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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 or advertising should be sent to: Business Manager of Tuatara, c/o. Victoria University of Wellington, Box 196, Wellington, New Zealand.
is the journal of the Biological Society, Victoria University of Wellington, New Zealand, and is published three times a year. Editor: H. B. Fell. Assistant Editor:
‘The term “plankton”, from the Greek planktos meaning drifting, was proposed by Hensen as a collective term for the small organisms which occur suspended or free-swimming in water and whose powers of movement are so restricted that they drift at the mercy of currents.’ It may seem paradoxical to refer to the ‘terrestrial plankton’ but the phrase ‘dry land’ is a misnomer, not even a desert is wholly dry. All terrestrial habitats retain moisture and the total volume of water held in these environments is probably almost equal to that of the volume of the freshwater lakes and rivers, 0.25 Gg. (Hutchinson, 1957, p. 223). Further, the freshwater lakes and rivers are being constantly replenished chiefly by water that has passed over or through terrestrial environments. This annual precipitation on land surfaces is of the order of a geogram (1020g.) or four times the total volume of all inland waters. The annual evaporation from land surfaces is equal to about two-thirds of this figure and the runoff to the sea is equal to about a fifth (Hutchinson, 1957, pp. 221-230). ‘Dry land’ is, therefore, deeply involved in the hydrological cycle and there is ample water to provide a rich variety of niches for aquatic organisms. The peculiarity of these niches is that the moisture is held in small discrete surface films or pore spaces, greatly restricted in volume, and contrasting sharply with the ocean, lakes, and rivers. Secondly, the currents to which this kind of water is subject are those of wetting and drying, of precipitation, drainage and evaporation. Thirdly, these waters tend to be much richer in mineral and organic nutrients than other natural bodies. Indeed the blooms of freshwater and marine plankton are often associated with the influx of fresh runoff carrying not only the major nutrients,
12 (Hunter et. al., 1956). Fourthly, and perhaps most significantly, there is the close association with higher plants, an organic cycle different to that of most freshwater and marine environments.
In terrestrial environments the variety of the plankton is not as great as that of the marine and freshwater habitats but the structure of the population is very similar. Exceptionally the organic cycle is dependent upon algal photosynthesis (e.g. Antarctica, Flint and Stout, 1960) but generally the vegetation is dominated by the higher plants. Romer has pointed out that the evolution of the higher plants was a necessary prerequisite for the evolution of terrestrial animals and it has also provided a wealth of niches for aquatic microbial life, not only in such bizarre reservoirs as those of the pitcher plant, the bladder wort, or the axils of Astelia but more typically on leaf. stem, and root surface and particularly in the decaying vegetable matter of the forest floor. Here at its richest and in its most typical form may be found the terrestrial plankton.
Algae and phytoflagellates, most commonly unicellular, bacteria, yeasts and protozoa form the nannoplankton. The three latter generally closely associated with fungal mycelium, fine roots, and decaying vegetation. The smaller metazoa include rotifers, nematodes, tardigrades, gastrotrichs. turbellarians, enchytraeids and other aquatic olgichaetes. The Crustacea are represented by copepods, cladocera, and ostracods. There are also insect larvae and minute gastropods. These organisms may attain very great populations. Bacteria may number 109 per ml. of free water, yeasts perhaps 1% of the bacterial total, protozoa several thousands, and so on. Some figures of populations estimated by a dilution technique are given below:—
No attempt has been made to estimate the mass of these organisms but it is clear, from the numbers alone, that they form an appreciable part of the terrestrial population.
The predominance of higher plants has displaced the importance of the algae in the food chain of the terrestrial plankton. Few of the zooplankton are obligate feeders on diatoms or other algae. The majority depend on bacteria, yeasts, or perhaps fungal mycelium. Some are phytophagous and others are micropredators. Ingestion of plant remains is rare among the smallest plankton although some of the nematodes and the larger animals, such as the copepods and aquatic oligochaetes, pass large quantities of plant detritus through their gut. However the greater part of
feeding on the plant debris but on its associated fungi and other micro-organisms. Because the restricted distribution of the free water in which the plankton live prohibits the use of such devices as filter feeding terrestrial predators are driven to the only alternative — a complete ingestion of the plankton and its substrate and the separation, by digestive processes, of the edible plankton from its inedible plant substrate. This may well explain the enormous activity of soil animals in plant litter and the failure in most cases to show the presence of significant amounts of cellulolytic enzymes. On the other hand the constant comminution of the dead plant material passing through the gut of soil animals renders it more accessible to microbial attack, and the animal droppings become active centres of microbial proliferation. The relationship may be seen therefore as one of symbiosis. Where larger animals tend to be absent, such as in peats, the process of degradation is slowed down and incompletely decomposed organic material tends to accumulate.
Some figures are available of the activity of the fauna both in the physical comminuation of plant litter and of its chemical degradation. Litter animals such as oribatid mites or amphipods may consume between 25 and 40% of their own weight of litter per day. Of this only about 20% is digested. In the case of mites it is estimated (Engelmann, 1961) that of the digested material by far the greater part is metabolised in the respiration of the animals but Clarke, in his study on the amphipods in a New South Wales podocarp-broadleaf forest, estimated that only about a sixth of the digested material was respired the rest being lost as dead animal tissue in the non-predatory mortality of the amphipod population. Such dead animal tissue, however, represents a far more readily accessible source of nutrients for other soil organisms than the plant tissue and one suspects that it would be rapidly metabolised by other organisms.
Physical comminution by soil animals is illustrated by Nef (1957). ‘If a pine needle 60 mm. long. 1 mm. broad and 0.5 mm. deep
2 is fed to an earthworm which reduces it to fragments of 1 mm. diameter the surface area will be increased to 240 mm.2 but if it is attacked by mites which reduce it to fragments of 1003BC diameter the surface area becomes 1.8 m.2 or 10,000 times the original.’
In Figure 1 an attempt is made to present the relationships of the terrestrial plankton to the larger animals in soil and particularly forest litter. The principal sources of available nutrients are:— (I) soluble nutrients, such as carbohydrates, amino-acids, and soluble proteins initially derived from leaf drip, dead leaves and twigs; and (II) insoluble nutrients, such as cellulose and lignin. The insoluble nutrients are rendered accessible to soil animals only by bacterial and fungal action and they become accessible in one of two ways, either in the form of microbial cell tissue or in solution as autolysed tissue. In the first case they may be eaten either by the microfauna or the macrofauna and in either case contribute to increase of animal tissue and respiratory activity. In the second case they contribute to the sum of soluble nutrients available in the system.
Similarly animals feeding on the microflora suffer either predatory or non-predatory mortality. In the first case their tissues are used in respiration or synthesis by their predators and in the second soluble nutrients may be released by autolysis or they may become centres of microbial proliferation. The relationships are complex but the pattern is uniform. The sum of synthesis and respiration, predatory and non-predatory mortality tends to release at least part of the available energy of the system in the form of soluble nutrients and these soluble nutrients augment the initial source from leaf drip; from frass, honey dew or other products of phytophagous arthropods; and from dead plant litter. It is this pool of soluble nutrients which constitutes the main substrate of microbial proliferation, supports the terrestrial plankton, and which directly or indirectly provides the basic nutrients of the great majority of soil animals. It also seems likely that it is the concentration of these nutrients in the soil profile which determines the rate of respiration rather than the size of population. Measurements on beech leaves have shown the highest rates tend to be in the more freshly fallen leaves — provided they are wet. Here the populations are lowest but it is likely that soluble nutrients, not yet leached away, are at their highest concentration. In beech leaves, which are not readily eaten by soil animals, the greater part of loss of weight of the litter can be accounted for by respiratory metabolism in situ, at least in the early stages of decomposition. It seems very likely that this reflects the predominant role of microbial growth and metabolism, which may well provide the immediate substrate of the associated animal population.
All planktonic organisms are minute but the terrestrial representatives are remarkable even within this range for their relatively small size. Thus the most common of terrestrial copepods are harpacticids, cyclopoids are rare, and the most common of the harpacticid copepods, Epactophanes richardi is only about 0.5 mm. in length. Similarly terrestrial ostracods are relatively small, the New Zealand species, Mesocypris audax, Chapman, 1961, being about 1.1 mm. in length. Of the aquatic oligochaetes the representatives of the Aeolosomatidae occurring in terrestrial habitats are all only about 1 mm. in length, the Naidid worms are larger, up to several mm. long. Phreodrilids and enchytraeids are larger again but in this case the worms possess a thicker body wall, a morphological character shared by the earthworms, which makes them less susceptible to variation in hydrostatic pressure.
The terrestrial nannoplankton, such as the protozoa, is similarly remarkable for its small size. Thus terrestrial species are almost invariably smaller than freshwater or marine representatives of the same genus and where more than one species is present it is typically the smallest which is the most common. Thus while a catch of terrestrial plankton has many similarities to a catch of fresh water or marine plankton the most striking difference is that it will need to be studied under a higher magnification and it is reasonable to associate this distinction with the confined character of their aquatic habitat which restricts moisture to thin films and narrow pore spaces.
A second feature of the terrestrial plankton is the relative simplicity of form and life history. Most groups are capable of asexual reproduction and the life cycle tends to be short and direct. Again it seems reasonable to associate these characters with the necessity of accommodating an aquatic mode of life to an environment capable of frequent desiccation. The formation of cysts or, in the case of copepods, eggs capable of enduring periods of drought is also typical.
Apart from the nannoplankton — the bacteria, the yeasts, and protozoa — little is known of the physiology of the terrestrial plankton. Many of the larger forms, such as the copepods, appear to be sensitive to high carbon dioxide concentrations or low oxygen tensions such as are associated with rapid decomposition under conditions of poor aeration. Most seem tolerant of acid pH, being common in sphagnum and forest litter with a pH below 5.0 and sometimes below 4.0. However from the few observations that have been made there is a suggestion that mull forest soils, such as those under puriri, may have a different copepod fauna to mor forest soils, such as those under beech, and this may imply physiological and ecological distinctions at the species or genus level. Little is known of the rate of reproduction or of any
It is this aspect, the successful colonisation of ‘dry land’ that has aroused speculative interest in the soil fauna generally (Ghilarov, 1956). How have animals evolved from strictly aquatic to strictly non-aquatic organisms? The fauna of the terrestrial environment, part rock, part water, part air, offers the most suggestive evidence on this problem. Three evolutionary pathways have been suggested. One, proposed by Hurley (1959) as the evolutionary pathway of terrestrial amphipods, suggests that a supralittoral fauna penetrated directly into the forest floor. A second possibility is the slow evolutionary adaptation of a fresh water pond fauna to increasing periods of desiccation until finally a true soil fauna enjoying brief periods of aquatic life is attained. The Tubificidate have been suggested as an example of this process. A third possibility is the evolution of a fauna originating in fresh water streams, extending through moist mossy banks and sphagnum bogs to the forest floor and so to mineral soil. This seems in the majority of cases to be the most convincing explanation. Thus with the naidid worms the closest relatives of one of the New Zealand species were recorded from shallow streams and adjoining moss carpets. The copepods and ostracods tend to occur in sphagnum as well as in forest litter (Harding, 1953, 1955), and this seems also the most convincing pattern of protozoan evolution. On the other hand the evolutionary trend is not solely towards greater emancipation from a permanently aquatic environment. The reverse trend is also evident. The occurrence of earthworms and pulmonate gastropods in fresh water lakes, and perhaps more dramatically the suggested evolution of hydracarines from terrestrial mites are cases in point.
The mobility of the fauna varies greatly. Some, such as protozoa, although very strictly aquatic are able to exploit the smallest and most transitory pockets of moisture; others, such as enchytraeids and ostracods, although requiring a high relative humidity, are able to move freely within such an atmosphere. These latter have close affinities both taxonomically and ecologically with earthworms and terrestrial amphipods and isopods. Their respiration is dependent upon relatively large moist exposed surfaces and they lack the cuticular waxes which are of such great value to the insects in their emancipation from water to air (Beament, 1961). Consequently they are susceptible to excessive transpiration losses. Such animals are always happier in a wholly aquatic medium than
Still the best and most readily accessible account of the forest fauna is that of Birch and Clark (1953). A more recent work is the new English translation by Norman Walker of Kuhnelt's Soil Biology (Faber). A number of papers have been published in recent years on the microfauna of New Zealand soils and these are also listed below.
