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Tuesday, January 31, 2017

Do snakes have a third eye?

This post will soon be available in Spanish

Limerick written by Annie Simminger about her nephew,
Richard Marshall Eakin, and published in his 1983 book The Third Eye.
Eakin and Robert C. Stebbins performed and published many
experiments on the structure and function of the third eyes of lizards
Many lizards have a parietal eye, also known as a third eye or pineal eye. This "eye" is a photosensory organ located on the top of the skull, in the center. It has a well-defined lens, cornea, and retina, and is lined on the inside with photosensitive cells that resemble the cones of the lateral eyes and contain the light-sensitive pigment vitamin A1. These cells are connected by the parietal nerve to the pineal organ in the brain, which produces melatonin2, the hormone that controls sleep patterns, circadian rhythms, and seasonal cycles such as mating, migration, and hibernation. The parietal eye can see light and is primarily used to sense changes in day length. Many lizards have a parietal eye, although it is most well-developed in tuataras, even serving as the inspiration for a New Zealand brewery.



Parietal eye (black outline) and parietal scale (white outline)
of Liolaemus bisignatus (Philippi's Tree Iguana).
From Labra et al. 2010
Recently, a Twitter conversation led me to evaluate the evidence for a parietal eye in snakes. As with many things, you would assume that if lizards have parietal eyes, then snakes have them too, since snakes are just one group of legless lizards. And, as with many things, you'd be wrong (probably; read on). It turns out that studies on the parietal eyes of snakes are almost non-existent. Maybe this isn't surprising, considering how little we know about other basics of snake physiology, like how well they can hear or whether or not they sleep. The evidence for the existence of  a parietal eye in snakes is scant at best, and despite evidence for its absence, "amazingly few species have been studied", just seven as of 1979, and barely any others since then. Detailed studies have been made on the pineal organ of just one species, Natrix natrix, the European Grass Snake, in contrast to a large body of work on the pineal complex of lizards and tuataras. The tale of the evolution of the parietal eye is helpful in understand the assumptions made about snake parietal eyes, in the absence of much direct research on them.

The "chimney-like" pineal foramen of
the extinct 3-foot-long 250 million year old
South African fossil therapsid Hipposaurus.
From Haughton 1929
Tuataras and many lizards have relatively well-developed parietal eyes. These organs face upwards between the parietal bones of the skull, and were it not for their covering of skin they would effectively connect the outside world with the brain (more or less as our "normal" [lateral] eyes do). There are no eyelids, or rather, like the lateral eyes of snakes, there is a fused, clear eyelid. In young lizards, the opening in the skull is large and T-shaped, like the familiar soft fontanelle of an infant human's skull, whereas in adult lizards the opening becomes ossified and may close completely late in life. Some extinct reptiles had bony protuberances around the margins of their parietal eyes: one, Hipposaurus, had a "chimney-like structure". For a long time paleontologists debated whether holes in the parietal bones of fossil skulls were necessarily evidence of ancient parietal eyes. The German-American paleoneurologist and "fossil brain" expert Tilly Edinger3 snarkily wrote that "if one doubts that this association existed also in extinct vertebrates, one may as well doubt that the orbits of fossil skulls contained eyes", because other than lizards and tuatara, no other living animals possess such holes. Many extinct tuatara relatives had even larger and more well-developed parietal eyes than do living tuataras—in some extinct pliosaurs, the opening was as large as 50 mm (2") by 20 mm (almost 1"), whereas in living tuataras it rarely exceeds 3 mm and modern lizards 1 mm. A more useful comparison may be the size of the parietal eye relative to that of the braincase: in living tuataras, this is about 1:7, whereas in living lizards it varies from 1:21 to 1:36 or less. The absence of any traces of musculature in fossil skulls or signs of more a complex past during embryonic development suggests that parietal eyes have never been any more elaborate in structure than they are in modern lizards and tuatara, although the larger parietal eyes of extinct reptiles were probably better at seeing than the tiny ones of living species.

Endocast of the brain of the dog-sized 250-million-year-old
dicynodont Lystrosaurus, the "humble badass of the Triassic",
showing the large parietal eye (dark structure at the top).
From Edinger 1955
Iguanids, agamids, varanids, cordylids, lacertids, and shinisaurids are diurnal, surface-active lizards that have well-developed parietal eyes. Several families of lizards that are mostly nocturnal and/or spend a great deal of time underneath cover or beneath the ground also have parietal eyes, including scincids, anguids, anniellids, xantusiids, amphisbaenids, and xenosaurids. Chameleons have a degenerated parietal eye that lies above the foramen; presumably it is redundant with the lateral eyes of chameleons, which can move independently and cover 180° horizontally and 90° vertically. Some surface-active (teiids). burrowing (dibamids), and intermediate nocturnal (geckos) and diurnal (helodermatids and lanthanotids) lineages lack parietal eyes. Many of the lizard genera lacking a parietal eye have more equatorial geographic distributions. It has been suggested that a long evolutionary history in the tropics could lead to the loss of the parietal eye, because changes in day length are so minor close to the Equator. Even though there are seasons in the tropics (normally wet and dry), they are not associated with day length or light level cues that animals could use to know when the switch between the two is going to happen (and alter their lifestyles accordingly). There are no truly polar reptiles or amphibians, but some polar mammals (e.g., walruses, Weddell seals) have unusually large pineal organs, whereas some tropical mammals (e.g., sloths, pangolins) have lost their pineal organs, suggesting that the function of the pineal complex is more important where day length is more variable.

Paired parietal foramina in the parietal (ptl)
bone of a Banded Krait (Bungarus fasciatus)
skull. From Scanlon & Lee 2004
It's thought that the parietal eye is retained in many burrowing lizards because these animals are occasionally exposed to light, and perhaps the parietal eye is a more suitable photoreceptor for a burrower than are lateral eyes, because it is already oriented upwards. If snakes evolved underground, as the leading hypothesis suggests, then it would make sense that they lost their parietal eye. Their normal eyes appear to have lost some muscles and modern surface-dwelling snakes have lost at least two of the five visual pigment (opsin) genes found in other vertebrates. Fossil and modern osteological evidence shows that a median parietal foramen like that of lizards was lost in an ancestor of all snakes (about 125 million years ago) and is not present in any living or fossil snakes. About 60 million years ago, small, laterally paired foramina evolved in early colubroids, and are present in many, but not all, living elapids, viperids and other colubroid groups. As in lizards, these may be present only in juveniles, becoming obliterated externally by bone growth later in life. Snake osteology expert John Scanlon told me that "Nobody, as far as I'm aware, has investigated whether the paired foramina [of snakes] are homologous or functionally similar to the median foramen of basal lepidosaurs [lizards]." The loss of parietal eyes is also supported by developmental formation and then fusion with the pineal gland in embryonic snakes, birds, and mammals4.

