Tag Archives: crocodilian

Crocodiles and Cane Toads

You can see them from a helicopter: the white, bloated bellies of dead crocodiles, limply floating down the Victoria River. Australian freshwater crocodiles live hard lives, and most hatchlings are quickly eaten by fish, herons, frogs, turtles, or adult crocodiles. By the time they reach adulthood, at more than 7 feet long, they’ve already proven themselves to be the toughest reptiles around, so finding dead ones didn’t used to be common. Starting in 2002 that began to change (Letnic et al. 2002). Bodies started turning up, floating on their backs, by the hundreds. In their stomachs, researchers found the culprit: cane toads.

Cane toads, an invasive species in Australia, are extremely toxic. Their skin and organs are filled with cardiac glycosides, molecules that induce heart failure. Pets that eat them often die. So do a few humans, who lick the toads hoping to experience the hallucinogenic effects* of toad poison.

A dead freshwater crocodile, after eating a cane toad. Photo by Adam Britton, used with permission.

A dead freshwater crocodile, after eating a cane toad. Photo by Adam Britton, used with permission.

The toads’ natural predators, to varying degrees, have evolved to handle toad poison (also called bufotoxin). Examples include certain army ants and the cat-eyed snakes, which eat the toads and their tadpoles with ease. Even outside the toads’ native range (tropical Latin America), predators are often able to tolerate them because they have already adapted to the toxins of their own local toads.

Australia has a special problem: the country has no native toads. None at all. Since the cane toads’ introduction, scientists have observed dramatic population declines in predatory reptiles, from monitor lizards to pythons to crocodiles. These reptiles are not adapted to living with toads: they don’t instinctively leave toads alone, and when they venture eat one, death by poison is often the result.

Australia is home to two crocodile species. The smaller of the two is the freshwater crocodile (Crocodylus johnstoni), which lives in ponds and the upper reaches of rivers, away from the northern coastline. At 7-10 feet in length, this species is not dangerous to humans unless provoked, instead subsisting on a diet of fish, amphibians, small mammals, and the like.

A freshwater crocodile. Photo by Richard Fisher, licensed under CC BY 2.0.

A freshwater crocodile. Photo by Richard Fisher, licensed under CC BY 2.0.

The larger is the saltwater crocodile (Crocodylus porosus), males of which are the largest crocodiles on earth, reaching lengths up to 20 feet. Although they often live alongside (and sometimes prey upon) freshwater crocodiles, saltwater crocodiles truly thrive in the more coastal habitats: estuaries, mangrove swamps, and sea-bound river deltas.

Both species are opportunists, and will happily snap up a toad if given the opportunity.

A saltwater crocodile. Photo by Lip Kee Yap, licensed under CC BY-SA 2.0.

A saltwater crocodile. Photo by Lip Kee Yap, licensed under CC BY-SA 2.0.

Dr.’s James Smith and Ben Phillips (2006) wanted to find out just how dangerous cane toads were to Australia’s native predators. They harvested the toxins from cane toads and then administered them to various Australian reptiles, including predatory lizards, pythons, and both crocodile species.

When scientists want to know how deadly a toxin is, they calculate LD50. The LD50, or median lethal dose, is simply the amount of poison that will on average cause the death of 50% of victims.

The LD50 depends both on the toxin and on the animal that ingests it. A rat, for example, has a 50% chance of death if it drinks 192 milligrams of caffeine for every kilogram that the rat weighs. Rats typically weigh about 1/3 of a kilogram, so the total LD50 for caffeine is 1/3 of 192, or 64 mg. More toxic substances have lower LD50’s, since it takes less poison to cause death. Caffeine isn’t that toxic. Aren’t numbers fun?

The mangrove monitor, a predator easily poisoned by cane toads. Photo by Jebulon, in public domain.

The mangrove monitor, a predator easily poisoned by cane toads. Photo by Jebulon, in public domain.

Smith and Phillips calculated that the LD50 for bufotoxin fed to freshwater crocodiles was about 2.76 milligrams. Cane toads, which can weigh up to 2 kilograms, are perfectly capable of killing freshwater crocodiles that eat them.

Here’s the odd thing: while freshwater crocodiles often died as a result of cane toad poisoning, none of the saltwater crocodiles did. To see if the poison was affecting them in other ways, the scientists conducted athletic tests — if the crocodile couldn’t run as fast after poisoning, that was interpreted as a sign the poison was harming the reptile. While the freshwater crocodiles slowed down after ingesting bufotoxin, saltwater crocodiles were just as energetic before as after their toxic meal.