Tuatara has over 700 subscribers, including 176 libraries. These, coupled with casual sales, now require a regular edition of of 1100 copies. The journal is distributed to Great Britain, United States of America, Union of Soviet Socialist Republics, Australia, Sweden, Belgium, Sudan, Fiji and Malta.
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‘To the memory of Daniel Carl Solander, F.R.S.
1733-1782’
So runs the dedication to Allan's 1961 Flora of New Zealand. But why Solander? Why not Forster, Manual (p.v.) ‘Every botanist who prepares a Flora starts from the standpoint reached by his predecessors in the same field’.
Solander had no predecessors — his was a virgin field. He had it is true the Species Plantarum at his hand. He had the advantage of personal tuition by Linnaeus. He had wide experience of botanical matters in Europe and in England, and he had, during 1769, botanised briefly in South America and Tierra del Fuego, and extensively in Tahiti. He was in fact a first class professional botanist. He had been offered the Chair of Botany in the Petersburg Academy of Sciences, was a fellow of the Royal Society and on the staff of the British Museum. He had also two very able colleagues — Banks, himself no mean botanist, with his vigorous intelligence, his youthful enthusiasm and his very necessary money — and Parkinson, with his technical skill and devotion. And in the background the master mariner Cook, who had brought them there and would take them home. The presence of Tupaia too was providential. To be able to discuss the native names and uses of the plants collected, with the people who had lived among them for centuries was invaluable. Solander's Pohutukawa and Kowhai — his modus praeparandi, are echoed unaltered 200 years later in the Floras of today. These things were in his favour. But against him was the very limited time ashore and the almost total strangeness of the vegetation he was studying.
This paper is based upon the typed copy of the Solander manuscript in the Auckland Museum. I am indebted to Dr.
Banks said of it (Beaglehole 2 : 1962, p. 9) ‘Sow thistle, garden nightshade, and perhaps one or two kinds of grasses were exactly the same as in England, three or four kinds of fern the same as those of the West Indies, and a plant or two that are common to almost all the world; these were all that had before been described by any botanist out of about 400 species, except five or six which we ourselves had before seen in Terra del Fuego’.
The Primitiae Florae is of necessity a coastal Flora and the shadow of the Endeavour hangs over it. Much of the botanising was done during wooding and watering, fishing, shooting and surveying trips, and was subject to the exigencies of service. The Maori comes into it too. His clothes and cultivations, his ornaments and his children, and many of his plant names. The few errors are more interesting than otherwise — one in particular, Avicennia resinijera. Cook (Beaglehole 1 : 1955, p. 204) says —‘ … in speaking of Mercury Bay I forgot to mention that the Mangrove trees found there produce a resinous substance … we found it at first in small lumps upon the sea beach, but afterwards found it sticking to the Mangrove trees and by that means found out from whence it came.’ The resin was the familiar Kauri gum and it was not produced by the Mangrove. The name though misleading, was perpetuated by Geo. Forster and having priority has stuck — like the gum it commemorates.
This first Flora was a major event in the botanical history of New Zealand, although it was never published. Its importance is emphasised by the number of Solander's names which were taken up by later botanists and his skill by the fact that 123 plants still belong in the genera in which he originally placed them. The near misses are revelant too. Smilax, Pandanus, Piper, Fagus, Panax, Aralia, Veronica, Myrtus, Mesembryanthemum, Passiflora, etc., are but further proof of his knowledge.
To read Solander for the first time is to experience a feeling of familiarity — one has trodden this path before. In spite of the Latin and the odd quirks of the Linnean system, this collibus et campis is home sweet home. His descriptions have a modern ring about them and his locality-habitat notes a photographic clarity.
For example :—
Avicennia resinifera — ad latera limosa fluviorum lacuum solsorum. Disphyma australe — copiose juxta littora marina praecipue, in fissuris rupium.
Lycopodium billardieri — in sylvis … in arboribus parasitica dependens.
Entelea arborescens — ad latera vallium et ubi sylvae incipiunt. and of
Odd words stand out here and there — Paesia scaberula — elegantissima and
That the work had so profound an influence on subsequent Floras of New Zealand was due partly to Banks' place in the scientific world and to his generosity in allowing the collections to be studied by those interested, and partly to his choice of secretaries. First Solander, then Dryander and finally Students' Flora of 1899 and were handed over to Cheeseman who used them while preparing the 1906 Manual. They are still preserved in the Auckland Museum and are the basis of these notes. Cheeseman says ‘of their scientific value I cannot speak too highly’. I believe there is a photostat copy of the original manuscript and another set of drawings in the Dominion Museum and in the Turnbull Library. The whole of the ‘Banks and Solander’ material was studied by Flora. All these botanists quote Solander freely and with respect.
205 Fig. Pict. are listed and there exist several others. One which interests me is an unfinished but recognisable sketch of Earina autumnalis which is not otherwise mentioned in the typescript. Another plant left out by Solander is the
Sonchus oleraceus — in graminosis et cultis.
Broussonetia papyrifera — culta in septentrionali parte Nov. Zel. sed rara.
Lagenaria vulgaris — forte culta utensilaria varia e hupis fructo formant incolae.
Discorea sativa — culta. Ipornoea batata — culta.
Solander's Maori names are sometimes amazingly accurate. His Kawakawa, Kowhai, Mahoe, Manawa, Manuka, Ngaio, Piripiri, Pohutukawa, Poroporo, Tawa, Ti, Tutu, appear as they do today. Several others are recognisable though mis-spelt by modern standards — Karaka (Chalacha), Karamu (Charamugh), Kiekie (Geagea), Kumara (Kumala), Ramarama (Lamalama),
Rangiora (Rangiola), Mangeo (Tangeo), and Kowhai ngutu kaka (Kowhai no tugaga). There are as many again that are meaningless to me. One name is worth comment. He uses Kowhai for Sophora tetraptera, and
There are 349 names in the typescript. Of these 15 were not identified by Cheeseman — 12 ferns and 3 Cyperaceae. The remainder fall conveniently into four groups :—
(i) In the current Floras (Cheeseman, 1925, for the Monocotyledones, Allan, 1961. for the remainder) 49 names read exactly as Solander wrote them. Of these specific names 45 originated with Solander, 4 with Linnaeus. Of the 35 genera, 28 are Linnean and 7 by Solander. The 7 are Astelia, Dacrydium, Metrosideros, Nertera, Pimelea and Pittosporum. Familiar plants in this group are — Arundo conspicua, Asplenium lucidum, Astelia nervosa, Avicennia resinifera, Clianthus puniceus, Dacrydium cupressinum, Linum monogynum, Metrosideros excelsa, Nertera depressa, Pimelea longifolia, Pittosporum crassifolium, P. tenuifolium, Pteris tremula, Ranunculus hirtus, Rubus australis, Salicornia australis, Scirpus frondosus, Senecio lautus, Sophora microphylla, S. tetraptera, Tetragonia trigyna, Trichomanes reniforme and
(ii) 40 plants bear the specific or varietal name given by Solander or derived therefrom, but the genus has been changed. Included are — Alectryon excelsum, Ascarina lucida, Blechnum discolor, Bulbophyllum pygmaeum, Carpodetus serratus, Celmisia gracilenta, Coprosma acerosa, Cordyline australis, Disphyma australe, Dracophyllum longifolium, Earina mucronata, Elatostema rugosa, Griselinia lucida, Haloragis erecta, H. procumbens, Hebe macrocarpa, H. pubescens, Hymenophyllum dilatatum, H. sanguinolentum, Litsaea calicaris, Lophomyrtus bullata, Luzula campestris, Neopanax arboreum, Nothofagus fusca, Pellaea rotundifolia, Phormium tenax, Pittosporum umbellatum, Pseudopanax crassifolium, Rhopalostylis sapida, Sarcochilus adversus, Schoenus tendo, and
(iii) 74 plants were placed by Solander in the genera to which they still belong, although the specific names have changed. 45 genera, 41 of them Linnean, 4 by Solander. They include species in genera like — Adiantum, Arundo, Asplenium, Astelia, Carex, Clematis, Coriaria, Drosera, Elaeocarpus, Epilobium, Gaultheria, Gnaphalium, Hydrocotyle, Juncus, Lepidium, Lobelia, Lycopodium, Myoporum, Myosotis, Plantago, Samolus, Scirpus, Senecio, Solanum, Tillaea, Trichomanes and Urtica.
(iv) A further 186 plants were described but the names were never taken up. The group includes Acaena, Aciphylla, Aristotelia, Arthropodium, Beilschmedia, Brachyglottis, Carmichaelia, Corynocarpus, Cyathea, Dendrobium, Discaria, Dysoxylum, Entelea, Freycinetia, Fuchsia, Geniostoma, Hedycarya, Hoheria, Ipomoea, Knightia, Lagenaria, Leptospermum, Macropiper, Melicope, Melicytus, Microtis, Myrsine, Olearia, Orthoceras, Paesia, Plagianthus, Podocarpus, Pomaderris, Pterostylis, Rhabdothamnus, Rhipogonum, Schefflera, Thelymitra, Uncinia, Vitex, Wahlenbergia and many more besides.
Two names show transposition — Senecio perdicioides was written
Cheeseman considered 6 species to be duplicated —
Calystegia tuguriorum (Convolvulus lacteus — C. versatilis).
Carex forsteri (C. debilis — C. latifolia).
Geranium pilosum (G. pilosum — G. patulum).
Gnaphalium involucratum (G. involucratum — G. collinum).
Penantia corymbosa (Meristoides paniculata — Fagoides triloba).
Podocarpus dacrydioides (Dacrydium thujoides — Lycopodium arboreum).
A number of Parkinson's drawings have been published from time to time. I am aware of eight books and papers (there may be others) containing them. Twenty-nine plants are illustrated.
The 349 species collected and described by Solander in New Zealand are contained in 206 genera and (counting the Filicopsida as a single family) 86 families. Of the genera 130 belong to the Dicotyledones, 48 to the Monocotyledones, 25 to the Filicopsida, 2 to the Coniferae and 1 to the Lycopodiaceae.
When it is remembered that manuscript Floras were prepared also for Tierra del Fuego, Tahiti and the eastern coast of Australia, and that each of them was as coherent as the New Zealand section, and that he wrote in addition on the marine and bird life encountered on the voyage, the genius of the man shines forth, and we begin to understand why the present Flora of New Zealand is dedicated to the Swedish Doctor from the University of Uppsala. Well might Linnaeus write of the ‘immortal Banks and Solander’.
The ticks are the largest of all Acarina. They may be distinguished by the presence of a movable capitulum, distinct from the fused thorax and abdomen and visible dorsally in most genera, and the prominent barbed hypostome. Unfed ticks in all stages are dorso-ventrally flattened but the bodies of engorged females may be spherical and up to 10 mm. in diameter, when the sclerotized parts which provide the main taxonomic characters become relatively inconspicuous. The basis capituli may bear cornuae postero-laterally or auriculae ventrally and in the females has two dorsal porose areas. The mouth parts are borne in the median line anteriorly and consist of a dorsal cheliceral sheath and a ventral toothed hypostome which enclose the chelicerae and are apposed to form a sucking tube. This structure is flanked on each side by a labial palp which is four-segmented, though the fourth segment is small and often not visible dorsally. The scutum is a flat shield-shaped plate on the dorsum of the thorax immediately behind the capitulum. The legs are six-segmented and bear a sensory organ (Haller's organ) on the distal tarsal segment of the first pair of legs. The spiracular plates are sub-circular and are situated ventro-laterally behind the fourth coxae. The integument of the remainder of the body, except in the males, has a thin unsclerotized integument which is capable of great extension during engorgement. The eyes, when present, are situated on the sides of the scutum but they are not present in New Zealand species.
