Chapter 10 Snakes on Islands

10. Snakes on Islands

When not foraging for food, sea kraits come ashore…, often in large numbers on small offshore islands sequestered from terrestrial predators….
Harold Heatwole et al., 2005

                The sun was just coming up over the South China Sea one Sunday morning when my two companions and I set out at low tide to walk a half-mile stretch of mud flat along Sabah’s coastline. Our destination was a pile of rocks emerging from the sea, and our plan was to search the rock pile for snakes, photograph them, and return to the main island before the tide returned. At high tide most of the rock island was covered with water, but even the highest tide did not cover the tiny island completely. We knew this because the top of the island was covered with green plants. Soon our boots were caked with mud and walking became more difficult, but thoughts of finding a sea krait, one of the most unusual snakes on the planet, kept us moving forward.
                Large boulders were strewn around the plant-topped rock pile, composing a small island habitat no more than 10 square meters. We climbed the rocks and, when our heads were even with the vegetation, we peered into the grasses and sea grape vines. Within moments, the black- and-blue bands of a sea krait were visible, and then another, and another. This highly venomous, but very gentle snake was present in good numbers on this rock; unfortunately, we did not have time to count them [Figure 10–1].

INSERT FIGURE 10-1.
Figure 10–1. The Yellow-lipped Sea Krait (Laticauda colubrina): Top: A small islet off the coast of Sabah, Malaysia. Middle: A sea krait coiled in a rock crevice. Bottom: A view of the head of Laticauda colubrina.  Sea kraits fill a unique coastal niche that involves using both terrestrial and marine microhabitats.

                We carefully lifted a large snake out of the vegetation and lowered it onto a ledge so it could be examined and photographed. On a similar islet off the coast of New Caledonia, Hubert Saint Girons found about five sea kraits per square meter.
                Sea kraits have a remarkable paddle-shaped tail for swimming, and the ability to compress their body from side to side so that the snakes turns into living oars. But they also have large ventral scales arranged in a single row along their entire belly, a characteristic of snakes that live on land. The snakes on this island had ticks, similar in appearance to those I have removed from my dogs after walking though Midwestern fields, though I knew these had to be a different species. The ticks had inserted their heads under the snakes’ scales and, attached as they were, went with the snakes as they left the island to go hunting in the sea. Sea kraits are unusual because they show a unique set of characters that adapt them to a double life. They specialize in finding and eating eels underwater, but digest their food, bask in the sun, mate, and lay their eggs on land. And, as in this case, the land is often a small offshore island. Our time on the rock pile was limited by the incoming tide, so we finished our photography session, returned the snakes to the vegetation on the top of the rock, and walked back to the mainland with the incoming tide lapping at our heels.
                The quote from Heatwole et al. suggests what we found on that small rock off the coast of Sabah was not unusual. In fact, it is difficult to find a sea krait on the actual coastline of a large island or continent, but go to offshore rocks and small islets and they are often plentiful. The reason may be small islands provide habitat secure from larger predators, as Heatwole suggests. However, safety is not the only reason snakes live on islands. In this chapter, we explore how snakes get to islands and disperse into new habitats.
                Excluding Antarctica and the Arctic islands, islands compose about 3% of the Earth’s land surface, and they support many species of vertebrates. In a survey of terrestrial vertebrates on islands, Ted Case found island snakes tend to be significantly smaller than their mainland counterparts. Exceptions included snake populations adapted to feed on sea bird chicks; these island snakes tend to be larger in size when compared to mainland populations. Dwarfs or giants, island snake populations are the result of the reduced competition, limited resources, and the available ecological niches.
                Snakes are excellent colonists. Their scale covered bodies are often resistant to water loss. They can survive with very little food; many can go months without food. Female snakes often mate with several males and store their sperm for future use. Thus, a single litter of sibling snakes is likely to have a greater diversity of genes than if they would have all had the same father. Under the right circumstances, female snakes will even produce offspring without sperm (see Chapter 2). All of these traits help snakes colonize new environments.

The Sea Kraits of Rennell’s Island
                Sea kraits use small islands for shelter but spend half their time in the water, foraging for eels on reefs and swimming between islands. Islands used for resting and mating are close to their food source, and islands supply secure locations for females to lay their eggs. Sea kraits are the only marine snakes known to lay eggs; all other coastal and marine species have live birth ― at least we think they do. Rock piles like the one we explored have crevices and cavities which are difficult for predators to access and, therefore they are secure locations for depositing eggs. 
                Eight species of sea kraits (Laticauda) are currently recognized and several have adapted to fresh or brackish waters. Rennell’s Island is one of the Solomon Islands due east of Queensland, Australia. It is a raised coral atoll 14 km wide, 80 km long, and about 110 m above sea level. At the center of the island is a large, brackish water lagoon, Lake Te-Nggano, with an average depth of 40 m. Two species of sea kraits live in the lake. The common and widespread Yellow-lipped Sea Krait (Laticauda colubrina) is large, reaching 1.4 m and a weight of one kilogram. Crocker’s Sea Krait (L. crockeri) occurs only on Rennell’s Island in Lake Te-Nggano; it is smaller reaching 0.7 m and weighs about 280 g. Field observations suggest these two species forage for food in the same places and often together. Interestingly, there is evidence that the Yellow-lipped Sea Krait will forage in cooperative groups, so the observation that it will forage with Crocker’s Sea Krait is not that surprising.
                The principle of competitive exclusion or Gause’s Law states that two species cannot compete for the same resources and co-exist, at least not for long. Of course, the Lake Te-Nggano sea kraits don’t compete for the same resources. The Yellow-lipped Sea Krait feeds only on the native eel (Anguilla obscura) and Crocker’s Sea Snake apparently feeds only on a native goby (Eleotris fusca). The Yellow-lipped Sea Krait frequently leaves the water to bask and mate and can stay submerged for five minutes, while Crocker’s Sea Krait does not appear to leave the water at all and can stay submerged for 11 minutes. The Yellow-lipped Sea Krait lays eggs, as do all other known sea kraits, but the people on Rennell’s Island say Crocker’s Sea Krait has live birth. Hard evidence for this has yet to be found.
                There is another difference between the two species. The Yellow-lipped Sea Krait has alternating black and blue-sliver bands on its upper body, while Crocker’s Sea Krait is almost jet black. The smaller, melanistic species may be able to more rapidly warm its body than the larger, more traditionally patterned sea krait.
                Sea kraits, with their paddle-shaped tails are good swimmers, but most snakes are terrestrial; they live on land and only occasionally enter the water. Land-dwelling snakes on islands are trapped by the surrounding water. And water, particularly deep water, is a barrier not only to most land living snakes, but for many semi-aquatic and shallow water species as well. The question here is, how do land dwelling snakes get to islands? There are several ways.
                Many islands sit along the continental shelf and as sea levels have risen and fallen through time; some snakes crawled overland, swam through shallow water, or floated on mats of vegetation to reach existing islands. Other islands are fragments of continents shattered by tectonic movements, and snakes that survived the ride from deep time to the present day represent ancient lineages still living today. Of course many, if not all, snake lineages used a combination of these methods over very long periods of time to get to where they are today. However, snakes also reach islands with the aid of human transport, accidentally or on purpose. Once on an island, a snake population is usually isolated; what happens to them depends upon the environment, their genome, and chance events.