Developmental origins of the parietal ("median") eye and the lateral eye.
The cilia are cellular structures that normally function for movement
(e.g., of debris out of the nose, of water over gills, of eggs into oviducts,
of sperm cells to the egg). In the eye, they have evolved into photoreceptors.
So, snakes join most mammals, birds, turtles, and most amphibians5 in having lost their parietal eyes but retaining a photosensitive pineal organ in the brain that is not directly exposed to the outside of the skull. However, a recent review of the function of the pineal complex in reptiles states that the pineal gland of adult snakes does not contain photoreceptor-like cells. Instead, the principal cells are pineal parenchymal cells, which secrete melatonin but do not sense light. Nevertheless, experiments on gartersnakes have shown that removing the pineal organ of male gartersnakes in the fall, before hibernation, alters their melatonin cycle and reduces their courtship behavior when they emerge in the spring, so the pineal organ clearly functions to regulate melatonin and annual cycles in snakes.

Diagram of the lizard parietal eye
From Solessio & Engbretson 1993
At first glance, it doesn't seem to make sense to have a deep brain photoreceptor that isn't connected to the outside world, because it doesn't seem possible for it to be able to sense light or darkness from inside of your skull. But, don't forget that the two lateral eyes allow light to enter the brain; it is this light that the pineal organ is sensing. Humans have pineal organs too, and clearly we have no third eye (except in Greek mythology and Grimm's fairytales). Think of how sleepy you feel when you have to get up before the sun, or how awake you feel when a bright light is turned on at night. This is because your pineal organ senses the ambient light or darkness and adjusts your melatonin levels, telling you (if it's bright) to wake up or (if it's dark) to stay asleep. Melatonin is also synthesized directly by the parietal eye of lizards. Although the pineal organ can only sense light and dark, there is evidence that the the parietal eye can also detect different colors of light, including ultraviolet but not infrared light, and that it may be especially sensitive to the order of appearance of  light of different wavelengths, enabling lizards to detect dawn and dusk with great precision. Detailed anatomical studies have shown that the pineal organs of certain lizards possess either a finger-like projection that extends toward the parietal eye, or convolutions of the pineal wall, both of which result in exposing and orienting more photoreceptor cells towards the skull roof, where they can detect light. Although these are sometimes occluded by cartilage or blood sinuses, their existence suggests that the pineal organ of lizards is a more important photoreceptor than previously realized.

Comparative morphology of the pineal complex in A) lamprey,
B) frog, C) lizard, and D) human. From Edinger 1955
The parietal eye of a Western Fence Lizard (Sceloporus occidentalis)
C = cornea; CC = connective tissue; L = lumen;
LS = lens; PN = parietal nerve; R = retina
Light micrograph from Eakin 1970
Many hypotheses have been put forth to explain the exact function of the parietal eye, which in some ways is still unclear. Rejected hypotheses include that the parietal eye is used for detection or deterrence of aerial predators. Even in tuataras, the parietal eye is barely noticeable (it wasn't described until the 1870s), so predator deterrence is unlikely. It may play a minor role in predator detection, because the photoreceptive cells can respond to changes in light intensity as quickly as those of the lateral eyes, but sending sleepiness signals by initiating a melatonin cascade would be counterproductive to predator avoidance, to say the least. The most straightforward hypothesis is that it measures light intensity, functioning in regulating seasonal seasonal behaviorphysiology, and thermoregulation. Although reptiles do have thermally sensitive neurons in their brains, we now know that the pineal complex does not directly sense heat. Instead, reptiles have specially-adapted transient receptor potential ion channels (TRPs), which are proteins found throughout the body that act as internal thermometers and external temperatures sensors. Blocking the genes that make these proteins causes crocodiles to abandon their typical regime of behavioral thermoregulation and leads to significantly altered body temperature patterns. Changes in melatonin levels also affect the body temperatures selected by some reptiles, but in opposite ways in lacertids and iguanids. There is also a great deal of evidence that the parietal eye is sensitive to polarized light: blocking the parietal eye disrupts sun-compass orientation and homing ability of displaced individuals in several lizard species. This makes sense because there is no evidence that lizards can see polarized light with their lateral eyes. 

Parietal spots of a Copperhead
(Agkistrodon contortrix)
One study of thirty species of South American Liolaemus lizards found that parietal eye size did not vary meaningfully with latitude, altitude, environmental temperature, thermal tolerance, or body size, and that there was no evidence of phylogenetic inertia and high intraspecific variation in parietal eye size, suggesting that parietal-eye size may not be under strong selection for accuracy. Another detailed study found that removal of the parietal eye and pineal organ did not prevent 8 species of lizards from four families from carrying out their normal circadian rhythms. They concluded that other photoreceptors within the brain were compensating, although the aforementioned extensions of the pineal organ may also be a factor in the occasional “failure” of parietalectomy experiments. It's actually not clear that we even have enough baseline data on seasonal changes in snake circadian rhythms to correctly interpret the results of experiments that attempted to manipulate the pineal organs of snakes.

Dorsal view of a Copperhead skull, from DigiMorph

Pigmented apical pits of a ratsnake
But could the paired parietal formaina of some snakes function as parietal eyes? The question that started me looking into this was about Copperheads (Agkistrodon contortrix), which usually have a pair of small dark spots on their parietal scales. Evidently a National Geographic documentary called them nostrils, which is totally absurd. But, the spots do seem to be in the approximate location of the parietal foramina in other snakes. The DigiMorph scan of a copperhead skull does not show any parietal foramina, although if it is of an adult specimen (not stated) then they may have closed up on top. A few other snake species also have such spots, and many snakes have pigmented sensory or apical scale pits elsewhere on their bodies. The parietal eyes of some lizards are also differentially pigmented. Do we need to open our (lateral) eyes to some new possibilities? I think it's clear that snake photoreception, although well-known in species with pit organs, is still relatively poorly understood for snakes as a whole.