The females are oviparous and the development of individuals of both sexes includes a larval and a nymphal stage. The larvae have only three pairs of legs and the nymphs lack the genital opening of the males and females. The males and females of Ornithodoros differ only in the form of the genital opening, but in the Ixodidae the males have the scutum covering the dorsum and more numerous ventral plates, while the females have porose areas on the dorsum of the basis capituli.
All stages except the males are blood-sucking. The skin of the host is pierced by the cutting chelicerae and the recurved teeth of the hypostome, which is inserted into the wound, act as a holdfast. The argasid ticks such as Ornithodoros feed quickly and leave the host at once, and all stages are commonly found in the nest, where they shelter, and not on the host. All stages
This habit is of significance in the transmission of the diseases of man and animals, especially in tropical countries, which are caused by the pathogenic viruses, rickettsiae, and protozoans which the ticks may carry. In some cases the pathogenic agent is transmitted to the progeny of the infected female tick through the eggs, and ticks which have never fed on an infective host may thus carry infection. Apart from their role as vectors of disease the ticks inject salivary secretions when feeding and in some species these have a neurotoxic constituent which causes ‘tick paralysis’ in man and animals, especially when the feeding site is near the brain or spinal cord.
The eggs, which are spherical and about half a millimeter in diameter, are extruded in large masses containing as many as 1000 eggs. They are found in the nest of the host, or on the ground where the female has dropped from the host. Host finding is easy for the larval ticks hatching from eggs laid in a nest, burrow, or lair which is constantly used or periodically reoccupied. The tick species infesting free-ranging mammals may drop from the host anywhere, though they would tend to be concentrated in favoured camping places. The larvae or newly moulted individuals of such species ascend grasses or other vegetation and wait for the passing hosts to brush against them.
Ticks have been known to survive unfed for very long periods but there is no doubt that a large part of the mortality amongst larvae and nymphs awaiting a host is due to adverse climatic factors. One small hymenopterous (chalcid) parasite of ticks is known elsewhere, but invertebrate predators may take a greater toll of ticks on the ground. Birds such as the starling may take the ticks not only from the ground but from the host also. Two unusual cases are known of a sea-bird tick taken from the faeces of a tuatara and a kiwi tick from the faeces of a cat. On the hosts the ticks aggregate in positions where they are not readily dislodged by self-cleaning or scratching.
Because of their medical and veterinary importance considerable work has been done on the physiology, ecology, and control, of ticks. In New Zealand the cattle tick (Haemaphysalis) is the only species which has been studied (Myers, 1924).
Recent taxonomic work on New Zealand ticks is accessible in previous papers (Dumbleton 1943, 1953, 1958, 1961), and detailed host lists are given in two of these (1953, 1961), A generalised host list is combined with the list of the species in the New
Haemaphysalis leachi Audouin, Hyalomma aegyptium Linnaeus, and Ixodes ricinus Linnaeus, have been recorded as present in New Zealand. They were considered (1953) as doubtfully established and are now omitted from the list as they have not been collected since that date.
Little can be said regarding the origin of the tick fauna. The single species of Aponomma, a genus largely restricted to reptiles, would appear to have been contemporaneous with Sphenodon.
The same may be true of Ixodes anatis Chilton the only New Zealand species confined to land birds, more especially the kiwi. This appears to belong to a group differing from that of the other New Zealand species. While there are few or no Australian species confined to land birds I. anatis has some affinities with the species of Ixodes (Sternalixodes) which occur there on land animals.
The species occurring on sea birds are either cosmopolitan or belong to species-groups which are widespread in the Subantarctic or in Australia.
Keys to the families, genera, and the males and females of the genus Ixodes are given below. Nymphs, and usually larvae, are identifiable by association with adults and similarities in morphology.
Scutum absent in all stages; capitulum ventral, visible dorsally in larva but not in nymphs and adults; integument mamillated, with symetrical pattern of smooth plaques on dorsal surface; sexes differing only in form of genital orifice (figs. 1 and 2) . . Argasidae.
Scutum always present, covering all (males) or not more than anterior half (females, nymphs, larvae) of dorsum; capitulum anterior, visible dorsally and with prominent basis capituli; integument smooth; females with porose areas on basis capituli, males with median and ad-anal plates (figs 3, 4, 5 and 6). Ixodidae.
Without a marginal sutural line, separating the dorsal and ventral surfaces and differing in sculpture from both …. Ornithodoros.
(One species. Body distinctly conical anteriorly; hood and cheeks, enclosing capitulum, distinctly separated [figs. 1 and 2] O. capensis).
Little is known about the root habit of many New Zealand plants. One of the few published works is a paper by McIndoe (1932).
One feature of at least some species of forest tree is their ability to form root grafts. This phenomenon seems to be common in the Nothofagus species and is probably found in others. There are several interesting ecological implications arising from root grafting as it has been shown overseas (see Fraser and Gaertner, 1961), that materials are transmitted from individual to individual through the root systems. Weak plants may survive in a dense stand in this way and this raises the question of the nature of competition in such a situation.
A set of observations on a peculiarity shown by some New Zealand gymnosperms was made by Foweraker (1929) and bears repeating. Foweraker found that Podocarpus totara could survive burial by quite deep deposits of river silt by sending out adventitious roots near the new ground level. Photographs show trees with as many as three series of roots girdling the stem and each separated by several feet. This ability could be important to species inhabiting the flood plains of rivers. Christensen (1923) showed that a number of other New Zealand trees and shrubs survived burial by riverbed gravel in the same way, while others succumbed.
Some of the most aggressive colonisers of bare ground in the mountains are able to produce adventitious roots from stems buried by silt or gravel, or shoots from erosion-exposed parts which are apparently root tissue in nature. These include Muehlenbeckia axillaris, Raoulia spp., Gaultheria rupestris and
It has been noted that some New Zealand trees and larger shrubs produce adventitious shoots readily from root systems which lie near the ground surface. Moar (1955) recorded this for Dacrydium colensoi and the author has seen it in species such as Hoheria glabrata. Griselinia littoralis, Dacrydium bidwillii and
Amongst the alpine vegetation in New Zealand there are many shrubs, many woody small plants which could be called shrublets and numbers of semi-woody species. There are, in fact, very few soft-stemmed herbs proper. Most of the herb-like species are partially woody or fully woody perennials which creep along at ground level, sending down adventitious roots. This applies, of course, to dicotyledonous plants such as Celmisia discolor, C. lyallii, C. laricifolia, Forstera tenella, Gaultheria depressa, Drapetes dieffenbachii, Coprosma pumila, Ourisia sessilifolia and Geum uniflorum, but even the long-lived monocotyledons like the snowgrasses (
On a recent expedition to Western Fiordland it was noticed that under the thick growth of mosses and liverworts on the trunks of Nothofagus menziesii trees, as much a 8-10 feet above ground level, there were numerous adventitious roots. An investigation of other species in the same neighbourhood— Griselinia littoralis, Coprosma linariifolia, C. ciliata. C. astonii, Neopanax anomalum and
The ‘feeding roots’ of forest species both in beech forest and mixed broadleaved podocarp forest in New Zealand are found in the humus layer of the soil. Similarly in the alpine grasslands — the actively growing root systems proliferate in the humus layer
Chionochloa, as in many other species, there are normally masses of old dead and rotting leaf bases which surround the living tillers. ‘Feeding roots’ are found in these rotting tissues which remain wet even in the driest weather. It is probable that both water and nutrient requirements are largely supplied in this way.
Some New Zealand forest species are obligate epiphytes but many other species are able to exist as facultative epiphytes if the atmosphere is moist enough. This phenomenon is at its best in places of very high rainfall such as Western Fiordland or the Upper Hokitika River. In the latter area the forest is dominated by Metrosideros umbellata and
The facility with which New Zealand plants produce adventitious roots and the ability to utilise humus or peaty material with little mineral matter in it for much of their nutrient supply is a striking feature of our vegetation. There is scope for much future research on the root systems of New Zealand plants.
Additional Note: Since this paper was written a paper has been published (
Present address: C/o, Canterbury Museum, Christchurch, New Zealand.
As many enquiries are made each season, and as early records are somewhat confusing, it is considered as well to clarify the position concerning food-plants of ‘monarch’ butterfly larvae in New Zealand. In various early records the ‘monarch’, Danaus plexippus Linnaeus, 1758. was recorded under the names archippus, erippus, and berenice.
Fereday (1874b BNZE) recorded that a Mr. Meinertzhagen was told by the Maoris that ‘The caterpillar … feeds upon the pollen of the gourd which they grow in that part of the country (Hawke Bay).’ This record is not reliable and is not accepted. Fereday also recorded caterpillars and pupae found by a Mr. Nairn who ‘… had been feeding some new kind of caterpillar …’ and had described ‘… the shrub on which he found the caterpillar as the Gomphocarpus ovata, one of the milk producing plants, and a native of the Cape of Good Hope.’ It is considered by the present author that this is a valid record of Asclepias fruticosa (= Gomphocarpus fruticosus) as a food-plant of Danaus plexippus. A. fruticosa, the common ‘swan plant’, was recorded as a horticultural escape in New Zealand, under the name of Asclepias nivea, by Kirk (1870), and this species is a native of the Cape of Good Hope.
Asclepias curassavica but, as it is not known if this plant was at that time present in New Zealand, it seems best to consider the record as Asclepias sp. Colenso (1878 BNZE) was alos obviously referring to an Asclepias when he described ‘cotton plants’ and ‘… green capsule having the remains of soft spines …’. Records by Butler (1878 BNZE) and Asclepias sp. was given by Danais archippus became abundant in Wanganui
Gomphocarpus, …’. J. J. Walker (1914 BNZE) mentioned Gomphocarpus fruticosus R.Br. as a food-plant at Sydney (Australia) but did not record it as such in New Zealand. Tillyard (1926b BNZE) recorded two plant species, as ‘… Asclepias physocarpa (Gomphocarpus fruticosus) and A. curassiva.’, but as they were not specifically for New Zealand they are here considered to be Australian records. Gomphocarpus fruticosus,’, while Cottier (1956) gave the first record of Araujia sericofera as a food-plant in this country.
The known food-plants in New Zealand are all of the family Asclepiadaceae, members of which are sometimes known as ‘milkweeds’ or ‘cotton plants’. The species concerned are as follows :-
Asclepias curassavica L. Commonly known as the ‘blood flower’ this plant has also been called ‘red-head cotton’ in Australia. It is not common in New Zealand but is grown in some gardens and is known to be a food-plant here. This is the first undoubted record for this country.
Asclepias fruticosa L. (= Gomphocarpus fruticosus R. Br.), This, the ‘swan plant’, is generally known as a food-plant in New Zealand. In Australia it has been known as ‘bladder cotton’, ‘white cotton’, etc. Asclepias physocarpa Schlect. (= Gomphocarpus fruticosus Sims, not R. Br.) is a species very close to A. fruticosa L. and. although apparently not known in New Zealand (apart from one mention in a commercial catalogue), may well be grown here under the name of ‘swan plant’. It is a potential food-plant.
Araujia sericofera Brot. (= Araujia sericifera auct.), Although ‘monarch’ caterpillars are not known to occur naturally on the ‘moth-catching plant’ they will readily feed on leaves of this plant when supplies of the ‘swan plant’ have been eaten out.
The author wishes to acknowledge the assistance of Dr.
All references included in the ‘Bibliography of New Zealand Entomology’ (Miller, 1956) are referred to that work, in the above text, by the appropriate date and letter, followd by the letters BNZE. e.g. Butler (1878 BNZE), Fereday (1874b BNZE). Other references are given below.
This paper is not only an attempt to reconstruct something of the vegetation pattern but also to draw the attention of botanists and others to the need for archival research required by a topic of this nature. Thanks are due to MissA. Simpson for checking the botanical nomenclature.
