Of the many unlikeable and inaccurate stereotypes maintained about animals in popular consciousness, among the most frustrating is what I term "old man turtle". This is the idea that turtles (by which I mean, all members of Testudines) are like decrepit, weak, bony little old men housed inside a box. It's not fair, and it's not at all accurate.


Here we look at just one aspect of turtle anatomy. In keeping with the stupid "old man turtle" idea, popular culture would have it that turtles are weak, flaccid, crappy organisms with dull social lives, stunted and barely functional internal organs and undersized sex organs. Well, wait a goddam minute…

Warning: the following article may be considered unsuitable for viewing by minors, or anyone frightened by the alien penivagina cobra in Prometheus... because that thing is tame compared to the penis of a turtle.




Believe it or don't, turtles are horrifically well endowed, and if the thought of learning more about the genitals of these oh-so-surprising reptiles doesn't appeal to you, look away now. Last warning. Ok, here we go.

Hydraulic intromittent male sexual organs – a variety of popular, alternative names are available – are not unique to mammals among tetrapods. They're also present in squamates, archosaurs and turtles. This phylogenetic distribution has led some authors to conclude that these organs were present in amniote common ancestors. However, in their details, the organs of these groups are all quite different and actually formed from non-homologous tissues. As shown by Kelly (2002), male intromittent organs therefore arose independently among tetrapods on more than one occasion. The turtle penis, for example, contains only one vascular erectile body and develops on the ventral surface of the cloaca, whereas the mammal penis contains two erectile bodies and is derived from non-cloacal tissue. In the diagram above – from Kelly (2002) – the penises of turtles, birds, mammals and snakes are compared in transverse section. Note how different the organs are in their cross-sectional structure.

Penis or phallus? Ahh, choice.

An intromittent organ of this sort is typically termed a ‘penis'. Some researchers suggest that this term should be restricted to mammals and that the convergently similar organs of turtles and archosaurs should be termed phalluses instead (Isles 2009). However, others argue that there's nothing about the term ‘penis' that means it has to be restricted in this way, and indeed there's nothing particularly special about the mammal penis when we compare it with the intromittent organs of other tetrapods. Accordingly, some biologists who publish on intromittent organs consistently term all of these organs penises (e.g., Kelly 2002, 2004, McCracken 2000). Biologists certainly haven't had a problem in using the term ‘penis' for the turtle organ in the past (e.g., Zug 1966).


How to build a turtle penis

The turtle penis is, like that of a mammal, a hydraulic cylinder that becomes engorged by fluid and is relatively resistant to bending when erect. Its single erectile body is divided into a collagenous corpus fibrosum and a highly vascularized, expandable corpus spongiosum. As a turtle's penis inflates, its length may increase by nearly 50%, its width by 75%, and its depth by 10%. Even an uninflated penis – tucked away inside the cloaca – is large. More on the issue of size later on.


A pair of long retractor muscles extend for most of the length of the organ's dorsal surface, and attach within the body cavity to the lumbar vertebrae. When at rest, the penis is doubled up on itself within the cloaca, and it's the contraction of the retractor muscles that causes it to un-double and protrude (Gadow 1887). During erection, the penis first emerges pointing posteriorly; "as the size and tension increases the penis bends ventrally and then slightly anteriorly" (Zug 1966, p. 4). Bishop & Kendall (1929) found that turtle penis retractor muscles were "physiologically rugged" and of "extreme endurance".


Collagen fibres reinforce the penis wall and are arranged either along, or perpendicular to, the organ's long axis, and in this respect the turtle penis is superficially similar to a mammalian one. However, while the mammal penis only has one layer of long-axis fibres, and one layer of perpendicular fibres, the walls of the turtle penis have multiple layers of these fibres. This array of stiffening collagenous fibres is still, however, highly similar in turtles and mammals: as noted by Diane Kelly in the title to her 2004 paper "Turtle and mammal penis designs are anatomically convergent" (Kelly 2004). The strong similarity observed in the erectile organs of these phylogenetically disparate groups suggests that there are few functional solutions permitting the evolution of cylindrical, inflatable intromittent organs (Kelly 2002, 2004). Kelly is well known for her previous work, widely reported in the media, on penis anatomy in armadillos (Kelly 1997) collected as roadkills near Tallahassee, Florida. Her publications can be obtained, free, from her homepage here.

In terms of overall macrostructure, the turtle penis consists of a shaft and a distinct head, or glans, that's typically dark grey, purple or blackish.