Snakes of the Remote Pacific
                Islands isolated by hundreds of kilometers of water might be expected to be snake-free, or at least free of terrestrial snakes. The ancestors to the Rennell’s Island sea krait populations were semi-aquatic snakes that could have swam or been swept by currents from Australia, or from other nearby islands.  At least four terrestrial snake species have dispersed over water to the island groups of Vanuatu, Fiji, Tonga, and Samoa, however. Two of these snakes are blind snakes in the genus Ramphotyphlops, tiny burrowing species that feed on ants and termites. These are species most likely transported by humans carrying potted plants with snake stowaways in the soil. But, Pacific island boas of the genus Candoia occur on New Guinea and are widespread in the South Pacific, ranging eastward to the Samoan Islands. The origin of these snakes has been, and continues to be, something of a puzzle. Their ancestor was hypothesized to have rafted from the Western Hemisphere across the Pacific, based upon the assumption that they are most closely related to Madagascar’s boa-like species. However, a recent molecular study suggests they are sister to the sand boas of the Middle East, Asia, and Africa. This would still require them to make the trip across the Pacific.
                 Elapids have also found their way to the Pacific Islands, the Solomon Islands and Fiji.  How snakes reached these small, remote islands is not known for sure, but all have close relatives in New Guinea. Traveling eastward from New Guinea, reptile species diversity decreases and geological evidence hints that series of island arcs formed as the boundaries of Pacific and Indo-Australian plates altered the direction of their movements. These island arcs are thought to have acted as stepping-stones, allowing snake populations to disperse over relatively short distances at any given time. Over millions of years, however, elapids have dispersed more than 3300 km east of New Guinea to the Fiji Islands, while those Pacific Island boas dispersed more than 7000 km from New Guinea to Samoa.
                Of particular interest are the anatomical and molecular clues that support a close relationship between the New Guinea Small-eyed Snake, the Solomon Island elapids, and the sea kraits. Mark O’Shea described the habitat and habits of the New Guinea Small-eyed Snake (Micropechis ikaheka) as swamps and monsoon forest creeks. O’Shea found the local dialect name ikaheka means “land eel,” a reference to its semi-aquatic habitat preferences. The other Pacific Island elapids existing today live in leaf litter or are burrowers. When DNA from the New Guinea Small-eyed Snake, the Solomon Island Coral Snake (Salmonelaps par), or the Solomon Island Small-eyed Snake (Loveridgelaps elapsoides) are included in studies with sea krait DNA,  all three appear to be related to the sea kraits and are estimated to be about 11.5 MY old. The ancestor of the Small-eyed Snake and the sea kraits may have been semi-aquatic or aquatic and it diversified into terrestrial Pacific Island elapids, the semi-aquatic marine sea kraits, and the land-dwelling Australasian elapids of today.
                Sail eastward from Sydney, Australia south of the Coral Sea, and through the southern Polynesian Islands to 27º10’S 109ºE 26W. After a trip of more than  9200 km, you’ll reach Easter Island, an 88 km2 volcanic island. The only snake reported in the vicinity of this island is the pelagic, Yellow-bellied Sea Snake, Pelamis platura, Samuel Garman wrote,

This sea serpent was taken in Lat. 26º 34’S; Long. 108º 57’W…about fifty miles northeast of Easter Island. It has been directly compared with numerous specimens… without discovery of characters on which to base so much as a variety.

There is but one snake species truly adapted for open water swimming and its has been able to disperse into the very remote Pacific; terrestrial snakes have apparently been unable to colonize Easter Island.

