behavioral temperature regulation in the pill bug, … · 2018-03-30 · behavioral temperature...

Crustaceana 47 (1) 1984, E. J. Brill, Leiden

BEHAVIORAL TEMPERATURE REGULATION IN THE PILL BUG, ARMADILLIDIUM VULG?RE (ISOPODA)

BY

ROBERTO REFINETTI

Department of Psychology, University of California, Santa Barbara, California 93106, U.S.A.

INTRODUCTION

Autonomie temperature regulation in crustaceans has been the subject of

various studies. These included measurements of body temperature (e.g.,

Edney, 1951a, 1953; Warburg, 1965), lethal limits of ambient temperature

(e.g., Edney, 1964; Orr, 1955), water loss by evaporation (e.g., Edney, 1951b;

Warburg, 1965), and respiratory metabolism (e.g., Demeusy, 1957; Edwards

& Irving, 1943). Behavioral thermor?gulation, on the other hand, has attracted

the endeavors of few zoologists. Aquatic crustaceans have received some atten

tion (e.g., Casterlin & Reynolds, 1977; Crawshaw, 1974; Fast & Momot, 1973)

but, with the exception perhaps of only two studies on thermotaxis (Barlow &

Kuenen, 1957; Warburg, 1964), terrestrial crustaceans have been left aside.

The present series of experiments on a terrestrial isopod has the purpose of

filling this blank. Studies were made of thermal pre fe renda, acclimation, costs

of thermor?gulation, huddling, circadian rhythm, burrowing, dormancy, and

learning.

The research described in this paper was conducted at the Department of

Experimental Psychology, University of Sao Paulo, Brazil.

MATERIALS

Subjects

A total of 551 specimens of Armadillidium vulg?re (Latreille, 1804) (Isopoda,

Armadillidiidae), both males and females, was used. The animals (9-16 mm

length) were collected in late fall and kept in a vivarium for at least two weeks

before being tested. Except for special cases described below, the conditions in

the vivarium were as follows. About 30 pill bugs were housed per tray in

several aluminum trays (25 x 35 x 6 cm), lined with a 2 cm layer of soil brought from the place where the animals were collected. Dry leaves, chips of plaster of

Paris, and fresh carrot slices were provided regularly. The trays were wetted

with tap water every day to provide high humidity. Room temperature was

22 ? 2?C and relative air humidity about 60% . A 10:14 hr light:dark photo

period was maintained throughout.

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30 ROBERTO REFINETTI

Apparatuses

Thermal tunnel. ? This apparatus was used in Experiments 1 and 2. It

consisted of a 3.8 cm diameter, 1 m length copper pipe heated at one end with

an ambiance-heating resistor and cooled at the opposite end with melting ice in

order to generate a thermal gradient. A longitudinal strip of the tube was

replaced by a Plexiglas lid thus allowing for easy manipulation and viewing of

the inside of the tunnel. Since 20 cm were isolated at each end for the thermal

devices, the useful area was only 60 cm long. This was lined with moistened

foam rubber, so that air humidity was presumably near 100% all along the

tunnel although floor temperature ranged from 10? to 40?C. Luminosity was

kept constant throughout (irradiance: 4W.m"2). Because the apparatus was maintained inside an air conditioned room,

temperatures along the gradient were fairly constant from day to day. Anyway, floor temperature was measured with a mercury thermometer (to the nearest

round degree Celsius) immediately after removing the animal at the end of

each session. Comparisons with measurements taken with a small tip tele

thermometer (accuracy: + 0.1 ?C) showed that measurements taken with the

mercury thermometer introduced errors not greater than ? 0.9?C in floor

temperature and that air temperature 5 mm above the floor was not different

from floor temperature by more than ? 1.2?C.

A modified thermal tunnel was also used for some measurements. It was like

the one just described except that walls were introduced to control for

thigmotaxis and dry ice was used for cooling instead of water ice. The tunnel

was partitioned into thirty 2 cm long booths interconnected by a hallway

running along the length of the tube (see Krafft, 1967, for a detailed descrip tion of a similar apparatus).

