785
Sea Snakes (Laticauda spp.) Require Fresh Drinking Water:
Implication for the Distribution and Persistence of Populations
Harvey B. Lillywhite1,*
Leslie S. Babonis1
Coleman M. Sheehy III1,†
Ming-Chung Tu2
1
Department of Zoology, University of Florida, Gainesville,
Florida 32611-8525; 2Department of Life Science, National
Taiwan Normal University, Taipei, Taiwan
Accepted 3/17/2008; Electronically Published 9/26/2008
ABSTRACT
Dehydration and procurement of water are key problems for
vertebrates that have secondarily invaded marine environments.
Sea snakes and other marine reptiles are thought to remain in
water balance without consuming freshwater, owing to the ability of extrarenal salt glands to excrete excess salts obtained either
from prey or from drinking seawater directly. Contrary to this
long-standing dogma, we report that three species of sea snake
actually dehydrate in marine environments. We investigated
dehydration and drinking behaviors in three species of amphibious sea kraits (Laticauda spp.) representing a range of
habits from semiterrestrial to very highly marine. Snakes that
we dehydrated either in air or in seawater refused to drink
seawater but drank freshwater or very dilute brackish water
(10%–30% seawater) to remain in water balance. We further
show that Laticauda spp. can dehydrate severely in the wild
and are far more abundant at sites where there are sources of
freshwater. A more global examination of all sea snakes demonstrates that species richness correlates positively with mean
annual precipitation within the Indo–West Pacific tropical region. The dependence of Laticauda spp. on freshwater might
explain the characteristically patchy distributions of these reptiles and is relevant to understanding patterns of extinctions
and possible future responses to changes in precipitation related
to global warming. In particular, metapopulation dynamics of
the Laticauda group of sea snakes are expected to change in
relation to projected reductions of tropical dry-season
precipitation.
* Corresponding author; e-mail: [email protected].
†
Present address: Department of Biology, Amphibian and Reptile Diversity Research Center, University of Texas, Arlington, Texas 76019.
Physiological and Biochemical Zoology 81(6):785–796. 2008. 䉷 2008 by The
University of Chicago. All rights reserved. 1522-2152/2008/8106-7208$15.00
DOI: 10.1086/588306
Introduction
The evolutionary transition of animals between land and water
alters selection forces and leads to dramatic changes in body
form, prey type, physiology, reproduction, and other characters
(Zimmer 1998; Mazin and Buffrenil 2001). The marine transition appears to be especially difficult, with salinity posing a
strong physiological barrier (Dunson 1979; Dunson and Mazzotti 1989). In spite of this, numerous reptilian lineages contact
or utilize coastal waters, including various turtles, crocodilians,
the marine iguana, and disparate lineages of snakes. However,
relatively few species have become adapted to a fully marine
existence. Five evolutionary lineages of snakes have invaded the
marine environment. The Laticauda group of sea snakes and
homalopsine and natricine colubrids all retain some connection
to terrestrial habitats, whereas hydrophiine sea snakes and acrochordids are entirely marine or aquatic. Collectively, the sea
snakes are exceptional in having numerous fully marine species
and being widely distributed throughout much of the world’s
marine, and particularly near-shore, tropical waters (Dunson
1975; Heatwole 1999). They can be locally abundant and are
important components of coral reef communities, many being
top predators on specific fishes (Heatwole 1999; Alcala 2004).
Currently about 60 species of sea snakes are recognized, belonging to either two families or two subfamilies, depending
on the taxonomic arrangement. One phylogeny separates terrestrial Asian, African, and American elapids plus oviparous
sea kraits (Laticauda spp.) that make up the Elapidae from the
Australo-Papuan elapids plus viviparous sea snakes classified
as Hydrophiidae (Smith et al. 1977). However, most authors
retain the family Elapidae for all species of elapids and follow
the aforementioned division by a separation into two subfamilies, the Elapinae and the Hydrophiinae, respectively. The relationship between the fully marine hydrophiine sea snakes and
the amphibious Laticauda has been the subject of much debate
(Rasmussen 1997). Most recent studies based on morphology
and molecular data do not support a close affinity of Laticauda
with Asian, African, and American terrestrial elapids, and Slowinski et al. (1997) formally moved Laticauda from the elapine
to the hydrophiine lineage. While it seems clear that all of the
lineages that are referred to as “sea snakes” are closely related
and originated from terrestrial elapid ancestors, Laticauda spp.
and the “true” sea snakes do not form a monophyletic group
and likely represent two separate invasions of the marine environment (Keogh 1998).
786 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
Studies of marine and estuarine snakes have demonstrated
that adaptation to seawater involves physiological as well as
behavioral specializations (Dunson 1980, 1984), and salt glands
are considered key adaptations for excreting excess salts gained
from prey or from the marine environment. Little is understood, however, concerning the basic requirements for water
balance and the potential role of salt glands in regulating water
homeostasis. Current opinions hold that sea snakes and other
marine reptiles such as sea turtles can exist in marine environments without freshwater because extrarenal salt glands can
desalinate saline water that is obtained from prey or from the
sea directly (Heatwole 1999; Randall et al. 2002).
Studies of the single marine species of file snake (Acrochordidae: Acrochordus granulatus, not a “sea snake”) have
demonstrated that these unusual reptiles are ammonotelic and
require a source of freshwater largely for elimination of nitrogenous wastes, which result from deamination of protein
loads associated with a fish diet (Lillywhite and Ellis 1994).
These snakes gradually dehydrate in seawater (Lillywhite and
Ellis 1994), in spite of the fact that they possess a functional
salt gland (Dunson and Dunson 1973). Sea kraits Laticauda
colubrina, which are amphibious and oviparous, have been observed drinking freshwater from island vegetation after rainfall
(Guinea 1991), while the pelagic and fully marine hydrophiine
species Pelamis platurus has been observed to drink freshwater
in the laboratory (Dunson and Robinson 1976). Indirectly,
these observations provide an important but previously underappreciated revelation concerning physiology. The thirst exhibited by snakes seen drinking freshwater in the wild indicates
that these animals were in negative water balance, and this
presumably would not be the case if these snakes could utilize
water from the ocean or from prey using salt glands. Thus a
fundamental question arises: Do the highly specialized “sea
snakes” require freshwater to remain in water balance? This
question has significant implications for understanding the distribution and persistence of snakes in marine habitats.