Island Snakes and Body Size
                Coastal southern Australia and the island of Tasmania are home to the highly venomous snake known to Australians as the Tiger Snake, and to science as Notechis scutatus. Tiger Snakes are so called because some populations are black with yellow bands, although other populations may be uniform yellow, solid black, or two-toned. The two toned snakes fade from yellow or red at the front of the body to black or gray on the posterior end of the body. Some populations of Tigers are small with an average size of about 0.7 m. However, other populations have body sizes that exceed 1.6 m. It seems likely that Tiger Snakes are the souther-most living venomous snakes. Go south off the southern coast of Tasmania and the next landfall is Antarctica.
                Tiger Snakes have confused those who study them for some time. The differences in body size and coloration from population to population suggested multiple species may have gone unrecognized. Current thought by those who work with them is that science should recognize them as one species undergoing evolution in many different environments. Tiger Snakes are in the process of evolving into multiple species.
                About 12,000 years ago the Antarctic ice sheet was at its maximum, global ocean levels were exceptionally low, and a large portion of Australia’s southern coastline sat exposed, linked by dry land, to what is now the island of Tasmania. Australia and Tasmania are presently separated by a body of water known as the Bass Strait containing small islands, many of which have Tiger Snake populations. In the mild climate of the Holocene (about 11,700 YBP to today), Tiger Snakes could have easily colonized land masses that would become islands once the ice sheet melted and the sea rose. The islands are all less than 10,000 years old, and most are only 5,000–7,000 year old.  Mainland Tiger Snakes colonized new environments where freshwater was scarce, prey was small, or prey was large, and they did so recently; thus, providing an opportunity to study evolution in action.
                On mainland Australia and the island of Tasmania Tiger Snakes eat mostly frogs.   On offshore islands it is a different story, however. On offshore islands they eat lizards, birds, and mammals. On the tiny island of Roxby in the Bass Strait, Terry Schwaner found dwarf Tiger Snakes and three species of lizards living together. The Roxby Tiger Snakes have the smallest average body lengths of all examined populations. Roxby lizards are small prey, and it seems likely that small snakes were favored over snakes with large bodies because they could find enough food to sustain themselves. However, some Bass Strait islands have large-bodied snakes. The largest individuals come from Chappell Island, and they are twice the length of the Roxby Island snakes.
                Hypotheses to explain body size differences are not in short supply. Male Tiger Snakes are not known to display male combat behavior in competition for mates, and tiger snakes are the top predator on the islands they inhabit. Therefore, hypotheses about competition, predation, and sexual selection can probably be ruled out as explanations for dwarf and giant Tiger Snakes on islands.
                Scott Keogh and colleagues, as well as previous researchers, thought natural selection acting to optimize snake body size with available prey was strongly supported because of the correlation between body size and prey size on each island. To test this Keogh and colleagues collected DNA from 33 individual snakes from various locations. The researchers included a population of dwarf tiger snakes from the mainland Flinders Ranges, as well as mainland populations from Western Australia, coastal eastern Australia, giant snakes from Nuyts Archipelago off the coast of Southern Australia, giants and dwarfs from the Sir Joseph Banks and Port Lincoln Island groups, as well as the Bass Strait islands. They discovered all populations to be closely related, that is none of them were genetically different enough to be distinct species. More importantly, the researchers found that adaptive plasticity, the ability to adapt to prey size, occurs very rapidly (in 5,000–10,000 years), and that gigantism and dwarfism has appeared in Tiger Snakes five different times, quite independently of each other.
                Mainland snakes eat mostly frogs but also take other prey (up to about 70 g), and have adult body sizes between 0.78 and 0.92 m. Dwarf populations have adult body sizes less than 0.7 m. Diet data were available only from the Roxby Island population, and they were feeding on lizards that were 10 g or less in body weight. The dwarf mountain population is thought to feed only on seasonally available tadpoles. The giant Tiger Snakes have body sizes that average about 1.20 m, but may exceed 1.60 m, and they feed on mammals or birds between 300 and 350 g. Snake populations trapped on islands adapt their body to the appropriate size for available prey. But how rapidly can these changes occur?
                The capacity for the environment to alter a population’s physical characters, such as body size, is known as phenotypic plasticity. Faben Aubret and Richard Shine collected gravid female Tiger Snakes from Carnac Island, a population that had been established by humans 80 years before. The island population feeds on sea bird chicks, but also on lizards. Aubret and Shine also collected gravid females from a mainland population at Herdsman Lake, a population that was known to feed on frogs. Snakes from the island population tended to be 13% longer and weigh 86% more than snakes from the mainland population. Offspring from each population were selected at random and fed a diet of mice and chicks; the snakes were then measured after nine months. The Herdsman Lake snakes were larger than those found on Carnac Island. Thus, phenotypic plasticity was responsible, at least initially, for the differences in body size seen in island and mainland Tiger Snakes.

The Smallest Snakes
Worm snakes (family Leptotyphlopidae) are small, usually less than 350 mm, and exceptionally slender―often just a few millimeters thick. All are short-tailed burrowing species specialized in feeding on ants and termites and have greatly degenerated eyes and teeth. Worm snakes use chemical trails left by the insects and follow them into their nests where the snakes use a raking motion of the lower jaw to collect insect pupae for ingestion (See Chapter 13). Bites from solider ants and termites are deterred by the highly polished scales that don’t allow the insects to puncture or gain hold of the snake. Worm snakes are of interest because they are the smallest of snakes, and the tiniest one lives on Barbados in the Lesser Antilles.
                Body size is important to snakes because it determines the prey size, number of prey needed, how quickly or slowly the snake will gain or lose heat, how many offspring (or eggs) a female can produce, and which predators can consume it. S. Blair Hedges found six species of worm snakes that are known to have total lengths less than 105 mm. Of the six, four are known from only one specimen and one of these is based on a juvenile specimen. In Kenya Leptotyphlops tanae is known from a series of specimens, nine of which are males and one of which is an immature female. The largest is a 103 mm male. Sex is difficult to determine in these snakes, but male worm snakes are usually smaller than females. Thus, it is likely that the 103 mm male is not representative of the species’ maximum size. However, Carla’s Worm Snake, Tetracheilostoma [formerly Leptotyphlops] carlae, is known from five specimens from Barbados, the largest of which is a 104 mm female containing one greatly elongated egg. Clutch size is closely correlated with body size in snakes, and it is not surprising that the world’s smallest known snake has a clutch size of one.
                The world’s smallest snake made headlines twice in the fall of 2008; first, when the snake’s discovery was announced and then, again, when Barbados residents protested Professor Hedges naming the new species after his wife instead of something related to the island.  Some Barbadians claimed their parents had shown them the snake. Unfortunately, neither the protestors’ parents, nor the current generation of Barbadians, were zoologists.

