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Tuatara aims to stimulate and widen interest in the natural sciences in New Zealand, by publishing articles which, (a) review recent advances of broad interest; or (b), give clear, illustrated, and readily understood keys to the identification of New Zealand plants and animals; or (c), relate New Zealand biological problems to a broader Pacific or Southern Hemisphere context. Authors are asked to explain any special terminology required by their topic. Address for contributions: Editor of Tuatara, c/o Victoria University of Wellington, Box 196, Wellington, New Zealand. Enquiries about subscriptions should be sent to: Business Manager of Tuatara, c/o Victoria University of Wellington, Box 196, Wellington, New Zealand.
(This issue edited by
is the journal of the Biological Society, Victoria University of Wellington, New Zealand and is published three times a year. Joint Editors:
Throughout the History of Man, disease has frequently played a dominant role. Plague, smallpox, malaria, tuberculosis, typhoid, cholera, diphtheria — these are only a few of the killing, crippling diseases to which man is subject. The mass effects of some epidemics of disease can be spectacular. During the Second World War, malaria caused five times as many casualties in the Pacific areas as did the actual fighting (Chandler, 1955); in 1916, an epidemic of malaria actually stopped a major war in Macedonia, no doubt to the great annoyance of the commanding generals (Lapage, 1950). The black plague killed 300,000 people in Naples in 1656, and caused an estimated 100,000,000 deaths in the sixth century. A macabre reference to plague is made in at least one nursery rhyme — ‘Ring-a-ring-a-rosy’ refers to the inflamed rosette on the chest which is one of the first symptoms of the plague, ‘a pocketful of posies’ refers to the aromatic herbs which were sniffed at intervals in the pious and totally misplaced hope that the action would keep away the plague, ‘a-tisket, a-tasket’ refers to the sneezing which is symptomatic of pneumonic plague, and ‘all fall down’ is self-explanatory.
Naturally, many different treatments were used in attempts to control and cure these diseases — mostly without conspicuous success. Nevertheless, long before any real insight into the nature of disease existed, some infectious diseases could be controlled by immunisation.
The real breakthrough came in the treatment of smallpox. It had been clear very early that people who had had the disease, and survived, very rarely contracted it again. With this observation in mind, material was taken from the vesicles of mild cases of smallpox and inoculated into people who had not had the disease, in the hope (with fingers crossed) that they would get only a mild local infection, and so gain immunity against the frightful generalised form of the disease which so often resulted in shocking disfigurement and widespread death.
The method of inoculation varied in different parts of the world. In India, children were wrapped in the clothing of smallpox patients,
“…‘my face is my fortune, sire’, she said.”
And her face was her fortune, simply because it was not pitted and scarred by smallpox. Jenner checked the observation in a very brief series of experiments, probably the first set investigation in experimental immunology. However, even though these experiments marked a major turning point in the treatment of disease, it is well to remember that the experiments were very scrappily done. In fact, the editors of the Philosophical Transactions of the Royal Society considered that there was not enough evidence for Jenner's sweeping claims, and refused to publish his account. Jenner therefore published his own account, became famous, and spent the rest of his life in controversies over priority and rewards (Burnet, 1963).
The next major contribution was made by Louis Pasteur, who set out to develop effective vaccines against a variety of diseases. His first breakthrough came in the treatment he devised for chicken cholera. The bacterium which causes the disease grows readily in a simple chicken broth, and Pasteur found that the injection of very small doses of pure culture killed off unprotected chickens in very short order. However, when chickens were inoculated from very old cultures which had been allowed to stand untouched for some months, the birds showed very mild symptoms of the disease and then recovered. They were then found to be immune to the virulent culture. Pasteur spent the rest of his career working out similar methods for ‘attenuation’ of other bacteria and viruses, and this approach has continued to yield very satisfactory results up to the present day.
It is clear that this approach is largely one of trial and error. While is has yielded enormous benefits in the treatment of disease,
The study of the way in which the body responds to disease has gathered momentum over the last decade to become one of the most active areas of science today. Scientists all over the world are slowly piecing together the jigsaw puzzle of the immune response, with varying degrees of success — the outline is now more or less complete, but many of the pieces are still missing, other pieces show an infuriating obstinacy in their refusal to fit into the pattern at all, and still others insist on fitting into all the wrong places. However, the gaps are slowly filling in, and we know far more about the immune response than we did even five years ago. It is now clear that the basis of the immune response to disease, with all its ramifications and complexities, lies in protein chemistry, and in particular in the chemistry of the antigen-antibody reaction.
A vertebrate animal is a highly complex entity, consisting as it does of a staggeringly diverse array of enormous molecules, each one tailor-made to carry out a particular function. All these different molecules are intricately dovetailed and integrated into an extremely complex and yet dynamically stable system. It seems obvious that the more complex the system, the greater the number of weak points at which it may be attacked by poisons, by viruses, and by bacteria. Of course, these assaults on the integrity of the body cannot be allowed to go unchecked, and the resultant policing of the body is the responsibility of a very capable immune response system, which has several major functions.
First, it must remove foreign particles, such as dead bacteria, fragments of disintegrated cells, and any small pieces of unwanted miscellaneous flotsam and jetsam found in the body.
Secondly, it must be capable of detecting molecules, and in particular protein molecules, which are foreign to the body. These foreign materials are called ‘antigens’ — the word antigen denotes a substance which, when introduced into the tissues of an animal, will cause the production of antibody molecules which neutralise it. Not all foreign proteins are antigens; gelatine, for example, does not trigger off production of antibody. Conversely, not all antigens are proteins; some large polysaccharides have antigenic effects. The important point here is that invading pathogens carry proteins, foreign
Third, the body must respond to the presence of an antigen by manufacturing an antibody which will deal with that antigen specifically, and with that antigen alone. One of the most characteristic features of the antigen-antibody reaction is the very high degree of specificity involved; for every antigen, there is one, and only one, corresponding antibody type, which is incapable of neutralising any other antigen.
Fourth, after the antigen has been introduced, detected, recognised, and dealt with, the body must retain an immunological memory of the whole ghastly experience, so that if a similar antigen appears in the body at a later date, the challenge can be met much more rapidly and effectively.
Where invasion of the body by a pathogenic organism is concerned, the reaction between an antigen and the antibody which is manufactured to neutralise it is the core of the immune response. This reaction has two important characteristics; first, it is highly specific, and second, it is quantitative — a given amount of antibody will neutralise a given amount of antigen.
One question now arises — just how does an antibody molecule react with an antigen to neutralise it?
At this point it is profitable to compare antibodies with enzymes. The activity of an enzyme is determined by its ‘active site’, an area on the surface of the protein molecule which has a definite configuration, and which is designed to ‘lock on’ to a complementary active site on the surface of the molecule with which the enzyme reacts (the substrate molecule). These active sites may be very small, with only two or three amino acids involved out of the many hundreds which make up the molecule, but it is on the precise shape of the active site that the activity of the enzyme depends. Every protein consists of a chain or chains of amino acids, arranged in a definite, predetermined order. The sequence of amino acids in the chain determines the shape of the molecule, and the shape of the molecule determines its properties. The two or three amino acids which form the active site need not be sequential along the chain. For example, in the enzyme alpha—chymotrypsin, the three amino acids involved in the active site are serine, methionine, and histidine. The histidine is on one chain, while the methionine and serine are on another. However, in three-dimnsional orientation the three are close together; they are brought together by folding and coiling of the protein molecule so that they form an active site on its surface (Koshland, 1963).
It appears that the active sites of antibodies are rigidly preformed in much the same way, and operate in much the same way. Antigen molecules also owe their activity to similar active sites on their surfaces. It is these active sites, otherwise known as ‘haptens’ or ‘antigenic determinants’, which the antibody molecule is manufactured to deal with. A hapten, or antigenic determinant group, can be defined as that specific chemical grouping to which a single antibody site conforms and with which it reacts. It is obvious here that an active site which consists of only two or three amino acids on the surface of an antibody can combine only with a determinant group on the antigen which is much the same size and of exactly complementary configuration.
When the nature of these combining sites is taken into account, the specificity of the antigen-antibody reaction becames understandable. Obviously a very wide variety of different hapten configurations is possible, and for each configuration there is only one possible complementary shape for the active site of the antibody. It thus follows that an antibody which is manufactured to neutralise a specific antigenic determinant cannot have any effect on a different antigen.
This concept also explains the quantitative aspect of the antigen-antibody reaction. One antibody active site will neutralise one antigenic determinant — as long as an antigenic deteminant occupies an antibody site, no other antigenic determinant can occupy the same site.
It must always be remembered that the active sites are very small areas compared with the molecule as a whole. Nevertheless, it is these minute active sites which enable the antibody molecule to grasp, fasten onto, bind, and neutralise the corresponding antigen.
The sizes of these active sites have been estimated, and they are minute. They range from a minimum size of 100 Angstrom2 to a maximum size of 2000 Angstrom2 (Day, 1966). (To give some idea of the size of an Angstrom unit — facial hair grows at the rate of about 30 Angstrom units per second).
