European Water Snakes and the competitive exclusion principle…

Author: Paul Storm, Biology lecturer, University Rotterdam
Publication: Litteratura Serpentium 2018, Volume 38, No. 2, pp. 59-87.


Years ago, when I worked as a guest worker at Naturalis, an Italian scientist gave me a beautiful prospect. Northwest-Italy, that was the region where I had to go, all the water snakes of Europe could be found there (Fig. 1, 2 and 3).

That sounded like the promised land: an area where viperine snakes (Natrix maura) and dice snakes (Natrix tessellata) coexist with grass snakes (back then this still was one species Natrix natrix). To be honest, coexist is a misleading phrase in this case. It is true that viperine snakes and dice snakes are found together in the same area, even in the same river, the Trebbia (Scali, 2011), but this intersection is a fraction of the gigantic distribution area of both species. If you go a little bit more to the west, you will only find viperine snakes (Fig. 2), a little bit more east and you will only find dice snakes (Fig. 3). This makes the promised land fairly small. The term ‘exclusion’ is more fitting according to the occurrence of these two snake species. Taking into account the distribution of both species, the competitive exclusion principle came to me automatically.

Fig. 1. Distribution area of grass snakes. Not so long ago only 1 species but recent studies show we are dealing with three species: Iberian grass snake (Natrix astreptophora); Barred grass snake (Natrix helvetica); Grass snake (Natrix natrix). (Source picture: Wikipedia).

Fig. 1

Roughly, this principle (Hardin, 1960) states that within a geographic area two species, which occupy exactly the same geographical niche, cannot coexist: ‘complete competitors cannot coexist’.

Competition between the two species will lead to only one of the two surviving and it happens to be the one who is (a little) better at occupying the mentioned ecological niche. In this article ecological niche, or short niche, refers to the role of an organism within a community, in particular concerning its food intake. Not to be confused with the term ‘habitat’, because this refers to the environment in which a species exists.

Fig. 2. Distribution area of the Viperine snake (Natrix maura). (Source: Wikipedia).

Fig. 2.

With only a handful of species that coexist together or mutually exclude each other, it seems that the occurrence of the genus Natrix within Europe is a classic example of the competitive exclusion principle (Storm, 2009, 2011). This group of water snakes (family Natricidae) can be divided in on the one hand grass snakes (until recently just one species Natrix natrix), which often feed on amphibians and on the other hand two snake species, the viperine snake, (Natrix maura) and the dice snake (Natrix tessellata), which mainly eat fish. Put simplistically: amphibian eaters and fish eaters can coexist, but the fish eaters exclude each other. Metzger et al., (2009) presented in their article the uniting of the viperine snake and the dice snake, with the introduction of the latter species at the lake of Geneva in Switzerland, as a test of the competitive exclusion principle.

Fig. 3. Distribution area of the Dice snake (Natrix tessellata). (Source: Wikipedia).

Fig. 3.


Yet the use of this principle could be called into question. Is it really that clear in practice? In this article, I would like to comment further on the existence of the genus Natrix in Europe and how competitive exclusion works in this group.

In the first place, by looking at arguments that seem to support this principle: the sympatric occurence of amphibian-eaters and fish-eaters, and the mutual exclusion of fish-eaters. Secondly, I will pay attention to the question marks about the effect of this principle; the differences in appearance and differences in niche between the fish-eaters, and the flexibility of their eating habits.

Nomenclature grass snakes in motion

Until recently there was only one species of grass snake (Natrix natrix) with a few subspecies. With that much variety within one species and a noticeably large distribution area, it isn’t surprising that not only was there a disagreement about the number of subspecies (Guicking et al., 2006) but also about the species status. In the early nineties of the last century, there was a claim for the existence of an independent species: Natrix megalocephala (Orlov & Tuniyev, 1992), which later was put into question again (Kindler et al., 2013). Now we are being treated; this time with two new species. As it happens, recent studies show that besides Natrix natrix, now also Natrix astreptophora (Pokrant et al., 2016) and Natrix helvetica (Kindler et al., 2017) have to be added to the species list. 

