Deciphering the past to ensure viper’s future on the Cyclades

Viper Figure1

Adult female long-nosed viper (Vipera ammodytes) in a coastal dune habitat. Photo by Stephen Roussos

Over the last five years, an international collaboration of scientists has investigated the evolutionary history of insularly isolated populations of long-nosed vipers (Vipera ammodytes) in the Cycladic archipelago. Morphometric and DNA analyses have revealed that Cycladic populations are evolutionary distinct from their mainland conspecifics exhibiting dwarfism and other morphological differences and significant genetic diversity. Variation is even evident from island to island, resulting in large amounts of variation between these isolated populations. During recent expeditions, two new island populations of vipers were discovered, extending the known geographic distribution of the species in the Cyclades from 13 to 15 islands.

Paleogeography of the Cyclades

The Cycladic Islands are the exposed mountain tops of the currently submerged Cycladic Plateau (CP). During the Pleistocene glaciations, the CP was more or less fully exposed and connected to what is now mainland Greece. Conversely, the CP was submerged during interglacial periods to different extents, depending on the intensity of the warming event. This cycle happened multiple times, characterizing the Cyclades as a complex land-bridge island landscape in the southern Aegean that has been repeatedly connected and disconnected due to eustatic sea-levels. About 200 thousand years ago (KYA) was when the CP most recently separated from mainland Europe at the beginning of the last interglacial period, existing as one large island (~ 6,500 km²) sometimes referred to as Cycladia. Subsequent to the end of the last glacial maximum (about 20-18 KYA), Cycladia began to fragment as the Aegean rose, submersing the lower elevations of the large island. The initial rise in sea-level was rapid (about 110 m in the first 13 KY), until about 5 KYA when the rising slowed down to about one metre every thousand years. This process has created the present day geography of the Cycladic archipelago.

Why the long-nosed viper?

Reptiles are excellent model organisms to study the effects of insular isolation because they adapt quickly to environmental changes and have fairly short generation times. In the Aegean, movement from island to island by either migration or human-mediated transport is nearly absent among most herpetofauna, and for that reason these species are terrestrially bound in the Cyclades with the sea acting as a significant barrier to gene flow.

Variation is even evident from island to island, resulting in large amounts of variation between these isolated populations

From a conservation perspective, herpetofauna are often indicator species of habitat and ecosystem health because they play important roles in food webs. The long-nosed viper is the only venomous snake species on the Cycladic islands it inhabits, and is a top microfaunal predator in the Cyclades playing crucial roles in the local food webs. These features among others make the Cycladic long-nosed viper populations good candidates for asking general evolutionary and ecological questions.

Dwarf Cycladic Populations

Insular dwarfism and gigantism among snakes has been observed around the globe. Much of this phenomenon has been found to be a result of shifts in available prey resources (plasticity), but it can also be attributed in part to other dynamics of fragmentation and isolation. On mainland Greece, adult long-nosed vipers primarily feed on small rodents, toads, birds and lizards, while neonates and juveniles feed on centipedes, lizards and the occasional newborn rodent or chick. In the Cyclades, vipers have adapted their feeding to available prey sources, as there is a low abundance of small rodents and a high abundance of small wall lizards and geckos.

Viper Figure2

Map showing the connectivity of the Cyclades following the
initial separation of Cycladia about 200 KYA. Different shades of
blue shows the depth of the sea in this part of the Aegean,
and correlates with the rise in sea-level at important times in the
paleogeography of the Cyclades. The western Cyclades separated
at much earlier periods of geological history, some assumed to be
isolated since about 5 million years ago (ie Milos). The present
geography of the Cyclades and Greece is coloured in green
or yellow. The current known distribution of the long-nosed viper
(Vipera ammodytes) in the Cyclades is shown in green. One can
clearly see that V. ammodytes is only found on islands that once
made up the ancient island Cycladia

We are currently testing hypotheses about why these insular vipers have evolved smaller sizes and whether it represents an adaptation to increase fitness in impoverished and semi-arid ecosystems. On some of the smaller and more impoverished islands these ‘body plans’ reach extreme dwarfism (reaching 50-60% of the snout-vent lengths found in mainland individuals). On some of the larger Cyclades, long-nosed vipers may still be considered ‘dwarfs’, but they can sometimes attain sizes close to their mainland conspecifics. The 15 known islands that harbour this species offer a complex set of study sites that act as a natural laboratory with separate experiments involving different variables.

DNA Analysis

Preliminary analyses of mitochondrial DNA sequences have allowed us to construct phylogenetic trees that should help us understand the evolutionary relationships between Cycladic V. ammodytes and mainland individuals. These phylogenetic trees show that the Cycladic populations are monophyletic but also genetically diverse, suggesting a recent radiation of genetically variable animals across the archipelago. This radiation seems to be fairly synchronized with the patterns of fragmentation that geologists have described for the Cyclades as evidenced by divergence events. Understanding the evolutionary and ecological mechanisms behind these patterns is challenging but can broaden our understanding of insular evolution patterns. At the same time, these findings help us to prioritize conservation efforts of these diverse and culturally important islands of Greece.

Conservation Implications

The natural history of long-nosed vipers in the Cyclades remains largely mysterious. There are at least four islands in the Cyclades that are not inhabited by vipers but are large enough to accommodate them and were recently connected (< 5 KY) to islands that currently have vipers. This implies possible extinctions of viper populations unless these islands house particularly cryptic animals, which we find to be unlikely because of numerous expeditions by biologists. If these islands represent recent extinctions, it would be interesting to know if they were caused by natural forces or by anthropogenic activities, since several civilizations have colonized the Cyclades at different times over thousands of years. In the last 50 years, tourism in the Cyclades has grown exponentially. This has bolstered local economies to the point where many depend almost entirely on tourism. Unfortunately this increase in tourism has also led to an increase in optimal viper habitat alteration or destruction. Educating the island communities about the local biota and sustainable development, along with management of the natural ecosystems, will be essential to maintain the beauty of these landscapes and to ensure they include the long-nosed viper for years to come.

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