Island Pitvipers
                Thirteen kilometers off the coast of northeast China’s Liaodong Peninsula is Shedao Island. Shedao literally means “snake island.” Although the island is in Chinese waters, the presence of a pitviper on Shedao was first reported to the scientific world by the Japanese when they occupied Manchuria in the 1930’s. This tiny island (about 0.73 km2) has a highly seasonal climate with cold, dry winters and warm, rainy summers, and it has a pitviper population estimated at 9100–11,500 (about 1 snake per square meter). The snake, the Shedao Mamushi (Gloydius shedoaensis), is similar to the Rock Mamushi (G. saxatilis), which also inhabits the Chinese mainland as well as the Liaodong Peninsula, North and South Korea, and eastern Russia.   Chinese scientists discovered adults feed almost exclusively on small birds (warblers and buntings) that make a migratory stop on this little island on their way to and from Siberia. The Shedao Mamushi climbs into bushes, lies along a branch, and waits for a bird to land within striking distance. Or, they lay on the ground concealed by leaves, waiting for a migrating bird to land nearby. Richard Shine and colleagues visited the island and found smaller snakes used ambush sites in bushes and trees, and larger snakes used ambush sites on the ground.      Experiments showed that smaller, and presumably less experienced snakes, had a lower rate of success capturing birds than did adults. Adults often struck the bird’s head while juveniles often struck the wing or body and had a less secure grip. Shine and colleagues hypothesized that the arboreal ambush sites increased the snakes’ hunting success because a pearching bird’s position was more predictable. Smaller birds used the perches while larger birds landed on the ground.
                Despite the large size of newborn Shedao Mamushi, they are apparently too small to feed on birds immediately. The few juvenile specimens examined with stomach contents contained centipedes and pill bugs (isopods). The neonates weighed twice as much as their mainland relatives at birth, and it seems likely this allows them a head start in being able to eat small birds after just a little growth. Prey is rare on the island and the survival of Shedao Mamushi depends upon the supply of migrating birds. Females give birth just before the fall bird migration, providing them the opportunity to replace the body weight lost during reproduction.
                How the Shedao Mamushi arrived on this island is not known, but the island is on the continental shelf in shallow water and at glacial maximum, an overland connection was undoubtedly present. Dispersal over water cannot be ruled out, however.
                Two tiny islands off the coast of southern Brazil support two species of endemic pitvipers. In many respects, the snake population on the Ilha da Queimada Grande is similar to China’s Shedao Island. The Golden Lancehead (Bothrops insularis) is found only on this 0.43 km2 island. Bothrops insularis occurs in a dense population, the snakes feed mostly on migrating birds, and it uses both the ground and low vegetation for ambush sites. The Golden Lancehead is perhaps best known for its exceptionally toxic venom that liquefies tissue, causes intense pain, and prevents blood from clotting. Local fishermen tell stories about the Lancehead to rival bad snake sci-fi cinema and the mamba story which began this book. The last lighthouse keeper and his family to live on the island were reportedly “attacked.” Snakes poured into the building through the windows forcing the family to flee through the vegetation only to be bitten by snakes hanging from trees and shrubs. The crew from a Navy supply ship supposedly found the bodies scattered around the island. And then there is the more believable story of a fisherman who went ashore to pick bananas and was bitten, but made it back to his boat. He was found dead, sprawled across the blood-soaked deck.
                Golden Lanceheads are also known for their unusual reproductive organs; many individuals are intersexual. Intersex snakes have reproductive organs of males and females, a condition also reported in other lancehead (Bothrops) species from mainland Brazil. Some intersex snakes with reduced male genital and ovaries have even been found to contain well- developed embryos. The Golden Lancehead reaches a total length of about 1.18 m, but most adults are about 0.7 m in total length.       
                Ilha da Queimada Grande is free of rodents and, in an interesting experiment using free-ranging Golden Lanceheads, Otavio Marques and Ivan Sazima presented the island snakes with house mice to see how the snakes would react. Much to their surprise, snakes naïve to mice responded in the way their mainland counterparts do; they struck and released the mice. These are the same snakes that are familiar only with birds as prey, and they strike and retain the bird in their jaws until it has been immobilized.
                About 35 km off coastal Sao Paulo, Brazil is Alcatrazes Island, a 1.35 km2 island covered with the remnants of Brazil’s Atlantic Forest. The Alcatraze Lancehead (Bothrops alcatraz) is a dwarf species, with males reaching 0.46 m, and slightly larger females growing to lengths of roughly 0.52 m. Like the Bass Strait tiger snakes, diet has been the major factor contributing to the dwarfism in this species. Litter sizes in this snake appear to be reduced, averaging only one or two offspring per litter with newborn snakes measuring only 150 mm at birth. Perhaps most interesting is the food chain on Alcatrazes Island. Snakes were found lurking under sea bird nests and were often white-washed with uric acid from the bird droppings. Cockroaches are abundant and feed on the birds’ guano; the roaches are eaten by centipedes, and the Alcatraze Lancehead feeds on the centipedes as well as the occasional lizard. This is currently the only species of Bothrops known to feed exclusively on ectothermic prey. The Golden Lancehead appears to be related to the Caatinga Lancehead (Bothrops erythromelas) and the Chaco Lancehead (B. diporus).
                In a recent survey, the Jararaca (Bothrops jararaca), a large species (1.6 m maximum size) that inhabits southeastern Brazil, was found on 11 of 18 islands. Based on this distribution, it appears that the Jararaca is continuing to disperse in the coastal environments. The Brazilian islands are on the continental shelf and it seems likely that the snakes arrived on the islands during times of lower sea levels. But again, over-water rafting cannot be ruled out, particularly for island populations of the Jararaca.