A long seminal groove, surrounded on both sides by raised ridges (termed seminal ridges), extends from the urethral opening down at the base of the penis to the glans. Obviously, we're talking here of an exposed groove, not an enclosed internal tube like that present in mammals. Mammals are actually unusual in possessing an enclosed tube in the penis: seminal grooves are the norm when we look at the organs of lizards and snakes, crocodilians and birds.

The seminal ridges in a turtle are largest right next to the glans; near the glans, they're surrounded on both sides by fissures, or sinuses. Anterior and posterior pairs of sinuses are also present on the upper surface of the glans. These structures, associated with mobile skin folds, give the glans a decidedly alien-like, unfamiliar look to we primates. Turtles seem to be able to control the movements of the ridges around the seminal groove as well as the openings and folds on the head of the glans. The structures on the upper surface of the glans can in fact open and close, in ‘flower-like' fashion, in a sort of pulsing or throbbing motion. There are some especially endearing videos showing this on youtube (one, featured here, shows a Red-footed tortoise Chelonoidis carbonaria forming a strong relationship with a rubber ball). However you respond to these images, don't feel ashamed.


The precise configuration of sinuses and associated folds, and thus the overall form of the glans, varies from group to group (Zug 1966). Some of the configurations involved look terrifying; others look really terrifying. The penis as a whole is seemingly simplest in sea turtles*. Here, the glans is pointed, with the seminal groove terminating in a single, deep fold. In mud turtles (Kinosternidae), big-headed turtles (Platysternon), land tortoises (Testudinidae), and batagurid and emydid river turtles, the glans is broad and fat. In many species, there's a pointed medial process at the tip of the glans. In land tortoises and the New Guinea pig-nosed turtle (Carettochelys insculpta), the seminal groove is bifurcated at its distal end; in Carettochelys, the tip of the glans has a tri-lobed appearance where each branch of the seminal groove extends distolaterally into its own lateral lobe, separated on the midline by a distomedial lobe (Zug 1966). Carettochelys is odd in lacking sinuses on its penis.


* Some experts prefer to write the name ‘seaturtle'. I don't think that this suggestion has caught on yet, so will stick with ‘sea turtle' here (and equivalent terms for other turtle groups).


Softshell turtles (Trionychidae) go one (or two) better, since their glans is five-lobed. Again, the seminal groove is bifurcated, with each branch leading distolaterally to the tip of a pointed proximolateral structure. But, before reaching the tip of that proximolateral structure, the groove branches again, with this more distal branch of the groove extending to the tip of a pointed distolateral structure (Zug 1966). Softshell turtles thus discharge semen from four distinct branches of the seminal groove. This might leave you wondering what the insides of a female softshell's cloaca are like. That's an issue I should discuss some other time.

Why do we need phylogenies? Why? To give us an evolutionary backbone to hang our hypotheses on, stupid.

Incidentally, the anatomically ‘simple' penis present in sea turtles has sometimes been regarded as peculiar given that phylogenies typically find this group to be nested fairly deep within Cryptodira (the so-called ‘hidden-necked turtle' clade). This topology means that sea turtles are surrounded in the phylogeny by softshells, snapping turtles, mud turtles and tortoises and river turtles (e.g., Gaffney & Melyan 1988, Shaffer et al. 1997, Hirayama et al. 2000), all of which have complex penises.


So, is it that the sea turtle penis has become secondarily ‘simplified' – presumably as a consequence of adaptation to pelagic life – or is it that the different, complex penises present in the other lineages evolved their complexity independently? To be honest, this issue hasn't been examined in detail in any phylogenetic analysis (to my knowledge). However, Joyce (2007) has more recently found sea turtles to be the sister-group to all remaining cryptodires. If this is correct, it might mean that the simplicity of the sea turtle penis is a primitive feature… but what about pleurodires (the so-called ‘side-necked turtles')?


Pleurodires – the closest living relatives of cryptodires – aren't as well studied as cryptodires, and less information is available on their genitalia. What little data I've seen (e.g., Cabral et al. 2011) suggests that the penises of some taxa at least are simple (that is, with a slender, pointed glans and little in the way of crazy folds and lobes) and superficially similar to those of sea turtles. My impression at the moment is that pleurodires and sea turtles share a ‘simple' penis as a symplesiomorphy (= shared primitive character), but this could be very wrong since I've seen little information on the pleurodire penis.


