Zoology 108 (2005) 107–120
The behavioral responses of amphibians and reptiles to microgravity on
Richard J. Wassersuga,?, Lesley Robertsb, Jenny Gimianb, Elizabeth Hughesb,
Ryan Saundersb, Darren Devisonb, Jonathan Woodburyb, James C. O’Reillyc
aDepartment of Anatomy & Neurobiology, Sir Charles Tupper Medical Building, 5850 College Street, Dalhousie University,
Halifax, Nova Scotia, Canada B3H 1X5
bArmbrae Academy, 1400 Oxford Street, Halifax, Nova Scotia, Canada B3H 3Y8
cDepartment of Biology, Cox Science Center, University of Miami, Coral Gables, FL 33124-0421, USA
Received 4 February 2005; accepted 2 March 2005
In the present study, we exposed 53 animals from 23 different species of amphibians and reptiles to microgravity
(mg). This nearly doubles the number of amphibians and reptiles observed so far in mg. The animals were flown on a
parabolic flight, which provided 20–25s of mg, to better characterize behavioral reactions to abrupt exposure to mg.
Highly fossorial limbless caecilians and amphisbaenians showed relatively limited movement in mg. Limbed
quadrupedal reptiles that were non-arboreal in the genera Leiocephalus, Anolis, and Scincella showed the typical
righting response and enormous amounts of body motion and tail rotation, which we interpreted as both righting
responses and futile actions to grasp the substrate. Both arboreal and non-arboreal geckos in the genera Uroplatus,
Palmatogecko, Stenodactylus, Tarentola, and Eublepharis instead showed a skydiving posture previously reported for
highly arboreal anurans. Some snakes, in the genera Thamnophis and Elaphe, which typically thrashed and rolled in mg,
managed to knot their own bodies with their tails and immediately became quiescent. This suggests that these reptiles
gave stable physical contact, which would indicate that they were not falling, primacy over vestibular input that
indicated that they were in freefall. The fact that they became quiet upon self-embrace further suggests a failure to
distinguish self from non-self. The patterns of behavior seen in amphibians and reptiles in mg can be explained in light
of their normal ecology and taxonomic relations.
r 2005 Elsevier GmbH. All rights reserved.
Keywords: Amphibians; Reptiles; Behavior; Microgravity; Parabolic flight
Although few vertebrate species have been observed
in microgravity (mg), certain common behavioral pat-
terns have been observed. Just as a cat will roll over if
dropped upside down from a height, most vertebrates
interpret mg as if they were upside down, and attempt to
roll over (Wassersug, 2001). In mg this leads to repeated
long-axis rolling, which has been interpreted as a
repetitive righting response, where the animals receive
no feedback that the action was successfully executed.
Such behavior has been seen in various mammals, frogs,
ARTICLE IN PRESS
0944-2006/$-see front matter r 2005 Elsevier GmbH. All rights reserved.
E-mail address: email@example.com (R.J. Wassersug).
However, some more unusual and unexpected beha-
viors have been observed for amphibians and reptiles in
mg, including an aggressive display by a snake towards
its own body (Wassersug and Izumi-Kurotani, 1993),
immobility in a caecilian (Wassersug, 2001), and sky-
diving postures in certain tree frogs (Naitoh et al., 2001;
Izumi-Kurotani et al., 1994). Wassersug and Izumi-
Kurotani (1993) hypothesized that the snake’s reaction
was the result of a loss of proprioception, such that the
snake did not recognize its own body as a part of itself.
The explanation for why the caecilian went limp is not
known, but one hypothesis is that highly fossorial
limbless animals, like the caecilian, that are never
exposed to reduced gravity such as during a fall may
not have strong defensive righting responses.
Based on our interest in the reaction of that caecilian
to mg, we examined here the reactions of other elongated
and limbless amphibians and reptiles to mg. In addition,
in order to determine whether there are phylogenetically
consistent patterns to how poikilothermic tetrapods
respond to mg, independent of their ecology (e.g.,
fossorial) or morphology (e.g., limbless), we examined
closely related genera in the infraorder Gekkota,
ranging from a limbless terrestrial pygopodid to limbed
arboreal geckos. Similarly, we examined a morphologi-
cally and ecologically diverse group of lizards within a
single family, the Scincidae, that also ranged from
limbless and fossorial to fully limbed and terrestrial.
A common reaction to mg, experienced by humans
and other mammals, is motion sickness (Crampton,
1990). Previous work has shown that most amphibians
are relatively immune to motion sickness in parabolic
flight, although some frogs do exhibit emesis after
exposure to multiple parabolas (Wassersug et al., 1993;
Naitoh et al., 2001). How sensitive reptiles are to mg-
induced emesis is not known. Thus we provide here
some data on that question.
Lastly, since most tetrapods react to freefall as if they
are upside down and initiate righting responses, the
question can be asked whether vertebrates that naturally
spend time inverted similarly show righting responses in
mg. This question has been tentatively explored for a bat
(Fejtek et al., 1995), but not for any poikilothermic
tetrapods. This inspired us to look at the reaction of the
hog-nosed snake Heterodon in mg compared to other
colubrids. Heterodon is unusual in that when frightened
in the normal 1g environment it will roll on its back and
Materials and methods
Fifty-three animals from 23 species (Table 1) were
flown aboard the Falcon 20 aircraft on March 30, 2004.
The amphibians examined were all caecilians (families
Ichthyophiidae and Caeciliidae). The reptiles included
worm lizards (Amphisbaenidae), glass lizards (Angui-
dae), curly tailed lizards (Tropiduridae), legless lizards
(Pygopodidae), geckos (Gekkonidae), anoles (Iguani-
dae), skinks (Scincidae), and snakes (Colubridae). We
selected species to study that were easily maintained in
captivity, neither rare nor endangered and not toxic.
They ranged from highly fossorial to highly arboreal
species and were meant to expand the ecological,
morphological and taxonomic diversity of the amphi-
bians and reptiles previously exposed to mg. The
majority of the specimens (i.e., Ophisaurus ventralis,
Lialis jicari, Thamnophis sauritus, Elaphe obsoleta,
Geocalamus acutus, Ichthyophis kohtaoensis, Dermophis
mexicanus, Chalicides ocellatus, Scincella lateralis, Py-
gomeles braconnieri, Leposternon microcephalum, and
Isopachys gyldenstolpei) were either collected by J.C.
