ISSN 0006 8241 = Bothalia

Bothalia

’N TYDSKRIF VIR PLANTKUNDIGE NAVORSING

A JOURNAL OF BOTANICAL RESEARCH

Vol. 24,2

Oct./Okt. 1994

TECHNICAL PUBLICATIONS OF THE NATIONAL BOTANICAL INSTITUTE, PRETORIA

TEGNIESE PUBLIKASIES VAN DIE NASIONALE BOTANIESE INSTITUUT, PRETORIA

Obtainable from the National Botanical Institute, Private Bag XI 01,

Pretoria 0001, Republic of South Africa. A catalogue of all available

publications will be issued on request.

BOTHALIA

Bothalia is named in honour of General Louis Botha, first Premier and

Minister of Agriculture of the Union of South Africa. This house journal

of the National Botanical Institute, Pretoria, is devoted to the furtherance

of botanical science. The main fields covered are taxonomy, ecology,

anatomy and cytology. Two parts of the journal and an index to contents,

authors and subjects are published annually.

A booklet of the contents to Vols 1-20 is available.

Verkrygbaar van die Nasionale Botaniese Instituut, Privaatsak XI 01,

Pretoria 000 1, Republiek van Suid-Afrika. 'n Katalogus van allebeskik-

bare publikasies kan aangevra word.

Bothalia is vemoem ter ere van Generaal Louis Botha, eerste Eerste Minister

en Minister van Landbou van die Unie van S«id- Afrika. Hierdie lyfblad van

die Nasionale Botaniese Instituut, Pretoria, is gewy aan die bevordering van

die wetenskap van plantkunde. Die hoofgebiede wat gedek word, is tak-

sonomie, ekologie, anatomie en sitologie. Twee dele van die tydskrif en ’n

indeks van die inhoud, outeurs en onderwerpe verskyn jaarliks.

’n Inhoudsopgawe tot volumes 1-20 is beskikbaar.

MEMOIRS OF THE BOTANICAL SURVEY OF SOUTH AFRICA

The memoirs are individual treatises usually of an ecological nature, but

sometimes dealing with taxonomy or economic botany.

THE FLOWERING PLANTS OF AFRICA (FPA)

This serial presents colour plates of African plants with accompanying

text. The plates are prepared mainly by the artists at the National

Botanical Institute. Many well known botanical artists have contributed

to the series, such as Cythna Letty (over 700 plates), Kathleen Lansdell,

Stella Gower, Betty Connell, Peter Bally and Fay Anderson. The Editor

is pleased to receive living plants of general interest or of economic value

for illustration.

Twenty plates are published annually.

An index to Vols 1-49 is available.

FLORA OF SOUTHERN AFRICA (FSA)

A taxonomic treatise on the flora of the Republic of South Africa,

Ciskei, Transkei, Lesotho, Swaziland, Bophuthatswana, Namibia,

Botswana and Venda. The FSA contains descriptions of families, genera,

species, infraspecific taxa, keys to genera and species, synonymy, litera-

ture and limited specimen citations, as well as taxonomic and ecological

notes.

Contributions to the FSA will also appear in Bothalia.

PALAEOFLORA OF SOUTHERN AFRICA

A palaeoflora on a pattern comparable to that of the Flora of

southern Africa. Much of the information is presented in the form

of tables and photographic plates depicting fossil populations. Now

available:

’n Reeks van losstaande omvattende verhandelings oor vemaamlik eko-

logiese, maar soms ook taksonomiese of plantekonomiese onderwerpe.

Hierdie reeks bied kleurplate van Afrikaanse plante met bygaande teks.

Die skilderye word meestal deur die kunstenaars van die Nasionale

Botaniese Instituut voorberei. Talk bekende botaniese kunstenaars het

tot die reeks bygedra, soos Cythna Letty (meer as 700 plate), Kathleen

Lansdell, Stella Gower, Betty Connell, Peter Bally en Fay Anderson. Die

Redakteur verwelkom lewende plante van algemene belang of ekono-

miese waarde vir afbeelding.

Twintig plate word jaarliks gepubliseer.

’n Indeks tot volumes 1-49 is beskikbaar.

'n Taksonomiese verhandeling oor the flora van die Republiek van Suid-

Afrika, Ciskei, Transkei, Lesotho, Swaziland, Bophuthatswana, Namibie,

Botswana en Venda. Die FSA bevat beskrywings van families, genusse,

spesies, infraspesifieke taksons, sleutels tot genusse en spesies, sinonimie,

literatuur, verwysings na enkele eksemplare, asook beknopte taksonomiese

en ekologiese aantekeninge.

Bydraes tot die FSA sal ook in Bothalia verskyn.

'n Palaeoflora met ’n uitleg vergelykbaar met die van die Flora van

suidelike Afrika. Baie van die inligting word aangebied in die vorm van

tabelle en fotografiese plate waarop fossiele populasies afgebeeld word.

Rqeds beskikbaar:

Molteno Formation (Triassic) Vol. 1. Introduction. Dicroidium, by/deur J.M. & H.M. Anderson.

Molteno Formation (Triassic) Vol. 2. Gymnosperms (excluding Dicroidium ), by/deur J.M. & H.M. Anderson.

Prodromus of South African Megafloras. Devonian to Lower Cretaceous, by/deur J.M. & H.M. Anderson. Ob-

tainable from/Beskikbaar van: A. A. Balkema Marketing, Box/Posbus 317, Claremont 7735, RSA.

ANNALS OF KIRSTENBOSCH BOTANIC GARDENS

A series devoted to the publication of monographs and major works

on southern African flora. Published: Vol. 14-19 (earlier volumes

published as Supplementary volumes to the Journal of South African

Botany)

’n Reeks gewy aan die publikasie van monografiee en belangrike werke oor

flora van suidelike Afrika. Gepubliseer: vol. 14—19 (vroeere volumes

gepubliseer as Supplementary volumes van die Journal of South African

Botany).

BOTH ALIA

’N TYDSKRIF VIR PLANTKUNDIGE NAVORSING

A JOURNAL OF BOTANICAL RESEARCH

Volume 24,2

Scientific Editor/Wetenskaplike Redakteur: O.A. Leistner

Technical Editor/Tegniese Redakteur: B.A. Momberg

NASIONALE BOTANiESE

instituut

Private toag X101 PRETORIA 0001

1994 -11- ?0

X 101 PRETORIA 0001

riONAL BOTANICAL

INSTITUTE

INSTITUTE

2 Cussonia Avenue, Brummeria, Pretoria

Private Bag X101, Pretoria 0001

ISSN 0006 8241

OctVOkt. 1994

Editorial Board/Redaksieraad

D.F. Cutler

B.J. Huntley

P.H. Raven

J.P. Rourke

M.J. Werger

Royal Botanic Gardens, Kew, UK

National Botanical Institute, Cape Town, RSA

Missouri Botanical Garden, St Louis, USA

Compton Herbarium, NBI, Cape Town, RSA

University of Utrecht, Utrecht, Netherlands

CONTENTS— INHOUD

Volume 24,2

1. Studies in the Ericoideae (Ericaceae) XV. The generic relationship between Erica and Ericinella. E.G.H.

OLIVER 121

2. A taxonomic re-assessment of Ammocharis herrei and Cybistetes longifolia (Amaryllideae: Amaryl-

lidaceae). D.A. SNIJMAN and G. WILLIAMSON 127

3. Studies in the Marchantiales (Hepaticae) from southern Africa. 6. The genus Asterella (Aytoniaceae :

Reboulioideae) and its four local species. S.M. PEROLD 133

4. Studies in the Marchantiales (Hepaticae) from southern Africa. 7. The genus Cryptomitrium (Aytoniaceae)

and C. oreades sp. nov. S.M. PEROLD 149

5. A new serotinous species of Cliff ortia (Rosaceae) from the southwestern Cape with notes on Clijfortia

arborea. E.G.H. OLIVER and A.C. FELLINGHAM 153

6. ESA contributions 1: Aquifoliaceae. S. ANDREWS 163

7. Notes on African plants:

Boraginaceae. Lobostemon regulareflorus — the correct name for L. grandiflorus. M.H. BUYS and

