Skeletal reconstruction of a young adult mesosaur (Mesosaurus tenuidens) from the Early Permian of Uruguay and Brazil (reproduced from Silva et al., 2017).
Mesosaurs and the Early Amniote Evolution
Mesosaurs represent the most amazing animals of the distant past. They are the oldest known amniotes that developed adaptations to aquatic environment. By the Early Permian, mesosaurs inhabited cold and salty water bodies resulting from the drought of an originally large inland sea that extended over what is now South America and Africa (Piñeiro et al., 2012b). Mesosaurs are represented by several species and a myriad of specimens, including well-preserved skeletons from the Lower Permian of Uruguay, Brazil, and southern Africa, which have been studied for a long time since the 19th century. Thanks to the specific geographic distribution of their remains, mesosaurs have even helped Alfred Wegener to formulate the theory of continental drift.
The study of mesosaurs is indeed important for a number of reasons. First of all, they represent so-called basal amniotes. It means that mesosaurs were quite close in the evolutionary tree to the last common ancestor of all sauropsids (a group including reptiles, their ancestors and relatives) and synapsids (a group including mammals, their ancestors and relatives). For instance, the discovery of well-preserved mesosaur embryos curled as within an egg, and one pregnant female has recently yielded clues about the reproductive biology of early amniotes (Piñeiro et al., 2012a). Interestingly, mesosaurs were viviparous or they laid eggs in advanced stages of development. Finds from Uruguay even suggest that there perhaps existed some kind of parental care in mesosaurs due to common associations of remains of adults with newborns.
Such data can be better understood when interpreted in a broader paleoecologic context. Therefore, out team composed of four researchers from Uruguay, Brazil, and Poland (R.R. Silva, J. Ferigolo, P. Bajdek, and G. Piñeiro) and lead by Graciela Piñeiro, has recently published a new paper on the biology of mesosaurs (Silva et al., 2017), which largely expands our knowledge about these animals. Here, we’d like to briefly sum up our conclusions regarding the feeding habits, physiology, and environment of mesosaurs of Uruguay and Brazil.
Putative mesosaur regurgitalites (fossil vomit) from the Mangrullo Formation, Uruguay; scale bars 1 cm (reproduced from Silva et al., 2017).
Unusual Finds from the Lower Permian of Uruguay and Brazil
Preserved gastric contents, cololites (fossil intestine matter), coprolites (fossil feces), and regurgitalites (fossil vomit) of mesosaurs that we have studied, tell us a lot about the feeding habits, physiology, and life conditions of mesosaurs. These fossils come from the Mangrullo Formation of Uruguay and the Iratí Formation of the State of Goiás, Brazil. Mesosaurids lived in an inland hypersaline water body, with exceptional preservation conditions that justified describing mesosaur-bearing strata as a Fossil-Lagerstätte.
First of all, our study represents an exceptional case where gastric contents, cololites, coprolites, and regurgitalites (i.e., all the “basic” bromalite types) of a single animal species are described. It gave us an uncommon opportunity to make certain observations on all these fossil types, such as to compare their general form of preservation and even the degree of digestion of swallowed remains in different stages of the digestive process.
Paleontologists hardly ever are able to link fossil feces to their producer. This case is different. No other tetrapod is found in the mesosaur-bearing strata. The coprolites have a non-spiral morphology that is typical for tetrapods, in contrast to all fish of the Permian Period. Finally, the content of the coprolites is comparable to that found in mesosaur stomach and intestine contents. Alternatively, the smallest of the coprolite specimens would have been produced by large crustaceans.
Such an uncommon opportunity to take a look at the feeding habits of an extinct animal must not be wasted. Previously, the diet of mesosaurs was only inferred from indirect evidence, what is in fact a kind of ‘educated guess’. For over a hundred years, various hypotheses have been proposed for determining mesosaur feeding habits: fish-eating, sludge filter-type habit, or crustacean-based diet. Now, let’s look deep into mesosaur stomachs…
Mesosaur skeleton (Brazilosaurus sanpauloensis) showing a preserved cololite (blue arrow) and several coprolites surrounding it (red arrows), from the Iratí Formation, Brazil (modified from Silva et al., 2017).
Cannibals and Scavengers under Environmental Stress
We found out that mesosaur diet included crustaceans as the main food item, corroborating some of the hypotheses. On the other hand, no fish remains were recognized in mesosaur gastric contents, cololites, coprolites, and regurgitalites, as no fish are found in the mesosaur-bearing strata. More surprisingly, acid-etched mesosaur bones and teeth are found in mesosaur bromalites.
The presence of mesosaur remains in mesosaur stomach content, regurgitalites, and other bromalites, is particularly interesting. Yet, easy assumptions in the study of bromalites are sometimes misleading. Were mesosaurs cannibalistic predators? Well, the jaw aperture in an average-sized mesosaur was much too small to allow even newborn mesosaurs to be swallowed whole, meanwhile mesosaur teeth seem not to be adapted to powerful biting. A predatory scenario would be hence a little surprising to us. Instead, we note that mesosaurs fed on crustaceans generally not exceeding 2 cm in length. Taking a close look at the gastric contents we can recognize no articulated skeletal elements, which would be expected to be still present in the earliest stage of the digestive process.
Explanation of the mystery requires a comment on the environment which the mesosaurs lived in. Mesosaur remains are found in rocks formed in a hypersaline water body and such environments are famous for extreme severity. The stress conditions might have been also caused by the extended volcanism and ash spread into the water body during the Early Permian. The environmental conditions and the faunistic poverty of the mesosaur-bearing ‘salty sea’ are the first key to the mystery. There were no fish in water, nearly nothing to eat for mesosaurs but crustaceans and… mesosaur dead bodies.
