale" could also be considered a mediating factor . With a halving of "spatial scale" there exists a quadrupling of complexity in terms of edges and figures or shapes in the environment . Four edges are "replaced" with sixteen, and one figure is replaced with four .

There are



3 49

several arguments, however, that indicate spatial scale is the more likely factor : First, one could suggest these changes are but a manifestation of scale changes . This is a weak but not irrelevant argument . Next, one could suggest that the scale change is by a factor of two (or one-half) and the complexity change is by a factor of four (or one-fourth) . But the behavioural results are in accord with a change in the magnitude of a factor of two, not four . The proportional symmetry would seem to rule out complexity, but how the nervous system actually perceives and translates scale might not . This is a somewhat stronger but still tenuous argument . Considerable support for accepting the presence of some type of experiential relativity, as opposed to complexity, as the mediating factor derives from earlier experimentations with human subjects (DeLong, 1981) . In these experiments different scale models were involved which were altered only dimensionally . Objects such as chairs have the same number of edges regardless of the actuall scale . Temporal experience was found to be directly related to the dimensional scale changes . In these earlier experiments, complexity can clearly be ruled out . In these experiments, it is also relevant to note that the effects of scale on temporal experience are based an scale defined in terms of linear dimensionality . For example, a model 1/12 full size is 1/12 in length, width and height, Thus in area it represents only 1/144 the full size room and 1/1728 of the volume . But temporal experience was found to be related to scale in terms of linear dimension only,

i .e .,

1/12 .

In the current experiment, all environments were kept constant in terms of volume so that volume per se could be ruled out as a variable . A consequence is that in manipulating scale changes on the surfaces of the environments four times as many objects and edges were present in the smaller scale environment . Nevertheless, if spatial scale by these animals is also experienced in terms of linear dimensionality (in this case in terms of length, width or height) then in any given dimension the animal would see twice as many objects in the small scale environment .

Thus, if

3 50

the perception of complexity in these animals is based on linear dimension, complexity would be a simpler explanation of the data than the postulation of some kind of experiential relativity . Although the contraints and limitations involved in this study preclude a clear answer to which interpretation is most appropriate, data on several species seem more consistent with the postulation of an experiential relativity than with the complexity interpretation . There is no doubt that visual complexity is related to temporal experience and information processing in humans . The work of Ornstein (1969) demonstrates just such connections for both visual and auditory modalities . Yet EEG experiments (DeLong and Lubar, 1979) which included conditions with scalemodels (versus a full-size room), small and large images (of the same picture) and approaching and receding colors (red and blue) all yielded similar results : the scale-reduced conditions generated an EEG from the motor cortex indicative of alerting and increased informatin processing despite relative complexity being constant . That information processing is also related to spatial scale (or relative size) was indicated in an experiment in which two independent samples played video games on two different sized monitors (7" and 23"),

resulting in a consistent 13-15%

improvement in performance on the smaller screen (DeLong, 1983) . In this counterbalanced study, practice-effects were eliminated and rate of movement per unit of space, brightness levels and complexity were all constant . In fish, Brown (see 1957) found that differences in the relative size between conspecifics significantly affected growth rates . Also the work of Borowsky on the social inhibition of maturation under natural conditions and in the laboratory (1978) implicates relative size relationships between juveniles as a central mediating factor in the onset and timing of maturation (personal communication) . In effect, the larger of two juveniles matures first . It is difficult to see how relative visual complexity could account for such findings .

35 1

The

data

in this context indicate that the experience of space and

time may be related in the central nervous system in a way which facilitates mutual transformations of time and space . Jones (1976) has also concluded that spatial scale, attention, and information processing are intimately related . It seems a reasonable working assumption that such an experiential relativity itself would be phylogenetically primitive, and not necessarily a function of higher cortical processing . Further, Braitenberg (1984) suggests just such a mechanism, the "neuronal zoom effect," in dicussing the clustering of neurons in the brain . If spatial scale, temporal experience, information processing and attention are logically-related transformations of one another, then the logic involved would seem more a function of the basic structure of the nervous system itself rather than a recent evolutionary development . Further experimentation is clearly indicated if we are to clarify the cause of the effect documented . It is reasonable that both linear complexity as welll as time-space experiential relativity are both operative and may even interact, if not dominate in different contexts . The existence of an experiential space-time relativity would present an integrative framework capable of synthesizing data from numerous sources ; and may well prove to offer the most parsimonious explanation . Similarities between taxi suggest an experiential relativity which is basic to the operation of the central nervous system itself, and may be phylogenetically primitive . Similar conclusions regarding the existence of a fundamental experiential relativity which may underlie the sensitivity and operation of the central nervous system were reached by Jones (1976, 1984) . This interpretation is supported by earlier studies also testing predictions based on the formulation, E = x(T),

which show alterations in

neurological functioning (EEG) and information processing via task performance as a function of scale reductions .



352

ACKNOWLEDGEMENTS This

research was supported in part by grant NSF :BNS-8406028 to N .G .

The authors gratefully acknowledge the close reading and thoughtful advice of Drs . Alicia Berry Greenberg and Gordon Burghardt .

REFERENCES Borowsky, R . Social inhibition of maturation in natural populations of Xiphophorus variatus (Pisces : Poeciliidae) . Science . 1978, 201 :933-935 . Brown, M .E . Experimental studies on growth, Chapter IX . In : The Physiology of Fishes . Vol . 1, M .E . Brown (ed), New York : Academic Press, 1957 . De Long, A .J . Phenomenological space-time : Toward an experiential relativity, Science . 213 :681-683, 1981 . De Long, A .J . Environment as code : Spatial scale and time-frames in behavior and conceptualization . In : J .B . Calhoun, Environment and population . New York : Praeger, ]983a, pp . 192-194 . De Long, A .J- Spatial scale, temporal experience and information processing : An empirical examination of experiential relativity . Environment Systems . 13 :77-86, l983h .

Man-

De Long, A .J . & Iubar, J .F . Effeccts of environmental scale of subjects on spectral EEG output . Society for Neuroscience Abstracts . 5 :203, 1979 . Greenberg, N . Exploratory behavior and stress in the lizard, Anolis Zeitschrift fur Tierpsychologie 70 :89-102, 1985 . carolinensis . Jones, M .R . Time : Our lost dimension . 1976 .

Psychological Review .

83 :323-355,

Jones, M .R . The patterning of time and its effects on perceiving . In : Timing and time perception . J . Gibbon & L . Allan (Eds), Annals of the New York Academy of Sciences, Vol . 423, 1984, pp . 158-167 .