The following is a quick review for the new book by J. Sean Doody, Vladimir Dinets, and Gordon M. Burghardt. The book came out last year and I feel like it received relatively little fanfare in the paleo and herpetological circles (though I did come across one review from the British Herpetological Society, as well as this podcast interview with Sean Doody).
The TL;DR version of this post is as follows: The Secret Social Lives of Reptiles is a landmark piece of literature that should become a foundational reference for any future study looking at reptile behaviour. The authors firmly describes where we currently are in reptile social behaviour studies, and just how much further we can still go. It’s a must read for any budding herpetologist, and a highly recommended read for herpetoculturalists / reptile fans. The best part of the book is its extensive bibliography, which offers a strong launching point for anyone interested in studying reptile behaviour. If you study any aspect of reptiles as organisms, then this book deserves a spot on your shelf.
So, go out and get it.
For more specifics about the book, feel free to read on from here.
Megalochelys atlas skeleton on display at the AMNH. Photo by Clair Houck (Wikipedia)
Today, the largest turtle alive is easily the leatherback turtle (Dermochelys coriacea), at a whopping 916 kg (2,015 lbs, Eckert & Luginbuhl 1988). On land, the largest turtle goes to Chelonoidis nigra (Galápagos tortoise) which has been reliably recorded as reaching up to 417 kg (919 lbs) in weight (Guinness World Records). However, both extant turtles are dwarfed in size by an immense land tortoise that lived as little as 1.7 million years ago, in the Pleistocene.
Leatherbacks are already viewed as unique, but you might be surprised at just how strange this species really is. Picture from: amigosdomarnaescola.com
Continuing the series, let us now take a look at one weird turtle species in particular: Dermochelys coriacea, the leatherback sea turtle.
While the utter weirdness of D.coriacea is ultimately the main reason for why it wound up in this series, there is an ulterior motive. Having searched the internet for general information on the species I found myself rather disappointed with the amount of utterly generic / wrong info regarding leatherbacks. Its Wikipedia entry is particularly disappointing. So here’s hoping this influx of information can help alleviate that.
A turtle without a shell?
Yes, it’s true, leatherback turtles have lost their shells. Shell reduction is relatively common in turtles. It seems a little funny. After going through all the trouble of evolving impregnable armour, many taxa then went out and removed large chunks of it. We see shell reduction in snapping turtles (Chelydra and Macrochelys), soft-shelled turtles, and even other sea turtles. None of them, however, reduced their shells to the point of actually removing them.
In leatherbacks the “shell” is nothing more than a loose collection of osteoderms spread over the back and belly. There is no longer a definitive carapace, or plastron. In fact leatherbacks don’t even produce Beta-keratin (the hard component of reptile scales). Instead this has all been replaced by thick, leathery skin.
A Galapagos tortoise struts about, secure in the knowledge that no one will ever know where the hell it came from. Photo from petcaregt.com
This is a long overdue follow up to my original Turtle Power article back in…yeah never mind the date.
As established previously, turtles are a strange, and highly diverse group of animals, but how did they come to be this way?
The turtle bauplan has been a phylogenetic double edged sword. On the one hand, the unique shell design, and the necessary body contortions associated with it, make chelonians a very easy group to classify. However, it is these same peculiarities that keep us from finding the ancestor to turtles. To date, there are no “half-turtles.” No good transitionals between one reptile group to that of turtles. As such, the list of turtle ancestors runs all over Reptilia. Some paleontologists believe the origin lies at the base with reptiles like procolophonoids, and pareiasaurs. Others believe turtles are a bit more closely related to extant reptiles, and belong in, or alongside the sauropterygians (plesiosaurs, nothosaurs, and placodonts). There is even some evidence to suggest turtles are actually in the same reptile group as dinosaurs and crocodylians (Archosauria).
Curse that shell! - Photo by tompain
How can the list be this extensive? Read on to find out.