When an antigen is detected, and antibody production starts, the first antibody molecules produced are fairly large. During the early stages of the response the animal produces an antibody molecule with a molecular weight around the 1 million mark, but after a while it switches over to production of a lighter version of the same antibody with a molecular weight of only 150,000. The heavy and light versions of the antibody are respectively referred to as 19S and 7S gamma globulin; the ‘gamma globulin’ refers to that fraction of the blood proteins in which antibodies are found, and the S refers to Svedburg units, which indicate the rate of sedimentation of a
The general structure of the antibody molecule has been determined in some animals. For example, rabbit antibody molecules can be broken down into four parts—four straight amino acid chains which are linked together in the complete molecule by disulphide bonds and hydrogen bonds. These chains come in two pairs — a pair of long, heavy chains each of molecular weight 50,000, and a pair of shorter chains, each of molecular weight 25,000. The two heavy ‘A’ chains are identical, and the two lighter ‘B’ chains also match each other. The A chains lie alongside each other, and the B chains flank the paired A chains on either side at one end of the molecule. Each antibody molecule has two identical active sites, carried at the end of the molecule which has the two B chains. This can be inferred from the finding that it is possible to break the A chains halfway along their length with suitable enzymes; this gives two fragments, one of which is inactive, while the other (which carries the two B chains) retains its activity unimpaired. When this fragment is split down the middle by breaking a single disulphide bond holding the A chains together, the resulting two fragments (each consisting of a B chain and half an A chain) can each neutralise on antigen molecule (Nisonoff and Thorbecke, 1964).
To sum up this far, then, the following sequence of events applies. A pathogen which carries antigen molecules enters the body. The antigens are detected by the body's immune response system, and antibody molecules specific for that particular antigen are produced. The antibody molecule carries two identical active sites, which may be contributed to by both the A and B chains of the molecule. Each of these active sites is capable of attaching itself to the antigenic hapten, or determinant group, and thus neutralising the antigen. This action is the core of the immune response, and it is now time to see how it is accomplished.
The arterial blood pressure in mammals is much higher than it is in the earlier, superseded models such as the amphibians. This high blood pressure enables the animal to operate much more efficiently, and confers major advantages, such as more efficient respiration, more economical elimination of waste products, and so on. Nevertheless, the increase in arterial blood pressure does introduce some important problems, which have to be solved. Due to the high pressure of blood in the arteries, a certain amount of fluid, together with some plasma proteins, leaks out through the capillary walls into the body tissues. Obviously, this fluid must be returned to the bloodstream, or the tissues will become flooded and
At intervals along the course of these lymphatic vessels, there are well-defined structures called lymph nodes. The fluid in the lymphatic vessels passes through the nodes on its way to the thoracic duct.
These lymph nodes are intimately concerned with the immune response. However, it is important to remember that the immune response system operates on the cellular level, rather than on the organ or organ system level. The cells which mediate the immune response show an extraordinary degree of flexibility, and many are very mobile. A number of different cell types wander through the blood and the body tissues, while others stay anchored in the lymph nodes and emerge into the blood stream only as the result of unusual pathological conditions.
In human blood, two nucleated cell types, or leucocytes, are predominant. These leucocytes are, of course, heavily outnumbered by the enucleate red blood cells, or erythrocytes, but these cells do not enter into immune reactions. By far the most numerous leucocyte type in human blood is the neutrophil — the nucleus in this cell is an elongate, bent or twisted body with several lobes, and the cytoplasm contains a large number of small granules. These cells are phagocytic; their primary function appears to be the engulfing and subsequent destruction of any foreign particles which appear in the blood or tissues. The other numerous cell type (20-25% of the blood leucocytes in man) is the lymphocyte. The lymphocyte is a spherical cell, with a large, nearly spherical nucleus surrounded by a thin rim of cytoplasm; the cytoplasm normally contains no granules. It is this cell type which has been attracting most attention over the last few years, as far as the immune response in concerned. Other leucocytes are found in the blood, but these are not numerous and their functions are not yet clear.
Situated in the lymph nodes are cells which look like larger versions of the lymphocyte. These ‘plasma cells’ have a greater amount of cytoplasm than do the lymphocytes, and this cytoplasm is well endowed with endoplasmic reticulum. This indicates that these cells are well equipped to synthesise large quantities of protein. Plasma calls almost never leave the lymph nodes. The lymphocytes, on the other hand, circulate freely around the body, through the
One striking feature of the lymphocyte is that it appears to have a very long lite span — a life span of 10 years has been established for it, and it could well be even longer (Buckton and Pike, 1964). This indicates that the lymphocyte is in a resting state in its normal condition.
Keeping this background in mind, we can now look at the typical course of events following an antigenic challenge.
In any response by a mammal to an antigenic challenge, there are a number of well defined stages, each marked by easily-recognisable changes in the lymphatic system at the cellular level. The first stage of the response centres around recognition of antigen. This appears to be the responsibility of the lymphocytes, but there is also strong evidence that a cell population resident in the lymph nodes is also capable of recognising antigen. When an antigen is injected subcutaneously, the first sign of a response by the host animal is an almost immediate and startling drop in the number of lymphocytes leaving the lymph node which drains the infected area. The lymphocytes detect the antigen, move to the lymph node, and remain there instead of passing through (Hall and Morris, 1965). The cell count in the lymph leaving the node may remain low for as long as 12 to 24 hours, before rising again. The mechanism which causes this unusual lymphocyte behaviour pattern is not yet certain, but it certainly has something to do with antigen recognition. The lymphocyte is a resting cell, inactive but pregnant with celestial fire, and contact with antigen stimulates it to give birth to its full potential. This process of antigen recognition applies also to some of the cells in the lymph node, and in allied structures such as the thymus gland, and these cells show significant changes in the nucleus which are associated with gene activation (Black and Ansley, 1965; Agrell and Molander, 1969). Lymphocytes are also capable of making the same type of response to an external stimulus (Burton, 1968). These changes are first detectable in the histone protein of the nucleus, and this is significant because it is highly likely that the function of histone is to mask those parts of the genetic code which are not required by a particular cell. Obviously, if a cell is going to undergo a marked change in behaviour, genetic information must be made available to it to control the change. Significantly, this change in histone protein is promptly followed by increased RNA synthesis, increased protein synthesis, and consequent growth of the cell leading ultimately to division.
Just how an antigen causes these cellular changes is not yet known. Nevertheless, antigen recognition is a recognisable
The next phase in the immune response is one of lymphocyte recruitment. About 24 hours after the antigen makes its first contact with the lymph node, the cell content of the lymph begins to increase. This increase enables the body to bring an enormous number of immunologically competent cells to bear on the antigenic concentration.
This phase of lymphocyte recruitment paves the way for the third stage. At the end of the first 72 hours, the plasma cells in the lymph nodes go into a phase of very active growth and division. A lymph node at this stage is a seething mass of actively dividing cells.
Antibody synthesis on a large scale commences at about this time. Most of the antibody is produced by the plasma cells resident in the lymph nodes — cells which are well equipped with endoplasmic reticulum, and which ordinarily remain in the lymph nodes and never enter the blood stream.
In the lymph, however, a population of cells appears which is capable of synthesising antibody. These are unlike the plasma cells in that they do not have a well defined endoplasmic reticulum (Cunningham, Smith and Mercer. 1966). At the height of the immune response there may be as many as 20,000,000 of these antibody-forming cells being carried away in the lymph every hour from the node where they were formed. However, it may well be that antibody manufacture is not their most important function. It appears that these cells are able to initiate immune reactions in other lymph nodes in the absence of antigen. This mechanism allows all the lymph nodes in the body to become involved in an immune response, thus enormously amplifying the response itself (Hall, Morris, Moreno, and Bessis, 1967).
By this time, any self-respecting pathogen is beginning to wonder if it has bitten off more than it can chew. In fact, as a result of all this frenzied activity on the part of the lymphatic system, the antigenic challenge may well be beaten off. However, this is by no means the end of the story. One of the most important properties of the immune response system is its capacity to respond to a second attack of a particular antigen much more rapidly and effectively than it responded to it the first time. It is clear that some memory of the first, or primary, response is retained by the lymphoid cells after the antigenic challenge is over; the presence of this immuno-logical memory allows the response to a second challenge by the same antigen to be rapid, massive, and effective. It is this property of the immune response which makes immunisation so successful. The vaccine is a very weakened version of the real thing, and it can easily be dealt with by the relatively weak primary immune response. Consequently, when the immunised body is exposed to the full-blooded
The nature of this immunological memory is not at all clear, but it appears to be twofold. There is plenty of evidence to show that the circulating small lymphocyte is responsible for a major part of this immunological memory, but there appears to be a sedentary population which has this ability as well. The nature of this ‘residential’ memory is not certain, but for some time after a primary challenge, a stimulated node can respond more vigorously and rapidly than one where antigen had not previously been encountered. (Morris, 1968).
There are, of course, a number of problems which have not yet been solved. The precise relationship between lymphocytes and plasma cells is not known, although it seems likely that the lymphocytes, once the antigen is recognised, pass relevant information to the plasma cells. The precise nature of this information transfer is not known, but there is some evidence that RNA is involved (Hashem, 1965). In any case, it seems very likely that antigen, as such, never comes in contact with the antibody-forming cells at all, and the circulating small lymphocytes may act in an intermediary role.
There are other problems as well. So far in this article, only the response to pathogenic organisms has been discussed. However, immune reactions of other types do occur, one being graft rejection. In this reaction, antibody synthesis (if it occurs) appears incidental to some cellular effector mechanism, although all the cellular steps listed above take place in the same way.
