Blood in the Desert: Phrynosoma spp.

Phrynosoma_1

Greater Short-Horned Lizard (Phrynosoma hernandesi) spotted in Petrified Forest National Park, Arizona.  Image credit: Curious Sengi.

Unlike your typical desert lizard that skitters away at the slightest movement, the horny toad — or rather, horny lizard — usually just sits there, looking rather overstuffed and grumpy.

It is a charming grumpy, however.

Horny toads (Phrynosoma spp.) are characterized by having flat, squat bodies, a frill of horns on the head, and a stumpy little tail that makes these lizards look more like their amphibian namesakes.  The genus is widely distributed from western Canada down to Guatemala, though the horny toad seems to have particularly captured the imagination of the American Southwest and Texas.

Phrynosoma_4

The short, stumpy tail and squat body makes this lizard look rather toad-like.  In fact, the genus name, Phrynosoma, means “toad” or “frog-bodied.”  P. hernandesi.  Image credit: Curious Sengi.

Phrynosoma_2

There something eccentric and wonderful about horny toads that have made this reptile a favorite character of the American desert.  Their image has been shaped into representatives of a classic motorcycle brand, household novelty items, team mascot for Texas Christian University, and soft plush toys.  Everyone loves horny toads!  Image credit (clockwise from top left): Thunderpress T-Shirt Shop, Rivers Edge Products, Wikipedia Commons, FluffEngine Etsy shop.

These oddly charismatic lizards can afford to be unhurried in the the face of danger.  Their cryptic coloration allows them to be camouflaged against the desert dirt, rocks, and vegetation.  But if they are discovered and charging would-be attackers with lowered horns and open mouth, or puffing out is not enough of a deterrent, horny toads can unleash a surprising defense:  squirting a stream of blood from their eyes.

Squirting Phrynosoma

Some species of horny toad can eject an impressive directed jet of blood as a defensive measure.  Image credit:  New Scientist via Tag the Bird.

Scientists, naturalists, and inquisitive children had long noted the discharge of red fluid from these lizards.  Oliver Perry Hay (1816 – 1930), an American paleontologist who spent much of his life on fossil turtles, was finally able to confirm that the ejecta was not some glandular secretion but indeed blood.  In his 1892 report:

Near my desk there was a specimen of Phrynosoma coronatum [sic] which had been sent from California by a member of Dr. Merriam’s exploring party.  About the 1st of August it was shedding its outer skin, and the process appeared to be a difficult one, since the skin was dried and adhered closely.  One day it occurred to me that it might facilitate matters if I should give the animal a wetting; so, taking it up, I carried it to a wash-basin of water near by and suddenly tossed the lizard into the water.  The first surprise was probably experienced by the Phrynosoma, but the next surprise was my own, for on one side of the basin there suddenly appeared a number of spots of red fluid, which resembled blood. . . . . I concluded that this was a good time to settle the question whether this fluid was blood or not.  A microscope was soon procured and an examination was made, which immediately showed that the matter ejected was really blood.

The affair now became very interesting.  Just where the blood came from I could not determine with certainty, the whole thing having happened so suddenly and unexpectedly. . . . There appeared to be a considerable quantity of the blood, since on the sides of the vessel and on the wall near it I counted ninety of the little splotches.  A consultation was had with Mr. Stejneger the next day with regard to the propriety of dashing the animal into the water again to discover, if possible, where the blood came from.  It was thought, however, that such blood-lettings must be somewhat exhausting, and that it would be better to allow the animal a day to recuperate.  While talking I picked up the lizard and was holding it between my thumb and middle finger, and stroking its horns with my fore-finger.  All at once a quantity of blood was thrown out against my fingers, and a portion of it ran down the animal’s neck; and this blood came directly out of the right eye.  It was shot backward and appeared to issue from the outer canthus.  It was impossible to determine just how much there was of the blood, but it seemed that there must have been a quarter of a teaspoonful.  I went so far as to taste a small quantity of it, but all that I could detect was a slight musky flavor.