J.J.A. VAN DER WALT 170

Proteaceae. A new species of Leucospermum from the southwestern Cape. J.P. ROURKE 167

8. An overview of Aspergillus (Hyphomycetes) and associated teleomorphs in southern Africa. A. LOUISE

SCHUTTE 171

9. The taxonomic value of epidermal characters in the leaf of Heteromorpha and some related genera

(Apiaceae). P.J.D. WINTER and B-E. VAN WYK 187

10. Inflorescence morphology of Lachnaea and Cryptadenia (Thymelaeaceae). J.B.P. BEYERS and J.J.A.

VAN DER WALT 195

11. Morphological and ultrastructural variations in Schizaea pectinata (Schizaeaceae: Pteridophyta). B.M.

PARKINSON 203

12. Plant defences against mammalian herbivores: are juvenile Acacia more heavily defended than mature

trees? R. BROOKS and N. OWEN-SMITH 211

13. The saltmarsh vegetation of Langebaan Lagoon. M. O’CALLAGHAN 217

14. The saltmarsh vegetation of the lower Berg River. M. O’CALLAGHAN 223

15. The saltmarsh vegetation of the lower Uilkraals River. M. O'CALLAGHAN 229

16. The marsh vegetation of Kleinmond Lagoon. M. O’CALLAGHAN 235

17. Chromosome studies on African plants. 1 1. The tribe Andropogoneae (Poaceae: Panicoideae). J.J. SPIES,

T.H. TROSKIE, E. VAN DER V YVER and S.M.C. VAN WYK 241

18. National Botanical Institute: list of staff and publications, 3 1st March 1994. Compiler: B.A. MOMBERG 247

19. Book reviews 261

20. Guide for authors to Bothalia (including new provinces of South Africa, May 1994) 263

Digitized by the Internet Archive

in 2016

https://archive.org/details/bothaliavolume2424unse_0

Bothalia 24,2: 121-126 (1994)

Studies in the Ericoideae (Ericaceae). XV. The generic relationship between

Erica and Ericinella

E.G.H. OLIVER*

Keywords: Africa, Blaeria , bract, bracteoles, Erica, Ericinella, Philippia, taxonomy

ABSTRACT

The small African genus Ericinella Klotzsch, with one species in Malawi and SW Tanzania and three in the Eastern Cape is

shown to exhibit variability in its delimiting characters that overlap with those of Blaeria L, and Philippia Klotzsch. both of

which have recently been included under Erica. It is postulated that the genus, like the two above, is unnatural and polyphyletic.

The genus is therefore included under Erica and the relevant nomenclatural changes are provided: Erica amatolensis E.G.H.

Oliv., nom. nov. (= Ericinella multiflora Klotzsch), E. passerinoides (Bolus) E.G.H. Oliv., comb, nov., E. hillhurttii (E.G.H.

Oliv.) E.G.H. Oliv., comb, nov., and E. microdonta (C.H. Wright) E.G.H. Oliv., comb. nov.

UITTREKSEL

Daar word aangetoon dat die klein Afrika-genus Ericinella Klotzsch, met een spesie in Malawi en SW Tanzanie en drie in

die oostelike Kaapprovinsie, variasie in sy afbakende kenmerke toon wat oorvleuel met die van Blaeria L. en Philippia

Klotzsch, wat albei onlangs onder Erica geplaas is. Die stelling word gemaak dat die genus, soos die twee hierbo, onnatuurlik

en polifileties is. Die genus word dus onder Erica geplaas en die nodige naamsveranderinge word gegee: Erica amatolensis

E.G.H. Oliv., nom. nov. (= Ericinella multiflora Klotzsch), E. passerinoides (Bolus) E.G.H. Oliv., comb, nov., E. hillhurttii

(E.G.H. Oliv.) E.G.H. Oliv., comb, nov., and E. microdonta (C.H. Wright) E.G.H. Oliv., comb. nov.

INTRODUCTION

The genus Ericinella Klotzsch belongs to the capsular

group of African genera of the subfamily Ericoideae

which until recently comprised Erica L., Philippia

Klotzsch, Blaeria L. and Ericinella. The genus Philippia

has been found (Oliver 1988) to possess a continuous

range of variation in the sole distinguishing character be-

tween the genera, the fully recaulescent bract in some

species, albeit only a few compared to the 757 species in

Erica. Also it was argued that the genus was not a

monophyletic unit. The genus was therefore reduced to

synonymy under Erica (Oliver 1987, 1992, 1993a;

Beentje 1990). As a result, the circumscription of Erica

became broader with the inclusion of those Philippia spp.

with stamen complements differing from the basic eight

stamens in most Erica spp. The most aberrant species of

this group is the tropical Erica nyassana (Aim & T.C.E.

Fr.) E.G.H. Oliv. [= Philippia nyassana Aim & T.C.E. Fr.]

with only four stamens.

The situation regarding the validity of Blaeria as a dis-

tinct genus was also examined in the light of its single

character difference from Erica of four versus eight

stamens. It has been shown (Oliver 1993b) that several

species of Erica , apart from those incorporated from

Philippia , showed an overlap in the number of stamens.

As in the case of Philippia it was shown that polyphyletic

origins exist for the various species groups currently in-

cluded within the genus Blaeria. As a result, the genus

*Stellenbosch Herbarium, National Botanical Institute, RO. Box 471,

Stellenbosch 7599.

MS. received: 1993-03-03.

Blaeria was reduced to synonymy under Erica (Oliver

1993b, 1993c).

ERICINELLA

This genus was described together with many other

genera by Klotzsch (1838) in his reclassification of the

subfamily Ericoideae. It was based on one species, E. mul-

tiflora Klotzsch, and was distinguished from other mem-

bers of the subfamily by a fully recaulescent bract, the

zygomorphic calyx condition, and no bracteoles coupled

with only four stamens and a 3-locular ovary. The sub-

sequent describing of Ericinella gracilis Benth. from

Madagascar (Bentham 1839) altered the circumscription

of the genus to include a 4-locular ovary. This was com-

pounded by the adding of E. mannii Hook. f. from tropical

Africa in 1862.

This broader circumscription of the genus was main-

tained by various workers in their publications for overall

treatments of the family or for large floras (Bentham 1839;

D. Oliver 1877; Drude 1897; Brown 1905).

When Aim & Fries (1927a) undertook the first com-

plete revision of the genus, they retained only three

species, the two Cape ones, E. multiflora and E. pas-

serinoides, and one from tropical Africa, E. microdonta

(C.H. Wright) Aim & T.C.E. Fr., which had originally

been described as a species of Blaeria. They purified the

genus by removing what to them were the two discordant

elements to Philippia, P. tenuissima Klotzsch (E. gracilis )

and P. mannii (Hook, f.) Aim & T.C.E. Fr..

122

Bothalia 24,2 (1994)

Phillips (1926) retained the genus as circumscribed in

Flora capensis (Brown 1905) in his The genera of South

African flowering plants, but later (Phillips 1944) com-

pletely changed his concept of the subfamily. In this work

he combined Ericinella with a number of genera not all

closely related, namely Philippia, Coccospernia Klotzsch

and Thamnus Klotzsch, under Blaeria L. He retained this

treatment in the second edition of The genera ... (Phillips

1951). The genus was retained in the same form as used

by Aim & Fries (Oliver 1975) and by Ross (1983) in

Flora zambesiaca with the single species, E. microdonta.

As currently construed Ericinella is a small genus with

the one species, E. microdonta, in tropical Africa and the

three species, E. multiflora, E. passerinoides and E.

hillburttii, in the Eastern Cape. It is distinguished only by

a combination of two characters, the fully recaulescent

bract and four stamens.

