Underwater flowers

Flowering plants (angiosperms) began to dominate the Earth’s vegetation about 100 million years ago and, while other, more primitive, plants continue to be abundant, the present diversity of angiosperms is remarkable. When thinking of flowering plants, our minds may turn to beautiful garden borders, meadows and occasional clumps of flowers in woods and verges. Yet angiosperms have also invaded water bodies; although this is really a re-invasion, as land plant evolved from distant aquatic ancestors.

Anyone visiting a stream draining from chalk strata is impressed by the amount of vegetation growing over its bed and invading from the margins. There are many microscopic algae that are only visible under a microscope, but two common flowering plants often dominate: water cress and water crowfoot. Of the two, water cress grows into the stream from the banks and can extend right across narrow channels, a habit that has been exploited in the development of commercial cress beds fed by water from chalk streams. The bulk of the plant remains above the water surface and this contrasts with water crowfoot, where plants grow in dense stands, rooted into the bed of the stream and affecting its flow pattern. Water crowfoot is a relative of the buttercup and its flowers are very similar in structure, although they are white, rather than yellow, in colour (see below). It is only during flowering that we see water crowfoot above the water surface, although stands can become so dense that, at times of low flow in summer, they may be exposed to the air. They are well adapted to life in flowing water. The drag on the mass of leaves is counteracted by an effective rhizome and root system that ensures anchorage on the stream bed and the plants engineer the stream around them. Stands provide an obstruction to flow that creates channels of faster-moving water between plants and this serves not only to keep the substratum clear of sediment, but the growing leaves are also unaffected by deposition and can thus photosynthesise efficiently. In contrast, the base of the plant is an area of sediment build-up and this includes much organic matter [1] that serves as a source of nutrients - another way in which the plants engineer their habitat to their advantage.

Although water cress and water crowfoot are both aquatic plants, with the former fitting the definition less easily than the latter, seagrasses are truly aquatic. As their name suggests, these plants are marine, spending the whole of their life cycle under water. Seagrasses have a world-wide distribution and are perhaps most commonly associated with tropical seas and, especially, reefs, where the water is clear and there is good light penetration to the substratum, allowing efficient photosynthesis. Nutrients needed for growth are taken up by roots and stored in rhizomes that also serve to stabilise soft sediments. Interestingly, seagrasses are more closely related to lilies and ginger than to grasses [2] and their colonisation of soft sediments results in large "grassy" meadows when conditions for their growth are favourable. These are then grazed upon by many animals and they also form shelter for many other organisms and a substratum for yet more.

Seagrasses are also found commonly in shallow temperate seas that have sufficient transparency to allow the plants to grow. As I grew up by the sea in Torbay, and had a love of Natural History, I knew about seagrasses, but had no idea that there were meadows of the plants so close to some of my collecting spots. Nor did I know that seagrasses were flowering plants. Like many, I thought that seaweeds alone were the dominant large marine plants around coasts.

Two of my favourite places to visit in Torbay were Elbury [Elberry] Cove and the rocks below Corbyn’s Head, where I spent time collecting marine creatures to keep in aquarium tanks. [3] Both locations now have interesting and informative signs (see below) describing the importance and susceptibility to damage by boats etc. of the seagrass meadows just offshore.

It is likely that Zostera is one of the seagrasses and Henry Gosse mentions this plant when describing the results of dredging a little further up the coast:

Now we have made our offing, and can look well into Teignmouth Harbour, the bluff point of the Ness some four miles distant, scarcely definable now against the land. We pull down sails, set her head for the Orestone Rock [just off Torbay], and drift with the tide. The dredge is hove overboard, paying out some forty fathoms of line, for we have about twelve or fourteen fathoms’ water here, with a nice rough, rubbly bottom, over which, as we hold the line in hand, we feel the iron lip of the dredge grate and rumble, without catches or jumps. Now and then, for a brief space, it goes smoothly, and the hand feels nothing; that is when a patch of sand is crossed, or a bed of zostera, or close-growing sea-weeds, each a good variation for yielding. [4]

As Gosse was a devout Creationist, the presence of flowering plants in soft sediments around marine coasts would be another example of the extraordinary events of the six days in which all living things - and all fossil ones - came into existence. [5] To those of us who cannot share such a view, the presence of flowering seagrasses under water is another example of the extraordinary powers of evolution.