Nevertheless, our present understanding of the workings of the lymphatic system has allowed us to make some advances in medical practice which were not possible ten years ago. Knowledge of the steps involved in the immune response, and of the cells which mediate the response, is vitally important in transplant surgery. A transplanted organ is obviously foreign protein introduced on a massive scale, and the body deals with it accordingly. As far as the surgeon is concerned (not to mention the patient) the process of rejection which results must be stopped or minimised. This can be done, at the moment, in two ways.
First, accurate tissue matching is important. If a donor can be found whose proteins match those of the recipient fairly closely, the risk of rejection is reduced. This has proved very successful in kidney transplantation, so much so that now 90% of transplanted kidneys survive at least five years, and the figures are improving all the time.
Second, it is possible to impair the immune response system by injecting antilymphocyte serum (A.L.S.). This serum is produced by injecting human lymphocytes into a horse, or similar animal,
However, there are major disadvantages involved in the use of this technique.
First, it reduces resistance to disease, in particular viral diseases and those diseases caused by the smaller bacteria. However, resistance to disease is not lost altogether, as the residential immunological memory is still intact.
Second, the technique is not completely effective — some lymphocytes survive, and they commence rejection of the transplant.
Third, the ALS is not pure, and some side effects show up — not only the lymphocytes are attacked by ALS.
Fourth, this type of treatment appears to make the lymphatic system more susceptible to cancers after a time.
It seems possible, however, that some progress will be made in another direction. It is possible to induce a degree of tolerance to introduced foreign materials. The combined use of induced tolerance, ALS, and accurate tissue typing probably holds out the best hope for successful long term organ transplantation in the foreseeable future.
Pending a most desirable monographic revision of the Stictaceae of the world, an interim key has been prepared with supplementary notes to facilitate recognition of the species indigenous to New Zealand.
Stictaceae is a large and well defined family of foliose lichens widely distributed in most temperate and tropical countries but attaining maximum development in New Zealand where approximately eighty species are currently recognised though several are admittedly of doubtful validity. To this family belong many of the largest known lichens with a thallus over a square foot in area. As in the Peltigeraceae and Pannariaceae, some of the species contain a bluegreen phycobiont (alga) and others a green phycobiont. The most distinctive feature of the Stictaceae is the presence on the lower surface of most species of either cyphellae or pseudocyphellae, the former being round, concave white or brownish pits or depressions lined with non-gelatinized hyphae and bordered by a distinct rim while pseudocyphellae are minute, unbordered pores filled with loose or protruding hyphae. The lower surface is usually more or less tomentose, whereas in Parmeliae of comparable size and aspect the tomentum is replaced by warts or long, black rhizines.
In the genus Lobaria cyphellae and pseudocyphellae are lacking. Some botanists place all other species in the genus Sticta, but others place pseudocyphellate species in the genus Pseudocyphellaria. Until recently those species with a blue-greeen phycobiont were placed in Lobarina, Cyanosticta, and Stictina but as lichens are now regarded as lichenized fungi and classified as such, the algae now play no part in the taxonomy of lichen genera and these genera are merged in Lobaria, Pseudocyphellaria, and Sticta respectively..
New Zealand Stictae at maturity range from a width of 3 to 5 cm. to as much as 35 cm. With few exceptions the species are highly plastic, and the resulting polymorphism makes the delimitation of some species very difficult. Some of the earlier ‘species’, apparently autonomous, were later found to be isolated plants in a more or less continuous range of forms belonging to another highly plastic species, and it appears probable that a further reduction in the number of valid or autonomous species will result from any future monographic study.
Though Colenso, Lyall, Sinclair, Helms, and Knight forwarded copious suites of specimens to overseas botanists for determination,
Stictaceae of the world numbering over 400 species. Some work towards this objective had been undertaken by P. James and J. Murray, but the accidental death of Dr. Murray in a motoring accident has led to some temporary postponement of the project. The inadequate descriptions of some of the ‘species novae’ by their authors, has made their more adequate description most desirable, and in many cases a reassessment of their taxonomic status. It has to be admitted that many descriptions fail to adequately portray the distinctive features that distinguish one species from another.
Illustrative of the difficulties encountered in the taxonomy of the Stictaceae Sir Pseudocyphellaria carpoloma, P. cellulifera, P. colensoi, P. flavicans, P. foveolata, P. impressa and P. richardii were not autonomous species but variants of one and the same species. He also regarded Sticta coriacea, P. glabra, and P. linearis as synonyms.
Similarly Babington regarded P. billardieri, P. cellulifera, P. foveolata, P. linearis and P. impressa as mere modifications of P. fossulata, and Nylander held a similar opinion. In his “Lichenes Novae Zealandiae” of 1941, Zahlbruckner relegated the following species to synonymy:—P. dissimilis (= P. cinnamomea); P. expansa (= P. glaucolurida); P. multifida (= P. psilophylla); P. parvula (= P lacera); P. physciospora (= P. impressa); and P. subvariabilis (= P. polyschista). He also (I think correctly) restored P. aurigera and P. xantholoma to their original status as varieties of P. mougeostiana. As access to original and type specimens, almost all of which are held overseas, has not been possible, the following tentative key has been based on the published descriptions (not always adequate), on an examination of (presumably) correctly named specimens in local herbaria, and on some acquaintance with most of the species in their natural environment.
In 1949, Dr. ‘Tuatara’ (vol. 2, pp. 97-101) a useful key to the more common species of Stictaceae indigenous to New Zealand; but, as almost half the recognised species were omitted its limitations
Most indigenous species of Sticta have white or brownish cyphellae, while in Pseudocyphellaria the pseudocyphellae with few exceptions are yellow or white. Yellow pseudocyphellae may, however, be associated with either a yellow or a white medulla. Cephalodia are present in many species but only in such as have a green phycobiont. As a rule they are small, more or less globular bodies on or partially immersed in the thallus and containing blue-green algae.
The Stictae are variously found on bark, twigs, rock, moss or soil; most occur sometimes as epiphytes, though a number — e.g. P. cinnamomea, P. fragillima, P. crocea, P. mougeotiana — clearly prefer a rock substrate. At subalpine levels many species normally epiphytic or epilithic may be observed growing on soil, commonly in grassland. The following have been so observed by Thomson, Galloway, and the writer — Lobaria laetevirens, Sticta ftlix, S. limbata, Pesudocyphellaria carpoloma, P. aurata, P. crocea, P. delisea, P. durvillei, P. endochrysea, P. flavicans, P. foveolata, P. freycinetii, P. gilva, P. lechleri and P. tnougeotiana; while Thomson lists twenty three species as having been collected by him on a rock substrate.
Most species are photophilous and avoid deep shade. In the dense forests of Westland and Fiordland, the commonest species on the trunks are P. glabra, P. homeophylla, P. billardieri, Sticta filix, and S. latifrons. The greatest concentration of species occurs in areas with an annual rainfall of not less than 30 to 40 inches evenly distributed over the year. Thus while fifty species are known from the environs of Dunedin with an annual rainfall of over thirty inches, only one species (P. mougeotiana) is found in parts of Central Otago where the annual rainfall is under twenty inches.
Among species recorded from New Zealand are a number wrongly determined, as S. orygmaea for P. coronata, S. filicina for S. filix, S. quercizans for S. weigelii, Lobaria herbacea for L. laetevirens, L. amplissima for L. laciniata. For lack of adequate detail the species known as Sticta elaphocera and Pseudocyphellaria dictyophora have not been included in the following key. The former has been regarded as a variety of Sticta coriacea and like it has a hairy margin. It bears some resemblance to S. damaecornis. The latter is a very small species found by Colenso near Napier, only about an inch in width, minutely isidiate, and possessing a blue-green phycobiont. Both plants lacked soredia, cyphellae and pseudocyphellae as well as apothecia.
Other recorded species omitted from the key include Pseudocyphellaria flotowiana, P. coronatoides, P. insculpta, P. linearis, and P. physciospora for the following reasons. According to James, who has examined part of the type collection, P. flotowiana is identical with P. billardieri. P. linearis and P. physciospora are regarded as
P. fossulata, the former distinguished solely by the smaller dimensions and less foveolate surface, and the latter by the more physcioid characters of the spores. The writer has failed to locate the description of P. coronatoides, the determination given to a plant growing on Leptospermum at Boulder Hill in Otago and secured by J. Scott Thomson. P. insculpta is a dubious inhabitant of New Zealand which scarcely differs from P. cinnamomea save in its dissected margins. Because the species most commonly labelled Lobaria glomulifera and L. montagnei are sometimes pseudocyphellate, they have been placed as species of Pseudocyphellaria, notwithstanding their parmelioid apothecia; and as already indicated P. aurigera and P. xantholoma are deemed mere varieties of P. mougeotiana.
Until some species have been more accurately defined, it is doubtful if any key can adequately distinguish the allied ‘species’ (?) in several groups of Stictae; hence when using the key that follows due allowance must be made for the plasticity of many species and for the resultant polymorphism which applies to almost every feature of the thallus; its colour, form, and size; its smoothness, rugosity or foveolation; the density (or absence) of tomentum on the lower surface; the degree of dissection of the thallus or thallus margin; or the concentration of isidia, soredia, cephalodia, cyphellae, pseudocyphellae, apothecia, or spermagonia. Thus it may be anticipated that two specimens of the same species may well present a very different aspect.