The fully recaulescent bract is present in a number of

Cape genera such as Salaxis Salisb., Coccospernia

Klotzsch, Scyphogyne Decne and Nagelocarpus Bullock,

but these minor genera have an indehiscent fruit. It is also

present in the philippioid components now included

within Erica.

Aim & Fries (1924) and Ross (1957) relied on anther

appendages and the shape of the stigma to distinguish

Ericinella from Philippia. These characters are clearly not

of any significance in generic delimitation because they

are only a reflection of the different pollination syndromes

present in the taxa — entomophily versus anemophily, both

of which are present in many species of Erica. It has been

pointed out (Rebelo et al. 1985; Koutnik 1987; Oliver

1991) that the reduction in flower size, loss of bright

colours and the increase in size of the stigma is associated

with anemophily in the southern African Ericaceae. To

this must be added the loss of anther appendages.

The only difference existing between Ericinella and

Blaeria in tropical Africa is the fully recaulescent bract

and lack of bracteoles in the former genus. However, Ross

(1980) stated that the bract can be inserted anywhere from

near the base of the pedicel to close under the calyx in

the tropical species of Blaeria [Erica] and that bracteoles

are only present when the bract is inserted at or below

the middle of the pedicel. This would then give the con-

dition of a partially recaulescent bract and no bracteoles

which does occur in some specimens of E. microdonta

that I have examined.

Ericinella microdonta has a 4-locular ovary, whereas

the three Cape species of Ericinella have 3-locular, very

rarely 4-locular ovaries. The very variable Cape species.

Erica equisetifolia Salisb. [Blaeria equisetifolia (Salisb.)

Druce, Blaeria dumosa Wendl., Blaeria campanulata

Benth.] possesses Bowers with 66% having 3-locular

ovaries in the localized montane form [Blaeria cam-

panulata]. The 3-locular condition is not confined to the

above species; it occurs occasionally in the widespread

tropical species Erica mannii (Hook, f.) Beentje and of

course the Madagascan species, Philippia gracilis (Benth.)

H. Perrier [Ericinella gracilis Benth.) mentioned above.

Also Aim & Fries (1927a) had created the subgenus

Afrophilippia to accommodate two East African species

with 3-merous flowers, P. excelsa Aim & T.C.E. Fr. [Erica

excelsa (Aim & T.C.E. Fr.) Beentje] and P. johnstonii

Engl, [still to be transferred to Erica].

DISCUSSION

In the discussion of the African capsular genera (Oliver

1988) it was stated that the relationships within this group

of genera are very close, with generic distinctions being

based on the flimsiest of morphological characters. This

would indicate that the genera have arisen from some an-

cestral ericoid stock by two processes: the shifting of the

bract and bracteoles from axial and partially recaulescent

to totally recaulescent; and by the reduction in stamen

number from 8 to 4. Both processes were involved in the

formation of the species placed under Ericinella, whereas

in Philippia, the first and in Blaeria the second process

has taken place.

Ross (1957) did not consider the possibility of any

close link existing between Philippia and Ericinella, in-

stead he regarded them as belonging to two separate

evolutionary lines in which the zygomorphic calyx,

produced by the totally recaulescent bract, has risen in-

dependently.

Aim & Fries (1924) when considering the phylogenetic

origins of the genera Philippia and Ericinella, were unable

to give any clear lineage for Ericinella from either Philip-

pia or Blaeria. They regarded E. microdonta as an outlier

of the genus whose origin lay in the region of the Cape

Flora.

These arguments are perhaps feasible if one accepts

Ericinella as a natural, well-defined genus. The tropical

species shows a clear relationship with the tropical species

of Erica that have been placed in the Section Arsace (Aim

& T.C.E. Fr. 1927b), Erica arborea L. and the complex

of six species included by Ross (1956) under E. kingaensis

Engl, as three subspecies. These ericas exhibit reductions

in their bract/calyx arrangement and in the number of

stamens. They all clearly arose from some ericoid an-

cestral stock independently of those much further south

in the Cape Province.

There is little doubt that the three Cape species are

closely related, but not to the tropical species, E.

microdonta. The Cape species are allied to several Eastern

Cape-KwaZulu/Natal species of Erica which are placed

in the section Arsace in the present, rather unsatisfactory,

subgeneric classification of the genus. These are Erica

dominans Killick, E. dissimulans Hilliard & B.L. Burtt

and E. anomala Hilliard & B.L. Burtt. E. dissimulans and

E. anomala both show a strong tendency towards the

philippioid reduced calyx. The former species also pos-

sesses 3-4-locular ovaries as does E. dominans, characters

which have not previously been recorded in the species.

There is also a relationship with the southeastern Cape

species complex based on Erica simulans Dulfer, which

is placed in the section Pyronium. In my opinion the genus

Ericinella, as it stands, is an unnatural one which is clearly

not monophyletic.

Bothalia 24,2(1994)

123

The clear and total overlap in the morphological char-

acters of partial versus total recaulescence of the bract,

the four stamens and 3- to 4-locular ovary indicates that

there can be no separation between the species currently

included under Ericinella and those which were formerly

in Philippia and Blaeria and are now included within

Erica. This fact coupled with the independent origin of

the two groups of species have led me to reduce the genus

to synonymy under Erica.

SPECIES & NOMENCLATURAL CHANGES

1. Erica amatolensis E.G.H. Oliv., nom. nov.

Ericinella multiflora Klotzsch in Linnaea 12: 223 (1838), non Erica

multiflora L. (1753) species mediterranea; Benth.: 697 (1839); N.E. Br.:

318 (1905); Aim & T.C.E. Fr. : 45 (1927a). Type: Winterberg near

Philippstown (ceded Territory), Ecklon & Zeyher s.n. (B, holo.f : BOL!,

K!, LD!, P!, UPS!, Z! iso.); ibid., distributed as Ecklon & Zeyher 257

(G!, MEL!, PRE!, S !, SAM!, W!). Lectotype (selected here): Ecklon &

Zeyher 257 [det. Klotzsch) (S).

Erica amatolensis is most closely related to the more

recently described E. passerinoides and E. hillburttii under

which the differences are discussed. These differences are

summarised in Table 1.

This species is restricted to the higher mountains of

the Eastern Cape Province from the Katberg along the

Amatola Range to Stutterheim (Figure 1). It forms erect

single-stemmed shrubs up to 1.5 m tall on the edges of

forest patches or among woody vegetation on rocky gras-

sy slopes from 1 000-1 600 m altitude and flowers from

October to December.

It is the most widespread of the three Cape species

discussed here, but does not appear to be abundant where

it does occur. For instance on the Katberg Pass, where

most records have been made due to easy access, the

plants are few and far between. Over its range there does

not appear to be any variation of significance in the char-

FIGURE 1. — Distribution of the Cape species; E. passerinoides , •; E.

amatolensis , #; E. hillburttii, ■.

acters. Occasionally, however, some anthers were noted

without any appendages.

McMasters (pers. comm.) noted that the bushes in the

Gubu Dam area near Stutterheim were inclined to have a

running root system from which new plants were

produced. This could well indicate that these plants may

survive burning by sprouting from the root system. This

would then relate to the condition found in E. hillburttii

with its thick woody rootstock and many stems above

ground. All the plants that I have seen in the wild pos-

sessed a single stem with regeneration having to take place

via seeds only.

The flowers have very rudimentary nectaries at the

base of the ovary and only a slightly obconic stigma.

Anemophily was clearly evident in the populations on the

Katberg Pass where clouds of pollen were produced when

TABLE 1. — Characters which distinguish the three Cape species of Erica

124

Bothalia 24,2 ( 1994)

the plants were disturbed. It is surprising therefore that

the flowers are a striking pink colour and that the exserted

anthers often have appendages, features which are as-

sociated with entomophily. Insects in the form of bees

foraging for pollen only, could perhaps play a minor role

in the pollination of this species.