The effects of the introduction into New Zealand of ‘European’ plants and animals have been described by a number of specialists in several fields notably Thomson, 1922, and Wodzicki, Others (Cumberland 1941 1961. 1962b; Holloway 1959; Johnston 1961) have attempted to reconstruct the pre-European vegetation on a New Zealand-wide basis. Clark (1949) notably, has shown in some detail, the successive impact of man and his plant and animal domesticates on a land that lacked indigenous grazing mammals. Clark, discussing the initiation of large-scale settlement in the South Island during the 1850's, rightly draws attention to the damage done to the vegetation by cutting, burning and the proliferating sheep. However, it is often not realised that a similar process was initiated in the Wairarapa district, almost a decade before settlement in the South Island began.
This paper is an attempt to describe the vegetation pattern of the Wairarapa on the eve of settlement in 1843, the manner in which the indigenous vegetation was attacked and the way in which new plants and animals were introduced.
The research on which the paper is based was predominantly archival and no attempt will be made to link present-day survivals with past conditions.
The vegetation of the Wairarapa in early European times was characterised by variety. The whole area was a patchwork of grass, swamp, scrub and forest mingled in varying proportions. This is well illustrated by Bidwill's description of the area adjoining Bidwill's Ridge, which is located between Featherston and Martinborough, about two miles from the latter. The land along the Ruamahanga River was in dense bush and fringing the Ridge was a swamp containing Phormium tenax. ‘About a mile to the north were low-lying ridges on which grew manuka (
To the west of Lake Wairarapa, the mixed podocarp/broadleaf forest extended down from the Rimutaka Range to reach the lake margin and similar salients of bush extended into the valley at several points, notably in a 20,000 acre block between the Waingawa and Waiohine Rivers. At its northern end the valley was closed off by an area of bush-clad hills and down-land that extended with little break to a clearing in the vicinity of the Manawatu Gorge. Bush then continued as far as the margins of the tussock lands of the Ruataniwha/Takapau basin. There is no reason to suspect that the podocarp/broadleaf forest was in any way unlike that covering much of the remainder of the North Island, although Colenso considered the North Wairarapa forest the most primeval of any he had seen in New Zealand. ‘The soil for many feet was composed of vegetable matter … and the trees were of immense size. The birds were very few … and a death-like silence reigned’ (Colenso, Journal), The last was probably a localised phenomenon since another observer claimed that ‘the woods are alive with kakas and pigeons’ (Weld in Lovat. 1914. p. 50). Colenso also noted some of the forest-dwelling grasses such as Oplismenus undulatifolius, Poa imbecilla, P. anceps, Microlaena spp., herbs such as
In the lowland short tussock, Poa anceps and Festuca rubra or F. littoralis (coastal) were probable co-dominants but Agrostis and Danthonia were also reported, particularly Agrostis parviflora, Deyeuxia quadriseta, Danthonia bromoides, D. semi-annularis, Agropyrum multiflorum and A. scabrum were also reported by Colenso as being abundant more especially on the hills and terraces above the actual valley floor (Hooker, 1867, p. 327). Mingled with the Graminae were Umbelliferae such as Angelica montana and
The swampland was of two types, neither of which were described in detail by then contemporary observers. In the vicinity of the present Morrison Bush was the Arundo conspicua), raupo (Typha angustifolia), Alxopecurus geniculatus, Hierochloe redolens, Zoysia pungens (especially near the sea),
The swamps and lake margins were the habitat of large numbers of ‘duck, widgeon and teal’ (Weld in Lovat, 1914, p. 50), probably pukeko (Porphyrio melanotus), the bittern ( Botaurus poiciloptilus) and ducks such as the paradise (
In the hill country to the east of the Wairarapa Valley, the four major elements of forest, grassland, fern and scrub and swamp were repeated but with grassland and swamp being found only in small discontinuous patches. The Haurangi and Maungaraki Ranges were largely in mixed podocarp/broadleaf forest with some beech at around 2,500 feet. However, the hills, as distinct from the ranges, were largely fern-clad but with a good deal of Angelica spp. and grass among the fern. Weld noted that this was the case near Whareama (Weld, 1844). At Castlepoint the hills were mainly in grass with small quantities of toe-toe, manuka and fern, although the hills furthermost from the coast were in bush (D'Urville, 1826-27, p. 104), Although most of the valleys in the area are steep and narrow, some of the larger valleys were sufficiently broad to contain a good deal of swamp. The lower Whareama Valley, for instance, was ‘swampy and ankle-deep in water, full of pig ruts and covered in toe-toe’ (Weld, 1844). At Porangahau the valley was less swampy and contained about 3,000 or 4,000 acres of grass (Thomas and Harrison, 1845). Grass extended inland from Porangahau in a broad strip that reached the
Into this wilderness of bush and scrub, swamp fern and grass, came successive small groups of men, numbering perhaps 100 in all. With them came mobs of sheep laboriously ‘back-packed’ past the Muka Muka rocks which were then washed by the sea. With the ‘squatters’, so named because they occupied the land illegally, came also cattle, dogs, horses, guns, axes — all to radically modify the ecology of the area. As the squatters changed the overall macro-faunal pattern by introducing grazing mammals into a fauna singularly poor in mammals of any kind, the herbivores in turn added to and modified the overall micro-faunal and floral patterns.
Direct attack on the vegetation by fire did not greatly affect the forest, not only because healthy forest is fairly difficult to destroy by this means (Sage 1954, p. 58, and Cumberland 1961, p. 146), but also because it was not really necessary to attempt this as there was plenty of unforested land available (Hill, 1962, p. 41). This land either did not need to be burned before use or it burned much more readily than bush. Burning of scrub, fern and tussock to promote fresh growth for stock was regularly carried out and casual travellers also fired the fern (Bannister 194, p. 5, and Weld, 1844). Where, however, the forest was fired, tall Sonchus spp. immediately sprang up (Allom, 1849, p. 201).
The needs of household fuel, house-building and post-and-rail fencing led to limited felling of bush and manuka. The open country was cleared by hand in parts, Aciphylla especially being removed while common English pastures grasses such as sweet vernal grass (Anthoxanthum ordoratum), timothy (Phleum pratense), Yorkshire fog (Holcus lanatus), cocksfoot (Dactylis glomerata) and couch (Poa spp.) were often sown. Other grasses, such as the Australian forms of Danthonia and Stipa undoubtedly entered adhering to the fleece of merino sheep imported from New South Wales. The Australian sheep burrs, Acaena ovina and Xanthium spinosum as well as the common thistle (Cnicus lanceolatus) and docks (Rumex spp.) must have been introduced in this manner and these were reported as particularly common along the coastal route between Wellington and the Wairarapa (Carter, 1875, p. 87). The escapes of pre-European adventive Brassica spp. have already been noted but the sheep station gardens, as well as the Maori gardens must have provided significant sources of escapes.
The macro-fauna was enriched by large numbers of sheep and cattle, about 40,000 sheep and 3,000 cattle by 1853, and to a lesser extent by horses, dogs and rabbits. Some cattle were driven
Pollenia villosa) and the ‘scab’ mite (Psoroptes communis var. ovis), there were no indigenous hosts to these species (Thomson, 1922, pp. 321-324, 352-354).
Of considerably more significance were the effects of grazing and browsing by sheep and cattle. The broadleaf forest shrubs and juvenile trees were reported as being ‘eagerly devoured’ by cattle (Allom, 1849, p. 201), karaka ( Corynocarpus laevigatus) being particularly favoured. Cattle thus had significant effects upon the species composition of all forest areas to which they had access, and in the absence of fences, these areas must have been quite extensive. The fern and scrub was also opened up by trampling and thus made available for sheep. ‘Cattle … speedily destroy the fern and grass takes its place … the fern has, in many parts, disappeared, and thousands of acres of the native rye-grass, and other grass are now to be found’ (Allom, 1849, p. 21). The grazing of sheep rapidly destroyed a number of species. Both
Although the squatters ‘lived off the country’ to a considerable degree, it is doubtful if they made significant inroads on the large numbers of edible birds. However, wild pigs were valued not only as food for the squatters, but also as items of trade between the Maori and the squatters and ultimately the citizens of Wellington. Hence a considerable diminution of the number of pigs was probable.
The change in both the plant and animal geography of the Wairarapa between 1840 and the mid 1850's is significant for two main reasons. It was this area that first felt the impact of many thousands of livestock spread over several hundred thousand acres, and saw the beginnings of a process that had its ultimate reward in the man-made deserts of Central Otago. That the Wairarapa did not become a desert instead of being largely only a botanical desert (at least in terms of indigenous species) is a tribute not only to the climate but also to the perspicacity of the Wairarapa farmers. The second significant point is that it was rarely the established pastoralists who were responsible for a frontal attack on the forest. Rather it was the small farmer on his 30-100 acre plot hacked and burned out of the bush who sought to replace the forest with pasture.
(Continued from Tuatara, vol. 9, page 97)
In part I, a general account of the anatomy, habits, and derivation of the New Zealand native slugs was given. No key to the species or genera could be given in Part I as two of the four genera and twelve of the species had only recently been discovered, and descriptions of them had not been published elsewhere. Part II, therefore, comprises a key to the New Zealand and Subantarctic Athoracophoridae.
Since the publication of Part I, more information on the derivation of the New Zealand Athoracophoridae has come to light. (Solem, pers. comm.) Solem states that the New Hebridean slugs, in company with other slugs in the North, show a tendency towards grouping of the external orifices, a reduced or absent central radula tooth, and a reduction in the slime producing organs. By analogy with other groups, he concludes that these features show that the northern representatives of the group are more advanced than those in the south, and he thus argues that the group evolved in the north and then spread south to New Zealand and the Subantarctic islands.
Some of the specimens mentioned in the key have been described from a single specimen. In the main, these species come from areas where very little collecting has been done. Many species, such as Pseudaneitea schauinslandi and Athoracophorus maculosus have a very limited range, and much more collecting needs to be done before a comprehensive picture of the number of species and their distribution can be formed.
There is only one species in this genus. This is P. verrucosus (Simroth) 1889.
Diagnosis. 20 lateral grooves, nearly all unbranched. Papillae very numerous, small, conical. Colour uniformly black, or yellowish-brown with a median black stripe, and bands of black streaks and spots flanking the midline on either side. Auckland Islands.
By
(Published by the American Entomological Institute, 5950 Warren Road, Ann Arbor, Michigan, U.S.A. Price $14.50).
The publication of this comprehensive and carefully compiled catalogue provides a valuable contribution towards a better understanding of the systematics and nomenclature of Oriental and Australasian Ichneumonidae. The catalogue covers a geographical area including southwest Asia, Australia, East Indies and the islands
Each citation in the catalogue gives the name adopted by the authors, the reference, notes on the contents of the reference, localities and host species, and in the case of original descriptions the sex and locality of the type and the museum where it is preserved. All references in the specific synonymy have been seen b ythe authors except where it is statd otherwise. The following statistics taken from the catalogue are given to indicate the considerable amount of research that has gone into the preparation of this indespensable work. Genera contained 383; species contained 2,579; new specific synonyms 316; new generic synonyms 207; new combinations 1,227; new names 47; and new genera 12.
The reviewer cannot agree with the systematic positions given to several Australian genera, as for instance in the case of the genus Labium Br. which the authors place in the subfamily Xoridinae, but in the reviewer's opinion is more correctly placed in the subfamily Ichneumoninae. However these differences of opinion on the systematic position of one or two genera, are of minor importance when the catalogue as a whole is considered and the authors are to be congratulated in considerably clarifying many problems in the systematics of this difficult family.
As far as the nomenclature adopted in the catalogue is concerned, the reviewer is not always in agreement with the authors on their choice of names for several genera and higher catagories, and it would appear that more general agreement will have to be reached before we can obtain a high level of stability that is so essential to the progress of knowledge in this family.
An important part of the catalogue are the keys to subfamilies, tribes and genera compiled by Henry Townes. These keys are the most satisfactory ones so far published, at least for the Australian and New Zealand faunas and with a little experience and care may be used with confidence and will be of great practical value to the student.
Finally there are generic descriptions of the new genera included in the keys, on pages 471-474, index to hosts and parasites and a comprehensive index of the names appearing in the catalogue.
The authors and publishers are to be congratulated on producing a very attractive volume and for the care they have taken in the setting up and printing of the catalogue.