(L. = Lobaria p. = Pseudocyphellaria S. = Sticta)
P. colensoi
P. coronata
P. aurata
P. durvillei
P. endochrysea
P. flavicans
P. glaucolurida
P. grandis
P. hirta
P. rubella
P. astictina
P. aurata
P. carpoloma
P. colensoi
P. coronata
P. crocata
P. durvillei
P. endochrysea
P. expansa
P. flavicans
P. gilva
P. glaucolurida
P. grandis
P. granulata
P. hirsuta
P. hirta
P. impressa
P. lechleri
P. lorifera
P. mougeotiana
P. multifida
P. obvoluta
P. rubella
S. fuliginosa
S. weigelii
P. chloroleuca
P. delisea
P. dissimilis (sometimes)
P. diversa
P. durvillei
P. flavicans
P. freycinetii
P. granulata
P. hirta
P. hookeri
P. polyschista
P. psilophylla
S. efflorescens
S. limbata
P. argyracea
P. aurata
P. cellulifera
P. colensoi
P. condensata
P. crocata
P. dozyana
P. granulata
P. intricata
P. mougeotiana
P. rubella
P. thouarsii
L. scrobiculata
*S. coriacea
*S. subcoriacea
*P. expansa
*P. grandis
P. hirsuta
P. muelleriana
P. obvoluta
P. rubella
* = submarginal only
S. fuliginosa
P. billardieri
P. carpoloma
P. cellulifera
P. colensoi
P. coronata
P. dozyana
P. durvillei
P. fossulata
P. foveolata
P. freycinetii
P. glaucolurida
P. grandis
P. homeophylla
P. hookeri
P. impressa
P. lorifera
P. richardii
L. retigera
L. scrobiculata
P. carpoloma
P. cinnamomea
P. condensata
P. crocata
P. elatior
P. expansa
P. fossulata
P. faveolata
P. glaucolurida
P. hookeri
P. impressa
P. lechleri
P. montagnei
P. muelleriana
P. richardii
The Term Flatfishes is reserved for a group of rather specialised fishes characterised by an asymmetrical body, flattened from side to side (i.e. compressed) with both eyes situated on one side of the head. They are one of the most successful and beautifully adapted of all the groups of bottom-living fishes. All flatfishes lie on one side of the body, i.e. the blind side, which is usually colourless, or spotted black or yellow, or sometimes only a little lighter in colour than the ocular side.
It is important to note that elasmobranchs such as skates and rays which are flattened from above downwards (i.e. depressed) and lie on their abdomen are not usually termed Flatfishes. Teleostean fishes such as John Dory or the Oarfish, which are compressed but swim vertically, are similarly not included in the order.
Except for their asymmetry Flatfishes are related to Perch-like fishes. For some days after hatching a young Flatfish, outwardly, appears to be bilaterally symmetrical, with an eye on each side of the head, and swims in a normal fish-like manner. However, it has been demonstrated, by the study of the optic nerve of larvae, that Flatfishes are never symmetrical (Parker, 1903). In bony fishes the optic chiasma is dimorphic, i.e., the right optic nerve crosses above the left as often as the left crosses above the right. In most Flatfishes the chiasma is monomorphic, i.e., the optic nerve of the migrating eye is dorsal and this condition is established even before the larva is hatched. After hatching, the chondrocranium of the larva undergoes torsion and one eye begins its slow migration to the opposite side of the head, and some 6-10 weeks after hatching takes up its final position. This eye migration accomplished, the young Flatfish sinks to the bottom and lies on its blind side. The mouth retains its original position although the upper and lower jaws on the blind side together with the teeth, show a greater development than those of the ocular side and thus it is not necessary for the fish to adopt a vertical position for feeding. Feeding in adult Flatfishes is mainly confined to the hours of darkness, when they swim about looking for marine worms and other small bottom-dwelling animals. Because of their movements during darkness they are more easily taken in trawl nets at that time than during hours of daylight when they almost bury themselves in sand or mud.
Flatfishes are masters of colour change and camouflage, and in this respect they are said to exceed the ability of the well-known
Flatfishes are found in most seas and are an important source of food. Most of them are small but some attain a considerable size, e.g., the Halibut (Hippoglossus hippoglossus, Family Pleuronectidae) of the Northern Atlantic grows to a length of 9 feet and may weigh 500 pounds.
Although the undulations with which they make their way through water would appear ineffective, Flatfishes are able swimmers. A New Zealand Black Flounder (Rhombosolea retiaria) tagged at Lake Ellesmere was taken six months later near Foveaux Strait, a distance of some 250 miles.
Eleven species of Flatfishes are known from New Zealand waters. All are entirely marine, except R. retiaria, which frequents estuaries and enters fresh waters. Two species, Arnoglossus scapha and Lophonectes gallus, belong to the sinistral family Bothidae in which the eyes are on the left side. Lophonectes gallus also occurs in south-eastern Australia and Tasmania. The remaining nine species belong to the sub-family Rhombosoleinae of the dextral (eyes on right side) Family Pleuronectidae. Subfamily Rhombosoleinae, which is given family status by some ichthyologists (Chabanaud, 1946), contains eight genera and fifteen species. This distribution of the Rhombosoleinae is confined almost entirely to the Australasian region. Eight species occur in Australian waters, nine in New Zealand, with only two species, Azygopus pinnifasciatus and R. tapirina, shared by Australia and New Zealand. However, one genus (one species) Oncopterus darwinii is found only along the south-eastern coast of South America. This distribution of the subfamily is an interesting one from the point of view of the dispersal mechanism involved. Fell (1962) presented a theory, drawing on evidence from several genera of circumpolar or partly circumpolar echinoderms, which suggested that larval echinoderms, other epiplanktons, and sea weeds drifted from west to east because of the west wind drift. Thus Australia stands as a ‘donor’ to New Zealand and similarly New Zealand to the islands east of it and these in turn to South America. Thus one can speculate that larval Rhombosoleinae drifted westward in a circumpolar path from its ‘home’ in the Australasian region, under the influence of the west wind drift.
Throughout New Zealand, many fish may be known by several different common names. For example, Rhombosolea plebeia is
Colistium nudipinnis and Colistium guntheri, others call both of them ‘Turbot’, while still others recognise that they are different species, and call them ‘Turbot’ and ‘Brill’ respectively. Many names such as ‘Brill’, ‘Turbot’, ‘Sole’, ‘Witch’, and ‘Melgrim’ refer to actual species which are confined to the Northern Hemisphere. Needless to say, such loose applications of common names create much confusion.
Except for the two species of Family Bothidae and Azygopus pinnifasciatus (Rhombosoleinae), the remaining eight are highly esteemed for their edible qualities. These eight species are known to fishermen and the New Zealand public as either ‘Flounders’ or ‘Soles’. According to this loose terminology, ‘Flounders’ include R. plebeia, R. leporina, R. retiaria and R. tapirina, while ‘Soles’ include Peltorhampus novaezeelandiae and Pelotretis flavilatus. The choice of the term ‘Soles’ is unfortunate as this name, in all other countries, is reserved for species belonging to Families Soleidae and Cynoglossidae, neither of which is represented in New Zealand. Contrary to Parrot (1960, p. 14) neither P. novaezeelandiae nor P. flavilatus is related to the Soles of Australia and European seas. Not all the eight edible species referred to above are abundant and only four species comprise the bulk of our commercial Flatfish catch, namely, R. plebeia, R. leporina, P. novaezeelandiae and P. flavilatus. During the year 1967 (according to the Report on Fisheries for 1967, N.Z. Marine Department) the total catch of ‘Soles’ and ‘Flounders’ amounted to 5,787,600 pounds in weight representing 7.24 per cent of the total quantity of fish landed in New Zealand. This quantity was valued at 721,005 dollars comprising 15.59 per cent of the value of all fish landed.
Between 1913 and 1917, attempts were made to introduce the European Turbot (Scopthalmus maximum of Family Bothidae) to New Zealand. A detailed account of this venture is given by Thomson and Anderton (1921). This species, whose eyes are situated on the left side, attains a length of three feet and may weigh up to fifty pounds or more. Its body is somewhat circular in shape and its colour is usually greyish or sandy brown with darker spots and blotches. Some 170 young S. maximus, brought out from England, were reared in Portobello Hatchery tanks and released in Tautuku Bay, about 60 miles south of Portobello. None have been seen since.
The pleuronectid Brachypleura novaezeelandiae (Subfamily Samarinae) has been included in various check-lists of New Zealand fishes, as it was thought to have been taken in New Zealand waters. Norman (1934, p. 401) questioned its occurrence in New Zealand since this species is strictly tropical, occurring from the Indian Ocean
According to the key below, the side on which both eyes are situated determines the family to which each New Zealand Flatfish belongs. However abnormalities are not uncommon in Flatfishes so that an occasional specimen of the normally right-eyed species may have eyes on the left side. Recognition of reversed or abnormal specimens is important since often in the past they have been described as belonging to a new genus or new species. A New Zealand example of such an error occurred when Kyle (1900) described a perfectly reversed R. plebeia as a new genus and species, i.e., Apsetta thompsoni. Further, specimens similarly coloured on both sides are sometimes encountered and so are albinos, in which no pigment is developed at all. Albinos are usually white or pink but as a rule, albinism is not complete, the fish retaining patches of dark pigments. Abnormal colouration is often accompanied by structural abnormalities, for example, development of both pelvic fins in Rhombosolea sp. where usually only one pelvic fin is present.