Continuing my trend of “catching up,” an article in the November issue of Natural History magazine, talks about a new study in the Quarterly Review of Biology, that finds group nesting to be very common place among extant reptiles.
That study would be:
Doody, J.S., Freedberg, S., Keogh, J.S.? 2009. Communal Egg-Laying in Reptiles and Amphibians: Evolutionary Patterns and Hypotheses. Quart. Rev. Biol. Vol.84(3):229-252.
In the paper, Doody et al (no laughing) did a massive search through the herpetological literature (both technical journals, and hobbyist magazines) to look at instances of communal egg laying in reptiles and amphibians (herps). I’m not being hyperbolic here either, as the paper states:
In total, our assembled database was gathered from 290 different sources, including 176 different scientific journals, 72 books or book chapters, 29 unpublished reports, and 13 unpublished theses. We also have included a number of reliable personal communications from herpetologists.
What the authors found was that group gatherings of herps are vastly more common than previously believed. Group egg laying was found to be present in 345 reptile species. Now you might be thinking 345 really isn’t all that much for a group composed of some 8700 species.
Well then aren’t you a Debbie Downer?
Ophisaurus attentuatus brooding her eggs.
Seriously though, the authors address this by mentioning:
Although the difficulty in locating nests hampers our ability to determine the actual frequency of communal egg-laying among species, we can better estimate this proportion by dividing the number of known communally egg-laying species by the total number of species, excluding those for which eggs have not been found. We conducted such a calculation for the three families of Australian lizards known to include multiple communally egg-laying species—Gekkonidae, Pygopodidae, and Scincidae—as gleaned from the Encyclopedia of Australian Reptiles database (Greer 2004). Proportions of these lizard families known to lay communally were 4–9%, but, when we exclude species for which nests are not known, these values rise dramatically to 73–100%
The biggest take home message to get from Doody et al’s review, is just how much we don’t know about extant reptiles.
…the present review highlights our inadequate knowledge of the nests and/or eggs of reptiles. For instance, the eggs or nests are known in only 7% of Australian lizards of the three families that commonly lay communally (N = 411 oviparous spp.) (Greer 2004).The extent of this knowledge for Australian lizards is probably similar to that for reptile eggs on other continents, particularly South America, Africa, and Asia, where the reproductive habits of reptiles are poorly known. This is in stark contrast to other vertebrates such as birds, for which complete field guides to the eggs and nests are available for several continents
Indeed, just by doing the brief research run needed to compile this blog post, it was apparent that communalism is much more common in reptiles than anyone ever thought. However, because so many of these reports are either anecdotal, or buried in obscure journals, it is easy to miss all the many cases where it is known.
This discovery lead the authors to the inevitable follow up question of: “why?” What benefit do mothers gain by nesting communally?
Numerous hypotheses for why animals nest communally, have been proposed.
Saturated habitat (only so many suitable nest sites)
Sexual selection (choice of males that live in a particular area)
Artifact of grouping for other reasons
Attack abatement (easier to hide a bunch of eggs in one site, than in multiple sites. Less chance that your eggs will be the ones that are eaten).
Maternal Benefits (save time and energy finding a suitable nest site by “freeloading”)
Reproductive success (if the nest site worked once before…)
Egg insulation
The authors reviewed all of these possible reasons for communal egg laying in herps. In the end, they found evidence for both the maternal benefits hypothesis, and the reproductive success hypothesis, though they felt a mixed model better explained things.
Python brooding her eggs.
Sadly, though the authors mentioned how a lack of information on the natural history of most reptiles is largely responsible for this sudden revelation about their nesting behavior, they nevertheless make repeated mentions of how “social interactions are generally less complex in reptiles and amphibians than in other tetrapods” or how herp sociality forms “relatively simple systems“.
The reality is that the old view of simplistic “loner” reptiles that only come together to mate, is not accurate. This is especially true for parental care in reptiles.
