My recent article on fruit-eating Italian Wall Lizards (Podarcis siculus) turned up an intriguing story about this lizard. In 1971 five pairs of this species were introduced onto the Croatian islet of Pod Mrčaru from a nearby islet, Pod Kopište, in the Adriatic Sea. Since that time the population has been studied intensively because, it was found, those on Pod Mrčaru ate far more plant material than those on Pod Kopište. Thirty-six years after the population was introduced plant material comprised 34% in spring and 60% in summer of the stomach contents, compared with 7% and 4% in the lizards of the original population.
Associated with that change in diet were a number of morphological changes. The heads were bigger and the bite force greater in the omnivorous lizards on Pod Mrčaru, changes attributed to the need to tear up plant material before swallowing. Particularly interesting to me was the finding of ‘caecal valves’ in the large intestine. In herbivorous lizards these structures are present and appear to impede the passage of digesta and thereby provide a fermentation chamber for the digestion of cellulose by micro-organisms. Nematodes were present in the gut of the omnivorous population suggesting they were ingesting the digested plant material.
The authors of this first study, published in 2008, were, in my opinion, unwise in appearing to favour the view that these changes within a species were caused by natural selection over a period of a few generations and were therefore an evolutionary event with a change in gene frequency akin to that seen in, say, industrial melanism in moths. The alternative but not mutually exclusive explanation is that lizards of this species have sufficient individual plasticity to respond in the way that they have to the ingestion of plant material. A paper published in 2010 by a largely different group not only extended the original observations but also obtained evidence that plasticity is the more likely explanation for the changes observed in the digestive system
A key experiment was of course to reverse the availability of plants in the diet. Genetically determined adaptations would not be reversed by a return to carnivory within a lifetime while adaptation brought about by a plastic response to the diet would be expected to lead to reversion. This experiment was done by the second group of researchers. Lizards from the introduced, omnivorous, were fed exclusively on arthropods for 15 weeks. One characteristic of the omnivorous lizards was a heavier and longer large intestine. In the arthropod-fed group, the size of the large intestine was smaller. Furthermore, there was no sign of a caecal valve in any of the 20 animals that had been fed exclusively on arthropods.
The second group of authors also cast doubt on whether the larger heads and bite strength of the lizards on Pod Mrčaru are directly related to their plant-rich diet. The greater population density of the lizards on Pod Mrčaru compared with Pod Kopište may have resulted in selection for greater ability for physical combat. That selection pressure rather than that from the tearing of plant material may have lead to the larger body sizes, the more robust heads and the greater bite force observed in the Pod Mrčaru lizards
While a mixture of selection and plasticity may explain the overall changes in the lizards on Pod Mrčaru, it does seem likely that with respect to the digestive system the changes are the result of plasticity not selection. This conclusion does not mean to say that in other species of lizard which are largely herbivorous the presence of a large colon containing a number of caecal valves is not genetically determined.
Worth noting here is the fact that the Wikipedia article on this lizard is misleading—as is so often the case on herpetological matters—and does not take into account later findings on the lizards of Pod Mrčaru.
If there are—as does seem to be the case—species of lizards that can change to a more herbivorous diet, develop the morphological and biochemical features necessary to digest plant material and absorb the nutrients produced in a reversible manner then three questions arise. The first is why the lizards introduced to Pod Mrčaru began to eat a larger proportion of plant material. Was it because the competition for food resources in the form of small invertebrates became intense as the population grew? The second question is the reversible mechanism by which the colon forms caecal valves.
Looking at photographs of the caecal valves in P. siculus and at those from other, mainly herbivorous species, it appears that the valve comprises a transverse infolding of the wall of the colon. It is relatively easy to envisage an area of localised cell division and development of a ridge which narrows the lumen. In reverse, local loss of cells would flatten the infolding. For those physiologists and cell biologists working on local signalling mechanisms in the intestine P. siculus is not without interest. Incidentally, research over the past forty years has shown the alimentary canal of reptiles to be highly labile in response to changes in food intake; far more so than would have seemed imaginable.
Later work, published in 2020, in again comparing the lizards on the two islets have not been so clear cut but do support plasticity as the explanation. I have some qualms about the methodology and the lack on information on the actual absorption of nutrients from the gut as opposed to concentrations found therein. However there was clear evidence that in 2013 no lizards were found on Pod Mrčaru with caecal (also known as hindgut) valves. The reason for that shift over time can be debated but these findings strongly support the view that the induction of enzyme and nutrient transport systems as well as the growth of caecal valves are part of the result of plasticity within an individual rather than the outcome of a process of natural selection.
The third question is whether lizards of this species turned to an omnivorous or largely herbivorous diet elsewhere in their large range. The current field guide to European reptiles describes Podarcis siculus as ‘an opportunistic feeder, taking a variety of invertebrates and plant matter’. The sort of response that given current knowledge would be expected could very much depend on the type of plant food being eaten. There is a world of difference in the sort of chemical digestion and nutrient absorption needed to process sugar-rich fruit, as in the grape-eating lizards from mainland Italy that made their way accidentally to UK, and other plant materials for which the digestion of cellulose by microorganisms is necessary.
The opportunistic nature of Italian Wall Lizards can be seen in the following photographs sent to me by a regular reader of these articles, David Lambert. They were taken at Punta del Capo, a small flat-topped rocky promontory near Sorrento. The lizards proved very willing to share a picnic and his photographs show them eating banana, tomato and bread.
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| David Lambert's photograph of an Italian Wall Lizard eating bread |
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| ...and banana |
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| ...and tomato |
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| The location of the islets in the Adriatic From Wehrle et al 2020 |
In chronological order:
Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, Van Damme R, Irschick DJ. 2008. Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the USA 105, 4792-4795 doi10.1073/pnas.0711998105
Vervust B, Pafilis P, Valakos ED, Van Damme R. 2010. Anatomical and physiological changes associated with a recent dietary shift in the lizard Podarcis sicula. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 83, 632-642 doi.org/10.1086/651704
Wehrle BA, Herrel A, Nguyen-Phuc B-Q, Maldonado S, Dang RK, Agnihotri R, Tadić Z, German DP. 2020. Rapid dietary shift in Podarcis siculus resulted in localized changes in gut function. Physiological and Biochemical Zoology 93, 396–415. DOI: 10.1086/709848
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