Tortoise hatchlings show a surprising preference for face-like stimuli.

Aspontaneous preference to orient toward faces and face-like configurations (three blobs arranged as an upside-down triangle inside an ellipse) has been observed at the beginning of life in Human neonates and fetuses. To date, this spontaneous preference has been investigated only in social species that rely on early parental care. Hence, a possibility is that the preference for facelike stimuli is an adaptation of social species for orienting toward the conspecifics and sustaining parental care. Alternatively, the preference for face-like stimuli might be a behavioral mechanism used to attend to living beings, or just a by-product of the architecture of the visual system. Only if these alternative hypotheses are correct would one expect solitary species without parental care to show a preference for face-like stimuli at birth. To clarify whether the preference for face-like stimuli depends on parental care, evidence from taxa with no parental care is needed. Land Tortoises are a convenient model system to investigate this issue because they can be tested soon after hatching and are solitary: Tortoises of the Testudo genus have no posthatching parental care, indicating that, for at least 30 million years, they have evolved with no parental care, they do not aggregate or form cohesive social groups, and hatchlings tend to ignore or avoid conspecifics, showing that, from the beginning of life, they are not gregarious. If the preference for face-like stimuli evolved as a behavioral mechanism to enhance parental care or interactions with conspecifics, Tortoise hatchlings should not show this preference.

In a paper punlished in the Procedings of the National Academy of Sciences of the United States of America on 29 September 2020, Elisabetta Versace of the Department of Biological and Experimental Psychology at Queen Mary University of London, and of the Center for Mind/Brain Sciences at the University of Trento, Silvia Damini, also of the Center for Mind/Brain Sciences at the University of Trento, and Gionata Stancher, once again of the Center for Mind/Brain Sciences at the University of Trento, and of the Fondazione Museo Civico Rovereto, present the results of a series of experiments which sought to test this hypothesis. 

Versace et al. measured the first approach responses of naïve Tortoise hatchlings of the genus Testudo to face-like stimuli vs. different control stimuli previously used in other studies. The first approach is not influenced by experience and is not affected by individual and species differences in speed. To parallel previous studies, Versace et al. used different alternative stimuli: upside-down face-like stimuli to test a preference for the orientation of the configuration, top-heavy stimuli to test the preference for a heavier part of the item in the absence of a triangular configuration, and asymmetrical stimuli to test the preference for the bilateral symmetry of the face-like stimulus. Because the previous experiments indicated a preference for face-like stimuli vs. upside-down and asymmetrical stimuli but not vs. top-heavy stimuli, Versace et al. ran an experiment to clarify whether vertical patterns elicit a preference over horizontal patterns and an experiment with a squared/noncongruent configuration vs. a scrambled/congruent configuration congruent with the horizontal orientation of the contour.

 

(A) (i) Face-like, (ii) upside-down, (iii) top-heavy, (iv) asymmetrical, (v) horizontal, (vi) vertical, (vii) squared/noncongruent, and (viii) scrambled/congruent to contour. (B) Test apparatus: The subject was located in the starting point facing a short wall, and the first area entered with the entire shell was scored. (C) Preference for the face-like (vertical/congruent) stimulus as percentage of choices. Versace et al. (2020).

In the face-like vs. upside-down experiment, Versace et al. observed a significant preference for the face-like stimuli: 70%; in the face-like vs. asymmetrical experiment, Versace et al. observed a significant preference for the face-like stimulus: 74%; in the face-like vs. top-heavy experiment, Versace et al. observed no significant preference for the face-like stimulus: 56%. The last two experiments suggest that the preference might be sustained by top-heavy patterns, with blobs congruent to the contour orientation. In fact, we observed a significant preference for the vertical vs. horizontal stimulus (68%) and for the scrambled/congruent vs. squared/noncongruent stimulus (66%).

