Chapter 11 - Life in the water
11. Life in the Water
…the gradations between the land and the
fresh-water species, and between the latter and the salt-water snakes…are, like
all other herpetological features, extremely close.
Catherine Hopley, 1882
It
was sunset over Thailand’s Andaman Sea coast, and we stood in water and mud
over our knees searching the mangrove for homalopsid snakes. Four of us were
spread out between mud lobster mounds waiting for dark. We had partially
excavated several lobster mounds earlier in the day, uncovering a few lobster
tunnels and a single, small lobster. Judging by the number of mounds and the
presence of large trees, this habitat was relatively undisturbed. The mound I
was standing next to was about five feet high with a tree growing out of its
side. The entrance to the lobster’s burrow was offset from the top of the mound
and crabs, mudskippers, and peanut worms were using the surface of the mound.
Crab-eating frogs (Fejervarya cancrivora) were also here, using burrow openings
to ambush passing crustaceans. It seemed likely that snakes were also using the
lobster’s burrows for refuge and foraging. Graduate students at the National
University of Singapore researching Mud Lobsters had reported finding snakes
when they excavated the mounds. And, of course, somewhere within the pile of
mud and muck were one or more Mud Lobsters (Thalassina anomala), the engineers
that had constructed the mound. Mud Lobsters are the earthworms of the mangrove
forest, filtering the soil for nutrients and piling up the undigested material
to form the mounds. Most of the lobster mounds are located on the landward edge
of the mangrove forest where some of the land is washed by the sea twice a day.
Still, leaf litter had accumulated in areas the sea could not reach.
Using
flashlights we walked between and around the mounds, searching the shallow
pools and the exposed mud for snakes. Shortly after our search began I heard
leaves rustling to my right. Expecting to find a foraging snake, I was quite
surprised to see an octopus moving overland through the leaf litter. After
another half-hour of searching, one of my companions found an Asian Bockadam
(Cerberus rynchops), one of the first species recognized to have grooved rear
fangs and the species Hermann Schlegel refused to believe venomous (see Chapter
4). The snake moved from land to water, diving into the mud slurry and
surfacing 10 meters away. It was the only snake we saw that night.
Water
changes the rules. Water supports an animal’s body weight and is slow to lose
or gain heat. Salt can render water
undrinkable, but some coastal and marine snakes are believed to have a salt
gland to remove excess salt. Salt also increases the density of water, making animals
more buoyant. Water provides other
opportunities. Warm water reduces the need for basking. Water also lowers the
risk of predation from terrestrial and aerial predators. Water provides
abundant food resources in the form of invertebrates, fish, and amphibians.
Water also presents a variety of new hiding places such as the intertidal
burrow system. Of course aquatic environments also expose their inhabitants to a
new set of predators and dangers from the physical environment.
Virtually
all snakes are capable of swimming, but some species are much better at it than
others. Most all major lineages of snakes have some species adapted to aquatic
habitats, and five lineages (file snakes, the homalopsids, elapids, dipsidids, and
the natricids) contain many species highly adapted for life in water. Snake
adaptations to water include modifications to virtually all organ systems.
However, all adaptations to an aquatic existence do not occur in every aquatic
snake, and while some species have extreme adaptations to life in water, others
appear to have very few. In the introductory quote, Catherine Hopley recognized
this and its significance. Dorsally
positioned nostrils and eyes allow the snake to breathe and observe without
exposing the head or body to air [Figure 11–1]. When diving, valves open and
close the nostrils, and the trachea opens opposite the internal nares to
exclude water from the respiratory tract. The body can be laterally compressed
to increase the surface for swimming, the ribs may be less bowed out, and they
may be elevated to exaggerate the surface on the sides of the snake. The tail
may also be flattened; it may be compressed slightly at the base, or turned
into a paddle with exaggerated fin-like flaps above and below the tail
vertebrae. Ventral scales are broad in land dwelling snakes so the snakes can
grip surfaces; in highly aquatic snakes, these are reduced so the belly scales
are similar in size to the dorsal scales [Figure 11–2]. Undoubtedly, this
reduction in ventral scales aids the snake in flattening its body for increased
surface area when swimming. Additionally, the snakes most adapted for an
aquatic existence swallow food while submerged and give birth in the water.
INSERT
FIGURE 11-1.
Figure 11–1. A dorsal view of the head of
Jagor’s Mud Snake, Enhydris jagorii. Note the eyes and nostrils are located on
or near the top of the head and that the mottling makes this snake’s head very
cryptic.
Snakes
using water to hunt are not always strong swimmers or even well adapted for
swimming. Ambush predators may simply use the water for concealment and retain
much of the morphology they used on land. Other snakes hunt shorelines and
search small pools without entering the water, and a few snakes hunt from
branches and strike prey from a perch over the water. The fact that arboreal
snakes can use aquatic resources without morphological modifications to aquatic
habitats is a great reminder of the impressive plasticity we see in life.
INSERT
FIGURE 11-2.
Figure 11–2. A: Ventral scales of the
semi-aquatic natricid, the Plain-bellied Water Snake (Nerodia erythrogaster)
are very wide, rounded scales. B: Ventral scales of the highly aquatic
homalopsid, the Tentacled Snake (Erpeton tentaculatus) are very narrow ventral
scales that are hexagonal and keeled (arrow).
Not
surprisingly, the largest snakes often use water. The largest living boa, the Green
Anaconda (Eunectes murinus), is highly aquatic and the largest pythons have
strong affinities for water. Not only does water provide buoyancy for heavy
bodies, but it allows the largest snakes to conceal themselves while hunting.
File Snakes
Bizarre
may be the best single word to describe file snakes of the family Acrochordidae.
The advantage to their unusual anatomy was a puzzle for a very long time.
Highly aquatic, file snakes are covered with loose skin and small, rough scales
that have sensory organs. They have short, stubby, prehensile tails and the
eyes and nostrils are located on top of the head. Their lack of muscle tone is
spectacular, and can only be fully appreciated by an attempt to hold one. The rough, file-like surface of the skin and
its loose folds aid these snakes in holding slippery, mucus-covered fish while
the snake maneuvers them into position for swallowing. Their maxillary teeth
are similar in size; all tend to be long, and are fluted on the sides and posterior
surfaces, a condition found in many fish-eating snakes. File snakes usually have more than 100 teeth when they
are counted on all the bones that carry them. Their thick bodies, slow
movements, and complete reluctance to leave the water make file snakes unusual.
