Snakes with feet, anti-goo saliva, and more recent updates

This post will soon be available in Spanish

More of the latest snake news and research (for other recent updates, see posts from March, June, and August)—and, perhaps the most exciting news of all is that I have defended my dissertation and will be returning to writing more in-depth content in the next few months!

Rattlesnake Roundups (I and II)

A Texas conservation licence plate ironically depicting
a Western Diamond-backed Rattlesnake (Crotalus atrox).
Funds from these plates support a variety of valuable
conservation projects in Texas under the Texas
Wildlife Action Plan, although none are specific to snakes.

Advocates for increasing state oversight of rattlesnake roundups in Texas received disappointing news this week when the Texas Parks and Wildlife Commission decided that they would not support a proposed ban on using gasoline fumes to collect rattlesnakes. Rather than reviewing and voting on the issue at their bi-annual meeting next month, the TPW Commission decided to remove it from their agenda entirely, citing "insufficient support from legislative oversight or the potentially regulated community". This decision marks the second time reviewing the ban has been put off, and unfortunately it is likely to be the last until the effort to reform roundups is re-initiated. The announcement included the statement that "TPWD [Texas Parts and Wildlife Department] staff still believe that there are better options for collecting snakes that do not adversely impact non-target species, and we will continue to work with the snake collecting community to develop and implement best practices that reduce potential impacts to these species", although in the absence of specific details it is hard to believe that this issue will remain at the fore of wildlife management in Texas without continued pressure from advocates of scientific rattlesnake management. However, Representative Susan King of Sweetwater's 2015 house bill 763 requires that petitions to state agencies (including TPWD) that are signed by <51% Texas residents are not valid, which means that the ability of non-Texans to influence policy on this issue is now greatly diminished.

If you're not familiar with the issues surrounding the gassing ban, I encourage you to read the 2016 Snake Harvest Working Group report, the same document that was available to the TPW Commission prior to their decision this week. Among other topics, it contains data on the adverse impacts of gassing on non-target endangered species, which is the primary impetus for the ban. It hints at human health impacts of consuming meat from gassed rattlesnakes. The SHWG report also summarizes previously unavailable data on roundup economics, showing that profits are not related to the number of rattlesnakes at an event and did not decline after gassing was banned in Alabama and Oklahoma. Stakeholder survey responses and the vast majority (>90%) of public comments from Texans were in favor of the gassing ban, as are many TWPD employees.

The TPW Commission is solely responsible for this decision. You can let the TPW Commission and Texas State Representative Susan King of Sweetwater (or your own state representative, if you live in Texas) know whether you think they are acting in the best interest of the majority of the public and in accordance with game management principles at the links provided (if you no longer have a fax machine, you can send a fax over the Internet here).

Goo-eating Snakes and the Eggs that Evade Them and Basics of Snake Fangs

Mandibular glands of Dipsas alternans
From Zaher et al. 2014

This discovery is from 2014, but it's newer than either of the past posts to which it's germane and I just found out about it. Perhaps you've seen the incredible rapid hatching behavior that treefrog eggs have evolved to escape from snake predators, including cat-eyed snakes (genus Leptodeira), blunt-headed tree snakes (genus Imantodes), and snail-sucking snakes (genera Sibon and Dipsas). These snakes also eat a variety of other gooey prey, such as earthworms, leeches, snails, slugs, adult frogs, caecilians, and, more rarely, non-gooey prey like lizards and reptile eggs. They have a number of adaptations that help them consume their sticky, viscous prey, including long, slender teeth, skull bones and muscles modified for extreme lower jaw extrusion, and a short-snouted, large-eyed look that resembles a snake embryo. Recently, a team of scientists from Brazil discovered a new one: a protein-secretion delivery system in the lower jaw.

Are the secretions venom? No. Dipsas and its relatives always extract snails using a sudden strike, followed by fast, alternating probing motions of the mandible inside the shell; this behavior could hardly depend on a chemical reaction of any kind. Instead, the gland secretions probably play a role in mucus control and prey transport rather than immobilization or killing of the prey. Although the glands in some species are associated with muscles, they are not connected to any teeth, but rather open onto the floor of the mouth, which in some species is covered with extensively loose, folded skin. Hypertrophied infralabial glands have been known from some dipsadine species since the 1960s, but the new paper describes the muscles and other soft tissues surrounding them and documents their variation among several dozen species of this very speciose group of snakes. On the other side of the world, pareatid snail-eating snakes have independently evolved a similar lifestyle, complete with upper jaw glands of perhaps similar function.

Why snakes are long and Why do snakes have two penises?