Versace et al. tested whether the spontaneous attraction for face-like stimuli found in social species with parental care, such as Human beings, Monkeys, and domestic Chicks, is present also in land Tortoises, that are solitary animals with no parental care. Surprisingly, naïve Tortoise hatchlings exhibited a preference for face-like configurations too. Versace et al. show that the preference for face-like stimuli is present in solitary species at the beginning of life. These results suggest that the predisposition to orient toward faces/face-like stimuli is not an adaptation for parental care or for sustaining engagement with conspecifics. Then, what is the functional value of this trait, if any? A possibility is that Tortoises are attracted to cues associated with living Animals, such as face-like stimuli, because living Animals provide relevant information, such as the availability of resources. Predispositions might be mechanisms to enhance the acquisition of information from other Animals. Indirect evidence for this explanation comes from the fact that Tortoise hatchlings initially explore unfamiliar individuals before actively moving away from them. Another possibility is that this predisposition has no functional adaptive value but derives from a sensitivity of the visual system to top-heavy patterns congruent with the orientation of the bounded area delimiting the features. Although this explanation is in line with the preference for patterns congruent with the contour, it does not account for the face-like vs. upsidedown preference. Briefly, Versace et al. showed that Tortoise hatchlings can discriminate between different configurations of blobs and that the preference for face-like stimuli is not limited to Mammals and Birds but extends to Reptiles. This suggests the presence of an ancient mechanism for orienting toward face-like patterns, evolved in the common ancestors of Mammals, Reptiles, and Birds more than 300 million years ago, possibly from a bias toward top-heavy, symmetrical stimuli congruent with the orientation of the outline. Versace et al.'s research calls for further studies to test the hypothesis that predispositions present at the beginning of life are mechanisms that enhance exploration and learning in both solitary and social species.

See also...

Follow Sciency Thoughts on Facebook.

Follow Sciency Thoughts on Twitter.

 

Crocodiles and Tortoises from the Late Pleistocene of Aldabra Atoll in the Seychelles

Understanding predator-prey relationships is a key part of reconstructing past ecosystems, yet this is often difficult to do. The most reliable ways to do this are to find traces of prey items within the digestive tracts of fossilised predators, but such fossils are extremely rare, so palaeontologists often look for other evidence, such as preserved material within copralites (fossilised feces) or bite marks on bones or shells. Testudines (Turtles and Tortoises) have been around since the Triassic, and their fossils often show signs of feeding traces from predatory animals. Thus fossil Testudines are known with damage assigned to the actions of a number of different predators, from Dinosaurs to Badgers, while modern Testudines are known to be predated by a wide range of Mammals, Crododylians, Birds, Sharks, Fish and even Crabs.

In a paper published in the journal Royal Society Open Science on 24 January 2018, Torsten Scheyer of the Palaeontological Institute and Museum at the University of Zurich, Massimo Delfino of the Dipartimento di Scienze della Terra at the Università di Torino, and the Institut Català de Paleontologia Miquel Crusafont at the Universitat Autònoma de Barcelona, Nicole Klein of the Steinmann Institut für Geologie, Paläontologie und Mineralogie at the Universität Bonn, Nancy Bunbury and Frauke Fleischer-Dogley of the Seychelles Islands Foundation and Dennis Hansen of the Zoological Museum and the Department of Evolutionary Biology and Environmental Studies at the University of Zurich, describe a series of Crocodylian and Tortoise remains from around a Late Pleistocene pool on Aldabra Atol in the Seychelles, and infer a predator-prey relationship between them.

Aldabra is currently home to about 100 000 Giant Seychelles Tortoises, Aldabrachelys gigantea, a population that was almost wiped out by Human predation in the nineteenth century, but which, like the Giant Tortoises of the Galapagos Islands, is thought to be largely immune from non-Human predation on account of the size and heavy armour of the Tortoises. Scheyer et al. record the discovery of a large number of disarticulated Tortoise shell fragments from the Late Pleistocene of Aldabra Atoll, which appear to have come from animals identical to the modern population, and are therefore assumed to be the same species. Many of these fragments show round puncture marks, thought most likely to have been caused by the bite of a large Crocodylian, as they are inconsistent with bite marks made by any known Mammal species (and no large Mammals are known from the Pleistocene of the Seychelles) but similar to bite marks made by living Crocodiles.

Overview of new Giant Tortoise material fromthe Late Pleistocene of Aldabra Atoll. (a) Large nuchal still sutured to first left peripheral in dorsal and ventral view; (b) small nuchal in dorsal and ventral view, note cervical scute in both nuchals; (c) larger costal fragment in ventral view; (d) a smaller costal fragment with sulcus in dorsal and ventral view; (e) smaller hyo- or hypoplastron fragment  in ventral and dorsal view; (f ) larger hyo- or hypoplastron fragment in ventral and dorsal view; (g) small shell fragment which might also pertain to a costal in purported dorsal view; (h–k) associated pelvic girdle elements; (h) distal part of an ilium in lateral and medial view; (i) fused pubes in angled anterodorsal view; (j) fused ischia in angled posterodorsal, angled posteroventral and posterior view; (k) fused pubes and ischia in natural articulated position in dorsal view. Scheyer et al. (2018).