O’Reilly or purchased from Glades Herp Inc. in Ft.
Myers, FL. They were express shipped from Florida to
Nova Scotia arriving 12 days before flight. The other
species (i.e., Elaphe bairdi, Heterodon platyrhinos,
Eublepharis macularius, Tarentola chazaliae, Uroplatus
guentheri, Uroplatus henkeli, Stenodactylus sthenodacty-
lus, and Palmatogecko rangei) were borrowed from local
collectors in Nova Scotia 4–10 days before the flight.
The remaining reptiles (i.e., Anolis carolinensis, and
Leiocephalus personatus) were purchased in the Halifax,
Nova Scotia area from a commercial supplier (Pets
Unlimited) a week before flight.
The animals were maintained in an animal care
facility at Dalhousie University to give them time to
recover from shipping, and to confirm that they were
healthy and feeding. They were kept in containers that
had variously sand, soil, wood chips, or paper towels on
the bottom, depending on the ecology of the animals.
Those that were fossorial were kept with enough
substrate to allow them to burrow freely. The tropical
reptiles were provided with either a heat lamp or heat
pad at one end of their container to give them access to a
graded thermal source. Water dishes were provided as
appropriate. Other holding containers were spray
misted, to help keep the humidity high and prevent the
animals from dehydrating.
The majority of the amphibians and reptiles were fed
either mealworms or crickets. The caecilians were fed
bloodworms. The Thamnophis were fed guppies placed
in their drinking water and the Elaphe were provided
with frozen, then thawed, rat pups. The Lialis were
given live S. lateralis or A. carolinensis for food.
Only animals that appeared healthy, active and
presumably feeding (assumed rather than confirmed
for some of the fossorial species, where food placed on
the top of the soil in their terraria disappeared over a
course of 2 days) were actually flown. [One exception,
the Leposternon, was flown even though it had reddish
skin and did not appear as healthy as the others.] The
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120 108
ARTICLE IN PRESS
Table 1. General information on the 23 species and 53 specimens exposed in this study
Ichthyophis kohtaoensis (Ichthyophiidae) – The Koh Tao Island Caecilian, from Southeast Asia, is a highly fossorial, active
burrower, which may ascend to the surface at night or during wet weather. (4: 34, 34, 35, 36)
Dermophis mexicanus (Caeciliidae) – The Mexican Burrowing Caecilian, from Central America, is a highly fossorial caecilian, which
actively burrows, but may leave its burrows at dusk to seek food. (4: 23, 38, 40, 32)
Elaphe obsoleta (Colubridae) – The Black Ratsnake, common throughout midwestern North America, is a semi-arboreal animal
that prefers heavily wooded habitats. (3: 38, 40a, 38)
Elaphe bairdi (Colubridae) – The Baird’s Ratsnake, found in the southwestern United States, prefers a habitat of dry, rocky terrain.
It is mainly terrestrial. (5: 36, 46, 43, 40, 45)
Thamnophis sauritus (Colubridae) – The Eastern Ribbonsnake, from eastern North America, is a thin, fast snake that is active
during the day, and may climb up onto low branches and tall grass to hunt for aquatic amphibians and fish in ponds and pools
below. Its preferred habitat is in vegetation along the banks of swamps, ponds, and other small bodies of water. (3: 45, 35a, 43)
Heterodon platyrhinos (Colubridae) – The Eastern Hognose Snake is a terrestrial snake found in woods and fields in much of the
eastern USA. It prefers sandy or loamy soil in which it can burrow. Wild-caught H. platyrhinos will feign death in stressful
situations, rolling over on its back and remaining limp. If then righted, it will commonly roll onto its back again. (1: 38)
Geocalamus acutus (Amphisbaenidae) – The Tanganyika Wedge-snouted Worm Lizard, from Tanzania, is a terrestrial limbless
reptile that lives in sandy soils. It is an active burrower. G. acutus is a highly fossorial animal, hardly ever seen above the ground. (3:
22, 27, 24)
Leposternon microcephalum (Amphisbaenidae) – The Small Head Worm Lizard, from the Amazon River basin, is a terrestrial
burrower, which rarely comes above the surface, spending most of its life underground. (2: 26, 30)
Ophisaurus ventralis (Anguidae) – The Eastern Glass Lizard, native to the Coastal Plains of the eastern USA, is a semi-fossorial
limbless lizard. It is fast moving when above ground. (2: 38, 48)
Anolis carolinensis (Iguanidae) – The green anole, native to southeastern North America, is a fast, agile, arboreal lizard that is
mainly found in trees and shrubs. (2: 13, 15)
Leiocephalus personatus (Tropiduridae) – L. personatus, native to the Caribbean, is a fast moving terrestrial lizard. Its preferred
habitat is warm sandy regions. (2: 14, 12)
Leiocephalus shreibersi (Tropiduridae) – Shreiber’s Curly Tailed Lizard, also known as the Red-sided Curlytail Lizard, is native to
Hispaniola. It is a terrestrial animal and lives mainly on sandy terrain, preferring hot, arid, open areas. L. shreibersi may burrow in
warm sand to hide. (2: 19, 21)
Isopachys gyldenstolpei (Scincidae) – The Gyldenstolpe’s Worm Skink, also known as the Malayan Striped Limbless Skink, is found
in Thailand and Burma. It is a fossorial limbless lizard that burrows in moist soil, and very rarely surfaces. (1: 24)
Pygomeles braconnieri (Scincidae) – The Short Skink, also known as the Malagasy Sand Swimming Skink, is native to Madagascar.