Fig. 4. Rio Nansa, Cantabria, Spain, where the Iberian grass snake (Natrix astreptophora) and the Viperine snake (Natrix maura) were found. (Picture Paul Storm, 2004).

Fig. 4. Rio Nansa, Cantabria, Spain, where the Iberian grass snake (Natrix astreptophora) and the Viperine snake (Natrix maura) were found. (Picture Paul Storm, 2004).

The border between species and subspecies is not always clear and with the development of new techniques, time will tell if more taxonomic shifting will take place. In short, with the emergence of genetical analysis, the taxonomy of the genus Natrix, such as many other taxa, is set into motion. It makes me think of a quote that was made more than 150 years ago. Darwin remarked in his world-renowned work (1859, page 64): ’The term species thus comes to be a mere useless abstraction, implying and assuming a separate act of creation.’ Evolution happens always and everywhere. The living world around us isn’t fixated, but moves constantly, whereby life forms move over into others, diverge into all kinds of other forms or die out. Our life is too short to see this constant movement. We see a still image as it were. As a result, we get the impression that life-forms around us exist out of a definite unit, but this isn’t the case (Storm, 2009). Having said that, concerning the nomenclature for grass snakes in this article I will follow the presentation from Kindler et al. (2017). For Europe, this means five watersnake species within the genus Natrix.

The supposed amphibian-eaters, in short grass snakes
– Iberian grass snake (Natrix astreptophora)
– Barred grass snake (Natrix helvetica)
– Common grass snake (Natrix natrix)

The supposed fish eaters
– Viperine snake (Natrix maura)
– Dice snake (Natrix tessellata)

The sympatric appearance of grass snakes and viperine snakes

The Iberian grass snake (‘Ibero-Maghrebian grass snake’, Natrix astreptophora) can be found, as the English name implies, on the Iberian peninsula and in the northern regions of Africa (Fig. 1). In Europe, this species is also found in the region of the French Pyrenees (Pokrant et al., 2016), besides Spain and Portugal. The viperine snake (Natrix maura) can also be found in the northern regions of Africa and the south-west of Europe, in Spain and Portugal but also further north, such as the south half of France, the south-west of Switzerland and the north-west of Italy (Fig. 2).

Fig. 5. Iberian grass snake (Natrix astreptophora), Cantabria, Spain. (Picture Paul Storm, 2004).

Fig. 5.

The Iberian grass snake and the viperine snake coexist in the north of Spain at rivers with a lot of cobblestones; I found them there in the summer of 2004, at the Rio Saja, as well as the Rio Nansa (Table 1; Fig. 4, 5 & 6).

Very exciting was the moment I found a juvenile black snake with a total length of twenty cm (Fig. 7) underneath a stone alongside the Rio Nansa. At that moment I wasn’t sure which species it was. By looking more carefully at the scales on the head it became clear it was an Iberian grass snake.

One day later, I saw a big snake move underwater in the Rio Saja. But once emerged, it turned out it was no longer in the land of the living. This also was a melanistic specimen of the Iberian grass snake, this time a bigger specimen of 80 cm long.

The other two, not melanistic Iberian grass snakes, I found underneath rocks alongside the Rio Saja.

I found viperine snakes 4 times underneath a rock on dry land and twice in the water.

Fig. 6. Viperine snake (Natrix maura), Cantabria, Spain. (Picture Paul Storm, 2004).

Fig. 6.

Regarding potential prey items, both in the Rio Saja as well as the Rio Nansa a lot of Eurasian minnows were mainly observed and frequently larvae of Anura (frogs and toads) were found. Underneath moist rocks every now and then a worm was found and in more slow %owing and still parts of the river also leeches.

Hailey and Davies (1986) studied the occurrence of grass snakes and viperine snakes at a small river in Spain (the Jalon). They considered grass snakes as day-active terrestrial predators of frogs; viperine snakes on the other hand as day and night operating semiaquatic sit-and-wait predators of fish. That is a clear difference in timing, hunting strategy, how they forage and prey preference. From this point of view, it isn’t surprising both species coexist together.