1 The function of vitamin A in eyesight was the basis for a WWII propaganda campaign that eating more carrots could improve human night vision. Although it's true that carrots and vitamin A are essential for good eyesight, the extent to which eating more carrots can improve a person's eyesight was apparently greatly exaggerated in 1940 to create a cover story for the novel abilities of Allied pilots to pinpoint Axis fighter jets at night, which in reality was due to on-board Airborne Interception Radar (although there is in turn some disagreement among historians as to how purposeful the deception was and how much both sides knew about the other side's radar capabilities).



2 Melatonin is synthesized from the amino acid tryptophan, which is the origin of another common myth: that eating a ton of turkey causes you feel sleepy.



3 Tilly Edinger was among the very last scientists of Jewish ancestry to leave pre-WWII Germany. A 1938 letter to the U. S. State Department in support of her immigration application from George Gaylord Simpson read "She is a research scientist of the first rank and is favorably known as such all over the world. She is everywhere recognized as the leading specialist on the study of the brain and nervous system of extinct animals and on the evolution of the gross structure of the brain. She is so preeminent in this field that she may really be said to have created a new branch of science, that of paleo-neurology, a study of outstanding value and importance”. She was the first female president of the Society of Vertebrate Paleontology, and authored over 1200 scientific papers and books, many sprinkled with sharp-witted, humorous phrases and observations. Her pioneering work in paleoneurology is well-chronicled here.



4 During embryonic development, the parietal eye and the pineal organ form together from a pocket formed in the brain ectoderm. The ancestral state is presumed to have been a possibly paired photosensory organ, as seen in extant lampreys. The parietal eye and the pineal gland of tetrapods are probably the descendants of the left and right parts of this organ, respectively. Some Devonian fishes have two parietal foramina in their skulls, suggesting an ancestral bilaterality of parietal eyes.



5 Crocodilians and some tropical lineages of mammals (some xenarthrans [sloths], pangolins, sirenians [manatees & dugongs], some marsupials [sugar gliders]) have lost both their parietal eye and their pineal organ. All amphibians have a pineal organ, but some frogs and toads also have what is called a "frontal organ", which is essentially a parietal eye. The word "pineal" comes from the shape of the human pineal organ, which resembles a pine cone.


ACKNOWLEDGMENTS

Thanks to Daniel, Helen Plylar, and David Steen for initiating a discussion of this topic on Twitter, to John Scanlon for providing additional details about the evolution of parietal bone anatomy in squamates, and to Sandy Durso and J. D. Willson for the use of their photos.

REFERENCES

Adler, K. 1976. Extraocular photoreception in amphibians. Photochemistry and Photobiology 23:275-298 <abstract>

Adler, K. and J. B. Phillips. 1985. Orientation in a desert lizard (Uma notata): time-compensated compass movement and polarotaxis. Journal of Comparative Physiology A 156:547-552 <link>

Arendt, J. 1994. Melatonin and the Mammalian Pineal Gland. Springer Science & Business Media <link>

Benoit, J., P. Manger, and B. Rubidge. 2016. Palaeoneurological clues to the evolution of defining mammalian soft tissue traits. Scientific Reports 6 <link>

Bertolucci, C., A. Foa, and G. Tosini. 2002. The circadian organization of reptiles. Pages 129-143 in V. Kumar, editor. Biological Rhythms. Springer <preview>

Bradshaw, W. E. and C. M. Holzapfel. 2007. Evolution of animal photoperiodism. Annual Review of Ecology, Evolution, and Systematics 38:1-25 <link>

Braun-Elwert, C. 2011. Tuatara and their living fossil label. Master of Science Communication thesis. University of Otago, Dunedin, New Zealand <link>

Buchholtz, E. A. and E.-A. Seyfarth. 1999. The gospel of the fossil brain: Tilly Edinger and the science of paleoneurology. Brain Research Bulletin 48:351-361 <link>

Caprette, C. L., M. S. Y. Lee, R. Shine, A. Mokany, and J. F. Downhower. 2004. The origin of snakes (Serpentes) as seen through eye anatomy. Biological Journal of the Linnean Society 81:469-482 <link>

Crews, D., V. Hingorani, and R. J. Nelson. 1988. Role of the pineal gland in the control of annual reproductive behavioral and physiological cycles in the red-sided garter snake (Thamnophis sirtalis parietalis). Journal of Biological Rhythms 3:293-302 <abstract>

Dendy, A. 1911. On the structure, development and morphological interpretation of the pineal organs and adjacent parts of the brain in the tuatara (Sphenodon punctatus). Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character 201:227-331.

Dodt, E. 1973. The parietal eye (pineal and parietal organs) of lower vertebrates. Pages 113-140  Visual Centers in the Brain. Springer.

Eakin, R. M. 1970. A Third Eye: A century-old zoological enigma yields its secrets to electron-microscopist and neurophysiologist. American Scientist 58:73-79 <abstract>

Eakin, R. M. 1973. The Third Eye. University of California Press <Google Book>

Eakin, R. M. and J. A. Westfall. 1960. Further observations on the fine structure of the parietal eye of lizards. The Journal of Cell Biology 8:483-499.

Edinger, T. 1955. The size of parietal foramen and organ in reptiles: a rectification. Bulletin of the Museum of Comparative Zoology 114:1-34 <link>

Engbretson, G. A. 1992. Neurobiology of the lacertilian parietal eye system. Ethology Ecology & Evolution 4:89-107 <abstract>

Foster, R., J. Garcia-Fernandez, I. Provencio, and W. DeGrip. 1993. Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. Journal of Comparative Physiology A 172:33-45.

Foster, R. G., M. S. Grace, I. Provencio, W. J. Degrip, and J. Garcia-Fernandez. 1994. Identification of vertebrate deep brain photoreceptors. Neuroscience & Biobehavioral Reviews 18:541-546.