It is a fossorial limbless lizard that burrows mainly in sand. (1: 23)
Chalcides ocellatus (Scincidae) – The Ocellated Skink, native to southwest Europe, northern Africa, and western Asia, prefers dry,
rocky or sandy terrain. It is fossorial and will burrow under stones or loose topsoil. (1: 12)
Scincella lateralis (Scincidae) – The Little Brown Skink, common throughout southern North America and Central America, is a
ground-dwelling animal. Its natural habitat is on the forest floor hiding in leaves during the day. (3: 11a, 7.5, 12)
Lialis jicari (Pygopodidae) – The New Guinea Legless Lizard, found throughout southern New Guinea and Indonesia, is active
during the daytime and is found mostly on top of the soil. It hides under loose debris and vegetation. Lialis are terrestrial animals
that remain mainly above ground. (3: 50, 42a, 37)
Palmatogecko rangei (Gekkonidae) – The Web-footed Gecko, from the Namib Desert, is terrestrial and uses its webbed feet to run
on sand. It burrows during the day and forages on the surface at night. (1: 9)
Stenodactylus sthenodactylus (Gekkonidae) – The Dune Gecko, native to northern Africa and southwest Asia, is a terrestrial,
nocturnal gecko that burrows under rocks and debris during the day. (1: 8)
Tarentola chazaliae (Gekkonidae) – The Helmeted Gecko, native to Northwest Africa, is terrestrial and hides under rocks, debris,
and camel dung, emerging only to bask in the sun or to forage for food. (1: 9)
Uroplatus guentheri (Gekkonidae) – Gunther’s Leaftail Gecko, from the dry deciduous forests of Madagascar, is arboreal and hides
during the day. (1: 11a)
Uroplatus henkeli (Gekkonidae) – Henkel’s Leaftail Gecko, also from Madagascar, is an arboreal nocturnal gecko that hides under
rocks or wood during the day. (1: 9)
Eublepharis macularius (Gekkonidae) – The Leopard Gecko is a terrestrial nocturnal lizard native to southern Asia. It is a slow
moving, ground dwelling gecko that inhabits arid regions, particularly rocky deserts and sparse grasslands. It avoids sandy deserts.
The bold number in parentheses after each species is the number of specimens for which we had one or more good video records from the parabolic
flights. The numbers that follow are the total lengths in centimeters of those specimens.
aThis animal was flown twice.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120109
animal care procedures and the use of the animals in the
experiment were approved by the Dalhousie University
Committee on Laboratory Animals and by the Cana-
dian National Research Council (Protocol Number 03-
096), who owned and operated the Falcon aircraft.
Two different sized tanks were used for the parabolic
flight, depending on the size of the animal. The smaller
containers were clear plastic terraria with dimensions
37cm, 25cm, 22cm (Faunarium, PT-2265, Hagen). A
stiff plastic sheet was fitted to the top of each small tank,
and then anchored in place underneath the original
snap-down plastic covers.
The larger containers were each composed of two,
large-sized terraria with dimensions 46cm, 34cm, 30cm
(Reptile Den Flat Homes, PT-2310, Hagen). These
containers were composed of two reptile dens each of
dimensions 46cm, 17cm, 30cm, with one inverted and
placed on top of the other.
The two containers were held together by hinges made
of twisted wire run through holes drilled in the abutting
plastic lips at the top and back of each container. The lip
at the front of the tank (i.e., the side facing the camera)
was removed with a sanding tool. Clear plastic tape was
used to seal the seam between the two tanks during the
flight. It was also used to cover slits in the sides of the
tanks. A Velcro strip was also used to seal the seam
between the two containers on the sides of the tanks.
The plastic feet on the tanks were abraded away, so
the tanks would sit flat on holding racks in the aircraft.
A few of the larger containers were fitted with a sheet of
foam glued to the bottom to hold water for the
All sides of the tanks, except for the front, were spray
painted with flat white paint so that the animals could
not see neighboring containers and were in a largely
muted, uniform environment with little visual detail or
landmarks. When mounted on the aircraft, the front
faces of the tanks were separated by the center aisle
(42cm wide) down the plane; this meant that the nearest
any animal visually to another was 460cm, and for
most of these animals (particularly the fossorial species,
with reduced eyes), beyond their visual range.
A small patch of unpainted space was left on each side
of the tank for lights. Two 13W, 6500K compact
fluorescent lights (SL-507, Budget Lighting Inc.) were
held by brackets to the tank, over these unpainted areas.
A total of 8 large and 12 small containers were
mounted on specially built racks in the Falcon 20
aircraft. Although we ideally wanted the longest axis of
the animals we flew to be shorter than the shortest axis of
the tanks in which they were tested, this was not always
possible because of the large size of some of the animals
available to us. Foam strips underneath each tank were
used to reduce vibration. Taut bungee cords held the
tanks in place. The ends of the cords were clipped onto
hooks built into the racks on either side of the tanks.
For each container, there was a dedicated camera
mounted on an opposing rack across the center aisle
of the aircraft. There were 17 Panasonic PalmCams
(PV-DC 152), one Panasonic PalmCorder, and two
Sony Digital8 Handycams (DCR-TRV 250 & DCR-
The animals were transported in their holding tanks
to a hangar at the Halifax International Airport a day
before the flight and were maintained overnight in a
heated room with the same heat pads and heat lamps
used at Dalhousie University.
An effort was made to feed as many of the animals as
possible before the flight. The majority of the animals
were provided food ad libitum immediately prior to the
flight; none was force fed, as we did not want to stress
the animals. The Heterodon, Dermophis, E. obsoleta, E.
bairdi, Anolis, Geocalamus, and Scincella were fed before
flight. The presence of vomit in their cage in the first
24–48h after flight was used to indicate the animal’s
susceptibility to motion sickness.
Each animal was singularly housed and filmed
on a single flight, with some exceptions noted below.
There were three flights, each consisting of four
parabolas that lasted 23–24s. They were performed
between 10:30a.m. and 5:15p.m. The cabin temperature
was maintained at 24711C during each flight. The
first set of 20 animals was loaded onto the Falcon
All the containers were washed between flights. The
cabin was kept between 28 and 321C during loading and
unloading in order to make sure that the animals stayed
warm and did not become lethargic because of the cold
air temperature in the unheated hangar and on the
runway. After the flights landed, each flight container
was checked for vomit before it was washed. The
animals were then transferred to holding containers, for
Between each flight the videotapes were quickly
surveyed to make sure that the cameras and lights had
functioned properly. In a few cases, there were problems
with the alignment of the cameras, or with the cameras
themselves. This required reflying the Chalcides, U.
guentheri, and one each of the Thamnophis, Tarentola,
Lialis, and Leposternon.