In terrestrial habitats, the fertilisation of ova by pollen is aided by insects, wind or other agents and there are a diverse range of adaptations to ensure that fertilisation is achieved - by evolving nectar and/or scent to attract insects, by evolving elaborate colour patterns that are attractive, by producing pollen in enormous quantities, etc. - yet flowers are retained by seagrasses where neither insects or wind can be involved in pollination. Seagrass plants bear both male and female flowers and the pollen from male flowers is released into the water and thus wafts around the plants. The use of water for fertilisation is, of course, extremely common in many marine organisms, including seaweeds and many animals, and that makes underwater flowers seem less unlikely than on first consideration. Natural History is full of such discoveries and one is always learning something new. That’s the satisfaction of it - that, and the sense of wonder at just what can evolve over millions of years and millions of generations. 

[1] Cotton, J.A., Wharton, G., Bass, J.A.B., Heppell, C.M. and Wotton, R.S. (2006) Plant-water-sediment interactions in lowland permeable streams: investigating the effect of seasonal changes in vegetation cover on flow patterns and sediment accumulation. Geomorphology 77: 320-324.

[2] http://www.seagrasswatch.org/seagrass.html

[3] Roger S Wotton (2012) Walking With Gosse: Natural History, Creation and Religious Conflicts. e-book.

[4] Philip Henry Gosse (1865) A Year at the Shore. London, Alexander Strahan.

[5] Philip Henry Gosse (1857) Omphalos: an attempt to untie the geological knot. London, John Van Voorst.

Parachutes and Wingsuits

If an insect falls from a plant it is rarely damaged as it has a low momentum and its body creates considerable friction drag as it falls. The force of the impact is reduced as a result and the insect then usually quickly scurries away.

Some larger animals are also adept at surviving falls and the offspring of tree-nesting ducks drop to the ground, being cushioned by leaf litter, by their down-covered bodies and by some flapping of their tiny wings. [1] Adult birds have little problem as they can fly down and then use sweeping movements of their wings to produce “reverse thrust” and thus decelerate gently, using the downward displacement of air to effect an easy landing.

Cats leap from trees, fences and walls, and their landing is cushioned by the shock-absorbing properties of the limbs, but surviving a fall from considerable height is much less likely, as maximum acceleration then results in high momentum. In arboreal mammals, swinging from the arms is a common feature and, together with the grip of the hands (and feet - and even tail in some monkeys) ensures that catastrophic falls are avoided. Yet some animals are able to leap from high in one tree to the base of a nearby tree while suffering no damage, thus moving more rapidly from one location to another than could be achieved over the ground. Two well-known examples of these “fliers” are tree frogs (in the genus Rhacophorus) and flying squirrels (genus Glaucomys).

Tree frogs spend their adult life in forest canopies, but, being amphibians, they must find water in which to breed. Some species use small rain pools in the axils of leaves or in tree holes, while the females of some Rhacophorus build nests of foam attached to tree branches overhanging ponds, the nest being created by rapid movements of the hind limbs (akin to whisking) in secretions made by the frog. Eggs are laid within this mass and these are fertilised by male frogs, hatching tadpoles then emerging into the foam and dropping into the water below to complete larval life. Froglets leave the pond and then climb adjacent trees, remaining in the canopy for the rest of their lives. Although they have pads on their toes to provide excellent adhesion to surfaces, adult frogs retain the webbed feet of the ancestral forms, even though they are not used for swimming. The webs are especially well-developed in some species and they act as parachutes to slow down the descent when frogs move from one tree to another, or from one branch to a lower one. 

Flying squirrels also use parachutes and these are formed from loose skin (termed a patagium), that runs between the fore and hind limbs, and between the fore limbs and the head. I was fortunate to be able to watch Glaucomys parachuting when visiting Dr Joe Merritt at the Powdermill Biological Station of the Carnegie Museum of Natural History in Pennsylvania. Dr Merritt had been studying these mammals for several years and laid out live traps so that we could then see the squirrels close up. Traps containing animals were collected and each trap was emptied into a cloth bag. In the photograph below you’ll see me (with Dr Merritt on the right and the late Prof. Björn Malmqvist on the left) at the moment when a captured squirrel bit me on the hand. I was told to take a firm grip of the skin over the neck of the animal, but it was still able to turn its head easily to defend itself from such unpleasantness. It was a lesson for me in just how much skin that flying squirrels possess. I let go immediately and the squirrel ran up a nearby tree, and then made a wonderful gliding flight before climbing rapidly, making another flight and then disappearing. The parachute of loose skin was very effective in slowing its descent, the squirrel covering tens of metres and with good directional control provided by the tail and by changing the profile of the patagium. It was most impressive and, in one way, I’m pleased that I was bitten.