Foureaux, G., M. I. Egami, C. Jared, M. M. Antoniazzi, R. C. Gutierre, and R. L. Smith. 2010. Rudimentary eyes of squamate fossorial reptiles (Amphisbaenia and Serpentes). The Anatomical Record 293:351-357 <link>

Freake, M. J. 2001. Homing behaviour in the sleepy lizard (Tiliqua rugosa): the role of visual cues and the parietal eye. Behavioral Ecology and Sociobiology 50:563-569 <link>

Gundy, G. C. and G. Z. Wurst. 1976. Parietal eye‐pineal morphology in lizards and its physiological implications. The Anatomical Record 185:419-431 <abstract>

Gundy, G. C. and G. Z. Wurst. 1976. The occurrence of parietal eyes in recent Lacertilia (Reptilia). Journal of Herpetology 10:113-121 <abstract>

Haldar, C. and R. Pandey. 1989. Effect of pinealectomy on annual testicular cycle of Indian chequered water snake, Natrix piscator. General and Comparative Endocrinology 76:214-222 <abstract>

Haldar, C. and R. Pandey. 1989. Effect of pinealectomy on the testicular response of the freshwater snake Natrix piscator to different environmental factors. Canadian Journal of Zoology 67:2352-2357 <link>

Hamasaki, D. and D. Eder. 1977. Adaptive radiation of the pineal system. Pages 497-548  The Visual System in Vertebrates. Springer <Google Book>

Haughton, S. 1929. On some new therapsid genera. Annals of the South African Museum 28:55-78 <link>

Hawley, A. W. and M. Aleksiuk. 1976. The influence of photoperiod and temperature on seasonal testicular recrudescence in the red-sided garter snake (Thamnophis sirtalis parietalis). Comparative Biochemistry and Physiology Part A: Physiology 53:215-221.

Hsiang, A. Y., D. J. Field, T. H. Webster, A. D. Behlke, M. B. Davis, R. A. Racicot, and J. A. Gauthier. 2015. The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evolutionary Biology 15:1-22 <link>

Ireland, L. C. and C. Gans. 1977. Optokinetic behavior of the tuatara, Sphenodon punctatus. Herpetologica 33:339-344.
Jenison, G. and J. Nolte. 1980. An ultraviolet-sensitive mechanism in the reptilian parietal eye. Brain Research 194:506-510

Kitay, J. I. and M. D. Altschule. 1954. The pineal gland. A review of the physiologic literature. Harvard Press, Cambridge, Massachusetts.

Labra, A., K. L. Voje, H. Seligmann, and T. F. Hansen. 2010. Evolution of the third eye: a phylogenetic comparative study of parietal‐eye size as an ecophysiological adaptation in Liolaemus lizards. Biological Journal of the Linnean Society 101:870-883 <link>

Leydig, F. 1872. Zur Kenntniss der Sinnesorgane der Schlangen. Archiv für mikroskopische Anatomie 8:317-357 <abstract>

Linder, H. 1913. Beiträge zur Kenntnis der Plesiosaurier-Gattungen Peloneustes und Pliosaurus. Neues Jahrbuch für Geologie und Paläontologie–Abhandlungen 15:337-409.

Lutterschmidt, D. I., W. I. Lutterschmidt, and V. H. Hutchison. 1997. Melatonin and chlorpromazine: thermal selection and metabolic rate in the bullsnake, Pituophis melanoleucus. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 118:271-277 <abstract>

Lutterschmidt, D. I., W. I. Lutterschmidt, and V. H. Hutchison. 2003. Melatonin and thermoregulation in ectothermic vertebrates: a review. Canadian Journal of Zoology 81:1-13 <link>

Lutterschmidt, D. I., W. I. Lutterschmidt, N. B. Ford, and V. H. Hutchison. 2002. Behavioral thermoregulation and the role of melatonin in a nocturnal snake. Hormones and Behavior 41:41-50 <link>

Menaker, M. and G. Tosini. 1996. The evolution of vertebrate circadian systems. Pages 39-52 in K. Honma and S. Honma, editors. Sapporo Symposium on Biological Rhythms: Circadian Organization and Oscillatory Coupling. Hokkaido University Press, Sapporo, Japan.

Menaker, M. and S. Wisner. 1983. Temperature-compensated circadian clock in the pineal of Anolis. Proceedings of the National Academy of Sciences 80:6119-6121 <link>

Mendonça, M. T., A. J. Tousignant, and D. Crews. 1995. Seasonal changes and annual variability in daily plasma melatonin in the red-sided garter snake (Thamnophis sirtalis parietalis). General and Comparative Endocrinology 100:226-237 <link>

Mendonca, M. T., A. J. Tousignant, and D. Crews. 1996. Pinealectomy, melatonin, and courtship behavior in male red‐sided garter snakes (Thamnophis sirtalis parietalis). The Journal of Experimental Zoology 274:63-74 <link>

Mendonça, M. T., A. J. Tousignant, and D. Crews. 1996. Courting and noncourting male red-sided garter snakes, Thamnophis sirtalis parietalis: Plasma melatonin levels and the effects of pinealectomy. Hormones and Behavior 30:176-185 <link>

Miller, W. H. and M. L. Wolbarsht. 1962. Neural activity in the parietal eye of a lizard. Science 135:316-317 <abstract>

Moore, A. F. and M. Menaker. 2011. The effect of light on melatonin secretion in the cultured pineal glands of Anolis lizards. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 160:301-308 <abstract>

Nelson, R. J., R. T. Mason, R. W. Krohmer, and D. Crews. 1987. Pinealectomy blocks vernal courtship behavior in red-sided garter snakes. Physiology & Behavior 39:231-233 <link>

Petit, A. 1968. Embryogénèse de l'épiphyse et de l'organe sous-commissural de la couleuvre à collier (Tropidonotus natrix L.). Arch. Anat. (Strasbourg) 52:3-25.

Petit, A. 1971. L'épiphyse d'un serpent: Tropidonotus natrix L. Zeitschrift für Zellforschung und mikroskopische Anatomie 120:94-119 <abstract>

Quay, W. 1979. The parietal eye–pineal complex. Pages 245-406 in C. Gans, R. G. Northcutt, and P. Ulinski, editors. Biology of the Reptilia. Volume 9. Neurology A. Academic Press, London <link>

Quay, W., J. A. Kappers, and J. Jongkind. 1968. Innervation and fluorescence histochemistry of monoamines in the pineal organ of a snake (Natrix natrix). Journal of Neuro-visceral Relations 31:11-25 <abstract>

Ralph, C. 1975. The pineal gland and geographical distribution of animals. International Journal of Biometeorology 19:289-303.