The distribution area of the newest grass snake species, the barred grass snake (Natrix helvetica) encompasses the distribution area of five earlier antecedent subspecies of Natrix natrix: cetti, corsa, helvetica, lanzai and sicula (Kindler et al., 2017). According to the new proposal this means that the barred grass snake has a distribution area that exists out of England, the Netherlands, Belgium, Germany, France, Switzerland, Italy and the islands Corsica and Sardinia. Barred grass snakes and viperine snakes don’t only overlap on the global distribution map (Fig. 1 en 2); experience shows that they’re also actually found in the same habitat.

I found the barred grass snake together with viperine snakes in France, alongside rivers with a lot of cobblestones, such as at the Ceze and the Gardon d’Anduze (Tabel 1; Fig. 8, 9 & 10). Both snake species were also found in the Limousin close to the Petite Creuse, in an area with a lot of cobblestones, but not in the same year. Besides, I found the barred grass snake here a little further from the water. This raises the question, if the coexistence of these two water snake species possibly isn’t only a matter of niche but also (micro)habitat. The latest would mean that on a smaller scale it certainly could be a matter of a partial segregation of the barred grass snake and viperine snakes in certain areas. In 2002 I asked Rob Veen what his idea was about the possibility of the coexisting of these two species in his focus area. He gave the next answer: ‘… the Creuse Natrix helvetica is much more numerous and lives in the whole area. Natrix maura only lives in stream valleys below six hundred meters. As habitat choice I found Natrix maura exclusively at streams and rivers with sandy and or gravelly shores, as a preference between three hundred and five hundred meters. Natrix helvetica is more bound to lakes, damp meadows with ditches, alongside hedges, village ponds and also anywhere where green frogs exist.’ In this perspective it is also interesting to note that Rob Veen later stated that on September 23rd of 2014, at an estimated 40 meter high rockformation approximately sixty meters from the river the Cher, in a ± twenty cm deep hole in the rocks on moist sand, he found twelve juvenile viperine snakes and two barred grass snakes together with fifteen empty eggs. In the summer of 2017, he showed me this spot and you could still see the empty eggs (Fig. 11 & 12). This shows that these two snake species also can (partially) be found in the same habitat in the Creuse.

The sympatric appearance of grass snakes and dice snakes

The dice snake (Natrix tessellata) has an impressively large distribution area, that consist of parts of Europe, Asia and Africa (Mebert, 2011) Fig. 3). From the west to the east this area goes from Northwest-Italy up to and including the utmost west of China. In the west part of its distribution area, this species occurs in the south in Egypt and the middle east; in the north in the Czech Republic and Germany.

Fig. 7. Iberian grass snake (Natrix astreptophora) (melanistic) Cantabria, Spain. (Picture Paul Storm, 2004).

Fig. 7.

For dice snakes, it also applies that on the map they clearly overlap with grass snakes (Fig. 1 en 3). Dice snakes exist in a diverse environment. So they are found in fresh-, brackishand saltwater (Mebert, 2011). In Italy, I found them in big lakes and in fast flowing rivers (Storm, 2016). Since dice snakes don’t seem to be picky when it comes to their habitat as long as there’s water nearby, there’s a good chance they can be found in the same habitat as the grass snake.

As such, I found two dice snakes and a death barred grass snake in the river the Torrente Arbia, in the summer of 2006 (Storm, 2016; Table 1), where a large number of stones were present and the river was shallow. One afternoon I found an impressive dice snake female there, with a total length of no less than 106 cm. Up until now the longest dice snake I’ve ever found. The air temperature in the shadow was 33°C and the temperature of the water was 30°C.

Fig. 8. Gardon d’Anduze, Gard, France, where the Barred grass snake (Natrix helvetica) and the Viperine snake (Natrix maura) were found. (Picture Paul Storm, 2011).

Fig. 8.