I was reminded of this incident when reading a quote from Jeb Corliss in The Independent:

At the beginning, there were probably only very few squirrels that even contemplated flying from tree to tree. The other squirrels thought they were crazy. I imagine that hundreds of them died in the attempt. But then, in the end, one of them managed it. Now that, to me, is evolution. And now we are evolving, through technology and through skill. I liken what we’re doing in proximity flying to the first animals that left the water. We are evolving and growing. And becoming stronger. What else is the purpose of life? [2]

Not quite the way I would express the likely evolution of parachuting in flying squirrels, but Jeb Corliss is an expert wingsuit flyer, not a Biologist. Of course, it is impossible for humans to control their descent to the land without an external parachute and the earliest examples have been transformed into steerable ‘chutes that enable precise landings. As Jeb points out, wingsuit flying has close similarities to the flight of Glaucomys, with webbing between the arms, legs and body, analogous to the patagium of flying squirrels, providing steerable flight. Proximity flying capitalises on this level of control to allow fliers to pass very close to objects, or the ground, while making their descent (see the video clip at the end of this post).

Whereas Rhacophorus and Glaucomys have both evolved changed body forms to enable them to move from tree to tree for various reasons, human use of wingsuits is solely for pleasure. The excitement comes from exposure to danger, a sense of freedom, and the thrill of depending on a skill where a small mistake can have disastrous results. Some of us are drawn to such activities and proximity flying is addictive, even though the number of fatalities is large relative to the number of those who fly. Wingsuit fliers, and others involved in the most extreme sports, are only too well aware of the dangers and most are not afraid of death, recognising that it is possible that flights can go very wrong, even after meticulous preparation. They feel very alive as a result, and their approach to death contrasts markedly with the fear of life ending that seems to haunt others within the human population - and which is the basis of many religions. While animals such as Rhacophorus and Glaucomys cannot be aware of danger in the same way as humans, I wonder if  they get a thrill from flying?

[1] http://www.bbc.co.uk/learningzone/clips/mandarin-ducklings-jump-from-their-tree-top-nest/10473.html

[2] http://www.independent.co.uk/sport/general/a-wingsuit-diver-died-in-the-swiss-alps-earlier-this-week--so-why-do-they-take-such-risks-9709871.html

Shells, floats and an interesting association

I grew up by the sea and always enjoyed walking on local beaches looking for shells washed up by the tide. There were many shell fragments, especially of cockles that must have grown in their millions just offshore, but also a wide variety of whole shells, especially those of snails. I continued to enjoy beachcombing and, while on a family holiday in Jersey, found an excellent beach, dominated by shells of the flat periwinkles Littorina obtusata and L. mariae. [1] Some were bright yellow, others orange, white, or of a reddish hue. We collected as many of the shells as we could and, more than twenty years later, they are still exhibited in a glass jar in our bathroom.

Occasionally, violet shells from the snail Janthina are washed up on beaches, especially after long periods of strong winds. They are similar in form to those I had collected in Jersey, but they have less strengthening than the Littorina shells, which need to be strong to withstand the erosive action of the water, and suspended mineral particles, over the shores on which the snails live. Can we assume, therefore, that Janthina exists in a less erosive habitat? Indeed it does - the snails live at the surface of oceans, attached to a float of bubbles.

 

In July and August 1954, there were sustained, strong westerly winds in Great Britain and Ireland and several people reported finding large numbers of Janthina shells on exposed beaches This prompted Dr Douglas P. Wilson of the Marine Biological Association to write a letter to The Times to ask readers for more information about sightings. Reports came in from many locations and, among all the shells, there were a few living specimens. These offered the scope for investigations of the formation of the float, adding to the information acquired by earlier investigators. 