                Convergence between the Shedao Mamushi and the Golden Lancehead was studied by Wolfgang Wüster and colleagues by comparing fang length, head length, and other anatomical features in both island species and their mainland relatives. The authors found both island species had elongated heads when compared to their mainland ancestors. The Golden Lancehead, with shorter fangs and a longer tail than its mainland relative, probably diverged from the ancestral mainland population about 2 MYA. The Shedao Mamushi has a fang length and tail length similar to those found in mainland populations; however, the fang length was already short in the ancestor. Wüster and colleagues proposed that the reduced fang lengths may be the result of a hunting technique that involves striking and holding the bird in the mouth until it can be swallowed. Mainland Jararaca strike and release mammals and then track the mammal until it is immobilized. The shorter fangs of island snakes may not break as easily when holding struggling prey.
                Early explorers found Caribbean islands relatively free of dangerous animals, with two exceptions; the volcanic islands of Martinique and St Lucia. Both islands supported populations of large, dangerous pitvipers. On Saint Lucia is the lancehead, Bothrops caribbaeus, commonly named for its home island. The Martinique pitviper has been called the Vipère Jaune, the Fer-de-lance, and the Martinique Lancehead (Bothrops laceolatus). The name Fer-de-lance has been used indiscriminately for many of the snakes in the genus Bothrops, but was original intended for the Martinique species. Unlike the Brazilian islands with pitvipers, Martinique and Saint Lucia have well-established human populations and these two snakes have had a long and turbulent relationship with humans.
                One 19th century author wrote that the total absence of idyllic and pastoral elements in Martinique literature resulted from the presence of the Fer-de-lance. The author attributed the fact that the flora and fauna of the island remained unknown because the Fer-de-lance “…renders all serious research dangerous in the extreme.”
                With the arrival of the Europeans in the 16th century, the Lesser Antillean forests were cut and crops were planted. This habitat alteration allowed the rat population and their predators to dramatically increase in number. In the 19th century, Saint Lucia’s George William Des Voeux estimated the annual snakebite fatality rate at 1.2 per 1000, or about 25–30 deaths per year (accurate records were not taken). He passed legislation to pay a bounty on venomous snakes. Within seven months, bounty was paid on 12,000 snakes and the allocated funds were exhausted. Continuation of Des Voeux’s plan was not without opposition; merchants living in towns were opposed because they were not in danger of being bitten, and the plantation owners were opposed because they recognized the snakes’ beneficial role in rat control, thus neither group wanted to pay for controlling the snakebite problem. Despite this, Des Voeux suggested the bounty worked and the number of deaths was steadily reduced: 22 in 1869, 16 in 1870, and 12 in 1871.
                Determined to solve the Saint Lucian snakebite problem, Des Voeux obtained several mongooses from Philip Scalter at the London Zoo and set-up a fight-to-the death match between a snake and one of the viverrids on the lawn of the Government Building. The mongoose killed the snake, and Des Voeux proceeded to introduce the species to Saint Lucia. Despite evidence that mongooses ate chickens, Des Voeux maintained that they were controlling the snakes, citing the reduced number of deaths, which was one by 1898. Of course, we now know the mongoose is a diurnal predator, prefers to eat birds, and rarely encounters the nocturnal Saint Lucian Lancehead.
                For the first half of the 20th century, the two island pitviper populations were considered the same species as the widespread South American common lancehead, the Barba Amarilla (Bothrops atrox). Herndon Dowling proposed Carib Indians had transported the snakes via canoe to the islands so they could be used as a biological weapon against the Arawak people. If true, this would make the island pitviper populations only a few hundred years old. Des Voeux also suggested a historical hypothesis about the origin of island pitvipers, stating that 16th century planters had imported them to prevent their slaves from hiding in the forests.
                However, detailed examination of specimens from known localities, as well as ecological and behavioral data, suggested the island species were distinct from the South American species and distinct from each other. Saint Lucian snakes had 25–29 scale rows at mid body and 198–212 ventral scales, while the Martinique animals had 29–33 rows of dorsal scales and 218–237 ventral scales. Both species also had uniform coloration on their belly while mainland populations had pigmented bellies. While both species climb, Saint Lucian pitvipers spend much of their time on the ground, whereas the Martinque snakes spend considerable time in the trees. There were also differences in the defense behavior of the two species. Despite the evidence that each island had its own endemic species, other commentators suggested that the islands were constantly being supplied with new genetic material from snakes that were floating out to the islands from the mainland.
                DNA sequences from the two populations settled the question. Wolfgang Wüster and colleagues used 1,600 base pairs from two genes and found the Lesser Antillean snakes were distinct from mainland South American species, and distinct from each other. The study suggested the mainland Barba Amarilla–Terciopelo species complex (B. atrox-asper) had a shared ancestor with the island species in the late Miocene or early Pliocene (8.9–4.2 MYA), and that the two island species had shared an ancestor 6.5–3.1 MYA. Thus, the Caribbean pitvipers are relatively old species, diverging from each other about 6–5MYA, not the few hundred to a few thousand years previously suggested.
                Rumors about pitvipers on other islands such as Tobago, Guadeloupe, and Dominica persist. These islands are relatively well known and none are currently known to support populations of pitvipers. Stories about Tobago pitvipers come from mislabeled specimens that originated on Saint Lucia. The British Museum of Natural History houses two specimens of Bothrops lanceolatus said to be from Guadeloupe, mislabeling is a possible explanation. But, Lafcadio Heam stated that the species was introduced into Guadeloupe to control a plague of rats. No date is given, but the introduction was likely to have occurred in the 19th century. If true, it could explain the locality given for the museum specimens. The Dominica locality remains a puzzle, but an unsuccessful human introduction cannot be ruled out.