The preoperculum bone of both Family Bothidae and Pleuronectidae has a free posterior margin covered over by the skin. In some species this character is more obvious than in others. Parrot (1960: 103-4) is incorrect in stating that some New Zealand Flatfishes have a second gill-opening. He is obviously referring to the slight folding of the loose skin under the posterior margin of the preoperculum. The skin however is continuous over the preoperculum and the other bones of the opercular series.
In the diagnoses and general discussion of the Families Bothidae and Pleuronectidae, Norman (1934) included the presence or absence of an oil globule in the egg as a taxonomic character, stating that bothids possessed a single oil globule while pleuronectids had none. However several pleuronectid exceptions have been recorded including some from New Zealand (Thomson, 1907; Thomson and Anderton, 1921; Orton and Limbaugh, 1953).
Common name: ‘Crested Flounder’.
This species grows to a length of 8 inches and is often confused with Arnoglossus scapha. When taken out of water the anterior rays are lying back against the blind side of the body and hence the crest is not noticed. In the male the second to fifth, six or seventh rays may be prolonged to about twice the length of the head. In the female fewer rays are prolonged to about half the head length. The body is brown or grey in colour with the pelvic of the ocular side usually black. Occurs in south-eastern Australia, Tasmania and the northern coasts of the North Island of New Zealand in depths between 30-100 fathoms. The numerous small bones and thinness of body make this species unsuitable for food.
(Fig. 3)
Common names: Witch’ or ‘Megrim’.
Attains a length of 18 inches. Distributed throughout New Zealand though more common around the South Island than the North. The teeth on the ocular side are larger than in any other New Zealand Flatfish, and small fishes are often encountered in their stomach. Grey or light brown in colour with numerous small black spots. In many check-lists of New Zealand fishes another species of Arnoglossus, namely A. boops, is included (see Norman, 1934, p.196); this species is based on one specimen incorrectly thought to have been taken at a depth of 400 fathoms. It has been shown that this specimen was taken from 150 fathoms together with another specimen which was described as A. scapha. Results of investigations (in progress at present) have led the author to believe that A. boops is a synonym of A. scapha. Though A. scapha is taken in large quantities by fishing trawlers, it is, like L. gallus, valueless fish for food.
(Fig. 4)
Common name: None in common usage but the term ‘ Spotted Flounder’ would seem appropriate.
This small fish (reaches 8 inches in length) is usually taken by deep-sea scientific expedition trawlers in waters between 190-400 fathoms. Coloured brown with small dark spots covering the entire ocular side and two prominent dark spots on the tail. Before the Danish Deap-Sea Expedition of 1950-52, this species was thought to occur in South Australian waters only, but since has been taken in New Zealand waters in the Bay of Plenty, around Chatham Islands and along the east coast of the South Island. Neilson (1961) examined the three specimens taken by the Danish Expedition and found that they differed from the Australian species in ‘several characters such as the diameter of the eyes, the number of gill rakers, lateral line scales, etc.’ and described the New Zealand specimens as a new subspecies, namely, A. p. flemingi.
(Fig. 5)
Common name: ‘Lemon Sole’ and ‘New Zealand Lemon Sole’.
Grows to 18 inches in length. The body is oval and the upper and lower profiles of the head are distinctly concave, with the upper eyes situated near the edge of the head. The colour is grey or brown on the ocular side with darker blotches. Occurs in shallow waters (down to 70 fathoms) around New Zealand and Chatham Islands but abundant only in southern waters, especially in Tasman Bay. The
P. flavilatus was studied in the 1930's by Rapson (1940). Its flesh is delicate and it is considered to be the choicest of our Flatfishes.
(Fig. 6)
Common names: ‘Turbot’ (Sometimes termed ‘Brill’).
This species is one of the largest and fattest of our New Zealand Flatfish, attaining 36 inches in length. It possesses a number of features which distinguishes it clearly from the closely related C. guntheri. The body is deep, nearly twice the body length; the rostral hook is long, extending below the level of the lower end of the maxillary of the ocular side; the pelvic fin has seven rays; the ocular is rich brown in colour with darker blotches. C. nudipinnis is seldom reported as abundant but is much more plentiful in very small quantities in Hawkes Bay and is occasionally reported from Northland and the
(Fig. 7)
Common names: ‘Turbot’ (Sometimes termed ‘Brill’).
Grows to a length of 36 inches but the body is not as thick nor as deep as that of C. nudipinnis. The following other features distinguishes C. guntheri from C. nudipinnis: The ocular side is dark grey in colour with the margins and fins almost black; the outer edge of each scale is black and this is responsible for the longitudinal black lines along the length of the body; the rostral hook is short and does not reach the level of the lower end of the maxillary of the ocular side; the pelvic fin of the ocular side over 9 or more rays. Its distribution is similar to that of C. nudipinnis and its flesh is highly regarded for food.
(Fig. 8)
Common names: ‘Sole’, ‘English Sole’, ‘New Zealand Sole’, and Patiki rori’ (Maori).
Grows to about 15-18 inches in length. Resembles C. guntheri and C. nudipinnis in the possession of a rostral hook, which in this case covers the mouth entirely on the ocular side. Another distinguishing feature is the long filamentous second upper ray of the ocular pectoral fin. The depth of the body is some 2-2½ times the body length. Specimens from around the South Island and Cook Strait have a distinctly deeper body than those from further north. P. novaezeelandiae is probably the most abundant of New Zealand Flatfishes. Young fish are encountered in large numbers on most of our beaches and harbours. Also occurs around Norfolk and Chatham Islands. An excellent table fish.
(Fig. 9)
Common names: ‘Black Flounder’, ‘River Flounder’, Estuary Flounder’, ‘Mud Flounder’ and ‘Patiki mohao’ (Maori).
Grows to about 14-17 inches in length. Its colour, body form and shape of head sets this fish apart from the remaining three species of Rhombosolea. The ocular side is deep olive or almost black in colour with numerous red or brown spots on the body and fins. The blind side is greyish in colour and often dark blotches are present. The body is oval in outline and the snout is somewhat blunt and certainly not as pointed as in the other Rhombosolea species. Whitley and Phillipps (1939, p. 231) considered that R. retiaria from North and South Islands of New Zealand differed sufficiently to necessitate the creation of a new subgenus and subspecies. They therefore named a specimen from the South Island (Hokitika) Rhombosolea (Adamosoma) retiaria adamas, based on an earlier description of R. retiaria by Phillipps (1925). This latter description is a general account of R. retiaria in New Zealand and gives only the fin formula, from a drawing by F. E. Clarke, of a fish taken on October 13, 1870 in Hokitika. The present author has been unable to trace the type specimen of the new subgenus and subspecies. In a more recent work, Graham (1956, p. 204) has adopted the new generic and specific names.
R. retiaria is distributed throughout New Zealand, preferring tidal reaches of rivers but is encountered in the sea or far upstream beyond tidal influence. It is a food fish but is not regarded as highly as the other flounders.
(Fig. 10)
Common names: ‘Sand Flounder’, ‘New Zealand Flounder’, ‘Dab’, ‘Tinplate’, ‘Diamond’, ‘Square’, ‘Three-corner’ and ‘Patiki’ (Maori).
Grows to about 17 inches. The adult is very distinctly diamond shaped and is easily recognised. The depth of the body is slightly more than 1½ times in the body length. Difficulty is often experienced in distinguishing between the young of R. plebeia and R. leporina. Here taxonomic characters such as proportional dimension of the eyes, number of gill rakers and dorsal rays should be considered. The eyes of R. plebeia are bigger, the eye diameter being 4-6 times in length of head. There are fewer gill rakers on the lower half of the first arch, ranging from 12-18 with 16 as the average. The dorsal rays are more numerous, ranging from 53-63 with 59 as the average. The ocular side is a dark grey or green in colour with the blind side invariably white with little or no pigmentation. R. plebeia is evenly distributed in shallow waters throughout New Zealand and is the commonest of the Rhombosolea species, comprising the bulk of our commercial catch.
(Fig. 11)
Common names: ‘Yellowbelly Flounder’, ‘Yellow Flounder’ and ‘Patiki totara’ (Maori).
Grows to about 13-15 inches in length. The body is oval with the snout more pointed than that of R. plebeia. Other distinguishing features include smaller eyes (6-8 times in length of head), greater number of gill rakers on the lower half of the first arch (14-23, average 19) and fewer dorsal rays (54-63, average 59). The ocular side is dark grey or green in colour, while the blind side is yellowish or orange with scattered black spots. The blind side of the young fish is usually white. Occurs throughout New Zealand inshore areas, frequenting estuaries and tidal rivers. Taken in large numbers by commercial fishermen. A good food fish.
(Fig. 12)
Common name: ‘Greenback Flounder’.
Grows to about 14-20 inches. This species is easily distinguished by its very pointed snout due mainly to the fleshy white process at the end of the snout. The ocular side is dark green while the blind side is entirely white. R. tapirina is widely distributed, occurring in shallow waters of southern New South Wales, South Australia, Tasmania, southern New Zealand waters, Auckland and Campbell Islands. Never abundant, it is sometimes taken in small quantities in commercial catches.
The author is indebted to Mr. J. M. Moreland for helpful discussions and the loan of specimens from the Dominion Museum, and to Professor
Present address: New Zealand Geological Survey, Department of Scientific and Industrial Research, Lower Hutt, New Zealand.
In the Past some workers in New Zealand palaeobotany did not designate holotypes or type specimens when describing new taxa (see Ettingshausen, 1891; Oliver, 1936). Thus lectotypes have to be designated by the first person to revise the work of these authors.