Cannibalistic behavior and scavenging are quite common under environmental stress, overcrowding and insufficient food resources. Mesosaurs probably ingested elements of mesosaurid carrion in partial decomposition. It seems possible that also the largest of the crustacean remains were scavenged from the bottom, as they often appear to be very weathered.
Mesosaurs regurgitated the biggest of bone fragments as well as seemingly crustaceans, which were too large to pass through the gastrointestinal tract. Various amniotes, as for example raptor birds, crocodiles, and probably ichthyosaurs, regurgitate most of the indigestible or hard-to-digest remains. Some of the objects might have been ingested accidentally, or were mesosaurs so hungry living in this harsh environment? Regurgitation might also have been caused by the environmental stress itself. Because digestion efficiency depends on body temperature, in extant reptiles undigested food remnants may be regurgitated during periods of unfavorable environmental temperature. Disease may also cause regurgitation.
Bone elements in the mesosaur coprolites are intriguing too. Reptiles are characterized by a strong digestion and many of them digest the swallowed bones practically completely. However, mesosaurs were fairly small and their period of digestion was not necessarily very long. Also, the presence of poorly digested remains in feces, caused by short digestion, may have to do with fluctuating food availability.
Epilog of the Mesosaur Story
Fossilization of the mesosaur remains and their bromalites was facilitated by microbial mats on the bottom of the water bodies and the volcanic events and ash spread. It gave us a fascinating, but also a little terrifying opportunity to investigate enigmas of the biology of some of the earliest amniotes. The study of mesosaurs has just begun!
Piotr Bajdek 1, Graciela Piñeiro 2, Rivaldo R. Silva 3, Jorge Ferigolo 4
1 Częstochowa, Poland
2 Universidad de la República de Uruguay
3 Universidade Luterana do Brasil
4 Fundação Zoobotânica do Rio Grande do Sul, Brazil
Piñeiro, G., Ferigolo, J., Meneghel, M., Laurin, M., 2012a. The oldest known amniotic embryos suggest viviparity in mesosaurs. Hist. Biol. 24, 630–640.
Piñeiro, G., Ramos, A., Goso, C., Scarabino, F., Laurin, M., 2012b. Unusual environmental conditions preserve a Permian mesosaur−bearing Konservat−Lagerstätte from Uruguay. Acta Palaeontol. Pol. 57 (2), 299–318. doi: 10.4202/app.2010.0113
Silva, R.R., Ferigolo, J., Bajdek, P., Piñeiro, G.H., 2017. The feeding habits of Mesosauridae. Front. Earth Sci. 5:23. doi: 10.3389/feart.2017.00023
Coprolite of a large carnivore, possibly an archosauromorph, from the Early Triassic of Australia (photo P. Bajdek)
Newest Russian and Australian Papers
So-called mass extinctions are full of mystery and used to constitute one of the most thrilling topics for anyone interested in the history of life. Today, I’ll focus on two recent publications treating the topic of the end-Permian mass-extinction (Niedźwiedzki et al., 2016a) and the recovery of life after this extinction (Niedźwiedzki et al., 2016b). I am the second author of both of these papers and you can see the name of Grzegorz Niedźwiedzki who was our team leader.
Coprolite Diversity and Mass-Extinctions
First, I’d like to mention another interesting study which actually is not mine. Probably the most famous, yet not the largest, mass extinction occured at the end of the Cretaceous Period (around 66 million years ago), when the dinosaurs among many other creatures died out. In 2012, came out a paper of five researchers from the New Mexico Museum of Natural History and Science. The team of Thomas L. Suazo studied the diversity of coprolites, i.e. fossil feces, in five geologic formations of New Mexico: three of them Upper Cretaceous (Campanian and Maastrichthian) and two of them Cenozoic (Paleocene and Eocene) in age.
In contrast to what some may expect, the researchers found out that coprolite morphologies do not change significantly across the Cretaceous–Paleogene boundary and concluded: „This suggests that either none of the preserved coprolites are dinosaurian, or that dinosaurian coprolites are homeomorphic with those of some other vertebrates, such as crocodyles.”
A basic problem in the study of coprolites is that feces used to provide few taxonomic information about their producers. Distinct animal groups sometimes produce quite similar feces, whereas feces of just one individual may vary a lot in appearance and all this is altered by the fossilization process. Comparison of coprolite morphotypes from clearly different paleobiologic contexts, as e.g. distinct geologic periods, may result particularly misleading.
In contrast, the recent study of our team (Niedźwiedzki et al., 2016a) focuses on the diversity of coprolite morphotypes across the Permian–Triassic boundary in several geologic profiles of just a single locality. Noteworthy, the end-Permian mass-extinction (around 252 million years ago) is considered the most severe extinction event ever, with up to 96% of all marine species and 70% of terrestrial vertebrate species becoming extinct.
I have already talked about coprolites from the Vyazniki site, Russia, as they provided possible evidence of hair in therapsids and yielded a great diversity of other microfossils. Rocks of the Vyazniki region allow us study the fauna of the latest Permian and the earliest Triassic. In the new study, we grouped the analyzed specimens (coprolites and possibly some cololites) into nine morphotypes and documented in detail their stratigraphic ranges and the type of sediments their are found in.