We investigated this question with respect to three species
of sea snake that are common at Orchid Island (Lanyu), Taiwan.
All three are Laticauda species (hereafter referred to as “sea
kraits”) with varying degrees of terrestrial tendency (see note
in Table 1). We have investigated directly whether these snakes
drink seawater or whether they require freshwater to rehydrate
after losses of body water. We also investigated whether these
marine species dehydrate when kept in seawater without a
source of freshwater for drinking. Here we report that three
species of sea kraits dehydrate both in air and in seawater and
that these snakes voluntarily correct for deficits of body water
by drinking fresh or relatively dilute brackish water while refusing to drink seawater or strongly brackish water. Further,
we demonstrate that populations of sea kraits are more abundant where there are sources of freshwater. These data are contrary to current textbook dogma concerning the role of salt
glands in regulating water balance of sea snakes, and they have
important implications for understanding the present and future biogeography of these marine reptiles.
Material and Methods
We investigated drinking behaviors and water requirements in
each of three species of Laticauda: L. colubrina, L. laticaudata,
and L. semifasciata. All animals were collected at coastal sites
around the perimeter of Orchid Island (Lanyu), Taiwan (Fig.
1), and were returned to the laboratory at the National Taiwan
Normal University in Taipei, where the laboratory work was
conducted. Field and laboratory studies were carried out during
July and August of 2005 and during June and July of 2006 and
2007.
Field Sites and Animal Collections
Preliminary observations at various field sites during early collections of snakes in 2005 suggested that Laticauda spp. were
relatively more abundant at a location where a freshwater spring
mixed with coastal seawater. Subsequently, we selected eight
different sites for making field observations of abundance, representing areas with and without known sources of freshwater
other than rainfall. Field sites were selected based on the prior
experience and knowledge of M.-C. Tu. Sources of freshwater
were identified by direct observation and the knowledge of local
indigenous people. We sampled the water at various locations
at each site during 2006 and measured the salinity using an
Atago S/Mill refractometer. The salinity measurements ranged
from 0 to 30 ppt in gradients consistent with topography of
the inlets and sources of freshwater at what we called “freshwater” sites and were a constant 32 ppt at strictly seawater sites.
At each site, the relative abundance of sea snakes was estimated
by the collective sightings of three to five people who searched
tidal pools, adjacent rocks, and shallow coastal areas for 1 h
during evenings after dark when the snakes were most active.
During repeated visits to various sites, we consistently covered
the same tidal pools, inlets, and rocks. There was no correlation
between the number of people searching and the number of
snakes observed (r p 0.121; P p 0.5518), suggesting that increasing the number of people did not increase the number of
snakes that were found.
Dehydration and Drinking
Air. In 2006, we collected live snakes of all three species from
coastal lagoons, rocks, and pools and returned 47 animals to
the laboratory at National Taiwan Normal University in Taipei
for dehydration and drinking experiments. A total of 35 animals
representing all three species were dehydrated in air, and another 12 L. semifasciata were kept in seawater. An additional
30 snakes (10 L. colubrina, six L. laticaudata, 14 L. semifasciata)
were collected for repetition of the seawater studies in 2007.
Snakes that were dehydrated in air (n p 35) during 2006
were held individually in marked mesh bags and weighed daily
for 2 wk. The bags were kept separated on shelves and exposed
to laboratory air during periods between mass determinations.
At the end of 2 wk, each snake was placed individually into
Freshwater Requirement of Sea Kraits 787
Table 1: Dehydration parameters (mean Ⳳ SE) for three species of sea snakes dehydrated for 2 wk in air, then offered
seawater followed by freshwater
Cumulative
Dehydration Deficit
Freshwater Drunk
Species
n
Body
Mass (g)
Total
Mass (g)
Mass
Percentage
Total
Mass (g)
Mass
Percentage
Deficit
Percentage
Laticauda colubrina
Laticauda laticaudata
Laticauda semifasciata
14
9
12
258.1 Ⳳ 65.5A
205.1 Ⳳ 16.2A
554.6 Ⳳ 38.4B
21.9 Ⳳ 3.7A
31.5 Ⳳ 2.3A
75.5 Ⳳ 4.8B
9.6 Ⳳ .5A
15.5 Ⳳ .5B
13.7 Ⳳ .4B
11.1 Ⳳ 2.5A
15.8 Ⳳ 2.6A
29.9 Ⳳ 4.4B
4.9 Ⳳ .7
8.0 Ⳳ 2.6
5.4 Ⳳ .6
51.8 Ⳳ 7.1A
51.2 Ⳳ 7.2AB
39.5 Ⳳ 4.5B
Note. No seawater was drunk by any snakes in this experiment. Species are listed in order of decreasing terrestrial tendencies. Laticauda colubrina
spends considerable time on land, hiding among rocks near shoreline; L. laticaudata emerges onto rocks but spends most time in water; L semifasciata
is nearly fully aquatic except for egg laying. Different superscript letters indicate data that are statistically different for comparisons of species within a
column (ANOVA, P ! 0.05).
seawater and observed for 1 h. After the 1-h period of observation, each snake was reweighed and then placed individually
in seawater within a plastic aquarium, where it was held overnight. All snakes were reweighed the following morning, 18–
20 h later. Each snake was then placed individually into a plastic
aquarium half-filled with freshwater (∼2 L) and observed for
1 h. Snakes were weighed at the end of the hour. Nearly all
snakes drank freshwater immediately, so they were not routinely
held overnight in freshwater to test for additional drinking.
However, six L. colubrina were held in freshwater overnight and
reweighed the following morning.
In addition to the above, three L. semifasciata and one L.
colubrina (dehydrated for 2 wk) were placed in 50% (16 ppt)
seawater for 1 h after their refusal to drink in full seawater.
After all snakes refused to drink 50% seawater, one of the three
L. semifasciata and the L. colubrina were placed in 25% (8 ppt)
seawater (1 h). The other two L. semifasciata were given the
opportunity to drink freshwater to rehydrate, similar to the
majority of snakes in the experiment.
