By Stamatis Kalogiannis
- Charles Darwin, The Voyage of the Beagle, 1891
Introduction
Island ecosystems have fascinated naturalists and biologists for centuries. Ever since the great Charles Darwin published his observations on natural selection from the Galapagos islands, it has become a well-known fact that the evolution of island populations works in peculiar ways. So much, that many experiments and studies working on resolving the wonders of evolution have taken place on islands, bringing us many fundamental theories of evolutionary biology along the way (e.g. Foster's rule).
In Greece, a large amount of research on ecology, phylogenetics, ethology and evolution has been devoted to insular reptiles. This has uncovered a remarkable diversity of taxa, a rich evolutionary and geographic history, and lots of interesting data on diet, sexual selection, spatial ecology, etc. In fact, Greece can be described as Europe's biggest evolutionary lab. Our country has so many islands and islets across so many different biogeographical units, and the majority of them host reptiles and amphibians - many of them being endemic. This sets an interesting area to study reptile and amphibian evolution in isolation, as well as their zoogeography and ecology.
Diversity of herpetofaunal taxa on Greek islands
The species composition of reptiles and amphibians on each Greek island largely depends on its location and paleogeographic history; for example, the Ionian islands mainly bear species of Balkan and southern European origin, while the composition of the Dodecanese islands consists of primarily Anatolian species. When it comes to the number of species present on each islands, it is not as simple, and one has to take many more factors into consideration. The islands with the most herpetofauna species are; Euboea (39 species), Corfu (38 species), Samos (28 species), Lefkada (28 species), Kefallonia (27 species) and Lesvos (27 species). Two common traits are shared between these islands; (a) the really large size (all larger than 320km2) and wide habitat diversity, and (b) the small distance from the mainland and the recent connectivity to it, with Euboea (which has the largest count of species) having being isolated only for 5,500 years. So, which is the main factor at play here?
First, lets take a look at the number of herpetofauna species on some island examples in Greece in relation to size and isolation time. The isolation times are very approximate, as only limited sources exist on this subject, but they provide a general idea.
- Crete, 14* species, 8,336km2 area, isolated since the Late Miocene (5.3mya*)
- Euboea, 38 species, 3,684km2 area, isolated since the Middle Holocene (5.5kya*)
- Lesvos, 27 species, 1,633km2 area, isolated since the Late Pleistocene (11kya)
- Skyros, 11 species, 209,5km2 area, isolated since the Early Pliocene (5mya)
- Skiathos, 15 species, 47,3km2 area, isolated since the Late Pleistocene (11kya)
- Kythera, 11 species, 278km2 area, isolated since the Middle Pleistocene (100kya)
- Symi, 16 species, 57,8km2 area, isolated since the Late Pleistocene (11kya)
- Ikaria, 13 species, 255km2 area, isolated since the Middle Pleistocene (100kya)
- Corfu, 38 species, 590km2 area, isolated since the Early Holocene (10kya)
- Karpathos, 9 species, 324km2 area, isolated since the Late Miocene (5.3mya)
- Samos, 28 species, 477km2 area, isolated since the Early Holocene (10kya)
- Elafonisos, 12 species, 18km2 area, isolated since the Late Holocene (3kya)
Looking at these examples, you can't help but notice that islands of similar size host significantly different numbers of herpetofauna species. The islands with the more limited species tend to have seperated from the mainland much earlier than those with the more diverse herpetofaunas. This is especially evident in the case of Crete, which is the 5th largest island in the Mediterranean, having a list of only 14 species. This is due to its isolation time, since Crete has not been connected to another landmass since the flooding of the Mediterranean sea after the Messinian Salinity Crisis ended, 5.3 million years ago. On the other hand, the tiny Elafonisos (only 18km2) was isolated very recently, in 1000 BCE, and has a total of 12 recorded species (just 2 species less than Crete, which is over 400 times larger!). Keep in mind that Elafonisos has not received much attention from herpetologists, and is expected to host more species, unlike the well-studied Crete. It is therefore evident that isolation time is a very significant factor, even more than size and abundance of resources. However, a larger island with more habitat diversity is expected to maintain more species throughout the millennia in comparison to a smaller one. But why exactly is isolation time so important? Which factors drive localized extinctions of reptiles and amphibians on islands with the passing of time?
