"Suspension feeding"

Most of the solar energy falling on the earth falls on the oceans. Most of the photosynthesis carried out in the oceans is carried out by phytoplankton --microscopic plants floating in the upper layer, known as the Euphotic zone. The major components of the phytoplankton are diatoms, dinoflagellates, smaller flagellated algae, and Cyanobacteria -- the prokaryotic organisms sometimes called blue-green algae.
This plant growth provides food for animals that are specialized for feeding on microscopic particles. Their food consists of phytoplankton, zooplankton, and detritus.
This mode of feeding is usually known as filter feeding, although suspension feeding is perhaps technically more correct, because some of the methods do not use filters.

Suspension feeding typically has two requirements:
I. Water currents to bring particles to the animal:
  1. external currents in the water -- streams.
  2. currents created by cilia and flagella
  3. currents created by muscular activity
    There are a few cases where gravitational settling of particles onto the surface of an animal may also be important.

II. Methods for removing the particles from the water:
  1. trapping by mucous.
  2. trapping without the use of mucous.

We can look at examples from all 6 categories, but first lets look at how mucous is used.

There is a large class of mucopolysaccharide materials that are extracellular secretions of cells. They share some properties with cell surface glycoproteins, but also have the property of forming gels. This class includes
The matrix known as "ground substance" in connective tissue and cartilage, which also contain lots of collagen fibers.
The organic matrix of mesoglea, which can form a gel with more than 99% water and still have significant elastic properties. Mesoglea can also contain collagen fibers.
The synovial fluid in joints between vertebrate bones.
The "vitreous humour" in the interior of the vertebrate eyeball.
Egg jelly coats.
Mucous, used for a variety of purposes:
1) collecting and transporting particles. Collecting for food, but also for elimination as in our repiratory tracts.
2) protective coatings on external surfaces, and gut linings. [External protective coatings are often enhanced by a content of other substances -- toxins, etc. The mucous retains them near the surface.]
3) lubricant for ingestion of large food (saliva)
4) adhesive used for locomotion by snails. [The slime trail remaining on the surface behind a snail or slug contains information, which is sometimes used so that the animal can follow the trail to return to its home location, and sometimes used by predators to catch its originator. Not known how animals detect the polarity of the trail.]
5) protection against dessication. [Terrestrial snails seal up the opening of their shell, or seal the edges to the substratum.]
6) as a structural material, similar to the ways in which spiders uses secreted protein threads. Prime example: slugs crawl out on tree branch, and a mating pair hangs from the branch by a rope of mucous, 10-20 cm long, while they mate. The mucous rope is elastic, and is stretched to about twice its rest length by the weight of the slugs, but it does not show plastic elongation. When they are finished they crawl back up the rope, and one of them usually eats it. [Rollo & Wellington, Nat. Hist. 86: 46-51 (1977)]
7) as a structural glue, to make shelters out of sand grains and other material from the environment.

How are these capabilities explained by the chemical nature of mucous? Good biochemical data is only available for mucous from a few sources. This is a current model: [Silberberg, Symp. Soc. Exptl. Biol. 43: 43-63 (1989)].

Basic glycoprotein molecule has a MW of about 500,000, with about 1000 amino acids and 2000 monosaccharide units.

This is a long, rod-like molecule, which can aggregate to form much longer strands.

One peptide chain, with two regions. The B-region contains about 400 amino acids - 20 of these are cysteines. The T-region contains the other 600 amino acids, and about 300 of these are serine or threonine. About 200 of these are esterified to a short polysaccharide chain -- avg 10 sugar residues. The components of the polysaccharide chain vary, but the standard pattern is alternation between A and B, where
A is N-acetyl glucosamine, either with or without a sulfate group.
B is either a glucuronic acid, or a glucose with a sulfate group.
There is at least one (-) group for each AB unit, sometimes two (-) for every AB unit.

These polysaccharides are referred to as glycosaminoglycans. ("GAGs ")

The highly acidic character of these polysaccharides is responsible for properties:
Very hydrophilic --> gels with high water content.
Electrostatic repulsion causes the side chains to stick out and occupy as much space as possible, and causes the entire molecule to have a linear form, about 200 nm long.
Lots of opportunities for ionic interactions with other materials. Sticky.

Mucous secretion is a process of exocytosis, and has some similarities to nematocyst discharge:
The mucous is in a highly concentrated form, and has a very high Ca++ content, when it is in an intracellular vesicle. After exocytosis, it very rapidly swells up to 100-1000 times its volume. Maybe final extent of swelling is determined by cross-links between B portions of molecule?

Examples of use of mucous for collecting food particles:

Urechis caupo is a simple worm, about 10-15 cm long, that lives in U-shaped burrows in mud at the bottom of shallow bays. Secretes a funnel of mucous, attached to the sides of the burrow and to the mouth. Pumps water through the burrow by peristaltic contractions of the body muscles. Water must pass through small pores in the mucous sheet. At intervals, eats the mucous sheet.