Thermal cylinder. ? This apparatus was used in Experiment 1 only. It con

sisted of an open glass cylinder (18 x 22 cm), attached to a circular glass tray

(22 x 6 cm), that was heated at the center and cooled in the periphery. Heating was obtained by placing the tray on a wooden plate with a 2 cm diameter

copper bar attached to a hole at its center, and generating heat from below with

a standard 100 W bulb. Cooling was obtained by placing pieces of dry ice

between the wall of the cylinder and the wall of the tray. The floor of the tray was lined with a damp cloth in which nine concentric circles (diameters: 2 cm, 4 cm, 6 cm, etc.)

were drawn.

Thermal alley. ? This apparatus was used in Experiment 1 and consisted of

a circular-alley thermal gradient. The same cylinder and tray of the thermal

cylinder were used. Here, however, the animals were put into the alley existing between the wall of the tray and that of the cylinder. The tray was placed on a

wooden plate with two 2 cm diameter copper bars attached to two holes 21 cm

apart. Thus, the tray was on two small copper bars lying, say, at 0? and 180?.

One bar was heated from below with a standard 100 W bulb; the other was

cooled in a 23% NaCl, 77% melting-ice refrigerant mixture.


TEMPERATURE REGULATION IN ARMADILLIDIUM 31

Huddling box. ? This apparatus was used in Experiment 3. It consisted of a

small Plexiglas box (9x9x3 cm) placed inside a cylindrical glass box (15 x 15

cm) with aluminum floor. The floor of the Plexiglas box was lined with foam

rubber in which nine squares (3x3 cm) were drawn. The lid was perforated with 25 holes of 4 mm diameter. Near saturated air (r.h.:95%) was pumped

into the glass box at 0.2 m.s"1 through a cone attached to the lid; two holes

beside the cone provided air outflow.

Floor temperature could be either increased above or decreased below room

temperature (20?C in this case). Warming was obtained by irradiating heat

from a 100 W bulb on the aluminum floor of the cylindrical box. Cooling was

obtained by placing the lower portion of the cylinder in a melting ice bath.

Activity apparatus. ? A small Plexiglas box (3x7x3 cm) served as

experimental chamber. The activity index used was the number of crossings of

the red light beam of a photocell system placed across the longer walls. The

chamber was put inside an aluminum tray partially immersed into a water

bath fitted with heating and cooling systems controlled by a thermostat.

Photoperiod was controlled by a timer. During the light period a 25 W white

bulb was turned on, thus providing an illuminance of 70 lux; in the dark period a mild red light (illuminance: 3 lux) was kept on. Feeding and wetting of the

cloth lining were provided weekly. Y-maze. ? This apparatus was used in Experiment 6. It consisted of a

Plexiglas Y-maze (starting box: 2x4x4 cm; goal boxes: 1.5 x 4 x 4 cm) with

copper floor and no cover. In fact, there were three floors, one floor for the

starting box and first centimeter of goal boxes and two floors for the remaining

parts of goal boxes. Each floor was the top of a box through which water at the

desired temperature was circulated. One goal box was painted black; the

other, white. A damp carpet was employed as in the preceding apparatuses. Because the starting box floor extended to the entrance of goal boxes, the

animals were not exposed to the temperature of either goal box before choosing one. Measurements with a small thermocouple (0.1 mm diameter) showed no

thermal gradient greater than + 0.1 ?C in the zone of choice. Thus, if a pill bug

consistently preferred the temperature of one of the arms of the maze this

should be attributed to learning and not to moment-to-moment sensing as it

happened in the thermal gradient apparatuses.

EXPERIMENT 1

Thermotaxis, and its relation with thigmotaxis, was investigated in this

experiment. First, single animals were put into the thermal tunnel (see

Materials) and their position was recorded 30, 60 and 90 min after entrance.

