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Journal of Herpetology, Vol. 37, No. 2, pp. 363–368, 2003
Copyright 2003 Society for the Study of Amphibians and Reptiles
Sustained Swimming Performance in Crocodiles (Crocodylus porosus): Effects of
Body Size and Temperature
PETER G. ELSWORTH,1 FRANK SEEBACHER,2
1
AND
CRAIG E. FRANKLIN1,3
Department of Zoology and Entomology, University of Queensland, Brisbane 4072, Australia
2
School of Biological Sciences, Heydon Laurence Building A08, The University of Sydney,
New South Wales 2006, Australia
ABSTRACT.—We examined effects of body size and temperature on swimming performance in juvenile
estuarine crocodiles, Crocodylus porosus, over the size range of 30–110 cm total body length. Swimming
performance, expressed as maximum sustainable swimming speed, was measured in a temperature- and
flow-controlled swimming flume. Absolute sustainable swimming speed increased with body length, but
length-specific swimming performance decreased as body length increased. Sustained swimming speed
increased with temperature between 158C and 238C, remained constant between 238 and 338C, and decreased
as temperature rose above 338C. Q10-values of swimming speed were 2.60 (6 0.091 SE) between 188C and
238C, and there were no differences in Q10 between crocodiles of different sizes. The broad plateau of thermal
independence in swimming speed observed in C. porosus may be of adaptive significance by allowing
dispersal of juvenile animals at suboptimal body temperatures.
Locomotory performance is intrinsically linked to
ecological performance and fitness, because it directly
impacts an animal’s ability to capture prey, disperse,
avoid predators, and, in the case of crocodilians, engage in social interactions linked to reproduction
(Bennett, 1982; Jayne and Bennett, 1990; Seebacher and
Grigg, 2001; Vliet, 2001). Sustained aquatic locomotion in fish is powered exclusively by red, aerobic
muscle fibers, whereas sprint performance is determined by a combination of red and anaerobic white
muscle fibres (Beddow et al., 1995; Gillies, 1998; Reidy
et al., 2000). However, differences in swimming performance between species and between higher taxonomic categories may be determined not only by differential power output of muscle fibers but also by
hydrodynamic forces associated with body shape,
which can play a major role in limiting locomotor performance (Wolfgang et al., 1999; Drucker and Lauder,
2000). In cetaceans, for example, different morphologies result in different hydrodynamic drag, and a
combination between drag and muscle power output
determines locomotor performance in these animals
(Fish, 1998). Hence, the energetic cost of swimming is
directly related to body shape and swimming mode,
and it may be particularly high in semiaquatic animals, which have to function both on land and in water (Frey and Salisbury, 2001). For example, the semiaquatic water rat Hydromys chrysogaster incurs a much
greater metabolic cost during swimming than fully
aquatic mammals do (Fish and Baudinette, 1999).
Crocodiles, like water rats, are semiaquatic so it may
be expected that swimming in crocodiles would be
relatively expensive compared to wholly aquatic animals such as fish. As a consequence, it may be that
sustained swimming performance, often measured as
Corresponding Author. E-mail: [email protected].
edu.au
3
the maximum sustainable swimming speed (Ucrit;
Holk and Lykkeboe, 1998; Plaut, 2000) is poorer in
semiaquatic animals compared to wholly aquatic animals. Nonetheless, crocodilians are primarily aquatic,
and most ecologically important behaviors, such as
prey capture (Sah and Stuebing, 1996; FS pers. obs.),
reproduction (Vliet, 2001), social interactions (Lang,
1987; Seebacher and Grigg, 1997; Seebacher and
Grigg, 2001), and dispersal (Webb and Messel, 1978;
Sah and Stuebing, 1996; Tucker et al., 1998; Munoz
and Thorbjarnarson, 2000) occur in water. Hence,
swimming performance is of greater ecological importance in crocodilians than terrestrial locomotion.
During much of their activity, crocodilians perform
only short bursts of locomotion which are almost exclusively powered by anaerobic metabolism (Bennett,
1990). However, sustained swimming, fuelled by aerobic metabolism, is important during dispersal (Tucker et al., 1997, 1998), and during long migrations
which may be up to thousands of kilometers (Brazaitis, 1973; Allen, 1974). Moreover, crocodilians are the
most social of all reptiles (Lang, 1987) and often show
sustained activity when establishing social hierarchies
(Grigg et al., 1998; Seebacher and Grigg, 2001) and
during mating (Vliet, 1989, 2001). Dispersal, social interactions, and reproductive behavior are linked to
life-history stage of these ectotherms, so that the interaction between body size and temperature in determining locomotory performance is likely to be ecologically important. It was the aim of this research to
determine the effects of body size and temperature on
the aerobic swimming performance, measured as the
maximum sustainable, or critical swimming speed
(Ucrit; Fish, 1984; Graham et al., 1990).