Are saltwater crocodiles immune to bufotoxin? It’s hard to say. The scientists wanted to kill as few crocodiles as possible, and they didn’t have enough crocodiles on hand to test much higher doses. Perhaps extremely high doses of bufotoxin would kill saltwater crocodiles, but the data is lacking.

What we do know is that saltwater crocodiles are much more resistant to cane toad poison than freshwater crocodiles. There are two potential reasons for this, and the most obvious is size. Saltwater crocodiles, males of which can weigh more than 2,000 pounds, are the largest crocodilians and the largest non-marine predators in the world. An adult saltwater crocodile simply cannot eat a toad large enough to reach a lethal dose.

A saltwater crocodile. Photo by fvanrenterghem, licensed under CC BY-SA 2.0.

A saltwater crocodile. Photo by fvanrenterghem, licensed under CC BY-SA 2.0.

Smaller crocodiles are more vulnerable. In 2013, an expedition to remote areas of northern Australia revealed that some populations of pygmy freshwater crocodiles, which only grow to 5 feet, have suffered declines upwards of 60% due to toad poisoning (Britton et al. 2013). The same research team, led by Dr. Adam Britton, is trying to raise money with a crowd-funding campaign to return to these remote sites, to study and help protect pygmy crocodiles. I strongly encourage you to visit the crowd-funding site here, as Britton has prepared a terrific video on pygmy crocodiles and the unique challenges they face.

A pygmy freshwater crocodile. Photo via Adam Britton, used with permission.

An adult pygmy freshwater crocodile. Photo by Adam Britton, used with permission.

The saltwater crocodiles in the Smith and Phillips study were not even close to 2,000 pounds — they were subadults, less than three feet long and closer to five pounds. So a few milligrams of cane toad poison should have killed at least some of them. Instead the walked away un-fazed, without so much as a skip in their gait.

Why? It may have to with the two crocodiles’ evolutionary history. In addition to being the largest, saltwater crocodiles are some of the widest-ranging** crocodiles, distributed from eastern India through Southeast Asia, Indonesia, and New Guinea. Because they can live in saltwater, they have been able to colonize many Pacific Islands (e.g., the Solomons) that are out of reach of other crocodilians.

A cane toad. Photo by Sam Fraser-Smith, licensed under CC BY 4.0.

A cane toad. Photo by Sam Fraser-Smith, licensed under CC BY 4.0.

Throughout their range they encounter a tremendous variety of potential prey. Saltwater crocodiles are not picky eaters, and have been observed feeding on fish (including sharks), frogs, lizards, snakes, turtles, crabs, snails, octopuses (during marine forays), deer, monkeys, pigs, cows, rats, otters, rabbits, porcupines, kangaroos, squirrels, wild cats, jackals, emus, geese, miscellaneous birds, and bats that fly just a little too close to the water.

Also, toads.

Even though Australian crocodiles never encounter toads, they have almost exactly the same DNA as their relatives in Asia and Indonesia. Perhaps they have inherited a tolerance for bufotoxin, while the freshwater crocodile, alone and isolated in Australia, has not.

Freshwater crocodiles might seem like the evolutionary dopes in this story, but there is hope for them. While some populations have been hit hard, others appear to be unaffected, perhaps because cane toads tend to avoid the habitats where freshwater crocodiles do most of their hunting (Somaweera et al. 2012). Research (like the pygmy crocodile project) is continuing to shed light on where cane toads are affecting crocodiles the most, why, and what can be done to protect them.

Finally, crocodilians are more intelligent than most reptiles. Studies with captive specimens have shown that after just a few encounters, hatchling freshwater crocodiles are able to quickly learn to avoid cane toads. Back in the field, some populations of crocodiles are already showing signs of learning, as cane toads are attacked less often and less enthusiastically than native frogs (Somaweera et al. 2011). As with humans, the best hope for freshwater crocodiles is in the next generation.

A young freshwater crocodile. Photo by Mike Peel, licensed under CC BY-SA 4.0.

A young freshwater crocodile. Photo by Mike Peel, licensed under CC BY-SA 4.0.

*Don’t even think about it.

