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.

---

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.^↩

---

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."^↩

---

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>

Bates, M. F. 1985. Notes on egg clutches in Lamprophis inornatus and Psammophylax rhombeatus rhombeatus. The Journal of the Herpetological Association of Africa 31:21-22.

Benedict, F. G., E. L. Fox, and V. Coropatchinsky. 1932. The incubating python: a temperature study. Proceedings of the National Academy of Sciences 18:209-212 <link>

Brashears, J., and D. F. DeNardo. 2012. Do brooding pythons recognize their clutches? Investigating external cues for offspring recognition in the Children's Python, Antaresia childreni. Ethology 118:793-798 <link>

Brown, G. P., and R. Shine. 2007. Like mother, like daughter: inheritance of nest-site location in snakes. Biology Letters 3:131-133 <link>

Brown, W. S., and F. M. MacLean. 1983. Conspecific scent-trailing by newborn timber rattlesnakes, Crotalus horridus. Herpetologica 39:430-436 <link>

Butler, J.A., T.W. Hull, and R. Franz. 1995. Neonate aggregations and maternal attendance of young in the Eastern Diamondback Rattlesnake, Crotalus adamanteus. Copeia 1995:196–198 <link>

Campbell, J. A., and W. W. Lamar. 1992. The taxonomic status of miscellaneous Neotropical viperids, with the description of a new genus. Occasional Papers of the Museum, Texas Tech University 153:1-31 <link>

Case, T. J. 1978. Endothermy and parental care in the terrestrial vertebrates. American Naturalist 112:861-874 <link>

Clark, R. W. 2007. Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites. Behavioral Ecology 18:487-490 <link>

Clark, R. W., W. S. Brown, R. Stechert, and H. W. Greene. 2012. Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis. Biology Letters 8:523-525 <link>

Cunningham, G. R., S. M. Hickey, and C. M. Gowen. 1996. Crotalus viridis viridis (Prairie Rattlesnake). Behavior. Herpetological Review 27:24 <link>

DeNardo, D. F., O. Lourdais, and Z. R. Stahlschmidt. 2012. Are females maternal manipulators, selfish mothers, or both? Insight from pythons. Herpetologica 68:299-307 <link>

Gans, C. 1996. An overview of parental care among the Reptilia. Pages 145-157 in J. S. Rosenblatt and C. T. Snowdon, editors. Parental Care: Evolution, Mechanisms, and Adaptive Significance. Academic Press, San Diego, California, USA <link>

Graves, B. M. 1989. Defensive behavior of female prairie rattlesnakes (Crotalus viridis) changes after parturition. Copeia 1989:791-794 <link>

Greene, H.W., P.G. May, D.L. Hardy, J.M. Sciturro, and T.M. Farrell. 2002. Parental behavior by vipers. Pp. 179-206 In Biology of the Vipers. Schuett, G.W., M. Höggren, M.E. Douglas, and H.W. Greene (Eds.).  Eagle Mountain Publishers, Eagle Mountain, UT <link>

Hibbard, C. W. 1964. A brooding colony of the blind snake, Leptotyphlops dulcis dissecta. Copeia 1964:222 <link>

Hoss, S.K. and R.W. Clark. 2014. Mother Cottonmouths (Agkistrodon piscivorus) alter their antipredator behavior in the presence of neonates. Ethology 120:933-941 <link>

Hoss, S. K., D. H. Deutschman, W. Booth, and R. W. Clark. 2015. Post-birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance. Biological Journal of the Linnean Society 116:637-648 <link>

Hoss, S.K., M.J. Garcia, R.L. Earley, and R.W. Clark. 2014. Fine-scale hormonal patterns associated with birth and maternal care in the cottonmouth (Agkistrodon piscivorus), a North American pitviper snake. General and Comparative Endocrinology 208:85-93 <link>

Leakey, J. 1969. Observations made on king cobras in Thailand during May 1966. Journal of the National Research Council of Thailand 5:1-10 <link>

Mori, A., and T. M. Randriamboavonjy. 2010. Field observation of maternal attendance of eggs in a Madagascan snake, Leioheterodon madagascariensis. Current Herpetology 29:91-95 <link>

Oliver, J. A. 1956. Reproduction in the king cobra, Ophiophagus hannah Cantor. Zoologica 41:145-152.

Reiserer, R., G. Schuett, and R. Earley. 2008. Dynamic aggregations of newborn sibling rattlesnakes exhibit stable thermoregulatory properties. Journal of Zoology 274:277-283 <link>

Savary, W. 1999. Crotalus molossus molossus (northern blacktail rattlesnake). Brood defense. Herpetological Review 30:45 <link>

Schuett, G., R. Repp, M. Amarello, and C. Smith. 2013. Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy. Journal of Zoology 289:101-110 <link>

Shine, R. 1988. Parental care in reptiles. Pp. 275-330 In Biology of the Reptilia. Gans, C. and R.B. Huey (Eds.).  Alan Liss, New York <link>

Smith, C. F., and G. W. Schuett. 2015. Putative pair-bonding in Agkistrodon contortrix (Copperhead). Northeastern Naturalist 22:N1-N5 <link>

Somma, L. A. 2003a. Parental Behavior in Lepidosaurian and Testudinian Reptiles: A Literature Survey. Krieger Publishing Company, Malabar, Florida, USA.