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| Species richness in Aegean and Ionian islands indicated by colors. Also shown is approximate exposed land area during the Last Glacial Maximum. |
1. Loss of genetic diversity
When a population of terrestrial animals gets geographically isolated, transfer of genetic material from the source population ceases to exist and genetic variation is significantly reduced. This is known as genetic drift or the Wright effect, and is what sometimes causes phenotypic aberration and speciation (hence why we have endemic taxa and weird phenotypes on islands, something further described by the Founder effect). In small populations, this leads to inbreeding and eventually accumulation of harmful mutations, a phenomenon called mutational meltdown. With harmful defects slowly piling up in an already small group of animals, individuals die before they are able to reproduce and their population eventually collapses. This is particularly common in islands, where gene flow from other populations is often impossible. In the depth of several millennia, this becomes a more prevalent occurence and can wipe out entire populations of a species or significantly lower its population densities on an island.
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2. Interspecific competition
Have you heard of the phrase 'This town ain't big enough for both of us'? Now imagine it being said between two different racer-type snake species that have just been isolated in a recently formed island. Eventually, they will outcompete one another. Competition between similar species that occupy the same ecological niche is really intense on islands, since both land area and resources are limited. Similarly to what the theory of natural selection says, the more versatile and better adapted species will usually dominate. Two perfect examples of snakes that share a somewhat identical niche in Greece are the Caspian whipsnake (Dolichophis caspius) and the Eastern montpellier snake (Malpolon insignitus), species that although often coexist in the mainland, they are rarely found alongside each other on islands. Only the larger and 'younger' islands host both species, and even in these cases, they are not found in the same abundances. For example, on Corfu and Kefallonia, Caspian whipsnakes are extremely rare and are only found in certain places, whereas Eastern montpellier snakes are in abundance everywhere. On the other hand, the northeast Aegean islands are home to bigger populations of Caspian whipsnakes, with Eastern montpellier snakes being more scarce. In other island clusters (e.g. the Cyclades), the presence of two or more large snake species on the same island is uncommon, and is restricted to islands closer to the adjoining mainland (e.g. Andros has both Caspian whipsnake Dolichophis caspius and Four-lined snake Elaphe quatuorlineata, with the latter existing in smaller numbers).
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| Caspian whipsnake (left) and Eastern Montpellier snake (right) |
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| An example of islands of similar size, divided only by a 3.7km strait, each hosting a different species of the same niche. |
Overall, multiple species of mutual niches rarely exist on more isolated islands, as there was enough time for pressure by competition to eventually push a species to localized extinction. Certain species may be less susceptible to aridity, scarcity of prey diversity, environmental changes and other pressures. The latter is discussed below.
The Pleistocene epoch was a period of repeated fluctuations in climate. Interglacial and glacial periods occured in frequent intervals, with the sea level often dropping as low as -120 meters. This largely affected the dispersal of herpetofaunal taxa among their southern refugia in Greece, with the end of the Last Glacial Maximum shaping their biogeography as we know it today. These climate shifts likely also played an important role in determining localized extinctions of taxa on isolated islands, especially those that were seperated earlier. As herpetofaunal populations were isolated on these islands during these repeated cold periods, they likely struggled to survive and many were wiped out. Islands that were only disconnected from other landmasses after the last cold period ended (10-20kya) tend to host more species, perhaps since reptiles and amphibians were able to re-colonize them as temperatures were rising. Isolated populations received more pressure from climatic extremes and with no land bridge available, gene flow or secondary re-colonization of species was impossible.
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| Reconstruction of the past 5 million years of climate history. © Wikimedia |
4. Natural disasters
This is not one of the more significant factors, but there is a case that is worth mentioning. The island of Santorini hosts one of the few active volcanoes in Greece. Its last big eruption occured in c. 1600 BCE, causing earthquakes and tsunamis that devastated the Minoan civilization. It was one of the largest volcanic eruptions in human history and completely altered the geomorphology of the island, giving it its crescent-like shape. Santorini is an oceanic island that was connected to other landmasses several times after its formation, likely allowing different biota to colonize it. It was permanently isolated approximately in the Middle to Late Pleistocene. It is believed that since 200,000 years ago, volcanic events occured repeatedly, each resulting in the formation of a caldera. These eruptions likely had a devastating effect on the local animal life, and probably completely wiped out most of the native herpetofauna. This is particularly evident in the fact that most recorded reptile species currently present on Santorini are especially susceptible to human-mediated translocations and are often associated with human presence on islands. Furthermore, some typical 'Cycladic' species are missing, and there are no amphibians or large snakes, while occuring species are not represented by well-diverged clades. It is therefore very likely that most - if not all - reptile taxa reached Santorini via human transportation after the Minoan eruption.