Pelvic girdles (dark blue) and hind limbs (red) of lizards,
living snakes, and extinct snakes with fully-developed limbs.
ZRS is the name of the SHH enhancer gene
that has been partially deleted in snakes.
From Leal & Cohn 2016

Many people are familiar with the tiny vestigial legs or "spurs" of boas, pythons, and other henophidian snakes. These structures are sexually dimorphic and are used by male boas and pythons in male-male combat and also to titillate females before and during mating. New data from the University of Florida describes how the spurs are formed: a weak flicker of activity by a gene called Sonic hedgehog (SHH) during the first few hours of embryonic development, in contrast to strong, sustained activity of this gene in lizard embryos throughout their development, forming legs. In snakes, unique genetic deletions from an enhancer of SHH explain its weak activity; transgenic mouse embryos with the same deletions showed similarly weak SHH activity, whereas mouse embryos grown with a lizard enhancer developed normally. Caenophidian snakes, such as vipers, gartersnakes, and cobras, had more extreme deletions and mutations, with the cobra barely retaining any of the SHH enhancer gene.

Amazingly, the researchers also found that HOXD13, the part of the limb-building gene that's responsible for building hands and feet, was unaltered in python embryos, and that python embryos develop not just a pelvic girdle and femur, which form the spur in adulthood, but cartilaginous templates of a tibia, fibula, and foot, which are reabsorbed prior to hatching. Although living snakes appear to follow a gradual pattern of limb shrinkage and loss, some extinct snakes that are thought to have been more similar to boas and pythons than they were to blindsnakes also had fully-developed, albeit small, limbs, complete with feet, as adults. This new discovery helps explain the apparent evolutionary "re-appearance" of these structures; they were never completely lost in the first place. As for the reason why not, snake HOXD genes and their regulators appear to be equally important to the development of their paired hemipenes, structures of obvious importance.

REFERENCES

Oliveira, L., A. L. Costa Prudente, and H. Zaher. 2014. Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology 275:87-99 <link>

Leal, F. & Cohn, M.J. 2016. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Current Biology DOI:10.1016/j.cub.2016.09.020 <link>

Leal, F. & Cohn, M.J. 2014. Development of hemipenes in the ball python snake Python regius. Sexual Development, 9, 6-20 <link>

Savitzky, A.H. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist, 23, 397-409 <link>

Texas Parks and Wildlife Department. 2016. Snake Harvest Working Group Final Report <link> <references> <summary>

Zaher, H., de Oliveira, L., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, M.M. & Prudente, A.L. 2014. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary Biology, 14, 1-28 <link>

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Virgin Birth, the Color of Fossil Snakes, and More Recent Updates

This post will soon be available in Spanish

As I did in March, I wanted to highlight some recent and exciting updates to some of my older articles.

Snakes That Give Virgin Birth

Phylogenetic pattern of parthenogenesis in snakes
Molecular tree on left, morphological tree on right
From Booth & Schuett 2016

When I wrote about asexual reproduction in snakes in February 2014, new records of this phenomenon were rapidly accumulating, from snakes as distantly related as cottonmouths and boa constrictors. In a new paper, Warren Booth and Gordon Schuett review the knowns and unknowns of "virgin birth" in snakes, a subject which has become their specialty (it even has its own Facebook group). Although obligate parthenogenesis is still known only from Brahminy Blindsnakes (Indotyphlops braminus), the new summary reports that facultative parthenogenesis has now been documented in 20 species of alethinophidian¹ snakes, and this list is anticipated to grow, although so far confirmed cases are limited to five lineages: boids, pythonids, Acrochordus, Crotalinae, and Natricinae. This new synthesis formalizes one of the trends that I wrote about in 2014, namely distinguishing between "Type A" facultative parthenogenesis, in which the offspring produced are large clutches of viable females that seem to have a strange "WW" sex chromosome arrangement (apparently typical of boas and pythons), and "Type B" facultative parthenogenesis, which is where all the offspring are male and few are born alive, many with extreme developmental abnormalities (apparently typical of colubroids).

Most intriguing is the hypothesis laid out for explaining this dichotomy: that boas and pythons (and possibly other basal alethinophidian snakes) might have an XY sex determination system rather than a ZW one like most snakes. Changes from ZW to XY or vice versa (and between genetic and temperature-dependent sex determination) have been documented in geckos and turtles, and could have been overlooked in boas and pythons due to their similar-looking sex chromosomes (tests are currently underway to falsify or verify this hypothesis). If true, this would explain the production of all-female offspring by facultative parthenogenesis; instead of WW, those females would be XX, just like humans!