Pilot observations had revealed that sessions longer than 90 min (up to 8 hr) were not necessary, for the positions did not differ significantly. Thirty animals

were run under normal conditions and 30 were run in absence of thermal



gradient. The results are shown in fig. 1. The control group (fig. 1A) showed

clear thigmotaxis in the last (90 min) observation: the major part of the animals

were found close to the ends of the tube. Data from the 30 and 60 min observa

tions are not shown; the distribution of animals was not different from that of

the 90 min observation (Kolmogorov-Smirnov test: D= 0.067, /?>0.05 and

Z>= 0.092, />>0.05, respectively).

Figure IB shows the distribution of experimental pill bugs 90 min after their

entrance into the tunnel. It is clear that they avoid the warm end but still have

a preference for the other end despite the low temperature. This is not due to

lack of exposure to the other parts of the tunnel, since (1) they entered the

tunnel at its center and had thus been exposed to other temperatures, and (2) on entering the tunnel they usually walked from one extremity to the other

several times before stopping at a given place. Barlow & Kuenen (1957) observed previously a similar conflict between thermotaxis and thigmotaxis in

Porcellio, Oniscus, and Armadillidium.

* A

fc*H LnDd

50 30.

20.

a

50

40_

30.

20. 10 .

Jn

ri'30 (cometed)

tio 0 10 20 30 40 SO 60

POSITION (cm)

10 15 20 25 30 35 40

TEMPERATURE CO

K> 15 20 25 30 35 40

TEMPERATURE CO

Fig. 1. Distribution of pill bugs along the thermal tunnel 90 min after entrance. A, control

group; B, experimental group; C, experimental group corrected for thigmotaxis and nonlinearity of the gradient.

No difference was found among the distributions in the three observations

(30 min vs 60 min: D = 0.133, p> 0.05; 30 min vs 90 min: D =

0.100, p> 0.05), but this is probably due to the masking effect of thigmotaxis on thermotaxis; in

the same apparatus sauba ants in groups of 15 individuals took 60 min to show

a thermal preference (Refinetti, 1982). Incidentally, both this masking effect of

thigmotaxis and a distorting effect of the nonlinearity of the gradient (i.e., when position in the tube is plotted against floor temperature the resulting curve is not a straight line) are corrected in the histogram of fig. 1C. The cor

rection was done as follows: (1) with data from all experiments that used the

thermal tunnel, a curve was drawn relating position in the tube to floor

temperature; (2) with this curve it was possible to find the floor temperature

corresponding to the position that had been recorded for the control group; (3) the distribution of both control and experimental group was tabled for classes

of 5?C range; and (4) for each class the frequency of experimental animals was

divided by the frequency of control animals (in the class 15-19?C control

frequency was null and an arbitrary value of 0.5 was chosen).



Next, a small alteration was made in the apparatus. The ends of the tunnel, which had been round because of the foam rubber lining, were cut flat.

Although this was quite a minor change it indeed affected the distribution of

animals. Thirty pill bugs were run individually and their distribution is shown

as striped blocks in fig. 2; white blocks are the same as those of fig. IB.

Thirdly, the partitioned thermal tunnel described above was employed.

Now, pill bugs could find plenty of angles all along the tunnel; thigmotaxis should not disturb thermotaxis. Forty animals were run individually and the

results are shown in fig. 3A. Unexpectantly, the data seem to indicate that

thigmotaxis is strong enough to abolish thermotaxis. That is, what is important

TEMPERATURE (?C)

Fig. 2. Distribution of pill bugs along the thermal tunnel 90 min after entrance. White blocks:

round extremities; striped blocks: flat extremities.

for a pill bug is finding a corner, no matter its temperature. Incidentally, it

should be noticed that many animals even died in the cold extremity (broken line in fig. 3A). In this case, however, cold torpor may play a part, as Dainton

(1954) showed for slugs.

Hence, in order to measure the thermopreferendum of pill bugs one has to

avoid offering corners. The thermal cylinder (see Materials) seemed a good solution. Thirty animals were run individually in this apparatus. As fig. 3B

suggests, however, pill bugs "know" that a circumference is made of infinite

straight lines, that is, a good number of animals prefer to freeze close to a

corner (frozen animals are shown in the broken-line block).