The popular view (among the public, and the scientific community) is that reptiles are “lay’em and leave’em” types when it comes to reproduction. Despite all the herpetological knowledge to the contrary that has been acquired in the past 50 years, it is still popular to spout the party line about reptiles being “uncaring parents.”
Zoologist Louis Somma took issue with this view of reptilian (in particular, chelonian and lepidosaurian) parenting. He conducted a literature search to see how often mentions of parental care in reptiles are recorded. In the end he wound up finding 1400 references to parental care in reptiles (Somma 2003)!
Somma’s survey covered various aspects of parental care. He found reported evidence of nest building and / or guarding in tortoises like Manouria emys (McKeown 1999), Gopherus agassizii (Barrett & Humphreys 1986) and 4 other species of chelonian.
Turning to lepidosaurs, Somma found parental behaviour to be present in 133 species of lizards and 102 species of snakes. Even a species of tuatara (Sphenodon punctatus) is known to guard its nests (Refsnider et al. 2009). Though these numbers appear small compared to the total amount of species that have been described; much like the Doody et al. paper, this is just based off of species whose nesting behaviours we do know. That these taxa all span a wide phylogenetic range, suggests that parental care is more commonplace than initially thought.
Nest guarding is usually a maternal trait, but some squamates exhibit nest guarding behaviour in both parents, such as some cobra and crotaline snakes (Manthey and Grossman 1997) , as well as tokay geckos (Zaworski 1987).
Not only active guarding of the nest, but actual brooding of the eggs is also commonly reported in squamates such as various python species (Harlow & Grigg 1984, Lourdais et al. 2007), and skinks (Hasegawa 1985, Somma & Fawcett 1989). Some species are even known to groom their newly hatched young (Somma 1987).
More interesting still are various reports and observations of parental feeding in some reptile species, such as the skink Eumeces obsoletus (Evans 1959), and the cordylid lizard Cordylus cataphractus (Branch 1998). Not to mention recent evidence of parental feeding in captive crocodylians.
This leads me to the only reptile group where parental care is well publicized: that of the 23 extant crocodylian species. I could, at this point, list references for parental care in crocodylians. However because this behaviour is so well documented for this group, it would seem unnecessary. It is better to shed light on the many (MANY) examples of parental care in other reptile species. I also didn’t include related examples like placental evolution in the skink genus Mabuya, or instances of egg binding in captive reptile mothers; due to a lack of appropriate substrate to lay their eggs.
In the end, the paper by Doody et al. adds to a growing body of evidence which suggests that the “lay’em and leave’em” reptile species of the world, are the exceptions? and not the rule.
~ Jura
Next time: Biomechanics of running suggest “warm-blooded” dinosaurs. Or: why the aerobic capacity model needs to die already.
References
Barrett, S.L. & Humphrey, J.A. 1986. Agonistic Interactions Between Gopherus agassizii (Testudinidae)
and Heloderma suspectum (Helodermatidae). Southwestern Naturalist, 31: 261-263.
Branch, B.. 1998. Field Guide to Snakes and Other Reptiles of Southern Africa. Third revised edition. Sanibel Island: Ralph Curtis Books Publishing.
Doody, J.S., Freedberg, S., Keogh, J.S.? 2009. Communal Egg-Laying in Reptiles and Amphibians: Evolutionary Patterns and Hypotheses. Quart. Rev. Biol. Vol.84(3):229-252.
Evans, L.T. 1959. A Motion Picture Study of Maternal Behavior of the Lizard, Eumeces obsoletus Baird and Girard. Copeia, 1959: 103-110.
Harlow, P and Grigg, G. 1984. Shivering Thermogenesis in a Brooding Python, Python spilotes spilotes. Copeia. Vol.4:959?965.
Hasegawa, M. 1985. Effect of Brooding on Egg Mortality in the Lizard Eumeces okadae on Miyake-jima, Izu Islands, Japan. Copeia, 1985: 497-500.