**Saltwater crocodiles, while secure in Australia, are endangered in Southeast Asia, where many populations have gone extinct.

Cited:

Britton A.R.C., E.K. Britton, and C.R. McMahon. 2013. Impact of a toxic invasive species on freshwater crocodile (Crocodylus johnstoni) populations in upstream escarpments. Wildlife Research 40: 312-317.

Letnic M., J.K. Webb, and R. Shine. 2008. Invasive cane toads (Bufo marinus) cause mass mortality of freshwater crocodiles (Crocodylus johnstoni) in tropical Australia. Biological Conservation 141: 1773-1782.

Smith J.G. and B.L. Phillips. 2006. Toxic tucker: the potential impact of cane toads on Australian reptiles. Pacific Conservation Biology 12(1): 40-49.

Somaweera R., J.K. Webb, G.P. Brown, and R. Shine. 2011. Hatchling Australian freshwater crocodiles rapidly learn to avoid toxic invasive cane toads. Behaviour 148(4): 501-517.

Somaweera R., R. Shine, J. Webb, T. Dempster, and M. Letnic. 2012. Why does vulnerability to toxic invasive cane toads vary among populations of Australian freshwater crocodiles? Animal Conservation 16(1): 86-96.

Advertisements

The Pelican, the Shark, and the Armadillo: Crocodile Evolution Part 1

Crocodiles are very TV-genic – scores of documentaries have focused on them, and most start off with a variant of the following: “Crocodilians are some of the most successful predators on the planet. They survived the dinosaurs, and have remained unchanged for millions of years.”

Crocodylus_acutus_mexico_01.jpg

An American crocodile (Crocodylus acutus). Photo by Tomas Castelazo, licensed under CC BY-SA 2.5.

Today I wanted to write about why that’s not entirely true, and why crocodilian evolution, far from monotonous, is instead dynamic and, like crocodilians themselves, full of surprises.

There are only 23 species of non-extinct crocodilians, compared to 327 turtles and tortoises and more than 9,000 lizards and snakes. The fossil record, however, is full of crocodile relatives, the crocodylomorphs, dating back to at least 225 million years ago (Bronzati et al. 2012; Russel and Wu 1998).

The first crocodylomorphs looked nothing like the crocodiles alive today. Instead they were small, nimble creatures that ran on four long legs. Their sharp teeth reveal a predatory lifestyle, but instead of waiting in ambush at the water’s edge, they were adapted for wandering about over land in search of prey.

These animals, the sphenosuchians, appeared during the Late Triassic period when dinosaurs were just beginning to evolve. With legs pointed down under the body (rather than splayed to the sides), the sphenosuchians were probably terrific at chasing down prey. One such reptile, Hesperosuchus, was about the size of a domestic dog.

Hesperosuchus_BW.jpg

Hesperosuchus. Illustration by Nobu Tamura, licensed under CC BY 2.5.

As the dinosaurs began to diversify, so did the crocodylomorphs. Although many stayed small, some got larger, and began to experiment with different lifestyles. I say “experiment” euphemistically, but evolution is blind — circumstances and natural selection simply allowed crocodylomorphs to fill a wider range of niches. There were large, land-dwelling predators, like Protosuchus:

Protosuchus_BW.jpg

Protosuchus. Illustration by Nobu Tamura, licensed under CC BY 2.5.

There were also marine crocodylomorphs, the thalattosuchians. These, too, were predatory and looked vaguely like modern crocodilians in that they had long jaws, a muscular tails, and laterally flattened bodies (Young et al. 2014). Here, from Europe, are three species of Machimosaurus:

Machimosaurus_illustration.jpg

Machimosaurus species. Illustration by M.T. Young et al. (2014), licensed under CC BY 4.0.

Others looked nothing like any modern animals, and had fin-like feet and tails. Dakosaurus, also from Jurassic Europe (Young et al. 2012), had such an un-crocodile-like skull that their fossils were at first mistakenly attributed to dinosaurs.

Dakosaurus_maximus.png

Dakosaurus maximus. Illustration by M.T. Young et al. (2012), licensed under CC BY 2.5.

Most of the sea crocodiles lived during the Jurassic Period, when dinosaurs on land were becoming truly massive (e.g., spike-tailed Stegosaurus and long-necked Brontosaurus*). Despite an uncanny resemblance, sea crocodiles did not “evolve into” modern crocodiles. Instead they represent an off-shoot of crocodylomorph evolution, a kind of “dead-end” with no modern descendants.