Ralph, C. L., B. T. Firth, and J. S. Turner. 1979. The role of the pineal body in ectotherm thermoregulation. American Zoologist 19:273-293 <link>

Ralph, C. L., S. Young, R. Gettinger, and T. O'Shea. 1985. Does the manatee have a pineal body? Acta Zoologica 66:55-60 <abstract>

Scanlon, J. D. and M. S. Lee. 2004. Phylogeny of Australasian venomous snakes (Colubroidea, Elapidae, Hydrophiinae) based on phenotypic and molecular evidence. Zoologica Scripta 33:335-366 <link>

Seebacher, F. and S. A. Murray. 2007. Transient receptor potential ion channels control thermoregulatory behaviour in reptiles. PLoS ONE 2:e281 <link>

Simões, B. F., F. L. Sampaio, C. Jared, M. M. Antoniazzi, E. R. Loew, J. K. Bowmaker, A. Rodriguez, N. S. Hart, D. M. Hunt, J. C. Partridge, and D. J. Gower. 2015. Visual system evolution and the nature of the ancestral snake. Journal of Evolutionary Biology 28:1309-1320 <link>

Solessio, E. and G. A. Engbretson. 1993. Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature 364:442-445 <abstract>

Stebbins, R. C. 1958. An experimental study of the" third eye" of the tuatara. Copeia 1958:183-190 <abstract>

Stebbins, R. C. and R. M. Eakin. 1958. The role of the" third eye" in reptilian behavior. American Museum Novitates 1870:1-40 <link>

Tilden, A. R. and V. H. Hutchison. 1993. Influence of photoperiod and temperature on serum melatonin in the diamondback water snake, Nerodia rhombifera. General and Comparative Endocrinology 92:347-354 <abstract>

Tosini, G. 1997. The pineal complex of reptiles: physiological and behavioral roles. Ethology Ecology & Evolution 9:313-333 <link>

Tosini, G., C. Bertolucci, and A. Foà. 2001. The circadian system of reptiles: a multioscillatory and multiphotoreceptive system. Physiology & Behavior 72:461-471 <abstract>

Trost, E. 1952. Untersuchungen über die frühe Entwicklung des Parietalauges und der Epiphyse von Anguis fragilis, Chalcides ocellatus und Tropidonotus natrix. Zoologischer Anzeiger 148:58-71.

Underwood, H. and M. Menaker. 1976. Extraretinal photoreception in lizards. Photochemistry and Photobiology 23:227-243 <abstract>

Underwood, H. 1989. The pineal and melatonin: regulators of circadian function in lower vertebrates. Cellular and Molecular Life Sciences 45:914-922 <link>

Ung, C. Y. J. and A. C. Molteno. 2004. An enigmatic eye: the histology of the tuatara pineal complex. Clinical & Experimental Ophthalmology 32:614-618 <abstract>

Vivien-Roels, B., P. Pévet, M. Dubois, J. Arendt, and G. Brown. 1981. Immunohistochemical evidence for the presence of melatonin in the pineal gland, the retina and the Harderian gland. Cell and Tissue Research 217:105-115.

Vollrath, L. 1979. Comparative morphology of the vertebrate pineal complex. Progress in Brain Research 52:25-38 <Google Book>

Wurst, G. and G. Gundy. 1982. Pineal morphology in amphisbaenians. Page 908 in Annual Meeting of the American Society of Zoologist. American Society of Zoologists, Louisville, Kentucky.

Zimmerman, K. and H. Heatwole. 1990. Cutaneous photoreception: a new sensory mechanism for reptiles. Copeia 1990:860-862.

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Friday, December 30, 2016

Life is Short but Snakes are Long 2016 Milestones

Dear reader,

Screenshot from 15 November showing Blogger's estimate
that Life is Short but Snakes are Long reached one million
views, which is probably a bit too optimistic.
As I did last year, I want to thank you for your readership in 2016. Life is Short but Snakes are Long reached three-quarters of a million unique views on September 6th this year, by over 430,000 unique readers from nearly every country. We're currently over 860,000 views and on track to reach one million in 2017. The more liberal Blogger statistics show that we're already at one million, but I suspect that many of these are bots, and I'm sticking with the more conservative estimates provided by Google Analytics. I'm so happy to have reached so many people. Furthermore, at least 34 new species of snakes were described in 2016—another reason to celebrate!

In addition to defending my dissertation and moving to Germany in 2016, I also published 5 scientific papers and co-authored a book chapter for the new 3rd edition of Mader's Reptile Medicine and Surgery, on the behavior of reptiles and amphibians, which will be published in 2017. I became a lot more active in the Facebook Snake Identification and Wild Snakes: Education and Discussion groups, which are fantastic resources for quick, reputable answers to questions about snakes. I recently accepted a position as an Associate Editor of the Snake Natural History Notes section at the journal Herpetological Review, and I was invited to become a curator at the Encyclopedia of Life project, where I've written several short summaries of snake taxa.

Life is Short but Snakes are Long was voted one of
Bel-Rea Vet Tech College's Top 25 Reptile/Amphibian Blogs in 2016
Life is Short but Snakes are Long was voted one of Bel-Rea Vet Tech College's Top 25 Reptile/Amphibian Blogs. The students and staff wrote that they particularly appreciated my efforts to reference my sources, and I was really glad to know that others appreciate my efforts to provide verifiable information (apparently there's all too little of that on the Internet these days).

I was particularly glad that the BBC's Planet Earth II featured Galápagos Racers so prominently this year, generating Internet-wide buzz about snakes and their feeding habits, a topic close to my heart. Since I wrote about these interesting snakes back in 2013, a lot of curious people found my blog, inspiring me to write an update and include much more detailed information. I also revisited several other favorite topics, including the relationship between dragonsnakes and filesnakes, rattlesnake roundupssnake penises, and snakes as state/provincial symbols. I have some really good content planned to debut in 2017, including articles on the roles that snakes play in ecosystems, the nitty-gritty details of courtship, sex, and mating in snakes, the little-known and seldom-seen ecology of blindsnakes, profiles of some fossil snakes, and venomous bites from "non-venomous" snakes.

Life is Short but Snakes are Long would not be possible without support from volunteer translators Alvaro Pemartin & Estefania Carrillo, from Utah State University, particularly my advisor Susannah French and the Ecology Center, and from my loving girlfriend and editor Kendal Morris.

Thank you, and happy 2017!

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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.

Sunday, November 27, 2016

Galápagos Racers: answers to your questions about the BBC Planet Earth II iguana chase scene

This post will soon become available in Spanish

Galápagos Racers (Pseudalsophis occidentalis)
on Fernandina Island, from the BBC's Planet Earth II footage
If you haven't seen the incredible footage of the "iguana chase scene" from the BBC's Planet Earth II Islands episode, I encourage you to watch it right away. In addition to being a highly dramatic cinematographic masterpiece, it raises a number of interesting questions about the biology of the snakes in the clip. For a few days after it aired, the Internet was buzzing with these questions, and I've cataloged the answers to some of the most popular ones below. If you have one that isn't listed, feel free to ask it in the comments! And, if you want to know more about the process I used to dig up some of this information, check out my tutorial for teaching oneself about obscure snakes.