Seawater. During 2006, 12 L. semifasciata (different individuals
than those used above) were divided into two groups and held
in large seawater tanks (110 cm long # 50 cm wide # 55 cm
high) with three snakes per tank. Each tank was filled halfway
with seawater (∼57 L) and provided with a floating cafeteria
tray under which snakes could hide. Six of the animals remained in seawater for the entire experiment (controls), while
the remaining six were transferred to freshwater aquaria and
given the opportunity to drink freshwater for 1 h every other
day. Each snake in the second group was weighed immediately
before and after access to freshwater. Snakes in the first group
were also weighed at this time. In this manner, all snakes were
weighed at 2-d intervals for 10 d, with half of the snakes given
a 1-h opportunity to drink freshwater at these times. Each snake
was dried with a towel before each mass determination.
The seawater dehydration experiment was repeated for a
longer period in 2007. Snakes collected in 2007 (14 L. semifasciata, 10 L. colubrina, and 6 L. laticaudata) were assigned to
various plastic aquaria with two to four animals per container,
depending on their size. Each container was filled to halfway
with seawater and contained flower pots for anchoring and
refuge. As in 2006, the larger containers were half-filled with
seawater (∼57 L) and also had a floating tray under which
snakes could hide. Based on the previous studies, we knew that
snakes dehydrated slowly in seawater, so the snakes we studied
in 2007 were weighed once every 3 d for a period of 37 d. As
in 2006, half the total number of each species was assigned to
each of two groups: a constant dehydration group (control)
and a group in which each snake was given the opportunity
to drink freshwater by being held in freshwater for 1 h at the
time of each mass determination. The groups were matched
for size within each species. At the conclusion of the dehydration period, each of the control snakes was offered water for
1 h in each of the following conditions, in sequence: 50%
seawater, 40% seawater, 30% seawater, 20% seawater, 10% seawater, and 0% seawater (freshwater).
During the dehydration trials in seawater, 10 individuals shed
their epidermis, and two individuals defecated, which affected
their subsequent mass measurements. To correct these measurements, the excess loss of mass attributed to shed skin or
feces was adjusted by determining the average mass loss between measurements over the entire trial, based on a calculated
mean of mass decrements between weight measurements but
excluding measurements that involved drinking, shedding, or
defecation events. The excess mass loss attributable to shedding
or defecation was then estimated as the difference between the
mean mass change between measurements (averaged over the
entire trial) and the single interval mass change associated with
a specific shedding or defecation event. This difference was
subtracted from the actual mass change, and such calculations
were carried out for each defecation or shedding event, separately for each species.
Validity. Considering all of our observations and experiments,
it is clear that water gained by snakes when placed in freshwater
was caused by drinking and not by net cutaneous uptake, which
should be negligible for the periods involved (Dunson and
Dunson 1973; Dunson 1978). Many of the snakes were observed to drink, and this always resulted in a gain of mass when
these snakes were subsequently weighed. In the numerous in-
788 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
Figure 1. Map of Lanyu (Orchid Island), Taiwan, with bars illustrating numbers of sea kraits (all species combined) observed at various sites
during 1-h nocturnal searches by three to five people at coastal pools during August of 2005 and June of 2006 and 2007. The vertical scale
indicates total number of snakes seen, and multiple bars or zeros represent surveys on different days. Locations of sites are indicated by arrows,
with solid arrows representing sites with known sources of freshwater, such as springs or streams. Note that there were significantly more
snakes observed at sites with freshwater than at strictly marine sites (t-test: P ! 0.004 ). Solid bars represent snakes seen during wet years (2005,
2006), and open bars represent snakes seen during 2007, which was relatively dry. This figure was modified from a map published by Chen
and Tso (2004). The darkened area around the perimeter of the island represents coastal vegetation, grassland, and cultivated woodland, and
the stippled interior represents primary forest.
stances when snakes were placed in freshwater and no drinking
was observed, they did not gain mass. Further, no snakes gained
mass when kept only in seawater. A net water influx is not
expected in theory insofar as seawater is hyperosmotic to the
snake’s body fluids.
mined from regression analysis, and differences among species
and treatment groups were analyzed by ANCOVA or ANOVA
followed by Fisher’s post hoc tests. Significance of all tests was
set at the conventional level of 0.05.
Results
Statistics
Relative Abundances at Field Sites
With respect to field data from Orchid Island, the differences
in mean number of snakes observed at freshwater and strictly
seawater sites were evaluated using a t-test. Correlation analysis
was used to examine variation in the abundance of snakes in
relation to precipitation preceding yearly visits to Orchid Island
as well as to evaluate the relationship between species richness
of sea snakes at various sites in Asia and the mean annual
precipitation at those sites. Rates of dehydration were deter-
Data for the census of snakes at the various field sites are shown
in Figures 1 and 2. Snakes were several to 70-fold more numerous at the sites having a known source of fresh water (other
than rainfall), and the mean differences for the total snakes
observed at the freshwater and strictly seawater sites (Fig. 1)
are highly significant (t-test: P ! 0.004).
There were also differences in the number of snakes observed
between different years. In particular, 2006 was a wet year at
Freshwater Requirement of Sea Kraits 789
overnight. None of these snakes were seen to drink seawater,
and none gained significant mass (10.5 g) during the total
period in seawater (18–20 h). Each snake was then placed individually into a container of freshwater, and nearly all were
observed to drink. The drinking response was pronounced and
almost immediate in the majority of animals, indicating a
strong degree of thirst. Snakes were weighed at the end of the
hour. All of the 35 snakes (three species) drank freshwater,
except for two Laticauda colubrina and one Laticauda semifasciata that did not gain mass. The mean rehydration from drinking freshwater varied from 40% to 52% of the cumulative mass
deficit (Table 1), or from 53% to 69% of dehydration deficit
if the estimated mass loss due to tissue metabolism was taken
into account (see below). Individual snakes drank from 6 to
62 g of water within the 1-h time limit, representing 3%–14%
of total body mass.
Six L. colubrina were held in freshwater overnight, and none
gained additional mass, including two that refused to drink
during the initial 1-h observation period. Insofar as dehydrated
snakes are not expected to urinate copiously, and no fecal material or urates were observed in the aquaria, the lack of mass
gain by snakes that were not observed to drink confirms that
the increase of mass in the other snakes was caused by drinking
and not by uptake across the skin.
Figure 2. Mean numbers of snakes observed at the two more productive
freshwater sites (Jade Lady and Dragonhead) during 3 yr of field studies. The numbers of snakes correlate positively with precipitation during the previous 6 mo and negatively with the number of dry days
during the previous 6 mo (R2 p 0.961 and 0.985, respectively). Days
were considered dry if the recorded precipitation was ≤1 mm.