Identifying Snake Sheds

True-color representation of the fossil snake
(MNCN 66503) in McNamara et al. 2016.
The dentition looks too solenoglyphous for a
colubrid, although the 10-million year old specimen,
which is missing its head, has not and
probably can not be identified to species.

Ever since the first reports of color from the skin and feathers of dinosaur fossils were published in Science in 2010, I've been fascinated by the ability of paleontologists to see in color when they look into the past. A new paper in the journal Current Biology reveals the color of a fossil snake, determined from using scanning electron microscopy (SEM) to examine microfossils of certain types of skin cells, called chromatophores. So far, only melanin-based chromatophores (melanosomes, which are responsible for brown and black color) have been detected in fossilized skin and feathers, probably because they are the most resistant to the decomposition process. But, this study was also able to detect and measure other types of chromatophores from fossilized skin, including xanthophores (responsible for yellow, orange, or red color, derived from carotenoids or pteridines) and iridophores (responsible for iridescence). By comparing the fossil's chromatophore abundance and position to that of living reptiles, they were able to reconstruct the original color and pattern of the fossil snake's skin. For example, in the skin of living snakes, xanthophores with many more pteridine granules than carotenoid granules produce a red hue, whereas xanthophores with equal amounts of carotenoid granules and pteridine granules—as in the fossil—produce yellowish hues. Skin regions with abundant iridophores and xanthophores, but relatively few melanophores, are associated with green hues in some living skinks, whereas skin regions with many melanophores, a few xanthophores, and no iridophores suggest correspond to dark brown or black tones. As you can see in the depiction, this snake seems to have had a pale, creamy venter and a green back and sides, with areas of brown/black and yellow/green, perhaps not unlike modern Green Watersnakes (Nerodia floridana) or Boomslangs (Dispholidus typus).

Snakes Flying Without Planes

Photo and diagram of courtship behavior of Chrysopelea paradisi
Taken at the Sepilok Jungle Resort in Sabah, Malaysia
Female shown in gray, males in blue, green, and orange
From Kaiser et al. 2016

A new report on the mating behavior of Paradise Flying Snakes (Chrysopelea paradisi) showed that their courtship can involve multiple males. Although several experiments have been performed on the gliding behavior of these snakes, almost nothing is known about their natural history in the wild. Males of many species of snakes court females en masse by rubbing their chins along their bodies, a behavior which allows them to sense her sex pheromones and jockey for position. The role played by the female in choosing a male is unclear in most snake species; although conventional biological wisdom suggests that females should be the choosy sex, male-male competition seems to dominate courtship behavior in several species of snakes. Multi-male courtship behavior precedes mating in some well-studied temperate snakes (e.g., gartersnakes emerging from hibernation), as well as in some tropical species (e.g., anacondas, some other southeast Asian colubrids, such as Boiga irregularis and Dryophiops rubescens). Of course, it seems that most female snakes can store sperm for long periods of time, and they may have some control over which male's sperm to use to fertilize their eggs, so the genetic contribution of a female snake's male partners may not follow from their courtship or mating success. Unlike the terrestrial or aquatic mating balls documented for other snakes, the flyingsnakes in this observation were able to move as a unit for almost 50 feet through complex habitat—under a porch, up a tree—an adaptation that seems to fit their active, arboreal lifestyle and might help reduce the likelihood of a predatory attack during what must otherwise be a vulnerable time.

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1 In a few places, the authors use "alethinophidian" to refer to boas, pythons, and their relatives but not caenophidians, when instead they should have either used "henophidian" or "basal alethinophidian" (they mostly use the latter term throughout). Many people don't like the term "henophidian" because it is a paraphyletic group, but it is a convenient way to refer to non-scolecophidian, non-caenophidian snakes. In my mind it's essentially synonymous with "basal/stem alethinophidian". Alethinophidians are all snakes except for blindsnakes (scolecophidians), and Caenophidia is a subset of Alethinophidia. There are also at least three references to "Caenophidia + Colubroidea", which is confusing because Colubroidea is a subgroup of Caenophidia, and Caenophidia = Colubroidea + Acrochordus, which is perhaps what they meant.^↩

ACKNOWLEDGMENTS

Thanks to Gordon Schuett for clearing up some of the details of his recent paper.

