The mysterious crystalline tentacles of snails

Author: Julián Monge Nájera, Ecologist and Photographer 

200 years ago, an Estonian zoologist described a strange worm that lived on the skin of freshwater snails. No one knew what it was doing there, and after 200 years, the answer is that it may be a protector of the snail, that it may be a parasite, or maybe both. It is important to me because I got to know these worms in person when I did my first scientific study almost four decades ago. They looked like dozens of liquid crystal tentacles protruding from the snail.

The whitish filaments in this Stagnicolasp. snail are worms of the species Limnaea stagnalis. Source: CC BY Michal Maňa.

When Estonian zoologist Karl von Baer, founder of embryology, dedicated the species to Linnaeus in 1827, he knew that Chaetogaster limnaei worms always were associated with freshwater mollusks, whether they were small clams or snails of very different species. But what the worms were doing there was a mystery for decades, and even today, we still don’t know for sure if there is a single species of worm with two personalities or several species at the moment indistinguishable except for their behavior. 

Karl Reinhold Ernst von Baer, 1792-1876, who described the worm Chaetogaster limnaei during the reign of Charles X.

I met these tiny worms in the early 1980s, when, as a biology student at the University of Costa Rica, I saw what looked like crystalline tentacles in the pond snails that I had on my desk and that I had collected in a pond in San Pedro de Pavas (Costa Rica). They fascinated me, but I didn’t know what they were, and Dr. Pedro Morera helped me prepare some and send them to Brazil, to be identified by an expert whose name I no longer remember.

As far as I know, the first to write that there was something strange about these worms was E. Michelson, who in 1964 noticed that, in addition to protecting the snails from the parasite Schistosoma mansoni, some of these worms appeared inside the snail’s kidney, where they would hardly be doing something good; but he did not know what the worms were doing there¹.

The following year, Welsh zoologist L. Gruffydd solved the first part of the problem: the worm appeared to have two subspecies, one, Chaetogaster limnaei limnaei, lived on the skin of the snail and ate parasitic trematodes that approached the snail, thus protecting the snail. The other, Chaetogaster limnaei vaghini, penetrated the snails’s kidney and parasitized it. He added that when the snail died, the worms looked for new homes and took advantage of these difficult times to mate. However, without the shelter of the snail, many died².

A quarter-century later, a team of investigators realized that the relationship was more complex. Yes, the worms that stay on the skin eat everything that comes near and fits in their mouth, protecting the snail from parasitic flukes, but if too many worms occupy a snail, they become a burden, and the result is that overloaded snails lay fewer eggs³.

That same year, studying Chaetogaster on the snail Helisoma anceps, it was discovered that there are few worms in snails when the weather is very cold and that the worms prefer snails infected by the trematode Halipegus occidualis, whose slow larvae are easy to capture and eat⁴.

But the most interesting thing is that nothing can be generalized about these worms: the conclusions are contradictory from one study to another. They protect the snail Biomphalaria glabrata from the dreaded parasite Schistosoma mansoni, but ironically, snails with the parasite grow better and lay more eggs! In that case, the concept of the trematode as a parasite is questionable because, by definition, a parasite must do net damage to its host⁵. 

Some notes about the worm Chaetogaster limnaei in my sketchbook. Large number of worms, similar to crystalline filaments, cover the skin of the snail in the photograph, taken by Michal Maňas.

Earthworms prefer snails of certain species; within a species the larger and more spacious individuals; and even if they are large, they avoid them if they lack parasites because only parasitized snails release the larvae that serve as food for the worm⁶.

For years I have wondered if these two «subspecies» are really two totally different species: vaghini, internal and clearly parasitic; and limnaei, which live outside and offer various degrees of benefit to the snail (depending on the environment and the species of snail). A 2015 study says no, the authors report that these worms are a rare case of “intraspecific plasticity” in which the same species can act as a parasite or as a protector and that it comes from an ancient worm that was an external parasite of mollusks⁷.

These researchers may be right, but I will continue to doubt until there is better evidence on the extremely complex relationship between these worms and their snails, which reminds us that, in nature, the answer is rarely as simple as it seems.

Originally published  in Blog Biología Tropical: 12 august 2020

*Edited by Zaidett Barrientos, Katherine Bonilla and Carolina Seas

REFERENCES

¹ Michelson, E. H. (1964). The protective action of Chaetogaster limnaei on snails exposed to Schistosoma mansoniThe Journal of Parasitology, 50(3),441-444.

² Gruffydd, Ll. D. (1965). The Population Biology of Chaetogaster limnaei limnaei and Chaetogaster limnaei vaghini (Oligochaeta). Journal of Animal Ecology, 34(3), 667-690 

³ Stoll, S., et al. (1991). Density-dependent relationship between Chaetogaster limnaei limnaei(Oligochaeta) and the freshwater snail Physa acuta (Pulmonata). The American Midland Naturalist, 125(2), 192-205.

⁴ Fernandez, J., et al. (1991). Population dynamics of Chaetogaster limnaei limnaei (Oligochaeta) as affected by a trematode parasite in Helisoma anceps (Gastropoda). The American Midland Naturalist125(2), 195-205.

⁵ Rodgers, J. K., et al. (2005). Multi-species interactions among a commensal (Chaetogaster limnaei limnaei), a parasite (Schistosoma mansoni), and an aquatic snail host (Biomphalaria glabrata). Journal of Parasitology91(3), 709-712.

⁶ McCaffrey, K. (2014). Patterns of multi-symbiont community interactions in California freshwater snails(Ph. D. Thesis). University of Colorado, Boulder, CO, USA.

⁷ Smythe, A. B., et al. (2015). Untangling the ecology, taxonomy, and evolution of Chaetogaster limnaei(Oligochaeta: Naididae) species complex. Journal of Parasitology101(3), 320-326. 

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