(continued from Vol. 11, p. 56)
The End
Clarendon Press, Oxford
xiii + 387 pp., N.Z. price 43/6
Endocrinology is a discipline which does not fall neatly into any of the major divisions of biology, or which may be studied using the techniques peculiar to any of these divisions. This does not mean that anyone can be an endocrinologist. but rather that the concerted efforts of anatomists, morphologists, histologist. physiologists, ecologists, biochemists, pathologists and geneticists are required for the advancement of this branch of biology, and that its material must be derived from all the divisions of the animal kingdom.
The book sets out to develop this proposition, in an orderly and logical framework, in fifteen chapters. Chapter I is introductory, explaining the principles applied to the exposition of the subject. In Chapter II one of the most primitive of the hormone systems — that concerned in the functioning of the alimentary tract — is dealt with at some length, for historical reasons, and because of the lessons that emerge from its description, regarding the pitfalls that abound for those who build elaborate generalisations on an insufficient coverage, both in width and depth, of the available animal material. Hence this chapter serves as an introduction to the methodology of the subject as a whole. As in subsequent chapters, the anatomy and histology of the relevant tissues are described, with adequate illustrations, as well as the physiological context, and due attention is paid to the evolutionary and phylogenetic aspects. The account is enlivened by intimate details of the actual discoveries, such as Bayliss and Starling's experiment on a denervated jejunal loop of January 16, 1902, which established the existence of secretin: I remember Staring saying: “Then it must be a chemical reflex” (when application of acid to the jejunal mucosa was followed by pancreatic response I. Rapidly cutting off a further piece of jejunum, he rubbed its mucous membrane with sand in weak HCI, filtered, and injected it into the jugular vein of the animal. After a few moments the pancreas responded by a much greater secretion than had occurred before. It was a great afternoon.’ It was from this occasion, too, that the term ‘hormone’ originated: this was suggested to them by Hardy, who derived it from the Greek hormaein, meaning ‘to impel or arouse to activity’; Bayliss later said that ‘although the property of messenger was not suggested by it, it has been generally understood as carrying this meaning.’
The subsequent vicissitudes of this, and of other supposed hormones of the digestive tract, are followed in an equally fively way, which involves the consideration of its conditioned and unconditioned reflexes, and is epitomised in a series of criteria of the existence of hormonal mechanisms. This chapter requires very little specialised knowledge, and could be read with enjoyment and profit by a second-year student of zoology, physiology, or biochemistry.
The parts played by hormones in control of metabolism are lucidly set out in Chapter II, which deals largely with the functions of insulin and other hormones regulating carbohydrates metabolism in a wide variety of vertebrate phyla, and which attempts to link the data with evolutionary considerations.
Chapter IV introduces the pituitary gland, called by Langdon-Brown, in 1931, ‘The leader of the endocrine orchestra’; the role of conductor of this orchestra now tends to be assigned to the hypothalamus. Vesalius regarded the hypophysis as being no more than a funnel for draining condensed humours from the brain into the nose. After decades of hollow laughter at this naive concept, we have reverted to something similar; the neurohypophysis is now thought to be little more than a temporary receptacle for neuro-humours draining from the hypothalamus. Barrington extends the scope of neurosecretion to all nerve cells, and this theme is developed in this and in subsequent chapters. The functions and chemistry of various polypeptide hormones are described for a range of vertebrate phyla. Here the terminology used is confusing to the non-biochemist; the oxytocins and vasopressins are described as being octapeptides, taking cystine as being a single amino acid, yet the numbering of the amino acids (p. 84) is based on a nonapeptide convention, involving two cysteine residues, with the penultimate member of the chain (leucine, lysine or arginine) designated as being the eighth of a nine-residue sequence.
The nature and physiological functions of the hormones concerned in reproduction of vertebrates are dealt with in the next two chapters. The structure of the mammalian ovary is first outlined, and this is followed by a description of the cyclical changes taking place in it, and in the vagina, during the oestrous cycle. The female sex hormones are then enumerated, their structural formulae are shown, and rules of nomenclature are explained, not altogether correctly with regard to the alpha— & beta— series of oestrogens. Incidentally, the structural formula for cholesterol (p. 101) is wrong — there should be no H at C-5. The role of the liver in inactivating oestrogens by coupling with glucoronic and sulphuric acids is not mentioned, although it is of extreme importance, both to the foetal and to the maternal organisms. The structure and function of progesterone, of both luteal and placental origin, are next discussed, for a range of mammalian species.
Much the same treatment is then given to the male gonad, with the structural formulae of the principal naturally occurring androgens. The author then proceeds to give a oclear description of the pituitary gonadotropins (follicle stimulating hormone, interstitial cell stimulating hormone, and prolactin), and of their complex interrelations with the gonadal and progestational hormones; thus he specifies ten or more hormones as being concerned in mammary gland functioning in the rat. The diverse effects induced by administration of prolactin to vertebrates other than mammals are described, and interesting speculations regarding its evolutionary history are advanced.
Having established that ovulation is regulated by release of follicle-stimulating hormone from the adenohypophysis. the author proceeds to an exposition of the evidence that this release is, in turn, under neural regulation, again from the hypothalamus, and probably mediated by the release into the infundibular portal system of a neurohormone. Finally, the feed-back mechanism of regulation of hypophyseal secretions, whereby the hormonal products of stimulation of the gonad suppress production and/or release of hypophyseal tropic hormones, is explained. Chapter V ends with a description of the phenomena of sexual periodicity in female mammals, and of the diverse factors, both intrinsic and environmental, associated with maintenance of the rhythm.
Chapter VI deals largely with the same problems as in the preceding chapter, as applied to vertebrates other than mammals, in particular, birds, amphibia, and fishes, and a fundamental uniformity of principle is shown to hold, side by side with a diversity of factors. A section of this chapter describes the effects of the various endocrine and environmental factors on behaviour, throughout the animal kingdom, and the possible implication of the thyroid gland is suggested. The problems of viviparity are expounded, and the contribution of the endocrine systems to their solution are explained. The role of the placenta as an endocrine organ in some mammals is described graphically as amounting to an early vote of no-confidence in the parent's capabilities by the embryo. Sexual differentiation in embryonic amphibians, birds, and mammals is followed in detail, and the phenomena of inter-sexuality and sex reversal are discussed in the light of the factors operative in determining foetal sex. Strangely enough, the author here makes no reference to the effects of excess or deficiency of X and Y chromosomes, as in the Klinefelter and Turner syndromes, although it was in 1959 that Jacobs et al. reported the association of the XXY karyotype with the former syndrome.
Chapters VII and VIII are devoted to the phylogeny, embryology and functions of the endocrine glands originating from the pharynx — the thyroid, parathroids, and thymus. In these chapters the author ranges far and wide in the field of thyroid functions. biochemistry, evolution, and pathology, giving a fascinating account
The well-known effects of thyroxine on metamorphosis of amphibians and teleost fishes, and the less-known effects on behaviour patterns of some fishes, are discussed impartially and judiciously, and the chapter closes with an account of mutual thyro-pituitary control.
Chapters IX and X deal with the adrenal gland. As in the earlier chapters the history of the elucidation of its anatomy and functions in different phyla is given, and this is followed by an account of the catechol hormones of the medullary portion of the gland, of which adrenaline was discovered by a Harrogate physician, Dr. Oliver, in 1896, while noradrenaline was only recognised as being physiologically the more important hormone fifty years later. The latter hormone is shown to be a specific neurosecretory product of the sympathetic system, and the importance of the sympathico-chromaffin complex in mammals and other vertebrates is discussed. Chapter IX ends with a brief discussion of the differences between hormones and neurohumours, arriving at the reasonable conclusion that no useful purpose is served by attempts at their rigid differentiation.
Chapter X is devoted to a consideration of the development, organisation, control, histochemistry, and products of the adrenal cortex. In view of the very voluminous literature of these subjects, the author is to be congratulated on the discrimination exercised in selecting from it the items strictly relevant to his main theme. Much more might have been included, such as, for example, the biochemistry of production of the corticosteroids, but in a relatively small book, such as is this one. much has, perforce, to be omitted.
Colour changes in vertebrates are dealt with in Chapter XI. The role and structures of the melanocyte-stimulating hormones of the adenohypophysis of different mammalian species are discussed, as well as their activity in other vertebrates. Very recent work on the part played by the pineal gland, with it characteristic secretion melatonin, is included here. In discussing the evolutionary aspects of colour control, the interesting proposition is advanced that this had survival value in bridging the transition between living in a fully aquatic environment and under terrestrial conditions, involving exposure to extremes of temperature.
Chapter XII covers, in twenty-five profusely illustrated pages, the organisation and evolution of the pituitary gland of a range of animals, from mammals to tunicates.
Chapters XIII and XIV deal, respectively, with hormones in crustacea and insecta. The subject is treated with the reserve and caution imposed by the small amount of work so far done on a very small minority of representatives of these classes, and these chapters should be of real use to biologists who have been trained in vertebrate physiology only. A very interesting, though necessarily brief, survey of the ectohormones (pheromones) of arthropods is included in Chapter XIV.
The book closes with a chapter on some evolutionary aspects of endocrine systems. It is supposed, reasonably, that such systems are phylogenetically more ancient than are nervous systems, and it is suggested that the thyroid, steroid, and neurohormones are direct legacies from the most remote ancestors of the present metozoa, although modifications in their functions may well have developed with increasing complexity of metazoan organisation. The key position of neurohormones is pointed out, and it is postulated that they are the initiators of sequences which spread throughout the organism, giving rise to end-effects on various target tissues, remote by two or three steps from the neurohormone. The last sentence is a quotation from an unnamed source: ‘a worried frown has replaced the lifted eyebrow as the proper expression for pundits’.
The book has an adequate index, and a very useful bibliography, giving recommended reading for those wishing to make a more profound study of the subject matter contained in the various chapters. It is well printed, on good paper, and is singularly free of typographical errors; the only ones noted by the reviewer were: simulation for stimulation; responsible for responsive: and prostrates for prostates, on pp. 112, 132. and 147 (Fig. 49). respectively. A pleasing feature of the book is the absence of distracting footnotes, and an even more pleasing one is its low price (43/6 N.Z.); it would be hard to find a reference book containing 139 figures and seventeen plates at a price approaching this. The book can unreservedly be recommended for undergraduate teaching in zoology, and for reading by all those concerned in the life sciences, at any level.
The cell wall is important biologically for four reasons: (1) Since it completely surrounds almost all plant cells, materials entering or leaving cells must pass through it. (2) As one of the main differentiating cellular elements it determines the morphology and to some extent the functions of the cell. (3) Since it is present early in the life of a cell and develops with it. it is possible that it carries with it some kind of developmental record. (4) Since it forms the limiting envelope of the cell it may be directly involved in regulating cell expansion. A study of the structure and properties of the cell wall, therefore, may give information about the nature of the growth process.
There are also technological reasons for knowing something about cell wall structure. The properties of timber, and of pulp and paper, are dependent to a very great extent on the molecular structure of the plant cell wall, and an understanding of wall structure might point the way to technological improvements.
As might be expected, a tremendous effort has been put into the study of the structure and growth of the cell wall over the years; but one of the surprising things that comes out of a consideration of the literature is how little is finally resolved about fundamental processes of wall formation and wall growth. In this paper, an attempt will be made to review the present state of our knowledge on these topics and to point to some of the fundamental problems which are so far unsolved.
The principal constitutents of the cell are cellulose, hemicellulose, pectic substances, lignin and proteins. Waxes, together with cutin, suberin and sporopollenin are also found.
There is another class of substances (gums, tannins, colouring matter, etc.) whose presence becomes noticeable as sapwood passes into heartwood. They are not regarded as normal constituents of the cell wall, as they generally appear after the death of the protoplasm. Technologically they are important, however, because they render heartwood less susceptible to attack by fungi, and insects.
Some cell walls also contain mineral deposits, e.g. calcium carbonate, and silicates.