The Little File Snake (Acrochordus granulatus) is the most marine of the three
species and has been found at sea, 15–20 km offshore. It has the highest blood
volume of any snake (13% of its body, most snakes are in the 5–6% range), and
the largest proportion of red blood cell of any snake (50%, most snakes are in
the 25–30% range). Not surprisingly, it has the largest oxygen-carrying
capacity of any snake. Underwater the file snake’s heart beat is slow but, in
anticipation of taking a breath as the snake surfaces, the heartbeat increases
so that more oxygen can be taken up by the blood flowing through the lungs.
File snakes and other aquatic snakes can also exchange gases through their skin,
increasing their dive time. Freshwater file snakes do not have the unusually
high blood volume or the oxygen-carrying capacity found in the marine species.
Three
file snake species range from coastal Mumbai, India eastward to Australia and the
Solomon Islands and southward into the Indonesian Archipelago. But fossil file
snakes dating to the the Miocene or early Pliocene, and found in Pakistan,
India, and Nepal suggest the family had a wider distribution and a larger body
size than they do today. Like all marine snakes, the file snakes probably
evolved first in freshwater and transitioned to saltwater later in their
evolution.
The
little file snake rarely reaches one meter in length; the mostly freshwater,
Australasian, Arafura File Snake (A. arafurae) may slightly exceed 2 m; and the
mostly freshwater [Figure 11–3] Southeast Asian Elephant Trunk Snake (A.
javanicus) may reach 2.9 m, although this size record is old and may be an
error, most large specimens reach about 2 m.
INSERT
FIGURE 11-3.
Figure 11–3. The Arafura File Snake
(Acrochordus arafurae) photographed near Darwin Australia.
My
experience with file snakes is limited. Despite months of field work on aquatic
snakes in Thailand, I have only seen the elephant trunk snake in markets.
However, Grant Husband at the Northern Territory Wildlife Park took me to a
stream outside Darwin in Australia’s Northern Territory to demonstrate how to
catch a file snake. The method consisted of walking the edge of a stream after
dark with a flashlight and looking for snake snouts to locate the position of
the snake. As the snake withdraws into the murky water, you plunge your hand
and arm into the water and attempt to grab the snake. File snakes are
relatively slow, and they depend on the dark water and holes in the stream bank
to avoid capture.
Ecological
studies on the Arafura File Snake suggest that it may not have a specific home
range; instead, they wander through the murky water. Some individual file
snakes stay at one location for a day or more, while others may move almost a
kilometer. The freshwater Arafura file snake lives in a seasonally wet climate,
and their wetland habitat expands and contracts with the rains as they follow
the water. During the dry season, populations may be highly concentrated in
small areas, a situation that offers opportunity for mating. Multiple males
compete for females in these situations and it seems likely that sperm
competition is present in this species, as it is in most snakes. With the rains,
the area covered by water expands and the snakes disperse to distant locations,
lowering the density of the snakes. Like all animals file snakes are greatly
impacted by climatic events, and Thomas Madsen and Richard Shine found high
rainfall late in the wet season resulted in abundant fish populations and fat
file snakes the following year.
Like
many aquatic snakes, file snakes laterally compress their body when swimming. This
produces a keel on their belly that increases the body’s surface area and makes
the snake a more efficient swimmer.
Questions
about file snake relationships were largely unresolved until DNA sequencing and
genetic comparisons became possible. While some authors hypothesized file
snakes were related to boas and pythons, others considered them colubrids, but
DNA sequences suggest that file snakes are the sister species to all of the
advanced snakes, the Caenophidia, and last shared an ancestor with them about
90.7 MYA. File snakes are not the only snake lineage adapted to a variety of
water salinities, the homalopsids span the range of freshwater to full sea
water.
Homalopsids
Today
Lake Songkhla is a large freshwater ecosystem in southern Thailand, but 150
years ago, however, it was a large bay separated from the Gulf of Thailand by
barrier islands. The openings between
the barrier islands became blocked and, as freshwater begins to drain into the
basin, the salt content of the water decreased, leaving a diverse fauna.
Freshwater, brackish water, and salt water fishes co-exist in the lake. The
aquatic snake fauna is also interesting: Little File Snakes, Pipe Snakes,
Brook’s Sea Snake, Checkered Keelbacks, and five species of homalopsids feed
and reproduce here. But one species numerically dominates the Songkhla system―
the Rainbow Mud Snake (Enhydris enhydris)
We
used baited funnel traps to collect snakes and we would find the occasional
Asian Pipe Snake (Cylindrophis ruffus), Puff -faced Water Snake (Homalopsis
bucatta), Plumbeous Mud Snake (Enhydris plumbea), or Checkered Keelback
(Xenochrophis flavipunctatus) in the traps. During the 1997 field season (13
days using 51 traps), we trapped 380 Rainbow Mud Snakes, and recaptured 144.
Preliminary results suggested 406 to 567 Enhydris enhydris lived on the study
site. Because this snake uses edge habitat, as opposed to open water, we
calculated its density at one snake per 2 meters of shoreline. In spite of the
fact that several of us worked the study site day and night over four field
seasons, only once did we ever actually see a live snake that was not in a trap
or in a ditch being drained by fishers. Despite its abundance, the Rainbow Mud
Snake is difficult to observe in the field. Muddy water is the reason.
Homalopsid
snakes like shallow, muddy water. Several other aquatic ecosystems in Thailand
were sampled and we found the same pattern: 3 to 5 species of homalopsid snakes
were present, but one species always dominated the assemblage, the Rainbow Mud
Snake. We know the E. enhydris occasionally leaves the water because of road
kills. We also know it may colonize urbanized areas by using drainages ditches
and drainage pipes when they are carrying water. Large shallow lakes, like
Songkhla, however, produce dense populations of this snake. Enhydris enhydris dominates
Lake Kabinburi in southeastern Thailand and the Great Lake of Cambodia, Tonlé
Sap. All of these ecosystems have one commonality― they are all modified by
human activity.