Somma, L. A. 2003b. Reptilian parental behaviour. The Linnean 19:42-44 <link>

Stahlschmidt, Z.R. and D.F. DeNardo. 2011. Parental care in snakes. Pp. 673-702 In Reproductive Biology and Phylogeny of Snakes. Aldridge, R.D. and D.M. Sever (Eds.).  Science Publishers, Enfield, New Hampshire <link>

van Mierop, L. H. S., and E. L. Bessette. 1981. Reproduction of the ball python, Python regius in captivity. Herpetological Review 12:20-22 <link>

Wall, F. 1924. The Hamadryad or King Cobra, Naja hannah (Cantor). Journal of the Bombay Natural History Society 30:189-195 <link>

Walters, A. C., and W. Card. 1996. Agkistrodon piscivorus conanti (Florida Cottonmouth). Brood defense. Herpetological Review 27:203 <link>

Wasey, G. K. 1892. A nest of King Cobra's eggs. Journal of the Bombay Natural History Society 7:257 <link>

Whitaker, N., P. G. Shankar, and R. Whitaker. 2013. Nesting ecology of the King Cobra (Ophiophagus hannah) in India. Hamadryad 36:101-107.

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 polish their scales, and why they do it

Click here to view the Spanish translation of this article!

Haga clic aquí para ver la traducción al español de este artículo!

Psammophis schokari eating a lizard, Phrynocephalus
mystaceus, in Kazakhstan

I really like these snakes, and they have about them a pretty interesting mystery. In the tribe Psammophiini (in family Lamprophiidae), there are at least 50 species of snake in 8 genera native to Africa, the Mediterranean, the Middle East, and central Asia. They are united by several unusual synapomorphies, the most unique of which is the presence of a morphological feature called the external narial valve. This structure, located in the loreal region between the eye and the nostril, is the outlet of a special nasal gland that secretes fluid containing long-chain fatty acids. The function of this secretion is enigmatic. Some experiments show that it can serve to retard evaporative water loss, and some evidence suggests that some of these molecules could be pheromones used in marking territories. Territoriality is only slightly less non-existent among snakes than herbivory, but according to some it is apparently present among certain psammophines, few of which have been well-studied in the wild. Aside from a very interesting study suggesting that releasing small mammals from competition with large herbivores can indirectly increase the abundance of their snake predators (including Psammophis mossambicus), we don't know much about their ecology, but careful observations have revealed a little about the lives of these intriguing snakes.

Subadult Montpellier snake, Malpolon monspessulanus

The external narial valve was described in 1956 by renowned Russian herpetologist Ilya Darevsky, the second person ever to earn a PhD in the Soviet Union and the discoverer of parthenogenesis and polyploidy in reptiles. Darevsky described the gland from a specimen of the Montpellier snake (Malpolon monspessulanus), and such glands have now been reported from all eight genera in the Psammophini. In addition to the gland, psammophines also share peculiar hemipene morphology - that is, the male reproductive organs are unusually thin and smooth for an advanced snake, most of which possess thick, spiny hemipenes that enable prolonged copulation. Sexual dimorphism is also quite pronounced in many of these snakes, although not of tail length (typically, the tails of male snakes are longer and thicker than those of females). For example, male M. monspessulanus are stout, uniformly colored, and up to 2.3 m long, whereas females are slender, spotted, and reach only 1.4 meters.

Beginning in 1898, the earliest observations of these snakes mention their peculiar behavior. Psammophines press the outlet of their narial valve to their skin and thoroughly apply a coating of colorless, fast-drying valve secretion all over their body. Watch this Malpolon insignitus to get an idea, because it's hard to describe.

This behavior has been variously called self-rubbing, self-polishing, or  grooming, and seems to be present in all species of psammophine observed. Several keepers in Europe have made extensive efforts to acquire and videotape species of psammophines, and self-rubbing has now been documented in seven of the eight genera. More intriguing, conspecific psammophines housed together occasionally rub one another, presumably anointing the other snake with secretion from their narial valve. What could this mean?

