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BRITISH HYPOGEOUS FUNGI by LILIAN E. HAWKER Departmentof Botany, Universityof Bristol

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BRITISH HYPOGEOUS FUNGI by LILIAN E. HAWKER Departmentof Botany, Universityof Bristol [ 429 ] BRITISH HYPOGEOUS FUNGI BY LILIAN E. HAWKER Departmentof Botany, Universityof Bristol (Communicatedby W. Brown,F.R.S.-Received 16 May 1953- Revised30 July 1953) CONTENTS PAGE INTRODUCTION 430 Methods of collection 430 Examination and preservation of material 431 Habitat 431 (a) Nutrition 432 (b) Soil conditions (H-ion concentration, texture and aeration) 432 (c) Weather 433 KEY TO THE GENERA OF BRITISH HYPOGEOUS FUNGI 435 PHYCOMYCETES 436 Mucorales. Endogonaceae 436 Systematic position of Endogone 444 ASCOMYCETES 444 Plectascales. Elaphomycetaceae 444 Systematic position of Elaphomyces 453 Tuberales 453 (I) Pseudotuberaceae 454 (II) Geneaceae 459 (III) Eutuberaceae 467 (IV) Terfeziaceae 503 Theories of relationship within the Tuberales 506 BASIDIOMYCETES 507 (I) Hysterangiaceae 507 (II) Hydnangiaceae 512 (III) Hymenogastraceae 523 (IV) Rhizopogonaceae 536 The relationship between the hypogeous Gasteromycetes and other fungi 540 REFERENCES 542 The study of hypogeous fungi has been neglected in Britain from the time of Berkeley & Broome until that of the present investigation. During the years 1948-53 some 700* collections have been made, mainly in the Bristol area, but also from other parts of England, Scotland, North Wales and Northern Ireland. These include members of the Phycomycetes (Endogonespp.), Ascomycetes (Elaphomycetaceae, Tuberales) and Basidiomycetes (Gasteromycetes). Some species were found sufficiently often to permit tentative conclusions to be drawn relating to the effect of weather and soil conditions on the production of fruit-bodies. Most of the species previously recorded in Britain have been collected and some new records made. Descriptions are given of all recorded British species, and most of these are illustrated by line drawings made from fresh material. Details of development are given for representative species and the probable relationships within the group and with other fungi are discussed. Increased to 1000 by end of 1953, later collections not listed in this paper unless of special interest. VOL. 237. B. 650. (Price 27s.) 52 [Published 17 February 1954 430 LILIAN E. HAWKER ON INTRODUCTION Many fungi pass the greater part of their life cycle within the soil, but the majority of those producing large fruit-bodies either produce them above the soil surface or if they are at first subterranean they emerge before maturing. The true hypogeous fungi, however, produce relatively large fruit-bodies which complete their development beneath the surface of the soil or are at least embedded in the covering of humus or litter. None of them has any dehiscence mechanism by which the spores are shed. The latter are set free by the decay of the surrounding hyphae or are probably dispersed by soil-inhabiting invertebrates or small mammals which eat the fruit-bodies. It is not known whether the spores are capable of normal germination. The hypogeous habit is found amongst the Zygomycetes, Ascomy- cetes and Basidiomycetes, but the similarity of habitat has induced a superficial morpho- logical resemblance between the mature fruit-bodies despite the great differences in their modes of development. The early studies of European hypogeous fungi by Micheli (1729), Fries (1822), Vittadini (I83I, I842), Tulasne (I843, i844, i851), Zobel (I854), Chatin (1892) and Hesse (i89I, 1894) have been continued by Fischer (I896-I927), Bucholtz (1897-1912), Jaczewski (I909), Hollos (i9II), Soehner (1913-5I), Bataille (192I, I923), Lohwag (I924-39), Knapp (I924-52), Malen~on (I938) and others. The North American species have been studied by Harkness (1899), Lloyd (I922), Gilkey (1916, 1939), Dodge & Zeller (I918-36) and Coker & Couch (1928), and the hypogeous Gasteromycetesof South Africa (Bottomley 1948)and Australasia (Cunningham 1944) have been investigated. The hypogeous fungi of Britain, however, have been neglected since the days of Berkeley & Broome (I846-75). Only occasional references occur in the Foray Lists published by the British Mycological Society, and these are usually to two common species of Elaphomyces.The present writer became interested in hypogeous fungi as the result of the collection of specimens of Tuberpuberulum by Dr P. H. Gregory at the Belfast Foray of the British Mycological Society in September 1948, and, with the aid of colleagues and students of the Department of Botany, University of Bristol, and of a few mycological colleagues elsewhere, has since made some 700 separate collec- tions. These include most of the species previously recorded for Britain, together with one new species, a new variety and several known species not hitherto recorded as British. Much of this