(a) Algae as Producers of Organic Matter
Since algae are autotrophic plants, they share with the remaining more advanced autotrophic members of the Plant Kingdom the capacity to synthesize complex organic molecules out of carbon dioxide and water, using various other major and minor elements in the process. This process — the biochemical kingpin of life on our planet — is called photosynthesis. On the unceasing performance of this process hangs the continuity of all animal life — which is utterly dependent on the plant world. Directly or ultimately, land animals depend on land plants for food and aquatic animals rely similarly on algae as their basic source of chemically-bound sunshine and hence energy.page 93
Let us diverge for a while to take a look at the very fundamental implications of this process called photosynthesis — the prerogative solely of the plant kingdom. This is the term applied to a set of reactions carried out in green plants whereby a simple gas of the air, carbon dioxide, is converted into much more complex compounds among which sugars, starch and oils are most important. Carbon as it exists in carbon dioxide is in its most highly oxidised state whereas it is partially reduced when found in sugars, starch, oils and indeed every form of organic matter. To synthesize these reduced complex compounds of carbon the plants require energy, and this comes from sunlight. Animals including ourselves and the non-green plants such as fungi consume this organic matter in some form or other and in the process of digestion break these compounds down again. The purpose of this break-down is to release the built-in sunlight energy which is then used to drive the cellular machinery and life processes of the animal kingdom and the non-green plants. So, plants photosynthesize organic matter and in doing so harness energy: animals degrade (or ‘desynthesize’) organic matter and release energy.
We must regard organic matter not only as a hotch-potch of complex organic chemicals but as a colossal lay-by or stockpile of available energy for the biological world. The more that is stock-piled the greater the animal populations that can be sustained, so that as far as humans are concerned the interdependence of this energy stock-pile and animal population is synonymous with food supply. The existence of animal life on earth is related to the amount of reduced carbon. In terms of a bank-balance of reserve biological energy, the amount of credit is synonymous with the surplus of reduced carbon over and above that used by animals and non-green plants. One cannot envisage a time or circumstance when the world will be ‘in the red’ for reduced carbon; but on one point we can be quite sure — we will never be alive to see this happen because all life on earth will quickly disappear the moment an overdraft of this commodity is established.
From this detour in our story, a couple of points emerge which must be kept in mind so as to get the correct perspective on what is to follow. Firstly, green plants (or more correctly, those containing the pigments capable of initiating photosynthesis) are the only organisms in the world which can synthesize complex organic matter from simple inorganic substances in sufficient quantities to bring about a surplus: and secondly, surplus of this organic matter is synonymous with available energy on which the rest of the biological world is absolutely dependent. It is necessary to reorient our thinking along these lines; and having done this, we are in a better position to appreciate the fundamental importance of the algae in the biological scheme of things.page 94
The proportion of our earth occupied by permanent water — fresh and marine — exceeds 71% of the total earth's surface; and except for a few freshwater ferns and seed plants, this is the undisputed and botanically uncontested domain of the algae, since they are predominantly water-plants. Because the algae are photosynthetic they must be synthesizing throughout this aquatic environment enormous quantities of organic matter — in other words, their contribution to the credit side of the biological bank-balance of energy must be colossal. This association of the ideas of the aquatic habit of algae and the vast aquatic surfaces of the earth leads to the posing of two questions: the first is — ‘How much organic matter is produced by the algae?’, and the second — ‘What happens to all this organic matter?’. The answer to the first question forms the subject matter of this present article; but the answer to the second is much more diffuse and will be found scattered throughout the rest of this series of articles. This first part is designed to enable you to achieve some realization of the quantities of organic matter estimated to be produced by algae, and meanwhile only sufficient reference will be made to its fate to fill out the story and set the scene for what comes later.
materials which are retained by the algal cells and built into cell material and food reserves for increase in cell size and reproduction
materials which are not retained by the algal cells but are excreted sometimes to the benefit or even detriment of other organisms.
the production of ectocrine substances which affect the metabolism of other algae and animalspage 95
the excretion into freshwater of chemicals referred to as ‘tainting chemicals’. These diffuse out of the algal cells into drinking-water in holding areas and produce those smells and off-flavours so well known to water-works engineers
the excretion of substances which act in an algistatic or antibiotic fashion
the production of substances excreted into stream waters which enable migratory fish to ‘home’ on the stream and scene of their nativity
the formation of chemicals highly toxic to fish, birds and other vertebrate animals
the excretion of synthesized nitrogenous compounds by nitrogen-fixing blue-green algae.