Scheyer et al. also report the discovery of a number of Crocodile bones from the site. These are not  assigned to a specific species due to their fragmentary nature, but are thought likely to have come from Aldabrachampsus dilophus, an extinct species previously described from Pleistocene deposits on the island. The original material assigned to Aldabrachampsus dilophus was from an animal estimated to have been about 2-2.5 m in length, and therefore unlikely to have been able to tackle Tortoises which themselves could exceed a meter in length, but the new material appears to have come from an animal as large as 3.7 m  long, much more likely to have been capable of handling such prey. Scheyer et al. stop short of positively identifying Aldabrachampsus dilophus as the animal responsible for the attacks, however, as the islands are known to have previously been home to at least one other large Crocodylian, the Saltwater Crocodile, Crocodylus porosus, which was present in the Seychelles until wiped out by Human activity in the early nineteenth century.

 Overview of new Crocodylian material from the Late Pleistocene of Aldabra Atoll. (a) Larger left dentary fragment with alveoli d3–d8 preserved in dorsal, medial and lateral view; (b) small left dentary fragment with alveoli d4–d6 preserved in dorsal and ventral view; (c) skull roof fragment consisting mainly of the left postorbital and partial frontal and parietal fragments in dorsal and ventral view; (d) dorsal procoelous vertebra with neural arch preserving the postzygapophyses in left lateral, right lateral and anterior view; (e) strongly eroded vertebral centrum still preserving the prezygapophyses in dorsal, ventral, right lateral and anterior view; (f ) isolated left prezygapophysis in dorsal view; (g) posterior half of osteoderm in dorsal, ventral and posterior view. Scheyer et al. (2018).

Scheyer et al. further note that all of the observed damage to Tortoise shell scutes (plates) is from the area around the front aperture of the shell, and that none of the shells show signs of having become disarticulated by any means other than natural decay. This indicates that the Crocodiles were using the front aperture of the shell to gain access to meat of the Tortoise, but that they were incapable of actually breaking open the shells.

 Size comparison of Crocodylian and Giant Tortoise remains. (a) Image and interpretative drawing of larger left dentary fragment; broken bone surface area indicated by grey patch) scaled and fitted to lower jaw of extant Crocodylus niloticus. In addition, the outline of right dentary fragment of Aldabrachampsus dilophus has been added for comparison; (b) image and interpretative drawing of skull roof fragment consisting of the postorbital (broken bone surface area indicated by grey patch), and frontal and parietal fragments scaled and fitted to skull of extant Crocodylus niloticus. For comparison, the outline of the right squamosal of Albadrachampsus dilophus; (c) dorsal and ventral sides of the larger nuchal with interpretative drawings of sutures and scute sulci superimposed. Note equidistance of some of the feeding traces (marked by white arrowheads connected by thin white stippled line), whichmight indicate repeated bites of the same Crocodylian jaw portion; (d) larger nuchal scaled to fit a large male Aldabrachelys gigantea with a headwidth of 95.1 mm and a curved carapace length of 114.4 cm. This specimen has a cervical scute width of about 30 mm, comparable to the maximum width of the same element in the fossil. ce, cervical scute;m1–2, marginal scute 1–2; d3–d10, dentary alveolus 1–10; df, dental foramina; f, frontal; n, nuchal; p, parietal; p1, first peripheral; po, postorbital, sq, squamosal, v1, first vertebral scute. Scheyer et al. (2018).

The presence of Crocodylian bite marks around the front apertures of Giant Tortoise shells could indicate that the Crocodiles were ambushing the Tortoises at water holes, hiding beneath the water then seizing the Tortoises as they attempted to drink with their vulnerable heads and necks extended, which would be consistent with the hunting methods of modern Crocodiles.