Under the rules of the International Code of Botanical Nomenclature, 1966 (hereafter called the ‘Code’), a holotype is ‘the one specimen or other element used by the author or designated by him as the nomenclatural type’ (Article 7, Note 2). Note 3 of the same article says that ‘if no holotype was indicated by the author who described a taxon … a lectotype … as a substitute may be designated’. Arber (1917) designated a single ‘type specimen’ for each new species he described. As this constitutes a definite elevation of one specimen of a series above the others, Arber's ‘type specimens’ are holotypes. The specimens associated with a holotype in a syntypic series may be called paratypes.
The Code states that a lectotype must be selected from the original material, taking into full account the original description and illustrations. It is recommended that the lectotype be selected from figured syntypes, which are those specimens mentioned by an author when no holotype was chosen (Article 7, Note 3).
In a revision of the systematics of the New Zealand fossil flora a type specimen for each species must be chosen from the material described by Ettingshausen (1891) and Oliver (1936). These type specimens will be either holotypes or lectotypes. There are three cases:
When only one specimen was found, validly described and illustrated as new species, this specimen becomes the holotype whether or not the original author designated it as such (Code, p. 71, para. 1). Knightia oblonga Oliver (1936) was represented by only one specimen and this becomes the holotype.
When a single specimen of a series was validly described and illustrated as a new species, this specimen may be either:
a holotype, if designated as such or as ‘the type’ by the original author or, a lectotype, if it was not designated as the holotype or as ‘the type’ by the original author.
Two specimens of Ulmophyllon pliocenicum Oliver (1936) were found; one was illustrated. This specimen becomes the lectotype. The associated specimen remains a syntype.
When two or more figured specimens of a series are validly described and illustrated as a new species, these specimens are syntypes. A lectotype may be chosen from the original illustrated specimens, taking the original description into full account. All specimens associated with the lectotype remain syntypes. Numerous leaf impressions of Fagus maorica Oliver (1936) were found; two specimens were illustrated. These are syntypes until a lectotype is chosen from them.
The meaning of Article 7, Note 6 of the Code is not entirely clear. It states that ‘the type of the name of a taxon of fossil plants of the rank of species or below is the specimen whose figure accompanies or is cited in the valid publication of the name. If figures of more than one specimen were given or cited when the name was validly published, one of these specimens must be chosen as type’. The word ‘type’ must in this context mean lectotype. Under this provision the choice of lectotypes is restricted to figured specimens even if there are better unfigured syntypes.
The designation of the lectotype should be made by a competent palaeobotanist because ‘the author who first designates a lectotype … must be followed’ (Article 8). If an author feels unable to designate a holotype or lectotype all specimens must be called syntypes.
Nature is Full of Rhythmic Changes. The environment in which we live changes from day to day, season to season, and, perhaps, from year to year in a rhythmic manner that is more or less predictable. The behaviour and abundance of animals often reflect these rhythmic changes in the environment; in fact, cycles in nature are universal in occurrence and of profound importance.
Cyclic changes in the earth's environment are induced primarily by the sun, e.g., the short-term variations in light, temperature, and humidity in the solar daily cycle, or long-term flux in these variables in the longer-term annual solar cycle. These changes profoundly modify the lives of organisms, and we find that animal behavioural patterns are highly adapted to avoiding harmful parts of the environmental cycles and utilising beneficial parts.
Although we naturally think first of the sun as responsible for changes in the earth's environment, the moon also has important effects, and information collected about many organisms indicates that certain parts of their activities recur at regular periods related to parts of the lunar cycle. In this general review the reader is introduced to some of the wide variety of animal responses to lunar-related environmental cycles, mostly in the sea.
The lunar orbit around the earth takes 27.29 days, but because of the earth's rotation and the moon's movement relative to the earth, the moon rises 50.5 minutes later each day, i.e., the lunar day is 24.84 hours long. The moon, sun, and earth are in the same positions relative to each other every 29.5 days, the lunar or synodic month.
Movements of the sun and moon interact in such a way that at full moon the moon rises at dusk and sets at dawn, and at new moon the moon and sun rise and set together. These relationships produce a lunar monthly cycle in the duration of moonshine at night.
The light intensity of the moon also varies with the lunar phase: at full moon 1.83 × 10-1 micro-watts/sq cm, at the quarters 2.12×10-3, and at new moon (i.e., no moon, clear sky) 1.8×10-4. Heavy cloud cover reduces these values about 10 times. The intensity of moonlight is about 1/500,000 that of sunlight (Moore, 1958).
Tides are caused by gravitational pull of the moon and sun on the earth, although because of the sun's great distance from the earth, despite its much greater mass, its gravitational effect is less than half that of the moon. The lunar cycle of tide-producing forces rotates around the earth each 24.84 hours, producing two pairs of tidal maxima and minima at any place each revolution. However, many factors affect the occurrence of tides, so that in some places there are no tides and in others up to four tides per day. Because the moon's orbit is at an angle to the earth's equatorial plane, there is an oscillating tidal asymmetry which varies 28° north and south of the equator. Since the lunar tide has a 24.84-hour cycle and the solar tide a 24-hour one, the effects of the moon and sun alternately amplify and oppose each other every 14.8 days, causing spring and neap tides (see Smith, 1968; Sverdrup, Johnson, and Fleming, 1942, for discussions of tidal phenomena).
Several secondary effects of the lunar cycle occur in the aquatic environment. Water pressure is a function of depth and so fluctuates with tides, varying with the daily and lunar-monthly tidal cycles. Similarly air exposure or water immersion varies on similar cycles. Brown (1962) hypothesised that forces like magnetism exhibit lunar cyclic changes, and he claimed that these forces are perceived in some fashion by organisms; but the evidence is extremely scanty.
Environmental variables affected by the moon may have lunar-daily (24.84 hours), semilunar (14.8 days), or lunar-monthly (29.5 days) periodicity. The most obvious environmental variables affected by the moon are light and tide, and of these the tide appears to have the greatest impact. For this reason lunar rhythms seem to occur mostly in marine species. In fact, Allee et. al. (1949) suggested that lunar periodicity ‘is of relatively little consequence to terrestrial communities as far as our present knowledge is concerned’. Cloudsley-Thompson (1961) concurred: ‘With the exception of marine animals, very few organisms are known that show lunar rhythms of activity.’
Species in diverse phyla exhibit lunar rhythms, mostly in their reproductive behaviour. In many littoral animals increases in activity occur with the rising tide; tide pool fishes leave rock pools to forage more widely, sea anemones expand as they are immersed by the rising tide, etc. But such examples are of little interest here, unless it is found that rhythmic activity patterns persist in the unvarying environment of the laboratory. Then we have the problem of determining how the continued activity is timed and regulated — the problem of ‘biological clocks’. Somewhat more complex is the problem of how animals time their activity and physiology on a long-term basis to specific parts of the lunar cycle and how they perceive and respond to lunar stimuli. Some of the examples discussed below have defied explanation up to the present time.
Protozoa: Ray and Chakraverty (1934) reported that the ciliate Conchophthirius lamellidens, parasitic in a freshwater mussel, conjugates most freely after full moon. This example, although cited in subsequent literature, has not been studied further, and no causal mechanism is known.
Coelenterata: Moore (1958) noted that a species of Pocillipora breeds throughout the year, but with a lunar rhythm. In winter, breeding is related to full moon and in summer to new moon. There is no correlation with tides, since in the winter the lowest neap tides are related to full moon and in summer to new moon. Response of the animal appears to be to tidal amplitude, water pressure, or air exposure. The rhythm is an irregular lunar-monthly one.
A sea anemone, Actinia equina, has a tidal rhythm in its cycle of expansion and contraction; although this would seem to be a simple case of direct response to tidal stimuli, the rhythm persisted in the laboratory for several days (Cloudsley-Thompson, 1961, after Pieron, 1958).
Platyhelminthes: Gamble and Keeble (1903) found that the intertidal flatworm Convoluta roscoffensis rises to the surface when the tide is low and retreats when the tide rises. The movements do not occur at night. This apparently simple tidal rhythm persists in the laboratory and so has some internal timing mechanism.
Annelida: Many examples of varying complexity are known in which annelids, all marine polychaetes, respond to lunar influences. Their periodicities and causation are variable and often poorly understood.
Odontosyllis enopla, the Bermuda fireworm, breeds about 55 minutes after sunset, for about half an hour, only on nights when there is no moon in the sky during the early part of the night, i.e., from two or three days after full moon until new moon. On such nights the worms swim to the sea surface from their tubes on the sea bed, apparently induced to do so by the decrease in light at dusk. The lunar rhythm seems to be a response to decline in light intensity, from sunlight to night sky without moon. The gonads mature with a lunar-monthly cycle which is in phase with the lunar-monthly cycle of a night sky without moonlight at dusk (Huntsman, 1948). Other species of Odontosyllis have similar cyclic breeding behaviour; in all these species breeding is thought to be a response to the lunar cycle of illumination (Korringa, 1957). Korringa listed similar periodicities in other annelids, including species of Platynereis and Ceratocephale.