The
Rainbow Mud Snake has a small head and a large, bulky posterior body, and it is
successful in part because it feeds on small fish. Humans have over-fished the
large, shallow lakes of Southeast Asia, reducing the number of large predatory
fish that would feed on snakes and smaller fish. With predators reduced and
food supply increased, the Rainbow Mud Snake’s populations have exploded. This
is most likely the result of the phenomenon biologists call mesopredator
release. When large predators are removed from an ecosystem, the medium-sized
and small-sized predators increase in abundance, hence meso (=middle-sized)
predator release. Humans have also increased the Rainbow Mud Snake’s habitat
with flooded paddy fields, shallow roadside ditches, lotus ponds, and other
landscape water features that are so desirable in Southeast Asia.
A
small, black-to-olive colored homalopsid, the Plumbeous Mud Snake (Enhydris
plumbea), is more terrestrial than the Rainbow Mud Snake. It lives in the
mud-root tangle, and it was studied by Harold Voris
and Daryl Karns in a wet pasture in
Sabah on the island of Borneo. Snakes were collected by hand around the edges
of buffalo wallows by pulling up grass mats at the edge of the wallow to expose
the snakes. The Plumbeous Mud Snake hunts frogs, tadpoles, and fish in the
security of the tangled grass roots, away from most predators.
Looking at museum specimens of homalopsids,
it became clear that the snake labeled Enhydris jagorii in most collections were,
in fact, composed of three different species. However, it was not until I
examined the type specimen of Hypsirhina jagorii described by Wilhelm Peters in
1863 that I knew which species was the real Jagor’s Mud Snake. Peters had given
the location of the type specimen as “Siam” and most of the specimens labeled
jagorii were from Thailand (formerly Siam). All three species had 21 scale rows
at mid body and a similar arrangement of scales on their head, but they had
distinctly different color patterns, body proportions, and ventral scale
counts. The most common of the three species labeled jagorii turned out to be
widespread in the Mekong River drainage. It had been previously described as a
subspecies of Rainbow Mud Snake, so it had a name― subtaeniata. One of the
other species labeled as jagorii did not have a name, and all of the 12
specimens lacked locality data or said “Thailand” or “Bangkok.” Harold Voris
and I named this snake after our friend and colleague Tanya Cha’nard of the
Thailand Natural History Museum. Despite efforts to find an extant population
of this snake, we have not. All existing specimens were collected in the first
part of the 20th century. Is it possible that the snake that lived in the
Bangkok area may now be extinct? Unlikely. A recent photograph published in a
field guide labeled Enhydris jagorii was in fact Enhydris chanardi.
We were also interested in locating the
real Jagor’s Mud Snake. Prior to our fieldwork, I had seen only nine museum specimens,
all of them collected between 1860 and 1980, and, again, all of them with
locality data suggested it lived in the Bangkok metropolitan area. Trapping in
the canals, rice fields, and roadside ditches in and around Bangkok did not
produce any specimens. Our efforts went un-rewarded until the summer of 2007
when Daryl Karns and I trapped snakes at several locations in Thailand’s
Central Plain. During a wetland reconnaissance trip near the city of Uttaradit,
we wandered into a small village, Bung Ka Lo. Some fishers lived along the road
bordering the wetland, and we talked with them with the help of our driver and
translator, Pon. It became obvious they were familiar with homalopsid snakes
and were willing to collect them for us for a small sum per snake. The snakes
frequently became entangled in their gill nets and the fishers considered them
an annoyance. Daryl, Pon, and I had worked with many Thai fishers, but these
people were exceedingly friendly, and some of them had no previous contact with
westerners. By the time we left the first meeting, we had consumed the better
part of a bottle of homemade whiskey and made some important field contacts.
Since we were working on their time, it was going to be several days before we
could get snakes; the villigers were celebrating a recent election and there
was a weekend festival of food and kickboxing. When we arrived Monday morning they
had several metal containers and bags full of snakes, including several Jagor’s
Mud Snakes. In three days of working at Bung Ka Lo, we bought 262 snakes
representing five species, including 26 E. jagorii.
Of the recognized homalopsid species, one
is totally aquatic and reluctant to leave the water, the Tentacled Snake
(Erpeton tentaculatus). Tentacled snakes are perhaps the most specialized
aquatic snakes, possibly more specialized than the true sea snakes. They have
two fleshy projections on their snout; very small ventral scales, strongly
keeled dorsal scales, a long, prehensile tail, and unexpectedly large eyes for
a homalopsid [Figure 11–4]. Picking one up will cause the snake to make its
body exceptionally rigid and stick-like. It wraps its tail around the
vegetation in turbid water with submergent plants and hangs in the water
column. Typical hunting posture involves turning its head and neck back toward
the body in a J-shape position. Rough, keeled scales provide a surface for the
growth of algae and other protists, adding to the camouflage that makes this
snake nearly impossible to see. In an aquarium stocked with floating hyacinths
and small Fighting Fish (Betta splendens), the snake remained motionless while
the fish graze the algal growth on its body. In 1999, Harold Voris and I
obtained a freshly caught Erpeton from Thai fishermen and videotaped its hunting
behavior. When reviewing the tape, we found the fish often disappeared with the
strike. It was filmed at 30 frames per second and the fish frequently disappeared
within one frame. INSERT FIGURE 11-4.
Figure 11–4. Views of the Tentacled Snake (Erpeton
tentaculatus) using a scanning electron microscope. A: The head showing the
eyes, nostrils, and tentacles. B: A single tentacle shows the forward facing
scales. C: A single scale on the tentacle with striations but no pits, hair
cells, ampullary organs or projections. Courtsey of Ken C. Catania.
Observers of the Tentacled Snake have
disagreed on the function of the tentacles; some hypothesized they are sensory
while others claim they are used for camouflage, breaking up the outline of the
head. Close examination shows that the tentacles are covered with scales and
that the anterior edge of the scale is free. The tentacles are also
exceptionally flaccid and retractable.
