Ocular blood-cannons - the how and why

A wide variety of chemical defenses have evolved in the natural kingdom, in creatures ranging from sponges to skunks. However, squirting blood from one’s eyes may seem to be taking self-defense a little too far. Besides, the animals that use it seem to be well-protected anyway, decked out as they are with spikes and prickles. So what’s up with blood-squirting in horned lizards? (picture of Phrynosoma douglassii from Wikipedia).

Blood-squirting from the eyesockets is the exclusive predator repellent of several species of horned lizard. All horned lizards (aka horned toads) are iguanids belonging to the genus Phrynosoma (literally, toad body), and hail from North America. They're very distinctive creatures, and hard to confuse with anything else; Pianka and Parker (1975) assembled a list of distinguishing features, including dorsoventral flattening, abundant spines (mostly around the back of the head), short legs, sluggish behavior, a diet based almost exclusively on ants, and specialized dentition and a huge stomach to cope with their myrmecine meals.

Not all horned lizards squirt blood, though. Apparently, the mechanism evolved early on and was then lost in later members of the genus. According to a recent study by Leaché and McGuire (2006), Phrynosoma can be subdivided into four main clades. Tapaja are viviparous with short or reduced horns, while Anota have especially prominent cranial horns. Doliosaurus lack blood-squirting, and hail from the Chihuahuan, Mojave, and Sonoran deserts. Finally, Brevicauda are viviparous with very short tails and no blood-squirting. The nifty cladogram adjacent (from Leaché and McGuire, 2006) makes it a lot clearer. Note the horn lengths in the different species, and the loss of blood-squirting, which happened several times over their history.

With the introduction and phylogeny out of the way, the bloody business can be breached, starting with the mechanism. The blood in question is ejected at high pressure from a circumorbital sinus between the eyeball and the orbital walls. A muscle found in most reptiles squeezes the internal jugular vein, rupturing the nictitating membrane and forcing blood out for several feet (Burleson, 1942). The actual behavior seems to be “rare but consistent” (Lambert and Ferguson, 1985). The blood-squirting defense seems to be primarily directed at canine predators (Middendorf and Sherbrooke, 1992), or at least larger mammals. Canids always elicited blood-squirting, as did canid saliva; roadrunners and grasshopper mice, on the other hand, did not stimulate blood ejection. When blood was ejected, the target regularly showed symptoms of irritation.

Does the blood have anything in it that makes it nastier than regular blood? It has been suggested that secretions from the Harderian and lacrimal glands give it its irritating quality (Burleson, 1942); however, not only did the secretions from the glands prove innocuous (Sherbrooke and Middendorf, 2004), but the blood squirted did not significantly differ from “regular” blood in the rest of the lizard’s body, which is also laced with antipredator chemicals (Middendorf et al., 2001). In other words, all of a horned lizard's blood is irritating. It is possible that the chemicals that render the blood distasteful are sequestered from harvester ants Pogonomyrmex (Sherbrooke and Middendorf, 2004). This is a likely conclusion, given that horned lizards are highly resistant to harvester ant venom, with plasma factors that neutralize the ants’ toxins (Schmidt et al., 1989). (picture of blood-spattered Phrynosoma asio from here).

The horns are a primary line of defense, as kit foxes are more likely to attack a dehorned lizard; once the lizards are attacked, the irritating jet of blood ensures they are not attacked again (Sherbrooke and Middendorf, 2004). Noxious systemic blood could function as a last-ditch resort, dissuading predators from eating any more horned lizards. Regarding how/why such a system would evolve remains open, however.

Finally, because I couldn't find a decent photo of a blood-squirting lizard, here's a National Geographic clip from Youtube. The first 5-10 seconds are enough. Ah, if only there could be more uploads like that redback mating clip...




References

Burleson, G. L. (1942) The Source of the Blood Ejected from the Eye by Horned Toads. Copeia, Vol. 1942, No. 4 (Dec. 28, 1942), pp. 246-248

Cutter, W. S. (1959) An Instance of Blood-Squirting by Phrynosoma solare. Copeia, Vol. 1959, No. 2 (Jul. 24, 1959), p. 176

Lambert, S. and Ferguson, G. M. (1985) Blood Ejection Frequency by Phrynosoma cornutum (Iguanidae). The Southwestern Naturalist, Vol. 30, No. 4 (Nov. 27, 1985), pp. 616-617

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

Middendorf, G. A. and Sherbrooke, W. C. (1992) Canid Elicitation of Blood-Squirting in a Horned Lizard (Phrynosoma cornutum). Copeia, Vol. 1992, No. 2 (May 1, 1992), pp. 519-527

Middendorf, G. A.; Sherbrooke, W. C.; and Braun, E. J. (2001) Comparison of Blood Squirted from the Circumorbital Sinus and Systemic Blood in a Horned Lizard, Phrynosoma cornutum. The Southwestern Naturalist, Vol. 46, No. 3 (Sep., 2001), pp. 384-387

Pianka, E. R. and Parker, W. S. (1975) Ecology of Horned Lizards: A Review with Special Reference to Phrynosoma platyrhinos. Copeia, Vol. 1975, No. 1 (Feb. 28, 1975), pp. 141-162

Schmidt, P. J.; Sherbrooke, W. C.; and Schmidt, J. O. (1989) The Detoxification of Ant (Pogonomyrmex) Venom by a Blood Factor in Horned Lizards (Phrynosoma). Copeia, Vol. 1989, No. 3 (Aug. 8, 1989), pp. 603-607

Sherbrooke, W. C. and Middendorf, G. A. (2004) Responses of Kit Foxes (Vulpes macrotis) to Antipredator Blood-Squirting and Blood of Texas Horned Lizards (Phrynosoma cornutum). Copeia, Vol. 2004, No. 3 (Aug. 20, 2004), pp. 652-658