After the last flight, the animals were kept for
2 more hours in their holding tanks before being
returned to their home terraria in the animal care
facility at Dalhousie University. The animals were
monitored for several days to weeks after the flight to
confirm that they were not injured, and were healthy
and feeding. With the exception of one Leposternon,
which had been sick earlier, all animals appeared to be
in good health.
The video recordings were transferred to a G4 iMac
and observed using iMovie. At least two research team
members carefully reviewed all the videotapes.
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120110
No vomitus was found in any of the flight containers,
nor were any animals observed to have vomited in the
subsequent hours after the flight. The flight behavior of
the animals is summarized below, ordered taxonomi-
cally. All of the animals were immobile during the
hyper-g phases of push-up and pull-out before and after
Ichthyophis kohtaoensis – None of the I. kohtaoensis
completely lost contact with the substrate on any
parabola, in part because of their large size compared
to the container. On several occasions, however, 90% of
their body was free-floating (Fig. 1a; see supplemental
video clip at www.elsevier.de/zoology; video clip 1,
ichthyophis.mov). Those animals showed some slow
body undulations in weightlessness. They also showed
concertina-like traveling waves of body contraction,
without bending, while in the mg phase. These waves
were not seen in hyper-g, the pull-out phase of the
parabolas. At the start of parabolas the animals often
lifted their heads slightly. They exhibited no long-axis
rolling during any of the flights.
Dermophis mexicanus – Of the four individuals tested,
one D. mexicanus maintained contact with the substrate
throughout the flight and showed no response to either
mg or hyper-g. The other three free-floated rarely and
were able to maintain substrate contact with part of
their body during most of the mg phase of each parabola.
The Dermophis showed moderate body undulations
comparable in speed to those exhibited during normal
burrowing motion (Fig. 1b). They showed some neck
extension when largely free-floating. They did not
exhibit any consistent long-axis rolling or high-velocity
body movements when free-floating. They did show
slow contact surface righting.
The activity level for both caecilian species did not
diminish over the series of parabolas. Thus their low
ARTICLE IN PRESS
Fig. 1. (a) Ichthyophis kohtaoensis. In mg (57:09) this individual
is 90% free-floating. It showed some moderate bending of the
body and slow undulations, but no long-axis rolling indicative
of a righting response in weightlessness. (b) Dermophis
mexicanus in mg (26:09). This individual is fully free-floating
and showing the maximum amount of curvature in its body
and undulation exhibited by this species in weightlessness.
Fig. 2. Elaphe obsoleta in mg during a series of parabolas. The
animal initially whipped its tail rapidly and twisted its body in
a series of long-axis rolling. (a) In the first parabola (15:08) the
animal eventually knotted its tail and ceased all other body
movements. (b) In the second parabola (40:13) the animal
knotted its whole body and once again ceased moving in mg. (c)
This posture was held through the next parabola (1:20:09) and
intervening hyper-g states between the parabolas.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120111
activity (compared to the reptiles) cannot be accounted
for simply by exhaustion.
Elaphe obsoleta – Of the three E. obsoleta tested, one
never lost contact and managed to wedge itself in the
seam between the top and bottom halves of its flight
container. Another free-floated extensively and main-
tained moderate curves in its body without traveling
waves. It showed strong righting responses (i.e., long-
axis rolling) upon contact with walls. On the earlier
parabolas, one E. obsoleta twisted its tail extensively
while in freefall.
One E. obsoleta on the first parabola, first whipped
its tail rapidly (at 4Hz) in a corkscrew-like fashion,
but soon tightly coiled its tail and froze in that posture
(Fig. 2a; see supplemental video clip at www.elsevier.de/
zoology; video clip 2, elaphe.mov). In the second
parabola, it formed a tight knot along most of its body
and held that posture during most of the mg phase (Fig.
2b). It unwound itself except for the knot at the tip of
the tail in the hyper-g phase. In the third parabola the
snake maintained the knotted posture in the tail and the
extensive ball-like form for its body while otherwise
floating freely (Fig. 2c). The animal held that knotted
posture through the next hyper-g phase and the last
parabola as well without any other body movements.
Elaphe bairdi – The animals were active throughout
both the mg and hyper-gravity phases. During the mg
phase, the animals were able to maintain contact with
the surface most of the time. However, when free-
floating, their tails rotated in a manner consistent with a
righting response. These motions were strongest and
most abrupt whenever the animal made contact with a
wall. The animals maintained their body in a loosely
curved fashion during mg with some occasional undula-
tions, but no intensive knotting like that seen in E.
Thamnophis sauritus – T. sauritus exhibited similar
behavior to that of Elaphe. The animals were active both
during the parabolas and between them. Approximately
one-third of the time, they were able to stay in contact
with surfaces. When largely free-floating, they made
broad undulations in their body and fast whipping
actions with their tail (tail beat frequency 6–10Hz). Any
contact with a wall initiated a righting response, which
most often propelled the animals back into the air.
Seven seconds into the first parabola, the largest T.
sauritus knotted its tail and held the mid-body and/or
tail in a knot for the rest of the parabola (Figs. 3a and b;
see supplemental video clip at www.elsevier.de/zoology;
video clip 3, thamnophis.mov). It unwrapped its tail
between the first and second parabola. This knotting is
similar to what was seen in one of the E. obsoleta.
Heterodon platyrhinos – This specimen exhibited
repetitive long-axis rolling and a moderate number of
righting responses upon contact with the walls of the
tank. Unlike the other snakes, it showed extensive
tongue flicking both during and between parabolas. The
animal exhibited full body undulations in mg. However,
these were not as rapid or as extreme as those seen in
T. sauritus or Elaphe.
Geocalamus acutus – This amphisbaenian tended to
keep its body straighter than the other limbless,
elongated reptiles and caecilians examined both in
normal and altered gravity. The animal showed some
bowing (Fig. 4; see supplemental video clip at www.
elsevier.de/zoology; video clip 4, geocalamus.mov),
however, particularly upon contact with a wall in mg.