Sky Island Snakes
                The trail was steep and covered with Ponderosa Pine needles and cones shed by the huge conifers. As the ground leveled out, the forest opened, revealing the base of the mountain’s peak and a huge jumble of eroded rocks. Within minutes I heard a low buzzing sound, and found the source to be a small, grey-spotted rattlesnake coiled at the base of a boulder. Twin-spotted Rattlesnakes (Crotalus pricei) are easily recognized by the double row of spots on the dorsum and the orange tipped tail at the base of the rattle [Figure 10–2]. It is one of several species of dwarf sky island rattlesnakes inhabiting the pine-oak forests of the southwestern USA and northern Mexico. Like snakes trapped on oceanic islands, snakes found in isolated islands of habitat on mountain tops tend to evolve small body sizes or large body sizes depending on available prey.

INSERT FIGURE 10-2.
Figure 10–2. The Twin-spotted Rattlesnake (Crotalus pricei) a small Madrean sky island species in southern Arizona.

                Islands are cauldrons for evolution and it does not matter whether it is land isolated by water or a terrestrial habitat isolated by another habitat. Islands produce endemic species because over time they separate gene pools. About 22 sky island complexes can be found around the world and the Twin-spotted Rattlesnake inhabits the Madrean Sky Island Archipelago from southeastern Arizona southward through Mexico’s Sierra Madre Occidental. Many of these populations are isolated in pockets of woodland or forest with rock outcrops that are between 1,850 to 3,200 m in elevation and separated by valleys with dry savanna and desert. The drier, more open habitats are alien landscapes to the Twin-spotted Rattlers. Thus, they move only when their habitat is more widely distributed into the lower elevations of the valleys during times of higher rainfall.
                Africa has a sky island complex that is particularly rich in endemic species, including snakes. The Dagger-toothed Vine Snake (Xyelodontophis uluguruensis) is endemic to the montane evergreen forests of East Africa’s Eastern Arc Mountain sky island complex. This species is a relative of the Boomslang and African vine snakes previously discussed in Chapter 4. In fact, the Usambara Vine Snake (Thelotornis usambaricus) is also an Eastern Arc Mountain sky island inhabitant, but uses coastal forests at lower elevations and has a relict population on the Kenya coast. Unlike the Twin-spotted Rattlesnakes, however, these species are not dwarfed, they are average size for their clade and slightly exceed a meter in length.
                Several of the small, broad-headed bush vipers of the Atheris complex are also Eastern Arc Mountain species. Bush vipers have stout bodies, prehensile tails, and heavily keeled overlapping scales. They are usually associated with hill forests that are over 1,200 m in elevation and their distributions seem to reflect changes in the vegetation during Pleistocene. Habitats in this sky island chain include rock escarpments, grasslands isolated by savanna, and dry and wet forests. Various species of bush vipers have adapted to different habitats and while some species occur throughout the Eastern Arc, others are restricted to a single mountain top.
                William Branch and Julian Bayliss recently described the remarkable Mount Mabu Viper (Atheris mabuensis) from mid level elevations (1,000 to 1,550 m) on Mount Mabu and Mount Namuli in northern Mozambique. The snake is a dwarf, reaching a maximum total length of 380 mm. Adults retain the brown and gold coloration seen only in juveniles of other species, and which camouflages the snake in forest leaf litter. This little viper will climb onto small twigs lying on the floor of its cage; it presumably does the same in the forest. It caudal lures to attract frogs and lizards. The discovery of this viper in 2008 emphasizes both the unique biodiversity of Africa’s sky islands and the fact that much remains to be learned about snake biodiversity.
                The Pantepuis sky island complex of northern South America has flat-topped mountains commonly known as tepuis that were made famous by Sir Arthur Conyan Dolye’s novel the Lost World. The tepui complex has few endemic snakes that have been discovered to date, but snakes can be notoriously difficult to find. In 2002, an endemic coral snake (Micrurus pacaraimae) was described from this area. It was collected in shrubby vegetation with rock outcroppings at the edge of a small river dissecting a valley. Not much can be said about it since it is known from a single specimen. However, more endemic snakes are likely to be found in this unusual sky island complex since there are a number of known endemic frogs and lizards from the flat topped mountains.

Arboreal Snake Dispersal Over Water
                The Natuna Islands form an archipelago of about 272 islands located midway between Borneo and peninsular Malaysia in the South China Sea. While these islands were connected to Borneo, Sumatra, and Malaysia during the Pleistocene, the Natuna snake fauna does not appear to be the result of simple overland migrations.
                An analysis done by Robert Inger and Harold Voris found 11 arboreal species, five terrestrial species, one aquatic species, and one fossorial species on Natuna. About 77 widespread snake species occur in Borneo, Malaysia, and Sumatra and, based on their ecological types, the Natuna Islands would be predicted to have five to six arboreal species and nine to ten terrestrial species.
                West of the Natuna Islands and much closer to the coast of peninsular Malaysia, is the Seribuat Archipelago, a cluster of 62 islands organized into three arcs. The inner arc is close to the mainland, and sits in water less than 10 m deep. The middle arc is about 12 km west of the first arc, in 10–19.5 m of water. The outer arc is about 20 km further east and in water that is 20–60 m deep. Lee Grismer and colleagues surveyed the herpetofauna of the archipelago and found 44 species of snakes, four of which are endemics. Their findings mirror the work done by Inger and Voris in the Natunas. Most of the snakes were arboreal, shrub and a tree trunk specialist, and only two were fossorial species. One species, the Reticulated Python (Broghammerus reticulatus), is a very good swimmer and undoubtedly capable of traveling between the mainland and many of these islands, but it also climbs trees.
                The absence of many of the terrestrial and fossorial species from both of these archipelagos is striking since they were connected by land as recently as 10,000 years ago at the last glacial maximum.
                Inger and Voris suggest that at least some of Natuna’s snakes dispersed not overland at times of lower sea levels, but by island hopping on trees swept out to sea as the large rivers reached flood stage. Borneo’s largest river, the Kapuas, empties into the South China Sea about 75 kilometers from the Natuna Islands. None of the known Natuna snakes are endemic to the islands and it would seem likely that the exaggerated arboreal snake fauna is the result of over water dispersal.
                Similarly, the east coast of Malaysia opposite the Seribuat Archipelago has about seven major rivers draining into the South China Sea. It would seem probable that the archipelago species would be the result of over water dispersal from peninsular Malaysia. However, molecular studies to support the origins of the Natuna and Seribuat faunas have yet to be done, and surprises are always possible.
                Treeboas (Corallus) are widespread in the West Indies, Central America, and South America. When Robert Henderson and S. Blair Hedges compared West Indian populations to mainland populations using mitochondrial DNA sequences, the West Indies populations turned out to be most closely related to populations from Guyana and the Amazon. This was unexpected, given that Trinidadian and Venezuelan populations were much closer to the Grenada Bank islands and St. Vincent. However, the South Equatorial current appears to be responsible for the Grenada Bank-St. Vincent populations of treeboas. Given the DNA results, it is more likely that trees washed into the Caribbean from a river in the Guianas or the Amazon carried the snakes into the West Indies, rather than vegetation mats from the Orinoco River or the island of Trinidad.
                Treeboas have been found swimming in the Caribbean 1.5–3.5 km from shore. Robert Henderson and Richard Sajdak reported the observations of Larry Maul and his wife who twice encountered treeboas during the summer of 2001. The snakes were not associated with floating debris. Henderson and Sajdak suggested that in most cases, the snakes would likely die from dehydration, drowning, or predation. However, should one survive to make landfall, it could colonize a new location.