All this material, cellular and excreted, is adding metabolic currency to our planet. Most of it supports active life and living organisms, and the excess — if it serves no other immediate purpose — contributes to the savings of reduced carbon in the world's bank balance of reserve biological energy. It is not intended to expand our treatment of any of the above effects at the present moment because this will be done later according to where each effect comes in the overall plan set out earlier; the intention is to spend some time discussing how much cell material and organic matter is produced by algae, because this will enable us to acquire some comprehension of the importance of this group of plants in the most fundamental aspect of plant life. Information will also be included on the chemical nature of compounds known to be excreted.
Much effort has been expended in an endeavour to estimate the total amount of organic matter produced by algae in the sea. About 71% of the earth's surface is occupied by saline seas, and therefore we can say that about 71% of the earth's surface is inhabited by a marine algal flora. Higher plants are restricted to the remaining 29% wherein they mostly occur on land or extend into very shallow brackish water. Returning to full-strength sea-water, we must realise that this is inhabited by algae as sole representatives of the photosynthetic section of the plant kingdom. The algae may be attached as seaweeds or free-floating as plankton; but according to Ryther (1960) 99% or over of the oceans are too deep to allow attached algae to grow and although some of the greatest concentrations of vegetation known are to be found in littoral algal stands, the littoral algae pale beside the planktonic as producers of organic matter.
To measure the total organic matter manufactured by planktonic algae is a difficult task and several attempts have been made using a number of different methods. As a group, the algae possess several different forms of chlorophyll — a pair of chlorophylls being found in each of the large divisions. But one chlorophyll page 96 of the pair is common to all divisions, namely, chlorophyll ‘a’. So methods of determining the concentration of phytoplankton have centred on estimating the amount of this particular form of chlorophyll. During the International Geophysical Year many determinations of chlorophyll ‘a’ were made as part of the oceanographic programme. Values for the upper illuminated layers of the Atlantic Ocean were found to fall within the range of 0.1-0.5 mgs./cubic metre of sea-water — with an average value of maybe 0.25 mgs. Ryther then calculates as follows:—
assuming the ratio of chlorophyll ‘a’ to dry weight (D.W.) of phytoplankton to be 1:100,
∴ the D.W. of plankton/sq. metre to a depth of 100 metres (a ‘round’ figure for the depth of ocean to which light will penetrate) would be 0.25 × 100 × 100/1000 gms. = 2.5 gms. on the average.
He adds a ‘generous 0.5 gms. to allow for the richer coastal waters and to include the benthic algae.’
This added to the 2.5 gms. for plankton gives us a figure of 3.0 gms.
∴ the oceans support an average standing crop of about 3.0 gms. D.W. of algal material/sq. metre of surface to a depth of 100 metres.
The saline areas of the world total 361 × 106 sq. kilometres of surface.
∴ the total figures for the D.W. of algal cellular material for the saline seas of the world are:
(361 × 106) × (3.0 × 106) gms./sq. kilometre. = 1.1 × 1015 gms. = 1.1 × 1012 kgs. = (1.1 × 1012) × 2.2/2240 tons = (1.07 × 109) tons D.W.
Although we might want to class this figure as a ‘guestimate’ (because of the large approximations made) it does represent a working assessment which gives some idea of the algal biomass of the world's oceans. This is often called the ‘standing crop’. The term is applied because the algal biomass is in essence a crop replete with food reserves of starch and oil. It is grazed by zooplankton and therefore acts as a starting point for many food chains.