The holotype, Ecklon & Zeyher s.n., was destroyed in

Berlin during World War II, and so it was decided to select

the numbered collection in Stockholm as the lectotype

because it was determined by Klotzsch himself.

Specimens examined

Cotterrell 39 (BOL, GRA); Ecklon & Zeyher 257 (G, MEL, PRE, S,

SAM, W) & s.n. (BOL, K, LD, P, UPS, Z); Esterhuysen 13226 (BOL,

NBG, PRE), 13257 (BOL); Hilliard & B.L. Bunt 10997 (PRE), 12369.

12396 (NU. PRE); McMasters 8. 70 (STE); Oliver 7967 (PRE, STE),

8066 (BM, E, MO, PRE, STE); Rattray 101. 350 (GRA), in BOL 14244

(BOL); Sidey 3787 (PRE, S, STE); Werdermann & Oberdieck 1070

(PRE).

2. Erica passerinoides (Bolus) E.G.H. Oliv., comb.

nov.

Ericinella passerinoides Bolus in Journal of the Linnean Society of

London, Botany 18: 393 (1881); N.E. Br.: 318 (1905); Alm& T.C.E. Fr.:

46 (1927a). Type: Sneeuberg, Koudeveld Mtns, 5000 ft, Dec. 1872, Bolus

2582 (BOL!, holo.; G!. K!, LD!, SAM!, iso.).

The true identity of E. passerinoides remains a problem

as the type and only collection does not have fully mature

flowers. Thus the true shape of the corolla, the position

of the anthers at anthesis and the position of the mature

style and stigma cannot be assessed. Fortunately an old

capsule remaining from the previous flowering season, al-

though somewhat disintegrated, could be used to

reconstruct the characters of the fruit.

Bolus’s diaries for that period do not give sufficient

details to pinpoint the exact locality. He appears to have

collected en route from Graaff-Reinet to Murraysburg,

presumably not far off the road. Several searches in the

area of the highest point of the road over the Sneeuberg

and environs to the north and south have proved unsuc-

cessful. Another species of Ericaceae, Philippia tristis

Bolus (= Erica caespitosa Hilliard & B.L. Burtt), also

known from its type collection gathered at the same

locality on the same day, has not been re-collected in that

vicinity either. As farms now stretch right to the summit

of these mountains where burning and overgrazing are

very evident, it is likely that both species have been ex-

terminated in the area.

Aim & Fries (1927a) retained the species with some

hesitation as they felt that it was only a young stage of

E. amatolensis (E. multiflora). However, a thorough ex-

amination of the type has revealed a number of characters

which point to the distinctness of E. passerinoides from

E. amatolensis (see Table 1). Brown (1905) used the

corolla shape and degree of exsertion of the style to

separate the two Cape species. Aim & Fries on the other

hand used the shape of the calyx lobes and leaf length to

separate them. These characters are of no real value in

distinguishing the species.

Until the material is found again in the wild I am

retaining E. passerinoides as a distinct species.

Specimen examined

Bolus 2582 (BOL, G, K, LD, SAM).

3. Erica hillburttii (E.G.H. Oliv.) E.G.H. Oliv.,

comb. nov.

Ericinella hillburttii E.G.H. Oliv. in Bothalia 16: 46 (1986). Type:

Cape, Elliott Dist., Bastervoetpad between Saamwerk and Mt Enterprise,

2 130 m, 16 November 1983, Oliver 8151 (PRE, holo.!, BM!, BOL!, E!,

GRA!, K!, MO!, NBG!, NU!, NY!, S!, STE! iso.).

This species forms erect multi-stemmed shrubs up to

1.5 m tall and occurs on rocky, grassy slopes at high al-

titude in the mountains northwest of Elliott in the Eastern

Cape. It flowers from October to December.

E. hillburttii was discovered as recently as 1983 by

Hilliard & Burtt. It is known to date from only one

locality, the Bastervoetpad. Accessibility in these moun-

tains is very limited, therefore additional populations

could well be discovered in the future farther north

towards Naude’s Nek.

The species is easily distinguishable from its nearest

ally, E. amatolensis , on a number of characters (Table 1 ).

The most noticeable of these characters in the field are

the multi-stemmed habit, greenish yellow colour of the

flowers and the included stamens. Examination of a

flower will show the relatively short filaments with broad

apex on which the awns are decurrent and the lanate

ovary.

The total lack of any nectaries below the ovary, the

broadly funnel-shaped stigma and the inconspicuous dull-

coloured flowers clearly point to anemophily in this

species. This syndrome could not be tested in the field

because of the wet overcast weather prevailing when the

type material was collected.

Specimens examined

Hilliard & B.L. Burtt 16662 (STE); Oliver 8151 (BM, BOL, E, GRA,

K, MO, NBG, NU, PRE, S, STE).

4. Erica microdonta (C.H. Wright ) E.G.H. Oliv.,

comb. nov.

Ericinella microdonta (C.H. Wright) Aim & T.C.E. Fr. in Acta Horti

Bergiani 8: 262 (1924); Aim & T.C.E. Fr.: 46 (1927a); Brenan: 494

(1954); R. Ross: 174 (1983). Blaeria microdonta C.H. Wright: 272

(1897). Types: Malawi, Mla'nje Distr., Mt Mlanje, I 800 m, McClounie

55. 75 & 95 ( K ! ). Lectotype (selected here by R. Ross pers. comm.):

McClounie 55 (K).

E. shinniae S. Moore: 287 (1916). Type: Malawi, Mlanje Dist. Shinn

s.n. (BM!, holo.).

E. brassii Brenan: 494 (1954). Type: Malawi, Mlanje Dist. Mlanje

Mtn, Luchenya Plateau, 1 870 m, June 1946, Brass 16454 (K!, holo.;

BM!, MO!, PRE!, SRGH, iso.).

E. microdonta var. craspedotricha Brenan: 495 (1954). Type: Mala-

wi, Mlanje Dist., Mlanje Mtn, southwest ridge, 2 400 m, June 1946, Brass

16497 (K!, holo.; MO!, PRE!, SRGH, iso.).

Bothalia 24,2(1994)

125

This species is from tropical Africa where it occurs

mostly on high ground in Malawi, just getting into SW

Tanzania (Figure 2). Ross (1983) recorded the species as

forming shrubs up to 3 m tall. Brass, on his various col-

lections, records the plants as occasional to plentiful,

sometimes gregarious, in grassland on the edges of rain-

forest and on rocky banks of streams subject to flooding.

One plant he recorded as a tree 4 m tall. I can confirm

these observations from my examination of plants on Mt

Mulanje.

Of the species listed here E. microdonta is by far the

most variable. The populations in central Africa were

regarded as comprising two distinct species, one with a

variety (Brenan 1954). The variation in the size and form

of the corolla is considerable, the smallest flowers being

from the type of E. brcissii Brenan and appearing very

distinct. However, Ross ( 1983) after examining a consid-

erable number of specimens from the whole area regarded

the variation in the indumentum on the branchlets, leaf

indumentum, leaf size, corolla size and stigma diameter

as of no taxonomic significance. He recognized only one

species with no varieties, and this view I support.

E. microdonta possesses well-developed nectaries

below the ovary, a poorly developed funnel-shaped stigma

and partially exserted anthers with appendages. This

would clearly indicate entomophily as the pollination

syndrome. During a visit to a few populations on Mt

Mulanje in Malawi during 1991, I was unable to record

any instance of the mass scattering of pollen from the

white flowers, but noted no visitation by any insect.

In correspondence some time ago on the lectotypifica-

tion of this species, which had not been done for Flora

zambesiaca , Ross recommended that McClounie 55 was

the best specimen to select. I therefore attribute the above

selection to him.