REFERENCES

Booth W, Schuett GW (2016) The emerging phylogenetic pattern of parthenogenesis in snakes. Biological Journal of the Linnaean Society 118:172-186 <link>

Gamble, T., J. Coryell, T. Ezaz, J. Lynch, D. Scantlebury, and D. Zarkower. 2015. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Molecular Biology and Evolution 32:1296-1309 <link>

Kaiser H, Lim J, Worth H, O’Shea M (2016) Tangled skeins: a first report of non-captive mating behavior in the Southeast Asian Paradise Flying Snake (Reptilia: Squamata: Colubridae: Chrysopelea paradisi). Journal of Threatened Taxa 8:8488–8494 <link>

Kuriyama, T., K. Miyaji, M. Sugimoto, and M. Hasegawa. 2006. Ultrastructure of the Dermal Chromatophores in a Lizard (Scincidae: Plestiodon latiscutatus) with Conspicuous Body and Tail Coloration. Zoological Science 23:793-799 <link>

Li, Q., K. Q. Gao, J. Vinther, M. D. Shawkey, J. A. Clarke, L. D’Alba, Q. Meng, D. E. G. Briggs, and R. O. Prum. 2010. Plumage color patterns of an extinct dinosaur. Science 327:1369 <link>

McNamara, Maria E., Patrick J. Orr, Stuart L. Kearns, L. Alcalá, P. Anadón, and E. Peñalver. 2016. Reconstructing Carotenoid-Based and Structural Coloration in Fossil Skin. Current Biology <link>

McNamara, M. E., D. E. G. Briggs, P. J. Orr, D. J. Field, and Z. Wang. 2013. Experimental maturation of feathers: implications for reconstructions of fossil feather colour. Biology Letters 9 <link>

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Snakes that are Good Parents

Click here to read this article in Spanish
Haga clic aquí para leer este artículo en español

Almost all mammals and birds care for their young to some extent, but most amphibians and reptiles do not. We tend to think of snakes as particularly asocial, and in many cases this is probably true. But, a growing body of evidence contradicts the generalization, made as recently as 1978, that "all reptiles produce precocial offspring without postnatal parental care", and shows that some snakes, in particular, are more caring parents than we typically think.

Vipers

A female Timber Rattlesnake (Crotalus horridus)
with her newly-born young

Probably the group of snakes most well-known for parental care are now the vipers, which is somewhat ironic considering the fierce but undeserved reputation of these venomous snakes. Although it was documented as early as 1850, parental care by vipers was not widely known or accepted by the scientific community until the 1990s; like crocodilians, it was assumed that these animals were too vicious to exhibit such caring behavior. When Laurence Klauber, at the time the world's foremost authority on rattlesnakes, wrote in 1956 that "Their propinquity [to aggregate]...does not result from any maternal solicitude; rather it is only because the refuge sought by the mother is also used as a hiding place by the young.", he was uncharacteristically incorrect; in hindsight, his words now seem almost willfully ignorant. In the 1990s, credible reports of parental care in wild pitvipers began to accumulate, corroborating the many older stories listed by Klauber, and in 2002, a seminal review paper based around two studies using radio-telemetry and DNA proved once and for all that mother rattlesnakes do stay with and care for their young. Today, you can read a whole blog about parental care in rattlesnakes, and we think that parental care is widespread (but not ubiquitous) among the ~230 species of pitvipers (aka crotalines or New World vipers). This is particularly remarkable because many of them give birth to live young, which they guard until the young's first shed, even though they may not have eaten for 9-10 months beforehand. It appears that the completion of the first shed cycle is the cue for them to separate, an event which is mediated by the same hormone in snakes as it is in birds and mammals. Because snakes swallow their food whole, the mother can't really feed her offspring, and they forage for themselves after they disperse. Pitvipers are the only snakes known to care for their living young; other snakes with parental care limit themselves to care of their eggs.

Pythons

A mother African Rock Python (Python sebae)
brooding her eggs

The next most well-known example of parental care in snakes is egg-brooding behavior in pythons, first documented in 1835. All 40 species of pythons lay eggs, and most of them coil tightly around them throughout incubation, forsaking food. As with vipers, early reports of this behavior were dismissed, but by the 1930s observations of pythons in zoos showed that they did indeed brood their eggs. Some species that live in cold climates, such as Indian Pythons (Python molurus) and Carpet Pythons (Morelia spilota), also generate heat using muscle contractions ("shivering"). Measurements taken of brooding Indian Pythons have shown that they can increase the temperature of their clutch by 7-10°F. Even though mother pythons may brood for up to 2 months, studies have found that, at normal temperatures, they rarely shiver and lose only about 6% of their body mass, suggesting that the costs of brooding are relatively small compared to the benefits, which also include reduced water loss by the eggs and hatchlings that develop faster and are larger and more active. The brooding instinct in mother pythons is very strong—lab experiments have shown that they will brood the eggs of other pythons just as readily as they will brood their own, and they will even brood rocks that are the same size as their eggs (a behavior reminiscent of the well-known fixed-action pattern of egg-retrieval behavior in graylag geese). Today, pythons are frequently used as models to study female reproductive behavior and life-history trade-offs.