Lourdais, O., Hoffman, T.C.M., DeNardo, D.F. 2007. Maternal Brooding in the Children’s Python (Antaresia childreni) Promotes Egg Water Balance. J. Comp. Physiol. B. Vol.177:560-577.
Manthey, U. and W. Grossman. 1997. Amphibein & Reptilien S?dostasiens. Natur und Tier Verlag, M?nster.
Mckeown, S. 1999. Nest Mounding and Egg Guarding of the Asian Forest Tortoise (Manouria emys). Reptiles, 7(9): 70-83.
Refsnider, J.M., Keall, S.N., Daugherty, C.H., & Nelson, N.J. 2009. Does nest-guarding in Female Tuatara (Sphenodon punctatus) Reduce Nest Destruction by Conspecific Females? Journal of Herpetology. vol.43(2):294-299.
Somma, L.A. 1987. Maternal Care of Neonates in the Prairie Skink, Eumeces septentrionalis. Great Basin Naturalist, 47: 536-537.
Somma, L.A. & Fawcett, J.D. 1989. Brooding Behaviour of the Prairie Skink, Eumeces septentrionalis, and its Relationship to the Hydric Environment of the Nest. Zoological Journal of the Linnean Society. Vol.95: 245-256.
Somma, L. 2003. parental Behavior in Lepidosaurian and Testudinian Reptiles: A Literature Survey. Krieger Publishing Company. 174pgs. ISBN: 157524201X
Zaworksi, J.P. 1987. Egg Guarding Behavior by Male Gekko gecko. Bulletin of the Chicago Herpetological Society, 22: 193.
They are such a unique group of animals, that one can’t help but be drawn to them. Yet despite their uniqueness, turtles tend to get thrown into the wastebin of “living fossils”. It’s not uncommon to hear documentaries, or books refer to turtles as having been static since their first appearance 200+ million years ago. It’s unfortunate because statements like these tend to downplay just how weird and wonderful turtles really are.
So why are turtles so weird? Well, as one might expect, it’s all about the shell. The turtle shell is an iconic image. Everyone knows what a turtle basically looks like. Even strange turtles like the mata mata (Chelus fimbriatus) are still recognizable as turtles. Contrary to popular belief, turtles can neither come out of their shells, nor does the shell act as their home. One cannot pull a turtle from its shell. The shell is the result of a phenomenal transformation of the backbone, ribcage, sternum, clavicles and gastralia.
Turtle shells are different from the armoured “shells” seen on dinosaurs like the ankylosaurs. It is also fundamentally different from the armour seen on armadillos, crocodylians and every other vertebrate out there. In all these other animals, the armour is composed of bony plates that are formed from bone which is made intramembranously in the dermal portions of the body. Turtles are the only animals we know of that develop their armour by using this dermal bone in conjunction with endochondral bones (i.e.. the vertebrae and rib cage).
A turtle “coming out of its shell.” Image from the Encarta website.