Finally, the thermal alley was used. Twenty-two experimental animals and

40 controls (i.e., without gradient) were run. The results (corrected as

described above) are shown in fig. 4, white blocks. In this apparatus all

temperature regions were equally devoid of corners, so that no concentration

in the corners was possible. The distribution is roughly uniform, with a peak in



the 22-23 ?C region. Regarding the lack of a clear-cut preferendum, it has been

previously found that crayfish avoid temperature extremes but do not prefer a

particular temperature (Crawshaw, 1974) and, most specifically, that

Armadillidium has a wider preference range than Porcellio and Oniscus (cf. Barlow

& Kuenen, 1957). On the other hand, it should be noticed that the peaks obtained in this experiment were at 20-24?C (figs. 1A and 3B) and at 22-23?C

(fig. 4, white blocks). As far as the peak of fig. 4 is a part of the peak of the

other two figures, it may be assumed that the thermopreferendum of the pill

bug is in the range between 22? and 23?C, provided it is not forgotten that this

is true only for 40-50% of the population. Barlow & Kuenen (1957) found a

slightly lower preference zone (19-20?C) in pill bugs tested in groups of 16

animals. However, their subjects were tested in the dark and this may decrease

the preferendum, at least in insects (Herter, 1924). Furthermore, acclimation

may also alter the preferendum (see Experiment 2). Unfortunately, Barlow &

Kuenen do not furnish information about rearing temperature for their

subjects.

TEMPERATURE CO TEMPERATURE PC)

Fig. 3. Distribution of pill bugs along the partitioned thermal tunnel (A) or around the thermal

cylinder (B) 90 min after entrance.

Figure 4 also shows the distribution of 22 experimental subjects run during the night (striped blocks). It seems that the thermopreferendum decreases at

night. This is obviously of advantage for the species since ambient temperature is usually lower at night.

EXPERIMENT 2

After thigmotaxis other constraints on thermotaxis were studied. First of all, the ambient temperature in the pill bugs' niche was measured. Temperature

measurements were made twice per day (at noon and midnight) during 14 days in late winter and early spring. Air temperature 2 cm above the ground and

shelter temperature were measured with mercury thermometers. The shelter

consisted of a lining of dry leaves close to a wall, under a small tree that was in

turn under a bigger one. The fact that after 14 days of measurements there



were still several animals there shows that measuring procedures did not

interfere too much with the animals. Data are shown in fig. 5. The first six

days are called "Summer" and the other ones "Winter" because mean air

temperature in these periods was 23 ?C and 18?C, which exactly corresponds to Sao Paulo's summer and winter averages. It should be noticed, first, that

changes in shelter temperature are much less steep and pronounced than

changes in air temperature. That is, the shelter is effective. Secondly, when air

temperature is higher than 20?C shelter temperature is lower than air

temperature; when air temperature is lower than 20?C shelter temperature is

higher than air temperature (the sole exception is day 9 at noon). Thirdly,

? 40

S in

I I J

D n=22 (corrected) DAY

0 n=22(corrected) NIGHT

L^

18 20 22 24

TEMPERATURE (?C)

Fig. 4. Distribution of pill bugs around the thermal alley 90 min after entrance. White blocks:

diurnal sessions; striped blocks: nocturnal sessions.

DAYS 28

26 J

Gz22

?5

\??20

I K 18

I 2 3 4 5 6 7 8 9 10 II 12 13 14

HOURS O 12 0 12 0 12 O 12 O 12 O 12 O 12 O 12 O 12 O 12 O 12 O 12 O 12 O 12 O

Fig. 5. Air and shelter temperatures in a pill bugs' natural habitat in late winter and early spring when mean air temperature resembled S?o Paulo's summer and winter mean (o: air; :

shelter).



"Summer" and "Winter" shelter temperature is in the range 17-21?C.

Because this range is about 4?C below the thermopreferendum found in

Experiment 1, it is quite possible that in nature thermotaxis is somehow

modulated by conflicting hygrotaxis, phototaxis, and so on.