MATERIALS
AND
METHODS
Juvenile estuarine crocodiles, Crocodylus porosus (N
5 10), were purchased from a commercial crocodile
farm (Cairns Crocodile Farm, Cairns, Australia). Cro-
364
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TABLE 1. Linear regression equations relating absolute (cm/sec) and length-specific (BL/sec) critical
swimming speed to body length (BL) for Crocodylus
porosus at five experimental temperatures.
T
(8C)
a
Absolute Ucrit
18
9.97
23 12.48
28 14.16
33 12.58
35 18.74
FIG. 1. Effect of body length on critical swimming
speed at 188C (N 5 13) and 338C (N 5 15) for Crocodylus porosus.
codylus porosus eggs (N 5 5) were acquired from a
commercial zoo (Australia Zoo, Beerwah, Australia)
and incubated at 308C. The resulting hatchlings were
grown for 8–10 months prior to experimentation.
These 15 animals were divided into three experimental size classes; 30–40 cm (N 5 5), 80–90 cm (N 5 5)
and 90–110 cm (N 5 5).
Critical (sustained) swimming speed was determined in a large (3.6 m long), oval-shaped swimming
flume. The flume was designed so that water speed
(between 0 and 90 cm.s21) and water temperature (6
0.58C) could be controlled remotely. The water temperature of the flume was controlled using a combination of heaters (Julabo Type-E thermomix) and coolers (Colora TK67). Water speed was controlled by altering propeller speed of two electrical outboard motors suspended in the flume.
Animals were confined to a 150 3 60 3 60 cm viewing area fitted with one-way perspex on the outside
which allowed observations without disturbing the
animals. Turbulence was decreased by a series of baffles, and water depth was 0.5 m. The smallest C. porosus were confined in a mesh basket (100 3 55 3 40
cm with 2 mm2 mesh at the front and back) within
the viewing area to prevent the animals from passing
through the baffles.
A pilot study was performed in order to determine
the starting speed for the critical swimming speed experiments (see below), and to accustom the animals
to the experimental set-up. When not used in experimental trials, crocodiles were kept in outdoor tanks
which were fitted with a basking platform, and in
which water temperature was controlled to 288C.
Swimming performance was determined over a
range of temperatures (15, 23, 28, 33, 35 and 378C) in
each crocodile, and the order of test temperatures in
the trials was assigned randomly. Animals were
placed individually into the swimming flume and
their body temperature was allowed to equilibrate to
water temperature (15 min for hatchlings and 60 min
for medium and large animals). Equilibrium times
b
R2
F1,14
P
0.29
0.38
0.36
0.42
0.30
0.75
0.09
0.84
0.74
0.70
45.24
125.04
75.32
40.57
34.09
,0.0001
,0.0001
,0.0001
,0.0001
,0.0001
0.64
0.84
0.81
0.62
0.54
26.29
73.20
62.47
23.69
17.54
,0.0001
,0.0001
,0.0001
,0.0001
,0.001
Length-specific Ucrit
18
0.64 20.0025
23
0.85 20.0035
28
0.88 20.0038
33
0.88 20.0038
35
1.07 20.0072
were estimated from equations given in Seebacher
(1999).
Trials to determine the critical swimming speed
(Ucrit) were performed over a four-day period for each
temperature. During the first three days the approximate critical swimming speed for each individual was
determined. Initial water speed was 5 cm s21 for
hatchlings, 23 cm s21 for the medium size class and
29 cm s21 for the large size class (determined from the
pilot study). Every 2 min, water speed was increased
by 4 cm s21 until the experimental animal could no
longer maintain its position in the water, which was
interpreted as a sign of fatigue. At this point, the animal was removed and rested for at least 20 h before
the next trial. The initial water speed for the next trial
was 8 cm s21 slower than the final speed of the previous trial. This procedure was repeated three times
for each individual at each test temperature. During
the fourth trial, the start speed was 4 cm s21 less than
the final speed of the previous trial, and speed was
increased by 2 cm s21 every 2 min. The critical swimming speed was calculated as: Ucrit 5 Uf 1 [(Tf/Ti) 3
Ui], where Uf is the greatest speed which animals
maintained for the full-time interval; Tf is the time
spent at the final speed; Ti is the time interval (2 min
in this case); and Ui is the speed increment (2 cm s21
in this case; Brett, 1965).
Scaling relationships were determined by type 1 linear regressions of Ucrit measured at each of five experimental temperatures (18, 23, 28, 33, and 358C).
Ucrit-values were compared by repeated measures
analyses of variance with body length class as an independent factor, and measurements at different temperatures as the repeated measures. All data are presented as means 6 S.E.M.
RESULTS
In C. porosus, absolute Ucrit, expressed in cm s21, increased significantly with increasing body length at
each of the five experimental temperatures (Fig. 1; regression results in Table 1). Length-specific Ucrit, expressed as body length s21 (BL s21), however, decreased significantly with increasing body length (Fig.