Days later I found a juvenile dice snake with a total length of 29 cm in the same river at a shallow part of only 7 cm. On that same day, I found a beautiful but unfortunately death and partially eaten barred grass snake. A question I immediately asked with this find was: does the barred grass snake really live in this part of the Torrente Arbia? Theoretically speaking the snake could’ve ended up there by a predator moving its prey.

The next observation of a barred grass snake in the habitat of dice snakes, seen in the summer of 2010, also carries some uncertainty. Early in the afternoon, I visited the small town Passignano at the north-side of the lake of Trasimeno. The weather was favourable for observing water snakes, that means, it was sunny and there was no strong wind, so the water was calm. In contrast to four years earlier (Storm, 2016), I didn’t see any dice snakes in the water. The water was less clear than in 2006. This time no large groups of fish; but there were smaller fish. The water level seemed lower as well. In the afternoon I drove to the east-side of the lake, to San Feliciano. At a certain moment, I saw a dice snake here and most likely also a barred grass snake. This is based on the fact that dice snakes will quickly dive under when disturbed, while my impression of grass snakes is that they’ll stay at the surface relatively long more often.

Fig. 9. Barred grass snake (Natrix helvetica), Gard, France. (Picture Paul Storm, 2011).

Fig. 9.

Apart from the above mentioned, unsure anecdotical vacation observations, research shows that dice snakes and grass snakes do sympatrically appear, such as at the lakes of Baćina in South-Croatia, where they live in the same habitat, but differ in preference regarding microhabitat and prey (Janev Hutinec & Mebert, 2011). Last named authors found out that dice snakes exclusively fed on fish, while the diet of grass snakes mostly exists of amphibians and, every now and then, fish. Filippi et al. (1996) already published in an earlier study, concerning the sympatric appearance of both species in Central-Italy, that the diet of dice snakes exists for more than 97% out of fish, while with grass snakes males and females this was respectively 17% and 9%. In South-Croatia dice snakes had a preference for slow running water and consumed more benthic fish, while grass snakes were more frequently found in still water such as puddles (Janev Hutinec & Mebert, 2011). These researchers also reported that dice snakes occurred more often in a rocky environment and that the two species differ in the use of the water column; dice snakes where often found foraging in the benthic zone and in the middle water layer, while grass snakes were almost always seen at the water’s surface.

Interesting is that also Ioannidis & Mebert (2011) established that in the south of Greece dice snakes and grass snakes admittedly use most of the available habitats near water, but that there is a difference between both when you zoom in on the different types of areas abounding in water. Such as, grass snakes, in opposition to dice snakes, will mostly use tempory puddles, wet grasslands, swamps and small artificial ditches. On the other hand, dice snakes were more often found at brackish- and saltwater lagunes. It’s very likely that these habitat preferences have a connection with the favorite prey items of both groups. The differences in habitat preferences of grass snakes and dice snakes (Janev Hutinec & Mebert, 2011; Ioannidis & Mebert, 2011) partially also brings to mind the previously mentioned comment of Rob Veen about the habitat choice of barred grass snakes and viperine snakes at the Creuse. This could mean that, ecologically seen, the dice snakes and viperine snakes are closer together and accordingly there’s a bigger chance at competition between these two species.

Viperine snakes and dice snakes and the competitive exclusion principle

The image that presents itself by looking at the distribution of Viperine snakes, Dice snakes and Grass snakes (Fig. 1, 2 en 3) matches with the global image that we have of the niches of these animals. Grass snakes overlap with viperine snakes and dice snakes, but the latter two species don’s overlap with each other. Grass snakes are mostly amphibian eaters (Creemers & Van Delft, 2009; Janev Hutinec & Mebert, 2011). The European watersnakes that are especially interested in fish are the viperine snakes (Patterson & Davies, 1982) and dice snakes (Filippi et al., 1996; Janev Hutinec & Mebert, 2011; Sterijovski et al., 2011). According to Capula et al. (2011), viperine snakes and dice snakes look a lot alike regarding sexual dimorphism (difference in size between females and males), hunting strategy (sit- and waitpredator) and composition of diet (mostly fish eating). So both species occupy a similar ecological niche (Guicking et al., 2006) and looking from the perspective of the competitive exclusion principle (Hardin, 1960), cannot coexist well together. Possibly the dice snake prevents a more eastwards distribution for the viperine snake and on its turn the viperine snake prevents the more westwards distribution of the dice snake (Fig. 2 en 3).