Fish have a rapid-escape response called
the C-start, a response that allows the fish to move left or right depending on
the direction of the moving water stimulus. The water disturbance triggers the
firing of the ipsilateral neuron, which, in turn, excites lateral motor neurons,
causing the fish to turn away from a predator. Kenneth Catania discovered the
Tentacled Snake exploit this escape reflex for capturing fish. About 1–3
milliseconds (ms) before initiating the strike, the snake creates a feint by
muscle movements that start at the head and travel down the forebody in
sequence; 5–12 ms later, the fish responds with a C-start. The snake’s subtle
movement startles the fish, enabling the C-start response. More remarkably, the
snake then predicts what the fish will do and directs the strike (before the
fish responds with the C-start) not toward the head of the fish, but where the
snake anticipates the fish to be when its open mouth arrives at the end of the
strike. Erpeton is exploiting the fish’s escape response (the Mauthner-mediated
escape response) to its own advantage and it raises the question: is the
individual snake learning this behavior? [Figure 11–5].
After two centuries of speculation about
how the tentacles function, Cantania and colleagues investigated further using
staining techniques that allowed them to view the branches of the trigeminal
nerve present in the tentacles. These nerves lie very near the tentacles’ surface.
The researchers used von Frey hairs (small filaments of nylon of varying
diameters used to test detection thresholds) on the tentacles and determined
they were extremely sensitive, detecting forces as low as 0.008 grams. The
labial scales (scales on the edge of the mouth) were much less sensitive. They
also tested responses of the trigeminal ganglion and the sensitivity of the
brain’s optic tectum. The results showed a close association between the
tactile sense of the tentacles and the visual input from the eyes, suggesting a
high level of integration between the two. When Cantania and colleagues placed
fish outside of the aquarium where the snakes could not obtain any mechanical
information, they oriented toward the prey; when shown a cartoon of a moving
fish they struck at it, suggesting they can rely on visual information alone to
hunt. This is not surprising. Most homalopsid snakes have very small, dorsally
oriented eyes. The Tentacled snake is an exception; they have large eyes that
are positioned laterally.
Cantania and co-authors compare the
sensory systems of the Tentacled Snake to that of the Barn Owl (Tyto alba).
Both have excellent vision, but when light is low or absent they can continue
to hunt effectively. The Tentacled Snake uses vibrations in the water and the
Barn Owl using sound cues. Erpeton can hunt day or night; it can hunt in clear
water or in water heavily laden with sediment. Given that it lives in the
drainage systems that carry water and sediments from the Himalayas, this snake
is highly adapted for its environment.
Mike Alfaro and colleagues suggested that
the Tentacled Snake and Bocourt's Mud Snake (Enhydris bocourti) shared an ancestor
about 14.1 (9.3–18.8) MYA. Both snakes share similar lowland, shallow water
habitats in the Indochinese peninsula, but have very different morphology and
life styles.
INSERT
FIGURE 11-5.
Figure 11–5. The Tentacled Snake’s strike
and the fish’s response when the fish is parallel to the snake’s jaws. (A)
Schematic of snakes position and the events during the strike. Numbers 1–3 show
body movements prior to striking, arrows show the direction of the feint. (B)
Frames from high speed video. (C)
Hydrophone recordings of strike showing pressure change (1–3) associated
with feint, Y-axis units arbitrary, numbers show events illustrated in A. Note
that latency to C-start is appropriate for body feint (7 milliseconds) but not
for strike (4 milliseconds). (D) Percent turns toward head during the strike.
(E) The long axis of the fish intersected line segment P. Courtesy of Kenneth
Catania, Vanderbilt University.
Many
homalopsids feed exclusively on fish, a few feed on fish and frogs, and some
are specialist for feeding on crustaceans; many are poorly studied, however,
and their diets remain subjects for future investigations. What is known about
homalopsid diets is that they take small prey, prey that is almost always less
than 1% of their body weight, and they eat multiple prey in a single feeding
session. Warm water allows them to do this. Small prey are more abundant than
large prey and small prey has a high surface-to-volume ratio, making digested
rapid. Therefore, these snakes can eat virtually around-the-clock. This is in
stark contrast to boas, pythons, and vipers infrequently taking a single, large
prey.
Swallowing
whole crustaceans can be a challenge. Crustaceans have an exoskeleton of
chitin, a complex carbohydrate that is impossible for most vertebrates to
digest. To make things even more complicated, crustaceans also often have
powerful pincers and live in submerged burrows. The Crab-eating Snake (Fordonia
leucobalia) has long been known to have a diet composed exclusively of
crustaceans. Fordonia takes crabs and Mud Lobsters and, while it often eats
small prey that can be swallowed with the strike, it will eat larger crabs,
dismembering them for easy swallowing. Crab-eaters have robust fangs for
cracking through the exoskeleton and, while their venom has yet to be studied,
it may contain the enzyme chitinase for the digestion of the chitin. Crab-eaters are widespread in coastal
habitats from Mumbai, India to Queensland Australia, a distribution almost
identical to that of the mud lobster.
Two
other homalopsids were found to eat crustaceans during our study. Gerard’s Mud
Snake (Gerarda prevostiana) is a down-sized version of the Crab-eating Snake
and its sister species. Its distribution is not as well known as the Crab-eater,
but it appears to occur in coastal habitats from Mumbai, India to the
Philippines; and it, too, seems to be associated with the Mud Lobster. Edward
Taylor collected a dozen or so specimens in a Thai mangrove forest and, when I
examined them to see what they were eating, they contained only the remains of
crabs. Bruce Jayne and colleagues studied this snake in Singapore and were
interested in seeing how it handled the crabs. Captive snakes were offered a
variety of species but showed no interesting in eating. Their appetite changed when
they were given crabs that had just molted their exoskeleton. The snake seized
the crab with its mouth, looped its body around the prey, and pulled the crab
through the loop, tearing it into pieces. To date, this is the only species of
snake known to tear its food into pieces. (As mentioned, its sister species,
the crab-eating snake, does appear to chew the legs off larger crabs). The advantage
to ripping crabs apart is the ability to swallow large prey that could
otherwise not be consumed.