We found out that there was indeed a reduction of coprolite diversity. In the earliest Triassic, only three of the nine morphotypes present in the sediments of the uppermost Permian reappeared. However, no taphonomic explanation, such as a significant change in the sedimentation process could be found to explain this reduction of coprolite diversity. In other words, it appears that most of the animals that produced the feces disappeared.
Recovery of Life After the Great Permian Extinction
Coprolites tells us also about the recovery of life after the end-Permian mass-extinction. The second paper of my authorship which I would discuss in this blog post (Niedźwiedzki et al., 2016b) describes coprolite material recovered from the Bulgo Sandstone which crops out along the coastal cliffs at Long Reef in the northern suburbs of Sydney, Australia. These rocks are lower Olenekian (Lower Triassic) in age what means that the coprolites we studied have been produced by animals that lived just around one million years after the Great Permian Extinction.
We distinguished eleven recurring morphotypes of tetrapod coprolites, as well as one fish bromalite specimen. Some of the coprolite morphotypes were ascribed most likely to archosauromorph reptiles and others to temnospondyl amphibians, whose bone remains are under study now. Undoubtedly, such a diversity of vertebrate fauna is interesting taking in consideration that these animals lived so shortly after the Great Permian Extinction. Let’s now say that by the Early Triassic the Sydney region was located close to the southern polar circle…
In the Early Triassic the climate was actually warmer than it is today and there were no polar ice caps, yet there must have been a reduced insolation at high latitudes. Biotic responses might have included reduced activity levels and estivation in burrows, or perhaps other behavioral and physiological mechanisms such as migration and homeothermy. Moreover, already in 2005, Caroline Northwood described diversified coprolites from the Lower Triassic Arcadia Formation, Queensland. Interestingly, some researchers suggested that Antarctica was a refugium for terrestrial tetrapods from the end-Permian mass extinction.
Niedźwiedzki, G., Bajdek, P., Qvarnström, M., Sulej, T., Sennikov, A.G., Golubev, V.K., 2016a. Reduction of vertebrate coprolite diversity associated with the end-Permian extinction event in Vyazniki region, European Russia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 450, 77–90. doi: 10.1016/j.palaeo.2016.02.057
Niedźwiedzki, G., Bajdek, P., Owocki, K., Kear, B.P., 2016b. An Early Triassic polar predator ecosystem revealed by vertebrate coprolites from the Bulgo Sandstone (Sydney Basin) of southeastern Australia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 464, 5–15. doi: 10.1016/j.palaeo.2016.04.003
Northwood, C., 2005. Early Triassic coprolites from Australia and their palaeobiological significance. Palaeontology 48, 49–68.
Enigmatic worm-like structure in a coprolite from the Permian of Russia (photo by K. Owocki; see Bajdek et al., 2016)
Parasites in fossil feces
The significance of coprolites, i.e. fossil feces, in the study of ancient food chains and physiology of extinct animals has been already discussed on the blog. Coprolites are indeed fascinating fossils for a number of reasons. For instance, feces often constitute an exceptional microenvironment allowing the preservation of extremely delicate remains, otherwise absent in the rocks. Let’s firstly discuss fossils of minute parasite eggs and soft bodies of worms.
In 2013, the team led by Paula C. Dentzien-Dias described well-preserved tapeworm eggs in a shark spiral bromalite from the Middle-Upper Permian of Brazil. I just briefly mention this paper because its full-version is freely available online. Apart from the amazing state of preservation of the eggs, it’s an interesting find as this is the earliest fossil record of tapeworm parasitism. In fact, Paula C. Dentzien-Dias has already published three important papers on the fecal material from the Rio Do Rasto Formation.
In the recent post of my blog I talked about bone fragments and the oldest possible hairs found in Upper Permian coprolites from the Vyazniki site, Russia. Well, the hair-like structures are important and I must admit I was very happy to see some media, including the National Geographic Traveler, to have noticed my research (Bajdek et al., 2016). However, I would like to highlight now that the coprolites we have studied have moreover yielded a great diversity of other interesting microfossils, described in the same publication (Bajdek et al., 2016).
Some of them represent possible parasites, as for example the rod-shaped and oval structures, typically 100–150 µm in length, which are interpreted as possible invertebrate eggs. Also, an enigmatic worm-like structure was found (picture above). I find this structure especially intriguing—it would be a worm body fossil (as a nematode) or alternatively a burrow. Ferreira et al. (1993) described nematode larvae preserved in coprolites from the Pleistocene of Italy. Moreover, a long, sinuous, 6 µm wide structure was found in one coprolite specimen from Vyazniki and indentified as a burrow.
These fossils might suggest that the coprolite producers had worm parasites. Yet, it’s hard to rule out entirely the opportunistic exploitation of feces by nematodes and other invertebrates after excretion. Such eggs could have belonged to parasites but alternatively they could be of coprophagous organisms, as for example insects. Nematodes and annelids decompose feces mostly in humid and cold ecosystems where coprophagous insects are less common.
Moreover, two different forms of putative ciliates were recognized (photo on the right; by K. Owocki; see Bajdek et al., 2016), 350 µm and 230 µm long. Some details as the cell shape and the position and length of cilia could be described. Once again, the interpretation as parasites is tantalizing but these microorganisms could have colonized the fecal matter after its excretion.
