Table Of ContentZOOLOGICAL SCIENCE 10: 505-509 (1993) © 1993 Zoological SocietyofJapan
The Behavioral Reactions of a Snake and a Turtle
to Abrupt Decreases in Gravity
Richard Wassersug1 and Akemi Izumi-Kurotani2
1Department ofAnatomy and Neurobiology, Faculty ofMedicine, Sir Charles
Tupper Medical Building, Dalhousie University, Halifax, Nova Scotia,
B3H 4H7, Canada, and 2Space Utilization Research Center, Institute
ofSpace andAstronautical Science, 3-1-1, Yoshino-dai
Sagamihara, Kanagawa 229, Japan
—
ABSTRACT Wereporthereonthebehavioralreactionoftworeptilestoabruptdecreasesingravity.
One striped rat snake, Elaphequadrivirgata, and three striped-neckpond turtles, Mauremysjaponica,
were exposed to microgravity (/u-G) on parabolic flight, during the filming of a documentary for the
NHKtelevision station in Japan. The video films revealed thatthe—snake reflexively responded to the
shift from hyper- to hypogravity by taking up a defensive posture on the first parabola, the snake
struck at itself. The turtles actively extended their limbs and hyper-extended their neck in /i-G, a
posture which is identical to that displayed during their contact "righting reflex", when placed
upside-down in normal gravity. The aggressive display of the snake was unexpected, although the
rightingresponse ofthe turtleswasconsistentwith thatshown byothervertebrates, includingfish and
mammals, exposed to fi-G. An implication of these observations is that the afferent signal for the
rightingreflexofvertebratesinnormalgravitymustbetheunloadingofventralreceptorsinthesensory
system, rather than the loading of dorsal receptors. These are the first behavioral records for any
reptiles exposed to hypogravity.
animal will react, for example, in freefall?
INTRODUCTION Earlyworkwithteleostfishes [e.g. 5, 6] suggests
that aquatic vertebrates reflexively pitch down-
In the nearly half century that man has been wardinp-Gandthatthisleadstolooping(forward
exploringspace,aplethoraoforganismshavebeen somersaults). More recent studies, however, with
exposed to microgravity (p-G) either briefly, on a larger variety of aquatic species (Wassersug,
parabolic flights, or for longer periods, on orbital unpublished data) suggest that such forward loop-
missions. Several birds, reptiles, amphibians and ing is not characteristic of all lower vertebrates
fishes, as well as a large variety of mammals have exposed to p-G. Some amphibian larvae, for
all beenexposedtop-G [2]. Mostofthisworkhas example, make forward somersaults (e.g. Xeno-
focused on the physiological consequences of re- pus), whereas others make backward somersaults
duced gravity. Surprisingly little attention has (e.g. Bufo). Others (e.g. Rana) float freely and
been given to the reflexive behaviors of these stillotherstwistandrollalongtheirlongaxiswhile
organisms upon their initial exposure to micro- swimming forward in short dashes [3, 7, 9, 10].
gravity. It is not known, for example, whether Clearly, more animals will have to be examined
there are consistent patterns in the reflexive re- before systematic patterns in the behavioral re-
sponses of animals to abrupt changes from hyper- sponses ofvertebrates to decreased gravity can be
to hypo-G. Do the responses of various verte- revealed. Ultimately, if behavioral research in
brates correlate with their phylogenetic rela- gravitation biology is to become a predictive sci-
tionships or way of life? Can we predict how any ence, such patterns should exist and be identi-
fiable.
Accepted March 16, 1993 As asteptowardsproducingabroaderdatabase
Received October28, 1992 on the behavioral responses of vertebrates to de-
506 R. Wassersug and A. Izumi-Kurotani
creased gravity, we report here on the behavior of meter to a third of a meter respectively. The
a snake and three turtles exposed to changing aquarium was braced in the pressurized, tempera-
gravity in parabolic flight. The behavior was ture-controlled cabin of a Mitsubishi MU 300
videotaped in the early spring of 1992 by the aircraft. A fix-mounted Sony Hi 8 video camera
Japanese television station NHK, in preparation continuously filmed the animals throughout their
fortheirApril6th, 1992televisionprogram "Kura- parabolic flights. The snake and turtles were each
bete Mireba" (Comparative Ethology for the exposed to eight parabolas. The parabolic ma-
General Public). Although the film sequences neuvers were performed between 6.6 and 8.5 km
discussed here were not used in the final produc- elevation and provided in excess of 15-18sec of
tion of the documentary, they were graciously fi-G (i.e. G<10~3), with intervening hyper-G
made available to us for study. episodes of approximately 2-G.