King Cobras

Top: A female King Cobra guarding her nest
Bottom left: A diagram of a typical King Cobra nest
Bottom right: King Cobra eggs in an excavated nest chamber
From Hrima et al. 2014

That female King Cobras (Ophiophagus hannah) use their coils to build a nest of sticks and bamboo leaves and guard their eggs for two to three months has been known at least since 1892¹. Detailed observation of nest-building and attendance were made in captivity at the Bronx Zoo from 1953-1956, and wild King Cobra nests were surveyed and detailed observations made in 1969². King Cobra nests are the largest and most complex of any snake's, measuring up to four feet in diameter and rising to a similar height, with an internal chamber for the 20-50 eggs and sometimes a second one above for the snake, which abandons the nest just before the eggs hatch. The female must select her nesting material and bring it to the nest site, because the species of bamboo that are most commonly used in building the nest are not the most abundant species in the surrounding area. There are also some anecdotal reports that male King Cobras will guard the nest and/or the female. Some sources suggest that female King Cobras are more aggressive towards humans when they are guarding their nests, but most suggest that their behavior is no different than at any other time.

Other snakes

A female Mudsnake (Farancia abacura)
coils around her eggs in a subterranean nest

Maternal attendance or guarding of clutches of eggs is widespread in snakes, but observations in the wild are still fairly uncommon, mostly due to the difficulty of locating nesting sites. There are several excellent reviews of this topic, including those written by Rick Shine (1988), Carl Gans (1996), Louis Somma (2003), and Zach Stahlschmidt and Dale DeNardo (2011).

Other snakes that have been observed guarding their eggs in the wild include:

• Other species of true cobras (King Cobras are more closely related to mambas), such as Shield-nosed Cobras (Aspidelaps scutatus) and some Asian cobras (genus Naja). Unlike King Cobras, they do not build nests but some may dig holes or enlarge existing holes.
• Other elapids, including kraits (genus Bungarus), coralsnakes (genus Micrurus), and possibly some sea snakes (genus Laticauda) and terrestrial Australian elapids (genera Demansia, Pseudechis, and Pseudonaja).
• Mud and Rainbow Snakes (genus Farancia), which spend most of their lives in water but lay and brood their eggs on land.
• South American Pondsnakes (Pseudoeryx plicatilis), which are also interesting because they are part of a lineage that is close to an evolutionary transition between egg-laying and live-bearing
• Malagasy Hog-nosed Snakes (Leioheterodon madagascarensis), which may leave their nest and return several times over a period of a few months.
• Rhombic Skaapstekers (Psammophylax rhombeatus), which guard their eggs under rocks in southern African grasslands, and possibly other species of Psammophylax as well.
• New Mexico Blindsnakes (Rena dissecta), which have been found with their eggs in small colonies in sandstone in Kansas. There are hints of parental care in other blindsnakes as well.

It's worth noting that, unlike the case with pythons, survival or physiological benefits to the eggs have not been documented in any of these cases. In addition, there are numerous anecdotal reports of egg attendance in other snakes, many of which are based on hearsay and are not backed up by data, photographs, or even descriptions. So, expect this list to grow, but keep in mind that parental care in snakes is still, and will probably always be, the exception rather than the rule.

Costs and benefits

Except for pythons and pitvipers, the costs and benefits of parental care in snakes have not been examined, and I've mentioned some of the evidence for both in pythons already. Why do rattlesnakes and other pitvipers care for their eggs or young? There are several non-mutually-exclusive theories, including:

A mother Pigmy Rattlesnake (Sistrurus miliarius) with
her brood. Because rattlesnake rattles are made of segments
that form each time the snake sheds its skin, newborn snakes
have only one segment and cannot yet make sound.

1. To protect them from predators. This might involve any or all of the following:

• Physical concealment, especially of the eggs, which are less well-camouflaged than the adults.
• Deterrence of predators, which may recognize an adult viper as a threat but not an egg or a juvenile.
• Active defense from predators, using venom or the threat thereof. This may be especially important prior to the first shed of the young, since they would probably suffer their heaviest mortality during this stage because of their small size, inexperience, hampered eyesight and pit organ sensitivity, and, in rattlesnakes, their inability to use their rattle.
• Socially-facilitated retreat from predators, in which the parent helps the young escape an attack by physically moving them, showing them what to do, or distracting the predator. These may seem like surprisingly sophisticated behaviors for snakes, but several observations of mother snakes and their young support this idea, and we are learning that many snakes have subtle but complex social lives and communication abilities that have long been underappreciated.