Within the coprolites from Vyazniki, there was also found a diversity of other microorganisms including bacteria, two kinds of cyanobacteria, and fungi, which would mostly have not represented parasites, as well as some indeterminate objects, possible arthropod remains and plant tissues. Cyanobacteria and fungi have been swallowed with food and water or colonized the fecal matter after its excretion. Bacteria preserved in coprolites may represent original microbiota of the gastrointestinal tract, yet our paper also discusses the possibility of contamination by environmental bacteria from the sediments. The role of bacteria in the fossilization of feces will be discussed in one of the forthcoming posts of the blog.
In conclusion, coprolites may constitute a valuable source of delicate fossil remains, including abundant microorganisms, otherwise usually impossible to detect in the rocks and study. Thus, coprolites are an incredibly rich source of paleoecologic information. I would differentiate three principal branches in my research on bromalites: (a) paleoecology (i.e. diet and other life habits of the source animals; environmental reconstruction; ecological relationships like parasitism, coprophagy, etc.), (b) physiology of the source animals, and (c) taphonomy and fossilization of feces and identification of coprolites.
In regard to fossil parasites and the significance of bromalites in general, there’s one very special find yet to be presented in this post…
Fossil parasites in gut contents
Trace fossils of possible parasites inside the gut contents of a hadrosaurid dinosaur from the Cretaceous of Montana (source; see Tweet et al., 2016)
To me personally, the most amazing dinosaur find ever. The specimen JRF 115H, known as „Leonardo”, is a skeleton of a subadult hadrosaurid dinosaur, Brachylophosaurus canadensis, from the Upper Cretaceous Judith River Formation of Montana, USA. First of all, the nearly complete skeleton of Leonardo, found in 2000, represents one of rather few „mummified” dinosaurs, what means that it’s excellently preserved showing some soft tissues. It moreover represents one of just a couple of known possible cases of preservation of gut contents in herbivorous dinosaurs.
Description of the probable gut contents of JRF 115H, which included leaf fragments and quartz grains encased in a clay matrix, was published back in 2008. Recently, in 2016, after a decade of work, came out a new paper in which paleontologists from the USA (J. Tweet, K. Chin, and A. A. Ekdale) describe trace fossils of possible parasites inside the gut contents of JRF 115H (photos above). The traces, about 0.3 mm in diameter, are interpreted most likely as burrows. The researchers had to carefully rule out other possibilities as traces of plant roots and fungi.
Most carcasses quickly attract a varied fauna of invertebrate scavengers, but only one type of trace fossil was found in the gut contents of JRF 115H. It should be also noticed that the state of preservation of JRF 115H suggests that it was buried rapidly. Thus, more likely the gut contents were burrowed either by (a) worms living in the sediment that buried the dinosaur carcass or (b) parasites of the gastrointestinal tract of the hadrosaurid (which survived the host’s death, or else newly hatched ones that emerged after the dinosaur’s death).
Finally, one of the most interesting aspects of the traces is that some of them share walls showing identical changes in direction (picture above, on the right). The researchers suggest that it may reveal intentional contact between individuals, perhaps for mating. Traces of this kind have been never reported before in the scientific literature!
Acknowledgments–I thank Justin Tweet and Karen Chin who kindly permitted me to reproduce the images of the trace fossils in the gut contents of JRF 115H.
Bajdek, P., Qvarnström, M., Owocki, K., Sulej, T., Sennikov, A.G., Golubev, V.K., Niedźwiedzki, G., 2016. Microbiota and food residues including possible evidence of pre-mammalian hair in Upper Permian coprolites from Russia. Lethaia 49, 455–477. doi: 10.1111/let.12156
Dentzien-Dias, P.C., Poinar, G.Jr., de Figueiredo, A.E.Q., Pacheco, A.C.L., Horn, B.L.D., Schultz, C.L., 2013. Tapeworm Eggs in a 270 Million-Year-Old Shark Coprolite. PLoS ONE 8 (1), e55007. doi: 10.1371/journal.pone.0055007
Ferreira, L.F., Araújo, A., Duarte, A.N., 1993. Nematode larvae in fossilized animal coprolites from Lower and Middle Pleistocene site, Central Italy. The Journal of Parasitology 79, 440–442.
Tweet, J.S., Chin, K., Braman, D.R., Murphy, N.L., 2008. Probable gut contents within a specimen of Brachylophosaurus canadensis (Dinosauria: Hadrosauridae) from the Upper Cretaceous Judith River Formation of Montana. Palaios 23, 624–635. doi: 10.2110/palo.2007.p07-044r
Probable hair in a therapsid coprolite from the Permian of Russia (photo by K. Owocki; see Bajdek et al., 2016)
Ectothermic or endothermic
An obvious difference between modern reptiles and mammals is that the former are ectotherms and the latter endotherms: whereas the body temperature of reptiles is dependent on the prevailing environmental temperatures, it is regulated to remain nearly constant in mammals. We can also note that: (1) mammals have fur and reptiles do not, and (2) reptiles are characterized by a much longer digestion (slower metabolism) than mammals of a comparable body mass. As a consequence, many modern reptiles have a “lower-energy” lifestyle than mammals.
It becomes less obvious when we go back in time… Mammals evolved in the Triassic Period, and questions paleontologists ask themselves are: when did the endothermy in their evolutionary lineage appear? Were already the late Palaeozoic and early Mesozoic ancestors of mammals (called therapsids or mammal-like reptiles) endothermic?