Phrynosoma solare bloody face

The bloody aftermath.  P. solare.  Image caption: John Cancalosi / NPL via BBC.

So blood it is.  But what was the mechanism behind this alarming feat?  Blood-squirting horny toads have a large orbital sinus — a pocket rich with venous blood — in the space between the eyeball and eyesocket, wrapping around to the inner wall of the eyelid.  Observers have noted that when harassed, the eyes of the horny toad took on a puffy, swollen appearance which quickly deflated if the animal was then left alone.  Scientists suspected that a rise in blood pressure was responsible for rupturing the thin walls of the orbital sinus.  An anatomical study by Henry L. Bruner revealed a minute, sphincter-like muscle specialized to pinch off the internal jugular vein (m. constrictor venae jugularis internae).  Though Bruner found this muscle in many of the reptiles he studied and hypothesized that it generated a “swell mechanism” associated with skin shedding, this anatomical feature could have been co-opted in horny toads to increase cranial blood pressure enough to squirt a stream of blood at least 3 ft away (0.9 m; reports of ejections 6 ft away have also been reported but not substantiated).

Phrynosoma_3

The horny toad’s preferred line of defense is blending in.  P. hernandesi hanging out at the margin of dried grasses and low scrub in Petrified Forest National Park, Arizona.  Image credit: Curious Sengi.

Hay’s well-intentioned effort to help the horny toad on his desk shed its skin by plopping it into a basin of water might be a clue into what motivates it to squirt blood.  Squirting does not seem to be a response to all threatening situations.  Some have noted the prevalence of this behavior during the perilous molting season.  But most curious of all, horny toads preferentially squirt when harassed by canines.

Even though horny toad predators include roadrunners (Geococcyx spp.) and grasshopper mice (Onychomys spp.), these encounters elicit opening of the mouth, head-down charging, and puffing up, but rarely (if at all) result in a squirt of blood.  Instead, this context-dependent defense was reserved for canid predators such as coyotes (Canis latrans), kit foxes (Vulpes macrotis), and even dogs (C. familiaris).  In order the understand this specificity, Middendorf and Sherbrooke (1992) staged a series of predator-prey encounters between horny toads that included supervised interactions with a “2-3 year-old female, yellow Labrador retriever” named Dusty.  After “. . . .attacks [involving] barking, pawing, gentle biting, nibbling, and picking up and tossing of the lizard” all 10 out of 10 lizards squirted blood.  On the other hand, humans mimicking dogs with “. . . .one of us on all fours, barked at, approached, chased, and physically manipulated the lizard (WCS touched, stroked, tapped, picked up, and tossed but did not bite)” only resulted in 20% responding.  Middendorf and Sherbrooke concluded that while tactile cues were important in inducing blood squirting, they have yet to pinpoint what is actually triggering this behavior.

Phrynosoma skulls

There are over a dozen recognized species of horny toad distributed all throughout western North and Central America.  The horns are bony outgrowths of the parietal and squamosal bones of the skull.  Another defensive tactic is for the lizard to charge at attackers, head down and horns at the ready.  Note that skulls are not to scale.  Image credit: Digimorph.

Taking a slightly different tack from using pets and researchers simulating dog attacks, Sherbrooke and Mason (2005) focused on the effect of blood squirting on potential canine predators.  It seemed remarkable that the blood ejected from the eyes was not a frantic spray, but a directed jet that targeted the eyes, nose, and mouth.  Hay’s 1892 account of tasting the blood only led him to comment on its “musky” taste, though he did quote a man who experienced eye irritation.  Another study found no difference in blood chemistry between ejected blood and blood circulating in the body.  However, compared to other lizards, horny toads did possess an unnamed compound in the blood related to the animal’s ability to detoxify venom from their preferred food, seed harvester ants (Pogonomyrmex maricopa).