How big? BIG.

As interesting as it is from the point of view of embryology, phylogeny, microanatomy and detailed anatomy, one thing particularly eye-opening (no pun intended) about the turtle penis is its SIZE. It really is large and formidable in some species. It's perfectly normal for some tortoise species to have a penis that is half the length, or more, of the plastron. I would guess that in a tortoise with a total length of 20 cm, the penis might be 8 cm long. (Featured here are giant tortoises mating. These animals are identified on wikipedia as Galapagos tortoises, but - following help from Jeannot Tihoti Maha'a - I think they're Aldabran giants. Look carefully! Photo by Minglex, licensed under Creative Commons Attribution 3.0 Unported license.)


So, small turtles can have proportionally huge organs. What about big turtles? Unfortunately, little data is available. A few days ago, Roger Close asked me on facebook if we know anything about the size of the male organ in Galápagos giant tortoises (Chelonoidis nigra and kin). While mating behaviour in Galápagos tortoises has been filmed many times, I have yet to see any good images of genital anatomy in these animals. Petterer & Neuville (1914) described penis morphology in Aldabran giant tortoises Aldabrachelys gigantea*, but didn't provide much information. If you have useful data, please say so!

*If you follow these things, I would say that this name has rightfully won out over Dipsochelys dussumieri. Does anyone know if the ICZN has published a ruling yet?


Sea turtles are another group of turtles famous for reaching large size. Surely they have large penises. Yup. In a Green turtle Chelonia mydas (maximum length c. 1.5 m, carapace length c. 80-110 cm), the penis is typically more than 30 cm long (Hamann et al. 2003). Hold your hands 30 cm apart and think about that enormous penis for just a moment.


What about the Leathery turtle Dermochelys coriacea? This amazing giant can exceed 2.2 m in total length and have a carapace length of 1.7 m. The original version of the article you're reading now was published back in 2007, and since then a Leathery turtle Dermochelys coriacea dissection has been featured on TV as part of the fantastic series Inside Nature's Giants. Unfortunately, I missed it when it was on and haven't been able to see it yet. Joy Reidenberg told me at the time that the male individual they examined was, indeed, well endowed. As you can see from the two screen-shots shown here, she wasn't kidding. [Thanks loads to Markus Bühler and Emilio Río Rodríguez for help in getting the images at short notice.]

You have an enormous penis — so, what do you do with it?

While it might seem like a bloody stupid question, you have to wonder exactly what it is that turtles do with these sometimes enormous organs. The evolution of the shell probably means that male turtles were forced to evolve innovative penises in order to make genital contact with their partners. In sea turtles, males have proportionally enlarged, prehensile tails, and the tails of other kinds of turtle are also usually longer and bulkier in males than they are in females. The cloaca isn't situated at the base of the tail, but some distance along its length, so it seems that part of the distance that the penis needs to reach in order to inseminate the female is covered by tail-reach, not by penis-reach alone. Incidentally, some fossil Cretaceous sea turtles have really long tails – way longer than those of any modern sea turtles. This may or may not mean something for penis anatomy, but I don't think we'll ever know.


As is the case in other tetrapods that possess proportionally large sexual organs (including certain ducks, cetaceans and, yes, some primates), observational data suggests that male turtles might employ their organs in display or aggression. Honda (2001) had this to say about captive specimens of the Common box turtle Terrapene carolina:

Sometimes males will distend their organ neither while mating, nor while in the presence of females. Usually while bathing or drinking, the turtle will submerge the front half of his body, rise up on his back legs, and drop his organ through the cloaca. It is a sight to behold, and one that can startle both novice and experienced herpetoculturalists alike. The organ itself is large in proportion to the turtle, and dark purple in color. After several seconds, the turtle will retract the organ back through the cloaca. It may repeat this process once or twice.


I also note the very interesting paper by de Solla et al. (2001): "Penis displays of common snapping turtles (Chelydra serpentina, pictured here) in response to handling: defensive or displacement behaviour?". [Adjacent photo credited to /r/Pics]. Leatherback turtles are also known to evert the penis as a response to handling (James 2004), and this behaviour has also been reported in pleurodires (Hydromedusa) and other turtles.


However, as tempting as it might be to imagine that some turtles are perhaps in the habit of intimidating enemies or competitors with their erect, 20-cm long, black, spike-tipped penises, it seems more likely that this penis eversion most often occurs as a displacement behaviour, practised when the animal's plastron is touched. Then again, given what we now know about play behaviour in turtles and other reptiles, it should be considered plausible that turtles expose their impressive genitals for fun, or when bored.