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| A more mild eruption of the Santorini volcano in 1950 |
Alternative methods of colonization
But there's more to it! Reptiles are known to colonize places via many different dispersal methods, and thus natural dispersal with past land bridges is not always the answer to a species' occurence on an island. An example of transmarine dispersal in reptiles has been demonstrated for the case of Crete by Kyriazi et al. (2012). Specifically, it was revealed that Cretan snakes originated through distinct colonization routes - 2/4 species (Hierophis gemonensis and Zamenis situla) dispersed from the west, likely from the Peloponnese mainland and through in-between 'stepping stones' (aka islands) by crossing the sea during the Pleistocene. The third species, Natrix tessellata, also reached Crete via transmarine dispersal, however originating from the Turkish mainland during the Plio-Pleistocene boundary. The fourth species, Telescopus fallax, reached Crete via a landbridge during the Messinian Salinity Crisis in the Miocene epoch, and is therefore the only species that was isolated by natural vicariance. The same colonization path as that of Natrix tessellata was also followed by the ancestors of the Balkan terrapins (Mauremys rivulata) on Crete, probably reaching the island by swimming from mainland Anatolia (Mantziou et al., 2004). In fact, Balkan terrapins have often been recorded to swim in the sea, and this is a very likely explanation as to how this species has managed to reach so many islands in the Aegean.
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| Potential dispersal paths of two Cretan snakes. 1) Mainland origin, 2) Passage into island, 3) Entering the sea. |
However, typical swimming is not the only explanation to oceanic dispersal. What is known as 'rafting' often results in colonization of islands - after events of floods, hurricanes and similar natural disasters, animals may become stranded on rafts of floating objects. One such case has been observed in the Caribbean, where after the hurricanes Luis and Marilyn in 1995, a floating raft of uprooted trees was seen carrying 15 or so green iguanas, eventually landing on Anguilla island, where they did not previously exist. Apparently, the iguanas had been stranded on the trees and travelled 320 km across the ocean from the island of Guadeloupe. This resulted in a colony that started breeding 2 years after the event (Censky et al. 1998). This shows that oceanic rafting can be a method of succesful colonization in reptiles, and many insular populations could be the result of such events, though the probability of a viable number of individuals reaching an island on floating vegetation and surviving upon arrival is arguably low.
Ancient hitchhikers
Ok, now that we've talked about natural dispersal, we need to elaborate on another really big factor. Humans have been crossing the sea since prehistoric times, with simple rafts and wooded boats being used as early as the time of Homo erectus. In ancient Greece, maritime trade was very important since the Minoan and Mycenean civilizations of the Bronze Age. Soon, the Greeks started dominating the field of shipping transport and expanded it to the coasts of Egypt, Phoenicea, Asia Minor and the Black Sea. This played an important role in shaping the distribution of reptile taxa throughout the eastern Mediterranean, with many species travelling as hitchhikers on ships and inside cargo. A study by Kornilios et al. (2010) examined the phylogeography of Ocellated skinks (Chalcides ocellatus), revealing that the Greek populations originated from Northern Africa, specifically Libya. It is suggested that ocellated skinks were transported in plant material or soil, likely silphium, which was in great demand and was exported in large numbers from the region of Cyrenaica. If this was the case, the human-mediated dispersal of ocellated skinks is estimated to have occurred around 2000-2500 years ago. This species has a rather patchy distribution in Greece, occuring in the southeast part of the mainland and on a number of islands such as Crete, the Cyclades and the Dodecanese.
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| Ocellated skink, Chalcides ocellatus. © Plato Stefanopoulos |
The ocellated skink is just one of several examples of species that have dominated insular Greece through human transportation. Other such species are geckos, starred agamas, tortoises and some snakes. But, this is a whole new topic that will be discussed extensively in a different article!
Closing remarks
[1] Kyriazi, P., Kornilios, P., Nagy, Z.T., Poulakakis, N., Kumlutaş, Y., Ilgaz, Ç., Avcı, A., Göçmen, B., & Lymberakis, P. 2013. Comparative phylogeography reveals distinct colonization patterns of Cretan snakes. Journal of Biogeography, 40.
[3] Censky, E. J., Hodge, K., Dudley, J. 1998. Over-water dispersal of lizards due to hurricanes. Nature, 395