It is at this point that turtles go from simply being unique, to just being weird. In order for the shell to protect the exposed limbs and head, the shell had to engulf the limb girdles. The rib cage had to actually grow over the pectoral and pelvic girdles. Think about that for a minute. Take a look in the mirror sometime and see how your arms are placed. Our arms, and the arms of every other tetrapod alive today, are set outside the rib cage. In fact, we actually can (and do) rest our arms along the outside of our ribs. Turtles can’t do that. Having one’s ribs on the outside can really hamper the ability to move the arms. The arms can extend, but they cannot bend without banging into the ribs. In order to fix this, turtles had to reverse the way their arms bend. Turtle arms bend towards one another, rather than away as they do in all other tetrapods. Imagine if your arms bent like your legs do, and you get the idea. Protection of the head required another unique innovation. Namely, turtles had to become double jointed. Turtle neck articulation follows a standard “ball and socket” arrangement that is widespread among various extant reptiles. However, within each species there is between one and two vertebrae that feature a “ball” on both sides (Romer, 1956). This biconcavity creates a hinge joint that can bend a full 90°. It is this special joint, more than anything else, that allows turtles to contort their necks in such a manner. For pleurodires, as the name implies, this articulation allows the neck to be tucked to the side of the body under a lip of the carapace. For cryptodires, these double joints allow the head and neck to literally go inside the body cavity; something no other tetrapod can do, and something that is decidedly weird. 🙂 Another issue with having a shell composed of fused ribs and vertebrae, is that flexibility is reduced to zero. This has a huge effect on speed. Turtles cannot extend their stride by bending their spine; a behaviour that all other tetrapods are capable of . The only way to increase stride length is to increase the lengths of the limbs. This puts an immediate limit on turtle speed. While longer limbs could be evolved, they would not be able to fit inside the shell. The only way for a turtle to go faster is to speed up the stride frequency. Turtles were thus forced to give up on ever being speedy. Though there are some chelonian members (e.g. my Terrapene ornata luteola) which put that statement to the test.
Yet another weird characteristic of turtles is how they have circumvented the issue of breathing while encased in armour.
Normally, in tetrapods, breathing is achieved through the bellow like pumping of the lungs. This is accomplished by muscles connected to the ribs. These muscles expand the ribcage, allowing air to enter. As turtles no longer had the joints that allow the ribs to move, they lost the muscles that moved them. This creates a problem unique to turtles. How does one get air both in, and out of the body cavity. This is a problem that seems to have been solved multiple times in turtle evolution. Tortoises can “rock” their pectoral girdles back and forth in order to pump the lungs. Many semi-aquatic turtles can use the buoyancy of water to push air out of their lungs, while others can use the weight of their viscera to pull down on the lungs and allow air in. Many, though, have evolved sheets of muscle connected to the lungs, which will either expand, or contract the lungs and allow for respiration. Some, such as box turtles (Terrapene) require a sheets of muscle that will both expand and contract the lungs. In these animals, both inhalation and exhalation, are an energetic process. The upshot to this, is that by having independent muscles for respiration, box turtles are able to breathe even when fully sealed inside their shells (Landberg et al, 2003).
One strange aspect of chelonians that is rarely brought up, is how incredibly diversified they are. If turtles had died out at the end of the Mesozoic, and all we had to go on were fossils, I doubt we would ever have realized just how “flexible” the turtle bodyplan actually is.
Despite being encased in a shell both above and below, turtles are capable of chasing down prey (e.g. Trionyx and Apalone). Some are adept excavators; making extensive burrows that can run as long as 9 meters (30ft) and be 3.6m (12ft) deep (Gopherus agassizii). Still others like pancake tortoises (Malacochersis tornieri) are proficient rock climbers. Probably most surprising are musk turtles (Sternotherus). These normally waterbound turtles are quite adept tree climbers. Sternotherus minor has been observed scaling cypress trees up to 2 meters (Orenstein, 2001). Both of these species have relatively small plastrons which give them added flexibility. Still, even stiffened tanks like Leopard tortoises (Geochelone pardalis ) have been observed scaling fences that were blocking their way. The animals would climb up one side and then just topple over the other (Orenstein, 2001).
Some, such as the big-headed turtle (Platysternon megacephalum) have evolved huge heads with strong jaws for crushing shellfish. Others are efficient filter feeders (Podocnemis unifilis); sieving the water of small food particles.
Many freshwater turtle species have re-evolved ?gills.? These are areas of thin, permeable skin usually around their cloaca. This allows these species to take in oxygen through the water.
Lastly, turtles don’t grow old (Congdon, 1992). Unlike most other animals, turtles show little to no signs of age related deterioration. 74 year old three toed box turtles (Terrapene carolina triunguis) were found to be just as reproductively active as turtles some 40 years younger than them. (Miller, 2001).