Among the first to make observations was Reynell Coates, who, in 1825, published a description of the float. Coates qualified as a medical doctor in Philadelphia and then set sail as a ship’s surgeon on a voyage to the East Indies. He was very interested in Natural History and took samples of organisms from the surrounding water (presumably when becalmed, or unable to continue the passage - the journey terminated at Kolkata after the outbreak of the Burmese War [2]). This is what he wrote about some specimens of Janthina:

Individuals being placed in a tumbler of brine, and a portion of the float being removed by the scissors, the animal very soon commenced supplying the deficiency in the following manner: the foot was advanced upon the remaining vesicles, until about two-thirds of the member rose above the surface of the water; it was then expanded to the uttermost, and thrown back upon the water.. ..it was contracted at the edges, and formed into the shape of a hood, enclosing a globule of air, which was slowly applied to the extremity of the float. A vibratory movement could now be perceived throughout the foot, and when it was again thrown back to renew the process, the globule was found in its newly constructed envelope. [3]

Wilson’s  description of float formation in Janthina included these observations:

Sometimes the new bubble fails to be attached and floats away as a tiny glassy sphere.. ..The completed float is firm between the fingers, springy and dry - it is not in any sense sticky. [4]

Although the bubbles are surrounded by mucus secreted from glands in the snail’s foot, there are clearly components of this secretion (proteins?) that, after dehydration of the mucus mass, form a solid coating for the trapped bubbles. This ensures that the float is near-permanent, although older pieces break off and need to be replaced. [4] To say that the float is important for the snail is an understatement as, specimens of Janthina that sink into the water column cannot regain the surface. [4]

Janthina is a predator and feeds on other members of the floating community at the air-water interface. It is especially associated with Velella (the “by-the-wind sailor”) [3], and both are blown ashore in masses. Velella is a colonial relative of jellyfish, with polyps attached to a secreted, flattened float that has a sail rising from it (see below), allowing the colony to be transported by wind. The polyps use stinging cells to capture small creatures from within the water column, such as invertebrates and small fish. Wilson quotes Mr Peter David in describing the manner in which Velella is preyed upon by Janthina, the snail cutting out semicircular pieces of the float and attached polyps “in much the same way as a caterpillar does on the edge of a leaf.” [4]

Gastropod snails, like Littorina and Janthina, have very similar body plans and it is relatively easy to see how the latter evolved from a shore-dwelling ancestor, but how did it develop an ocean-going existence? Observation of pond snails shows that some individuals move across the underside of the water surface while the foot is held in the surface film and, to these snails, the interface is like a solid surface. [5] They move here as they do over the substratum, using muscular contractions of the foot, and feed as they go. A characteristic of pond snails is their relatively thin shell, as strengthening calcium salts are not as available in fresh waters as they are in the sea. It is likely that the ancestral Janthina did not strengthen the shell in the way that Littorina does and that it moved under surface films as well as over the substratum, just like some pond snails. In time, the mucus used for lubrication and attachment during crawling was used to coat bubbles formed by the foot and this resulted in the development of the float. They then lost the power of locomotion, or it was highly reduced, and their feeding changed from scraping materials from surfaces to the removal of sections of prey such as Velella, into which they had drifted, or which had been blown towards them.

How Velella evolved its current form is a mystery. There are various theories on how gastropod molluscs evolved from their ancestral molluscan form, but how did the colony of polyps develop, complete with a float to which they were attached? Velella has many sedentary colonial relatives (members of the Cnidaria), but how did life at the ocean surface begin - and what were the origins of the sail?

[1] Gray A. Williams (1990) The comparative ecology of the flat periwinkles, Littorina obtusata (L.) and L. mariae Sacchi et Rastelli. Field Studies 7: 469-482.

[2] W.J.Snape (1968) Reynell Coates (1802-1886): politician, poet, editor, naturalist, lecturer and physician. Transactions and Studies of the College of Physicians of Philadelphia 35: 112-118.

[3] Reynell Coates (1825) Remarks on the floating apparatus, and other peculiarities, of the genus JANTHINA. Journal of the Academy of Natural Sciences of Philadelphia 4: 356-360.

[4] Douglas P. Wilson and M. Alison Wilson (1956) A contribution to the biology of Ianthina janthina (L.). Journal of the Marine Biological Association of the United Kingdom 35: 291-305.

[5] Roger S. Wotton and Terence M. Preston (2005) Surface films: areas of water bodies that are often overlooked. BioScience 55: 137-145.