Seawater. In the dehydration trials in seawater conducted during 2006, the mass lost by L. semifasciata in seawater was about
one-third that of conspecifics in air (Fig. 3). ANCOVA demonstrated that rates of mass loss were significantly different in
the two groups (P ! 0.05 using log-transformed data), with
mass loss in seawater greater for snakes denied access to fresh
drinking water (Fig. 3; slopes for percentage body mass change
per day for animals with and without fresh drinking water p
⫺0.24 vs. ⫺0.35, respectively). One snake in each group ap-
Orchid Island, whereas 2007 was exceptionally dry during a
prolonged period preceding our visit. Streams were dry and
water was depleted in some of the local villages during our visit
in 2007. The total number of snakes observed at the two freshwater sites where snakes were most abundant correlated positively with precipitation recorded during the 6 mo preceding
each of our visits in the different years from 2005 to 2007 (Fig.
2). Rainfall data were obtained from Web site postings of the
weather station at Orchid Island. Numbers of snakes also varied
inversely with the number of dry days (≤1 mm) during the 6
mo preceding each of the sampling periods (which we also use
as a measure of drought; Fig. 2).
Dehydration and Drinking
Air. After 2 wk of dehydration in air, the mean cumulative mass
deficits ranged from ⫺10% to ⫺16% of body mass in the three
species (Table 1). The snakes were then placed individually into
aquaria with seawater and observed for 1 h before being held
Figure 3. Time course of changes in body mass for Laticauda semifasciata kept in seawater with access to freshwater every other day
(SW ⫹ FW), in full seawater only (SW), or in air (Air) during 2006.
Data points are means (ⳲSE) of the cumulative changes in body mass,
computed as percentage of original mass.
790 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
Figure 4. Plots illustrating patterns of mass loss in four individual
Laticauda semifasciata kept in full seawater with and without (control)
periodic access to freshwater during 2007. Departures of data points
from those of the control snake correspond to drinking events and
result in reversals of mass loss in the three snakes that have access to
freshwater. Note that the threshold for drinking varies among the
snakes illustrated, and one of the snakes experiences a net gain of mass
as a result of repetitive drinking over the course of the experiment.
peared thin and somewhat emaciated when captured, and the
thin individual in the drinking group ingested 62 g of freshwater
(14% of body mass) during the course of the 10 d. This observation confirms past impressions that sea snakes can become
severely dehydrated in nature (H. B. Lillywhite, unpublished
observations; see below).
We obtained data for mass change and dehydration in seawater for all three species in 2007, although relatively few individuals of Laticauda laticaudata were available for study. Mass
changes of L. semifasciata kept in seawater followed a pattern
similar to that found in 2006, except we were able to extend
the trial for a longer period.
All snakes lost mass at relatively constant rates when kept
in seawater without access to freshwater (control in Fig. 4). No
snake displayed any evidence of drinking while in seawater. On
the other hand, snakes that were given periodic access to freshwater were observed to drink and gained mass periodically at
various intervals throughout the trial. Individual patterns were
highly variable. Some snakes drank early in the trial, whereas
others drank later during the trial. At the extremes, one individual refused to drink throughout the trial up to the day
before the final measurement, when the individual died. Another individual drank at six out of 12 opportunities during
the trial and gained, rather than lost, mass overall (Fig. 4).
Other individuals exhibited variable drinking patterns in between these two extremes (Fig. 4). The thresholds of mass loss
at which snakes first drank freshwater were variable, as summarized in Figure 5.
During the collection of snakes in 2007, we tested whether
a subset of snakes would drink freshwater during the day immediately following their capture. For this purpose, each of 13
snakes was placed in a plastic container with freshwater, ob-
served for drinking behavior during a 1–2 h period, and
weighed before and after. None of the snakes were seen to drink,
and none of the snakes gained mass. Given the variability of
drinking among snakes dehydrated in seawater (Figs. 4 and 5),
we assume that the various snakes began the dehydration trial
at variable levels of hydration, although not critical dehydration, because there was no initial expression of thirst. Experiments in 2006 demonstrated that snakes do not drink freshwater until they have experienced a moderate degree of
dehydration.
The overall regression slopes relating mass change with time
were significantly different among species (F p 28.183, P !
0.0001) and between control and freshwater groups (F p
9.036, P p 0.0061; Fig. 6). Further, if slopes relating mass loss
with time are based on data for time periods that begin when
drinking of freshwater commences, those of snakes with access
to freshwater are much less steep than are those of control
groups (in one case slopes were even positive; Fig. 4). As observed in 2006, L. semifasciata lost mass in air approximately
three times faster than in seawater (P ! 0.0001 ; cf. Table 1 and
Fig. 6). However, L. colubrina lost mass at approximately equal
rates in air and in water (P p 0.1268 ), whereas the pattern in
L. laticaudata was intermediate between those of the other two
species (t-test for difference: P ! 0.0001 ; cf. Table 1 and Fig. 6).
At the conclusion of the 2007 trial, all snakes in the control
group were offered access to a graded series of brackish water
samples ranging from 50% seawater to freshwater. No individual snake drank 50% seawater, and most snakes did not drink
until offered very dilute brackish water (10%–30%) or freshwater (Table 2). Generally, the amounts of water ingested by
the control snakes increased with the brackish value (i.e., seawater percentage; see Table 2). These data are complementary
Figure 5. Histogram showing thresholds of mass loss at which snakes
first drank seawater during dehydration trials in seawater. Mean Ⳳ
SD of drinking thresholds for each species are as follows: Laticauda
colubrina, 9.5 Ⳳ 8.1; Laticauda laticaudata, 9.5 Ⳳ 9.8 ; Laticauda semifasciata, 8.8 Ⳳ 2.5.
Freshwater Requirement of Sea Kraits 791
Figure 6. Interaction bar plot illustrating differences in daily mass loss
(means Ⳳ SE) for all three species of sea snakes kept in seawater
during 2007. Filled bars represent control snakes (full seawater only),
and hatched bars represent snakes having periodic opportunities to
drink freshwater. The daily mass losses of snakes were computed from
regression analysis. Both species and group effects were significantly
different from controls (P ! 0.005; see Table 2).
to observations of those few snakes that were offered brackish
water in 2006.