 Possible Pleistocene trophic interaction scenario including Crocodylian and Giant Tortoise based on new fossil evidence. Hunting Crocodylian attracted by drinking Tortoise. The attack likely occurred frontally or fronto-laterally where the head, neck and soft tissue parts of the anterior shell aperture are exposed. Scheyer et al. (2018).

However it cannot be ruled out that the Crocodiles were simply scavenging the bodies of Tortoises that had died for other reasons (also consistent with the behaviour of modern Crocodiles), and that they were concentrating this scavenging around the front aperture as this was the only way in which they could gain access to the meat of the Tortoises.

Second possible Pleistocene trophic interaction scenario including Crocodylian and Giant Tortoise based on new fossil evidence. Decomposing tortoise carcass at breakdown stage 2 (putrid stage, with Dipterans and Ants) attracting scavenging Crocodylian and Coconut Crab. The spreading of the latter throughout the Indo-Pacific region has been proposed to have happened during the Pleistocene, and today this Crab is one of the most active decomposition agents on Aldabra Atoll. As in the previous scenario, the Crocodylian is hypothesised to approach the carcass from the front, at the point of easiest access to the viscera. Scheyer et al. (2018).

See also...

Follow Sciency Thoughts on Facebook.

Understanding the origins of the Giant Tortoises of the southwest Indian Ocean.

Giant Tortoises were once numerous on both continental and island landmasses, though most of the continental species became extinct in the Late Pleistocene and most of the island species in the Holocene, all of which extinctions have been linked to a single cause, the spread of Modern Humans around the globe. Today only two species of Giant Turtle remain, Chelonoidis nigra in the Galapagos and Aldabrachelys gigantean on Aldabra Island, a small coral atoll in the Indian Ocean, about 400 km north of Madagascar and about 600 km west of the east coast of Africa. The southwest Indian Ocean was formerly somewhat of a hotspot for Giant Tortoise diversity, with at least two species on Madagascar, plus two species on Mauritius, two species on Rodrigues and one on La Réunion.

An Aldabra Giant Tortoise, Aldabrachelys gigantean. Wikipedia.

How the Tortoises got to these islands is somewhat of a mystery; the ancestors of the Giant Tortoises of Madagascar presumably reached there while Madagascar was still attached to the Gondwanan supercontinent in the Cretaceous, or floating there from Africa in the Eocene or earlier, when prevalent currents in the southwest Indian Ocean ran from Africa towards Madagascar (Giant Tortoises seldom voluntarily swim, but float well and can survive long periods at sea, so Tortoises swept out to sea by, for example, flood events, have a reasonable chance of surviving till they reach a new landmass). However from the end of the Eocene onwards, prevalent currents in the southern Indian Ocean have all flowed east-to-west, making it highly unlikely that a Tortoise could drift from island to island in this direction without swimming hundreds of kilometres against the current. This makes the presence of Tortoises on smaller Indian Ocean islands hard to understand, as all of these islands have appeared since the end of the Eocene; Mauritius having first appeared about 8.9 million years ago, La Réunion about 2.2 million years ago and Rodrigues about 1.5 million years ago, while Aldabra, with a highest point only eight meters above sea level, has emerged from and been covered by the sea several times during the past million years, and is thought to have been continuously exposed only for the last 80 000 years.

In a paper published in the Journal of Biogeography on 11 March 2016, Lucienne Wilmé of the School of Agronomy at the University of Antananarivo, and the Missouri Botanical Garden's Madagascar Research & Conservation Program, Patrick Waeber of Forest Management and Development at the Swiss Federal Institute of Technology Zurich, and Joerg Ganzhorn of Animal Ecology and Conservation at Hamburg University, discuss the possibility that Giant Tortoises may have reached the islands of the southwest Indian Ocean not by drifting on ocean currents, but by active movement by Humans.

The earliest Humans arrived on Madagascar about 4000 years ago. These were fairly advanced, already having metal tools, and are thought to have come from Southeast Asia, with subsequent waves of arrivals from Arabia, Africa and eventually Europe. People from Southeast Asia began making ocean-crossing journeys about 45 000 years ago, hopping from island-to-island to reach remote parts of the Indian and Pacific Oceans, as well as the continent of Australia, and possibly South America.