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FIG. 2. Effect of body length on length-specific critical swimming speed at 188C (N 5 13) and 338C (N
5 15) for Crocodylus porosus.
2; regression results in Table 1), indicating that relative
to their body length, smaller C. porosus showed greater
sustainable swimming capabilities.
There were significant differences in absolute (F2,12
5 32.31, P , 0.0001) and length-specific (F2,12 5
424.14, P , 0.0001) Ucrit between size classes. Moreover, Ucrit differed significantly between the different
temperature treatments both in absolute terms (F5,60 5
50.90, P , 0.0001) and when expressed in length-specific units (F5,60 5 110.91, P , 0.0001). None of the
crocodiles swam at 158C, and there was a considerable
increase in Ucrit between 15 and 238C. However, Ucrit
remained stable between 23 and 338C, but it decreased
sharply at 358C except for the small size class where
there was an increase at 358C and a very pronounced
decrease at 378C (Fig. 3). Crocodylus porosus in different
size classes responded differently to the temperature
treatments which was indicated by the different regression slopes in Figures 1 and 2 (examples for 188C
and 338C), as well as by the significant interactions
between size class and temperature treatment (absolute Ucrit: F10,60 5 12.73, P , 0.0001; length-specific Ucrit:
F10,60 5 108.24, P , 0.0001).
Q10-values for Ucrit between 188C and 238C did not
differ significantly between size classes (one-way ANOVA, F2,14 5 0.63, P 5 0.55), and the mean Q10 for all
animals was 2.60 6 0.091.
DISCUSSION
Although absolute critical swimming speed (m s21)
increased with increasing body length, relative aerobic
swimming performance (in BL s21) decreased in larger
C. porosus. Hydrodynamic resistance associated with
swimming (Johnson et al., 1998; Stelle et al., 2000) may
explain this pattern, because larger animals have a
greater surface area and would, therefore, experience
greater friction. Moreover, compared to fully aquatic
animals, the critical swimming speed of crocodiles
and other reptiles is significantly lower (Table 2). Statistical comparisons (one-way ANOVA) of the data in
Table 2 reveal that there are significant differences
365
FIG. 3. The effect of temperature on length-specific
critical swimming speed for small (30–40 cm), medium (80–90 cm) and large (90–110 cm) size classes of
Crocodylus porosus (N 5 5 for each size class, all values
are mean 6 S.E.M.).
(F2,26 5 4.59, P , 0.05) in length-specific Ucrit between
fish (3.97 6 1.56), mammals (1.70 6 0.24) and reptiles
(0.55 6 0.05). Interestingly, fish show the greatest
length-specific Ucrit, which may indicate that physical
resistance to swimming, which is associated with
body shape, may outweigh possible performance advantages gained from endothermic metabolism. Even
among fish, endothermy does not increase swimming
performance (Sepulveda and Dickson, 2000). Differences in swimming efficiencies may also be attributable to mode of propulsion, with fish that use comparable modes of propulsion (e.g., Lemon Shark, subcarangiform locomotion) outperforming C. porosus
(Table 2).
The biomechanical design of crocodiles is a functional hybrid enabling locomotion on land and in water and, in particular, the bracing system of crocodilians is designed for locomotion on land rather than
for optimal locomotory performance in water (Frey,
1988; Frey and Salisbury, 2001). Although crocodiles
are primarily aquatic, they are secondarily so, and,
compared to fish, water flow patterns, and vortices
surrounding the body may be far less than optimal
(Drucker and Lauder, 2000).
The effects of temperature on physiological performance are well known (Huey, 1982), and underlying
physiological mechanisms such as metabolic rate and
muscle activity are likely to determine whole animal
performance, especially locomotion (Bennett, 1982;
Bennett, 1990). Interestingly, temperature did not affect swimming performance in the smelt Hypomesus
transpacificus (Swanson et al., 1998), which may indicate that these fish are very efficient at physiological
compensation for varying temperatures (Crawford et
al., 1999). In addition, temperature may affect swimming performance by altering the physical properties
of the surrounding water, and temperature-dependent
changes in kinematic viscosity have been shown to
affect swimming performance in fish (Johnson et al.,
366
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TABLE 2. Comparisons of critical swimming speed between different species. All values measured over a
temperature range of 20–258C. Ucrit is given in absolute (cm/sec) and length-specific (BL/sec) units, and the
body length (BL) of the study animals is shown.