Its most distinctive feature in mg was shivering-like
waves and high frequency, but low amplitude, vibrations
along the whole length of the body. Upon contact with a
surface, the animal showed distinctive contact righting
Leposternon microcephalum – The L. microcephalum’s
response to mg was similar to that of Geocalamus (and
Pygomeles, see below). It exhibited the same shivering
behavior when it lost substrate contact in mg see
supplemental video clip at www.elsevier.de/zoology;
video clip 5, leposternon.mov). The animal remained
largely extended and kept its body either relatively
straight or slightly arched. The specimen, however,
exhibited moderate undulations of the tail, not seen in
Ophisaurus ventralis – In mg O. ventralis held its body
with one or two curves and showed continuous long-axis
rolling when most of the body was out of contact with
surfaces. In terms of the curvature of the body, it was
midway between the snakes and the amphisbaenians
described above. It was relatively still and calm between
Anolis carolinensis – The smaller of the two A.
carolinensis was able to hold itself on the vertical wall
through the flight, including during both the mg and 2g
phases. The other A. carolinensis floated freely during
the first two parabolas, showing enormously violent,
multi-axial motions with extremely high (46Hz) tail
beat frequencies and amplitudes, as high as the length of
the tail itself. The legs were rapidly protracted and
retracted in synchrony with body undulations; presum-
ably in an attempt to grasp surfaces. In the last two
parabolas, the animal held onto the wall and showed no
Leiocephalus personatus and shreibersi – All Leioce-
phalus lost surface contact within a second or two of the
mg phase of the parabolic flight. They then exhibited
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120112
explosive thrashing of the limbs and tails (Figs. 5a–f;
see supplemental video clip at www.elsevier.de/zoology;
video clip 6, leiocephalus.mov). During these periods of
rapid motion they beat their tails at speeds 410Hz.
They appeared to attempt to grasp the smooth walls of
the aquaria whenever they contacted them and to right
themselves in reference to any surfaces they contacted in
mg. Consequently, they showed much long-axis rolling
and multi-axis gyrations as they were propelled from
one wall of the container to another.
These bouts of explosive activity were followed during
the latter parts of the mg phase with periods when the
animals were stiff and completely inactive. However,
they were not completely exhausted, as they showed
immediate righting responses upon contacting the
bottom of the container at the end of the mg phase of
the flight. They were also active during the 1g periods
The amount of time the animals spent immobilized
increased with each parabola. One of the L. shreibersi
was immobile for most of the third parabola and all of
L. shreibersi showed dewlap displays during much of
the mg phase of the parabolic flight.
Scincella lateralis – The limbs of the S. lateralis were
held in full extension most of the time. However, when
in contact with a surface they were rapidly adducted.
The animals executed undulations of extremely high
frequency and amplitude (see supplemental video clip at
www.elsevier.de/zoology; video clip 7, scincella.mov),
with tail beat frequency reaching 15Hz. They exhibited
multi-axis spinning in mg. They gyrated wildly in an
attempt to right themselves, or grasp any surface that
they contacted. These rapid movements were followed
by quiescent periods where the lizard was completely
still and stiff. They occasionally executed complete air
Isopachys gyldenstolpei – This limbless lizard showed
violent righting responses immediately upon the start of
the mg phase, including long-axis rolling and massive
body oscillations. The animal also exhibited violent
contact righting responses whenever it touched a surface
in mg. It was active between the parabolas. In all
parabolas the animal exhibited violent righting re-
sponses in the first half of the parabola, and in the last
few seconds became quiescent and ceased all movement.
The animal was less active on the last parabola than the
first three, suggesting possible exhaustion.
ARTICLE IN PRESS
Fig. 4. Geocalamus acutus in mg. This frame shows the
maximum amount of body curvature observed in this species
in mg (5:51:08). Although shivering-like motions and vibrations
were observed in mg, no undulatory waves were observed or
any successful long-axis rolling.
Fig. 3. Thamnophis sauritus in mg. (a) Similar to the E. obsoleta
seen in Fig. 2, this snake also hooked its own body with its tail
after a period of high activity and immediately became
quiescent. (a) and (b) are from the same parabola separated
by 13s (10:10, 23:10). They indicate how consistently the
animal held its posture during mg.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120113
Pygomeles braconnieri – This animal had low activity
and was able to maintain contact with the substrate
during most of the time in mg. However, when free-
floating, it tended to arch its body and showed high
supplemental video clip at www.elsevier.de/zoology;
video clip 8, pygomeles.mov) similar to those seen in
Leposternon. It used these same motions to initiate a roll
upon contact with a surface. It kept its body relatively
extended, with never more than one or two curves in the
Chalcides ocellatus – This animal held its body in the
largely extended and arched posture seen in Pygomeles.
It showed contact righting responses, but with the
camera resolution we had, the shivering movement seen
in other limbless non-ophidian reptiles was not obvious.
Lialis jicari – All L. jicari specimens were longer than
the shortest dimension of their flight containers.
Consequently, they rarely lost complete contact with a
wall. When in freefall L. jicari’s behavior was similar to
Ophisaurus, but with tail beats that were of slightly
lower amplitude and frequency (4Hz).
Palmatogecko rangei – This lizard held its limbs
in an abducted and extended position throughout most
of the parabolas. The body was slightly arched but the
static posturewas sustained
throughout most of the flight (see supplemental video
clip at www.elsevier.de/zoology; video clip 9, palmato-
for both specimens
gecko.mov). Both specimens showed some lateral
undulations in the tail and a weak tendency to extend
the tail and initiate a righting response upon contact
with a surface. Both specimens, however, maintained
a stiff fixed posture while in mg throughout most of
Eublepharis macularius – The animal arched its back,
elevated its tail, and extended its limbs during the mg
phase. It made occasional rapid forelimb movements
during the mg phase, when its ventral surface began to
lose contact with the substrate. After that it extended
and abducted its limbs fully to the side and kept its tail
arched forward. The animal kept its limbs and tail
largely still during most of the mg phase of the flight. It
showed prompt righting responses upon contact with
the substrate at the end of each parabola. Buccal
oscillations – reflecting increased respiration or possibly
increased olfaction in a novel environment – were
elevated after the first parabola.
Tarentola chazaliae – Its behavior was essentially
identical to that of Eublepharis except that T. chazaliae
exhibited more extensive and rapid limb movements
when it came in contact with a surface during mg.