Discussion
Drinking in Sea Kraits: Physiology and Behavior
Our studies are the first to examine in detail whether sea snakes
require freshwater for water balance. Data from three species
of the Laticauda group demonstrate conclusively that (1) these
snakes dehydrate in air and in seawater, (2) they refuse to drink
seawater or strongly brackish water, and (3) they voluntarily
drink fresh or dilute brackish water to replenish body water
deficits.
This new information is highly important in context of physiology because sea snakes possess salt glands that are thought
to secrete excess salts and enable water balance based on consumption of seawater. As an example, the authors of a current
textbook in comparative physiology state, “Marine reptiles (e.g.
marine iguanas, sea turtles, estuarine crocodiles, sea snakes)
and marine birds drink seawater to obtain a supply of water”
(Randall et al. 2002, p. 590). This statement cannot be true for
the species of sea kraits we investigated in Taiwan.
The sea kraits we studied experienced considerable dehydration before they drank water, and the volumes consumed
at drinking were relatively small (Tables 1, 2). This behavior is
in contrast to that of some other snakes, including marine file
snakes (H. B. Lillywhite, unpublished data). Some of the variability in drinking behavior probably reflects individual differences in levels of hydration at the beginning of the dehydration trials. Yokota et al. (1985) suggested that the
hydrophiine sea snake Aipysurus laevis has a limited capacity
to eliminate water loads and regulate volume, which may explain the small volumes of water ingested by the species we
studied; water deficits appear to be made up by intermittent
drinking of modest volumes of water rather than ingesting a
large volume at one time (see Fig. 4). This being said, ingested
water volumes increased with degree of dehydration and with
salinity of the water (Tables 1, 2).
The overall rate of mass loss for Laticauda semifasciata dehydrated in air was about three times greater than that of
conspecifics in seawater (⫺0.98% vs. ⫺0.35% body mass/d;
Fig. 3). Generally, individuals of the more aquatic species (L.
semifasciata) lost water in air at faster rates than did the more
terrestrial species (Laticauda colubrina, Laticauda laticaudata),
and this ranking matches differences in area-specific water vapor resistance of skin (lowest in L. semifasciata, highest in L.
colubrina; H. B. Lillywhite, unpublished data). If these data are
interpreted as adaptations for minimizing water loss that vary
as a function of habitat use, they support the inference that
freshwater is a limiting resource for these snakes. Moreover,
the highly aquatic species, L. semifasciata, exhibits lower rates
of water loss in seawater compared with the more terrestrial
species (Fig. 6). Indeed, rates of water loss in air relate inversely
with the rates of water loss in seawater among the three species
we investigated. The ordering might suggest adaptive species
differences in resistance to water loss related to prevailing habitat and behavior, or it might be explained by spurious factors
such as differences in activity. The former explanation appears
more likely in view of our observations of behavior and our
unpublished measurements of skin resistance.
Table 2: Summary of salinity thresholds at which snakes dehydrated in seawater for 37 d (controls) drank water
when exposed to a graded series of brackish water at the end of the dehydration period
Seawater
50%
Seawater
40%
Seawater
30%
Seawater
Laticauda colubrina
0
0
0
0
0
Laticauda laticaudata
0
0
0
0
Laticauda semifasciata
0
0
0
1
(6.2)
1
(12.6)
3
(4.6 Ⳳ .9)
Species
20%
Seawater
10%
Seawater
0% Seawater
(Freshwater)
3
(6.9 Ⳳ 1.56)
1
(8.9)
2
(2.2 Ⳳ .9)
2
(3.0 Ⳳ 1.1)
1
(2.8)
…
Note. Table entries for each species indicate number of snakes drinking from indicated water source when offered in series. Numbers in
parentheses indicate the percentage original body mass of water ingested (mean Ⳳ SE).
792 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
other observations (e.g., Guinea 1991) indicate that sea snakes
become significantly dehydrated in nature.
Our data suggest that sea kraits are resistant but not immune
to dehydration, and they experience varying degrees of dehydration status in the wild. The variability in drinking threshold
related to mass loss (Figs. 4, 5) probably reflects variability in
individual tolerances relative to thirst, variability in hydration
at the beginning of experimentation, or both. While some of
the snakes we collected in 2007 might have ranged closely to
the sites of capture, others likely dispersed into the sites from
the surrounding seas resulting in a heterogeneous sample of
snakes with respect to prior freshwater access (see Tu 1987).
Whatever the initial levels of hydration were, different snakes
initiated drinking at all levels of dehydration imposed by the
experiment (Fig. 5).
Water Balance in Marine Environments:
Theoretical Considerations
Figure 7. Photographs illustrating “dimpled” condition of scales (arrows) on sea kraits that have experienced significant dehydration (15%
body mass) while exposed to laboratory air (A). The individual Laticauda colubrina (B) was photographed during the 1975 summer dry
season in Papua New Guinea, and the skin condition suggests that
this and other snakes had dehydrated significantly in nature.
Yellow-lipped sea kraits L. colubrina are abundant around
coral reefs and islands in the western Pacific Ocean, and they
inhabit some places where summer rains are scarce and other
sources of freshwater are absent. On various occasions, we have
observed these snakes in conditions where they appeared to be
severely dehydrated. One of us (H. B. Lillywhite), together with
R. S. Seymour, visited a large aggregation of dozens to perhaps
a hundred or more sea kraits on an old grounded marine vessel
in Port Moresby, Papua New Guinea, during mid-July of 1975.
All of the snakes appeared to be uniformly thin or emaciated.