Species
Oncorhynchus nerka (Sockeye Salmon)
Negaprion brevirostrus (Lemon Shark)
Negaprion brevirostrus (Lemon Shark)
Negaprion brevirostrus (Lemon Shark)
Sphyrna lewini (Hammerhead Shark)
Danio rerio (Zebrafish)
Oncorhynchus mykiss (Rainbow Trout)
Hypomesus transpacificus (Smelt)
Hypomesus transpacificus (Smelt)
Eumetopias jubatus (Sea Lion)
Pseudorca crassidens (False Killer Whale)
Delphinapterus leucas (Beluga Whale)
Orcinus orca (Killer Whale)
Tursiops truncatus (Bottlenose Dolphin)
Amblyrhynchus cristatus (Iguana)
Crocodylus porosus (Crocodile)
Crocodylus porosus (Crocodile)
Crocodylus porosus (Crocodile)
BL (cm)
(cm/sec)
(BL/sec)
Reference
64.1
36.0
77.0
103.0
60.0
4.4
30.3
4.2
7.1
230.0
375.0
364.0
474.0
261.0
97.0
35.5
88.2
97.9
128.0
46.8
89.0
89.3
83.1
56.0
72.7
28.0
28.0
315.0
746.0
270.0
791.0
601.0
45.3
25.6
45.03
50.6
2.1
1.6
1.2
0.9
1.4
15.5
2.4
6.7
3.9
1.4
2.1
1.1
1.5
2.4
0.5
0.7
0.5
0.5
Brett and Glass (1973)
Graham et al. (1990)
Graham et al. (1990)
Graham et al. (1990)
Lowe (1996)
Plaut (2000)
Holk and Lykkeboe (1998)
Swanson et al. (1998)
Swanson et al. (1998)
Stelle et al. (1998)
Fish (1998)
Fish (1998)
Fish (1998)
Fish (1998)
Bartholomew et al. (1976)
this study
this study
this study
1998), although these biophysical effects were minor
compared to physiological changes.
The effect of temperature on sustained swimming
performance of C. porosus is similar to that seen in the
American Alligator (Alligator mississippiensis), in
which Ucrit increased between 158C and 208C, but remained constant from 20–308C (Gatten et al., 1991).
The Q10-values of Ucrit measured in this study were
similar to corresponding Q10-values in aerobic metabolic rates in C. porosus and alligators (Grigg, 1978;
Lewis and Gatten, 1985; Wright, 1986; Emshwiller and
Gleeson, 1997). Interestingly, active aerobic metabolic
rates of A. mississippiensis remained constant between
258C and 358C (Emshwiller and Gleeson, 1997). The
temperature range of this metabolic plateau corresponds to that observed for the plateau in Ucrit in C.
porosus and in A. mississippiensis (Gatten et al., 1991),
which may indicate that maximal aerobic metabolic
rates are limiting sustained swimming performance.
However, this conclusion is not substantiated by other
studies which found that resting (Grigg, 1978; Lewis
and Gatten, 1985; Wright, 1986; Emshwiller and Gleeson, 1997) and active (Lewis and Gatten, 1985; Wright,
1986) metabolic rates of C. porosus and A. mississippiensis increased continually over temperature ranges
of 108C–358C. These latter data indicate that metabolic
correlates by themselves do not explain the observed
patterns in swimming performance and that other factors such as temperature-dependent changes in muscle activity (Wilson and Franklin, 1999) may have an
effect as well. In future studies, it would be of interest
to quantify the relative effects of different physiological parameters as well as of biomechanical factors on
the swimming performance of crocodilians.
Crocodiles are typical heliothermic thermoregulators, and they are the largest living reptiles spanning
a huge ontogenetic size range (Seebacher and Grigg,
1997; Grigg et al., 1998; Seebacher et al., 1999). Hence,
both body size and temperature effects on locomotion
are of biological importance. Ecological demands for
sustained swimming change with ontogenetic stage;
for example hatchlings often travel considerable distances when their creches disperse, and subadult
males are often forced to leave their natal areas by
larger resident animals and must travel to uncontested sites often many kilometers away (Tucker et al.,
1997; Tucker et al., 1998; Munoz and Thorbjarnarson,
2000). In contrast, activity associated with reproduction would be restricted to larger, adult animals (Vliet,
2001). Moreover, intraspecific aggression may force
smaller individuals to disperse at body temperatures
that are significantly lower than those of undisturbed
animals (Seebacher and Grigg, 2001). If it is selectively
advantageous for crocodiles to sustain activity over a
broad body temperature range, the thermal plateau in
locomotory performance observed in this study may
be of adaptive significance.
Acknowledgments.—This work was funded by a
small Australian Research Council Grant to CEF. We
thank L. Fletcher for building the 3.6-m long flume in
which the crocs were swum.
LITERATURE CITED
ALLEN, G. R. 1974. The marine crocodile Crocodylus
porosus from Ponape, Eastern Caroline Islands with
notes on food habits of crocodiles from the Palau
Archipelago. Copeia 1974:553.
BARTHOLOMEW, G. A., A. F. BENNETT, AND W. R. DAWSON. 1976. Swimming, diving and lactate production of the marine iguana Amblyrhynchus cristatus.