Stenodactylus sthenodactylus – The S. sthenodactylus’s
behavior in mg was similar to Eublepharis’s and
Tarentola’s but it tended to not arch its back as much
during mg or show as extensive limb movements. This
lizard largely remained stiff during mg but occasionally
ARTICLE IN PRESS
Fig. 5. This is a Leiocephalus sp. in mg during a single parabola. The six frames shown here (a–f) represent less than 1s. During this
period the animal thrashed its tail at a high frequency (410Hz), which accounts for the blurred image. At the same time it showed
rapid repeated clawing motions with the limbs indicative of a futile attempt to grasp a surface outside its reach in freefall.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120 114
showed some moderate-amplitude lateral undulations of
Uroplatus guentheri – At the beginning of the first
parabola, the animal drifted slowly into the corner of
the container without losing complete contact with the
surface and maintained that position during the rest of
the flight. The second specimen showed no movement
during the mg phase of the parabolas.
Uroplatus henkeli – At the beginning of the first
parabola the lizard extended its limbs, arched its back
and elevated its tail (Fig. 6a; see supplemental video clip
at www.elsevier.de/zoology; video clip 10, uroplatus.
mov). It held this position while free-floating, showing
occasional rapid lateral movements of the tail (Fig. 6b).
It was able to maintain contact with its ventral surface
during most of the mg phases of the parabolas. This
lizard also showed high speed, but low amplitude,
oscillations in the tail and in the hind limbs when its
ventral surface was on or near the substrate. While free-
floating, it showed an abrupt righting response when it
happened to contact a surface.
Although we did not witness emesis, it would be
premature to conclude that caecilians and squamate
reptiles are completely resistant to motion sickness. Not
all of our animals fed voluntarily before flight and those
that did eat may not have filled their stomachs fully,
which would have increased their sensitivity to motion
sickness. In previous studies with caecilians (Naitoh
et al., 2000), salamanders, and squamate reptiles
(Wassersug et al., 1994) no emesis was observed. Emesis
has been observed though in frogs exposed to parabolic
flight (Wassersug et al., 1993; Naitoh et al., 2001), but
those flights included six–ten parabolas, rather than the
four parabolas of our own experiment, and it was only
the frogs that gyrated maximally in mg that vomited.
Three animals were flown twice: T. sauritus, U.
guentheri, and L. jicari. However, there was no
difference in the behavior observed in the first and
second flights of each animal.
As a result of the current study, more genera and
species of amphibians and reptiles have now been
observed in mg than for any other vertebrate classes.
Our data confirm for reptiles some stereotypic beha-
vioral patterns previously observed in amphibians (e.g.,
Wassersug et al., 1994; Wassersug, 2001). Thus terres-
trial and semi-arboreal limbed lizards (geckos are
exceptions, see below) typically make long-axis thrusting
motions of their body and high-amplitude, high-
frequency tail thrashing movements in mg. These move-
ments are interpreted as repetitive righting responses
previously observed in ground dwelling frogs (plus
turtles and some mammals). At the same time, contact
with a surface while in mg commonly elicited frantic
grasping movements by the lizards, which seem to be
protective efforts to stop freefall.
In contrast, highly arboreal species, such as geckos,
react to mg like highly arboreal tree frogs. They take up
an extended limb posture, previously compared to the
skydiving posture used by trained humans in freefall
(Wassersug et al., 1994; Wassersug, 2001).
It is worth noting that these ‘‘strategies’’ for dealing
with freefall are mutually exclusive. The skydiving
posture, which maximizes frontal area and therefore
frontal drag during falling (although not in an aircraft
on parabolic flight), requires that the limbs be abducted
and extended. However, in order to grasp a substrate the
limbs must be brought in under an animal’s body and
therefore total frontal area is reduced. Long-axis rolling
similarly requires limb retraction in order to provide
torque about the center of gravity. Essentially, an
animal in freefall, as experienced in mg, can execute
actions to reorient (long-axis rolling), slow the rate of
fall (skydiving), or ‘‘stop’’ the fall (grasping). However,
it cannot do these actions concurrently.
In addition to these three broad ‘‘defensive’’ beha-
viors, we witnessed a large array of more specific
behaviors among the different taxa we studied. Most
of these, which include shivering (e.g., G. acutus), a
defensive strike by a snake (Elaphe quadrivirgata;
Wassersug and Izumi-Kurotani, 1993), knotting of the
tail in snakes (E. obsoleta, T. sauritus), tail grasping in a
lizard (Lacerta viridis; Wassersug, 2001), tongue flicking
in a snake (H. platyrhinos), increased buccal pumping
ARTICLE IN PRESS
Fig. 6. (a) and (b) Uroplatus henkeli in mg (23:16, 05:04:22)
showing the extended limb and arched back posture commonly
held by both arboreal and non-arboreal geckos in mg. This
posture resembles the ‘‘skydiving’’ posture previously observed
in tree frogs exposed to mg on parabolic flight.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120115
ARTICLE IN PRESS
Table 2. Summary of all amphibian and reptile species observed in microgravity to date
OrderFamilySpeciesHabitLimbs Activity EmesisRighting
Ceratophrys sp. Ac
Ceratophrys sp. Bc
R.J. Wassersug et al. / Zoology 108 (2005) 107–120
ARTICLE IN PRESS
The species in bold were the subjects in the most recent parabolic flight campaign. Abbreviations: Fos ¼ fossorial, Semi-Fos ¼ semi-fossorial, Aq ¼ aquatic, Semi-Aq ¼ semi-aquatic,
Arb ¼ arboreal, Semi-Arb ¼ semi-arboreal, Ter ¼ terrestrial, N ¼ none, L ¼ low, M ¼ moderate, V ¼ variable, and H ¼ high.
aNaitoh, T., Yamashita, M., Izumi-Kurotani, A., Takabatake, I., Wassersug, R.J., 2000. Emesis and space motion sickness in amphibians. Adv. Space Res. 25, 2015–2018.
bWassersug, R.J., Izumi-Kurotani, A., Yamashita, M., Naitoh, T., 1993. Motion sickness in amphibians. Behav. Neural Biol. 60, 42–51.
cWassersug, R.J., Day, C., Izumi-Kurotani, A., Yamashita, M., Naitoh, T., 1994. Behavioral responses of vertebrates to microgravity. Proceedings of the 11th ISAS Space Utilization Symposium,
dNaitoh, T., Wassersug, R.J., Yamashita, M., 2001. Factors influencing the susceptibility of anurans to motion sickness. J. Comp. Physiol. A 187, 105–113.
eWassersug, R.J., Izumi-Kurotani, A., 1993. The behavioral reactions of a snake and a turtle to abrupt decreases in gravity. Zool. Sci. 10, 505–509.