So chelonians are weird, but how did they come to be this way? For that, you’ll have to stay tuned.
~Jura
Extra geek points to folks who got the reference to the Partners in Kryme song from the first TMNT movie. Id est: the original turtle rap. None of that Vanilla Ice crap.
References
Congdon, J. 1992. Senescence in Turtles: Evidence from Three Decades of Study on the E. S. George Reserve. Senescence in Organisms in Natural Populations. American Association of Gerontologists. Washington, D.C.
Landberg, T., Mailhot, J.D., Brainerd, E.L. 2003. Lung Ventilation During Treadmill Locomotion in a Terrestrial Turtle, Terrapene carolina. J.Exp.Biol. Vol. 206: 3391-3404.
Miller, J.K. 2001. Escaping Senescence: Demographic Data from the Three-Toed Box Turtle (Terrapene carolina triunguis).
Orenstein, R. 2001. Turtles, Tortoises and Terrapins: Survivors in Armor. Firefly Books. 304 pps. ISBN 1-55209-605-X
Romer, A.S. 1956. Osteology of the Reptiles. U.Chicago Press. ISBN: 0-89464-985-x 772pps
It has been a painfully slow week in terms of herpetology and paleo. I’ve noticed that when I tend to talk about things being slow, there is usually a sudden surge in topics. Here’s hoping that will happen this time too.
Though their’s is an old story, it’s so unique that I felt it deserved mentioning on my site at least once.Plus it was recently dugg, so I felt a need to respond.
For those who don’t know the story; back in 2004 during the infamous tsunami disaster, a baby hippo was found stranded on a little piece of land out from the coast of Kenya. The baby hippo, Owen (named after one of the rescuers), was brought to Haller Park near Mombasa. There, the frightened hippo ran from its caretakers and hid by an old, crotchety aldabra tortoise (Geochelone gigantea) named Mzee (MIZ-ZAY). At first, Mzee wanted nothing to do with Owen, but the little (relatively speaking) hippo wouldn’t leave him alone. Eventually he grew to tolerate Owen’s constant harassment.
Then something wonderous happened. Mzee and Owen became friends. Owen would follow Mzee around everywhere. They would eat together, bathe together, and sleep together. Mzee (the tortoise) invented a way of speaking to Owen. When Mzee wanted to go somewhere, he would gently nibble the tail of Owen. Soon Owen caught on and would do the same, when he wanted to go somewhere. It was an awesome spectacle to behold. This was completely different from what we see with, say, humans and their pet dogs, or cats. It was also different from the agricultural relationship between humans and livestock, or ants and aphids. This was a case of a genuine friendship between two very different animals (separated by over 300 million years of evolution!).
Owen and Mzee had even developed their own way of talking to each other. They were also very protective. Neither would passively allow a human keeper to get near the other. It was and is one of the most heartwarming, and amazing things to ever be observed in the natural world.
In 2006, a children’s book was released, documenting the story. Owen and Mzee became world famous, with visitors wanting to see the dynamic duo in person.
Back in 2007, it was decided that Owen needed to make friends with other hippos. His relationship with Mzee resulted in Owen acting more, and more like a giant tortoise (a hilarious sight to behold). Unfortunately, the friend that they chose for Owen (a female named: Cleo), was too much of a rough houser with the giant tortoises, so they had to separate Owen and Mzee. It’s hard to say if either animal suffered any heartbreak from this separation (I haven’t read any mention of it anywhere). I also don’t know if the two guys are sharing adjacent enclosures, so they might be able to still hang out.
Nonetheless, the story of Owen and Mzee is one that will live in infamyfor the ages. An amazing case of inter-special friendship between a mammal and a reptile that, prior to this, no one probably ever thought was possible.
It’s amazing, and it’s all completely documented on their official site: OwenandMzee.com Make sure to watch the documentary. It’s a heartstring puller.