In the 1970s, the American paleontologist Robert T. Bakker published innovative ideas on the physiology of mammal-like reptiles (and dinosaurs). He hypothesized that therapsids had fur and provided several lines of evidence that they were endotherms: (1) Therapsid bones lacked growth rings and had closely packed blood vessels and Haversian canals. (2) Some of them were distributed in cold temperate zones. (3) Short, stocky body proportions in many therapsids might have been a device to conserve heat. (4) Their predator–prey ratios, which depend on the energetic requirements of the predators, were lower than those of ectotherms.
R.T. Bakker’s ideas on the physiology of therapsids (and dinosaurs) have been accepted by most paleontologists and are well-known to the public. Nevertheless, because many of them are rather indirect lines of evidence, we now seek for new clues. Coprolites, i.e. fossil feces, being metabolistic byproducts provide such new and valuable data on the metabolism of their producers. In fact, the study of coprolites has during the last couple of years shed new light on the physiology of mammalian ancestors and their relatives. For example, it was argued in the article on coprolites of a giant dicynodont from the Triassic of Poland, that these herbivorous and toothless therapsids had a rather slow metabolism.
Furthermore, in 2016, another piece of the puzzle of mammalian endothermy was added when our team composed of seven researchers from Poland, Sweden, and Russia (P. Bajdek, M. Qvarnström, K. Owocki, T. Sulej, A.G. Sennikov, V.K. Golubev, and G. Niedźwiedzki) published a new paper on coprolites. The coprolites we studied were produced by Late Permian carnivorous therapsids, over 252 million years ago, and excavated during a Polish–Russian expedition to the Vyazniki site, European Russia.
Undigested bones and the fast metabolism
The Vyazniki site has yielded various morphotypes of coprolites (which will soon be discussed again on the blog). Our paper from 2016 focuses on only two big coprolite morphotypes: A and B. Whereas undigested bone fragments are present in the type-A coprolites, they are quite rare and highly degraded in the type-B coprolites. As said above, reptiles are characterized by a much longer digestion than mammals, and, for example, crocodiles practically completely digest the bones they ingest. On the contrary, undigested bones are commonly found in the feces of mammals. Following these arguments, the bone-rich coprolites of type A would have interestingly been produced by some kind of animals of a fast metabolism.
As such, the team of Krzysztof Owocki and Grzegorz Niedźwiedzki ascribed, in 2012, the bone-rich type-A coprolites to therapsid carnivores and the bone-barren type-B coprolites to archosauromorphs or other non-therapsid carnivores. Both therapsids and archosauromorphs are known from the fossil record of Vyazniki, but therapsids would have been more expected to have a fast metabolism than early archosauromorphs (ancestors of modern crocodiles and birds). This interpretation is supported by finds from the Upper Permian of South Africa. Already in 2011, the paleobiological context allowed Roger M.H. Smith and Jennifer Botha-Brink to link several bone-rich coprolite morphotypes from the Upper Permian of South Africa to carnivorous therapsids.
The oldest hairs
The researchers from South Africa have found more than just bones in the Permian coprolites. Some coprolites contain enigmatic elongated structures, that are on average 14 μm in diameter and reaching up to 5 mm in length. Roger M.H. Smith and Jennifer Botha-Brink suggested that these structures were remains of plants, fungi or, perhaps, hairs. It was exciting to our team to find comparable structures in a therapsid coprolite from the Upper Permian of Vyazniki, Russia. By the use of light and scanning electron microscopes we studied them in great detail, including their geochemistry. The structures we described from Russia are ten time larger in diameter than those from South Africa, and the largest one is over 5 mm long. They are interpreted as molds of hair-like elements; some even appear to show bifurcated hair roots! Hairs are well-resistant to digestion and often found in feces of modern carnivores.
If this interpretation is correct, these hairs are two times older than the previously earliest record of known hairs from Jurassic-Cretaceous mammals and imply that some therapsids had acquired insulation by the latest Paleozoic, prior to the rise of mammals. Hairs would probably have had a thermoregulatory function, as an insulation. Some researchers have also suggested that hairs could be tactile in origin. In 1968, G.H. Findlay hypothesized that perforations present in a skull of the Late Permian therapsid Olivera parringtoni reveal the presence of tactile hairs. Such hairs could have been of great use especially if mammals are descended from nocturnal reptiles. Hairs would make up for poor vision and moreover allow to conserve heat at night.
The discoveries from South Africa and Russia suggest that Late Permian therapsid carnivores had developed (1) an insulation (fur) and (2) an accelerated metabolism. Taken together, these features make us suspect that the late Paleozoic ancestors of mammals were already endotherms.
1 Częstochowa, Poland
2 Uppsala University, Sweden
Bajdek, P., Owocki, K., Niedźwiedzki, G., 2014. Putative dicynodont coprolites from the Upper Triassic of Poland. Palaeogeogr. Palaeoclimatol. Palaeoecol. 411, 1–17. doi: 10.1016/j.palaeo.2014.06.013
Bajdek, P., Qvarnström, M., Owocki, K., Sulej, T., Sennikov, A.G., Golubev, V.K., Niedźwiedzki, G., 2016. Microbiota and food residues including possible evidence of pre-mammalian hair in Upper Permian coprolites from Russia. Lethaia 49, 455–477. doi: 10.1111/let.12156
Bakker, R.T., 1971. Dinosaur physiology and the origin of mammals. Evolution 25, 636–658.
Bakker, R.T., 1975. Dinosaur renaissance. Scientific American 232, 58–78.
Findlay, G.H., 1968. On the scaloposaurid skull of Oliviera parringtoni, Brink with a note on the origin of hair. Palaeontologia Africana 11, 47–59.