Tothebestofourknowledge, therearenoother
records of the behavior of reptiles in parabolic
RESULTS
flight. The great morphological difference be-
tween a snake and a turtle and their dramatically
different responses, as noted below, emphasize Snake
how different the responses of organisms to de- Before the first parabola, the snake was actively
creased gravity can be. exploring its cage. The animal had climbed the
verticaledgewiththefronthalfofitsbody andwas
MATERIALS AND METHODS probing an upper corner with its head, as if
searching for a crack or crevice to enter. As the
The snake used in this experiment was a single aircraft entered /x-G on the first parabola, the
specimen of the common striped rat snake of snake immediately retracted its head into three
Japan, Elaphe quadrivirgata. This an active, tight curves. The animal thrashed aboutviolently,
semi-arboreal snake. The turtles used were speci- twisting and rolling. Three seconds into p.-G, a
mens of the Japanese striped-neck pond turtle mid-portion of the snake's body came within
Mauremys [Clemmys] japonica. All specimens approximately 10cm ofits head. At that moment
were on loan to NHK from a local pet store in the snake struck at itself (Fig. 1). As soon as the
Nagoya, Japan, and were returned to that store at head hit the body, it was withdrawn. The action
the end of the mission. Species identifications was so fast that we could not confirm from the
were confirmed by the supplier, but regrettably no video images (only alternate ones of which are
other information on the specimens was recorded. shown in Fig. 1) whether the mouth was open
Judgingfrom the size ofthe containers holding the during this snout-body contact or whether teeth
animals during the flight, we estimated that the were planted in the skin.
snake was 75 cm long. The carapace lengths for For the remainder of the parabola the snake's
the three turtles were similarly estimated at 6-8 head stayed cocked, as ifprepared to strike again.
cm, 10-12cm and 13-15 cm respectively. All At the initiation ofreduced gravity on each subse-
animals were active and in clearly good health. quent parabola, the snake immediately cocked its
The behaviorofan additional turtle ofthe same head into the pre-strike posture just described.
species and size of the largest turtles exposed to Additional strikes, however, were not observed.
fi-G was examined in the laboratory atthe Biology On the 3rd, 4th and 6th parabolas, the animal
Department of Shimane University, Matsue, successfully braced a portion of its body between
Japan. the top and bottom of its aquarium and stayed in
The snake was flown alone; the three turtles contact with the container throughout p-G. This
were flown together. For flight the animals were bracingeliminatedmostofthe chaotictwistingand
housed in a simple, smooth-sided aquarium with- rolling seen in the earlier parabolas.
out water. The maximum and minimum dimen- The snake's response to the hyper-G phase of
sionsoftheircontainerswere on the orderofhalfa the parabolic trajectory before its first and subse-
Reptiles in Microgravity 507
quent exposure to ju-G was, in contrast, subdued. body elevated during hyper-G, it could be seen
Whenever G increased from <1 to >1 the snake straining to maintain its posture. However, at no
was, understandably, forced toward the bottom of timeinhyper-Gdiditrespondeitherhyperactively
itscontainer. When the animal hadaportionofits or aggressively, as it did during the shift from
hyper-G to hypo-G on the first parabola.
Turtles
The reaction of the turtles to reduced G, in
contrast to that of the snake's, was slower and
more subdued. At the onset of /u-G, the turtles
either stayed in contact with a substrate or were
thrownbetweensurfacesduetofluctuation intheir
acceleration relative to that of the aircraft. The
turtles had no control over their trajectory in pt-G
and tumbled until they hit a wall or one another.
They did not withdraw into their shells. On the
contrary, they extended their necks and raised
their heads while at the same time fully extending
andelevatingtheirlimbs (Fig. 2). Thedigits, most
notably on the hind limbs, were spread while the
foot was rotated along the long axis of the limb,
Fig.2. A video image of a pond turtle, Mauremys
japonica, inmicrogravity. Notethehyper-extension
of the neck and the asymmetric dorsal deviation of
the extended limbs. The same hyper-extension of
head and limbs is used by M. japonica in normal
gravity to generate torque through its long axis and
thustorightitselfwhenupside-downbyrollingover.
The video imagehasbeencomputerenhancedasin
Fig. 1.
Fig. 1. Four sequential video frames of the rat snake,
Elaphe quadrivirgata, in microgravity. In the first
frame (a) the snake's head is in the middle of the
field. In the subsequent two frames (b, c), the
snake's snout strikes its body then descends to the
bottom left of the field (d). The frames are sepa-
rated by 20msec. The video images have been
computer enhanced to remove extraneous reflec-
tions from the container's walls.