What kind of snakes are they?

Throughout the clip, Attenborough calls them "racer snakes"1, but herpetologists would normally call the snakes on the screen Galápagos Racers. Although these snakes are called "racers", they're not closely related to North American racers (genus Coluber); it's been about 45 million years since these two snakes last shared a common ancestor.

Galápagos Racers belong to the genus Pseudalsophis. Depending on which sources you consult, there are between 4 and 7 species of Pseudalsophis in the Galápagos, as well as one in mainland South America.

Pseudalsophis slevini eating a gecko on Pinzón Island
Just like Galápagos tortoises, finches, and many other organisms, there are different species of Galápagos Racers on the different Galápagos Islands (one of the concepts that sparked Darwin's theory of evolution by natural selection). The film was made on Fernandina, the youngest, westernmost, and most volcanically-active island in the Galápagos. Fernandina has two species of snakes, Pseudalsophis slevini and Pseudalsophis occidentalis. The snakes in the film must be Pseudalsophis occidentalis, because they are too large and not boldly banded enough to be P. slevini. You can read the original descriptions of both species here.

None of the sources reporting which species is shown in the film are authoritative, but without exception when the species is given it is given as Pseudalsophis biserialis. This is not correct under any modern taxonomy, although there is also a good explanation for why it is mistakenly being used—P. occidentalis was briefly a subspecies of P. biserialis, but has mostly been and is now treated either as a subspecies of P. dorsalis or as its own species. See below for much more (probably too much) detail.

Why are there so many of them?

Galápagos Racer (P. dorsalis) among adult Marine Iguanas
on Santa Cruz, which are much too large for it to eat
Most snakes are not social, and because they must swallow their food whole they cannot share prey. These snakes are not found at such high densities year-round, but rather aggregate around consistent Marine Iguana nesting sites in May when the eggs are hatching.

Just as when baby sea turtles emerge from their nests, predators congregate at the temporary buffet, returning afterwards to their usual densities. Around the world, there are numerous examples of avian and snake predators exploiting emerging hatchling iguanas. Researchers working at other iguana nesting sites in the Bahamas, the West Indies, and Venezuela have hypothesized that snakes and other predators also converge on the nesting sites of these other iguanas to exploit the temporary food source. Another example of snakes congregating around abundant prey resources is that of Puerto Rican and Cuban boas, which aggregate around the openings of massive bat caves.

The rest of the year, Galápagos Racers eat lava lizards, geckos, insects, marine fishes, and hatchling birds, as well as introduced rats and mice.

Are they really hunting in a pack?

Almost certainly not. Again, most snakes are not social, and because they must swallow their food whole they cannot share prey. Pack-hunting behavior is unknown in snakes.

Two P. occidentalis trying to eat the same iguana
Jaw-walking is a fixed action pattern in snakes and they
may eat things that only vaguely resemble their food
once they start jaw-walking them.
From Planet Earth II Behind the Scenes
Some species have surprisingly social behaviors. It would be really interesting to examine social behavior in these snakes. To my knowledge no one has done so. Although they obviously cannot share a single food item, but if they are foraging in the same time and place on a limited resource, there might be an opportunity for the evolution of social cues. At least one paper suggested that this might be the case with a pit viper. Even though the BBC videographers saw snakes actively fighting over the same prey items and in some cases eating one another, it's possible that more closely-related snakes are less likely to fight over food or eat one another, or that males are less likely to compete with or try to eat females. These are testable hypotheses. However, these are not well-studied snakes. I don't think they are helping each other, but there's a lot that we don't know about snakes. Some snakes exhibit dominance hierarchies, and one study suggested that individual recognition occurs and persists over time in gartersnakes.

Few scientists are currently studying these snakes. It's a testament to the BBC that they are consistently able to film natural phenomena that are still unknown to science. Hopefully this tape will stimulate some research on this exact question, and on the ecology of Galápagos Racers. When I wrote about Galápagos Racers in 2013, not much was known about their ecology, and that's still the case. It's amazing that so little research has been done on these snakes, particularly in contrast to Galápagos tortoises and marine iguanas (not to mention finches and other non-avian reptiles).

Why don't the female Marine Iguanas just lay their eggs somewhere else, closer to the ocean maybe?

Fates of rock iguana hatchlings, over half of which were
eaten by Cubophis and Epicrates snake predators in their
first month of life. From Knapp et al. 2010
Marine Iguanas have to dig nests and lay their eggs in soft sand, away from the rocky, tidal foraging grounds of the adults. They choose protected lava reefs for this purpose, which are in short supply on most islands. One estimate suggested that the cost of migrating to their nesting sites represented half the reproductive effort of female Galápagos land iguanas.

Many species of reptiles nest in areas where they otherwise do not spend much time, especially aquatic species (reptile eggs need to "breathe" air and cannot be laid underwater). Female Marine Iguanas may all use the same nesting sites because those are the only sites available, or they may choose to nest near one another because, just like with sea turtles, synchronous hatching of the young increases their probability of survival.

In a study of Bahamian rock iguanas (Cyclura cychlura), snake predation was the most likely cause of mortality for newborn iguanas dispersing away from their nests. They estimated that about 20-30% of hatchling iguanas survived their first month, and those that moved quickly and linearly away from their nests were the most likely to survive, perhaps because predators had learned to hang around the nesting area. Another study of Galápagos land iguanas showed that predation attempts by Galápagos hawks were more than three times as likely to be successful when the body temperature of the iguana hatchlings was below 90°F. And, baby Galápagos marine iguanas that hung around their hatching area had about a 10% lower survival rate than those that moved to the coast, which the researchers attribute mostly to higher risk of predation at the nesting area.

Studies on the population biology of Marine Iguanas have shown that most of their mortality is caused by "predation, starvation (sometimes as a result of being trapped by a rock), crushing by a rock, being beaten against rocks by the sea, and suffocation in collapsed nest burrows. Animals may also die after being swept out to sea by offshore currents". So, actually, predation may be the best way for them to go. Besides Galápagos Racers, their other predators include Galápagos Hawks, Short-eared Owls, crabs, and Giant Hawk-fish.

Are they venomous/dangerous to humans?