It is interesting to set this figure alongside figures for land production. Ryther has also assembled this information. Various people have determined the relative proportions of the earth's land surface according to plant cover — these proportions are as follows:—page 97
|Wasteland (desert, arctic regions, mountains)||50%|
|Cultivated land, grasses, sedges, brush, etc.||20%|
We can neglect the first category because of its paucity of vegetation: so 50% of dry land contributes virtually nothing each year in terms of plant production. The contribution of the second category is worked out as 1.5 × 1013 kgs.; and that of the third category as 1.1 × 1015 kgs.
|Oceans||1.1 × 1012 kgs.|
|Crops, grasses||1.5 × 1013 kgs.|
|Forests||1.1 × 1015 kgs.|
Ryther then points out that the productive land plants, occupying one-eighth of the area inhabited by marine algae, maintain a biomass more than 1000 times greater.
|Ocean||3.6 × 1013 kgs./year.|
|Crops, grasses||3.0 × 1013 kgs./year.|
|Forests||2.2 × 1013 kgs./year.|
These figures represent net production i.e. the excess of a plant's production over its respiratory and reproductive requirements.
‘The interesting fact which emerges from all this is that the annual rate of organic production on land and in the sea is about the same despite the fact that the latter is accomplished by a flora less than one thousandth the biomass of the terrestrial vegetation. The explanation for this is that most of the bulk of land plants is in the form of slowly-growing, non-photosynthetic structural tissue’ (Ryther 1960). This gives us some idea of the marine algal contribution in terms of material retained within the cell.
Now let us consider the material excreted by the cell. If we take a sample of fresh or sea-water, it is possible to show by chemical means that it contains organic matter in true solution. This organic matter can be produced either by decomposition of plant and animal bodies or by direct excretion by living algae and animals as a normal function of their metabolism. Fogg (1959) page 98 has quoted a figure for the total amount of organic matter estimated in the oceans and it is of the order of 6.75 × 1012 tons i.e. 6,750,000,000,000 tons. No insignificant amount of soluble marine compost!
Commenting on the loss of organic matter from algal cells, the same author (1959) wrote — ‘It seems unlikely that the organization of any cell can be so perfect as to prevent entirely the escape of the soluble organic substances which it contains to the surrounding water, and evidence is accumulating which shows that algal cells do, in fact, ‘leak’ to an appreciable extent’. It is not difficult to give examples of algae which excrete appreciable amounts of organic matter. The first to mind is the green alga Spirogyra, the green scum that grows on the surface of fish-ponds — notable for the amount of slime on the outside of its filaments. In fact, the presence of slime is a rough and ready diagnostic feature of this particular alga. Among the brown seaweeds Macrocystis should be mentioned as a slime-producer, along with many of the red seaweeds. Some blue-greens are continuously shedding mucilage from the outside of the cell wall. In diatoms with a raphe, the cytoplasm is in contact with the ambient medium — there being only a thin membrane separating the cytoplasm from the aqueous environment.
When estimates of standing crop are made by determining chlorophyll ‘a’, the figure gives an index of the accumulation of cells only — the living biomass. We have no way of knowing how much organic matter has leaked out up to the time of sampling and will leak out during the life-time of the algal plankton. Put in another way, the ‘standing crop’ figure gives us a rough idea of intracellular organic matter but not the faintest clue to the amount of extracellular organic matter that has been lost up till and after the time of sampling. For fisheries purposes, the intracellular figure is the major one of significance; but for our purposes trying as we are to formulate some idea of the algae as producers of total organic matter, the extracellular figure would be necessary to know. As yet there seems no way of estimating this. All we can say is that some fraction of this 6.75 × 1012 tons of organic matter in the sea represents leakage and excretion from algal planktonic cells.