Sherbrooke and Mason used captive coyotes to test which sensory system was targeted by horny toad blood.  Feeding coyotes whole lizard carcasses resulted in regurgitation.  One particular coyote was determined to keep down its meal:  “. . . . the coyote regurgitated (<1 min) a food bolus containing the remains of the lizard.  Then the coyote went through 3 series of reingestion-regurgitation episodes with the same bolus.”  It is not known if this pattern of repeated ingestion is normal, but both coyotes and foxes have been found the horny toad remains in their stomachs.  The researchers then used five test fluids (saline control, blood plasma and whole blood from horny toad, blood plasma and whole blood of a Sceloporus lizard) and squirted them into the eyes, nose, and mouth of their perhaps not-wholly-willing test subjects.  The most pronounced response was from the introduction of horny toad blood into the nose and mouth — the coyotes opened and closed their mouths and shook their heads in what appeared to be efforts to get rid of the distasteful substance.  So even though horny toads certainly fall prey to canine hunters, the targeted blood squirting defense might provide enough of a distraction to potential predators for the horny toad to scurry away and blend back into the dirt and vegetation.

Phrynsoma phylogeny

Phylogenetic tree reconstructed for the genus Phrynosoma based on mitochondrial and nuclear DNA.  Note the black bars crossing the branches.  ABS (antipredator blood squirting is present at the very base of the tree, suggesting that this ability is ancestral to all horny toads.  This phylogeny hypothesizes four independent losses of blood squirting (marked as “ABS loss”).  Image credit: Leache & McGuire 2006.

Despite the iconic image of blood streaming from the eye of the horny toad, not all members of this genus squirt.  A molecular-based phylogeny indicate loss of blood-squirting in at least four groups of horny toad species that are not directly related to each other.  It is not clear if these animals simply do not exhibit the behavior, or if they have lost some key anatomical feature necessary for the process.  The study’s authors readily admit that reconstructing the horny toad family tree is challenging and it is unclear how many times blood squirting ability was lost.  But we can conclude from their results that blood squirting is part of the essence of horny-toadness and appears at the base of the Phrynosoma tree as the ancestral state.

Phrynosoma_5

This sweet little P. hernandesi is just chilling.  No need for blood squirting here.  Image credit:  Curious Sengi.

References

Bruner, Henry L.  1907.  “On the cephalic veins and sinuses of reptiles, with description of a mechanism for raising the venous blood-pressure in the head.”  American Journal of Anatomy 7 (1):  1 – 117.

Burleson, Gretchen Lyon.  1942.  “The Source of the Blood Ejected from the Eye by Horned Toads.”  Copeia 1942 (4):  246 – 248.

Hay, Oliver P.  1892.  “On the Ejection of Blood from the Eyes of Horned Toads.”  Proceedings of the United States National Museum 15 (907):  375 – 378.

Leaché, Adam D. & Jimmy A. McGuire.  2006.  “Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data:  Evidence for a misleading mitochondrial gene tree.”  Molecular Phylogenetics & Evolution 39 (3):  628 – 644.

Middendorf III, George A. & Wade C. Sherbrooke.  1992.  “Canid Elicitation of Blood-Squirting in a Horned Lizard (Phrynosoma cornutum).”  Copeia 1992 (2):  519 – 527.

Middendorf III, George A, Wade C. Sherbrooke, & Eldon J. Braun.  2001.  “Comparison of Blood Squirted from the Circumorbital Sinus and Systemic Blood in a Horned Lizard, Phrynosoma cornutum.”  The Southwestern Naturalist 46 (3):  384 – 387.

Sherbrooke, Wade C. & J. Russell Mason.  2005.  “Sensory Modality Used by Coyotes in Responding to Antipredatory Compounds in the Blood of Texas Horned Lizards.”  The Southwestern Naturalist 50 (2):  216 – 222.

Winton. W.M.  1916.  “Habits and Behavior of the Texas Horned Lizard, Phrynosoma cornutum, Harlan.”  Copeia 36:  81 – 84.

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