Fig. 10. Viperine snake (Natrix maura), Gard, France. (Picture Paul Storm, 2011).

Fig. 10. Viperine snake (Natrix maura), Gard, France. (Picture Paul Storm, 2011).

Since the fall of 2015, I take care of a female Lataste’s Viper (Vipera latastei gaditana). Viperine snakes and dice snakes are much more active in their terrarium than this sit-and-wait, predator. What do I want to say with this? You can ask yourself if both above-mentioned water snake species could be seen as typical sitand-wait-predators. When it comes to hunting both the viperine snakes and dice snakes are capable of more than just a passive sit and wait strategy.

You don’t only see indications for this inside the terrarium, but also in the field (Storm, 2016). According to Metzger et al. (2011) viperine snakes, as well as dice snakes, show five obvious hunting strategies, that can be separated in passive and active ways of hunting:
1. passive, outside of the water, with the head above the water
2. passive, outside of the water, with the head underwater;
3. passive, in the water, anchoring itself with the tail;
4. active swimming in open water;
5. actively swimming over the bottom, searching between rocks.

It is striking that two different European fisheating water snake species not only show a strong overlap regarding their diet omposition
(Metzger et al. (2009), but also regarding their hunting strategy (Metzger et al., 2011). In this relation, the research of Schaeffel and Mathis (1991) is extremely interesting. Because their research shows that grass snakes don’t accommodate their lens underwater, while viperine snakes and dice snakes can adequately focus in the air as well as water. This is a clue that, in contrast to grass snakes, viperine snakes and dice snakes in the course of evolution are adjusted to hunting underwater. Looking from this perspective, grass snakes are badly equipped for hunting on fish. The above clearly shows that viperine snakes and dice snakes occupy a similar ecological niche.

Fig. 11. Rock-formation, not far from the river the Cher, Creuse, France, where empty eggs were found together with juvenile viperine snakes (Natrix maura) and juvenile barred grass snakes (Natrix helvetica) in a hole between the rocks (information Rob Veen). (Picture Paul Storm, 2017).

Fig. 11. Rock-formation, not far from the river the Cher, Creuse, France, where empty eggs were found together with juvenile viperine snakes (Natrix maura) and juvenile barred grass snakes (Natrix helvetica) in a hole between the rocks (information Rob Veen). (Picture Paul Storm, 2017).

The idea that viperine snakes and dice snakes cannot coexist on grounds of the niche overlap is supported by a research done at the lake of Geneva, Switzerland (Metzger et al., 2009). What is written in this paragraph, is based on the above-mentioned research. Originally the viperine snakes existed in the lake of Geneva. In the early twenties of the last century the dice snake was introduced into this lake (see also Mazza et al., 2011), followed by several introductions in the fifties and sixties, which led to a large population of hundreds of individuals at the north side of the lake (Metzger et al., 2011). From the moment these two species were being monitored in the nineties, a drastic decrease in the population of viperine snakes was observed. The study showed that prey composition and prey size were very similar in both species. The researchers found a large overlap regarding the niches of both snake species. This could explain the drastic decrease of the viperine snake after the introduction of the dice snake. The dice snake could be considered an invasive species in the lake of Geneva, who is replacing its ecological “image”.

Question marks

Taking into account the above, it seems that the appearance of viperine snakes and dice snakes is an outstanding example of the competitive exclusion principle. Both in Europe existing snake species for a large part occupy the same ecological niche, it seems they can both be described as not too big semi-aquatic predators who are in particular after fish. No wonder they’re usually not found together and that where they have been brought together, the lake of Geneva, problems occur. But if you zoom in closer on both species, shadows do loom up.