What is the chemical identity of these excreted compounds? Over the last decade many algae have been studied in the laboratory in pure culture; and with our improved analytical methods, we have been able to identify some of their metabolic end-products much more accurately than before. A lot of work has been done in this field and Fogg (1962) in summarizing this research has divided the extracellular products in the following way depending on their chemical nature:
lactic and succinic, under semi-aerobic conditions; by Prototheca zopfii.
acetic and lactic — anaerobic conditions; by Chlorella.
oxalic, tartaric, succinic; by Oscillatoria.
glycollic, oxalic and pyruvic; by Chlamydomonas.
One interesting reference is to the work of Tolbert and Zill (1956) who cultured Chlorella pyrenoidosa with a radioactive source of carbon and found that with only one minute of illumination this alga loses to the medium between 3 and 10% of the carbon it fixes. This ‘lost’ carbon appears in the form of glycollic acid.
Long-chain fatty acids are also produced.
(ii) Amino Acids and Peptides:
Certain blue-green algae liberate considerable amounts of nitrogenous extracellular products in the form of peptides and compounds containing amide-nitrogen: but free amino acids are generally found in small quantities only. One writer reported the presence of alanine, glutamic and aspartic acids in the culture fluid of Calothrix brevissima (Watanabe). Fogg (1959) quoted the amount of nitrogenous product excreted by Anabaena as 10% of the increase in normal nitrogen of the cell contents — and 20% or more when the culture fluid was deficient in iron.
The phenomenon of nitrogen excretion is not confined to the nitrogen-fixing blue-greens, because the same sort of thing occurs with non-nitrogen-fixing members of this group. Nor is the phenomenon confined to the blue-green algae. It has been reported for Chlorella pyrenoidosa, Chlamydomonas spp, Tribonema aequale, Navicula pelliculosa and even in the brown alga Ectocarpus confervoides.
(iii) Carbohydrates and Mucilages:
Oscillatoria splendida excretes polysaccharides into the medium; and Anabaena cylindrica loses to its growing medium a complex polysaccharide which consists of glucose, xylose, glucuronic acid, galactose, rhamnose and arabinose in the molar ratios of 5:4:4:1:1:1 (Fogg 1962). In the genus Chlamydomonas, 18 species were found by Lewin (1956) to produce some sort of polysaccharide — which in most cases consisted mainly of galactose and arabinose. As mentioned earlier, Spirogyra, Macrocystis and many algae excrete mucilage continuously.
(iv) Vitamins and Growth-Influencing Substances:
interference with the dark reaction in photosynthesis
reduction of oxygen consumption of bacteria
blockage of mitosis.
interference with the filtering action of Daphnia (Hartman)
the poisoning of fish and other animals — even possibly humans
the effect on the filter-feeding rate of oysters of ‘rhamnoside’ — a suspected extracellular metabolite of algae (Fogg 1962).
Referring more specifically to antibiotic substances in the popular meaning of this word, we find reports of Chlorella pyrenoidosa filtrates exhibiting antibacterial activity; and this has been shown due to oxidation products of unsaturated fatty acids. Oscillatoria splendida, Stichococcus bacillaris and Protosiphon botryoides are also reputed to produce antibacterial substances. Working with Phaeocystis pouchetii a common marine planktonic unicell, Sieburth put forward evidence that the thermolabile antibiotic which he found in the culture fluid was acrylic acid.
Harder in 1917 (quoted by Fogg 1962) showed that a species of Nostoc was able to use starch and other high molecular weight compounds as a source of carbon. This implies that an extracellular enzyme must be excreted to hydrolyse these sources of carbon down to smaller assimilable substances. Similarly, Nitzschia putrida is thought to do the same thing because Pringsheim showed that it is able to liquefy gelatine: in this case the enzyme must be proteolytic.