Invasive Snakes on Islands
                On a rainy tropical morning sometime after World War II, possibly in 1948, a cargo plane loaded with wooden crates and scrap metal took off from a base in the Admiralty Islands and landed on the island of Guam. Guam is the southernmost island in the Mariana Island group and a United States Territory in the southwestern Pacific. The plane was carrying used war equipment and metal for recycling, but it was also carrying a stowaway.
                A slender Brown Treesnake (Boiga irregularis), about 1.5 m long, had been living on the Solomon Island airbase hunting roosting birds and lizards. This female was very successful at capturing food, and she converted her prey’s energy and molecules into stored fat and body mass. The lipids altered her odor, making her more attractive to males. She mated with several males while on the air base and stored their sperm in her reproductive tract.
                In time she grew restless, her body had started to convert the fat into eggs. In a few more weeks she would fertilize her eggs with the stored sperm and she needed a safe place to deposit the eggs. A wooden crate provided refuge; the female crawled inside and found a secure hiding placing in the packing materials.
                As the cargo was unloaded, so was the female snake. After dark, she crawled across the runway into the nearby forest. The female snake did not realize it, but she had just won reproductive success for her genes and offspring at a level few animals ever experience. The safe landing of the plane carrying the Brown Treesnake corresponds with the start of an ecological disaster. The disaster was a quite one, and went unnoticed for more than 30 years.
Guam is an oceanic island with a mixture of grasslands and forests. It had 18 species of birds; 10 were forest dwelling species, and five were endemic to Guam. Fifteen of these eighteen bird species have now disappeared. Guam also had lizards. Some like the house gecko, and the oceanic geckos were species that probably stowed away on ships and traveled with humans to the island. But others had been on Guam long enough, like some of the birds, to become distinct species, endemics found nowhere else. Many of Guam’s lizards, particularly the geckos, now appear to be extinct or greatly reduced in numbers. Only the introduced House Gecko (Hemidactylus frenatus) has increased its numbers on the island, and this may be due to the reduced competition from other species, but it may also have something to do with its ability to live on walls of buildings that are inaccessible to the Brown Treesnake.
Guam had only three native mammals, all species of bats. One was a small species of fruit bat and it has not been seen since 1968. While the snake is suspected of causing its extinction, scientific evidence does not exist to support the suspicion. The Marians Fruit Bat is a large species, its numbers had been reduced to about 50 animals in 1978, but the species rebounded to more than 1000 animals by 1982. Since that time the species has gone into decline, possibly due to the snake feeding on the young bats when they cannot be protected by the parent. The Pacific Sheath-tailed Bat (Emballonura semicaudata) has not been recorded on Guam since 1972 and the Guam population is believed extinct. Again the Brown Treesnake is the suspect.
                Not only has the Brown Treesnake been a disaster for the Guam fauna, but it has caused numerous problems for humans living there as well. Perhaps most unusual are the power outages it causes. Between 1978 and 1994, there were almost 1,200 power outages attributed to treesnakes. The snakes would ascend guy wires used for support and gain access to a set of conducting wires that were surrounded by ionized air. When the snake reached these wires it caused a flashover fault resulting in a power outage.
                The Brown Treesnake is a rear-fanged species with grooved fangs, venom, and an attitude that results in attempts to swallow food items much larger than it can actually deal with, including human infants. A survey of 284 Guam residents asked them about finding tree snakes in their houses and yards, 79% said they had seen the snakes in or around their home. These snakes are quite aggressive and are not deterred from entering an area when humans are present. Between 1989 and 1993, 166 bites were reported, 11 of these were considered serious. All serious bites were sustained by sleeping infants less than a year old. Most occurred between dusk and dawn when Brown Treesnakes are hunting and it seems likely the bites were attempts to consume the newborn humans. The snakes involved in the bites were large, usually more than 1.3 m long, and in seven cases the snakes tried to constrict the infants. The Brown Treesnake is now estimated at population densities of more than 5000 per km2 in some forested areas and it seems unlikely that control is possible.
                Invasive species are out of place, they are in environments where they did not evolve, and their presence can have long term, cascading consequences that are difficult to predict. Hanne Mortensen and colleagues examined the impact of the Brown Treesnake on vertebrate pollinators visiting the Black Mangrove Tree (Bruguiera gymnorrhiza) and Tiger Claw Tree (Erythrina variegate). The study compares tree pollinator behavior in Guam with its high snake population to the behavior of the same or similar pollinators in Saipan where there are few snakes. Both species of trees are pollinated by birds. On Guam, no birds visited either of the tree species under observation, while on Saipan bird visits per day to both tree species approached 120. Insects and lizards also visited the flowers, but only the lizards were considered potential pollinators of these flowers. As expected, Saipan trees produced more seeds than did the trees on Guam. Treesnakes have had a significant impact on the Guam ecosystem, affecting organisms well beyond their prey species.
                Cozumel Island is a well known point of debarkation for tourists in México, but it became the destination for a group of common Boa Constrictors (Boa constrictor) in 1971. Someone working for a film production company released Boa Constrictors near Palancar Beach after the filming was complete. While the Boa Constrictor is native to México, it was absent from Cozumel Island until the release of the snakes, and it very quickly increased its numbers. A wildlife survey 25 years later reported 1.8 boas for every 100 km of forest surveyed. Road surveys done by Irene Romero-Nájera and co-workers in 2001 and 2002 found 0.03 boas for every 10 km of roads driven and they found the snake widespread and relatively abundant. Boas were present in virtually all habitats, including the city. Romero-Nájera and colleagues recognized the paradox, the snake is considered threatened on the Mexican mainland, but has become invasive on Cozumel.
                A similar situation seems to be occurring on the Dutch West Indies island of Aruba. The Boa Constrictor was first discovered in 1999 with five specimens captured that year. In 2001, forty snakes were captured, and by 2003 the annual capture rate was 273 snakes. The boas ranged in size from neonates to 2.8 m adults and included two pregnant females. John Quick and colleagues documented the snakes island wide and examined the stomach contents of 47 specimens. They were eating lizards, birds, and mammals. The origin of the invasion remains unknown. Quick and colleagues point out that a major difference between the Aruba Boa Constrictor  invasion and the Brown Treesnake invasion on Guam is that Aruba does not have many endemic species. Most of the island’s vertebrates are derived from nearby mainland populations where the Boa Constrictor occurs naturally. Therefore, the native vertebrates may be better equipped to respond to the sanke.

