Paleozoic Puzzle: the Origins of Abalone

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Orecchio di Venere — the ear of Venus. Adriatic Sea. Haliotis tuberculata. Photo by Marcello Francesco. http://www.marcellodifrancesco.com/

Around the world they are  called abulón, awabi, bàoyú, ormer, ormeau, pāua, perlemoen, pauhi, haliote but all are abalone. Abalones (family Haliotidae) are all in the genus Haliotis (“ear shells”) a worldwide group of snails known for their beautiful iridescent shells and incredible tasty meat. In many places of the world abalone are (or were) multi-million dollar fisheries that were initially sold at beach hamburger stands but with declining rarity have turned into a highly coveted epicurean delight In some places they sell for as much as $420 per pound and are marketed by gang cartels. But abalone are much more then that: they are an ancient lineage of primitive snails that may shed light on the early diversification of gastropods: a group (a class) of coiled, single-shelled snails second in diversity only to insects. And abalone, despite their ancient origins, are a remarkably successful group in the present with 56 species that occur in both temperate and tropical seas around the world, (Geiger and Owen, 2012).

Among the defining characteristics of abalone are an ear-like shell lined by iridescent mother-of-pearl and a row of respiratory pores along the side of the shell. The pores are generally thought to be an early evolutionary “solution” in primitive snails, the Vetigastropods, to the consequences of torsion: a unique developmental process found only in snails whereby the gut, liver and gonads (the “visceral mass”) rotates early in life (see below). Why this occurs is still a mystery but all snails do it. The consequence, which is thought to be the advantage of doing so, is it places the chamber containing the gills (the mantle cavity) over the head which may have allowed a protective retreat into this chamber to escape from predators. When you pick up a garden snail you will witness this as the snail pulls back inside and seals itself within the shell with a protective trap door.

Illustration of Torsion in snails.

Illustration of Torsion in snails whereby a backwards facing mantle cavity is rotated forward so the head can retreat into the shell.

However, this ancient evolutionary jump — which is a defining characteristic of all snails — despite its great advantages, is thought to have created a “sanitation problem” by placing the discharge from the digestive system (the anus) above the head, potentially fouling the gills and sense organs and conflicting with the discharge of sperm and eggs. As such, for hundreds of millions of years following this “breakthrough” primitive snails adapted to the “sanitation problem” in a variety of ways. Abalone seem to have solved this problem with their row of holes which allows water to move out the backward facing pores.

abflow

Illustration and photo of water flow through abalone pores which solved the problems created by torsion. Sources: Asnailsodyssey.com (left); Photo by Derek Stein (right).

But here’s the mystery: this type of adaptation and similar “solutions” in other primitive snail families occurred a long, long time ago: perhaps during the Cambrian period (about 500 million years ago or before fish appeared). Yet fossil abalone are completely unknown prior to the Cretaceous period (about 80 million years ago) so there is a huge gap in our knowledge of the early origins of abalone and how they relate to their defining characteristic. More importantly, our understanding of these changes is largely based on the comparative anatomy of modern species but all we have in the past are preserved shells or casts from shells. Thus, there is a lot of uncertainty.

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The oldest know abalone fossil. Haliotis lomaensis, Point Loma, California. from the Cretaceous (Maastrichian) period, about 80 million years ago. Source: Cox, 1960.

So here’s what we do know: there are several primitive groups of mollusks that are believed to be the earliest primitive snails: the Helicionellids, Igarkiellids, Pelagiellids, and the Bellerophonts. I know, fun names but there won’t be a quiz so relax. Although the exact relationship of these early groups of snails to the abalone lineage (the Vetigastropods) is not entirely clear, what is important is that they all seem to be adapting to the “sanitation problem” created during torsion by channeling water flow around the mantel cavity in different ways. Helicionellids had backwards facing snorkels or ridges that channeled water; Igarkiellids had an internal cavity that funneled water away from the head; Pelagiellids had asymetrical shells that funneled water in from the sides and over the gills; and most bellerophonts had a sinus or groove that served as an exhalant structure moving water away from the head. One bellerophont in particular, the genus Tremanotus (far left in figure below) had a row of respiratory pores much like modern day abalone. Clearly, given the broad range of adaptations shown, water flow through the mantle cavity was an important issue for these primitive snails and many species came up with solutions similar to abalone: holes, slits or openings to funnel water over the gills.

snails-flow

Illustration of different shell adaptions in Paleozoic Gastropods showing inferred water flow patters in the mantle. Various sources: Parkhaev, 2008; Knight et al., 1960.