No. Like many snakes, Galápagos Racers are rear-fanged. This means that, although technically they are venomous, they don't pose a danger to humans. Rear-fanged snakes have grooved teeth (rather than hollow fangs) on the back of their upper jaw (as opposed to the front); they can use these teeth to get venom into their prey once they are biting it, but they cannot strike out and deliver venom the way a viper can. A small minority of rear-fanged snakes have delivered medically-significant bites to humans, but almost all of these take place in a captive setting. You can read more about the different types of snake fangs here.

I didn't know there were snakes in the Galápagos. How did they get there?

Map showing the estimated age of each of the
Galápagos Islands. From Ali & Aitchison 2014
Galápagos Racers colonized the Galápagos Islands from mainland South America, just like all of the other Galápagos fauna and flora. The modern Galápagos Islands formed from volcanoes over the past 4 to 5 million years, although some of them have been building beneath the ocean surface for up to 15 million years. It is thought that there have been islands in the Galápagos for at least 8 million years, but the oldest islands have eroded and are now back beneath the ocean surface.

Because the Galápagos Islands are located only six hundred miles off the coast of Ecuador, it is easier for them to be colonized by plants and animals from the mainland than for a more remote island chain such as Hawaii (which is >2,500 miles away from the nearest snake-inhabited landmass).

Molecular dating of the divergence time between Galápagos Racers and their closest mainland relative, Pseudalsophis elegans, suggests that it has been about 15 million years since they last shared a common ancestor. This suggests that the mainland ancestor of Galápagos Racers probably went extinct sometime over the last 15 million years, and that the ancestors of Galápagos Racers probably colonized the Galápagos Islands before any of the current islands existed (as is also the case for the Marine Iguanas). Until genetic work is done, we won't know how many times snakes colonized the Galápagos archipelago or how many distinct lineages there are. [Edit 12/30/2016: I have recently learned that Massey University ecologist Luis Ortiz-Catedral and his colleagues are working to understand the evolution of all the species in the genus Pseudalsophis and definitively answer this question.]

Could the film have been staged?

Obviously the scenes are spliced together, but in my opinion there's no chance the Galápagos National Park would allow something like this to be staged. They are among the strictest places in the world for researchers to conduct scientific work. However, more recent episodes of Planet Earth II have been criticized for incorporating fake sound effects.


One of the few phylogenies to include Galápagos Racers
Broadly, Pseudalsophis is nested within a large clade of Caribbean, Central, and South American xenodontine snakes including, among numerous others, the genus Alsophis, which once contained Galápagos Racers and after which their current genus is named. They have been in a variety of genera since their description, especially Dromicus, which is no longer in use, from 1876 to 1997.

In 1973, herpetologist Charles Myers wrote: "The classification of colubrid snakes in general, and of South American colubrids in particular, is in a notoriously unsatisfactory state." Unfortunately, we are not that much better off today when it comes to Galápagos Racers. It seems pretty clear that the nearest relative of P. biserialis, P. dorsalis, and P. occidentalis is Pseudalsophis elegans, the only species in the genus found on the mainland (in Ecuador, Peru, and extreme northern Chile). Beyond that, there isn't a lot of clarity about their next-closest relatives. They are possibly most closely related to obscure South American "groundsnakes" in the genus Psomophis, or to the even more obscure genus Saphenophis, which was described by Myers as "quite lacking in peculiar or unique features" and so named "in allusion to one incontrovertible fact about these snakes...from the Greek saphenes (evident truth, clear) + ophis (a serpent), meaning 'clearly a snake'". We don't really have a great hypothesis about how the different lineages of Galápagos Racers are related to one another, or even if they are all descended from a single common ancestor, because we only have DNA from one of them so far.

Hypothesized scenario for the evolution of Pseudalsophis snakes
So far, we have no DNA evidence that would support or refute this model
From Ali & Aitchison 2014
Two reviews based on morphology addressed this question in the late 1990s. The first (Thomas 1997) focused exclusively on Galápagos Racers and suggested that P. biserialis, P. dorsalis, and P. occidentalis are descended from a shared common ancestor with P. elegans, but that P. hoodensis is more closely related to the mainland species Philodryas chammissonis, and that P. slevini and P. steindachneri are most closely related to Caribbean species. The other study (Zaher 1999), which looked at hemipene morphology over a much larger group of snakes, disagreed, finding a shared derived character—an inflated papillate ridge, placed far medially, on the medial surface of the lobes—linking the Galápagos Racers together with the mainland species P. elegans. Statements that Galápagos Racers have “very similar hemipenes” notwithstanding, Zaher was criticized for not describing the specific characters uniting the Galápagos species to the exclusion of others.

Maglio (1970) noted that the tooth counts and arrangement and the and shape of the premaxilla bone was most similar among the three Galápagos species that he examined (P. biserialisP. dorsalis, and P. slevini), and different from the West Indian species that Taylor later suggested are P. slevini's closest relatives. More recently, a study led by Grazziotin claimed that they "unequivocally support...Zaher's (1999) hypothesis based on morphology that continental Pseudalsophis elegans is closely related to the Galápagos Island species of Xenodontinae (herein represented by Pseudalsophis dorsalis), rather than to West Indian Alsophis and Antillophis, and mainland Philodryas (Thomas, 1997)." However, they obviously didn't read Thomas's paper very carefully, because he also hypothesizes that P. dorsalis is closely related to P. elegans, and the Grazziotin paper didn't sequence any DNA from P. slevini, P. steindachneri, or P. hoodensis, and therefore didn't test any hypotheses about them.

As for whether or not the snakes in Planet Earth II should be called P. occidentalis or P. dorsalis occidentalis, that's really a lumper/splitter question. But, both the IUCN and the 2014 edition of Snakes of the World recognize P. occidentalis as a full species; it was originally described as such by Van Denburgh in 1912, sunk to a subspecies of P. dorsalis by Mertens in 1960, and re-elevated to a full species in a 1999 paper by Zaher that was not primarily concerned with taxonomy and appears to have subsequently been neglected. The Reptile Database is currently a holdout for the subspecies designation, which has not been disputed but which is also not explicitly supported by unambiguous data. Perhaps wisely, the official webpage of Galápagos National Park chooses not to use scientific names and refers to the Fernandina racers as the "western subspecies". The truth is that, until more research is done, we won't be able to settle on an accurate taxonomy for these snakes.



1 This sounds a bit redundant to a snake biologist, but it isn't incorrect. The one thing that I wish BBC programs would do is identify the species in them more precisely. I'm advocating for a "biologist mode" that can be activated which would show the location and identity of species in all clips, similar to the old MTV show Pop-up Video.