The standard thermal tunnel was employed in all studies of this experiment. In one study a black cloth was put on the Plexiglas lid except at the 20-24?C

area (irradiance in this area remained 4 W.m"2; in the covered area it fell to 0.1

W.m-2). Thirty animals were run individually. The results are shown in fig.

6B, white blocks (the data from fig. IB are shown in striped blocks for com

parison). It is clear that a light intensity that is about 30 times as dim as open

sky luminosity is sufficient to put all pill bugs out of their thermopreferendum.

Negative phototaxis has been previously found in Oniscus and Porcellio (cf.

Abbott, 1918), although conflict with thermotaxis was not studied then. On the

other hand, Warburg (1964) found positive phototaxis (illuminance: 800 lux)

Table I

Number of animals in the illuminated side at different moments of a 90 min

session

Time (minutes) 0 5 15 30 60 90

No. of animals 20 11 9 3 1 0

in A. vulg?re. However, before testing the conflict between thermotaxis and

phototaxis I found that pill bugs display negative phototaxis when irradiance is

4 W.m2 (? 300 lux illuminance for a standard incandescent lamp). Twenty animals were put individually in Petri dishes lined with damp filter paper for

24 hours. At the end of this period the dishes were partially covered with black

cloth so that one half of the dish was illuminated and the other was nearly dark

(about 4 lux). Ambient temperature was 25?C. As shown in table I, all animals

were left in the illuminated side at minute zero but nine animals had already

gone to the dark side at minute 5 and no pill bug was in the illuminated side at

minute 90.

In another study the 20-24?C zone was dried with little silica gel rocks

placed under the carpet. The results are shown in fig. 6C (white blocks)

together with the data from fig. IB (striped blocks here). It can be seen that

drying the preferendum altered the distribution, although not as much as

changing light conditions (fig. 6B). Positive hygrotaxis in Armadillidium has

been found in various studies (e.g., Warburg, 1964) but the conflict between

hygrotaxis and thermotaxis has not been previously studied.

Next, the effect of adaptation to previous levels of ambient temperature on

the thermopreferendum of pill bugs was studied. Thirty animals previously acclimated to 12?C for 9-13 days and 30 animals acclimated to 32?C for 38-42



days were tested. Their distribution, together with that of the animals of

Experiment 1 (that had been housed at 22?C), is shown in fig. 6A. Com

parison of the cold adapted group (white blocks) with the normal group (ver tical stripes) shows a slight decrease in thermal preferences, if any. The warm

adapted group (horizontal stripes), on the other hand, shows a marked shift to

the cold region. This compensatory effect, instead of a real acclimation effect, is not always easy to explain but has been found in a number of species, in

cluding lizards (Wilhoft & Anderson, 1960), mice (Baldwin & Ingram, 1968), rats (Carlton & Marks, 1958), and pigs (Baldwin & Ingram, 1968).

20\

TEMPERATURE CCJ

15 20 25 30 35 40

TEMPERATURE PC)

K) 15 20 25 30 35 40

TEMPERATURE TO

Fig. 6. Distribution of pill bugs along the thermal tunnel 90 min after entrance. A, animals

acclimated to three different ambient temperatures; B, white blocks are data from sessions where

the 20-24?C area was more illuminated than the rest and striped blocks are experimental con

trols; C, white blocks are data from sessions where the 20-24?C area was dried and striped blocks

are experimental controls.

EXPERIMENT 3

Thermoregulatory huddling was the subject of this experiment. Groups of

three animals were tested during 100 min in the huddling box (see Materials). Ten groups were tested at each one of three ambient temperatures: 10, 20 and

30?C. Huddling was investigated as follows: (1) the animals were observed 90,

95, and 100 min after the beginning of the session; (2) in each observation a

mark was computed, "one" if the animals were in different squares, "two" if

there were two animals in the same square, and "three" if all animals were in

the same square; (3) the mean of the three marks was considered as a huddling index of that group. The means of the ten indices for each ambient

temperature were: 1.95 (10?C), 1.70 (20?C), and 2.43 (30?C). Analysis of

variance indicated a significant effect of temperature (F= 3.50; df: 2, 27;

/><0.05), due to the difference between 20?C and 30?C (F= 5.63; df: 1, 27;

p<0.03) but not between 10?C and 20?C (F= 0.78; df: 1, 27; />>0.05). The

absence of huddling in the cold is expected in ectothermic animals. On the

other hand, it should be noticed that huddling in the heat may help prevent

evaporative water loss even when relative air humidity is not altered, but this

response has no apparent value for thermor?gulation (in the heat evaporation is used to prevent hyperthermia in most endotherms).