Copeia 1976:709–720.
BEDDOW, T. A., J. L. VAN LEEUWEN, AND I. A. JOHNSTON. 1995. Swimming kinematics of fast starts
are altered by temperature acclimation in the marine fish Myoxocephalus scorpius. Journal of Experimental Biology 198:203–208.
BENNETT, A. F. 1982. The energetics of reptilian activity. In C. Gans and F. H. Pough (eds.), Biology of
SHORTER COMMUNICATIONS
the Reptilia. Vol. 13, pp. 155–201. Academic Press,
London.
. 1990. Thermal dependence of locomotor capacity. American Journal of Physiology 259:R253–
R258.
BRAZAITIS, P. 1973. The identification of living crocodilians. Zoologica 58:59–101.
BRETT, J. R. 1965. The relation of size to the rate of
oxygen consumption and sustained swimming
speed of sockeye salmon (Onchorhynchus nerka).
Journal of the Fisheries Research Board of Canada
23:1491–1501.
BRETT, J. R., AND N. R. GLASS. 1975. Metabolic rates
and critical swimming speeds of sockeye salmon
(Onchyrhynchus nerka) in relation to size and temperature. Journal of the Fisheries Research Board
of Canada 30:379–387.
CRAWFORD, D. L., V. A. PIERCE, AND J. A. SEGAL. 1999.
Evolutionary physiology of closely related taxa:
analyses of enzyme expression. American Zoologist 39:389–400.
DRUCKER, E. G., AND G. V. LAUDER. 2000. A hydrodynamic analysis of swimming speed: wake structure and locomotor force in slow and fast labriform
swimmers. Journal of Experimental Biology 203:
2379–2393.
EMSHWILLER, M. G., AND T. T. GLEESON. 1997. Temperature effects on aerobic metabolism and terrestrial locomotion in American alligators. Journal of
Herpetology 31:142–147.
FISH, F. E. 1984. Kinematics of undulatory swimming
in the American alligator. Copeia 1984:839–845.
. 1993. Power output and propulsive efficiency
of swimming bottlenose dolphins (Tursiops truncatus). Journal of Experimental Biology 185:179–
193.
. 1998. Comparative kinematics and hydrodynamics of odontocete cetaceans: morphological
and ecological correlates with swimming performance. Journal of Experimental Biology 201:2867–
2877.
FISH, F. E., AND R. V. BAUDINETTE. 1999. Energetics of
locomotion by the Australian water rat (Hydromys
chrysogaster): a comparison of swimming and running in a semi-aquatic mammal. Journal of Experimental Biology 202:353–363.
FREY , E. 1988. Das Tragsystem der Krokodile—eine
biomechanische und phylogenetische Analyse.
Stuttgarter Beiträge zur Naturkunde Serie A 426:
1–60.
FREY, E., AND S.W. SALISBURY. 2001. The kinematics
of aquatic locomotion of Osteolaemus tetraspis Cope.
In G. C. Grigg, F. Seebacher, and C. E. Franklin
(eds.), Crocodilian Biology and Evolution, pp. 165–
179. Surrey Beatty, Chipping Norton, New South
Wales, Australia.
GATTEN, R. E., J. D. CONGDON, F. J. MAZZOTTI, AND R.
U. FISCHER. 1991. Glycolysis and swimming performance in juvenile American alligators. Journal
of Herpetology 25:406–411.
GILLIS, G. 1998. Neuromuscular control of anguilliform locomotion: patterns of red and white muscle
activity during swimming in the American eel Anguilla rostrata. Journal of Experimental Biology 201:
3245–3256.
GRAHAM, J. B., H. DEWER, N. C. LAI, W. R. LOWELL,
367
AND S. M. ARCE. 1990. Aspects of shark swimming performance determined using a large water
tunnel. Journal of Experimental Biology 151:175–
192.
GRIGG, G. C. 1978. Metabolic rate, Q10 and respiratory
quotient (RQ) in Crocodylus porosus, and some generalizations about low RQ in reptiles. Physiological
Zoology 51:354–360.
GRIGG G. C., F. SEEBACHER, L. A. BEARD, AND D. MORRIS. 1998. Thermal relations of large crocodiles,
Crocodylus porosus, free-ranging in a naturalistic
situation. Proceedings of the Royal Society of London B Biological Sciences 265:1793–1799.
HOLK, K., AND G. LYKKEBOE. 1998. The impact of endurance training on arterial plasma K1 levels and
swimming performance of rainbow trout. Journal
of Experimental Biology 201:1373–1380.
HUEY, R. B. 1982. Temperature, physiology and the
ecology of reptiles. In C. Gans and F. H. Pough
(eds.), Biology of the Reptilia. Vol. 12, pp. 25–92.
Academic Press, London.