Cantor’s
Mud Snake (Cantoria violacea) also proved to be feeding on crustaceans, but we
did not find crabs or mud lobsters in them. A mangrove and mudflat-dwelling
species, Cantor’s Mud Snake is known from relatively few specimens. At first
sight its rounded head, elongated body, and banded pattern suggested it may be
a true sea snake in the genus Hydrophis. But it lacks a paddle tail and the
front fangs found in elapids, and molecular studies place the species in the
same clade with the other crustacean-eating homalopsids. Harold Voris and I
have found only small snapping shrimp (Alpheus) in their digestive systems. Snapping
shrimp inhabit the intertidal burrow system, and use their enlarged claw to
produce a snapping sound by compressing a gas bubble that forms in the pincer.
It seems possible that this snake may locate snapping shrimp by their odor, by
the vibrations of the collapsing bubble, or the light generated by the
pressurized gases in collapsing bubbles.
Thirty-seven
species of homalopsids inhabit the tropic and subtropical world from the Indus
River Valley of Pakistan eastward to the Philippines and southward into India,
Indochina, Indonesia, New Guinea, and northern Australia. Most species occur in
the Indo-Chinese peninsula, Thailand, the Malaysian Peninsula, and the adjacent
Sunda Shelf islands. They are absent from the fossil record, though various
studies estimate the origin of the family between 65 and 22 MYA using the DNA
clock.
Natricids
The
shallow, clear water at the edge of a flooded limestone quarry in the Chicago suburbs
revealed a foraging Queen Snakes (Regina septemvittata). I observed the
Northern Water Snake (Nerodia sipedon) catching fish across the quarry. Just a
few meters from the shoreline, in wet grassy habitat shaded by trees, an Eastern
Garter Snakes (Thamnophis sirtalis) was hunting for earthworms and frogs. The
small, ground-dwelling Dekay’s Snake (Storeria dekayi) were abundant beneath limestone
slabs, boards, and tar paper around the quarry where they feed on slugs and
worms.
All
of these North American natricid species shared an ancestor that emigrated from
Eurasia some time prior to the early Miocene (~19–18 MYA). We know this because
the earliest known Western Hemisphere natricid fossils date to the early
Miocene, and we know they shared an ancestor because of shared anatomy and DNA.
Michael
Alfaro and Steve Arnold compared three genes from many of the North American
natricid snakes and found not only that they shared a distant ancestor, but
that they formed three distinct clades: a water snake clade, a garter snake
clade, and a novel semi-fossorial clade. Living around the suburban quarry were
members of each of the three clades. Alfaro and Arnold’s work suggested that
the most basal Western Hemisphere natricid is the small, fossorial Kirtland’s Snake
(Clonophis kirtlandi) [Figure11–6a]. While Kirtland’s Snake is not known from
the area around the quarry, there is a population within 10 miles. Both the Kirtland’s
Snake [Figure 11–6b] and its sister, Dekay’s Snake, occur in wet prairie or
grassland habitats. But Kirtland’s Snake is of particular interest because it
is mostly fossorial, appears to use burrows of the chimney building crayfish as
a hibernation site (suggesting it hibernates underwater or at least in the
water), and its isolated populations are widely scattered over Illinois,
Indiana, Ohio, and bordering states.
North
American natricids are perhaps the best known serpents. Garter snakes, water
snakes, and brown snakes are often abundant in urban areas with remnant
habitats. Natricids have adapted to aquatic habitats numerous times and then
reverted to a life on land, only to return to the water. At least a few garter
snakes are completely terrestrial, but many hunt along streams or in ponds, and
others are almost totally aquatic.
Jean-Claude
Rage proposed that natricids and colubrids invaded North America from Europe
via a land-bridge. Since the oldest natricid fossils are from the early Miocene,
the migration and colonization of the land-bridge must have occurred prior to
this date. An early Eocene land-bridge connecting Europe-Greenland-North
America with a subtropical climate may explain the expansion of these snakes into
the Western Hemisphere. But how probable is it that snakes used a high latitude
land-bridge to disperse from Europe through Greenland and into continental
North America in a mild or even cold climate?
A
snake den in an abandoned railroad yard in Portage County, Wisconsin provided a
valuable clue. A friend had discovered the snake den near his summer house and
took several of us for a tour. The circular cement foundation was mostly
covered with rusted metal; it had been used as a giant turntable to switch
railroad cars from one track to another, the cement cistern was about 2.4 m
deep and partially filled with water. Shade from the metal covering had insulated
the layer of ice and kept it from melting, but the ice cover was completely solid
and transparent. Eastern Garter Snakes (Thamnophis sirtalis) [Figure 11–6d] and
Western Fox Snakes (Pantherophis vulpinus) were submerged in water beneath the
ice with their posterior bodies wrapped around debris. The snakes had been in
the water since the previous fall; this was early May. With a solid ice cover
in place since January or earlier, the snakes had not filled their lungs with
air for at least five months.
Experiments
done by Jon Castanzo comparing submerged and non-submerged garter snakes from
this Wisconsin den later found submerged snakes in total darkness at 5º C.
These snakes had their oxygen consumption reduced 54% and heart rate reduced
77% over experimental snakes hibernating in air under the same conditions.
While hibernating underwater, the snakes were living in acidic (5.5–6.5 pH),
hypoxic (dissolved oxygen was 2.9 ppm) ground water. And yet, the snakes were
carrying out aerobic respiration, using oxygen that diffused through their skin
from the water for five months, a remarkable ability, but one that could have
been anticipated. Charles Carpenter studied garter snakes in Michigan in the early
1950’s and observed five Eastern Garter Snakes hibernating in the burrow of a
crayfish. He wrote,
…many snakes hibernate completely
submerged in water in underground tunnels. It seems that this should be
possible provided the water is very cold.
Costanzo’s experiments and the
significance of snakes being able to spend months submerged in cold water have
been long overlooked.