ACKNOWLEDGMENTS

Thanks to Andy Kraemer and Jim Moulton for the use of their photographs.

REFERENCES

Ali, J. R. and J. C. Aitchison. 2014. Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. Journal of Biogeography 41:1227-1241 <full-text>

Bisconti, M., W. Landini, G. Bianucci, G. Cantalamessa, G. Carnevale, L. Ragaini, and G. Valleri. 2001. Biogeographic relationships of the Galapagos terrestrial biota: parsimony analyses of endemicity based on reptiles, land birds and Scalesia land plants. Journal of Biogeography 28:495-510 <full-text>

Carpenter, C. C. 1966. The marine iguana of the Galapagos Islands, its behavior and ecology. Proceedings of the California Academy of Sciences (Series 4) 34:329-376 <full-text>

Carpenter, C. C. 1984. Dominance in snakes. Special Publication, University of Kansas Museum of Natural History 10:195-202 <full-text>

Christian, K. A. and C. R. Tracy. 1981. The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia 49:218-223 <abstract>

Geist, D., H. Snell, H. Snell, C. Goddard, and M. Kurz. 2014. A paleogeographic model of the Galápagos Islands and biogeographical and evolutionary implications. The Galápagos: a natural laboratory for the Earth Sciences. American Geophysical Union, Washington DC, USA:145-166 <full-text>

Grazziotin, F. G., H. Zaher, R. W. Murphy, G. Scrocchi, M. A. Benavides, Y.-P. Zhang, and S. L. Bonattoh. 2012. Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics 28:437-459 <full-text>

Grehan, J. 2001. Biogeography and evolution of the Galápagos: integration of the biological and geological evidence. Biological Journal of the Linnean Society 74:267-287 <full-text>

Günther, A. 1860. On a new snake from the Galápagos islands. The Annals and Magazine of Natural History 3:78-79 <full-text>

Hedges, S. B., A. Couloux, and N. Vidal. 2009. Molecular phylogeny, classification, and biogeography of West Indian racer snakes of the Tribe Alsophiini (Squamata, Dipsadidae, Xenodontinae). Zootaxa 2067:1-28 <full-text>

Knapp, C. R., S. Alvarez-Clare, and C. Perez-Heydrich. 2010. The influence of landscape heterogeneity and dispersal on survival of neonate insular iguanas. Copeia 2010:62-70 <full-text>

Laurie, W. and D. Brown. 1990. Population biology of marine iguanas (Amblyrhynchus cristatus). II. Changes in annual survival rates and the effects of size, sex, age and fecundity in a population crash. Journal of Animal Ecology 59:529-544 <full-text>

Maglio, V. J. 1970. West Indian xenodontine colubrid snakes: their probable origin, phylogeny, and zoogeography. Bulletin of the Museum of Comparative Zoology 141:1-54 <full-text>

Merlen, G. and R. A. Thomas. 2013. A Galapagos ectothermic terrestrial snake gambles a potential chilly bath for a protein-rich dish of fish. Herpetological Review 44:415-417 <full-text>

Mertens, R. 1960. Über die schlangen der Galápagos. Senckenbergiana Biologica 41:133-141 <not available online>

Myers, C. W. 1973. A new genus for Andean snakes related to Lygophis boursieri and a new species (Colubridae). American Museum Novitates 2522 <full-text>

Parent, C. E., A. Caccone, and K. Petren. 2008. Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences 363:3347-3361 <full-text>

Pyron, R. A., F. Burbrink, and J. J. Wiens. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13:93 <full-text>

Pyron, R. A., J. Guayasamin, N. Peñafiel, L. Bustamante, and A. Arteaga. 2015. Systematics of Nothopsini (Serpentes, Dipsadidae), with a new species of Synophis from the Pacific Andean slopes of southwestern Ecuador. ZooKeys 541:109-147 <full-text>

Radder, R. S. and R. Shine. 2007. Why do female lizards lay their eggs in communal nests? Journal of Animal Ecology 76:881-887 <full-text>

Rassmann, K. 1997. Evolutionary age of the Galápagos iguanas predates the age of the present Galápagos Islands. Molecular Phylogenetics and Evolution 7:158-172 <full-text>

Rodríguez-Durán, A. 1996. Foraging ecology of the Puerto Rican boa (Epicrates inornatus): bat predation, carrion feeding, and piracy. Journal of Herpetology 30:533-536<full-text>

Shine, R., L. X. Sun, M. Fitzgerald, and M. Kearney. 2002. Accidental altruism in insular pit-vipers (Gloydius shedaoensis, Viperidae). Evolutionary Ecology 16:541-548 <full-text>

Steindachner, F. 1876. Die schlangen und eidechsen der Galapagos-inseln. Zoologisch-botanischen Gesellschaft, Wien, Germany <Google book>

Swash, A. and R. Still. 2000. Birds, Mammals and Reptiles of the Galapagos Islands. Pica Press <Amazon>

Thomas, R. 1997. Galapagos terrestrial snakes: biogeography and systematics. Herpetological Natural History 5:19-40 <full-text>

Van Denburgh, J. 1912. Expedition of the California Academy of Sciences to the Galápagos Islands, 1905-1906. IV. The snakes of the Galapagos Islands. Proceedings of the California Academy of Sciences (Series 4) 1:323-374 <full-text>

Wallach, V. W., Kenneth J. and J. Boundy. 2014. Snakes of the World: A Catalogue of Living and Extinct Species. CRC Press, Boca Raton, Florida, USA <Google book>

Weinstein, S. A., D. A. Warrell, J. White, and D. E. Keyler. 2011. "Venomous" Bites from Non-Venomous Snakes: A Critical Analysis of Risk and Management of "Colubrid" Snake Bites. Elsevier, Amsterdam <Google book>

Werner, D. I. 1983. Reproduction in the iguana Conolophus subcristatus on Fernandina Island, Galapagos: clutch size and migration costs. American Naturalist 121:757-775 <abstract>

Yeager, C. P. and G. M. Burghardt. 1991. Effect of food competition on aggregation: evidence for social recognition in the plains garter snake (Thamnophis radix). Journal of Comparative Psychology 105:380-386 <abstract>

Zaher, H. 1999. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the American Museum of Natural History 240:1-168 <full-text>

Zaher, H., F. G. Grazziotin, J. E. Cadle, R. W. Murphy, J. C. Moura-Leite, and S. L. Bonatto. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Papeis Avulsos de Zoologia (Sao Paulo) 49:115-153 <full-text>

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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.