There’s plenty more to say about fossil crocodylomorphs in the Jurassic, but we’ll skip to the Cretaceous, the last period of non-bird dinosaurs with Tyrannosaurus, Triceratops, and the like. Crocodiles, too, were reaching a magnificent crescendo with on of their most diverse lineages, the Notosuchia.

The Cretaceous saw crocodylomorphs occupying all sorts of unusual ecological roles. There were, of course, the usual land-dwelling predators like Baurusuchus:

Baurusuchus_BW.jpg

Baurusuchus. Illustration by Nobu Tamura, licensed under CC BY 2.5.

Others had turned over a new leaf, so to speak, and adopted a life of plant-eating. Simosuchus, one such herbivore (or omnivore — see Buckley et al. 2000), hardly looked like anything you might call a crocodile:

1024px-Simosuchus.jpg

Simosuchus clarki. Illustration by Smokeybjb, licensed under CC BY-SA 3.0.

There were still weirder crocodylomorphs. Armadillosuchus had armor plates over its back — it looked, and quite possibly behaved, very much like a modern armadillo, only 6 feet long and with sharp, fang-like teeth.

Armadillosuchus.jpg

Armadillosuchus arrudai. Illustration by Smokeybjb, licensed under CC BY-SA 3.0.

Meanwhile, some of the predatory crocodylomorphs had returned to the water, where they began to take full advantage of the lifestyle that would someday become the trademark of crocodilians. Many could be easily mistaken for true crocodiles — they had long snouts, flattened bodies, and spent their time ambushing visitors to the water’s edge. Some were colossal, and scientists have found evidence that some of the largest species (Sarcosuchus and Deinosuchus) preyed on dinosaurs (Boyd et al. 2013), just as Nile crocodiles today pick off unwary wildebeest and zebras.

Size comparison of two extinct and three living crocodylomorphs. Figure by Matt Martyniuk, licensed under CC BY-SA 3.0.

Size comparison of two extinct and three living crocodylomorphs. Figure by Matt Martyniuk, licensed under CC BY-SA 3.0.

Modern-day crocodilians belong to the Neosuchia (“new crocodiles”). This group also evolved in the Mesozoic and includes such strange beasts as Stomatosuchus, a 30-foot-long behemoth with a broad, spoon-like snout. Paleontologists aren’t sure exactly what it ate, but some suspect the lower jaw supported a pouch-like membrane for gulping fish, just like a pelican (Nopsca 1926).

Stomatosuchus2.jpg

Stomatosuchus inermis. Photo by Dmitri Bogdanov, licensed under CC BY 3.0.

Neither Sarcosuchus nor Stomatosuchus were “true” crocodilians, but crocodylians start to appear in the fossil record at around the same time. The oldest crocodilian fossils date back around 80 million years, during the Late Cretaceous (Russel and Wu 1998).

Just 15 million more years — a blink of an eye, really — until Earth’s most recent apocalypse. The same mass extinction that wiped out the dinosaurs (except birds), likely caused by a meteor, also wiped out most of the crocodylomorphs. Perhaps owing to their aquatic habits and (relatively) small size, crocodilians were one of the few survivors. A few other groups, like as the sea-faring dyrosaurids, lingered into the so-called Age of Mammals, but these too gradually fell away until only the true crocodiles, alligators, caimans and the gharial remained.

Guarinisuchus munizi, one of the few marine crocodylomorphs after the K-T extinction event. Illustration by Nobu Tamura, licensed under CC BY 3.0.

Guarinisuchus munizi, one of the few marine crocodylomorphs after the K-T extinction event. Illustration by Nobu Tamura, licensed under CC BY 3.0.

So we arrive at the present day, with 23 living species of crocodilians. Those 23 are the survivors survivors, here today because they are adaptable, tough, and a little bit lucky. They bear witness to an ancient lineage of incredibly diverse, versatile, and often bizarre animals, most of which have died. They are the ones that lived through mass extinctions, competition with dinosaurs, and climate change. They may even survive us.

NileCrocodile--Etiopia-Omo-River-Valley-01

A Nile crocodile (Crocodylus niloticus). Photo by Gianfranco Gori, licensed under CC BY-SA 4.0.