The
ability of natricids to survive submerged under ice for months at a time is not
only valuable for surviving long Midwestern winters, but it could explain how
snakes dispersed from Eurasia to North America by colonizing high latitude land
bridges. Even if the land bridges had a seasonally cold climate, these snakes
could have made the trip. Fox snakes were also under the ice and the literature
reports Blue Racers and Black Ratsnakes can be at least partially submerged
during hibernation. The Massasaugua is well known for using crayfish burrows as
hibernacula, so it too can most likely used submerged hibernation. Vipers and
colubrids, families composed primarily of terrestrial and arboreal species,
also dispersed from Eurasia to North America prior to the early Miocene.
Submerged hibernation may have also have been involved in their dispersal.
More
than 100 species of natricids use aquatic environments to varying degrees, and
most feed on aquatic animals. Joke Bilcke and colleagues compared feeding
behavior in natricids believed to be dietary generalists and specialists. The
generalists were thought to forage for food by open-mouth searching, holding
their mouth open and sweeping it through the water until they made contact with
prey. These species tend to strike slowly to the side, perpendicular to the
long axis of the body, and do not seem to depend upon vision. Specialists were
thought to hunt from ambush, be visually alerted by the presence of prey, and
strike forward, parallel to the long axis of their body. However, Bilcke and
colleagues also looked for a correlation between prey density and strike
behavior. Two European natricids’ (Natrix tesselata and Natrix maura) were compared
to the North American Banded Water Snake (Nerodia fasciata), and they found prey-capture
strategies in natricid snakes were not correlated with diet but with prey
density. Snakes feeding on fish in a school or concentrated in shallow water
use the open mouth technique, while snakes feeding on fish in low density
strike from ambush.
Toby
Hibbits and Lee Fitzgerald noted that the narrow-headed garter snake
(Thamnophis rufipunctatus) [Figure 11–6c] and Harter’s water snake (Nerodia
harteri) have narrow heads and an elongated snout. Both snakes live in
fast-moving water. The authors hypothesized that narrow-heads are more hydrodynamic
when striking underwater in a swift current. They also posited a narrow snout
increases binocular vision, allowing the snake to better judge the distance of
the prey. Hibbits and Fitzgerald measured heads and calculated proportions for
a variety of natricid species and found the two stream-dwellers had better
binocular vision and experience less drag during a forward strike. Because
these two snakes are in different clades, the similarity of head shape is
considered the result of convergence.
INSERT
FIGURE 11-6.
Figure 11–6. Representative North American
natricid snakes. A. Kirtland’s Snake (Clonophis kirtlandi). B. Dekay’s Snake (Storeria
dekayi). C. Narrow-headed Garter Snake (Thamnophis rufipunctatus). D. Eastern
Garter Snake (Thamnophis sirtalis) feeding on a Leopard Frog (Lithobates
pipiens). E. Northern Water Snake (Nerodia sipedon) feeding on a hybrid sunfish
(Lepomis). F. Salt-marsh Snake (Nerodia compressicauda).
Dipsidids
The
South American snakes of the genus Helicops are ecologically and
morphologically similar to the North American natricids but they are in a
different lineage, the dipsidids. There are 15 species of Helicops with dorsal
eyes, dorsal nostrils, and rear fangs. Compared to the North American
watersnakes, the dipsidids are poorly studied but of interest because some
species are live-bearing while others lay eggs, and one species (H. angulatus)
appears to have populations that do both. Rob son
W. Àvila and colleagues examined more than 400 specimens of the spotted
watersnake (Helicops leopardinus) from the Pantanal of central Brazil. The two
most common prey items were knife fishes (Gymnotiformes) and treefrogs
(Hylidae). This snake inhabits floating vegetation where they live in close
contact with their prey and Àvila and colleagues suggest it actively forages
for prey.
Another
poorly known aquatic group is the genus Hydrops; closely related to Helicops,
Hydrops is widely distributed in the Amazon basin. They have small dorsal eyes
and narrow ventral scales and are found in many aquatic habitats where they
feed on fish including synbranchid eels. Perhaps the most interesting aquatic
dipsidids, however, are the snakes in the genus Tretanorhinus, locally known as
the Catívo in Cuba. Four species are
known from Ecuador, Central America, Cuba, and the Bahamas. The long head,
square muzzle and long tail suggest this snake may be convergent with the
Tentacled Snake (Erpeton tentaculatus) from Southeast Asia. Few herpetologists
have examined these snakes since Wilfred Neil observed them in Cuba in 1949 and
reported them hunting in shallow water and to be nocturnal and highly aquatic. They
move very slowly and use freshwater and well as brackish, and possibly full sea
water as well. Neill observed them snapping at small fish in shallow pools
stating that they were quite successful in capturing their prey.
Aquatic Elapids
American
coral snakes are well known for their highly potent venom, contrasting patterns
of red, black, and white or yellow rings. About 75 coral snake species are
known for their leaf litter, crevice-dwelling, and burrowing habits. One species
group, the triad coral snakes, has a pattern of rings arranged in groups of
three, short parietal scales that are usually black, and very short tails.
Triad corals are mostly Amazonian species and they are of particular interest
because at least seven of the 20 species have habitat descriptions that include
some mention of aquatic environments. One species, the Aquatic Coral Snake
(Micrurus surinamensis), appears to spend much of its time in the water, but it
has also been found above ground in vegetation. Its eyes and nostrils are
located on top of the head, and its venom is particularly effective at killing
knifefish. The Aquatic Coral Snake is the most basal species of the triad
group, suggesting the ancestor of the triad coral snake group may, too, have
been aquatic. The South American coral snakes (M. lemniscatus species complex)
are also semi-aquatic or aquatic depending on the definition, and are known to
feed on synbranchid eels and shallow water fish. When I collected this snake on
Trinidad it was often near water, though I never had the opportunity to observe
it in water.
The
kraits (genus Bungarus) of Southeast Asia also tend to be ground-dwelling, leaf
litter snakes. They will hunt in streams and ponds as well as along the ocean’s
shoreline, and they do not hesitate to enter the water. We have seen them in
fishermen’s gill nets, and they will eat homalopsid snakes but their aquatic
habitats are not well known. Shou-Hsian Mao found the Taiwan banned krait
(Bungarus multicinctus) to feed on fish, and the semi-aquatic plumbeous mud
snake (Enhydris plumbea). Kraits are in a different lineage of elapids than are
the coral snakes and they also show aquatic tendencies.