Cellulose is the skeletal substance of the cell wall, and is the most aboundant substance in the plant kingdom. It is a polymer of B- d- glucose residues joined in long chains by 1-4 links (Figs. 1a and b). Over certain parts of their length these chains lie parallel to each other and are very regularly spaced, so as to form long crystalline microfibrils. A microfibril may be thought of as having a highly crystalline core (70Å × 30Å in cross-section) surrounded by a para-crystalline region, which makes the overall dimensions about 100Å × 50Å. About 80 molecular chains occupy the cross-section of the core, the width and breadth of which is generally about 70Å × 30Å. In some species (Valonia and Cladophora, for example), the crystalline core is much bigger in section (200Å × 100Å). Around the outside of the crystalline core there are one or two layers of chain molecules, the crystallinity of which is upset by the incorporation of chain compounds other than glucans. A cross-section of a microfibril is shown in Fig. 2. The appearance of microfibrils on the inner wall of a Nitella cell is shown in Fig. 3 (a) and the appearance of individual microfibrils in Fig. 3 (b).
The hemicelluloses are a class of substances which dissolve in alkali. but are not soluble (or are only slightly soluble) in water. On hydrolysis they yield mainly d-xylose. d-galactose, d-mannose, l-arabinose and l-rhamnose. In contrast to cellulose, the hemicelluloses are generally not crystalline in their natural condition, although they have been found in a crystalline state after extraction (Roelofsen. 1959).
The pectic substances are polymers of galacturonic acid which are found mainly in the middle lamella and in primary walls. They are probably amorphous in the concentrations in which they are usually found, although crystalline regions have been found in the walls of certain collenchyma cells which have a high pectin concentration (Roelofsen and Kreger, 1951).
Lignin is an amorphous substance which occurs as an incrustation between cellulose microfibrils. The concentration is highest in the
The outermost wall of the epidermis of most above-ground organs in land plants is completely covered by a water-repellent layer called the cuticle. It consists of cutin probably with an admixture of wax. Another closely related substance, suberin, occurs mainly in the periderm.
Protein: Although in some preparations much of the protein is undoubtedly derived from cytoplasmic debris, there is no doubt that some part of it occurs in the wall itself (Tripp et al., 1951). Preston (1960) has reviewed the role of polysaccharide-protein complexes in both plant and animal physiology, and points out that although there is no direct biochemical evidence of close association between cellulose and protein in plant cell walls, morphological and structural determinations, together with evidence from parallel conditions in animals (where there is an apparent association) is strongly suggestive that there may be an association in the plant cell. Ginsburg (1961) has investigated the factors which modify the action of chelating agents in dissolving the intercellular cement in plant tissue (pea root tips), and has reached the conclusion that the intercellular cement can be regarded as an oriented gel structure containing protein molecules cross-linked by two types of metallic ion. the metallic cross linkage being chelate in character.
The characteristic feature of cellulose which distinguishes it from the other components is that is normally occurs in the form of crystalline microfibrils, whereas the other components are not normally thought to be in this form. Its structure is such that it can only be elongated by stretching primary valence bonds and by opening valence angles. Treloar (1960) has estimated the modulus of elasticity of cellulose from the strength of the C-C linkages and the C-O-C linkages. The value of 10 × 106 Ib./sq.in. so obtained is in good agreement with the highest value obtained on well-oriented native fibres (14.5 × 106). For comparison, the corresponding figure for steel is 28 × 106 Ib./sq.in. The fact that these cellulose microfibrils are such effective reinforcing cell wall components has great signifiance in any discussion on how the wall deforms during growth and, in particular, in any discussion on the way in which particular arrangements of microfibrils in the wall influence the shapes which cells ultimately acquire. It is fortunate, that because of its crystallinity, it can be studied in great detail by a number of techniques, and such studies have thrown a great deal of light on the nature of the growth process.
In discussing cell wall organisation it is usual to distinguish between two types of wall. The wall which surrounds the growing cell while it is increasing in area is the ‘primary’ wall. About the time the cell ceases to increase in area, it starts to lay down a ‘secondary’ wall inside the primary wall. As a rough approximation, one can think of the primary wall as increasing in area, while remaining constant in thickness, and the secondary wall as remaining constant in area while increasing in thickness.
The primary and secondary walls are different in chemical composition and in fine structure, and therefore, have different physical properties. It is the thickened secondary walls which comprise the great bulk of the material we call wood.
The principal constituents of some selected cell walls are given in Table 1.
In the wood of Pinus radiata the percentages of cellulose and lignin are high while the pectic substances are present only in trace quantities, if at all. In the growing cells of the cambium, however, lignin is absent and the percentage of pectic substances is quite high.
A clear distinction between the composition of growing (extending) and mature walls is also shown in the case of cotton hairs.
Because of its ability to form gels, it has been thought in the past that pectin was a necessary component of rapidly expanding cell walls—e.g. the high pectin content of the cambium and of growing cotton hairs. The pectin content of the primary wall of Avena coleoptiles is very low, however, and it seems that in this case the special properties of these walls depend more on the presence of a high proportion of hemicelluloses than on the small amount of pectin. More will be said about this later.
The figures in Table 1 are on a dry weight basis, but the primary wall in particular, in its native state, is highly hydrated. Roelofsen (1959) obtained a figure of 60% for the water content of isolated walls of corn coleoptiles. Figures as high as 90% are often quoted.
The cell plate arises in the equatorial plane of the fibril spindle which connects the two daughter nuclei. It usually shows a gradual expansion, by which it finally reaches the cell wall and it is commonly assumed that this is due to new material being deposited along its circumferences. The cell plate is considered to consist partly, or perhaps mainly of pectin, but the chemical evidence for this view is, however, rather meagre. It is usually isotropic between crossed nicols but later it becomes positively birefringent. At this stage the cell plate consists of three layers; namely, the middle lamella and two primary walls. There are two different opinions with regard to the way in which the two primary walls join the wall of the mother cell. One view is that the daughter cells form new and completely continuous primary cells within the envelope of the mother cell. The other is that the primary walls formed on the cell plate become continuous with the existing wall by a process which involves breaking down the old wall to some extent and re-synthesising this local area of wall so that the new and old primary walls are fused. The weight of evidence seems to be in favour of the first view, but it is not proposed to consider this further here.
The plant cell wall can be separated into two distinct phases; a highly crystalline phase consisting of the microfibrils and an ‘amorphous’ phase which is the matrix in which the microfibrils are embedded. The bulk of the growing primary wall is made up of the amporhous matrix and water. Estimates of the volume of the primary wall occupied by cellulose microfibrils is of the order of 5 to 10% of the wet wall volume.
A very great deal of work has been done on the structure and organisation of the wall, and on the changes which take place as the wall increases in area. The study of cell physiology during growth and, in particular, in the presence of plant growth substances, has resulted in various suggestions being put forward as to possible mechanisms of cell elongation. Before we can consider these, however, certain basic information is required. For example, it is important to know something about the structure of the primary wall.
The arrangement of cellulose microfibrils in some young isodiametric cells is such that they run in all directions within the plane of the wall with no preferred direction; for example, in apical initials of onion roots (Scott et al., 1956) and in the first formed wall of Valonia (Steward and Muhlethaler (1953).
If the cell is elongated, however, one usually observes a net transverse orientation. Several types of elongated cells were studied by Roelofsen and Houwink (1953, 1954) who carried out an electron microscope examination of the cell wall of Phycomyces sporangiophores, and of growing hairs of Gossypium (cotton), Ceiba and Asclepias, Tradescantia staminal hairs, and root hairs of Zea mays. They were struck with a feature which was common to all of these cells, viz., that on the inner wall there was a compact transverse arrangement of microfibrils while, on the outside, there was a very loose texture with the microfibrils either oriented in an approximately axial direction, or in what appeared to be a completely random manner. They suggested that this difference in the arrangement of the microfibrils could be explained if one made the following assumptions:
As the area of the wall increases and as deposition of new transverse fibrils at the inner surface keeps pace with it, any given group of microfibrils will: (i) tend to assume an axial orientation, (ii) appear to migrate towards the outside of the wall, and (ii) suffer a reduction in fibril density. These changes are shown in diagrammatic form in Fig. 4. The appearance of the Nitella inner surface is shown in Fig. 3a, and the outer surface in Fig. 5.
Because the outside of the wall looked like a loosely meshed fishing net they called this ‘multinet’ growth. It seems to provide a satisfactory explanation of the microfibrillar morphology of elongating walls in which transverse microfibrils are deposited. The theory applies in its simplest form to cells in which growth is uniform over the entire cell wall; for example, in Nitella (Green, 1954). There appears to be no reason, however, why cells in which localised growth occurs should not be regarded as special cases of uniform growth, and, indeed, it was in the attempt to explain wall morphology in cells in which growth is localised (root hairs, sporangiophores, etc.) that the theory was first developed.
The multinet theory does not, however, explain the presence of well defined and well oriented longitudinal bands of microfibrils, which occur on the outside of many cells; for example, parenchyma cells of oat coleoptiles (Wardrop and Cronshaw, 1958), collenchyma cells (Beer and Setterfield, 1958), cortical parenchyma cells of bean stems (Probine, 1963), etc. These bands have often been classified as secondary thickening, but they appear to be present during elongation in even very young cells. What is very puzzling, however, is that they occur on the outer wall of the cell, remote from the cytoplasm.
Roelofsen (1958) has attempted to explain these longitudinal bands by an extension of the multinet theory and by invoking a purely physical process. It does not, however, adequately explain all features relating to these bands.
Although the presence of these longitudinal bands in some cells is not satisfactorily explained, there is little doubt that the multinet theory accounts for most features of the microfibrillar morphology of cell walls with ‘transverse’ synthesis. It has nothing to say, however, about the mechanism by which the microfibrils come to be oriented transversely at the inner surface of the wall in the first instance, or anything about fundamental mechanism of wall extension. These topics will be treated in a later section.
In the almost spherical cell, Valonia (an alga), the first formed wall has no preferred direction of microfibril orientation—the microfibrils are completely random in the plane of the wall.
Transitional lamellae develop, however, which show successively less scatter of microfibrils until, finally, a type of structure is developed which is completely different from ‘multinet’ structure referred to above. The cellulose microfibrils in Valonia ventricosa, for example, are present in three orientations, in separate lamellae. The two ‘major’ directions (A and B) lie on an average at rather less than at right angles to each other; the third orientation (x), which is much less frequent, forms a bisector of this angle. The repeat from one lamellae to the next can be something like ABABAxBABAxBABAxBABABAB. Within each lamella the alignment of the microfibrils is very perfect (Fig. 6).
The Valonia cell remains roughly spherical in shape as it grows so that the microfibrils undergo no major oreorientation as do the transverse fibrils in elongating cells which give rise to ‘Multinet Structure’. Valonia does show another type of wall change during growth, however. Steward and Muhlethaler (1953) have reported that growing sporelings, about sixteen hours old, show a complete primary wall. With further cell growth this wall is stretched and finally torn, so that fragments of this first-formed wall may be seen as patches on the lamellated wall which follows it. The outermost layers of the lamellated wall also tear, but in this case the tears are along lines parallel to the microfibrils. The spaces which open up are not filled with new microfibrils. This is called ‘tearing growth’. It is not much in evidence in walls of higher plants—probably because they are much less crystalline and the microfibrils can slip over and past one another more easily in the gel-like amorphous matrix.
This type of structure is not confined to spherical cells, however. A rather similar structure is also formed by the filamentous green algae Cladophora and Chaetomorpha. In Chaetomorpha growth is entirely intercalary and elongation is confined to the part of cell nearer the base of the filament. The outermost lamellae may be seen to be torn and roll back as flakes forming a collar, which arises from this rupture of outer lamellae in the region of growth. In Cladophora growth is confined to part of a cell nearer the apex of the filament but the lamellae do not roll away—possibly because the amorphous matrix contains pectic compounds in the outer region and this may well make the wall more extensible. Frei and Preston (1961) have found, however, that lamellae from different depths in the wall differ markedly in structure. These differences are of the kind to be expected if the wall has been passively extended during growth, i.e. microfibrils which were laid down a little off axis become more nearly longitudinal and are very straight; those with almost transverse orientation become less nearly parallel to each other.