In retrospect, it seems more probable that these snakes were
all dehydrated rather than starving from a common lack of
prey. Port Moresby receives little rainfall during the period from
June to October, when prevailing southeast trade winds act as
a medium for dry air movement, causing arid conditions during
this period. Similarly, H. B. Lillywhite and F. H. Pough found
apparently dehydrated sea kraits beneath objects on small islands in Fiji during a similar drought period (July 1981). Photographs taken of snakes found on small islands at both Papua
New Guinea and Fiji during periods of summer drought suggest
that these snakes were dehydrated at the time because of a
dimpled appearance of the scales (Fig. 7). We noticed during
our dehydration studies that body scales of sea kraits exhibited
a dimpled appearance (with central indentations) when dehydration had proceeded to moderate levels (Fig. 7). These and
It is not known how salt glands function in wild and free-living
snakes. Salt glands may well be important for aspects of ion
balance, but their function appears to be insufficient for water
balance in the species we studied. Previously, it was noted that
many completely marine snakes have “tiny” salt glands with
comparatively low rates of secretion (Dunson and Dunson
1974). One can calculate that a 100-g Aipysurus laevis (a fully
marine hydrophiine sea snake) ingests 5.48 mmol Cl⫺, 4.7
mmol Na⫹, and 0.09 mmol K⫹ with 10 mL of seawater. Based
on data from Dunson and Dunson (1974), elimination of these
ions by means of salt glands requires 6.93 mL of water secreted
over 50.4 h. If median values are assumed for urine flow rates
(Yokota et al. 1985), cloacal water loss during this period would
equal 0.55 mL; thus, total losses of water attributable to both
urine and salt gland secretions would equal 7.48 mL, or 75%
of the water ingested. However, this budgeting for water does
not include cutaneous or respiratory losses (during air
breathing between dives). Further, if the urine flow rates are
assumed to be equal to those measured during salt loading
(Yokota et al. 1985), the water loss attributable to both urine
and salt gland secretions is 10.36 mL, so the snake does not
make a profit in usable water even if we neglect cutaneous and
respiratory losses. It is not known how much urinary water
may be reabsorbed in the cloaca or how much additional water
is required to eliminate nitrogenous wastes (see below). These
and other aspects of water balance are in need of further study.
However, preliminary analysis as shown here suggests that marine snakes cannot drink seawater and depend on salt gland
function to remain in water balance. Although these figures are
approximate and tentative, it is striking that theoretical considerations complement the empirical results we have obtained
for the three Laticauda species.
Some amount of water is gained from marine prey. However,
a conservative input/output analysis of water balance indicates
that snakes in seawater will indeed dehydrate whether snakes
are fasting or fed. Based on assumptions put forward previously
Freshwater Requirement of Sea Kraits 793
by Lillywhite and Ellis (1994), a 100-g snake must consume
0.062 g of wet prey tissue per day to support its maintenance
metabolism. This level of tissue utilization releases 0.047 mL
of preformed water (assuming 76% of tissue mass), and complete oxidation to CO2 produces an additional 0.028 mL, to
yield a total of 0.075 mL water—equivalent to 0.075% body
mass—intake from food. This value is conservative, and marine
fishes generally exhibit lower body water content than do sea
snakes (Thorson 1961; Dunson 1978). Averaging the net water
efflux data for fasting L. semifasciata reported by Dunson (Dunson and Dunson 1973; Dunson 1978), we estimate a net loss
of body water on the order of 0.25% body mass per day. Therefore, if a snake is consuming food sufficient to support its
maintenance metabolic requirement, there remains a net daily
water loss of 0.175% body mass, even assuming excretion of
uric acid and urate salts without water. Comparing net water
efflux data (Dunson and Dunson 1973; Dunson 1978) with
rates of mass loss in the current experiments (control L. semifasciata in Fig. 6), we estimate that approximately one-quarter
of the total loss is attributable to metabolism of tissue in L.
semifasciata (⫺0.08% body mass/d).
Any added water requirement for nitrogen excretion after
the ingestion of fish will worsen the water deficit, depending
on the degree of ammonotelism (Lillywhite and Ellis 1994).
The dependence of marine file snakes (Acrochordus granulatus)
on freshwater is likely attributable to ammonotelism, and even
a freshwater species of homalopsine snake becomes thirsty and
drinks freshwater after a fish meal (Lillywhite and Ellis 1994).
While the metabolic and excretory processes for nitrogen are
unknown in sea snakes, the ammonia concentration in urine
of the hydrophiine sea snake Aipysurus laevis is actually quite
high, making up about half the urine osmolality, assuming
association with a monovalent ion (S. D. Yokota, S. Benyajati,
and W. H. Dantzler, unpublished data). Our calculations for a
feeding snake indicate there remains a net water deficit
(⫺0.175% body mass/d), even assuming that uric acid and
urate salts are excreted without water. This is surely not the
case, so the calculated estimates are very conservative.
While aquarists generally have experienced difficulty in
maintaining sea snakes in captivity, some report having kept
specimens for long periods evidently without access to freshwater (Klemmer 1967). However, the habitat source of the prey
that was fed to these snakes is not known, pointing to a need
for investigations of water balance in sea snakes that are feeding
on normal prey.
Ecology and Distributional Implications
The spatial distribution of sea kraits and other species of sea
snakes is characteristically patchy (Heatwole 1999; Lukoschek
et al. 2007). Some dependence on sources of fresh or diluted
brackish water might explain, in part, some of the patchy distributions, where persistence or extirpation of local populations
might be correlated with historical precipitation patterns.
Clearly, our data from Orchid Island indicate that distributional
patterns of Laticauda spp. are correlated with sources of freshwater (Fig. 1). We cannot judge at present whether such distribution is related to a requirement for drinking freshwater or
to some other associated factor(s) such as prey abundance.
However, the distribution of Laticauda generally coincides with
mean annual low salinity surface waters in the tropical Indian
and Pacific Ocean (Guinea 1991), and this larger-scale pattern
complements our data from Orchid Island. The distribution of
Laticauda spp. among small islands also is quite heterogeneous
(Heatwole 1999). Thus, one might hypothesize a dynamic
metapopulation or biogeographic model in which populations
persist in some areas receiving adequate precipitation and either
die out or emigrate from others during periods of drought.
The latter sites might become repopulated by dispersing individuals during later periods of appropriate climate change.
Generally, there are two principal sources of fresh or dilute
brackish water available to marine snakes: coastal estuaries or
springs and freshwater lenses that form on the ocean surface
during rainfall events. The importance of freshwater lenses as
possible sources of water for marine snakes has been emphasized previously (Dunson and Robinson 1976; Lillywhite and
Ellis 1994; Heatwole 1999). Surface lenses of fresh or brackish
water are characterized by depressions in sea surface salinity,
Table 3: Drinking behavior and water requirements of marine snakes
Taxon
Colubridae:
Natricinae
Homalopsinae
Acrochordidae
Elapidae:
Laticauda spp.
Hydrophiinae
Drinks
Freshwater?
Requires
Freshwater?
Salt Gland
Present?
Source
Yes
Yes
Yes
Yesa
Yesa
Yes
No(?)