All this evidence demonstrates the excretion of chemicals under laboratory conditions; but does excretion occur in nature? Fogg conducted some experiments in Lake Windermere to determine the amount of carbon excreted by algae under natural conditions. He filtered samples of lake-water to which C14-bicarbonate had been added and determined the amount of C14-labelled organic matter in the filtrates. The experiments, carried out at times when diatoms were the most abundant component of the algal plankton, showed the apparent liberation as extracellular products of 3 to 90% of the total carbon fixed. The proportion of extracellular product page 101 tended to increase with depth, and the main form of excreted product seemed to be glycollate (Fogg 1962). Glycollic and other acids have been detected in sea-water by Koyama and Thompson; and Fogg and Nalewajko have estimated glycollic acid in concentrations of the order of 1 mg./litre (1 p.p.m.) in both sea-water and freshwater (Fogg 1962).
We also know that other substances as yet unidentified are produced by many freshwater algae. The water-works engineer is only too familiar with taints and off-flavours of water supplies. These effects can be produced by Synura, Dinobryon, Aphanizomenon, Fragillaria, Asterionella, Peridinium — to mention but a few. Virulent toxins which cause the death of higher animals such as fish, birds and cattle, are also produced by some algae in standing or stagnant freshwater. While the nature of these compounds is not known, as least by their effects we know they are produced. In some cases laboratory work has definitely shown that these toxins are excreted — as with Prymnesium parvum, Microcystis and Anabaena (Prescott): but for others there is the possibility that the toxin may be released only after cell disintegration.
Despite the examples quoted, it seems reasonable to say that of the 6.75 × 1012 tons of organic matter calculated to be in the seas the major part would be contributed through the decay of plant and animal body; but it must be remembered that an unknown proportion of this total is due to compounds excreted by the planktonic algae. Some of the more noticeable examples of effects of excreted metabolic products occur in freshwater and small bodies of standing water — and not in sea-water, with the exception of products released by red-tide organisms. So while the effects of these toxins and other substances may be startling, the amount of organic matter involved need not be very great.
Algae, planktonic and attached, occur in freshwater also; and in lakes, ponds, rivers and rills make their ceaseless contribution to the world's organic matter. But again it is impossible to assess the extent of this contribution. The sea is a reasonably uniform medium as a chemical environment (apart from the seasonal fluctuation of nitrogen, phosphorus, silicon and one or two trace elements) and extrapolation of analytical figures can be made on a world-wide basis. But the contribution of freshwaters cannot be assessed in quite the same way. There are numerous barriers to this.
Due to suspended colloidal matter, the depth to which light penetrates in many if not most freshwater areas would not be anywhere near the 100 metre figure of the open ocean areas. In fact it has been stated that light will penetrate only to about 10 to 15 metres in freshwater. Many areas in any case would not attain 100 metres in depth. So when we realise that the page 102 total area of freshwater lakes and rivers is roughly 0.7% of the total area of oceans and when we take into account this low light penetration in freshwater, it would appear that they are no match for the oceans in the production of cellular material. Yet it must not be forgotten that many freshwater unicellular algae including diatoms are very much larger in cell size than those of oceanic plankton and there are many multicellular algae in freshwater plankton which do not exist in the seas. Desmids for instance, a common member of freshwater plankton, do not occur in the seas at all.
The composition of freshwater varies enormously and differs with location and local climate, surrounding geological formations and types of land cover. Some of these bodies of water are ‘hard’ whilst others are ‘soft’ — with correspondingly different algal floras. Desmids for instance in England are associated with a high ratio of sodium + potassium to calcium + magnesium. Griffiths (1938) wrote that ‘water blooms are more common in large bodies of water especially in those on the newer geological formations; for this reason they are uncommon in the larger British lakes, most of which are situated on old geological areas. Water-blooming is very common on the rest of the great North European Plain of the Continent.’ The pH of water is another variable to be reckoned with. Again, rivers have an algal flora all the year round: due to constant flow, there can be no thermal stratification to act as a regulator of growth as found in large lakes and oceans.
Another problem associated with the freshwater habitat is the assessment of the production of extracellular organic matter. We would have no way of determining the amount of this commodity since now the organic matter figure could be grossly affected by what leaches from the land plus the debris and humus which comes from terrestial plant life on the banks of these fluviatile areas.