Differences in appearance and niche differences between viperine snakes and dice snakes

Let me start with the differences in appearance. Looking superficially, viperine snakes and dice snakes, of course, look alike: not too big snakes, often with a greyish, brownish, army green basic color and some contrast. But on average dice snakes are longer and slimmer than viperine snakes. As such, female dice snakes can easily reach a total length of more than ninety cm (Bol, 1998; for ’snout-vent length’ see Ajtić et al., 2013), while a lot of female viperine snakes will not get much longer than approximately 65 cm (Storm, 2011). The dice snake has a somewhat longer head proportionally, than the viperine snake. It wouldn’t surprise me if the above-mentioned differences between these two snake species imply differences in prey. Besides, the viperine snake usually, has a very outstanding pattern for a non-viper, the zigzag pattern on the back, from which he mostly got his name.

Fig. 12. The hole between the rocks (Fig. 11) where (still visible) empty eggs were found together with juvenile viperine snakes (Natrix maura) and juvenile barred grass snakes (Natrix helvetica) (information Rob Veen). (Picture Paul Storm, 2017).

Fig. 12. The hole between the rocks (Fig. 11) where (still visible) empty eggs were found together with juvenile viperine snakes (Natrix maura) and juvenile barred grass snakes (Natrix helvetica) (information Rob Veen). (Picture Paul Storm, 2017).

The idea is that fish-eating water snakes show a tendency to have a slim streamlined head, while species that feed on frogs have a wider head (Brecko et al., 2011). The logic behind this thinking goes as followed. Generally speaking, snakes have an advantage with a wider head if it’s solely about eating voluminous prey such as frogs and toads. However, a wider head can also be in the way, which is the case with snakes that need to catch fish underwater. With a wider head, you won’t move so fast in water. To move fast in water, you need a slim streamlined head. This difference can be beautifully seen when we compare dice snakes and grass snakes with each other. The dice snake (Fig. 13) has a somewhat slimmer head than the grass snake (Fig. 14). Interesting is that the viperine snake, as a fish-eater, doesn’t seem to possess the long slim head of the dice snake. The appearance of the dice snake strongly reminds of the American, also fish hunting species, Thamnophis rufipunctatus (Rossman et al., 1996; Salo, 2017). The snout of the viperine snake looks a bit puffier.

Fig. 13. Dice snake (Natrix tessellata), Lake Garda, Italy. This snake clearly has eaten not long before. (Picture Paul Storm, 2016).

Fig. 13. Dice snake (Natrix tessellata), Lake Garda, Italy. This snake clearly has eaten not long before. (Picture Paul Storm, 2016).

In terms of appearance, this means, regarding length, posture, pattern, and shape of the head, the viperine snakes and dice snakes don’t look so much alike as you would assume at first sight; this could partially mean that there is a niche difference between these two species. This niche difference does seem to be there. As a keeper of both snake species, I realize this all too well. In the terrarium, the viperine snakes also accept other kinds of food more easily, besides fish, than the dice snake. Such as, it is very convenient that young viperine snakes eat worms, which dice snakes, as far as I know, don’t do. From the perspective of easier feedings, I rather breed viperine snakes than dice snakes. This difference also becomes apparent from studies. Dice snakes often eat fish for the most part (Filippi et al., 1996; Capula et al., 2011; Janev Hutinec & Mebert, 2011; Sterijovski et al., 2011; Ajti􀃤 et al., 2013), while viperine snakes, besides eating fish, also feed on worms, leeches, amphibians and their larvae (Hailey, 1981; Santos Llorente, 1998; Rugiero et al., 2000; Scali, 2011). So it seems, looking globally, that the smaller viperine snake feeds itself with a wider spectrum of different groups of animals than the more strongly specialized dice snake.