JAYNE, B. C., AND A. F. BENNETT. 1990. Selection on
locomotor performance capacity in a natural population of garter snakes. Evolution 44:1204–1229.
JOHNSON, T. P., A. J. CULLUM, AND A. F. BENNETT.
1998. Partitioning the effects of temperature and
kinematic viscosity on the c-start performance of
adult fishes. Journal of Experimental Biology 201:
2045–2051.
LANG, J. W. 1987. Crocodilian behaviour: implications
for management. In G. J. W. Webb, S. C. Manolis,
and P. J. Whitehead (eds.), Wildlife Management:
Crocodiles and Alligators, pp. 273–294. Surrey
Beatty, Chipping Norton, New South Wales, Australia.
LEWIS, L. Y., AND R. E. GATTEN. 1985. Aerobic metabolism of American alligators Alligator mississippiensis, under standard conditions and during voluntary activity. Comparative Biochemistry and Physiology 80A:441–447.
LOWE, C. G. 1996. Kinematics and critical swimming
speed of juvenile scalloped hammerhead sharks.
Journal of Experimental Biology 199:2605–2610.
MUNOZ, M. DEL C., AND J. THORBJARNARSON. 2000.
Movement of captive-released Orinoco crocodiles
(Crocodylus intermedius) in the Capanaparo River,
Venezuela. Journal of Herpetology 34:397–403.
PLAUT, I. 2000. Effects of fin size on swimming performance, swimming behaviour and routine activity of zebrafish Danio rerio. Journal of Experimental
Biology 203:813–820.
REIDY, S. P., S. R. KERR, AND J. A. NELSON. 2000. Aerobic and anaerobic swimming performance of individual Atlantic cod. Journal of Experimental Biology 203:347–357.
SAH, S. A. M., AND R. B. STUEBING. 1966. Diet,
growth, and movements of juvenile crocodiles Crocodyles porosus Schneider in the Klias River, Sabah,
Malaysia. Journal of Tropical Ecology 12:651–662.
SEEBACHER, F. 1999. Behavioural postures and the rate
of body temperature change in wild freshwater
crocodiles Crocodylus johnstoni. Physiological and
Biochemical Zoology 72:57–63.
SEEBACHER, F., AND G. C. GRIGG. 1997. Patterns of
body temperature in wild freshwater crocodiles,
Crocodylus johnstoni: thermoregulation versus ther-
368
SHORTER COMMUNICATIONS
moconformity, seasonal acclimation, and the effect
of social interactions. Copeia 1997:549–551.
. 2001. Social interactions compromise thermoregulation in crocodiles Crocodylus johnstoni and
Crocodylus porosus. In G. C. Grigg, F. Seebacher, and
C. E. Franklin (eds.), Crocodilian Biology and Evolution, pp. 310–316. Surrey Beatty, Chipping Norton, New South Wales, Australia.
SEEBACHER, F., G. C. GRIGG, AND L. A. BEARD. 1999.
Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and
stable body temperatures. Journal of Experimental
Biology 202:77–86.
SEPULVEDA, C., AND K. A. DICKSON. 2000. Maximum
sustainable speeds and cost of swimming in juvenile Kawakawa tuna (Euthynnus affinis) and
Chubb Mackerel (Scomber japonicus). Journal of Experimental Biology 203:3089–3101.
SOKAL, R. R., AND F. J. ROHLF. 1981. Biometry. W. H.
Freeman and Company, New York.
STELLE, L. L., R. W. BLAKE, AND A. W. TRITES. 2000.
Hydrodynamic drag in Steller Sea Lions (Eumetopias jubatus). Journal of Experimental Biology 203:
1915–1923.
SWANSON, C., P. S. YOUNG, AND J. J. CECH JR. 1998.
Swimming performance of Delta smelt: maximum
performance, and behavioural and kinematic limitations on swimming at submaximal velocities.
Journal of Experimental Biology 201:333–345.
TUCKER, A. D., C. J. LIMPUS, H. I. MCCALLUM, AND K.
R. MCDONALD. 1997. Movement and home ranges
of Crocodylus johnstoni in the Lynd River, Queensland. Wildlife Research 24:379–396.
TUCKER, A. D., H. I. MCCALLUM, C. J. LIMPUS, AND K.
R. MCDONALD. 1998. Sex-biased dispersal in a
long-lived polygynous reptile (Crocodylus johnstoni). Behavioral Ecology and Sociobiology 44:85–90.
VLIET, K. A. 1989. Social displays of the American
Alligator (Alligator mississippiensis). American Zoologist 29:1019–1031.
. 2001. Courtship of captive American Alligators (Alligator mississippiensis). In G. C. Grigg, F.
Seebacher, and C. E. Franklin (eds.), Crocodilian
Biology and Evolution, pp. 383–408. Surrey Beatty,
Chipping Norton, New South Wales, Australia.