Yes
Yes
Dunson 1980; L. S. Babonis, unpublished data
Dunson and Dunson 1979
Lillywhite and Ellis 1994; Lillywhite 1996
Yes
Yes
Yes
?a
Yes
Yes
This study
Dunson and Robinson 1976
Note. A freshwater requirement is based on knowledge that animals experience mass loss in seawater, which stimulates thirst, and restore
water balance by voluntarily drinking freshwater but not seawater or strongly brackish water.
a
Snakes survive in seawater for long periods but gradually dehydrate. The role of food in providing water is not known. Only one or a
small number of representative species have been investigated.
794 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
Figure 8. Increase in species diversity (richness) of sea snakes (P p
0.047) with mean annual precipitation for strictly tropical regions of
Asia and Australasia identified and inventoried by Heatwole (1999).
Precipitation data were averaged for the period 1980–2004 and are
available from the Global Precipitation Climatology Project (Pidwirny
2006).
and the freshwater can extend to depths of 20 m (Tomczak
1995). The resultant salinity variations are associated with the
temporal and spatial variability of precipitation, and the lifetime
and depth of these lenses depend on the convective regime in
which the precipitation occurs (Tomczak 1995; Schrage and
Clayson 2003). Freshwater lenses are not well studied in relation
to the context we discuss here, but such lenses likely persist at
lower salinities where rainfall is intense or protracted at shallow
coastal waters or lagoons formed by fringing reefs or atolls.
The behaviors of marine file snakes (Acrochordus granulatus)
from mangrove populations suggest that these animals naturally
obtain fresh or brackish water from surface lenses that are
formed by rainfall (Lillywhite and Ellis 1994; Lillywhite 1996).
At present, species representing four of the five phylogenetic
lineages of marine snakes require freshwater (or dilute brackish
water) for normal water balance (Table 3). We cannot at present
extend this conclusion to the fully marine hydrophiine species;
however, further investigations related to a hypothesis of freshwater requirement will be of much interest in light of the currently available data (Heatwole 1999). Studies of water flux
rates in hydrophiine sea snakes indicate that there is a net water
efflux in seawater, and the pelagic species Pelamis platurus reportedly dehydrates when fasting in seawater (Dunson and
Dunson 1976; Dunson 1978, 1979).
Using data for known distributions of Laticauda and hydrophiine species combined, we demonstrate that global patterns
of sea snake density (species richness) correlate positively with
mean annual precipitation within the tropics (Fig. 8). Of course,
rainfall seems unlikely to influence speciation processes directly.
However, evolving populations having a physiological requirement for freshwater are more likely to survive in regions of
high precipitation. This could be true even if freshwater were
not an absolute requirement but simply physiologically advan-
tageous. This might well be reflected in our time series of data
relating changes in abundance of Laticauda spp. with precipitation at Orchid Island (Fig. 2). The stochastic nature of rainfall
patterns, both temporally and spatially, likely limits at least
some marine snake distributions and could explain recent extirpations or extinctions of sea snake populations (Lukoschek
et al. 2007). Changing availability of freshwater therefore potentially influences the dynamics of reef system communities
where these snakes exist as predators. However, we are unaware
of any studies comparing fish densities in reef systems with
and without sea snakes present.
Sea snakes occur largely in tropical and subtropical waters
throughout the Indo–West Pacific region. Precipitation has generally decreased over the tropics since the 1970s (Hulme et al.
1998) and is projected to decrease during dry seasons and
thereby intensify tropical summer droughts (Neelin et al. 2006;
Christensen et al. 2007). Patterns of climatic changes and biological responses to climate are expected to be complex in the
tropics because precipitation changes are projected to be abrupt
(Thompson et al. 2006) and to have strong spatial variation
with positive and negative anomalies on a regional scale (Chou
et al. 2006; Christensen et al. 2007; Meehl et al. 2007). Because
of their tropical distribution and dependence on freshwater, we
may expect to see changes in at least some marine snake populations in response to the projected alterations of precipitation.
Conclusions and Directions for Further Research
In summary, several species of marine snakes cannot maintain
water balance without a source of freshwater, despite the ability
of salt glands to ameliorate ion balance (Dunson and Robinson
1976). This conclusion might also apply to other marine reptiles
that drink and appear to rely on freshwater (Dunson 1970;
Dunson and Dunson 1979; Dunson and Mazzotti 1989). Understanding the water requirements of all sea snakes could
prove to be very important to their conservation and to consideration of these reptiles as possible indicator species for the
health of coral reefs (Alcala 2004). Distributional patterns of
sea snakes and possibly other marine reptiles are likely to change
as a result of current and future climatic trends or anomalies,
including those related to precipitation. We are pursuing such
investigations, and we hope soon to clarify whether representative hydrophiine sea snakes might require freshwater as do
the Laticauda spp. that we report and discuss here.
Acknowledgments
We thank the National Geographic Society (CRE [Committee
for Research and Exploration] grant 8058-06 to H.B.L.), the
University of Florida, and the National Taiwan Normal University for supporting this research, which was conducted with
approval of the Institutional Animal Care and Use Committees
of the University of Florida and the National Taiwan Normal
University. We are also grateful to Kent Hatch, Denise Doiron,
Freshwater Requirement of Sea Kraits 795
Hui-Min Chu, Chun-Jui Chang, Chelsey Campbell, and Ryan
McCleary for assistance in the field and laboratory, and we
thank Harold Heatwole and Jamie Gillooly for comments and
information that helped to improve the manuscript. We greatly
appreciate the approval granted from the Orchid Island administrative office to remove snakes that were used in this study.
Literature Cited
Alcala A.C. 2004. Marine Reserves as Tool for Fishery Management and Biodiversity Conservation: Natural Experiments in the Central Philippines, 1974–2000. Silliman University, Angelo King Center for Research and Environmental
Management, Dumaguete City.
Chen K.-C. and I.-M. Tso. 2004. Spider diversity on Orchid
Island, Taiwan: a comparison between habitats receiving different degrees of human disturbance. Zool Stud 43:598–611.
Chou C., J.D. Neelin, J.-Y. Tu, and C.-T. Chen. 2006. Regional
tropical precipitation change mechanisms in ECHAM4/
OPYC3 under global warming. J Clim 19:4207–4223.
Christensen H.J., B. Hewitson, A. Busuioc, A. Chen, X. Gao,
I. Held, R. Jones, et al. 2007. Regional climate projections.
Pp. 848–940 in S. Solomon, D. Qin, M. Manning, Z. Chen,
M. Marquis, K.B. Averyt, M. Tignor, and H.L. Miller, eds.
Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report
on the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
Dunson W.A. 1970. Some aspects of electrolyte and water balance in three estuarine reptiles, the diamondback terrapin,
American and “salt water” crocodiles. Comp Biochem Physiol 32:161–174.