EXPERIMENT 4

The influence of cyclic variations of light and temperature on the daily

rhythm of activity of pill bugs is the subject of the present experiment. So far

only preliminary observations on one animal are available but they are worth

reporting. An adult pill bug (14 mm length, 157 mg weight) was tested in the

activity apparatus described above. The results are shown in fig. 7. Level of

activity is given for 38 consecutive periods of 12 hours. During the first seven

days, when there were neither photoperiodism nor thermoperiodism, there is

no clear diurnal rhythm of activity. There is perhaps a 48 hr cycle (through the

19 days) but this is another matter. From day 8 to day 14, when light and

darkness alternated in 12 hr periods, activity during the light phase was always

higher than during the dark phase. This is in agreement with Arthur et al.'s

X 6 fe?

z\3\4\3\e\rt?\9\io\n\a\a\i4?/3

*A A

L^Lf^?=f=r

17 I IB I 19

LIGHT 9 DARK DID ?r

Fig. 7. Activity of a pill bug during 19 days in the activity apparatus. (When the animal crossed

the cage it interrupted a light beam and hence provided a signal to an event counter.)

(1951) finding that Armadillidium is most active during the morning. From day 15 on, when ambient temperature rose to 29?C during the light phase, the

animal's cycle reversed so that activity was more intense during the night

(except in the first day). This is in agreement with occasional observations I

made while collecting data about temperature in a natural pill bugs' shelter

(fig. 5). Especially on warm days, I used to find more pill bugs walking in the

garden during the night than during the day. This is probably due to the fact

that ambient temperature is milder at night.

EXPERIMENT 5

Because the thermopreferendum of A. vulg?re is about 22?C (see above), and

because its lower lethal temperature is about -2?C or higher (Edney, 1964), the

question arises about the survival of these small animals during winter in



temperate countries. Two thermoregulatory responses that could answer the

question were studied here, viz., burrowing and torpidity. In order to study burrowing I used a glass cylinder (15 x 15 cm) partially

filled with argillous soil. After various observations at 5?C and 25?C I found

no evidence that pill bugs would make burrows. In contrast, it is known that

Oniscus and Porcellio burrow under stones (Kaestner, 1970), but my observa

tions were limited to single animals and argillous soil. Hiding in burrows

already excavated was studied next. A burrow 10 cm depth, 8 mm diameter, tilted 60? vertically was made in each cylinder. Black paper was wound around

the cylinder. The animal's position was recorded 30 min after having been

placed in the cylinder. Ten animals were tested at 25?C and ten at 5?C. Only a

slight effect of temperature was found. Mean depth of animals was 1.6 cm at

25?C and 2.6 cm at 5?C, but the difference is not significant (t =

0.917; df: 18;

/>>0.05).

Table II

Number of pill bugs that recovered from freezing at different ambient

temperatures for different time spans (figures in parentheses are from groups of

juvenile animals)

Duration of exposure Ambient temperature

-20?C -10?C 0?C

1 hr 2 (0) 4 (3) 8 (8) 2hr 0 3

48 hr 5

Since no clear evidence was found of greater burrowing in cold ambiances,

torpidity was studied next. Several groups of 8 animals were placed, one

animal per dish, in Petri dishes lined with lightly moist filter paper and exposed for different time spans to different ambient temperatures inside a refrigerator.