WEBB G. J. W., AND H. MESSEL. 1978. Movement and
dispersal patterns of Crocodylus porosus in some
rivers of Arnhem Land, Northern Australia. Australian Wildlife Research 5:263–283.
WILSON, R. S., AND C. E. FRANKLIN. 1999. Thermal
acclimation of locomotor performance in tadpoles
of the frog Limnodynastes peronii. Journal of Comparative Physiology B 169:445–451.
WOLFGANG, M. J., J. M. ANDERSON, M. A. GROSENBAUGH, D. K. P. YUE, AND M. S. TRIANTAFYLLOU.
1999. Near-body flow dynamics in swimming
fish. Journal of Experimental Biology 202:2303–
2327.
WRIGHT, J. C. 1986. Effects of body temperature,
mass, and activity on aerobic and anaerobic metabolism in juvenile Crocodylus porosus. Physiological Zoology 59:505–513.
Accepted: 2 May 2002.
Journal of Herpetology, Vol. 37, No. 2, pp. 368–370, 2003
Copyright 2003 Society for the Study of Amphibians and Reptiles
Chromosomes of New Zealand Skinks, Genus Oligosoma
T. BRUCE NORRIS
School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand;
E-mail: [email protected]
ABSTRACT.—Karyotypes from the New Zealand skinks Oligosoma nigriplantare nigriplantare, Oligosoma
nigriplantare polychroma, and Oligosoma microlepis are presented. All have a chromosome complement of
30, and there are no sex-related heteromorphisms. Comparisons with the other New Zealand skink genus,
Cyclodina, and the Mauritius skink Leiolopisma telfairi, indicate Oligosoma and Leiolopisma share a common karyotype and that the Cyclodina karyotype is derived from Oligosoma.
The skink biota of New Zealand consists of eight
species of Cyclodina and 22 species of Oligosoma (5
Leiolopisma; Daugherty et al., 1994; Patterson and
Daugherty, 1995). Delineation of these species was the
result of extensive morphological study (Hardy, 1977),
allozyme examination (Daugherty et al., 1990; Patterson and Daugherty, 1990; Vos, 1988) and 12S mitochondrial DNA analysis (Hickson et al., 1992). Oligosoma nigriplantare polychroma, Cyclodina aenea, Cyclodina
ornata (O’Malley, 1971), and Cyclodina oliveri (Hardy,
1979) each have eight macro and seven micro chromosome pairs with Cyclodina species all showing a
heteromorphism in chromosome 6. With DNA, allozyme and morphological research on New Zealand
skinks revealing a reasonably complete evolutionary
tree, it was appropriate to examine chromosomal variation within additional species and put this work in
context with that involving other Australasian skinks.
MATERIALS AND METHODS
Skinks were kept at room temperature, injected intraperitonally with a 1% colchicine solution at 0.5 ml/
5 g body weight, incubated at room temperature for
two to three hours, and euthanized by ether immersion. The gut was removed, split open, and placed in
distilled water (hypotonic) for 20 min. Testes were removed and soaked in distilled water (hypotonic) for
20 min. Gut tissue was then agitated, placed in 5 ml
SHORTER COMMUNICATIONS
369
FIG. 1. Prepared karyotypes from New Zealand skinks (A) Oligosoma nigriplantare nigriplantare (gut epithelial
preparation) 2n 5 30; (B) Oligosoma nigriplantare polychroma (gut epithelial preparation) 2n 5 30; (C) Oligosoma
microlepis (testis preparation) N 5 15.
of ice-cold fixative (3:1 methanol:acetic acid), scraped
vigorously to remove cells, and the mixture funnelled
into a 10 ml nonadditive collection tube and spun for
10 min at 500 rpm. Resulting supernatant was removed down to 0.5 ml; fresh ice-cold fixative was then
added until the mixture became slightly milky; and
the solution was stored at 2208C until further prepared. Testes were placed directly into ice-cold fixative and stored at 2208C. Chromosome spreads were
obtained by squashing the testes onto a microscope
slide. Gut cell spreads were obtained by dropping the
cell mixture onto slides from a height of 50 cm and
370
SHORTER COMMUNICATIONS
staining with 10% Giemsa (BDH) in phosphate buffer
for 10 minutes. Good quality chromosome spreads
were then photographed and karyotyped by aligning
chromosomes in putative homologous pairs in descending length order. Chromosome nomenclature follows Green and Sessions (1991).
The following specimens were examined: Oligosoma
microlepis from Taharua River in the Northern Kaimanawa Ranges, North Island, New Zealand (FT
3692, ?); Oligosoma nigriplantare nigriplantare from
Mangere Id. (FT 3618, /), and South Eastern Island,
Chatham Islands group, New Zealand (FT 3622, ?;
3629, /; 3630, /; 3635, /; and 3636, ?); and Oligosoma
nigriplantare polychroma from Wakemans clearing, Taupo, New Zealand (FT 3694, /), identified by R. A.