———. 1975. The Biology of Sea Snakes. University Park Press,
Baltimore.
———. 1978. Role of the skin in sodium and water exchange
of aquatic snakes placed in seawater. Am J Physiol 235:R151–
R159.
———. 1979. Control mechanisms in reptiles. Pp. 273–322 in
R. Gilles, ed. Mechanisms of Osmoregulation in Animals.
Wiley-Interscience, New York.
———. 1980. The relation of sodium and water balance to
survival in sea water of estuarine and fresh water races of
the snakes Nerodia fasciata, N. sipedon, and N. valida. Copeia
1980:268–280.
———. 1984. The contrasting roles of the salt glands, the integument and behavior in osmoregulation of marine reptiles.
Pp. 107–129 in A. Pequeux, R. Gilles, and L. Bolis, eds.
Osmoregulation in Estuarine and Marine Animals. Springer,
Berlin.
Dunson W.A. and M.K. Dunson. 1973. Convergent evolution
of sublingual salt glands in the marine file snake and the
true sea snakes. J Comp Physiol 86:193–208.
———. 1974. Interspecific differences in fluid concentration
and secretion rate of sea snake salt glands. Am J Physiol 227:
430–438.
———. 1979. A possible new salt gland in a marine homalopsid
snake (Cerberus rhynchops). Copeia 1979:661–672.
Dunson W.A. and F.J. Mazzotti. 1989. Salinity as a limiting
factor in the distribution of reptiles in Florida Bay: a theory
for the estuarine origin of marine snakes and turtles. Bull
Mar Sci 44:229–244.
Dunson W.A. and G.D. Robinson. 1976. Sea snake skin: permeable to water but not sodium. J Comp Physiol 108:303–
311.
Guinea M.L. 1991. Rainwater drinking by the sea krait Laticauda colubrina. Herpetofauna 21:13–14.
Heatwole H. 1999. Sea Snakes. Krieger, Malabar, FL.
Hulme M., T.J. Osborn, and T.C. Johns. 1998. Precipitation
sensitivity to global warming: comparison of observations
with HadCM2 simulations. Geophys Res Lett 25:3379–3382.
Keogh J.S. 1998. Molecular phylogeny of elapid snakes and a
consideration of their biogeographic history. Biol J Linn Soc
63:177–203.
Klemmer K. 1967. Observations on the sea-snake Laticauda
laticaudata in captivity. Int Zoo Yearb 7:229–231.
Lillywhite H.B. 1996. Husbandry of the little file snake, Acrochordus granulatus. Zoo Biol 15:315–327.
Lillywhite H.B. and T.M. Ellis. 1994. Ecophysiological aspects
of the coastal-estuarine distribution of acrochordid snakes.
Estuaries 17:53–61.
Lukoschek V., H. Heatwole, A. Grech, G. Burns, and H. Marsh.
2007. Distribution of two species of marine snakes, Aipysuruss laevis and Emydocephalus annulatus, in the southern
Great Barrier Reef: metapopulation dynamics, marine protected areas and conservation. Coral Reefs 26:291–307.
Mazin J.-M. and V. de Buffrenil. 2001. Secondary Adaptation
of Tetrapods to Life in Water: Proceedings of the International Meeting, Poitiers. Pfeil, München.
Meehl G.A., T.F. Stocker, W.D. Collins, P. Friedlingstein, A.T.
Gaye, J.M. Gregory, A. Kitoh, et al. 2007. Global climate
projections. Pp. 748–845 in S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, and H.L.
Miller, eds. Climate Change 2007: The Physical Science Basis.
Contribution of Working Group I to the Fourth Assessment
Report on the Intergovernmental Panel on Climate Change.
Cambridge University Press, Cambridge.
Neelin J.D., M. Münnich, H. Su, J.E. Meyerson, and C.E. Holloway. 2006. Tropical drying trends in global warming models
and observations. Proc Natl Acad Sci USA 103:6110–6115.
Pidwirny M. 2006. Global Distribution of Precipitation.
http://www.physicalgeography.net/fundamentals/8g.html.
Randall D., W. Burggren, and K. French. 2002. Eckert Animal
Physiology. W.H. Freeman, New York.
Rasmussen A.R. 1997. Systematics of sea snakes: a critical review. Symp Zool Soc Lond 70:15–30.
Schrage J. and C.A. Clayson. 2003. Precipitation and fresh water
lens formation in the tropical western Pacific. Proc. 12th
796 H. B. Lillywhite, L. S. Babonis, C. M. Sheehy III, and M.-C. Tu
Conference on Interactions of the Sea and Atmosphere, extended abstract J5.5.
Slowinski J.B., A. Knight, and A.P. Rooney. 1997. Inferring
species trees from gene trees: a phylogenetic analysis of the
Elapidae (Serpentes) based on the amino acid sequences of
venom proteins. Mol Phylogenet Evol 8:349–362.
Smith H.M., R.B. Smith, and H.L. Sawin. 1977. A summary of
snake classification (Reptilia, Serpentes). J Herpetol 11:115–
121.
Thompson L.G., E. Mosley-Thompson, H. Brecher, M. Davis,
B. León, D. Les, P.-N. Lin, T. Mashiotta, and K. Mountain.
2006. Abrupt tropical climate change: past and present. Proc
Natl Acad Sci USA 103:10536–10543.
Thorson T.S. 1961. The partitioning of body water in Osteich-
thyes: phylogenetic and ecological implications in aquatic
vertebrates. Biol Bull 120:238–254.
Tomczak M. 1995. Salinity variability in the surface layer of the
tropical western Pacific Ocean. J Geophys Res 100:20499–
20515.
Tu M.C. 1987. Ecological Studies of the Sea Snake (Laticauda
semifasciata) around Orchid Island, South Eastern Taiwan.
MS thesis. National Sun Yat-sen University, Kaohsiung.
Yokota S.D., S. Benyajati, and W.H. Dantzler. 1985. Renal function in sea snakes. I. Glomerular filtration rate and water
handling. Am J Physiol 249:R228–R236.
Zimmer C. 1998. At the Water’s Edge: Macroevolution and the
Transformation of Life. Free Press, New York.