Different species of garter snakes in a dunearea in San Fransisco

Despite morphological and niche differences the viperine snakes and dice snakes exclude each other (Fig. 2 en 3). Apparently, the competition between these two snake species despite these differences is so big, that it is impossible they coexist together. Except for of course that very small part in Italy. The more surprised I was to find out that on the other side of the Atlantic Ocean, near San Fransisco, there’s a dune area with no less than three different garter snakes species coexisting together. In addition, as the genus Natrix, they also belong to the family of water snakes (Natricidae). It’s about the following species: Thamnophis atratus, Thamnophis elegans and Thamnophis sirtalis. ’Seeing is believing’. In the spring of 2014 we had the chance to visit this area and on a misty, damp spring day with barely any sun, we found all three above mentioned species, not far away from each other! Now you could think, as with the case of the viperine snakes and dice snakes that the overlap of these three garter snake species is negligibly small, but on the map, they overlap in a large part of the west of the united states (Rossman et al., 1996). The impression is that Thamnophis atratus is mostly after fish and amphibians; just like the food spectrum of Thamnophis elegans, the diet of Thamnophis sirtalis is wide, but in Calafornia this last mentioned species seems to be eating mostly amphibians (Rossman et al., 1996).

Possibly, Thamnophis atratus, Thamnophis elegans and Thamnophis sirtalis live next to each other in the same habitat, because they occupy partially different niches, but it is good to realize that within a species there could be ontogenetic and geographical differences. Such as, at a North-California population of Thamnophis elegans the diet of juveniles existed out of leeches, while the adult snakes ate voles (Rossman et al., 1996). Furthermore, based on research data it seemed that populations that live near the coast have a stronger genetic predisposition for eating banana slugs than populations in the mainland. The %exibility of a species in space and time regarding the diet could have as a result that it is hard to tie one species to an exact described ecological niche.

The flexibility of eating habits of European water snakes

This flexibility doesn’t only concern the North-American Natricidae, but also the European Natricidae. Generally, the dice snake is seen as a typical fish eater and different studies confirm this image, but the reality is more complex. As so, at Chinese fishponds the diet of these snakes indeed existed almost completely out of fish, while dice snakes in rice fields hunted on small toads and tadpoles but not on fish and in other area’s they even ate insects and rodents (Liu et al., 2011). Also Göçmen et al. (2011) made a notion about dice snakes eating insects and rodents, in this case in Turkey; they gave the following percentages: fish (72,4%); amphibians (14,5%); insects (7,9%) slugs (2,6%); reptiles (1,3%) and mammals (1,3%). Remarkable in this context is the article of Brecko et al., (2011), that talks about museum specimens, the dice snakes with fish in their stomachs had a narrower and more streamlined head than individuals with frogs in their stomach. The above suggests caution regarding a too narrow view in relation to the ecological niche of dice snakes.

Fig. 14. Grass snake (Natrix natrix persa), Lesbos, Greece (Picture Paul Storm, 2009).

Fig. 14. Grass snake (Natrix natrix persa), Lesbos, Greece (Picture Paul Storm, 2009).

The idea that amphibian-eating grass snakes and fish eaters, such as viperine snakes, coexist together without any problems, probably
isn’t always right. Research from Rugiero et al. (2000) on two populations of viperine snakes on Sardinia showed that with one of the populations amphibians were an important part of the diet (86,6%). Theoretically speaking, the viperine snake therewith comes into the food territory of the local grass snake. Scali (2011) does note that in Sardinia there’s a strong competition between viperine snakes and grass snakes (Natrix natrix cetti). Both snake species mostly feed on amphibians and there is a great overlap in their diet (Scali, 2011).

Fig. 15. Viperine snake (Natrix maura), underwater in a small lake in the Provence, France, probably hunting. (Picture Paul Storm, 2015).

Fig. 15. Viperine snake (Natrix maura), underwater in a small lake in the Provence, France, probably hunting. (Picture Paul Storm, 2015).

Not only dice snakes and viperine snakes can change their diet, grass snakes also seem %exible. The opportunistic character of these
snakes shows through in a research, done in southeast England; grass snakes also eat mammals (25%), fish (10%) and birds (1%) besides amphibians (63%) (Gregory & Isaac, 2004). With a shortage of amphibians, the relative proportion of other prey can be higher (Creemers & Van Delft, 2009).