*Brontosaurus may or may not be the same as Apatosaurus. If they are the same, then Brontosaurus is not a valid name. I’m not a paleontologist, so I have no opinion on the matter — I used the name Brontosaurus here since I think it is more recognizable, although I may be wrong about that, too. To learn more, check out this article by zoologist and writer Darren Naish.

I’ll be writing more about crocodilian evolution tomorrow, this time with an amazing species that is alive today. If you want to read more about extinct crocodylomorphs, read this article, also by Darren Naish. If this kind of stuff interests you, I recommend following his blog Tetrapod Zoology at the same link.

Finally, if you are interested in a more technical review of crocodylomorph evolution, some good papers to read are Bronzati et al. (2012) and Russel and Wu (1998), cited below.

Cited:

Boyd C.A., S.K. Drumheller, and T.A. Gates. 2013. Crocodyliform feeding traces on juvenile ornithischian dinosaurs from the Upper Cretaceous (Campanian) Kaiparowits Formation, Utah. PLOS ONE 8(2): e57605. doi: 10.1371/journal.pone.0057605

Bronzati M., F.C. Montefeltro, and M.C. Langer. 2012. A species-level supertree of Crocodyliformes. Historical Biology 24(6): 598-606.

Buckley G.A., C.A. Brochu, D.W. Krause, and D. Pol. 2000. A pug-nosed crocodyliform from the Late Cretaceous of Madagascar. Nature 405: 941-944.

Nopcsa F. 1926. Neue Beobachtungen an Stomatosuchus. Centralbl. Min. Geol. Palaontol, B212-215.

Russel A. and X.-C. Wu. 1998. The crocodylomorpha at and between geological boundaries: the Baden-Powell approach to change? Zoology 100(3): 164-182.

Young M.T., S. Hua, L. Steel, D. Foffa, S.L. Brusatte, S. Thüring, O. Mateus, J.I. Ruiz-Omeñaca, P. Havlik, T. Lepage, and M. Brandalise de Andrade. 2014. Revision of the Late Jurassic teleosaurid genus Machimosaurus (Crocodylomorpha, Thalattosuchia). Royal Society Open Science doi: 10.1098/rsos.140222

Young M.T., S.L. Brusatte, Marco Brandalise de Andrade, J.B. Desojo, B.L. Beatty, L. Steel, M.S. Fernández, M. Sakamoto, J.I. Ruiz-Omeñaca, and R.R. Schoch. 2012. The cranial osteology and feeding ecology of the mentriorhynchic crocodylomorph genera Dakosaurus and Plesiosuchus from the Late Jurassic of Europe. PLOS ONE 7(9): e44985. doi: 10.1371/journal.pone.0044985

 

The Alligator’s Nest

by Joseph DeSisto

If you are careless in wandering along the swamps of the southeastern United States, you may hear this sound emanating from the brush:

[Recording by Adam Britton, used with permission.]

That is the hiss of an angry American alligator — if you hear it on land, you may have stumbled upon an alligator nest. If so, do not delay in your retreat. A mother alligator’s warning is no bluff.

An American alligator (Alligator mississippiensis) from South Carolina. Photo by Gareth Rasberry, licensed under CC BY-SA 3.0.

An American alligator (Alligator mississippiensis) from South Carolina. Photo by Gareth Rasberry, licensed under CC BY-SA 3.0.

If you could stay, however, you might be surprised at the tenderness with which alligators treat their offspring. When a female is ready to lay, she hauls herself on shore and finds a shaded, protected area not too far from the water. She lays her eggs in a pile of mud and leaf litter, then heaps more litter on top of them, so that the end result is a leaf-and-mud pile 2-3 feet tall and 5-7 feet wide (McIlhenny 1935).

A thick layer of insulating leaves also keeps the eggs at a more-or-less constant temperature. On a daily basis, even though the environment might go through wild changes in temperature, the inside of the nest stays within 3° F (Chabreck 1973). Alligator eggs usually take around 2 months to develop, and stable temperatures are critical.

Baby American alligators from the Okefenokee Swamp in Georgia. Photo by William Stamps Howard, licensed under CC BY-SA 3.0.

Baby American alligators from the Okefenokee Swamp in Georgia. Photo by William Stamps Howard, licensed under CC BY-SA 3.0.