Other adaptations found in modern snails like abalone, which are probably close relatives, involve slits in the shell such as in slit shells (Pleurotomariids, Scissurellids, and Temnotropids), a single pore at the top of the shell or slit at the edge as in keyhole limpets (Fissurellids), or the loss of one gill and no holes or slits as in turban snails (Geiger et al., 2008).  The latter situation is the pattern that most all other snails follow and only these primitive species show these “early solutions” of holes, slits, etc. So what does all this mean? I don’t think these adaptations have anything to do with the “sanitation problem” at all but rather these primitive snails are responding to energetic advantages of their new condition: one derived from induced water flows.

Modern snails with abalone-like adaptations to the gills and shell. Left: Slit shells. Photo: Barry Brown; Center: Keyhole Limpet. Photo: Mary Jo Williams; Right: Turban snail, Callistoma ligatum. Photo: Gary McDonald.

Induced flow is a consequence of fluid dynamics, a simple property of moving fluids, such as air or water. In the 1700s Daniel Bernoulli developed the principle that changes in fluid velocity, picture water flowing up and over an abalone shell, result in changes in fluid pressure. As a result changes in pressure can drive flow patterns passively, that is without any energy from the living organism. A great example of this exists in sponges (Vogel 1988). Their elevated mound-like hollow body filled with pores creates currents that pulls water through their bodies passively, providing them with food-laden seawater which they use as a food source. The key point is that it is a completely passive process: the sponge doesn’t  need to expend energy pumping water through its body; it is simply a consequence of its shape and the physics of induced flow. So stay with me here because this is really cool.

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Passive water flow in a sponge.

Janice Voltzow, in a classic 1983 paper, was the first to recognize that this process was occurring in abalone. Yes! They do it too. Their pores act like the big hole at the top a sponge: the backward facing pores create high-velocity low-pressure flow dynamics that passively pull seawater in and over the gills, flushing waste products, sperm and eggs, whatever, out the back with minimal abalone energy —  a great advantage and a potentially key energetic savings. In a 1995 paper Voltzow and Collin show that induced flows also occurs in keyhole limpets. Surprise! These critters are taking advantage of induced flow and energetic dynamics, not responding to any “sanitation problem” which may sound like an important issue to us humans; but as yucky as it sounds saving energy is probably more important. Recent research on sponges indicates this energy savings may be as high as 28% of their total energy budget (Leys et al., 2011). This is really important because, you know, when you save energy you have more to expend elsewhere: like for reproduction! which clearly is important in the long run and survival over hundreds of millions of years, which these snails groups have done.

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Induced flow in a the black abalone. Dye injected in forward facing pores is passively pulled over the gills and exits in the back. This worked with live and dead animals. See Tissot, 1992. Photo: Brian Tissot.

So here’s the bottom line: I believe that all of these primitive snails, Helicionellids, Igarkiellids, Pelagiellids, Bellerophonts and of course the Vetigastropods, were taking advantage of these induced flows. And that ultimately this explains their defining characteristics of holes, pores, slits, snorkels, and grooves. Eventually, snails came up with another solution, the loss of one gill and flow across the head (as in turban snails), that all others adopted because it had some other evolutionary advantage. But these primitive species still show these early adaptations, which is both cool and amazing and makes them unique.

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Black abalone shells accumulate on the beach during mortality in 1992. After several weeks these shells would be broken into small pieces; not a good environment for fossils. Photo: Dan Richards.