The results are shown in table II. The figures indicate the number of survivors

as checked 24 hr after the end of exposure in each group. Figures in paren theses are from groups of juvenile animals (between 2 and 3 mm long) born in

the vivarium; the rest are from adults (more than 9 mm long). All adult

animals exposed to -20?C were frozen at the end of the session; nevertheless, two out of eight pill bugs exposed for 1 hr recovered from freezing. At the end

of the -10?C sessions all adults exhibited the posture of dead animals (i.e. they were motionless, incompletely curled up, and slanted or easily slantable); nevertheless, half of the subjects exposed for 1 hr recovered from freezing. After exposure to 0?C all animals were torpid and did not run or curl up, as

they usually do when stimulated with a pencil; nevertheless, a good number of



them endured 48 hr of cooling and none succumbed to the 1 hr exposure. Tor

pidity, therefore, is a mechanism that can be used by pill bugs of temperate

regions to withstand winter. Juveniles and adults respond similarly (table II),

though in mammals the young survive deeper hypothermia than adults (e.g.,

Popovic & Popovic, 1963).

EXPERIMENT 6

This last experiment investigated whether pill bugs would learn a thermo

regulatory response. The efficacy of thermal stimuli as reinforcers has been

shown in numberless animals, from molluscs (Downey & Jahan-Parwar, 1972) to primates (Carlisle, 1971).

In this experiment the Y-maze described above was used. Floor temperature in the starting box and in one of the goal boxes was 32?C; the other goal box

was at 17?C. A moist cloth lined the entire maze and was not changed during the 40 consecutive trials of each animal. Thus, the subjects were free to

associate floor temperature with wall brightness (see Materials) and/or any odor they were leaving on the cloth. Twelve animals were tested, the cold rein

forcer being at the left side for six subjects and at the right side for the others.

Twelve controls were also run when the entire maze was at 20?C. Only the

choices made by each animal in the last 10 trials were used in the data analysis, as follows: (1) in the experimental group the number of choices of 17?C was us

ed; (2) in the control group the number of choices of the most frequently chosen

goal box was used; (3) the mean number of choices of both groups was com

pared. The experimental group had a mean of 7.50 and the control group a

mean of 5.17. The difference is significant (/= 2.757; df: 22; p<0.05) and thus

it may be concluded that the experimental animals learned to escape the warm

stimulus.

GENERAL DISCUSSION

It seems that pill bugs, Armadillidium vulg?re, are able to choose a shelter that

renders the changes in air temperature less steep and less intense; all over the

year shelter temperature may remain in the range of about 18? to21?C (fig. 5).

Among terrestrial isopods, A. vulg?re is one of the species that are most

resistant to low humidity (Edney, 1960), being exceeded, as far as known, only

by desertic forms such as Venezillo arizonicus (Mulaik, 1942) (cf. Warburg,

1965). Nevertheless, the high humidity found in the shelters must certainly be

at least as important as temperature in the choice of a shelter. First, because

the thermopreferendum of the species is in the range 22? to 23?C (fig. 4), that

is, about 3?C above the measured shelter temperature; this suggests a conflict

of preferences. Second, drying the preferendum in a thermal gradient shifts the

preferred zone (fig. 6C). Third, the relative scatter in the thermopreferendum

histogram (fig. 4) shows that a population of pill bugs is unable to choose a



clear-cut thermal zone. Anyway, the resistance of pill bugs to desiccation is

intimately linked to ambient temperature (Edney, 1951). Also important in the choice of a shelter is the presence of corners or

something alike, for pill bugs display strong thigmotaxis (fig. 1A) which can

modify the thermotactic responses (figs. IB, 2, 3). Besides, light intensities well

below open sky luminosity also seem to direct the choice of a shelter as far as

they can provoke a radical emptying of the thermal preference zone (fig. 6B).

Also, A. vulg?re usually displays negative phototaxis to relatively dim light at

low ambient temperature but may display a positive reaction if temperature increases (Henke, 1931; as A. cinereum (Panzer, 1798)), and changes the

positive reaction into a negative reaction if ambient temperature is even higher

(Warburg, 1964). Thus, Armadillidium presumably goes to the warm sunlight when it is cold and ambient temperature is increasing, and seeks a shelter when

sunlight is too warm, an example of thermoregulatory behavior guided by

photoreactions as well as by thermoreactions.