Much
has been written about Lake Tanganyika, the African Great Lake. Perhaps it is
most well known for the two British explorers, Richard Burton and John Speke,
who discovered the Lake in 1858. Or perhaps its fame comes from its size, as
the second deepest freshwater lake (~ 500 m), and the third largest in volume on
the planet. A species swarm of more than 250 cichlid fish has made this lake
famous among biologists and fish hobbyists, because the fish are a well-studied
example of rapid evolution and popular in the pet trade. But there is a fish
predator living here that is also of interest, Boulenger’s Water Cobra (Naja
annulata).
Arthur
Loveridge, a Harvard University herpetologist, was one of the first to make
this snake known. At Kasanga, rocky promontories extend into the lake, and one
was built by the Germans for their Bismarckburg military base. These peninsulas
are protected by a natural breakwater of jumbled rocks and it is here Loveridge
observed the aquatic cobras. He wrote,
According to native reports, which my own
experience confirmed in some points and contradicted in none, when the sun
rises and strikes the rocks the cobras emerge from their retreats beneath them
and bask for a short time on the tops of the rocks. Shortly afterward, ―and I
found none on the rocks an hour and a half after sun up―they take to the water
in search of fish. I was told on a calm day one might see as many as ten in the
course of a morning’s fishing. We saw four in a little over three hours.
The snakes come out of the water in the
evening and they are said to bask under the rocks. Loveridge suggested that
this is probably correct because the evenings were cool and the snakes may
absorb heat from the rocks and avoid the cool wind blowing in mid-May.
Boulenger’s
Water Cobra [Figure 11–7] is usually banded with strongly contrasting
black-brown bands separated by yellow, but individuals vary and they may have a
mostly grey-brown or yellow-brown dorsum.
They are quite large, reaching a size of 2.7 m, and the species is
distributed across central Africa, from the Cameroons to Tanganyika, where it
is often associated with flooded forest. It can dive to at least 8 m, stay
submerged for 10 minutes or more, and this species may hunt in co-operative
groups. When not looking for food, it uses rocks, bank holes, tree holes, and
root clusters for refuge. Human encounters with water cobras are probably few,
and the snake poses little danger to anyone except when it becomes entangled in
fishermen’s nets or in the nets of herpetologists trying to trap it. Kate
Jackson described a harrowing experience of trying to remove a large specimen
from a gill net.
INSERT
FIGURE 11-7.
Figure 11–7. The Water Cobra, Naja
annulata from Brazzaville, in northern Congo. Photo by Kate Jackson.
The
water cobra is morphologically distinct from the common cobras and was placed
in the genus Boulengerina, named after George Boulenger of the British Museum
of Natural History. However, Wolfgang Wüster and colleagues’ molecular study
found that the water cobra was, in fact, a part of the common cobra clade, and the
researchers proposed that the aquatic cobra be placed in Naja. I follow that
arrangement here. DNA suggests that the water cobra’s sister species is the
Forest Cobra (Naja melanoleuca), a large species that shares a similar
geographic distribution with Boulenger’s Water Cobra. The Forest Cobra shares
aquatic foraging behavior as well as a diet that includes fish with the aquatic
cobras.
A
second, poorly known species of water cobra inhabits the lower reaches of the
Zaire River, Boulengerina christyi. A DNA sample of this snake was not included
in the study done by Wüster and co-workers, and it is unclear where this
species falls phylogenetically. Karl P. Schmidt erected a new genus, Limnonaja,
for it in 1923 because he considered it morphologically distant from N. annulata.
Sea
kraits are widespread in the Indian and Pacific Oceans. The eight sea krait species
represent an interesting evolutionary experiment in the terrestrial – marine
transition. They may be viewed as a terrestrial snake’s incomplete attempt to
invade the oceans, or they may be viewed as the fulfiment of a highly
specialized niche, one that uses a unique microhabitat and lifestyle. Females tend
to be larger than males and lay eggs in rock cavities, presumably above the
high tide mark. The body size difference is also reflected in diet. Large
females tend to feed in deeper water on members of the conger eel family
(Congridae), while males hunt in shallow water and feed on moray eels (Family
Muraenidae). Sexual dimorphism in sea krait feeding behavior may allow larger
populations to exist than would otherwise be possible because the sexes are not
competing for food.
The
freshwater Rennell’s Island Sea Krait (Laticauda crockeri) has already been mentioned
in (Chapter 10). There is some evidence that of the other seven species some
show habitat differences. Xavier Bonnet and colleagues examined microhabitats
in New Caledonia and found St Girons’Sea Krait (L. saintgironsi) used a variety
of terrestrial refuges including puffin burrows, tree root cavities, logs, and
buildings. However, the Brown-lipped Sea Krait (Laticauda laticauda) was found
only under beach rocks.
Harvey
Lillywhite and colleagues discovered sea kraits require freshwater. Prior to
this study, sea snakes, including Laticauda, were thought to regulate their salt/water
balance with salt glands located under the tongue. Standing on the deck of a wrecked
ship off the coast of Papua, New Guinea in 1975, Lillywhite observed 100 or
more emaciated-looking sea kraits stretched out on the ship’s deck. At the time,
he thought it unusual that they could not find enough food. Now he has decided
that hunger was not their problem. He wrote,
Although surrounded by the vast waters of
the Pacific Ocean, they were most likely severely dehydrated. They might even
have been early harbingers of climate change.
Lillywhite
and colleagues investigated the drinking habits and dehydration problems in
three species of sea kraits. They found dehydrated snakes refused to drink sea
water, but would drink freshwater or slightly brackish water. Furthermore, they
found a correlation between the sea kraits’ distribution and locations where
freshwater was available. A look at the distribution of all sea snakes revealed
that there is greater species diversity in areas with high annual precipitation.