Flexibility doesn’t only show in the fact that water snakes hunt on different groups of animals, but also the convenience with which they switch over to eating non-native species. In thespring of 2015, in the Provence, France, I observed a young viperine snake, swimming near eastern mosquitofish (Gambusia holbrooki) and pumpkinseeds (Lepomis gibbosus), probably hunting (Fig. 15). As it happens most of the time viperine snakes go into the water to forage. A characteristic you can thankfully use with the care inside the terrarium; if viperine snakes go into the water, there’s a good chance they’re hungry. At another occasion in South-France, I once found a viperine snake with a pumpkinseed in its mouth. From my terrarium experiences, I know that viperine snakes will accept live mosquitofish and pumpkinseeds as food. Research shows that grass snakes and dice snakes are capable of adapting quickly and will also feed on non-native species (Šukalo et al., 2014). As such, the above-mentioned researchers declare that after the drainage of most of the waters in Barda􀃪a, grass snakes started to feed on non-native fish (exclusively) instead of Anura (frogs and toads). In a word, for water snakes probably also counts: specialism doesn’t mean the exclusion of opportunism (Storm, 2009).

Concluding remarks

On one hand, we are dealing with impressive data, such as the global distribution area, diet composition, hunting strategy, anatomical adjustment and displacement with introduction, that support the idea that in Europe the genus Natrix forms a strong example of the competitive exclusion principle. On the other hand, there are also question marks regarding the operation of the principle, such as the differences in appearance and ecological niche differences between the viperine snakes and the dice snakes and the %exibility of eating habits which makes it hard to pin down species on one specific niche.

Have we reached a gap between theory and practice? It seems so. Hardin (1960, page 1293) writes: ‘The “truth” of the principle is and can be established only by theory, not being subject to proof or disproof by facts, as ordinarily understood.’ With the competitive exclusion principle, it’s about a logical theoretical train of thought, which seems contumacious in practice, because of a lot of variables that play a role in the appearance of a species in a certain area. Take for example the fact that grass snakes don’t focus their lens underwater. A clear indication that they’re less well adapted on hunting on fish than the viperine snakes and dice snakes, but this doesn’t take away that research shows that grass snakes do eat fish and therefore come into the niche of these two fish eating snakes. How successful grass snakes will be in this depends on different factors which will differ per area. As such I can imagine that grass snake could catch fish more easily in a situation where there are low water levels and large amounts of fish than in a situation
with deep water and lower fish counts.

So must we leave the idea of the competitive exclusion principle as a too theoretical, impossible to test error of thought? I don’t think so, on the contrary, because of this principle we can ask questions, formulate hypotheses, which in my mind leads to a better understanding of the existence of organisms in original and invasive situations. The occurrence of the European watersnakes forms a beautiful case because of the extreme widely spread occurrence of different species, morphological adaptations, the invasive role of the dice snake at the lake of Geneva and the often clear visibility of water snakes in the wild. The last mentioned could well possibly be the reason why relatively seen there’s already been so much published about this group of snakes; I for one already have numerous joyful hours to thank for.

Words of thanks

I want to thank Rob Veen for the information he’s given about the appearance of barred grass snakes and viperine snakes at the Creuse, France. Emma Versteegh, I am grateful for her remarks about the concept version of this article. Without the indications of Steven Bol we probably never would’ve been so successful in finding three different garter snake species in a dune area near San Fransisco. Last but not least I want to thank my wife Barbara van der Hout for her acceptance regarding the pursuit of my hobby and her notes to make the article more readable.

Table 1: sympatric appearance of European Natrix species (observations author).

Table 1: sympatric appearance of European Natrix species (observations author).

*= Natrix maura observed in 2002 en 2007, Natrix helvetica in 2014.
?= determination somewhat unsure, couldn’t observe snake quietly.
#= it was a dead snake that could have gotten there because of a predator.

Translation into English: Soleya Witte.

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