FIGURE 2. — Distributions of the species; E. passerinoides, •; E.

amatolensis, ★; E. hillburttii, ■; E. microdonta , ©.

Specimens examined

Brass 16416, 16446, 16454 (MO, PRE), 16502 (MO), 16770 (MO,

PRE), 16852 (MO, PRE); Goodier 269 (PRE), 289 (PRE); Goyns 45a

(PRE); Oliver 9816 (STE); Phipps 2787 (PRE).

REFERENCES

ALM, G. & FRIES, T.C.E. 1924. Monographic tier Gattung Blaeria L.

Acta Horti Bergiani 8: 223-261.

ALM, G. & FRIES, T.C.E. 1927a. Monographic der Gattungen Philippia

Klotzsch, Mitrastylus gen. nov. und Ericinella Klotzsch.

Kungliga Svenska Vetenskapsakademiens Handlingar Ser. 3, 4,4:

1-19.

ALM. G. & FRIES, T.C.E. 1927b. Die tropischen Arten der Gattung

Erica L. Arkiv for botanik 21A,7: 1-21.

BEENTJE, H. 1990. Name changes in East African Ericaceae. Utafiti 3,1:

13.

BENTHAM, G. 1839. Ericaceae. In A.P De Candolle, Prodromus sys-

tematis naturalis regni vegetabilis 7: 580-733. Paris.

BOLUS, H. 1881. Ericinella passerinoides. Journal of the Linnean

Society of London, Botany 18: 393.

BRENAN, PM. 1954. Plants collected by the Vemay Nyasaland Expedi-

tion of 1946 (continued). Memoirs of the New York Botanical

Garden 8: 409-510.

BROWN, N.E. 1905. Ericaceae. In W.T. Thiselton-Dyer, Flora capensis

4,1: 315-336. Reeve, Ashford.

DRUDE, O. 1897. Ericoideae-Ericaceae. In H.G.A. Engler & K.A.E.

Prantl, Die Natiirlichen Pflanzenfamilien 4, 1 : 57-65. Engelmann,

Leipzig.

HOOKER, J.D. 1862. Ericinella mannii. Journal of the Linnean Society

of London, Botany 6: 16.

KLOTZSCH. J.F. 1838. Ericearum, genera et species. Linnaea 12: 211 —

247.

KOUTNIK, D. 1987. Wind pollination in the Cape flora. In A.G. Rebelo,

A preliminary synthesis of pollination biology in the Cape flora:

126-133. South African National Scientific Programmes Report

No. 141.

LINNAEUS, C. 1753. Species plantarum edn 1,1: 355.

MOORE. S. 1916. Ericinella shinniae. Journal of Botany, London 54:

287.

OLIVER, D. 1877. Flora of tropical Africa: 482-485. Reeve, London.

OLIVER, E.G.H. 1975. Ericaceae. In R.A. Dyer, The genera of southern

African flowering plants 1: 429-439. Botanical Research In-

stitute, Pretoria.

OLIVER. E.G.H. 1986. A new species of Ericinella from the southern

Drakensberg. Bothalia 16: 46-48.

OLIVER, E.G.H. 1987. Studies in the Ericoideae (Ericaceae). VII. The

placing of the genus Philippia into synonymy under Erica: the

southern African species. South African Journal of Botany 53:

455-458.

OLIVER. E.G.H. 1988. Studies in the Ericoideae (Ericaceae). VI. The

generic relationship between Erica and Philippia in southern

Africa. Bothalia 18: 1—10.

OLIVER. E.G.H. 1989. The Ericoideae and the southern African

heathers. Botanical Journal of the Linnean Society 101: 319-327.

OLIVER, E.G.H. 1991. The Ericoideae (Ericaceae) — a review. Contribu-

tions from the Bolus Herbarium 13: 158-208.

OLIVER, E.G.H. 1992. Studies in the Ericoideae (Ericaceae). VIII. New

combinations for Philippia are made in Erica for the Flora zam-

besiaca region. Kew Bulletin 47: 665-668.

OLIVER. E.G.H. 1993a. Studies in the Ericoideae (Ericaceae). X.

Nomenclatural changes for the Flore des Mascareignes region.

Kew Bulletin 48: 767-769.

OLIVER. E.G.H. 1993b. Studies in the Ericoideae (Ericaceae). XI. The

generic relationship between Erica and Blaeria. Kew Bulletin 48:

771-780.

OLIVER, E.G.H. 1993c. Studies in the Ericoideae (Ericaceae). XII. The

placing of the genus Blaeria into synonymy under Erica,

nomenclatural and taxonomic changes for the southern African

region. Bothalia 23: 1-7.

PHILLIPS, E.P 1926. The genera of South African flowering plants, 1st

edn: 457—4-65. Division of Botany and Plant Pathology, Pretoria.

PHILLIPS, E.P. 1944. Notes on the minor genera of the Ericaceae.

Journal of South African Botany 10: 69-73.

126

Bothalia 24,2 (1994)

PHILLIPS, E.P. 1951. The genera of South African flowering plants , 2nd

edn: 558-562. Division of Botany and Plant Pathology, Pretoria.

REBELO, A.G.. SIEGFRIED, W.R. & OLIVER, E.G.H. 1985. Pollina-

tion syndromes of Erica species in the southwestern Cape. South

African Jounutl of Botany 51: 270-280.

ROSS, R. 1956. On some African tree heathers. Annals and magazine of

natural history 9: 89-96.

ROSS, R. 1957. Notes on Philippia. Bulletin du Jardin Botanique de

l 'Etat, Bruxelles 27 : 733-754.

ROSS, R. 1980. Notes on Ericaceae from the Flora zambesiaca region.

Boletim da Sociedade Broteriana, Ser. 2, 53: 123-149.

ROSS, R. 1983. Ericaceae. Flora zambesiaca 7,1: 157-181.

WRIGHT, C.H. 1897. Diagnoses africanae. Kew Bulletin 1897: 272.

Bothalia 24,2: 127-132(1994)

A taxonomic re-assessment of Ammocharis herrei and Cybistetes longifolia

(Amaiyllideae : Amaryllidaceae)

D.A. SNIJMAN* and G. WILLIAMSON**

Keywords: Amaryllidaceae, Ammocharis herrei , anemogeochory, Cybistetes longifolia, seed number, seed size, synonymy

ABSTRACT

The inlructescence of the poorly known Ammocharis herrei F.M. Leight. is similar to that which is diagnostic for Cybistetes

longifolia (L.) Milne-Redh. & Schweick. In the absence of distinct morphological differences A. herrei is placed into synonymy

under C. longifolia. Plants of the amplified C. longifolia have fewer, large seeds in Namaqualand and the Richtersveld and

smaller, more numerous seeds in the Western Cape. This pattern is postulated to reflect divergent strategies of resource

allocation in different habitats. It is suggested that the infructescence of C. longifolia , a highly derived structure suited to

tumbling, evolved from the unspecialised condition in Ammocharis as an adaptation to the high winds of southwestern Africa.

UITTREKSEL

Die vrugstadiumbloeiwyse van die betreklik onbekende Ammocharis herrei F.M. Leight. is soortgelyk aan die wat

diagnostics is vir Cybistetes longifolia (L.) Milne-Redh. & Schweick. In die afwesigheid van duidelike morfologiese verskille,

word A. herrei in sinonimie onder C. longifolia geplaas. Plante van die vergrote C. longifolia het minder, groot sade in

Namakwaland en die Richtersveld en kleiner, meer sade in die Wes-Kaap. Die veronderstelling word gemaak dat hierdie patroon

uiteenlopende strategies van hulpbrontoewysing in verskillende habitats weerspieel. Daar word voorgestel dat die

vrugstadiumbloeiwyse van C. longifolia, ’n hoogs afgeleide struktuur wat kan rol, van die ongespesialiseerde toestand by

Ammocharis as ’n aanpassing by die sterk winde van suidwestelike Afrika ontwikkel het.