Chaetopterus variopedatus is a segmented, Annelid, worm, similar-sized, that lives in U-shaped, papery tubes constructed of mucous and dirt. Pair of appendages on a segment near the mouth extend up and form a ring inside the tube. They secrete a mucous net that extends back to a collecting organ that rolls the net up into a ball that can be transported anteriorly to the mouth and ingested. Water is pumped through the tube by dorsal vanes on three segments posterior to the collecting organ. Again, water must pass through small pores in the mucous sheet.
Net consists of an orthogonal mesh of fine fiber-like strands. In one direction, fibers have about 0.1 m diameter and 0.5 m spacing. In other direction, fibers are much finer- about 0.01 m diameter, and about 0.8 m spacing. Can easily explain previous observations indicating very high efficiency in removing micron-sized particles from the water stream.

Bivalve molluscs, such as Mytilus. In this case,feeding occurs inside the shell, and is more difficult to observe. However, it is well established that water currents are set up by cilia on the ctenidia : These organs probably evolved originally as gills for respiration, but now this function is quite secondary in bivalves.

This roughly represents the appearance of the ctenidia inside the shell of a Mytilus . Each of the 4 ctenida is a sheet of parallel filaments. In cross-section:

Each demibranch is a row of folded filaments held in shape by interlamellar junctions. Water is pumped into the interior of the demibranch by lateral cilia between the filaments. The water current leaves the animal at the posterior end of the body, in some bivalves via a siphon.
The filaments of the ctenidia are separated by spaces about 20 m wide -- too wide to explain the efficient filtering of small particles from the water current. There are three theories about how filtering takes place:

1) A continuous sheet of mucous covering the surface of each ctenidium. [Proposed by MacGinitie[Biol. Bull. 80:18-25, 1941], who was responsible for early observations on Urechis and Chaetopterus . Based on observations through windows implanted in shell, showing transport of particles over the surface of the gill at an angle to the filaments].
2) Filtering by the laterofrontal cilia. These stick out into the water stream as it passes between the filaments. Although the spacing between the laterofrontal cilia (ca. 5 m) is too large to explain filtering, SEM observations show that each laterfrontal cilium is a compound cilium, and the individual cilia feather out with spaces between them less than 1 m. Idea is that particles are trapped by the laterofrontal cilia, which then bend over and transfer the particles to mucous strands on the frontal surface of the ctenidial filaments. [Moore (1971)Marine Biol.11:23-27]
3) [Jorgensen (1989) Comp.Biochem.Physiol.94A:383-394] Because resistance to water flow through laterofrontal cilia is so high, most water flow is concentrated into gap between their ends. Result is a steep velocity gradient, which causes particles to drop out of the flow and move towards the frontal surfaces of the filaments, where they are caught by mucous.
In both (2) and (3), it is the stickiness of the mucous, rather than its ability to form a fine-meshed net, that is important. In all three hypotheses, once particles are trapped by mucous, the mucous transport, driven by the frontal cilia, carries them to the mouth.

MacGinitie's mechanism of a continuous mucous net has also been thought to be true for lower chordates -tunicates and Amphioxus - but this has recently been challenged.

In all these cases, a dominant them is trapping of food particles by mucous, followed by ingestion of the mucous along with the food particles. Some studies have reported that as much of 80% of the metabolism of the animal is spent in synthesizing and recycling mucous, but this is probably not true for Mytilus , where most of the metabolism is used to pump water.

Other examples of use of mucous for feeding:

Aurelia simply secretes a layer of mucous on the oral surface of the animal. As it floats or swims around in the water, particles stick to the mucous. The mucous sheet is transported by cilia to the edges of the disc, and then transferred to the oral arms, where ciliary currents transport it to the mouth. Some anemones use mucous sheets in a similar manner.

Serpulorbis , a sessile tube snail, simply sends out sheets of mucous into the water currents, and then reels them in and eats them.

Some insect larvae living in streams secrete elaborate mucous nets.

Feeding without mucous:

Crustaceans have a hard exoskeleton covering the body, which is not appropriate for either mucous secretion or cilia. Typically use appendages covered with fine bristles -- setae -- that can collect food particles as they are moved through the water.
Especially copepods and larvae in Zooplankton, and barnacles. However, although barnacles in still water, for instance in an aquarium, with reach out and move their legs to feed, most of them normally live in places where all they have to do is extend their legs out into a current of moving water.

Suspension feeding by vertebrates: Fish, Birds, Whales
Fish: basking sharks, herring, mackeral. Structures called gill-rakers extend into the water stream going from the mouth to the gills. Originally thought to act as filters (but they are not very fine). One newer study indicates that they simply act to deflect water flow up to the roof of the mouth, where particles are trapped by mucous.

Birds: common for aquatic birds to strain material out of the water, using a fringed edge of the upper bill. Especially developed in the group known as prions, or whale-birds.

Whalebone whales : "whalebone" of keratin extends down from roof of mouth. Whale swims at surface with mouth open, water exits from sides of mouth. When mouth is closed, tongue squeezes out the rest of the water, and the collected plankton is swallowed.
Especially feed on larger crustaceans (Euphausia) that are seasonally abundant in Antarctic waters.

In general, these vertebrates are not obligate filter feeders, and can also take larger food. Success as filter feeders probably depends on being intelligent enough to locate and follow areas that are especially rich in plankton.