One of the best known annelids with lunar spawning rhythms is the Pacific palolo, Eunice viridis, which spawns in immense concentrations on Pacific island coral reefs. The reproductive part of the worm (epitoke) detaches from the benthic, tubicolous, vegetative part (atoke) and swims to the surface. Swarming is reported seven to nine days after the full moon, at low tide, when the coral reefs
Odontosyllis. It is believed that breeding is related to the lunar cycle in such a way that the gonads become ripe at the third quarter of the moon, perhaps in response to the lengthening dark period after full moon, as the moon rises later and later in the night with the approach of the time of new moon (Korringa, 1957). Eunice viridis differs from Odontosyllis in that gonad maturation has an annual cycle which is independent of the lunar cycle except that the gonads finally ripen apparently in response to changes in lunar illumination.
The Atlantic palolo, Eunice fucata, is reported to have similar breeding patterns to E. viridis (Clark, 1941).
Spirorbis borealis, another benthic, tubicolous polychaete, releases its larvae at the first and third quarters of the moon. But Knight-Jones (1951) showed that this is due to the occurrence of breeding at new and full moons. Thus breeding which occurs at the spring tides manifests itself by neap tide release of larvae. Environmental variables to which the worms respond are undescribed.
Lunar periodicity in the settlement of another tubicolous polychaete, Hydroides norvegica, has interesting economic implications. Dew and Wood (1955) found that it is better not to clean the hulls of ships near the spring tides, because this worm exhibits spring tide (semilunar) periodicity in larval settlement. Ships cleaned at other parts of the tidal cycle were found to remain unfouled longer than those cleaned during spring tides.
Other invertebrate phyla—Mollusca, Echinodermata, Arthropoda: Instances have been reported of lunar rhythms in all these groups, although most are poorly documented. A chiton, Chaetopleura apiculata, exhibits lunar periodicity in breeding activity (Grave, 1922); Mytilus edulis matures during the new moon period and spawns at the following neap tide; the oyster Ostrea edulis spawns at about the spring tides (Korringa, 1957) and so do Chlamys opercularis (Wilson, 1951) and Pecten maximus (Mason, 1958). Littorina neritoides lives at about high-water mark of high spring tides and releases its larvae when immersed by the sea. It thus exhibits semilunar breeding rhythm (Moore, 1958). Clarke (1965) recorded a Red Sea echinoid the gonads of which reached maximum volume at certain parts of the lunar tidal cycle. Lunar rhythms of various types have been claimed for the crab Uca pugnax by Brown (1962, and numerous papers in Biological Bulletin, Marine Biological Laboratory, Woods Hole, not listed here).
Naylor (1963) showed that the chilling of Carcinus maenas will lead to replacement of a circadian (solar-daily) rhythm by a tidal rhythm which ‘though not phased with external tides … indicates that the ability to show tidal rhythmicity is deep seated in British Carcinus’ (Williams and Naylor, 1967). Williams and Naylor found that chilling of crabs reared from eggs in the laboratory will cause ‘spontaneous’ establishment of a similar tidal rhythm, confirming that ‘tidal rhythmicity is deep seated’ and suggesting that ‘it may be inherited’. They postulated that in nature, phasing of activity is corrected to harmonise with tides by tidal variables like hydrostatic pressure, temperature changes and periodic immersion.
One of the better documented, and therefore most informative, instances of lunar rhythm is that of Clunio marinus, a marine, tidal chironomid (Insecta, Chironomidae). The larval insects live among intertidal algae, and the adults emerge from their pupae when the water level is low. As the female is short lived and wingless, emergence at low tide facilitates the males reaching the females to copulate, and allows the females to deposit their eggs among shore algae without interference from the water. In Heligoland it was found that adult emergence occurs with semilunar periodicity, at the spring low tide. But populations in the Black Sea were found to emerge and copulate when offshore winds drive the water level down and expose the algae. The chironomids would seem to be responding directly to ‘tidal’ fluctuations, but it was found that animals in the laboratory maintained their rhythmic emergence in synchrony with their parental populations (Korringa, 1957, after Caspers, 1951).
Vertebrata Pisces: Perhaps the best known example of lunar periodicity is that of the Californian grunion, Leuresthes tenuis. This small, silvery, atherinid fish leaves the sea to deposit its eggs in the sand of several Californian beaches. Spawning lasts from late February until early September, but takes place only on three or four nights after full or new moon. It commences from one to three hours after the peak of high spring tide and lasts for about an hour and a half. The female swims on to the beach with an ingoing wave, usually accompanied by several males. She digs her tail into the wet sand and releases the eggs about 2 in. beneath the sand surface. Accumulation of sand on the beach as the tide falls leaves the eggs buried by 8 to 10 in. of wet sand. The eggs are washed out of the sand again at the next spring tide cycle and hatch rapidly under the stimulus of wave agitation.
This cycle is highly adapted to the tidal cycle. Since spawning follows the highest of the spring tide series, the spawning bed is not again disturbed by the tides until the next spring tide cycle, about 12 days later. At this time development is complete and the larvae are ready to hatch. In the meantime the eggs have a safe refuge buried in moist sand. On the particular tide at which spawning occurs the
Korringa (1957) could not ascertain environmental variables to which the grunion responded to time its spawning movements. He rejected light intensity, since spawning is semilunar, and he claimed that it is not related to setting of the sun. He suggested that the tidal rhythm may be the causal factor, but posed the question ‘How do the animals know which is the maximum tide of the spring series, and when the particular tide has passed its peak?’ Walker (1952) has shown that there is a semilunar cycle in ovarian maturation, but the basis for the cycle and the precise spawning response remain undetermined.
Hubbsiella sardina is another atherinid species which spawns in similar fashion on beaches of the Gulf of California. It differs from L. tenuis by spawning during the day as well as at night (Rechnitzer, 1952). Hypomesus pretiosus (family Osmeridae), the Pacific surf smelt, is not closely related to the above fishes, but it was found to have a spawning peak at high tide, the higher the tide the higher the spawning peak. This appears to be a simple response to water volume on the beach. Like those of the above atherinids, the eggs are deposited in beach sand (Loosanoff, 1937).
Although the spawning of Galaxias maculatus is less widely publicised than the grunion's it is equally fascinating, and even more difficult to understand. Larval G. maculatus live in the sea, but juveniles migrate into fresh water, and juvenile and adult life is spent in lowland streams and rivers, usually beyond tidal influence, often many miles upstream from the sea. It is one of very few well authenticated examples of lunar rhythms in non-marine species (although actual spawning is estuarine and tidally controlled). The gonads mature mostly in summer and breeding occurs mostly in early autumn. Burnet (1965) found that the mature fish migrate downstream to spawning grounds at full moon, but other workers (see Hefford, 1932) have found fishes spawning at both full and new moon spring tides. Ripe adults move up on to the grassy flats of river estuaries in immense shoals, penetrating to areas covered by water only at the spring tides. The eggs are deposited among grasses and are eventually washed down among the bases of grass clumps, where air humidity remains high and temperatures are stable and low. The eggs develop and usually hatch at the next spring tides that cover the grasses, although if low temperatures retard development, hatching will be delayed until later tides (McDowall, 1968).
This spawning pattern exhibits some of the adaptive features of the grunion. The most notable difference is that lunar-related spawning migration begins when the fish are far, perhaps many miles, from the
Deelder (1954) discussed migration in the ‘silver eel’ of Anguilla anguilla and concluded that it is influenced by the moon ‘to a high degree’. He found that in the Upper Rhine Valley the peak of migration was prior to the last quarter and comprised mostly females. In the Baltic and in Dutch waters migration was after the last quarter and involved mostly males. Bertin (1956) reported that females live mostly in inland waters and males in coastal waters, so that this apparently sexual difference in migratory pattern may in some way function to co-ordinate the sexes in their seaward migration. Deelder concluded that lunar influence is not exerted by light occurring at migration, as the eels exhibit their lunar rhythm regardless of moonlight conditions, and heavy migrations are known on stormy nights. He suggested that the lunar light cycle may establish an endogenous rhythm so that migration occurs at the appropriate time, regardless of night sky conditions prevailing on the night of migration. Lowe (1952), on the other hand, found that eels will migrate at full moon only when water is turbid, but that lunar influence on the silver eel migration is disrupted by cloud. Lowe suggested that light quantity may be critical. It seems that eel migration does exhibit a lunar rhythm, but present information is confusing and at times contradictory.
Gibson (1965, 1967) described a tidal activity rhythm in Blennius pholis, an intertidal, rock-pool species, peak activity occurring about the time of high tide (lunar-daily rhythm). This rhythm was found to persist in the laboratory, disappearing over a period of several weeks. Gibson suggested that this rhythm may be connected with feeding migrations outside tidal pools in which the fishes were found at low tide. Gibson (1965) also found a very short-lived rhythm in another species, Acanthocottus bubalis.
Savage and Hodgson (1934) detected a ‘definite rhythm’ in the quantity of herring caught off East Anglia, a monthly rhythm which reached its peak at about full moon. More recently Blaxter and Holliday (1963) have suggested that this periodicity, and those in other clupeid fisheries, may reflect behaviour of either fish or fishermen, and they have found periodicity less evident in recent years; this they attributed to improvement in fishing methods.
Lunar rhythms in other commercial fisheries have been reported, e.g., hake and bream (Moore, 1958).
Vertebrata Reptilia: Carr (1967), in his search for understanding of the breeding migrations of the Atlantic ridley turtle, Lepidochelys kempi, on to beaches of the Gulf of Mexico, suggested that they may be related to the full moon. This seemed in part the product of local Mexican folklore and in part educated conjecture by Carr.