INTRODUCTION

The monotypic Cybistetes Milne-Redh. & Schweick.

is a Western Cape representative of Amaryllidaceae tribe

Amaryllideae with a specialised infructescence in which

the pedicels elongate, spread apart, stiffen and ultimately

radiate equally in all directions. Its separation from the

widely distributed sub-Saharan Ammocharis Herb, was

based on the interpretation of Milne-Redhead & Schweick-

erdt (1939) that the pedicels of the infructescence and the

dry, strongly ribbed capsules constitute a substantially dis-

tinct set of characters from the basic infructescence struc-

ture of Ammocharis in which the pedicels neither reflex

nor elongate and the fruits remain submembranous and

subglobose. This treatment, however, rendered uncertain

the taxonomic position of A. herrei F.M. Leight. whose

fruits have remained unknown until now.

Even in the absence of fruiting material, Milne-Red-

head & Schweickerdt (1939) commented on the close

resemblance of the type of A. herrei to the Western Cape

species, C. longifolia (L.) Milne-Redh. & Schweick. They

noted differences, however, in inflorescence characters

and ovule numbers.

Several recent collections of Amaryllidaceae from the

Richtersveld in the Northern Cape Province match the type

of A. herrei , which consists of leaves and an inflorescence

from a bulb originally collected by H. Herre south of Kom-

* Compton Herbarium, National Botanical Institute, Private Bag X7,

Claremont 7735.

** P.O. Box 406, Alexander Bay, 8290.

MS. received: 1993-09-17.

maggas, Namaqualand in the Northern Cape Province and

later cultivated at the Stellenbosch University Garden. The

position and status of this taxon are re-assessed and the

current data on the fruits and seeds of Cybistetes are dis-

cussed.

INFRUCTESCENCE, INFLORESCENCE AND

OVULE NUMBER

The new infructescence data given here were taken

from three recent collections of Amaryllidaceae from the

Richtersveld [Van Jaarsveld et al. 3511 (NBG, PRE), G.

& F. Williamson 4626 (K, MO, NBG, PRE) and G. & F.

Williamson 4637 (NBG, PRE)]. They augment the pre-

viously collected flowering data of A. herrei from the

same area [ Hall 592 (NBG), Williamson 2943, 2944 and

Williamson & Gassner 2925 (BOL)]. This new material

has roughly spherical, stiff, infructescences with long

pedicels and dry indehiscent capsules (Figure IB. C).

These characters fully match those diagnostic for Cybis-

tetes and clearly align the material with this genus.

Milne-Redhead & Schweickerdt (1939) had noted that

in A. herrei the number of flowers per umbel is greater,

the pedicels are longer and the number of ovules (2-4)

per locule is smaller than is usual for C. longifolia (8-19).

These differences are reduced, however, by the subsequent

collections of Hall 1081 and Snijman 435, 1314 at NBG &

PRE, from near Vanrhynsdoip. Observations based on all

the available material at BOL, NBG, PRE and STE show

that plants of C. longifolia from the south have 13-40-

flowered umbels and pedicels up to 100-210 mm long;

those from further north near Vanrhynsdorp have 35-47-

128

Bothalia 24,2 (1994)

FIGURE I . — Cybistetes longifulia on the alluvial plains of the Orange River, Richtersveld. A, solitary bulb with two inflorescences; B, developing

infructescence showing damage by a snout beetle (Brachycerus sp.); C, dispersed infructescence having released its seeds through tumbling;

D, leaves withering back after a short growth flush in February.

flowered umbels and pedicels up to 125-175 mm long;

whereas the Richtersveld plants from yet further north,

have 37-90 flowers per umbel and pedicels up to 100-150

mm long. Data on variation in ovule number in plants

from throughout the range are lacking but differences in

the abundance of seed per capsule from plants within the

Western Cape, near Vanrhynsdorp and the Northern Cape

in the Richtersveld support the observations of Milne-

Redhead & Schweickerdt (1939) on divergent ovule num-

bers from plants (Table 1 ). Infructescences collected near

Vanrhynsdorp and Namaqualand have a greater maximum

number of seeds per capsule than the fruiting material

collected in the Richtersveld. The capsules from the south

also tend to be longer and narrower than those in the north

(Figure 2). The differences, however, are not discrete and

the increase in seed number per capsule from the north

to the south appears to be continuous. There is also an

inverse relationship between seed size and seed number

per capsule within the species’ distribution range (Table

1 ). Thus plants in the Richtersveld and Namaqualand tend

to have especially large seeds (up to 29 mm across)

whereas the seeds of those in the south are smaller (7-19

mm across) (Figure 2). Seed size within a capsule is

nevertheless variable throughout the distribution range.

DISCUSSION

In the absence of any vegetative, floral or clearly dis-

continuous fruiting characters to distinguish A. herrei from

the variable C. longifolia, we propose that A. herrei is

conspeciftc with C. longifolia (L.) Milne-Redh. & Schweick.

but that plants of C. longifolia produce few, large seeds in

TABLE 1 . — Seed number and seed size in individual plants of Cybistetes longifolia throughout the distribution range

Bothalia 24,2(1994)

129

FIGURE 2. — Variation in size of capsules and seeds of Cybistetes longifolia. A, disintegrating capsule revealing many seeds from Gordon's Bay,

Western Cape (Duncan s.n.); B, seed from Gordon’s Bay (Duncan s.n.): C, capsules and seed from Beauvallon, Richtersveld (Williamson

4637); D, large seed from Annisrivier, Richtersveld ( Williamson 4639). Scale bars: 10 mm.

the semi-arid environments of the Richtersveld and Nama-

qualand, and many, relatively small seeds in the more equ-

able south. Accordingly A. herrei is treated here as a

synonym of C. longifolia.

As regards the comparative biology of individuals

within the amplified C. longifolia , the most noteworthy

variables are seed size and seed number. According to

Harper et. al. (1970) and Stebbins (1974) seed size and

seed number represent alternative strategies in the disposi-

tion of reproductive resources. However, due to divergent

and often conflicting advantages and disadvantages of

seed size versus seed number, most plant species have

evolved compromise strategies which depend on various

conditions of their habitat as well as their evolutionary

ancestry (Stebbins 1974). In the Richtersveld the annual

vegetative growth period of C. longifolia is often more

variable and shorter than that of plants in the Western

Cape whose foliage leaves are green for five to six months

throughout the winter rainfall season. The fleshy seeds of

C. longifolia, which germinate immediately after being

shed in autumn, are potentially susceptible to desiccation

injury before the onset of winter rain. Thus within the

constraints of the restricted and unpredictable growing

season for C. longifolia in the semi-arid Richtersveld and

Namaqualand the selection of large seeds, which have op-

timal reserves for their initial growth, appears to have been

favoured at the expense of seed numbers. In contrast, the

more reliable growing season of the Western Cape may

have promoted the selection of large seed numbers over

seed size to increase the probability that some seeds lodge

in suitably open habitats amongst the otherwise densely

vegetated communities of this region.

In several evolutionary lines Stebbins (1970) observed

the transference of function of a particular structure. A

notable example is the functional shift in the fruit wall

from that of providing protection for developing ovules

to one of effecting the dispersal of mature seeds. This

pattern is paralleled in Ammocharis and Cybistetes whose

indehiscent fruit walls initially protect the fleshy seeds

during development, but thereafter effect divergent disper-

sal strategies.

The lax infructescences of Ammocharis, which favours

seasonally moist habitats, initially elongate then flop to

the ground, releasing their seeds close to the parent plants.