And that is just about everything I know about turtle penises. Well, there's the TMNT porn, slash fiction and so on that I've discovered online, but let's not mention that. To those of you who recall reading this article the first time round (as I said above, it first appeared at Tet Zoo ver 2 back in 2007), I hope you enjoyed revisiting it in updated, augmented form. To those of you for whom this information is new… I trust that you'll never look at a turtle in the same way again.



This post by Darren Naish originally appeared at Scientific American's Tetrapod Zoology. Naish is a science writer, technical editor and palaeozoologist (affiliated with the University of Southampton, UK). He mostly works on Cretaceous dinosaurs and pterosaurs but has an avid interest in all things tetrapod. He has been blogging at Tetrapod Zoology since 2006.

Top image via Shutterstock

References

Bishop, G. H. & Kendall, A. I. 1929. Action of formalin and histamine on tension and potential curves of a striated muscle, the retractor penis of the turtle. American Journal of Physiology 88, 77-86.


Cabral, S. R. P., de Souza Santos, L. R. Franco-Belussi, L., Zieri, R., Zago, C. E. S. & de Oliveira, C. 2011. Anatomy of the male reproductive system of Phrynops geoffroanus (Testudines: Chelidae). Acta Scientiarium: Biological Sciences 33, 487-492.

de Solla, S. R., Portelli, M., Spiro, H. & Brooks, R. J. 2001. Penis displays of common snapping turtles (Chelydra serpentina) in response to handling: defensive or displacement behaviour? Chelonian Conservation and Biology 4, 187-189.


Gadow, H. 1887. Remarks on the cloaca and on the copulatory organs of the Amniota. Philosophical Transactions of the Royal Society of London B 178, 5-37.

Gaffney, E. S. & Meylan, P. A. 1988. A phylogeny of turtles. In Benton, M. J. (ed) The Phylogeny and Classification of the Tetrapods, Volume 1: Amphibians, Reptiles, Birds. Clarendon Press (Oxford), pp. 157-219.


Hamann, M., Limpus, C. J. & Owens, D. W. 2003. Reproductive cycles of males and females. In Lutz, P. L., Musick, J. A. & Wyneken, J. (eds) The Biology of Sea Turtles, Vol. II. CRC Press, Boca Raton (Florida), pp. 135-161.

Hirayama, R., Brinkman, D. B. & I. G. Danilov. 2000. Distribution and biogeography of non-marine Cretaceous turtles. Russian Journal of Herpetology 7, 181-198.


Honda, M. 2001. Chelonian notes. Art Journal 60 (2), 96-100.

Isles, T. E. 2009. The socio-sexual behaviour of extant archosaurs: implications for understanding dinosaur behaviour. Historical Biology 21, 139-214.


James, M. C. 2004. Dermochelys coriacea (Leatherback sea turtle). Penis display. Herpetological Review 35, 264-265.

Joyce, W. G. 2007. Phylogenetic relationships of Mesozoic turtles. Bulletin of the Peabody Museum of Natural History 48, 3-102


Kelly, D. A. 1997. Axial orthogonal fiber reinforcement in the penis of the nine banded armadillo (Dasypus novemcinctus). Journal of Morphology 233, 249-255

Kelly, D. (2002). The Functional Morphology of Penile Erection: Tissue Designs for Increasing and Maintaining Stiffness. Integrative and Comparative Biology, 42 (2), 216-221 DOI: 10.1093/icb/42.2.216


- . 2004. Turtle and mammal penis designs are anatomically convergent. Proceedings of the Royal Society of London B 271 (Suppl 5), S293-S295.

McCracken, K. G. 2000. The 20-cm spiny penis of the Argentine lake duck (Oxyura vittata). The Auk 820-825.


Petterer, E. & Neuville, H. 1914. Du penis et du clitoris des crocodiles et des tortues. Rendu Hebdomadaire des Seances et Memoires de la Societe de Biologie, Paris 76, 101-103.

Shaffer, H. B., Meylan, P. & McKnight, M. L. 1997. Tests of turtle phylogeny: Molecular, morphological, and paleontological approaches. Systematic Biology 46, 235-268.


Zug, G. R. 1966. The penial morphology and the relationships of cryptodiran turtles. Occasional Papers of the Museum of Zoology, University of Michigan 647, 1-24.