material was in sufficient abundance to permit developmental studies to be made. Most of the descriptions given below were compiled as a result of the examination of fresh material which was compared with herbarium specimens and checked against earlier descriptions. A few, which are indicated in the text, were based solely on a study of preserved material at the Herbarium, Royal Botanic Gardens, Kew, and at the British Museum (Natural History). Methodsof collection The edible truffles are still collected in France, Italy and elsewhere on the continent of Europe with the aid of trained pigs or dogs. No such trained animals are available in this country, and search has been made by scraping away the leaf litter and loose surface soil under suitable trees with a small hand-rake. While many fruit-bodies may be missed by this method it has the advantage that the collection is not limited to mature specimens of those species whose scent is attractive to animals, but is likely to contain a representative BRITISH HYPOGEOUS FUNGI 431 collection of these and of immature specimens or specimens of odourlessvarieties. Experience soon showed what type of site would be most likely to yield fruit-bodies, while it was often advantageous to investigate the neighbourhood of small holes dug by animals. Complete records were kept of the places where specimens were collected, and these included particulars of the nature and H-ion concentration of the soil, surface vegetation, if any, and the species of tree beneath which the fungus was found. Records of weather were also made. These have given some indication of the conditions favouring development of the commoner species. Examinationand preservation of material A full record was made of size, colour, general external and internal appearance, spore type and size, odour, etc., of each collection in a fresh condition. The specimens were then either dried or preserved in formalin alcohol. Frequently, half of a particular collection (or fruit-body) was dried and half was pickled. For the study of development, portions of fruit-bodies were fixed and embedded in wax by a method employing butyl alcohol and avoiding the use of xylol (which causes shrinkage and distortion) based on that used by Professor Nannfeldt of the University of Uppsala, Sweden. Serial sections were cut and stained with carbol fuchsin (or safranin) and light green for the study of gross morphology or with iron alum haemotoxylon counter-stained with light green for cytological studies. Staining with gentian violet did not in general give good cytological preparations of these fungi. For the investigation of mature fruit-bodies, hand sections or occasionally freezing microtome sections were preserved in glycerine. All drawings, other than those of whole fruit-bodies, were made with the aid of the camera lucida. Habitat The large majority of the collections were made under trees, usually in woodlands but occasionally under isolated trees in parks or hedgerows. A few specimens were obtained some distance from the nearest tree, but in these examples the soil had been undisturbed for long periods and thus it is possible that the unbroken mycelium extended through it for a considerable distance. Some species were found under a number of different kinds of tree, but many were associated with one only. Beech, evergreen oak, lime and conifers (both indigenous and planted) have been the most usual tree associates, while ash and deciduous oakwoods have been relatively poor in hypogeous fungi. There is little doubt that many of these fungi are intimately associated with tree roots in the formation of ectotrophic mycorrhizal mantles. Claims have been made for a mycorrhizal association between various trees and Elaphomycesgranulatus (Reess i88o), E. muricatus(Lewton-Brain 1901), Tuber borchii (Mattirolo 1934), T. magnatum(Sappa 1946), Rhizopogonluteolus (Young 1937) and R. roseolus(Modess I939). Fruit-bodies of various species collected by the writer have been found to be in very close association with mycorrhizae, and others have been equally closely associated with pseudomycorrhizae (Melin 1917), e.g. Endogonemicrocarpa. The hyphae of the true mycorrhizal mantles often show a close resemblance to those of parts of the fruit-body and its surrounding mycelium. The latter may sometimes be traced through the soil from fruit-body to root. An unusual orange mycelium which, in culture, felts together to form a sheet of hyphae with a greenish black metallic sheen, was isolated from the mantles of beech mycorrhizae and from immature fruit-bodies of Tuberexcavatum. 52-2 432 LILIAN E. HAWKER ON This mycelium has not been induced to produce truffles, but both isolates have caused the development of typical mycorrhizal roots on beech seedlings grown under aseptic con- ditions. Further work of this type is planned. The conditions which favour the development
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