It has been found that animals can synchronise their activities to a great diversity of natural, geophysical rhythms, e.g., diurnal (24 hours), tidal (12.4 hours), semilunar (14.8 days), lunar (29.5 days), annual, seasonal, or photoperiodic (365 days), etc. The environmental variables that in complex and various ways stimulate and control the activities of animals are poorly understood and subject to much conjecture. Opinions about how these activities are timed and maintained vary widely and really are not understood. In some instances behavioural patterns depend on receipt of direct stimuli from the environment, in others the repeated pattern of environmental stimuli results in short-term imprinting of a behavioural sequence in the animal. This may persist temporarily in the laboratory; sometimes it is found to persist indefinitely, because the repeated pattern of stimuli in the past has led to a recurrent and persistent pattern of behaviour in the species. Thus some animals exhibit rhythmic behaviour dependent on environmental variables, while others are to some extent independent, but display cyclic behavioural patterns which nevertheless correlate with cyclic fluctuation in environmental variables. Sweeney and Hastings (1962) used these differences to define exogenous (dependent) and endogenous (independent) rhythms; Brown (1962) called the latter ‘biological clocks’.
Endogenous rhythms apparently arose by long-term adaptation and synchronisation to persistent cycles in the physical environment, the cycles induced almost exclusively by the sun and moon. Brown (1962) considered that since much of the evolution of life occurred in the intertidal zone, over hundreds of millions of years the ancestors of many organisms may have been subjected to the rhythmic fluctuations of the tide. He suggested that this may explain the origin of animal rhythms of tidal nature. With some animals this may be so, but it is clear that this generalisation is not broadly applicable. Some animals are found to respond to lunar rather than tidal stimuli.
Clunio marinus discussed above has clearly not resulted from exposure to millions of years of tidal fluctuations, since one population has an endogenous rhythm correlating with a wind-induced ‘tidal’ rhythm. This seems to be a product of relatively short-term adaptation to prevailing ‘tidal’ conditions.
The experiments of Williams and Naylor (1967), demonstrating spontaneous establishment of rhythms in laboratory-reared animals, show that tidal rhythms in activity may be genetically fixed and are not necessarily experimentally induced: but at present we cannot generalise from Williams and Naylor's results. Brown (1962) suggested that timing of ‘biological clocks’ does not depend on obvious environmental stimuli like light and temperature; he stated this because there is no obvious response to these stimuli in some species and because the animal cycle sometimes continues if environmental variables are artificially modified. Brown has resorted to subtle geophysical forces to explain rhythm, claiming, though not demonstrating, that these forces correlate with other, more obvious environmental variables; e.g., he claims to have found responses to a magnetic field in the planarian Dugesia and also in Ilyanassa (Gastropoda), Drosophila (Diptera), and Paramecium (Protozoa). Careful analysis of Brown's work on the crab Uca pugnax shows that some of the lunar responses he has reported are mutually exclusive; e.g., in the sea Uca was reported to have tidal rhythm out of phase with the local lunar rhythm; in the laboratory at Woods Hole it was found to transfer to a strictly lunar rhythm, but when transferred 3000 miles west to California it maintained a lunar rhythm in synchrony with the Woods Hole lunar rhythm, not responding to the Californian lunar rhythm.
Korringa (1957), in contrast with Brown's view believed that we do not need to utilise factors like periodic changes in the moon's declination, gravitational influences, air ionisation, and other subtle geophysical forces. Korringa maintained that moonlight and tide are most probably of primary importance and is able to uphold this view in a number of instances. But others do exist where there is no apparent relationship between rhythms in animal activity and obvious environmental variables. The types of influences that Brown has investigated may need continued recognition and study.
Korringa believed that periodicity is called forth by the sequence of neap and spring tides in those localities where tidal amplitude is large, but that where tides are small, other factors can be held to be the cause of the animal's cycle, e.g. in those animals sensitive to light, the alternation of dark and moonlit nights appears to correlate sometimes with sexual maturation. Close relationship to the
Dictyota, which, although not an animal, but a marine alga, is an informative example. Hoyt (1927) found that it releases its gametes on a semilunar cycle at the spring tides in Europe, where there are large and regular semilunar tides; but in North Carolina, where one of the monthly spring tides is much greater than the other, gametes are released only once each month. And in Jamaica, where tides are irregular, there is no lunar periodicity in gamete release. Obviously the algae are responding rather directly to existing tidal conditions and are exhibiting profound adaptability.
However, Korringa's view does not explain the spontaneous establishment of lunar rhythms in laboratory-reared crabs (Williams and Naylor, 1967) or the persistence of endogenous rhythms in animals held under stable laboratory conditions.
Adaptations to cyclic variations in conditions of the environment are of obvious value to animals, enabling prediction of imminent events in their habitat, of either catastrophic or beneficial character, and allowing compensatory behavioural changes to be made. This is particularly true of endogenous rhythms, with their great predictive value in producing behaviour harmonic with environmental rhythms. The very existence of endogenous rhythms in many diverse animals shows that there are ecological and evolutionary advantages. Some of these advantages can be observed readily; others can be deduced, but of many we are probably largely unaware.
Convoluta receives an obvious and simple benefit by emerging from the sand at low tide and retreating again as the tide rises. Exposure allows the receipt of sunlight for phytosynthesis (Convoluta carries symbiotic green algae), and burrowing into the sand prevents the worms from being washed away by wave action. Copulation and oviposition among intertidal algae by the chironomid Clunio are obviously facilitated by occurring at low tides. Foraging by Blennius at high hides is more profitable, because the foraging area accessible to the fishes becomes larger. Leuresthes tenuis and Galaxias maculatus share the advantage of being able to deposit their eggs in the supratidal environment, where they are protected from egg predators.
In addition to such advantages in specific cases, there are generalised advantages in the occurrence of lunar rhythms. Most animals that react to the lunar cycle do so in a part of their reproductive cycle. Especially in species that broadcast their reproductive products into the sea in haphazard fashion, periodicity is of great value in concentrating spawning activity in both space and time. When spawning occurs at very low tides, especially in shallow water, there is a further advantage in having gametes concentrated in a reduced volume of water, so that chances of fertilisation are further increased.
At the basis of lunar cycles, as in all cycles in nature, there is the fundamental advantage of responding to sthmuli which correlate with recurring environmental conditions. Thus the animals respond to these stimuli with a background of ‘species experience’ that such stimuli are associated with near optimal conditions for the imminent activity; or the activity may increase survival. In simple terms, lunar periodicity in breeding tends to produce concentrated breeding activity in stable breeding conditions year after year.
I am grateful to Professor
A Guide to the Identification of Helminth Parasites Recorded from Wild Ruminants in New Zealand. pp. 67-81.
Frameworks of Marine Ecology. pp. 27-29.
Immunity. pp. 95-105.
Primary Productivity and Nutrient Cycling in Terrestrial Ecosystems. pp. 49-66.
Observations on Growth and Behaviour of Galaxiidae in Aquariums. pp. 34-46.
Marine Diatoms — Past and Present Distributions. pp. 30-34.
Manikiam, J. S.
A Guide to the Flatfishes (Order Heterosomata) of New Zealand. pp. 118-130.
Martin, W.
New Zealand Lichens and their Habitats. pp. 20-26. Key to the Stictaceae of New Zealand. pp. 106-117.
Extinction and Endemism in New Zealand Land Birds. pp. 1-12. Lunar Rhythms in Aquatic Animals — A General Review. pp. 133-144.
Macroscopic Plant Remains in Recent Lake Sediments. pp. 13-19.
The Selection of Lectotypes in Palaeobotany. pp. 131-132.
Tilted Marine Beach Ridges at Cape Turakirae, New Zealand. pp. 82-93.
Birds —
Extinction and Endemism in New Zealand Land Birds, by
Diatoms —
Marine Diatoms — Past and Present Distributions, by
Ecology —
See Ecosystems and Marine Ecology.
Ecosystems —
Primary Productivity and Nutrient Cycling in Terrestrial Ecosystems, by
Flatfishes —
A Guide to the Flatfishes (Order Heterosomata) of New Zealand, by J. S. Manikiam. pp. 118-130.
Galaxiidae —
Observations on Growth and Behaviour of Galaxiidae in Aquariums, by
Geology —
See Raised Beaches.
Helminth Parasites —
A Guide to the Identification of Helminth Parasites Recorded from Wild Ruminants in New Zealand, by
Heterosomata —
See flatfishes.
Immunity —
Immunity, by
Keys and Guides —
A Guide to the Identification of Helminth Parasites Recorded from Wild Ruminants in New Zealand, by
Lichens —
New Zealand Lichens and their Habitats, by W. Martin. pp. 20-26. Key to the Stictaceae of New Zealand, by W. Martin. pp. 106-117.
Lunar Rhythms —
Lunar Rhythms in Aquatic Animals — A General Review, by
Marine Ecology —
Frameworks of Marine Ecology, by
Palaeobotany —
Macroscopic Plant Remains in Recent Lake Sediments, by
The Selection of Lectotypes in Palaeobotany, by
Raised Beaches —
Tilted Marine Beach Ridges at Cape Turakirae, New Zealand, by
Reviews —
Of Margaret A. Leslie's ‘Animals of the Rocky Shore of New Zealand’, by E. C. Brace. pp. 46-47.
Stictaceae —
Key to the Stictaceae of New Zealand, by W. Martin. pp. 106-117.