When, however, the pill bug can not find a suitable shelter, many other

behaviors may be employed in thermor?gulation. Its lower and upper lethal

temperatures are about -2?C and 36?C, respectively (Edney, 1964). Within

this range, it may huddle with conspecifics when exposed to elevated

temperatures (Exp. 3). During the night, its thermopreferendum is decreased

(fig. 4), thus assuring a better adaptation to the lower temperatures of the

night. Perhaps also a change in the tolerance to desiccation occurs, as far as

Cloudsley-Thompson (1952) found in Oniscus a difference between the intensi

ty of the humidity reaction of animals tested in the light and in the dark. Fur

thermore, though A. vulg?re is a diurnal animal it may be more active during the night if temperature in the light period is increased (fig. 7). Pill bugs can

also benefit from the advantages of the capacity to learn relations between ther

mal stimuli and visual and olfactory stimuli (Exp. 6). In addition, acclimation

to high or low temperatures shifts their thermopreferendum downwards (fig.

6A). Finally, it is known that they do not expose their offspring to cold

temperatures as far as reproduction takes place mainly during periods of long

days (i.e., about summer) or in response to sudden increases in ambient

temperature (Madhavan & Shribbs, 1981). In temperate countries, however, the pill bug must face, during winter,

temperatures well below its lower lethal limit, even when it is inside its shelter.

On this matter, it is known that acclimation can decrease the lethal limit a few

degrees Celsius (Edney, 1964). But this will probably not help too much.

Evidence of burrowing in the cold, on the other hand, was not found (Exp. 5). It seems, however, that pill bugs are able to enter in a state of dormancy when

ambient temperature falls below 0?C (table II) and this probably assures their

survival in cold winters when ambient temperature is way below their thermal

optimum.



ACKNOWLEDGEMENTS

The author is indebted to J. C. Ribeiro and Renato Refinetti who helped in

the elaboration of various apparatuses. Thanks are also due to D. F. Ventura

for comments and suggestions, to R. M. Refinetti, to J. A. Gon?alves, and to

K. B. Tiedemann. The experiments were done while the author was on a

CNPq fellowship.

ZUSAMMENFASSUNG

Diese Arbeit befa?t sich mit dem Verhalten der Rollassel Armadillidium vulg?re (Latreille,

1804), das zum Temperaturausgleich f?hrt. Es wurde beobachtet, da? diese Landisopoden

Unterschl?pfe suchen, in denen die Temperaturschwankungen der Umgebung gemindert wer

den. In Laboratoriums versuchen zeigte sich die Rollassel in der Lage, in einem W?rmegradien ten ein gewisses Temperaturgebiet (22-23?C) mit einer relativen Genauigkeit zu w?hlen. Diese

Vorzugstemperatur kann leicht durch einen Konflikt zwischen der Thermotaxis und der Thig

motaxis, Phototaxis oder Hygrotaxis ver?ndert werden. Des weiteren kann diese Vorzugstempe ratur durch vorherige Gew?hnung an K?lte (12?C) oder W?rme (32?C)

um einige Grade nach

unten verschoben werden. Unter W?rmeeinflu? gesellen sich die Rollasseln zu Gruppen zusam

men, was wahrscheinlich zu einem geringeren Wasserverlust f?hrt. Eine andere wichtige Eigen schaft des Verhaltens dieses Tieres ist die M?glichkeit, Verbindungen zwischen thermischen und

optischen oder chemischen Reizen zu lernen. Es wurden keine Beweise gefunden, da? die Roll

assel sich bei K?lte in tiefere Erdl?cher verkriecht; jedoch wurde beobachtet, da? bei Temperatu ren unter dem Gefrierpunkt die Rollassel in ein Schlafstadium verfallt. Zuletzt wurde noch fest

gestellt, da? die Rollassel, obwohl sie tagaktiv ist, diesen Zyklus umkehren kann, wenn die Tem

peraturen in der Helligkeitsphase erh?ht (30?C) und in der Dunkelphase neutral (20?C) gelassen werden.

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Received for publication 7 December 1982.


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