Antipredator benefits of parental care in snakes may vary geographically or in other ways, because some species of pitvipers do not seem to change their defensive behavior when they are guarding their young, but others are more defensive, and still others are less defensive but more distracting.

Young Tiger Snakes (Notechis scutatus) snuggling
and data showing that the more litter-mates
they snuggle with, the more slowly they cool off
From Aubret & Shine 2009

2. Litters or clutches of several species of young snakes, including some rattlesnakes, aggregate together, without their mothers, in order to conserve water or heat—which, if they were mammals, we would call snuggling. Experiments have shown that they prefer to snuggle—sorry, I mean aggregate—inside shelters that contain their own scent cues, and that snuggling kept them warm, which helped them slither to shelter faster. No one has tested whether young pitvipers that snuggle with their mothers have higher body temperatures or lower rates of evaporative water loss than those snuggling with one another, but physics suggests that they would, since larger animals have a lower surface-area-to-volume ratio and thus lose heat and water more slowly. The presence of the mother may also offset the increased visibility or olfactory conspicuousness to predators of a bunch of aggregated young snakes. If this is the primary benefit, it is easy to see how maternal attendance of eggs could evolve into maternal attendance of the young, because we think that live birth has evolved many times in snakes, and parental care may have evolved and been lost as many as six and ten times, respectively, in vipers. It's probable that we will continue to fill in the gaps in our knowledge. For example, perhaps we're overlooking the behavior in some poorly-studied vipers, as we did in North American pitvipers for over a century.

Viper family tree showing the evolution of parental care.
A few details have changed but the basic shape of the tree
is the same. Abbreviations: O=oviparous, V=viviparous;
Tr=tropical, Te=temperate. From Greene et al. 2002

3. The week or so of parental care may represent an imprinting period for the young snakes to learn the scent of their mother and of one another, similar to the time a young sea turtle spends imprinting on its natal beach or a young salmon on its natal stream. This would be especially important for snakes in cold climates because they use each others' scent trails to locate hibernation sites. Although there is no direct evidence for the third hypothesis, it is suggestive that, at least in the Americas, temperate pitvipers stay with their young, but live-bearing tropical pitvipers, which do not need to hibernate, do not³. Other explanations include that memories of their siblings' scents help young snakes avoid inbreeding later in life, or that they promote other social behaviors, such as communal basking. Some new data suggest that the adult behavior of pitvipers differs when they are deprived of a maternal attendance period. Tall tales about snakes abound, and initially social behavior ranked among them (there are still false tales about parental behavior in snakes, such as the idea that they swallow their young). Parental care in vipers may just be the tip of their social iceberg. Research over the last decade has shown that vipers make use of chemical information left behind by other vipers when they choose their foraging sites, like a dog sniffing a fire hydrant. This kind of cryptic sociality in snakes can lead to things like inheritance of birthing rookeries, nesting sites, and hibernation sites over many generations. Some research even suggests that pair-bonding might happen between male and female copperheads. Some lizards build multi-generational homes; might we one day discover snakes doing the same? If we do, my money is on vipers.

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1 Rudyard Kipling's The Jungle Book, containing the story Rikki Tikki Tavi, which describes a King Cobra pair, nest, and parental behavior, was originally published in 1893-4, just a year later.^↩

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2 The Kenyan herpetologist J.H.E. Leakey collected eggs from these nests and acknowledged in his paper the support of "the management of the International Hotel, who never once raised any objections to our housing live King Cobras in our rooms."^↩

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3 Intriguingly, the only two Neotropical pitvipers known to have parental care are also the only two that lay eggs. One is the Colombian toad-headed pitviper (Bothrops colombianus), about which very little is known. The other, the Bushmaster (Lachesis muta), well-known by comparison, is nevertheless a secretive denizen of primary rain forests. In 1910, Inaugural Bronx Zoo herp curator Raymond Ditmars and his Trinidad correspondent, R. R. Mole, were the first to publish a photograph of a female Bushmaster guarding her eggs. They wrote of Bushmasters guarding their eggs in the wild, and numerous subsequent captive snakes have borne these observations out. Although Eyelash Pitvipers (Bothriechis schlegelii) have not been observed to guard their young, they may do so because their young shed several days after birth, like those of temperate pitvipers, rather than within 24 hours of birth, like most tropical live-bearing pitvipers. The pattern of parental care in Old World vipers, about which we have far less information, appears to be more complicated still.^↩

ACKNOWLEDGMENTS

Thanks to my parents, for indulging my interest in snakes and encouraging me to pursue a career studying them, and to Jim Williams, Peter May, J. Lanki, and Matt Nordgren for the use of their photos.

