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Bird guts, not muddy feet, may help snails migrate overseas

This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American


When I'm not spending my time writing about the weird bugs I find in the garden, or even weirder creatures I just think the world ought to know about, I study land snails from Pacific Islands. That means every time I give I talk I spend the first couple of minutes convincing people that - along with colourful fish, tropic birds and beautiful Hibiscus - land snails are one of the characters tic creatures of Pacific ecosystems. Snails might seem like unlikely overseas travellers, but they've made it to the most isolated and the youngest islands. Anak Krakatau is so young that it's still smouldering, and it has a native land snail. Rapa Nui (Easter Island) is 2 000 km of open sea from its nearest neighbour, but still managed to develop its own land snail fauna before it was lost in that islands ecological collapse.

Land snails don't simply make it to islands, once they establish themselves they can set off explosions of diversity. In Hawai'i there were 40 species of O'ahu tree snails, in Rarotonga (the site of my fieldwork) there was an extensive radiation in the genus Sinployea (small snails related to the one I found in my garden the other day) and, most famously, the Society Islands of French Polynesia played host to a staggering collection of partulid snails. I used the past tense there because all those evolutionary radiations, each of which could have been a natural laboratory for us to study the origin of species, have been destroyed (or at least severely eroded) by introduced pests.

There are a few Pacific land snail radiations that have survived to the present day, and one of my favourite examples comes from the Ogasawara (Bonin) Islands to the South of Japan. About 2 million years ago the ancestors of the snail genus Mandarina made it to the Ogasawara islands and set off one of those explostions of diversity the Pacific land snail fauna is so full of. Over the last couple of decades Satoshi Chiba from Tohoku University has worked with scientists from around the world to unravel the history and the ecology of the Mandarina radiation. Together, they've found that sometimes evolution can be predictable.


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Each of the larger islands (and regions within the largest) in the group have their own mini-radiation, and in each of these smaller explosions species have independently evolved to fill similar ecological niches. Ecologically similar species even look the same, snails that specialise in living on trees have relatively flat shells that are lightly coloured, while those that are adapted to particular ground habitats are darker and have shells with higher spires:

Left: Mandarina ecotypes from different islands reproduced from Davison and Chiba (2006) doi: 10.1111/j.1095-8312.2006. 00624.

Chiba has even been able to look into how his snails came to be so diverse. One some islands, the different ecological niches are taken up not by different species, but, by different populations within in a single species. It's quite possible the ecological competition that Chiba has been able to measure between these ecologically specialised populations is a key driver to formation of distinct species.

I haven't yet provided an answer to the question that Pacific Island land snail fauna seems to scream at us. How did these proverbially sedentary and salt-intolerant animals manage to get to so many islands separated by such vast seas? The distribution of snails was a particular concern for Darwin. His theory did away with he prevailing idea of naturalists at the time, that species were created for their habitat (creationist nonsense about the distribution of animals fitting a post-flood diaspora is a pretty modern idea) but still needed to explain how islands could become inhabited. When Darwin wrote to his friend Joseph Hooker to "confess" his ideas about the non-fixed nature of species, Hooker turned to his notebooks on the snails of Madeira and Porto Santo in the hope of finding a counter argument. He failed to find one, and in time became one of Darwin's greatest allies, but the distribution of snails and other molluscs (grouped under the name "shells" in most of Darwin's writing) was still a big enough concern for Darwin that he stuck snails to ducks to see if they'd survive and tested their hardiness in salt water (an experiment the blogosphere's preeminent malacologist, Aydin Orstan, is repeating even as we speak).

Since Darwin's time we've found that birds probably do move snails between islands (stuck to bodies or feet) and it's likely the wind is a more common driver of dispersal. Most snails are small and quite capable of becoming part of the "aerial plankton" that is floating above, and raining down on, the land all the time. The Pacific also seems to have a high proportion of tree snails, that spend their time on shrubs with broad leaves that would make great wind sails in a cyclone. On top of those methods you can add human introductions, either accidental as in the case of the "tramp species" that are coming to dominant Pacific ecosystems, or those introduced deliberately for trade by Polynesians like the beautiful Partula shells from the Society Islands. Recently, we've learned about a much more surprising way that snails might move from island to island, and it's thanks again to Satoshi Chiba and his colleagues working in the Ogasawara islands.

This new mode of conveyance again resolves around a bird, and one that will be immediately familiar to readers from Australasia or Hawai'i.