R.J. Wassersug et al. / Zoology 108 (2005) 107–120
(E. macularius), and dewlap displays (L. personatus and
L. shreibersi), were not predictable in advance. The
majority of these responses, including explosive activity
in general, suggest that these animals find abrupt
exposure to mg stressful. However, we cannot conclude
from the behavioral displays alone whether some
amphibian and reptile taxa are more or less distressed
by mg than other taxa.
Perhaps our most impressive result is the broad
diversity in the reactions of amphibians and reptiles to
mg, even when they have similar morphology and
ecology. Some of this diversity can be accounted for
by differences in surface moisture and body size. The
wet bodies of the caecilians allowed them to adhere to
the walls of the plastic containers, which meant that they
were less likely to float freely than the similarly
elongated fossorial reptiles. The small size of one of
our Anolis allowed it to maintain constant surface
contact during both mg and hyper-g and it did not show
any unusual behavior in altered-g.
The caecilians were typically less active and less likely
to flail about in mg. The Ichthyophis and Dermophis did,
however, show slow contact righting responses and
waves of contraction in their bodies, which were
somewhat different from the behavior of the one
caecilian, the aquatic Typhlonectes, previously exposed
to mg (Naitoh et al., 2000). Our two terrestrial caecilians
were both more active than the Typhlonectes sp.
previously observed. Collectively however, the caecilians
were less active than the limbed and limbless reptiles in
weightlessness or limbed amphibians previously exposed
to freefall on parabolic flight (Table 2). This may reflect
the general differences in the activity levels of the
caecilians vs. reptiles and limbed amphibians. Typhlo-
nectes, as an aquatic caecilian, was previously exposed
to mg in water (Naitoh et al., 2000). The pressure of the
surrounding water on that caecilian may have accounted
for the animal experiencing less distress and demonstrat-
ing fewer defensive behaviors than the terrestrial
caecilians in mg. The behavior of other caecilian species
needs to be examined in mg in order to understand how
much variation there is in the responses of caecilians to
None of our snakes struck at themselves at any time
during our study. This differs from the defensive
response of an E. quadrivirgata, which struck at its
own body at the beginning of the first parabola in a
previous parabolic flight (Wassersug and Izumi-Kur-
otani, 1993). However, one of the five Elaphe that we
flew in March 2004 knotted its tail on the second
parabola and then knotted its whole body on the third
parabola. And one of our T. sauritus showed this same
self-embrace on its second parabola. Although this
behavior seems profoundly different than an aggressive
display directed towards a snake’s own body, both the
strike seen in E. quadrivirgata and the self-embrace seen
in E. obsoleta and T. sauritus share the basic common
feature of loss of proprioception. Both indicate that in
the absence of gravity, snakes have difficulty distin-
guishing self from non-self. A similar self-embrace has
been seen in one semi-arboreal lizard, Lacerta agilis
(Lacertidae), which held on to its own tail with its hind
limbs (Wassersug, 2001). The fact that these animals
became quiescent as soon as they were able to grasp
themselves suggests that they give primacy to tactile
information, which signaled stability, over vestibular
input, which indicated freefall in mg.
Although our taxonomic sample of this self-embra-
cing behavior is limited, we have not observed anything
like it in the fossorial animals that we have studied,
regardless of their taxa. This difference may reflect
simply greater flexibility in the terrestrial snakes and
limbed lizards compared to the stiffer-bodied fossorial
amphibians and reptiles. In general, the limbless
fossorial reptiles studied, which actively burrowed
through resistant substrates, were stiffer than the
snakes, although both are elongated and limbless. The
stiffer, active burrowers similarly showed less body
curvature in mg and may not have the necessary
flexibility for self-embrace. Alternatively, self-embracing
may reflect a true defensive adaptive strategy on behalf
of these animals to anchor themselves and stop ‘‘falling’’
when they are in mg. This behavior may then be absent
in highly fossorial species that may rarely, if ever,
experience falling on earth.
Previous studies with animals flown group-housed in
mg (Wassersug, 2001), indicate that holding behavior in
mg is common and can profoundly alter the behavior
(Ronca and Alberts, 2000) and subsequent physiological
responses of vertebrates to mg (Fejtek and Wassersug,
Among the elongated and limbless reptiles that were
studied, the H. platyrhinos is particularly interesting
because of its death-feigning behavior in normal-g (Zug
et al., 2001). Most vertebrates avoid being on their
backs, as the abdomen is a more vulnerable surface than
the dorsum (which is protected by vertebrae and ribs)
during predator attack. Therefore, most animals show
strong righting responses when in the supine posture
It has been suggested that the repeated righting
responses of animals in mg are due to the fact that the
animals treat the diminished stimulus to mechanical
receptors in their vestibular system as if they are upside
down. The fact that H. platyrhinos can suppress its
contact righting response in 1g suggested that it would
similarly show a muted reaction to weightlessness.
However, this was not observed. Our H. platyrhinos
showed a substantial amount of thrashing and long-axis
rolling in weightlessness, like most other elongated
reptiles. However, this individual snake did not exhibit
death feigning in 1g and would not voluntarily hold
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120118
itself in a supine position. So it still is possible that other
H. platyrhinos, that do show death feigning in 1g, may
be less likely to roll (i.e., attempt to right themselves) in
Animals that are highly flexible, e.g., Scincella, can
accomplish long-axis rolling in freefall without contact-
ing a surface. Consequently, they show an enormous
amount of spinning and twirling in weightlessness.