REFERENCES

Aubret, F., X. Bonnet, R. Shine, and S. Maumelat. 2005. Energy expenditure for parental care may be trivial for brooding pythons, Python regius. Animal Behaviour 69:1043-1053 <link>

Aubret, F., X. Bonnet, R. Shine, and S. Maumelat. 2005. Why do female ball pythons (Python regius) coil so tightly around their eggs? Evolutionary Ecology Research 7:743-758 <link>

Aubret, F., and R. Shine. 2009. Causes and consequences of aggregation by neonatal tiger snakes (Notechis scutatus, Elapidae). Austral Ecology 34:210-217 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Can snakes hear?

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Last month I wrote about whether snakes sleep, a topic that is far more interesting than the minuscule amount of research devoted to it. Another common question is whether snakes can hear, since they don't have external ear openings. The short answer is yes, snakes can hear, but the long answer is (as usual) more complicated. Happily, there is a good deal of research on this question, including a recent review. In general, many popular sources and some scientific ones have incorrectly claimed snakes to be deaf, whereas a plethora of behavioral, neurological, and physiological experiments, particularly those performed by the eminent Princeton hearing researcher Ernest Glen Wever in the 1960s and 70s, by UC-San Diego neurologist Peter Hartline in the 1970s, and by herpetologist and anatomist Bruce Young from the 1990s to the present, have conclusively shown that snakes can detect and respond to sounds.

Anatomy of the human ear

Most tetrapods have a three-part ear (outer, middle, and inner) that is useful for detecting airborne sounds. The boundary between the outer and middle ear is called the tympanic membrane or "ear drum", and its function is to convert airborne sounds from the outer ear into fluid-borne ones in the inner ear¹, by way of one or more middle ear bones. Sounds are ultimately converted by auditory hair cells called stereocilia into nerve impulses, which travel to and are interpreted by the brain. At many stages along the way, the sounds are amplified by the vibrations they produce in the different parts of the ear, including the middle ear bones (more on these in a minute). It's been suggested that this three-part system evolved (possibly multiple times) around the beginning of the Triassic Period, in concert with the evolution of sound production in insects, the probable prey of many early amniotes. Many modern animals, such as songbirds, bats, dolphins, humans, frogs, and crocodilians, have very sensitive hearing that can detect extremely quiet airborne signals in spite of the presence of other competing noises.

Micro-CT scan of a ball python's skull and ear.
Red: mandible; dark blue: quadrate;
green: columella; purple/light blue: inner ear chambers
From Christensen et al. 2012
Click here for an interactive 3-D model.

You're probably familiar with the three bones of the middle ear in mammals, the malleus, incus, and stapes (also known as the hammer, anvil, and stirrup). Snakes and other reptiles have only a single middle ear bone, which is usually called the columella, although it is homologous with the mammalian stapes. The malleus and the incus evolved from the articular and quadrate bones in the lower jaw of early mammal-like reptiles, leaving modern mammals with a single lower jaw bone, the dentary. Modern reptiles still have three bones in their lower jaws, where they play a role in detecting vibrations, particularly those propagating through the ground. Most modern lizard ears are essentially like those of modern mammals, with a small external ear leading to a large ear drum close to the body's surface, which passes sound from the air (or the jawbones) to the columella and thence to the inner ear. In contrast, snakes lack all traces of an outer ear as well as an ear drum. Instead, a snake's columella is in direct contact with, and picks up vibrations from, its quadrate bone (the dark blue bone in the diagram above). You might suspect that this arrangement would only be useful for detecting ground-borne vibrations, and you'd be partially right: snakes are exquisitely sensitive to ground-borne vibrations. But, they can also detect airborne sounds.²

Diagram of the ear of a watersnake (Nerodia)
Modified from Wever 1978

Both older and several more recent experiments suggest that snakes can hear the vibrations produced by airborne sounds. Physiological data suggest that they are able to detect certain airborne frequencies directly using the inner ear, although the specific bioacoustic mechanisms remain poorly known. Instead, most airborne sounds are probably detected in using "somatic hearing". This happens when airborne sound waves strike a snake's body  and some of their energy is transferred to its bones, tissues, and organs, particularly the head and lung. The snake's vibration-sensitive hearing system can then pick up on and translate the vibrations from the rest of its body into fluid-borne vibrations and, ultimately, nerve impulses. So a snake probably can't hear, say, most music³ or human speech directly, but it can hear the sound of its own body vibrating in response to those sounds. So, instead of being deaf, snakes essentially have two auditory systems that are at least peripherally distinct. Whether signals from these two systems are integrated into a single neural pathway, as is the case for the eye and the pit organ, or whether they serve different functions, remains to be studied and determined.