Right: A white-eye. Image is CC 3.0 thanks to wikimedia user Benchill

White-eyes are a profoundly successful group of birds that have managed to get themselves to almost every piece of land between Japan and New Zealand (in fact, they are probably the most common bird in my garden down here in Dunedin, New Zealand, which is quite a feat since they only established themselves here in 1855). One of the keys to their success is that they are generalists, quite happy to eat insects, seeds of berries given the chance. They are so indiscriminate in their tastes that they move happily between native forests and disturbed pastures, and in New Zealand and Hawai'i in particular, they play a large role in moving the seeds of invasive plant species into places we'd rather they didn't grow. The Ogasarawa islands have populations of the Japanese White-Eye (Zosterops japonicus) and researchers on Hahajima island in particular started noticing these birds were seeking out a tiny snail, Tornatellides boeningi,  as something to eat.

Left: I couldn't find a good photo of T. boeningi, but this a species from the same genus from my field work in Rarotonga  

We've known for a long time that birds have moved invertebrates and even fish between lakes in their bills, is it possible these birds, already famous for their ability to move seeds around, could be vehicles for snail dispersal?

The researchers did the obvious thing, and started feeding live snails to caged White-Eyes and collecting them at the other end of a trip through the bird's digestive system. Amazingly, about 15% of the snails survived that journey!

Right: Excreted snails, from Wada Kawakami & Chiba (2011) doi: 10.1111/j.1365-2699.2011. 02559.x

It's not quite clear how they managed that trick. The small size and high-spired shape of the shell probably makes them strong enough to resist the pressures exerted by bird's gut, indeed, the researchers report larger snails are occasionally found in bird droppings but always with broken shells. Snails have a few other tricks that might help, many snails in tropical places avoid the hottest and driest parts of the day by entering a dormant state called aestivation (analogous to hibernation in animals that live in cold climates), and before they hunker down for the day they cover their shell opening with a layer or dried mucous called an epiphragm which might prevent digestive acids getting to the animal. The mucus itself might also being playing a role in the snails survival. As much as it looks life a gross slime to us, snail mucus is actually a pretty remarkable material. It's a non-Newtonian fluid that's principally used to help snails slide freely over the bumpy roads life throws at them, but it's also been repurposed into a set of bubbles that can keep snails afloat at sea, and it's used as part of a sexual subterfuge in snails of the rocky shore while a sea of mucus bubbles is a pretty common defense against predators for land snails. Perhaps the thick mixture of proteins and carbohydrates slows the progress of the bird's digestive juices and gives the snail a chance to survive.

However they do it, the revelation that T. boeningi gives us another way that small land snails might be moved between islands. To get a better idea of what impact this may have had, the researchers looked at the genetics of this species. They could show that there is very little genetic structure to populations when they're compared to species that don't survive digestion by white-eyes. (that is, populations one side of an island are are not genetically distant from populations on the other side). That may simply be a result of a large and dense population with plenty of gene flow between adjacent regions, but it could also be evidence that predation by white-eyes, and the occasional deposition of survivors into distant regions, is keeping these snails connected to each other. I'll certainly be playing closer consideration to birds next time I'm doing fieldwork!

Notes:

The paper revealing the remarkable hardiness of T. boeningi is: Wada S, Kawakami K, Chiba S. Snails can survive passage through a bird’s digestive system. Journal of Biogeography (Epub ahead of print) doi: 10.1111/j.1365- 2699.2011.02559.x

And here are some of the key papers on the Mandarina radiation:

Chiba, S. 1996 Ecological and morphological diversification within single species and character displacement in Mandarina, endemic land snails of the Bonin Islands. Journal of Evolutionary Biology 9, 277-291. (doi:10.1046/j.1420-9101.1996. 9030277.x)

Chiba, S. 2002 Ecological diversity and speciation in land snails of the genus Mandarina from the Bonin Islands. Population Ecology 44, 179-187. (doi:10.1007/s101440200021)

Davison, A. & Chiba, S. 2006 Labile ecotypes accompany rapid cladogenesis in an adaptive radiation of Mandarina (Bradybaenidae) land snails. Biological Journal of the Linnean Society 88, 269-282. (doi:10.1111/j.1095-8312.2006. 00624.x)

Davison, A. & Chiba, S. 2006 The recent history and population structure of five Mandarina snail species from subtropical Ogasawara (Bonin Islands, Japan). Molecular Ecology 15, 2905-2919. (doi:10.1111/j.1365-294X.2006. 02990.x)

 

About the Author: David Winter is a PhD Student at the University of Otago, who usually blogs at The Atavism which is part of the Sciblogs, a network of blogs written by New Zealand scientists and science communicators. When David started his reseach on land snails from the Cook Islands he thought of his snails as "little bags of genes that help him ask interesting evolutionary questions", but as he came to know snails he fell for them. Now he frequently finds himself describing the wonders of a slimey life to people at parties (their only mistake having been to ask what he does for a living). That was, at least, when he still went to parties: no matter what time you are reading this post, and whereabouts you are in the world there is good chance he's writing his thesis right now.

The views expressed are those of the author and are not necessarily those of Scientific American.

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