In contrast, the indehiscent fruits of Cybistetes, which in-

habits open, dry situations, become dry, rigid capsules,

that radiate outward to form a sphere which then tumbles

in the wind (Markotter 1936; Martley 1938; Milne-Red-

head & Schweickerdt 1939) (Figure 1C). Following the

concept of transference of function (Stebbins 1974), it is

postulated that the basic protective function of the fruits

has shifted to include a derived dispersive function in

Cybistetes, where the entire infructescence serves as the

unit of dispersal. Clearly, the specialised infructescence

characters defined by Milne-Redhead & Schweickerdt

(1939) as separating Cybistetes from Ammocharis are

highly integrated and functionally interrelated to effect

dispersal by tumbling (anemogeochory of Van der Pijl

1982). It does not seem unlikely that this syndrome of

characters evolved from a most recent common ancestor

within Ammocharis as an adaptation to the high winds of

the Western Cape which probably date from the inception

of its Mediterranean-type climate in the Late Pliocene

(Deacon et al. 1992; Tankard & Rogers 1978). This in-

130

Bothalia 24,2 (1994)

terpretation suggests that Ammocharis sensu Milne-Red-

head & Schweickerdt (1939) is paraphyletic and that the

current classification of Cybistetes and Ammocharis war-

rants re-examination. Evidence of this, however, awaits a

phylogenetic analysis of all the species in the generic com-

plex and a character analysis of the closely related and

variable genus Crinum L.

In Amaryllideae anemogeochory is also known in

Boophane Herb, and Brunsvigia Heist. In most taxa the

infructescences detach at ground level and roll away in

the wind with the scape intact. The scape, which ap-

proximates the length of the radiating pedicels in most

species, appears to confer symmetry on the infructescence,

a configuration which Maddox & Carlquist (1985) have

shown ranks highly in tumbling ability. Boophane disticha

(L. f.) Herb, and Boophane haemanthoides F.M. Leight.

are exceptional in having infructescences which detach

from the scape distally. The resultant dispersal unit lacks

symmetry and appears to lose its integrity rapidly. These

observations suggest that Cybistetes, Boophane and

Brunsvigia offer interesting possibilities for experimental

studies in wind dispersal.

Cybistetes longifolia (L.) Milne -Redh. & Schweick.

in Botanical Journal of the Linnean Society 52: 192

(1939); Adamson & T.M. Salter: 211 (1950). Type: figure

in P. Herm., Paradisus batavus: t. 195 (1698), lecto.!, here

designated.

Amaryllis longifolia L.: 293 (1753). Crinum longifolium (L.)Thunb.:

59 (1794) pro parte, excl. descr. Ammocharis longifolia (L.) M. Roem.:

62 (1847).

Crinum falcatum Jacq.: 34, t. 60 ( 1 776). Amaryllisfalcata ( Jacq. ) L’ Her. :

13 (‘1788’, 1789). Haemanthus falcatus (Jacq.) Thunb.: 58 (1794).

Brunsvigia falcata (Jacq.) Ker Gawl.: t. 1443 (1812). Ammocharis falcata

(Jacq.) Herb.: 17 ( 1821 ); Baker: 96 (1888); Baker: 204 ( 1896) pro parte

(excluding Ammocharis coranica Herb. & Amaryllis coranica Burchell).

Type: figure in Jacq., Hortus botanicus vindobonensis 3: t. 60 (1776), lecto. !,

designated here.

Amaryllis coranica var. pallida Lindl. (sphalm. Burchell) sec.

Markotter: 13 (1936), non Lindl.: t. 1219 (1829).

Ammocharis herrei F.M. Leight.: 110 (1932), syn. nov. Type: South

Africa, Namaqualand, 60 miles S of Kommaggas, fl. ex hort. Stellenbosch,

April 1931, Herre sub SUG 3072 (BOL, holo.!).

Bulb solitary, ovoid to globose, 100-150 mm across,

extended into a neck up to 60 mm long, entirely subter-

ranean; outer tunics dark brown, tough and leathery; inner

tunics fleshy, cream-coloured. Leaves present or absent at

anthesis, 9-14, biflabellately arranged, spreading, strap-

shaped, more or less falcate, variable in length and width,

with the inner narrower and shorter than the outer, 6-270

x 13-55 mm, glaucous, smooth; margins scarious,

obscurely toothed or entire; apex truncate in mature

leaves, obtuse in young leaves. Inflorescence 1 3^-90-

flowered, ranging from somewhat clustered to widely

spreading, 150-340 mm across; scape erect, up to 200

mm long, compressed, about 10 x 22 mm, fleshy, smooth,

detaching from the bulb at ground level when dry; spathe

valves 2, reflexed, broadly lanceolate, 20-30 x 40-75 mm,

thinly coriaceous; bracteoles filiform; pedicels 50-110

mm long at anthesis, somewhat triangular in cross section,

radiating outward, stiffening and lengthening to 100-210

mm in fruit. Perigone widely trumpet-shaped, slightly

zygomorphic due to the declinate style, ivory to pink, turn-

ing deeper pink with age, dark reddish when collapsed,

sweetly scented; tube subcylindrical, widening slightly

towards the mouth, 8-15 mm long, firm and fleshy; lobes

oblanceolate, 40-65 x 8-15 mm, spreading and slightly

recurved distally, with a raised midrib on the abaxial sur-

face; stamens spreading, very slightly declinate, fused to

the perigone tube just below the throat, otherwise free;

filaments filiform, more or less equalling the perigone

lobes; anthers dorsifixed, about 12 mm long and cream-

coloured before opening; pollen cream-coloured. Ovary

about 10 mm long, narrowly fusiform, obscurely trian-

gular in cross section, placentation axile, 1-19 ovules per

locule; style slender, slightly longer than the perigone

lobes, declinate; stigma truncate, penicillate. Capsule inde-

hiscent, pyriform, ovoid, ellipsoid to subfusiform, 25-100

x 10-35 mm, somewhat triquetrous, strongly 6-ribbed,

bluntly beaked distally. Seeds subglobose or somewhat

bluntly angled by pressure, 5-29 mm wide, fleshy,

greenish; outer covering corky, pale; embryo green.

Chromosome number 2n = 22 (Gouws 1949). Figure 1.

Flowering phenology

Bulbs usually produce a single inflorescence between

December and March or occasionally in early April. Dis-

sections of mature bulbs from the wild retain evidence of

many aborted inflorescences which indicates that flower-

ing is sporadic. Despite this irregular flowering pattern,

inflorescence buds arise consistently in mature bulbs at

four-leaf intervals. Each vegetative shoot consists of a

non-amplexicaul bladeless prophyll, two amplexicaul

foliage leaves and a non-amplexicaul foliage leaf. This

leaf series is also known in Ammocharis heterostyla (Bul-

lock) Milne-Redh. & Schweick. and several species of

Crinum but, unlike Cybistetes, two inflorescences often

develop from each bulb within a few weeks of each other

(Hannibal 1955). Only rarely does the bulb of C. lon-

gifolia produce two inflorescences simultaneously (Figure

1A). The infructescences of C. longifolia usually mature

and detach within four weeks of flowering but during rare

wet autumn seasons the period from flowering to fruit

dispersal may last three months.

Vegetative phenology

Foliage leaves are present only when conditions are

favourable. Usually two growth flushes occur in response

to alternating wet and dry sequences throughout the year.

Thus leaves often appear briefly after late summer or

autumn rains when the bulbs may flower, but may soon

die back with the onset of a warm, dry period when the

infructescences are released (Figure 1 D). Thereafter suc-

cessive winter showers initiate rapid regrowth of the

withered leaves. The leaves may persist up to six months

in the wetter Western Cape (Markotter 1936), unlike the

more variable pattern of growth in the semi-arid Rich-

tersveld, where the leaf blades may elongate and die a

further two times during the year (G. Williamson pers.

obs.). This growth sequence gives the leaves the truncate

apices which are also found in A. coranica. Morphological

studies of A. coranica have shown that the regrowth of

mature leaves is due to a well-developed intercalary

meristem (Troll 1954).