Hitchmough. Specimens were deposited in the fixed
tissue collection at Victoria University of Wellington.
RESULTS AND DISCUSSION
The six largest chromosomes were metacentric (Fig.
1); chromosomes 7 and 8 were submetacentric and
subtelocentric, respectively. There were no sex-related
heteromorphisms identified in Cyclodina or Oligosoma,
and there were no chromosomal differences present
between the Oligosoma species I examined.
Donnellan (1991) interpreted Hardy’s (1979) results
to indicate that male C. oliveri were the heteromorphic
sex but, Hardy did not examine females. O’Malley
(1971) found male and female C. ornata and female C.
aenea heteromorphic at chromosome 6. There is no evidence of sex chromosomes in either Cyclodina or Oligosoma, but neither is there an explanation for the
maintenance and nature of the heteromorphism in Cyclodina.
King (1973) and Donnellan (1991) suggested that
the ancestral Gondwanic skink karyotype may have
been metacentric and that subsequent speciation led
to inversions that established a heteromorphism in the
Australasian Scincidae. The karyotype Hardy (1979)
presented for Leiolopisma telfairi from Mauritius was
identical to that of Oligosoma in New Zealand. This
similarity in karyotype between L. telfairi and Australasian skinks suggests a conserved karyotype and,
possibly, a Gondwanic origin for their common ancestor.
The genus Cyclodina appears to be derivative of Oligosoma in which a heteromorphism became established on chromosome 6. Heteromorphism in chromosome 6 appears genus wide, suggesting a pericentric inversion established before significant species divergence. On limited evidence, it appears that New
Zealand skinks share a conserved karyotype with L.
telfairi, which differs from that of Australian skinks.
Species in the genus Oligosoma have a karyotype identical to that of L. telfairi, and the New Zealand Cyclodina karyotype is a derivation from a similar karyotype in Oligosoma.
Acknowledgments.—I thank C. H. Daugherty for access to the skinks, G. K. Rickards for supervision and
critical reading of the manuscript, R. A. Hitchmough
for identification of skinks, and Leigh, Adrian, and Frances for support.
LITERATURE CITED
DAUGHERTY, C. H., G. B. PATTERSON, C. J. THORN, AND
D. C. FRENCH. 1990. Differentiation of the members of the New Zealand Leiolopisma nigriplantare
species complex (Lacertilia: Scincidae). Herpetological Monographs 4:61–76.
DAUGHERTY, C. H., G. B. PATTERSON, AND R. A.
HITCHMOUGH. 1994. Taxonomic and conservation
review of the New Zealand herpetofauna. New
Zealand Journal of Zoology 21:317–323.
DONNELLAN, S. C. 1991. Chromosomes of Australian
lygosomine skinks (Lacertilia: Scincidae) II. The
genus Lampropholis. Genetica 83:223–234.
GREEN, D. M., AND S. K. SESSIONS. 1991. Nomenclature for Chromosomes. In D. M. Green and S. K.
Sessions (eds.), pp. 431–432. Amphibian Cytogenetics and Evolution. Academic Press, San Diego,
CA.
HARDY, G. S. 1977. The New Zealand Scincidae (Reptilia: Lacertilia); a taxonomic and zoogeographic
study. New Zealand Journal of Zoology 4:221–325.
. 1979. The karyotypes of two scincid lizards,
and their bearing on relationships in genus Leiolopisma and its relatives (Scincidae: Lygosominae).
New Zealand Journal of Zoology 6:609–612.
HICKSON, R. E., D. PENNY, AND D. B. SCOTT. 1992.
Molecular systematics and evolution in New Zealand: applications to cryptic skink species. New
Zealand Journal of Zoology 19:33–44.
KING, M. 1973. Karyotypic studies of some Australian
Scincidae (Reptilia). Australian Journal of Zoology
21:21–32.
O’MALLEY, F. M. 1971. The karyotypes of three species of New Zealand lizard (Scincidae): a preliminary study. Unpubl. BSc honors thesis, Victoria
Univ. of Wellington, Wellington, New Zealand.
PATTERSON, G. B., AND C. H. DAUGHERTY. 1990. Four
new species and one new subspecies of skinks, genus Leiolopisma (Reptilia: Lacertilia: Scincidae)
from New Zealand. Journal of the Royal Society of
New Zealand 20:65–84.
. 1995. Reinstatement of the genus Oligosoma
(Reptilia: Lacertilia: Scincidae). Journal of the Royal
Society of New Zealand 25:3 327–331.
VOS, M. E. 1988. A biochemical, morphological and
phylogenetic review of the genus Cyclodina. Unpubl. BSc honors thesis, Victoria Univ. of Wellington, Wellington, New Zealand.
Accepted: 20 August 2002.