So, in the face of all these ‘if's, of's, and's and but's’ and conflicting variables, it appears we have to abandon all hope of arriving at figures for intra- and extracellular organic matter production of freshwater algae. Before closing however, we should mention that algae grow and proliferate on ice and in snow, and areas such as the Arctic and Antarctic despite their cold and inhospitable habitat are not without their algal contribution to the world's organic matter. Neither must we forget the world's mantle of soil since this supports an algal flora also. Any attempt at assessing the contribution of organic matter from algae in this medium is at present impossible — and may remain that way. Certain types of cultivated land such as paddy fields would have a high figure for both forms of algal organic matter; but many others such as the dry deserts would be wanting in it. However, page 103 in between these extremes there is a lot of soil harbouring an algal flora that is imperceptibly building up the level of carbon compounds.
Perhaps it is time now to attempt distillation of a few pure ideas from this crude liquor of facts and figures. The total area of the seas is much greater than the total area of freshwaters and it is unlikely that the algae of freshwaters produce as much organic matter in toto as those of marine habitats; but these freshwater ones do produce some — how much, is anybody's guess. As in the seas, there are extensive food-chains in freshwater environments which have their starting point with planktonic algae. So, alongside Ryther's figure for cellular organic matter production by marine algae, we are unable to put a similar figure either for freshwater or for soil algae; and we have no idea of the amounts of excreted organic matter of either freshwater, marine or soil algae.
In tabular form the situation may be summed up as follows:—
Intracellular organic matter — marine = 1.07 × 109 tons D.W.
" " " — freshwater = ?
" " " — soil = ?
Extracellular organic matter — marine = ?
" " " — freshwater = ?
" " " — soil = ?
Total algal contribution to the world's organic matter = 1.07 × 109 tons D.W. + ?????.
And this is where we have to leave the organic matter story at the present time — one ‘guestimate’ and a gaggle of question marks. Consequently we cannot even hazard a guess for the total algal contribution to the world's organic matter production. But having in mind the dictum of The Ancient Mariner — ‘Water, water, every where, …’ and remembering that the presence of water in its varying forms is almost synonymous with the presence of algae, we can say without question that the algae would undoubtedly be the greatest contributors to the world's lay-by of available biological energy in the form of organic matter.
However, there is one further point to bring out before closing. On land, our organic matter production is subject to great inroads by parasites — we merely harvest what the birds, the rodents, the insects, the nematodes, the fungi, the bacteria, the viruses, the weeds and the climate leave us. Insects alone are said by some to ravage a third of our crops. On land, nothing living (except bacteria) seems free from insect attack — they have invaded every ecological niche and preyed on every form of life. The only niche that has been hostile enough to prevent colonization is the sea. While the marine algae have not escaped the ravages page 104 of bacteria and fungi (and possibly viruses), at least they are not devastated by insects. Presumably therefore, the wastage of the sea's annual organic matter production in terms of cellular material could be extremely low; but unfortunately this cannot be said for the land's production — a major point in favour of the algae.
Description of DinobryonChrysophytes, loricate, forming arbusculate colonies (rarely solitary), planktonic and free-swimming (rarely sessile); lorica cylindrical, vase- or funnel-shaped and often with a slightly broadened mouth; lorica consisting primarily or entirely of cellulose and protein, formed by successive loops of fibrils extruded during rotation of the cell; cells Ochromonas-like, attached to base of lorica by a thin protoplasmic strand; 2 unequal flagella; chloroplast(s) 1 (bilobed) or 2; eyespot large, associated with base of short flagellum; 1-2 contractile vacuoles, anterior, median or posterior; chrysolaminaran vacuole large, posterior; nutrition phototrophic and phagotrophic; reproduction by longitudinal cell division, after which one daughter cell swims away or often moves to mouth of parental lorica and forms a new lorica, whereas the other daughter cell occupies the parental lorica; stomatocysts formed asexually or sexually; several species wide-spread and very common in freshwater lakes and ponds; blooms sometimes causing odor problems; some species also occurring in estuaries and coastal marine waters including Antarctica.