Owocki, K., Niedźwiedzki, G., Sennikov, A.G., Golubev, V.K., Janiszewska, K., Sulej, T., 2012. Upper Permian vertebrate coprolites from Vyazniki and Gorokhovets, Vyatkian regional stage, Russian Platform. Palaios 27, 867–877. doi: palo.2012.p12-017r
Smith, R.M.H., Botha-Brink, J., 2011. Morphology and composition of bone-bearing coprolites from the Late Permian Beaufort Group, Karoo Basin, South Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 312, 40–53. doi: 10.1016/j.palaeo.2011.09.006
Coprolite of a marine carnivore with bivalve shell fragments, Upper Cretaceous, Poland (reproduced from Bajdek, 2013)
Marine food chains
The ichthyosaurs were an extraordinarily adapted to life in water group of reptiles of the Mesozoic Era. Due to the hydrodynamic body shape, it’s commonly believed that the ichthyosaurs preyed on agile and fast animals. Indeed, the ichthyosaur gastric contents described from the Lower Jurassic of Lyme Regis and Charmouth, England, as well as Holzmaden, Germany, contain remains of belemnites, which were generally slim cephalopods resembling modern squids.
Certain accumulations of belemnite rostra are interpreted as ichthyosaur regurgitalites (fossilized vomit). For instance, such an accumulation from the Jurassic of Peterborough, England, was presented in 2001 by Peter Doyle and Jason Wood. Because it seems improbable that the strong and sharp rostra passed through the entire gastrointestinal tract and were excreted in the form of feces, the find was interpreted as a regurgitate of an ichthyosaur. This interpretation is supported by the etching marks on the surfaces of the rostra, and also the fact that they belonged mostly to juvenile individuals.
It was surprising the stomach content of an ichthyosaur from the Upper Albian (Lower Cretaceous) of the Toolebuc Formation, Queensland, described in 2003 by a team of researchers led by Benjamin P. Kear. Apart from fish bones, in the stomach there were present remains of a turtle, and a bird. Turtle fossils are common in those rocks; it also seems that the turtle was an easy prey. The bird was most likely consumed in the form of carrion. Possibly, the dietary habits of ichthyosaurs were much more flexible than previously thought. The finding is also interesting because it’s one of the latest ichthyosaurs – at the end of the Cenomanian, 10 million years later, the ichthyosaurs went extinct. Some speculated that the dietary specialization of ichthyosaurs were a contributing factor in their extinction. This explanation seems however inconsistent with the discovery from the Toolebuc Formation.
What did the turtles cf. Notochelone, which the ichthyosaurs preyed on, eat? The Cretaceous turtles of the family Protostegidae are an extinct group whose diet was unknown. However, three years later Benjamin P. Kear described stomach contents and coprolites (fossilized feces) of the turtles from the Toolebuc Formation. They contained crushed shells of bivalves belonging to the family Inoceramidae. As the bivalves were benthic organisms, it means living on the seafloor, the conclusions one more time were inconsistent with the expectations. Some supposed that these turtles were pelagic predators and fed on ammonites in the water column.
Taken together, the findings from the Australian Toolebuc Formation give an unusual opportunity to take a look at ancient food chains, which encompassed the turtles feeding on bivalves, and the ichthyosaurs feeding on turtles, fishes, and even the carrion of birds.
The marine depths
In 2013, I described a little younger coprolite from the Upper Cretaceous of the Carpathian Mountains, Poland. Similarly to the coprolites from Australia, the putative coprolite from Poland contains crushed shells of bivalves belonging to the family Inoceramidae. Unfortunately, it’s not easy to determine what animal it was produced by: although a reptile cannot be ruled out as the producer, a teleost fish seems the most simple explanation. In contrast to the specimens from Australia, which come from shallow-marine sediments, the coprolite from the flysch of the Carpathians was found in rocks formed in the marine depths. Its geologic context is indeed interesting. The feces were buried beneath sediments of a so-called turbidity current, i.e. a submarine avalanche transporting sediments to the oceanic depths. The specimen is also interesting because it contains numerous shells, whereas the host rocks are extremely poor in body macrofossils of animals. Feces constitute an exceptional accumulation of remains. The dietary residues can be moreover transported in the gastrointestinal tract of the fecal producer far away, even to a different environment.
The juvenile prey
In 2015, a team of researchers led by David R. Schwimmer described an interesting find from the Upper Cretaceous of South Carolina. The spiral bromalite, i.e. feces or an intestinal cast, contains partially articulated vertebrae of a baby freshwater turtle. Due to the small size of the bromalite, the researchers suggest that the shark itself was juvenile as well. These observations might carry interesting ecologic implications showing that the shark fed closely to a freshwater river environment and the breeding sites of the turtles. The researchers consider even the possibility that juvenile sharks migrated far upstream.
Gastric contents of plesiosaurs reveal remains of ammonites, belemnites, bivalves, and fishes. An unusual find from Wyoming was described in 2009. The stomach of a Late Jurassic plesiosaur contained ichthyosaur remains. Strictly speaking, it was an embryo of an unborn ichthyosaur!