Their need for freshwater may explain why the distribution of many sea snakes
is so patchy. Freshwater is available to
sea snakes from two sources: streams and rivers draining into the ocean, and
the lenses of low density freshwater that tend to stit on top of the more dense
saltwater before they mix. The distribution of Laticauda coincides with low
salinity surface water over most of its distribution. Sea kraits might be
expected to rely on freshwater since they spend considerable time on land, but
what about the true sea snakes, the hydrophiines? Lillywhite suspects they, too,
may need freshwater. The most extreme sea snake is the Yellow-bellied Sea Snake
(Pelamis platura) because it is pelagic. In the lab, it will drink freshwater
and dehydrates rapidly when it is fasting in salt water and not obtaining
metabolic water from its food. Living in the ocean is physiologically
comparable to living in the desert, there is a shortage of freshwater in both
habitats.
The
true sea snakes of the sub-family Hydrophiinae compose about 60 species of
poorly studied marine snakes with paddle tails and front fangs. While more
scientists have been examining specimens and diving with snakes to observe
their behavior in the last few decades, there is still much to learn. These are
the only living snakes to have successfully colonized the oceans, but, of these
species, most are restricted to the waters of the continental shelf near
sources of freshwater. All of the species studied to date are live-bearing and
females produce relatively small litters, usually with less than 17 young and
often as few as one to three young.
Megan
Kerford and colleagues studied the movements of the Bar-bellied Sea Snake
(Hydrophis elegans) at Shark Bay in Western Australia. Bar-bellied Sea Snakes
are specialist predators on snake eels (Family Ophichthidae) that live in
burrows on open sand flats. During high tides, Tiger Sharks have access to most
of the areas of Shark Bay, and Keford and co-workers discovered H. elegans move
into adjacent sea grass beds at high tide. The dense grass cover provides few
opportunities to forage on eels, but does provide cover for the snakes to avoid
sharks.
Photoreceptors
are usually associated with the head of vertebrates, but Kenneth Zimmerman and Harold Heatwole found photoreceptors on the tail of
the Olive Sea Snake (Aipysurus laevis). They observed the Olive Sea Snake’s
tail was more often concealed during the day than at night, and that the tail
will be pulled out of the light when it is exposed. By masking parts of the
tail with tape so they could not be stimulated by light, they determined the
photoreceptors were located mostly on the dorsal portion of the tail. The
nature of the photoreceptors was not determined but the snake’s behavior
revealed their presence.
Only
one sea snake has become truly pelagic, drifting with open ocean currents, the
Yellow-bellied Sea Snake (Pelamis platura).
This is not to say that it does not occur over the continental shelf,
because it occasionally gets washed up on beaches from Africa’s east coast to
the coastlines of western North and Central America. The Yellow-bellied Sea Snake
aggregates along slicks or drift lines. Floating debris accumulates in the
slicks, and it may remain for days or weeks before a change in wind speed or
current direction breaks them up. Aggregations of snakes in these drifts numbered
from five to several thousands, and are composed of juvenile and adult snakes.
Other animals inhabiting the drifts are jellyfish medusa, fish, porpoises, and
sea turtles, with sea birds often following the lines of floating debris. Snakes
aggregated here because the slicks are a useful place to locate food and mates.
The degree to which these snakes have adapted to the marine environment is
significant given they represent a recent evolutionary radiation.
Ancient Aquatic Snakes of the Eocene
The
Eocene started 55.8 MYA and ended 33.9 MYA. During this time, the continents
were drifting toward their present position. It is a period often described as
a “greenhouse,” with global warming attributed to an increase in atmospheric
carbon dioxide. The early Eocene is notable for species’ distributions now
significantly different than those we see today. There were palm trees in
Alaska and the northern Rockies, crocodiles on Ellesmer Island above the Arctic
Circle, and forests covering much of Antarctica. Primates spread from Asia to
Europe and through North America, and the rivers, estuaries, and oceans
contained snakes, large aquatic snakes.
Snakes
in the family Palaeopheidae are known exclusively from their vertebrae and ribs,
and they inhabited both hemispheres, from the Upper Cretaceous to the Eocene.
Their fossils are always associated with rocks deposited in watery
environments. The vertebrae tend to be tall and narrow, and the ribs are only
slight curved, characteristics found in the most aquatic snakes living today,
the sea snakes. Those who study Palaeopheidae fossils consider the group
relatives of the boids, but others have suggested that they are close to the
file snakes (the acrochordids). Size estimates for the paleophids range from
0.5 to 9 m or more and, while some lived in near-shore environments such as
estuaries and mangroves, others were using open ocean habitats far from shore.
Palaeophis
colossaeus was described by Jean Claude Rage in 1983 based upon some 34 mm
vertebrae collected in Mali. We don’t know how many vertebrae the snake had,
but given that a typical boa or python has about 270, it is likely this snake
could have been 9180 mm, or more than 30 feet. Another very large snake from
this family is Pterosphenus schucherti, a species described from coastal North
America from Texas to New Jersey. Remains from Florida indicate that during the
late Eocene the snake died at least 300 km from the nearest mainland where it
was buried with cartilaginous fish, bony fish, and an ancient whale.
Why
these ancient aquatic snakes disappeared near the end of the Eocene is
uncertain, though their extinction is very likely linked to cimate change. Global
cooling at the start of the Oligocene occurred as oceanic circulation was altered
with Antarctica’s disconnection from Australia and South America and led to the
formation of the South Pole’s continental ice sheet. The extinction of many
warm water species undoubtedly followed.
Aquatic
snakes and semi-aquatic snakes occur in almost all major lineages of snakes,
the exceptions appear to be the scolecophidians and the vipers. Scolecophidians
seem to be specialized for burrowing and feeding on ants and termites, making
aquatic adaptations less useful and unlikely to occur. Vipers have only one
semi-aquatic species, the Cottonmouth. The poor representation of vipers in
aquatic environments was hypothesized by Bruce Young to be due to the “…the
poor hydrodynamic profile of the 'typical' viper head.” But, this would not
preclude vipers from hunting from ambush in the water like an anaconda. Vipers
tend to have a large bulky body, but so do anacondas and many homalopsids. As
to why vipers have not invaded aquatic environments to the degree seen in other
snake lineages remains largely unexplored.
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