,
508 R. Wassersug and A. Izumi-Kurotani
bringing the anterior, leading edge upward. The On the other hand, Elaphe snakes are naturally
impression created was one ofthe animal tryingto preyed upon by hawks in Japan and they occa-
reach or contact, with its head and limbs, objects sionally experience aerial suspension when cap-
dorsal to it. The limbs on both sides were not tured. In this situation, it is in the snake's best
extended or elevated equally; that is, the maneu- interest to strike, even to strike blindly! Such a
ver was not performed symmetrically. response may have been demonstrated by E.
The dorsal extension just described was exhi- quadrivirgata duringthe shift from hyper- to hypo-
bited by a turtle during normal gravity in the G.
aircraft when it "landed" upside-down. The pos- Snakesvarygreatlyin theirresponse totiltingin
ture was used by the turtle specifically to right 1-G, depending on whether they are terrestrial or
itself. IfwascompletelyduplicatedbyM.japonica arboreal [4]. In thisregard, itwouldbe particular-
in the laboratory at Shimane University by simply ly interesting to see whether other snakes that are
putting the turtle upside-down on a styrofoam more or less arboreal than Elaphe show the same
sheet. In that position, the turtle was able to defensive response in /u-G and parabolic flight.
contact the surface with its extended snout and The turtles responded to p-G as if they were
claws and hold itself in place, such that it could upside-down [1]. This has implications to under-
quickly flip over, i.e. "roll" in aviation parlance. standing the stimulus for their righting reflex in
On the smooth surface ofthe flight container, the 1-G. Specifically, the afferentsignal forthe hyper-
maneuver was futile except in one case involving extension of the neck and limbs used in the right-
the smallest turtle. ing maneuver cannot be the loading of dorsal
The turtles showed little response to either the sensory receptors. Ratherit must be w«loading of
initial or subsequent episodes ofhyper-G. Ifthey ventral receptors.
were free floatingwhen G shifted from <1 to >1 Hyper-extension of the axial skeleton with
they were propelled toward the bottom of their asymmetrical limb movements has been observed
aquarium. They did not, however, retreat into in other vertebrates in fi-G. The combined limb
theirshells orexhibitothersignsofundue stressin and axial movements lead to long-axis rotation, or
hyper-G. No progressive changes in the behavior rolling. In 1-Gthisappearstobeanimportantpart
of the turtles were seen as they went through the of a righting reflex best known in arboreal and
multiple parabolas. semi-arboreal vertebrates, such as the cat. The
same maneuver is seen, however, in a variety of
less arboreal animals in /u-G. These range from
DISCUSSION
aquatic animals, such as the adult clawed frog
The behavior ofreptiles in decreasing G can be (Xenopus) and salamander larvae [3, 8], to strictly
readily understood as a manifestation ofbehaviors terrestrial mammals, such as the rabbit (on the
that theyshowin 1-Gunderspecial circumstances. NHK video film, unpublished data). What distin-
There is nothing in their behavioral repertoire guishes these behaviors in /x-G from the 1-G
duringparabolic flight that can be saidto be either situation is that they are more repetitive and
G or "space specific." The behaviorthat the snake protracted in freefall, simply because they are not
exhibited was, however, quite different from that effective. The ability to duplicate these displays in
of the turtle. turtles and many other animals bysimply inverting
The cocked neck and strike shown by E. quadri- them supports the conclusion that they are man-
virgata as G decreased was clearly of a defensive ifestations of a natural righting reflex.
sort. The writhing and twisting, particularly in
early parabolas, is indistinguishable from that of ACKNOWLEDGMENTS
the normal frightened and threatened E. quadri-
virgata. The fact that the snake actually struck at We thank Dr. M. Yamashita and NHK television for
itself suggests that the animal suffered loss of facilitating access to videofilms of animals in micrograv-
ity. Laboratory space at Shimane University was gra-
proprioceptive clues about body position in ju-G. ciously provided by Dr. T. Naitoh. Drs. R. Marlow and
Reptiles in Microgravity 509
B. Young helped us access relevant literature. Mr. S. OppenheimerJM, SalinasGA, von Baumgarten RJ
Pronych and Ms. M. Fejtek prepared the illustrations. (1976) Killifish hatching and orientation (Experi-
Dr. H. Lillywhite, Mr. S. Pronych and Ms. M. Fejtek ment MA-161), Apollo-Soyuz Test Project Pre-
reviewed drafts of the manuscript. This work was liminary Science Report. In "NASA Technical
supported by Canada's Space Agency and its Natural Memorandum X-58173" Washington DC, pp281-
Science and Engineering Research Council, as well as a 305
grant from the Japan Science and Technology Fund. 6 Von Baumgarten RJ, Baldrighi G, ShillingerJr GL
(1972) Vestibularbehavioroffishduringdiminished
G-force and weightlessness. Aerospace Med 43:
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