Why is this important for early abalone evolution? Well to truly take advantage of currents they must live in relatively shallow waters (< 100 ft) which the vast majority of existing abalone species do. Because these shallow habitats are high quite rare as far as marine environments go (most of the ocean is deep-sea mud), and have high wave action, we wouldn’t expect many abalone fossils because they would be mostly broken up on the shore. Thus, their shallow habitat, which is due to their feeding on kelps and other algae, is probably why we have a large gap in the fossil record. In contrast, close relatives of abalone, the slit-shells (Pleurotomariids) are currently found in deep-sea environments and have a rich fossil record that extends back into the Cambrian period. Thus, it is likely that abalone have been around since that same time period and are therefore an ancient lineage of snails. Their worldwide distribution, high abundance and diversity certainly support that conclusion.

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High shell diversity and variation in pore size, elevation and shape is common among abalone species. Photos: Brian Tissot

References:

  • Cox, K. 1960. California Abalones, Family Haliotidae. California Fish and Game Bulletin 118. 130 pp.
  • Geiger, D. L., and L. T. Groves. 1999. Review of fossil abalone ((Gastropoda: Vetigastropoda: Haliotidae) with comparison to recent species. J. Paleontology, 73 5): 872-885.
  • Geiger, D. L. &  B. Owen. 2012. Abalone – Worldwide Haliotidae. Conchbooks, viii + 361 pp.
  • Harper, J. A. and H. B. Rollins. 2000. The Bellerophont Controversy Revisited. Amer. Malacological Bull.15(2): 147-156.
  • Haszprunar, G. 1988. On the origin and evolution of the major Gastropod groups, with special reference to the Streptoneura. J. Molluscan Studies 54(4): 367-441. 
  • Geiger, D. L., A. Nützel, & T. Sasaki. 2008. Vetigastropoda. In: W. Ponder & D. Lindberg, eds. Evolution of the Mollusca. University of California Press, Berkeley: 297–330.
  • Knight, J. B.  L. R. Cox, A. Myra Keen, A. G. Smith, R. L. Batten, E. L. Yochelson, N. H. Ludbrook, Robert Robertson, C. M. Yonge, and R. C. Moore. 1960. Treatise on Invertebrate Paleontology, Part I, Mollusca 1. Geological Society of America / Univ. Kansas Press.
  • Leys, S. P., G. Yahel, M. A. Reidenbach, V. Tunnicliffe, U. Shavit and H. M. Reiswig. 2011. The sponge pump: the role of current induced flow in the design of the sponge body plan. PLoS One 6(12): e28887-e277878.
  • Parkhaev, R. Y. 2008. The early Cambrian radiation of Mollusca. Chapter 3 in: W. F. Ponder, David R. Lindberg (eds). Phylogeny and Evolution of the Mollusca. Univ. California Press.
  • Tissot B 1992. Water movement and the ecology and evolution of the Haliotidae. In: Abalone of the World: Biology, Fisheries and Culture. Proceedings of the First International Symposium of Abalone, LaPaz, Mexico, 1989. Shepherd SA, Tegner MJ, & Guzman del Proo SA, eds., pp. 34-45. Fishing News, Oxford, England.
  • Vogel, S. 1988. How organisms use induced flow. American Scientists 76(1): 28-34.
  • Voltzow J 1983. Flow through and around the abalone Haliotis kamtschatkana. Veliger 26(1): 18-21. 
  • Voltzow, J. and R. Collin. 1995. Flow through Mantle Cavities Revisited: Was Sanitation the Key to Fissurellid Evolution? Invertebrate Biology, 114 (2): 145-150.

  2 comments for “Paleozoic Puzzle: the Origins of Abalone

  1. Chorchat
    June 18, 2015 at 3:49 am

    Very interesting, thank you very much for such a good knowledge 🙂

  2. August 12, 2015 at 11:32 pm

    Nicely done Dr. Abalone 2 …Respectfully, Dr. Abalone 1

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