Bajdek, P. 2013. Coprolite of a durophagous carnivore from the Upper Cretaceous Godula Beds, Outer Western Carpathians, Poland. Geological Quarterly 57 (2): 361–364. doi: 10.7306/gq.1094
Kear, B.P. 2006. First gut contents in a Cretaceous sea turtle. Biology Letters 2: 113–115. doi: 10.1098/rsbl.2005.0374
Kear, B.P., Boles, W.E., and Smith, E.T. 2003. Unusual gut contents in a Cretaceous ichthyosaur. Proc. R. Soc. Lond. B (Suppl.) 270: 206–208. doi: 10.1098/rsbl.2003.0050
Lomax, D.R. 2010. An Ichthyosaurus (Reptilia, Ichthyosauria) with gastric contents from Charmouth, England: first report of the genus from the Pliensbachian. Paludicola 8 (1): 22–36.
Nature News, 12 February 2002. Jurassic vomit comes up at meeting. doi: 10.1038/news020211-3
O’Keefe, F.R., Street, H.P., Cavigelli, J.P., Socha, J.J., and O’Keefe, R.D. 2009. A plesiosaur containing an ichthyosaur embryo as stomach contents from the Sundance Formation of the Bighorn basin, Wyoming. Journal of Vertebrate Paleontology 29 (4): 1306–1310.
Illustration by Dmitry Bogdanov under the CC BY 3.0 License: source
The giants from the Triassic of Poland
The robust animal in the picture calls attention as the youngest, in the sense of the geologic age, and also the largest member of dicynodonts. The dicynodonts constituted one of the branches of the mammal-like reptiles, which the ancestors of mammals (and hence the remote ancestors of humans) also belonged to. Shortly before the disappearance of the dicynodonts by the late Late Triassic, there had evolved some gigantic forms as the species discovered at the Lisowice site in Poland.
During the last 10 years, the Lisowice site has yielded lots of interesting findings, the most famous of which are two giants: (1) An unnamed yet, robust, 5–6 meters long dicynodont was the biggest known herbivore of its time. (2) The carnivorous dinosaur Smok wawelski, of a comparable length of 5–6 meters, was the largest terrestrial predator of its epoch too. The Lisowice site presents an ecosystem of the Norian or Rhaetian, the Late Triassic, dated back to around 208 million years ago. The epoch of the mammal-like reptiles was about to be finished, leaving nevertheless the legacy of the first mammals, whereas the dinosaurs had recently begun to proliferate.
The giant dicynodont has left for paleontologists its bones, footprints, and scats, which still are being studied. Now, let’s make a preliminary reconstruction of that animal and its habits in the environment of the Triassic of Lisowice.
Ecological niche of the dicynodont
In 2011, during my visit to the site, the paleontologist Grzegorz Niedźwiedzki showed me numerous and enigmatic, oval, dark gray structures, mostly below 10 cm in length. The finding appeared to be exciting as we were talking about possible coprolites, it means fossilized feces of the dicynodont. Herbivore coprolites (or their descriptions) are exceptionally rare on a world scale, but first and foremost these fossils constitute an invaluable source of information about the diet and the physiology of extinct animals whose bone remains we unearth. Three years later came a preliminary publication on this material, whose I’m the first author in collaboration with Krzysztof Owocki and Grzegorz Niedźwiedzki.
Although the putative coprolites contain organic matter, in the macroscopic view most of them reveal very few plant remains. The herbivorous diet of their producer was corroborated by analyses of the isotopes of carbon (δ13C) and nitrogen (δ15N). The coprolites enclose several types of pollen and also tissues of gymnosperms. There are also some very rare specimens of another type that are replete with wood fragments.
Sedimentological analyses, it means the study of the deposited sediments, as well as the geochemical analyses, suggest that the Lisowice site represented an environment comparable to the wetlands of the Everglades, Florida. The lack of woody plant elements in the vast majority of the coprolites of the giant dicynodont might be explained simply by the consumption of soft plants.
Now, let’s compare the dicynodont to the hippo. Although the hippopotamuses consume soft aquatic plants, this food resource is insufficient for these sizable animals. At night, the hippos leave the water pools to graze on grasses, but the grasses hadn’t yet evolved in the Triassic. Here, the rare wood-rich coprolites appear interesting. In 2007, Karen Chin described wood-rich coprolites produced by the herbivorous dinosaur Maiasaura from the Cretaceous of Montana. Although it would seem a weird custom in modern animals, Karen Chin suggested that the coprolite producers intentionally ingested rotted, partially decomposed wood and noticed the lack of grasses in the ecosystems of the Cretaceous. The rotting wood might be easily accessible in the wetlands of Lisowice.
Dicynodont coprolites are fairly numerous at the Lisowice site and it’s not ruled out that the dicynodont lived in herds, although scats tend to be abundant around sources of drinking water. In 2013, there were described copious accumulations of dicynodont coprolites from the Triassic of Argentina. The team of researchers led by Lucas Fiorelli suggested that the dungs were made in communal latrines, just as some modern mammals do it, in particular large herbivores. The hippopotamuses form small herds too.
Physiology of the dicynodont
Below, I list the titles of several of the numerous papers of German physiologists that constitute a source of a scientific inspiration for me and allowed a preliminary draft of the physiology of the dicynodont from Lisowice in the publication of 2014. On my blog, in various occasions I will highlight the significance of fossil feces for the understanding of the physiology of extinct animal groups.
To say something about the physiology of the dicynodont, firstly we note that modern reptiles are characterized by a long retention of food in the gastrointestinal tract, i.e. by a slow metabolism. On the other hand, the mammals used to initially triturate the food in the mouth and then it passes rapidly through the gastrointestinal tract. The mammalian groups vary between each other in the digestive strategy too. To eat more not always means to gain more. With the increase of consumption, accelerates the passage of the ingesta through the gastrointestinal tract as well, resulting in a worse digestion. For example, the hippo is capable to consume 45–50 kg of forage a day (I mean a dry matter). Each additional kilogram would paradoxically cause an energetic loss and no longer a gain, so that the hippopotamuses spend only 30% of a day foraging. This phenomenon is minimized in the elephants, which spend 75% of a day foraging.