During this process they introduced many animals and plants to the islands they visited, such as Pacific Rat, Rattus exulans, Chicken, Gallus gallus, Sweet Potato, Ipomea batatas, Taro, Colocasia sp., and Banana, Musa sp.. Giant Tortoises have been considered to be excellent eating by most cultures that have encountered them (most species being wiped out by encounters with hungry European sailors in the eighteenth and nineteenth centuries). It is not, therefore, an outlandish idea that early navigators might, having encountered Giant Tortoises on Madagascar, have moved small populations to other islands in the Indian Ocean as a potential food source, either for colonists living permanently on the islands or for other sailors visiting the islands (European sailors introduced Sheep and Goats to many small islands for similar reasons).

Giant land tortoises, geology, oceanography, archaeology of the south-western Indian Ocean, and distance between islands and ocean surface currents prevailing since the closure of the Tethys Ocean. (SdM = Saya de Malha; N = Nazareth; StB = St Brandon; LGM = Last Glacial Maximum). Wilmé et al. (2016).

Wilmé et al. note that no ancient archaeological sites have been found on the Mascarine Islands (Mauritius, Rodrigues and La Réunion), which would seem to present a problem to this theory. However they note that sealevels have varied considerably over the past few thousand years, which has a particularly strong effect on small islands, so that it is quite possible ancient coastal settlements around these islands may have been covered by rising seas.

More problematically, the Tortoises of the southwest Indian Ocean are considered to have belonged to eight different species, which seems unlikely if they were all transplanted from Madagascar (where only two species are known). Wilmé et al. do not dispute the current accepted taxonomy of these species, however they do observe that species isolated on small islands are known to evolve rapidly, and that Tortoises, which produce particularly large clutches of young, are potentially more prone to this effect than slower breeding groups such as Birds or Mammals.

See also...

Follow Sciency Thoughts on Facebook.

The death of Lonesome George and the extinction of the Pinta Island Giant Tortoise.

On 24 June 2012 Edwin Naula of the Galápagos National Park announced the death of a Giant Tortoise named Lonesome George at the Charles Darwin Research Station on Santa Cruz Island. Lonesome George had been a resident of the Station since 1972, after it was discovered that his native habitat on the remote, volcanic, Pinta Island had been devastated by introduced feral goats.

Lonesome George. Galápagos National Park.

Lonesome George was almost certainly the last member of his species, the Pinta Island Giant Tortoise, Chelonoidis nigra abingdoni, (there is another male Tortoise rumored to be a member of the species in Prague Zoo, but this animal has never been formally described in any scientific publication), meaning that his death comes the extinction of the species. The Charles Darwin Research Station had made several attempts to mate Lonesome George with females of the closely related Isobella Island Tortoise, Chelonoidis nigra becki, but this had failed to produce viable eggs (note: technically Chelonoidis nigra abingdoni and Chelonoidis nigra becki are subspecies, but most biologists define species as reproductively isolated units, which would seem to apply here). This was combined with the clearing of feral goats from Pinta Island, with a view to re-introducing the (hybrid) tortoises; it is likely that the Island will now be re-populated by Tortoises from elsewhere in the Galapagos. 

The Galapagos Islands have (or had) a distinctive fauna of Tortoises, with many islands, and some regions on larger islands, having evolved their own distinctive strains of Tortoise adapted to local conditions. When Charles Darwin visited the Galapagos in 1835 the Vice Governor of the islands, Nicholas Lawson, boasted of being able to tell what island a tortoise originated from at a glance. 

Scientists currently recognize twelve different varieties of Galapagos Tortoise, all currently classified as subspecies of a single species, Chelonoidis nigra. The Pinta Island Tortoise is the second of these to go completely extinct, after the Charles Island Tortoise, Chelonoidis nigra nigra, with the Duncan Island Tortoise, Chelonoidis nigra duncanensis, also extinct in the wild. In addition the Hood Island Tortoise, Chelonoidis nigra hoodensis, is considered Critically Endangered under the terms of the IUCN Red List of Threatened Species, with another four strains being considered Endangered, and the remainder Vulnerable.

See also An Eucryptodiran Turtle from the Early Cretaceous of Spain, A new species of Giant Side-Necked Turtle from the Palaeocene of Columbia, New species of Catshark from the Galapagos, Lost fossils of Charles Darwin and Joseph Hooker rediscovered and Reptiles on Sciency Thoughts YouTube.

Follow Sciency Thoughts on Facebook.