Psammophis leightoni from Namibia

Several hypotheses have been put forth to explain this unique and intriguing behavior. To date, none have been sufficiently tested to unequivocality, nor are they mutually exclusive. Prior to the 1970s, the prevailing thought was that, since psammophines generally inhabit arid regions, the gland might aid in salt excretion, evaporative cooling, or water retention. In 1978, William Dunson and colleagues published their work on the histology of the gland, and concluded that it did not contain the specialized cytological features associated with salt secretion in the salt glands of reptiles such as sea snakes and marine iguanas. Dunson also characterized the chemical composition of the secretion for the first time, and suggested that the long-chain fatty acids he found might help retard water loss through the skin.

Dunson tested five Malpolon to see if their dermal water loss was unusually low, and indeed it was, approximately ten times lower than that of Kingsnakes (Lampropeltis getula), although water loss rate varied depending on where in the shedding cycle the snakes were. Malpolon also lost proportionally more water via the mouth and cloaca (and less via the skin) than did other reptiles. Dunson also kept Malpolon without giving them access to water, and they did not lose weight, indicating that they were capable of obtaining all the water they needed from their prey. In another experiment, he showed that dehydrated Malpolon did not secrete salt from their narial valve. He made the interesting observation that several frog species of the genus Phyllomedusa decrease their dermal water loss by wiping lipid secretions from skin glands over the surface of their skin:

Could psammophids be accomplishing the same thing with their narial valve secretions? Dunson did not test whether snakes that had just applied the secretion lost less water than those that had not. The snakes polish themselves frequently, especially after ecdyisis and feeding, so water loss rate could be tracked over time. 

Other mysterious pits have been described from the head scales of psammophines: parietal pits on the top of the head and infralabial pits on the lower jaw, both of which seem to be sporadically occurring. Series of shed skins from the very same snake sometimes show these features and sometimes do not. Because histology is lacking for these features, it is difficult to say what they might represent.

Dipsina multimaculata

Because of the remote areas inhabited by many of these snakes, most studies to date are insufficiently replicated to permit concrete conclusions about the function of the polishing behavior. Furthermore, determining the sex of living psammophines is quite difficult on account of their small hemipenes, so behavioral studies are often hampered by inadequate knowledge of the sex of the animals involved. Observations of captive psammophines suggest that these snakes have complex social behaviors, not the least of which is their tendency to polish one anothers' scales. Could this behavior represent mate guarding? A nuptial gift from males to females of fatty acids to help them avoid water loss during pregnancy? Do these snakes mark their territories? Only replicated, scientific studies will tell; until then, competing hypotheses will continue to wax on and wax off.

ACKNOWLEDGMENTS

Thanks to Heather Heinz for drawing my attention to this fascinating system, to Jane Bugaeva for translating Darevsky's 1956 article from Russian, and to photographers Bernard Dupont, Altyn Emel, Michael & Patricia Fogden, and Jeremy Holden, and videographer Ton Steehouder.

REFERENCES

Microdermatoglypic SEM photograph of Dipsina scale.
The lipid layer covering the scale is visible.
From de Pury 2010

Darevsky IS (1956) O stroyenni i funktsionirovani nosovoy zhelezy u yashtsheritsnoy zmei Malpolon monspessulanus Herm. (Reptilia, Serpentes). [On the structure and function of the nasal gland in the lizard snake Malpolon monspessulanus Herm. (Reptilia, Serpentes)] Zoologicheskij Zhurnal-Moskva 35:312-314

Dunson WA, Dunson MK, Keith AD (1978) The nasal gland of the Montpellier snake Malpolon monspessulanus: fine structure, secretion composition, and a possible role in reduction of dermal water loss. Journal of Experimental Zoology 203:461-473

de Grijs P (1898) Beobachtungen an reptilien in der gefangenschaff. Zoologischer Garten 39:233-247

de Haan CC, Aymerich M (2012) Des comportements frotteur et marqueur, pour la chasse et la vie sociale. In: Aymerich M (ed) A la Découverte de la Faune du Maroc Oriental

de Haan CC, A Cluchier (2006). Chemical marking behaviour in the psammophiine snakes Malpolon monspessulanus and Psammophis phillipsi. Proceedings of the 13th Congress of the Societas Europaea Herpetologica, 211-212. <link>

Mimophis mahfalensis killing a chameleon in Madagascar

de Haan CC (2003) Extrabuccal infralabial secretion outlets in Dromophis, Mimophis and Psammophis species (Serpentes, Colubridae, Psammophiini). A probable substitute for ‘self-rubbing’ and cloacal scent gland functions, and a cue for a taxonomic account. Comptes Rendus Biologies 326:275-286. <link>

de Pury S (2010) Analysis of the Rubbing Behaviour of Psammophiids: A Methodological Approach. PhD dissertation, Rheinischen Friedrich-Wilhelms-Universität Bonn, Bonn, Switzerland.

McCauley, D. J., Keesing, F., Young, T. P., Allan, B. F. & Pringle, R. M. 2006: Indirect effects of large herbivores on snakes in an African savanna. Ecology 87, 2657-2663. <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.