The length and arrangement of the auditory hairs in the inner ears of snakes appears to be fairly uniform across species, at least relative to the variation seen in lizards, which can have very different auditory hair anatomy among families and often even among closely-related species. Snakes mostly have simple, tuatara-like papillae, which suggests that they have secondarily lost a more complex type of auditory organ. This might be due to the aquatic or burrowing lifestyle of their ancestors and/or to specializations of their lower jaws in response to their unusual eating habits. There is some variation in inner ear anatomy (and presumably in hearing capacity) among snakes: burrowing snakes have the longest papillae, arboreal snakes the shortest, and terrestrial snakes have papillae of intermediate length. Many mammals have over 10,000 auditory hair cells, whereas most snakes have only about 250 (although acrochordids have nearly 1,500). Supporting cells of unclear function are relatively more numerous in snakes and these cells have ultrastructural features that suggest that they are more specialized than those of other reptiles.

Hearing range of various animals, not including snakes

The louder and lower frequency airborne sounds are, the more easily a snake can detect them. This isn't entirely unlike our own hearing—although we do hear high-pitched airborne sounds directly more easily than snakes do, we also rely on amplification provided by our ear drums, inner ear hairs, and other parts of our bodies. Studies have shown that snakes can hear sounds in the 80-600 Hz range optimally, with some species hearing sounds up to 1000 Hz (for comparison, the range of human hearing is from 20-20,000 Hz). This means that a snake could hear middle C on a piano, as well as about one octave above and two below, but neither the lowest key (which is 27.5 Hz) nor the highest (which is 4186 Hz). The average human voice is around 250 Hz, which means that snakes can hear us talking as well. Of course, there is likely a lot of variation among snake species, and the hearing of most species has not been examined, so these are generalizations.

Use the player above to hear how the airborne parts of Led Zeppelin's classic "Good Times, Bad Times" would sound to a snake. Parts of the song below 80 Hz (some bass & drums) or above 600 Hz (almost all guitar, vocals, and cymbals) have been muted. This doesn't include their sensitivity to the groundborne vibration parts of the song, which you could simulate by turning the bass on your speakers all the way up.

Audibility curves for living reptiles, including birds (left). The lower
the curve, the quieter a sound can be detected at a given frequency.
You can see that snakes cannot hear very quiet sounds, but
otherwise are not that much worse than other reptiles
(although their hearing sucks compared to, say, owls).
Note the different y-axes. From Dooling et al. 2000.

What do snakes do with their hearing? Unlike frogs, birds, and insects, snakes don't seem to use sound for communication with each other. Although many snakes hiss and some use tail rattling, growling, scale rubbing, or cloacal popping to send messages to their would-be predators, these sounds are mostly above 2,500 Hz, so the snakes themselves cannot hear them. Some species are capable of producing sounds whose frequency overlaps with their hearing range, such as the loud, robust hisses of pinesnakes and gophersnakes (Pituophis), the bizarre and intimidating growling sounds of king cobras (Ophiophagus), and the famous rattles of some large rattlesnakes (Crotalus). Some people have suggested that rattlesnakes find their hibernacula by following the rattling sounds of other rattlesnakes, but this idea has been disproven because the power output of rattling is insufficient to serve as a long-distance signal, and playback experiments have not yielded a behavioral response to rattling.

Snakes might eavesdrop on the alarm calls of other, more vocal animals, as some lizards do with bird alarm calls, but probably not since most of these calls are between 2,500 and 10,000 Hz, well above their optimal frequency range. Most likely, snakes use their hearing to monitor their environment for sounds produced by approaching predators or prey, many of which are ground-borne vibrations. Snakes can hear in stereo and can use their hearing to determine the directionality and thereby the sources of sounds. One genus of snakes that probably relies quite heavily on vibration to hunt are Saharan sand vipers (Cerastes). These snakes ambush lizards and rodents from a position partially or completely buried in sand. Experiments have shown that their reliance on chemosensing and thermal cues was minimal and that, although snakes with their eyes obscured had altered strike kinematics, they were still able to capture prey.