The microfibrils in these ‘crossed-fibril’ walls therefore, undergo translation and rotation as a consequence of cell extension, in general harmony with the ‘multinet growth’ hypothesis.
In presenting this brief picture of secondary wall organisation the main methods of investigation will be indicated. The conifer tracheid will be singled out for special attention because it is very important technologically.
1. When conifer tracheids are viewed in transverse section in a polarising microscope it is apparent that the secondary wall consists of three layers distinguished by their different optical properties. They are usually indicated by the labels S1, S2 and S3. The S1 layer, which is nearest the primary wall, and the S3 layer, which is nearest the lumen, are usually rather thin. The central, or S2 layer is variable in thickness, being thin in early (spring) wood and thick in late (summer) wood.
The polarising microscope observations may be interpreted as meaning that the orientation of the cellulose microfibrils in the S1 and S2 layers trace out a flat helix around the wall. In the central layer (S2) the microfibrils trace out a steep helix around the wall (Bailey and Kerr, 1935). This interpretation was confirmed by Wardrop and Preston (1947) using a more sophisticated optical analysis. A diagram showing wall structure in Pinus radiata tracheids is shown in Fig. 7 (this anticipates a different interpretation of the S
It was discovered by Preston (1934, 1948) that there was a systematic variation of fibrillar helix angle with cell length. In long
2 layer had a more nearly axia orientation than they had in short tracheids. Preston and Wardrop (1949) have shown that this sort of relation holds for the S3 layer also. Expressed analytically:
L = A + cot theta
where theta = helix angle
L = tracheid length
A and B are constants
A curve for a sample of Pinus radiata is shown in Fig. 8. The dependence of anisotropy of cell structure on cell length has some significance from the point of view of anistropy of wood properties and will be referred to again later.
2. The technique ofX-ray diffraction has also been used to investigate the wall structure of conifer tracheids (Preston and Wardrop, 1949). Two typical diagrams of Pinus radiata (late wood) reproduced in Figs. 9a and b. They are from the third and ninth annual rings, respectively, of a thirteen-year-old tree. The beam was directed through the wall in the radial direction. The helix angle can be estimated from the distribution of X-ray intensity around the 002 arcs, and for the examples given are 11° and 32°, respectively. Because the middle layer of late wood is normally thicker than the other two layers, its structure dominates the X-ray diagrams.
It is not obvious from the X-ray method that there is a three-layered wall structure. The method does, however, provide additional information:
The identity and crystal form of the crystalline material can be confirmed.
It is possible to determine whether a particular crystal plane tends to lie parallel to the wall surface;
An estimate can be made of the degree of crystallinity;
Although it tends to over-estimate the fibril angle, it provides a much quicker and more suitable method for routine measurements than does the polarising microscope.
3. The electron microscope provides a third and newer method of investigating cell wall structure. With the advent of this method, microfibrils could be seen for the first time and the pattern of wall organisation determined in much greater detail. The structure of conifer tracheids determined by other methods was largely confirmed. The S1 layer, however, which lies closest to the primary wall, was found to have a more complex structure than had been thought previously. It has a crossed fibrillar arrangement rather than a single helix of microfibrils (Wardrop, 1957). The sign of the helix changes in alternate layers. The angle between the microfibrils in adjoining layers is about 100° and the microfibrils in each layer make an angle of about 50° with the cell axis. The fibrils are not equally shared between the two directions—one direction dominates the other. This accounts for the apparently misleading evidence of the polarising microscope.
The S2 and S3 layers are also laminated, but do not possess a crossed fibrillar arrangement. The signs of the helices are:
Harada et al. (1958) consider that in addition to the S1, S2 and S3 layers there are a number of lamellae of intermediate orientation between the layers S1 and S2 and between S2 and S3, but there seems little doubt that they are few in number (Harada et al., 1958). Wardrop (private communication) pictures the wall as being organised as shown in Fig. 10.
It has been considered by many people that there is another wall layer inside the S3 layer which is so different in properties as to deserve the name,Tertiary cell wall. Very little clue as to its nature has been found from staining reactions, but it is resistant to a wide range of reagents. It is covered with ‘warts’.
The warty layer has been fully described by Wardrop et al. (1959). They consider that the first indication of the formation of a wart is a localised withdrawal of the plasmalemma from the cell wall and the formation of localised thickenings on the wall. In most cases the indentation of the plasmalemma could be caused by localised wall thickening—but cause and effect here are difficult to separate. Inside each wart. at the tip, there is a small spherical body. This is assumed to be the denatured remains of an organelle which is enclosed by the tonoplast and plasmalemma as the sytoplasm dries on the surface of the lumen. Since each wart seems to have a small spherical body associated with it, it is interesting to speculate on the association between this organelle and the cell wall thickening.
The warty layer can be cross-linked with formalin and when the cellulose is removed with sulphuric acid the layer can be recovered in beautiful sheets. When stripped in this way the warts are often seen in a systematic array as though arranged in a series of helices—this may give some clue to the mechanism of microfibrillar arrangement.
Wardrop (private communication) does not, however, regard it as a ‘Tertiary’ wall layer, and considers it, as was implied above, to be the remains of the plasmalemma and tonoplast.
Returning to the consideration of the secondary wall proper, it is reasonable to assume that the almost axial arrangement of microfibrils in the S2 layer in tracheids of Pinus radiata would result in an anistropy of mechanical properties. This will not be the only factor modifying properties—e.g. anatomy of the specimen and the nature of intercellular adhesion must also be taken into account. Nevertheless, cell wall organisation is important. This was shown by Wardrop (1951) who measured the variation in breaking load in tension of tangential longitudinal sections of
In the case of single fibres, the dependence of mechanical properties on structure is, perhaps, even more striking than in the case of wood because one is dealing with a single cell, and not a group of cells aggregated to form a tissue. Preston (undated) has reported for sisal the figures given in Table 2.
It is generally considered that extension growth of cell walls ceases at, or about, the time that the secondary wall begins to be laid down. Wardrop (private communication) suggests that the tip of differentiating fibres may still be in the extension growth stage after the deposition of the secondary wall has begun. Electron microscope and autoradiographic evidence suggests that the change in microfibril orientation during enlargement of the primary wall is consistent with Roelofsen's multinet hypothesis. Other investigations have shown that the secondary wall is formed by the deposition of successive lamellae of cellulose microfibrils. It does not appear, however, that apposition occurs uniformly over the cell wall. Wardrop has examined developing fibres using the interference microscope and found that the wall is thicker near the centre of the cell than at the ends.
He therefore imagines that secondary wall lamellae are initiated near the centre of the cells and grow in the direction of microfibril orientation towards the tips. This means that the tip may still be in the extension stage after deposition of the secondary wall has already begun at the centre of the cell.
There are cells such as root hairs, stamen hairs, etc., in which marker experiments have shown that extension is confined to a localised region of the cell wall near the tip. The question arises whether the localised extension occurs generally, or whether, in general, extension is uniform over the entire cell surface. (N.B. At this point only the sites of extension are being considered; not sites of synthesis.)
On the basis of electron microscopic examination of cells isolated from elongating coleoptiles by maceration, Muhlethaler (1950) concluded that extension growth in parenchyma took place by what he called ‘bipolar tip growth’. He observed that at an early stage the parenchyma showed thickenings, at the corners of the cell, composed of longitudinally oriented microfibrils. To quote Frey-Wyssling (1953): ‘It is evident that a wall fortified by numerous parallel textured ribs cannot be extended in the longitudinal direction. Therefore, an extension growth, in the classical sense, of such a cell is not possible.’ Muhlethaler also observed that in some cells the walls were thinner and looser in texture towards the ends and the
The autoradiographic studies which showed that the deposition of cellulose takes place over the entire surface of the cell, did not lend support to this theory. Further, in a study of the number and distribution of pit fields in the wall of the elongating Avena coleoptile, Wardrop (1955) showed that the number of pit fields per cell did not change in coleoptile parenchyma at different degrees of extension: or, to put it another way, the number of pit fields per unit of cell surface decreased in cells of increasing length.
If it is assumed that primary pit fields are not transient structures then the conclusion that growth must take place over the entire surface of the wall seems inescapable. This seems to rule out ‘bipolar tip growth’ unless some pit fields in the non-extending portion of the wall are eliminated and new ones created in the newly-formed parts of the wall. This does not appear probable.
Extension must therefore be uniform over the wall surface.
In considering mechanisms of growth the question arises as to whether the cell wall is a living structure, or whether it is merely a non-living secretion product.
Heyn (1940) postulated that there were three theoretical possibilities for the mechanism of wall enlargement:
Active increase in wall material so that enlargement of the wall is a result of deposition of new substances within the wall.
‘Passive’ increase of wall material, intercalation of new particles in the wall being only possible when there is elastic extension under turgor pressure. This extension becomes permanent as a result of the deposition (intussusception) of new particles.
Plastic stretching of the wall under the influence of turgor pressure.
In the first of these, growth is controlled by direct regulation of wall synthesis, while in the other two, growth is regulated by controlled changes in the physical properties of the wall. These possibilities will be examined below.
The ‘active growth mechanism is not much in favour for various reasons. Firstly, there are cases in which cell wall synthesis is much less than proportional to cell enlargement so that the wall becomes thinner during growth (for example, oat coleoptile sections growing in auxin plus sugar — Bayley and Setterfield, (1957),
Further light has been shed on the question by considering the actual site of synthesis during growth. Green (1958) grew Nitella cells in a medium containing tritium which is incorporated into the wall in place of hydrogen. He showed by a counting method that the difference in activity between the outside and inside of the wall was consistent with deposition being confined to the inner surface.
In the study of cell wall organisation in Cladophora and Chaetomorpha already referred to, Frei and Preston (1961) observed (i) that microfibrils were twisted around each other, (ii) that microfibrils from one lamella may pass through the next lamella and become part of the next-but-one lamella of the same direction, (iii) microfibrils from one lamella may interweave with those of the next, and (iv) microfibrils from one lamella may turn through 90° and become part of the next lamella. From this and other evidence, they concluded that while the major microfibril-synthesising machinery must be located in the outer region of the cytoplasm, it must nevertheless be three-dimensional, and cannot be confined to a surface. They considered that it must be limited in thickness, however — perhaps two or three lamella thick, outside which microfibril synthesis cannot occur.
Setterfield and Bayley (1958) published autoradiographs of cross-sections of the outer wall of the epidermis of oat coleoptiles which had been grown in tritium-labelled sucrose, and from these they concluded that both cellulose and non-cellulose material are deposited throughout the thickness of the wall. Ray (undated) has pointed out, however, that while their evidence for the incorporation of non-cellulosic materials throughout the thickness of the wall seems clear enough, Setterfield and Bayley's autoradiograph of the cellulose residue does not support their conclusion that cellulose is synthesised throughout the wall, but supports to the opposite view, viz. that cellulose synthesis had occurred only on the inner surface of the wall.
The ‘multinet’ theory also provides indirect evidence that synthesis of cellulose occurs only on the inner surface of the cell wall, in that it accounts for the difference in microfibrillar arrangements on the inner and outer surfaces of the cell. As was pointed out earlier, however, in the walls of parenchyma cells of oat
Acetobacter xylium, and showed, in an electron microscope study, that microfibrils grew at their tips without contact with the surface of the cells. More work is needed, therefore, before the last word is said on this question of wall synthesis.
In general, however, with the exception that the presence of these longitudinal ribs is not satisfactorily explained, the weight of evidence is that synthesis, of at least the cellulose component, occurs on the inner face of the wall and therefore, active incorporation of material within the wall is not the basis of extension growth. Setterfield and Bayley's work (loc. cit.) indicates that non-cellulosic materials may be synthesised within the walls, but here, too, more work is required.
A variant of the ‘active’ growth mechanism was proposed by Frey-Wyssling and Stecher (1951) and Stecher (1952). In an electron microscope study of actively growing tissue they observed that in the normally loose network of microfibrils in the primary wall, there were, in addition to the normal gaps between fibrils, larger open perforations ranging up to about 1/4 to 1 micron in diameter. On the basis of this observation, they suggested that the cell wall is transiently penetrated by the protoplast at points on the surface and that the microfibrils in this region are pushed aside. New microfibrils are subsequently woven into these areas, the total area of the wall having been increased.