However, to eat more involves to be less choosy and to ingest foodstuffs of a lower quality. Apart from the mentioned exceptions, the food of the dicynodont from Lisowice used to be non-fibrous and hence it seems that it ate little. It’s important to note that the dicynodont was toothless. In modern herbivorous mammals a better mastication of food allows to increase the total consumption. It can be observed via juxtaposition of different groups of mammals, or mammals with reptiles. We conclude that the dicynodont consumed relatively small amounts of forage and then it was retained for a long time in the gastrointestinal tract. Thus, in this mammal-like reptile we can see a strategy more typical of reptiles than mammals, yet it supports the comparison to the hippopotamus, which is an animal of a low-energy lifestyle.
The coprolites of the dicynodont from Lisowice contain a good deal of quartz grains. So-called gastroliths are hard objects missing a nutritional value that are found in the gastrointestinal tract. It’s very common to highlight the role of gastroliths in the crumbling of food particles in the stomach of some animals. However, such a mechanism seems unsubstantiated in the case of the dicynodont from Lisowice. The mineral grains in the coprolites are rather small and could be swallowed accidentally in large amounts in the wetlands with forage or turbid water. The amounts of sand and small gravel found in the stomachs of hippopotamuses are astonishing, sometimes reaching one third of the weight of their (wet) content.
Finally, we can note that the increase of the body size can serve as a strategy allowing a prolonged food retention in the gastrointestinal tract and a better digestion. The body size of dicynodonts was increasing across the Triassic, and the latest of their members, it is the dicynodont from Lisowice, was a real giant. A super strong digestion of a weak food might explain in general the high fragmentation of the plant remains in the coprolites of the dicynodont (although in part it was caused by destructive processes when the fresh dung was turned into a rock). In mammals, after an initial mastication the ingested plant tissues do not reduce in size significantly during the passage through the gastrointestinal tract. In modern herbivorous reptiles, which are characterized by a much longer digestion, the ingested plant tissues do indeed get crumbled due to the digestive processes. In spite of such a reduction, the residues in the feces of reptiles on average are still of larger dimensions than in feces of herbivorous mammals (of a comparable body mass). Today’s reptiles, as some lizards, are however very small animals and none of them can be compared to the gigantic dicynodont from Lisowice.
As it was noted by the team of Grzegorz Niedźwiedzki in 2011, meanwhile the body size of dicynodonts was increasing during their evolution, the predators were growing too. Tooth marks on the bones of the dicynodont moreover suggest that it was under the pressure of the mentioned carnivorous dinosaur Smok wawelski. It’s very interesting the way the physiological innovations, new feeding strategies, and the expansion into new ecological niches, fitted into the race between herbivores and predators.
Bajdek, P., Owocki, K., and Niedźwiedzki, G. 2014. Putative dicynodont coprolites from the Upper Triassic of Poland. Palaeogeography, Palaeoclimatology, Palaeoecology 411: 1–17. doi: 10.1016/j.palaeo.2014.06.013
Chin, K. 2007. The paleobiological implications of herbivorous dinosaur coprolites from the Upper Cretaceous Two Medicine Formation of Montana: why Eat Wood? Palaios 22: 554–566. doi: 10.2110/palo.2006.p06-087r
Clauss, M., Streich, W.J., Schwarm, A., Ortmann, S., and Hummel, J. 2007. The relationship of food intake and ingesta passage predicts feeding ecology in two different megaherbivore groups. Oikos 116: 209–216. doi: 10.1111/j.2006.0030-1299.15461.x
Dzik, J., Sulej, T., and Niedźwiedzki, G. 2008. A dicynodont-theropod association in the latest Triassic of Poland. Acta Palaeontologica Polonica 53 (4): 733–738. doi: 10.4202/app.2008.0415
Fiorelli, L.E., Ezcurra, M.D., Hechenleitner, E.M., Argañaraz, E., Taborda, J.R.A., Trotteyn, M.J., Belén von Baczko, M., and Desojo, J.B. 2013. The oldest known communal latrines provide evidence of gregarism in Triassic megaherbivores. Scientific Reports 3, 3348. doi: 10.1038/srep03348
Fritz, J., Hummel, J., Kienzle, E., Streich, W.J., and Clauss, M. 2010. To chew or not to chew: fecal particle size in herbivorous reptiles and mammals. J. Exp. Zool. A Ecol. Genet. Physiol. 313A (9): 579–586.
Martin, R.B. 2005. Transboundary Species Project. Background Study: Hippopotamus. Namibia Nature Foundation, Windhoek.
Niedźwiedzki, G., Gorzelak, P., and Sulej, T. 2011. Bite traces on dicynodont bones and the early evolution of large terrestrial predators. Lethaia 44: 87–92. doi: 10.1111/j.1502-3931.2010.00227.x
Niedźwiedzki, G., Sulej, T., and Dzik, J. 2012. A large predatory archosaur from the Late Triassic of Poland. Acta Palaeontologica Polonica 57 (2): 267–276. doi: 10.4202/app.2010.0045
Schwarm, A., Ortmann, S., Wolf, C., Streich, W.J., and Clauss, M. 2009. More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comp. Biochem. Physiol. A 152 (4): 504–512.