In human beings, the presence or absence of a Y chromosome decides whether one develops into a male or female. In other words, human sex determination is chromosome-dependent. Alligators instead, like many reptiles, show temperature-dependent sex determination. Between days 20 and 35 of incubation, if eggs are kept between 86° and 93°F, a roughly even mixture of females and males will be the result (Ferguson and Joanen 1983). If, however, the batch stays above 93°, only males will emerge, and if below 86°, only females.

Alligator babies aren’t the only things that grow in alligator nests. The heap of dead leaves, twigs, and mud provides a haven for bacteria and other microorganisms. As bacteria digest the rotting vegetation, they produce heat — enough to keep the eggs 3-4° warmer than the habitat outside the nest (Chabreck 1973). In fact, bacteria keep alligator nests so consistently warm that the nests are also home to unique, heat-loving fungi (Tansey 1973).

More baby alligators! Photo by Ianaré Sévi, licensed under CC BY-SA 3.0.

More baby alligators! Photo by Ianaré Sévi, licensed under CC BY-SA 3.0.

Eggs, alligator or otherwise, look simple but are surprisingly complex. The “solid” shell is mostly made of calcium, but it’s far from a perfect seal — the whole surface is peppered with thousands of tiny holes, allowing the egg to take in oxygen and water, while “exhaling” carbon dioxide (Kern and Ferguson 1997). The thickness of the shell must be precise — too thin and the egg is easily crushed or infected by disease, but too thick and breathing, drinking, and hatching become difficult.

On alligator farms, where alligators are bred and raised for their skins, roughly 30-60% of eggs hatch successfully. Meanwhile more than 90% of alligator eggs hatch successfully in the wild (Kern and Ferguson 1997), as long as the nest isn’t flooded or raided by predators first. Experiments have shown that captive alligator eggs are less porous than their wild counterparts, and of the captive eggs, the least porous are doomed to die before hatching (Wink et al. 1990). Captive alligator eggs also have much thicker shells than wild eggs. So where is the difference coming from?

A baby American alligator. Photo by Ianaré Sévi, licensed under CC BY-SA 3.0.

A baby American alligator. Photo by Ianaré Sévi, licensed under CC BY-SA 3.0.

The bacteria in wild alligator nests, aside from producing heat, also produce acids. These acids aren’t strong or abundant enough to harm the developing reptiles, but over the 2 months it takes for them to develop, acids gradually erode the hard, calcium shell around each egg (Ferguson 1981). By the time the alligator is ready to hatch, its shell is significantly thinner than when the egg was first laid — just thin enough for the hatchling to easily break through.

[Recording by Adam Britton, used with permission.]

As they leave their eggs, baby alligators sound an alarm to their mother, who industriously digs them out of the nest where they spent the first two months of their lives. Although these months might seem uneventful, they are in fact full of challenges, which alligator eggs, however simple and unassuming, have ways to overcome.  Those hatchlings that survive face yet another gauntlet of obstacles, including predators and ruthless competition from their siblings. It’s tough being a baby alligator, and maybe even tougher being an egg, but the toughest few have a chance to become some of the most awe-inspiring top predators in North America.

Dr. Adam Britton, a crocodile researcher at the Charles Darwin University in Northern Territory, Australia, has graciously allowed me to use the audio files in this article. More files, along with a wealth of information about crocodilian biology and conservation, can be found at his website, crocodilian.com.

Cited:

Chabreck R.H. 1973. Temperature variation in nests of the American alligator. Herpetologica 29(1): 48-51.

Ferguson M.W.J. 1981. Increased porosity of the incubating alligator eggshell caused by extrinsic microbial degradation. Experientia 37(3): 252-255.

Ferguson M.W.J. and T. Joanen. 1983. Temperature-dependent sex determination in Alligator mississippiensis. Journal of Zoology 200(2): 143-177.

Kern M.D. and M.W.J. Ferguson. 1997. Gas permeability of American alligator eggs and its anatomical basis. Physiological Zoology 70(5): 530-546.

McIlhenny E.A. 1935. The Alligator’s Life History. Christopher Publishing House, Boston. 117 pp.

Tansey M.R. 1973. Isolation of thermophilic fungi from alligator nesting material. Mycologia 65(3): 594-601.

Wink C.S., R.M. Elsey, and M. Bouvier. 1990. Porosity of eggshells from wild and captive, pen-reared alligators (Alligator mississippiensis). Journal of Morphology 203(1): 35-39.