This is an example of growth by intussusception and Frey-Wyssling called it ‘Mosaic Growth’. It now appears, however, that this theory was based on a misinterpretation of the appearance of wall fragments in the electron microscope, and it has fallen from favour.
We now come to consider the evidence for the plastic-extension type of mechanism. The initial suggestion that plastic stretching of the wall by turgor pressure was the primary mechanism of extension growth, was made by Heyn (1955). He measured the elastic behaviour of coleoptiles severed at their bases and placed in humid chambers. Cutting and application of hormone took place an hour and a half after decapitation. Subsequent bending under a weight
More recently, Professor Preston and the author have re-examined this relationship between wall properties and growth (Probine and Preston, 1961, 1962, and Probine, 1963) and the findings of this work are summarised below. The internodal cells of Nitella were used since they are most convenient objects for the study of wall structure and growth. They are so large that the physical properties of the wall can be measured with comparative ease. Further, the wall grows uniformly over the whole wall surface as the cell
It is not clear, however, that this has anything to do with growth, as the extensions concerned are static extensions. When the phenomenon of plastic flow is looked at, however, the situation is even more significant. When a strip of wall cut parallel to the transverse axis is loaded it stretches slightly, but no matter how long the load is left applied no further change in length occurs. When a strip cut parallel to the longitudinal axis is loaded, however, it continues to get longer and longer — it exhibits the phenomenon of plastic flow.
In order to attempt an assessment of any connection between plastic flow and wall growth, the rate of flow was measured on wall strips cut from a series of cells, the growth rates of which were known at the time of cutting. A strip cut from a cell which had grown 16% in length in 24 hours increased its length by plastic flow to the extent of about 13% during the 100 minutes that a load of 0.8 units was applied. On the other hand, a strip cut from a cell had grown in length only 1% in 24 hours, increased its length by plastic flow to the extent of only 1% under the same load. See Fig. 12 for complete results.
These curves should not be taken as literal statements of the behaviour of the material in situ, in the cell, since the load is applied uniaxially in the test specimens, but multiaxially in the cell. Nevertheless, they do show a difference in physical properties between a growing and a non-growing wall, which is consistent with the idea that plastic stretching of the wall by turgor pressure might be involved in the growth process. Further, the direction in which wall plasticity is greatest, is the direction in which growth rate of the cell is greatest. Since wall plasticity in different directions (and, if the plastic flow hypothesis is correct, cell growth) is determined by the arrangement of the reinforcing microfibrils in the wall, it could well be that it is the pattern in which microfibrils are laid down which determines the shape which a cell will ultimately
The idea that growth is indeed controlled by wall properties is reinforced by the fact that spiral growth in Nitella can be accounted for by wall structure (Probine, 1963). Further, it has been found possible to modify wall structure and thereby to produce changes in cell shape (Probine, 1963 (b)). There is not space, however, to discuss this here.
If plastic stretching of the wall is indeed involved in growth, it is to the plastic properties of the amorphous matrix we must look for a further understanding of cell wall growth. The cellulose microfibrils will only vary the plasticity of the wall in different directions. The view is generally held in botanical literature that the walls of growing cells contain a high proportion of pectin (polygalacturonic acid partially esterified with methanol). Because of its ability to form gels it was thought it was the pectic matrix which was responsible for the ‘plasticity’ of growing walls.
It has been shown by Ordin, Cleland and Bonner (1957) that esterification of pectin by methyl-derived carbon is an auxin controlled reaction. This suggests that methylation of carboxyl groups of adjacent pectin molecules, under influence of auxin, may be involved in the splitting of anhydride or calcium bridges which contribute to the mechanical properties of the wall. The bond splitting may require methyl esterification as a primary part of the reaction or may require it to stabilise the split once made. Bennet-Clark (1955) has summarised the effect on elastic properties of the sort of mechanism discussed above as follows: ‘It will probably be agreed that the plastic and elastic extensibility of a poly-galacturonic acid, or in general, of an oxidised hemicellulose, will be markedly controlled by the condition of the carboxyl groups. If these long chain molecules are associated with multivalent cations, minimum extensibility will be found owing to electrovalent binding together of adjacent molecules. If the carboxyls are free, hydrogen bonding will provide considerable tensile strength, but much less than that formed in presence of cations and, finally, when or if, they are converted to methyl esters, there will be a minimal tensile strength as hydrogen bonding will be replaced by Van der Waals forces and so extensibility will be maximal.’
A difficulty in the way of the pectin hypothesis is that Jansen et al. (1960) reported that the hot-water-soluble fraction is almost fully esterified, and in any case this is only 20% of the total cell wall uronic acid. It appears, therefore, the number of possible double salt cross-links, in which auxin does promote methylation, is very small indeed, and it is hard to see how these could be critical in cell
One may conclude this section by pointing out that the issue of cell wall growth is far from resolved. At this stage it is only possible to conclude that, on balance, it seems likely that the primary mechanism of extension is cell wall plasticity, but the changes in the wall which induce the changes in plasticity, which lead to extension growth, must surely be under metabolic control. The nature of this control is, however, not at all clear.
The arrangement of microfibrils in the plant cell wall is highly specific and complex — particularly in the secondary wall. It seems clear that the direction of microfibril deposition must be controlled by the protoplasm, but the mechanism of this control is not yet understood. There are some clues, however. Probine and Preston (1958) have shown that, in Nitella, there is a highly significant correlation between the direction of protoplasmic streaming and the direction in which microfibrils are laid down in the wall. This is not to say that the microfibrils are actually oriented by streaming; merely that the direction of streaming is an expression of a polar structure in the cytoplasm — in particular, a structural polarity of the periphal cytoplasm adjacent to the cell wall (plasmalemma?).
In this regard, it may be significant that in the first-formed wall in Valonia, microfibrils are laid down at random and it is only after the polarity of the cell is established that an oriented system of microfibrils is established. Again, Frei and Preston (1960) have shown that when Chaetomorpha cells are plasmolysed, microfibrils are laid down at random. When the cell recovers from plasmolysis the normal crossed-fibrillar structure is resumed — after the cytoplasm has regained its original configuration.
That microfibril orientation is related to protoplasmic streaming has often been discounted on the grounds that the direction of streaming and the direction of microfibrils do not coincide. There seems to be no difficulty here, however. There is abundant evidence that microfibrils can be laid down by the cytoplasm in at least three directions relative to some reference direction; for example. Valonia. Frei and Preston (loc. cit.) have pointed out that the wall patterns of Valonia and four species of Cladophora and Chaetomorpha, conform to a general pattern, so that it is formally possible to pass from the wall structure of one plant to another merely by changing the orientation of a rectangle (representing the principal axis of the cell) lying over a common grid (Fig. 13).
It may well be that the three directions in Valonia constitute a basic pattern of microfibril synthesis. In a given type of cell, it may be that microfibrils are laid down in only one of these directions giving, say, transverse synthesis which leads to multinet structure in many primary walls. In another type of cell, it may be that two of the possible directions are selected giving the ‘crossed-fibril’ type of structure. In a few cells, e.g. Valonia, all three are selected. The pattern may not only vary from species to species, however, but may also vary in the same cell stages of differentiation (as in the S1, S2 and S3 layers of the conifer tracheids).
This generalisation, however, leaves the details of the mechanism far from understood. Perhaps the next advance will come from an understanding of the surface properties of the plasmalemma.
Regarding the mechanism of extension growth, much more remains to be done. A great deal of evidence points to wall plasticity being fundamental to extension, but the way in which this comes under metabolic control is far from clear. For example: how is plasticity controlled in those cells in which growth is localised?
If wall plasticity is indeed fundamental to extension growth, then the arrangement of microfibrils in the wall (which determines its plasticity in different directions) will set the pattern of wall extension, and, hence, determine the ultimate shape which the cell will acquire. This, clearly, has morphogenetic implications. There is no doubt that, in general, there is a correspondence between cell wall structure and cell shape, and this has been recognised in the form of an often quoted generalisation, viz., microfibrils tend to be laid down at right
Microfibrillar morphology is, of course, not the only factor determining cell shape. For example, Valonia and Cladophora have a similar wall structure but one is nearly spherical and the other is nearly cylindrical. The difference is not one of wall structure, but of localisation of growth. Valonia grows uniformly over its surface and, as one would expect from its structure, grows into a sphere. In Cladophora growth is localised at the apex of the cell so that it grows into a cylinder. Again, in a tissue, while cell shape may be more or less dependent on wall structure, it will also depend to some extent on interactions with neighbouring cells.
Although there is evidence against ‘active’ growth of the wall being the primary cause of extension, there is nevertheless a parallelism between extension growth and synthesis, which cannot be ignored. For example, while wall extension and synthesis are not directly related in Nitella (Green, 1958), they do follow one another sufficiently closely to make one feel that they cannot be entirely unrelated. The mechanism of this interrelation is, however, obscure. The number of cases in which the plant seems to be able to compensate for increased mechanical stress, for example, suggests that a ‘feedback’ mechanism may be involved.
It was pointed out in the discussion of Table 1 that the chemical constitution of primary and secondary walls differed greatly. The
A number of workers have studied cytoplasmic organisation in differentiating cells in the hope of throwing additional light on the problem of cell wall differentiation, but the results so far have been disappointing.
Perhaps the best way to close is to say: Much has been done; little is yet really understood; much more remains to be done. The result of this future work should be rewarding.
Apropos ‘I.F's.’ comments on the gyrations of the hedgehog, the following may be of some interest.
For two good reasons hedgehogs practise, in the gloaming, the old proverb: ‘One good turn deserves another.’ If I.F. had carried the observations further, in a true biological spirit, instead of damping their ardour with a glass of cold water, she would have, undoubtedly, discovered, at least, one of the reasons for the monotonous hilarity of the ‘hedgehog reel’.
During the mating season, when two well-behaved hedgehogs meet, it is a signal for the commencement of the ‘reel’. On meeting, two males will ‘doff’ the prickles of the ‘forehead’ at each other with an angry ‘snuff’ by way of a challenge. The greetings over, they move round to a point of vantage to commence the first movement of the ‘reel’. Recently, an American biologist inquired of me whether the hedgehogs in the Southern Hemisphere rotated clockwise or counter-clockwise, but as my observations do not describe the complete cycle I merely quoted the above proverb!
Nature has provided hedgehogs with an almost impenetrable armour of acute prickles which can be swivelled round to form a protective shield on the side it is most needed. The only vulnerable area is the
chassé — there is no other reply to the adherent ball of prickles. The last movement is the parting of the ways — the vanquished, freeing its foot between ‘chews’. makes a fast get-away with a mangled foot or an abbreviated limb!
A variation to the male ‘reel’ is seen when the opposite sexes meet. The opening bars are very similar to those already described, but the female usually stays put, adjusting her armour to meet the point of attack or pivots round to face her suitor as he circles round her at ‘hedgehog speed’. At times, she will make off, with the male in hot pursuit, trying to cut off her retreat. If he succeeds, the ‘reel’ is resumed once more to the accompaniment of much snuffing and puffing. This ceremony continues for a considerable time. Occasionally, the ‘duet’ is transformed into the ‘eternal triangle’ or into a ‘quadrille’. Under such circumstances the female is kept whorling as the males beat a measured tread round her, snuffing and puffing as they go. But I have never witnessed the ‘grand finale’. However, it is interesting to observe that when the female is beseiged by several males, the males ignore each other and continue the ‘reel’.
(Tuatara, Vol. 7, page 131, 1959)
Persephonaster neozelanicus, as also the three Indonesian species P. euryactis, P. luzonicus and P. anchistus, have broadened inter-radial inferomarginal plates, separated by fascioles. In this regard they differ from Persephonaster croceus (the type species), and from other known species. The four first-named species may be considered as comprising a distinct genus, for which the name Proserpinaster nom. nov. is proposed, with type P. neozelanicus Mortensen. The key entry 12(11) is to be amended accordingly.