Rare Island Snakes
                The isolation of islands and reduced numbers of species makes them more sensitive to environmental disruptions. The Lesser Antillean island of Antigua and its satellites have a land surface area of about 282 km2 and are home to the Antiguan Racer (Alsophis antiguae). The Antiguan Racer was once found over most of this area. By 1936, H. W. Parker at the British Museum declared the species extinct. But in 1991 Rick Sajdak and Robert Henderson reported the species restricted to Great Bird Island, an area about 0.1% of the original distribution of the snake. Populations elsewhere had been destroyed by the introduced Asian mongoose. Jenny Daltry and colleagues surveyed the last population in 1995 and estimated 51 snakes remained, but reported the snakes were being seriously injured by the introduced Black Rat (Rattus rattus). An attempt to breed the snakes in captivity was made in 1996 at the Jersey Zoo, but failed because the snakes were highly sensitive to snake mites (Ophinonssus natricis), a common parasite in captive snake collections. In 1999, a trial re-location was attempted, 10 snakes were moved to Rabbit Island where the Black Rat had been eradicated. The colony took hold. By 2002 the snakes were reproducing, and by 2006 the Rabbit Island population was estimated to be 40 to 50 snakes. A rat eradication program on Great Bird Island was successful, and soon after the Antiguan Racer populations increased dramatically; it doubled in the first 18 months and increased by 300% over the next nine years.
                The Mascarene Islands of the Indian Ocean are remote. They are volcanic in origin and were created by the Reunion hot spot, with the first island formed about 35 MYA. Round Island is a small (169 hectares) member of this island group and is located about 20 km northeast of Mauritius. It is home for two related, ancient snakes placed in the family Bolyeriidae. The DNA clock suggested these snakes evolved in the Cretaceous, about 97 MYA. The Round Island snakes are sometimes called “boas” but they are not; they are more ancient than boas and are of interest because together they form the sister to shield-tailed snakes (Uropeltidae) and the booid snakes (Boidae, Pythonidae, Xenopeltidae, Loxocemidae, and the Pythonidae). Bolyerids have an unusual jaw divided into front and rear sections, which may be an adaptation to feeding on skinks but little is known of their natural history.
                Goats and rabbits introduced to Round Island in the 19th century subsequently destroyed the native vegetation. Nine species of reptiles were known to inhabit the island and several of them are thought to have passed into extinction with the help of humans and the introduced herbivores. The Round Island Burrowing Snake (Bolyeria multicarinata) has not been seen since 1975, but the Round Island Keeled-scaled Snake (Casarea dussumieri) is still present, though probably in low numbers. The Jersey Zoo’s captive breeding attempt with Casarea met with some early success, but ended in the early 1990’s. The Zoo was again successful after the discovery that the snakes need vitamin D3 to reproduce. In 2005, eggs were successfully hatched. Casarea was also found on the island of Mauritius but its population on that island appears to have become extinct shortly after it was discovered. The Round Island goat population was eradicated by 1978, and the rabbits were gone by 1986. The lizard and snake populations were predicted to recover, and while some of the lizard populations have increased their numbers, Casarea numbers have not increased significantly.
                Evolution of island species may increase after the founding members find themselves in isolation. The island may be free of both competitors and predators and resources may be severely limited or very abundant. Island invaders encounter new food resources and a new community of organisms to interact with. While island populations may lead to a dead end for many species, the possibility of species dispersal from islands back to the mainland or dispersal off a mountain top into lowland environments cannot be ruled out. Understanding species survival on islands will become increasingly important as humans fragment virtually all habitats into islands across the globe. Fragmented habitats can be expected to accelerate extinction for many species, but the species that do survive will be following the rules of island biogeography.

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