Animals that are longer and stiffer, like the majority
of the limbless lizards tested, have greater difficulty
executing rolls without surface contact. However, many
of these, such as Isopachys, Geocalamus, and Leposter-
non exhibited a shimmying action consistent with body
contractions while in freefall. These movements suggest
that they were attempting to roll, but could not displace
their center of gravity far enough away from their center
of rotation to complete the action. All of these animals,
however, showed contact righting responses when they
touched a surface while in mg.
Our non-gekkonid limbed lizards, whether they were
terrestrial (Scincella), arboreal (Anolis), or semi-fossorial
(Leiocephalus), exhibited the most violent and extensive
rolling and tumbling in weightlessness. We believe that
this is in part due to the fact that with limbs, these
animals were more capable of producing torque around
their center of gravity, and thus could more easily
negotiate rolls, pitches, and yaws. They also frantically
grabbed at the surface with their fore and hind limbs
when they contacted a wall during the mg phase of the
parabolic flights. These actions all appeared to be
designed to anchor the animal as a defense against
freefall. They were, however, largely ineffective on the
smooth walls of their flight containers.
The gekkonid lizards, in contrast, whether they were
terrestrial (Eublepharis), arboreal (Uroplatus), or semi-
fossorial (Palmatogecko), all held their limbs extended
laterally when in mg. Several even exhibited this ‘‘sky-
diving’’ posture when their ventral surfaces came in
contact with the wall of the container during mg. Thus
there appears to be a true family difference between
geckos and limbed lizards of other families (e.g.,
Iguanidae, Tropiduridae) with similar ecology and of
similar size. Elsewhere, Wassersug (2001) has argued
that highly arboreal animals, such as certain tree frogs,
react to weightlessness by taking up a skydiving posture
that would normally limit their rate of fall. The geckos,
like the tree frogs, appear to show the skydiving posture
regardless of the ecology of the individual genera.
In general, our results indicate that both ecology and
phylogeny can account for some of the patterns or
variations seen in the responses of amphibians and
reptiles to weightlessness. Our results also indicate that
the variation among animals that are basically similarly
formed (e.g., snakes vs. limbless lizards) can be radically
different in mg. Given this variation, one must be
cautious in selecting species as model organisms for
orbital space flight experiments (Wassersug, 1994).
Clearly, not all animals react the same to mg even when
they have similar morphology, ecology, and evolution-
We thank the following for assistance with animal
acquisition and care, and technical support both before
and during our 2004 parabolic flight campaign: John
Severance, Neil Meister, Denise Ryder, Lesley Barton,
Kerri Oseen, Monika Fejtek, Nicole Buckley, Stefanie
Ruel, Ron Wilkinson, Tim Leslie, Dave Marcotte, Ed
Pinnell, John Croll, Karen Fougere, Gary O’Meara, and
IMP Shell Aerocenter. This research was supported by
the Natural Sciences and Engineering Research Council
of Canada, the Canadian Space Agency, the Natural
Research Council of Canada, Rolf C. Hagen Inc., and
Armbrae Academy (Halifax, Nova Scotia).
Appendix A. Supplementary data
The online version of this article contains additional
supplementary data. Please search for doi:10.1016/
j.zool.2005.03.001 at http://dx.doi.org.
Crampton, G.H., 1990. Motion and Space Sickness. CRC
Press, Boca Raton, FL.
Fejtek, M., Wassersug, R.J., 1999a. Effects of laparotomy,
cage type, gestation period and spaceflight on the abdom-
inal muscles of pregnant rodents. J. Exp. Zool. 284,
Fejtek, M., Wassersug, R.J., 1999b. A survey of how space-
flight affects rodent skeletal muscle. Adv. Space Biol. Med.
Fejtek, M., Wassersug, R.J., 2001. Effects of spaceflight and
cage design on the abdominal muscles of male rodents.
J. Exp. Zool. 289, 330–334.
Fejtek, M., Delorme, M., Wassersug, R.J., 1995. Behavioral
reactions of the bat Carollia perspicillata to abrupt changes
in gravity. Biol. Sci. Space 9, 77–81.
Izumi-Kurotani, A., Yamashita, M., Kawasaki, Y., Kurotani,
T., Mogami, Y., Okuno, M., Oketa, A., Shiraishi, A.,
Ueda, K., Wassersug, R.J., Naitoh, T., 1994. Behavior of
Japanese tree frogs under mg on MIR and in parabolic
flight. Adv. Space Res. 108, 419–422.
Naitoh, T., Yamashita, M., Izumi-Kurotani, A., Takabatake,
I., Wassersug, R.J., 2000. Emesis and space motion sickness
in amphibians. Adv. Space Res. 25, 2015–2018.
Naitoh, T., Wassersug, R.J., Yamashita, M., 2001. Factors
influencing the susceptibility of anurans to motion sickness.
J. Comp. Physiol. A 187, 105–113.
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120119
Ronca, A.E., Alberts, J.R., 2000. Physiology of a microgravity Download full-text
environment. Selected contribution: effects of spaceflight
during pregnancy on labor and birth at 1 G. J. Appl.
Physiol. 89, 849–854.
Wassersug, R.J., 1994. Should the space station be an ark?
Space Policy 10, 199–206.
Wassersug, R.J., 2001. Vertebrate biology in microgravity.
Am. Sci. 89, 46–53.
Wassersug, R.J., Izumi-Kurotani, A., 1993. The behavioral
reactions of a snake and a turtle to abrupt decreases in
gravity. Zool. Sci. 10, 505–509.
Wassersug, R.J., Izumi-Kurotani, A., Yamashita, M., Naitoh,
T., 1993. Motion sickness in amphibians. Behav. Neural
Biol. 60, 42–51.
Wassersug, R.J., Day, C., Izumi-Kurotani, A., Yamashita, M.,
Naitoh, T., 1994. Behavioral responses of vertebrates to
microgravity. Proceedings of the 11th ISAS Space Utiliza-
tion Symposium, pp. 61–62.
Zug, G.R., Vitt, L.J., Caldwell, J.P., 2001. Herpetology: An
Introductory Biology of Amphibians and Reptiles, second
ed. Academic Press, San Diego.
ARTICLE IN PRESS
R.J. Wassersug et al. / Zoology 108 (2005) 107–120120