Bothalia 24,2(1994)

131

Pollination

Markotter (1936) reports that wild plants of C. lon-

gifolia from Stellenbosch in the Western Cape are pol-

linated by night-flying moths. Other visitors to flowers of

C. longifolia in the Richtersveld are moths during the

early morning and two common butterflies, the painted

lady and green-yellow lucerne butterfly during the day

(G. Williamson pers. obs.). Snout beetles ( Brachycents

sp.) have been observed eating all parts of C. longifolia

(Figure IB).

Distribution and habitat

Cybistetes longifolia is widely distributed in south-

western Africa from the Orange River to the Cape Penin-

sula (Figure 3). The bulbs favour open, flat terrain either

in light sandy soil or hard gravelly clay.

Sandberg, (-AA), Van Jaarsveld, Forrester & Jacobs 85] 1 (NBG, PRE).

3017 (Hondeklipbaai): 60 miles S of Kommaggas, (-DA), Herre sub

SUG 3072 (BOL).

WESTERN CAPE. — 3118 (Vanrhynsdorp): 1 mile S of Widows

River, (-DA), Hall 1081 (NBG, PRE); flats between Wiedouw River and

Klaver, (-DA), Snijman 435 (NBG, PRE); 2.2 km S of Wiedouw River

towards Klawer, (-DA), Snijman 1314 (NBG, PRE); Farm Sandkraal,

Vanrhynsdorp Dist., (-DB), Van Breda 4377 (PRE). 32! 8 (Clanwilliam):

Farm Vondeling Op De Nardouwsberg, (-BB), Snijman 1315 (NBG);

Eendekuil, (-DB). Peers s.n. (BOL 16389). 3317 (Saldanha): Saldanha,

(-BB), Duncan 304 (NBG). 3318 (Cape Town): Darling Flora Reserve,

(-AD), Marais 10 (NBG); Lion’s Head, (-CD), Compton 21950 (NBG);

Rietvalley, (-DC), Zeyher 4115 (SAM); near Paarl, (-DB), Barker 5329

(NBG); Stellenbosch, (-DD), Duthie sub NBG 1353/26 (NBG). 3319

(Worcester): Breederivier, Worcester Dist., (-CB), Walters 2443 (NBG).

3418 (Simonstown): Sandy Bay, (-AB), Snijman 1017 (NBG); between

Faure and Lynedoch, (-BA), Esterhuysen 10113 (BOL, NBG, PRE); flats

between Gordon’s Bay and Strand, (-BB), Goldblatt 6463 (PRE). 3320

(Montagu): near Bonnie vale, (-CC), Smith (BOL 21376).

ACKNOWLEDGEMENTS

DISTRIBUTION RECORDS

NORTHERN CAPE. — 2816 (Oranjemund): Annisrivier, (-BD), G.

Williamson 2943 (BOL); Richtersveld, Grootderm, (-DA), Hall 592

(NBG, PRE); Arrisdrif, about 40 km E of Oranjemund, (-DA), G. & F.

Williamson 4626 (K, MO, NBG, PRE); Beauvallon, (-DA), Williamson

4637 (NBG, PRE); Williamson & Gassner 2925 (BOL); Beesbank,

(-DA), Williamson 2944 (BOL). 2817 (Vioolsdrif): Richtersveld,

FIGURE 3. — Known distribution of Cybistetes longifolia.

We thank Dr J.C. Paterson-Jones for the photographs

of seeds and fruits.

REFERENCES

ADAMSON, R.S. & SALTER, T.M. 1950. Flora of the Cape Peninsula.

Juta, Cape Town.

BAKER, J.G. 1888. Handbook of the Amary II ideae. George Bell, London.

BAKER, J.G. 1896. Amaryllideae. In W.T. ThiseltonDyer, Flora capensis

6,3: 529-536. Reeve, London.

DEACON, H.J., JURY. M.R. & ELLIS, F. 1992. Selective regime and

time. In R.M. Cowling, The ecology offynbos: nutrients, fire and

diversity. 7-22. Oxford University Press, Cape Town.

GOUWS, J.B. 1949. Karyology of some South African Amaryllidaceae.

Plant Life 5 : 54—8 1 .

HANNIBAL. L.S. 1955. Flowering habit of Ammocharis. Plant Life 11:

55, 56.

HARPER. J.L., LOVELL, P.H. & MOORE, K.G. 1970. The shapes and

sizes of seeds. Annual Review of Ecology and Svstematics 1:

327-356.

HERBERT, W. 1821. An Appendix. James Ridgway, London.

HERMANN, P. 1698. Paradisus batavus. Elzevier, Leiden.

JACQUIN, N.J. 1776. Hortus botanicus vindobonensis 3. Josephi

Michaelis Gerold, Vindobonae.

KER GAWLER, J.B. 1812. Brunsvigia falcata. Curtis's Botanical

Magazine 35: t. 1448.

LEIGHTON, F.M. 1932. Ammocharis herrei. South African Gardening

and Country Life 22: 110.

L'HERITIER DE BRUTELLE, C.L. 1789. Sertum anglicum 1. Graeffer,

London.

LINDLEY, J. 1829. Amaryllis coranica var. pallida. Edwards’s Botanical

Register 15: t. 1219.

LINNAEUS, C. 1753. Species plantation 1, Facsimile of 1st edn, W.T.

Stearn (ed.). Bartholomew, Dorking.

MADDOX, J.C. & CARLQUIST, S. 1985. Wind dispersal in Californian

desert plants: experimental studies and conceptual considerations.

Aliso 11: 77-96.

MARKOTTER, E.I. 1936. Die lewensgeskiedenis van sekere geslagte

van die Amaryllidaceae. Annale van die Universiteit van Stellen-

bosch 14, A, 2: 1-84.

MARTLEY, J. 1938. Ammocharis falcata. Herbertia 5: 225-228.

MILNE-REDHEAD, E. & SCHWEICKERDT. H.G. 1939. A new con-

ception of the genus Ammocharis Herb. Botanical Journal of the

Linnean Society 52: 159-197.

ROEMER, M.J. 1847. Familiarum naturalium regni vegetabilis synopses

monographicae 4. Landes-Industrie-Comptoir, Weimar.

STEBBINS, G.L. 1970. Transference of function as a factor in the evolu-

tion of seeds and their accessory structures. Israel Journal of

Botany 19: 59-70.

STEBBINS. G.L. 1974. Flowering plants, evolution above the species

level. Harvard University Press, Massachusetts.

132

TANKARD, A.J. & ROGERS, J. 1978. Late Cenozoic palaeo-environ-

ments on the west coast of southern Africa. Journal of Biogeog-

raphy 5: 319-337 .

THUNBERG, C.R 1794. Prodromus plantation capensium 1. Edman, Uppsala.

Bothalia 24,2 ( 1994)

TROLL, W. 1954. Praktische Einfuhrung in die Pflanzenmorphologie 1:

Der vegetative Aufbau. Gustav Fischer, Jena.

VAN DER PUL, L. 1982. Principles of dispersal in higher plants.

Springer- Verlag, Berlin.

Bothalia 24,2: 133-147 (1994)

Studies in the Marchantiales (Hepaticae) from southern Africa. 6. The genus

Asterella (Aytoniaceae: Reboulioideae) and its four local species

S.M. PEROLD*

Keywords: Asterella , A. bachmannii , A. marginata, A. muscicola , A. wilmsii, Aytoniaceae, Hepaticae, Marchantiales, Phragmoblepharis ,

Reboulioideae, section Saccatae, southern Africa

ABSTRACT

A taxonomic account of the genus Asterella , and four local representatives, A. muscicola. A. bachmannii, A. marginata and

A. wilmsii, subgenus Phragmoblepharis , is given here. A key to the species is provided. Two specimens identified by Amell

(1963) as Reboulia hemisphaerica, Collins 775 and Eyles CH 1175, are actually A. wilmsii: the presence of the genus Reboulia

in southern Africa is therefore not confirmed and should be deleted from the annotated checklist by Magill & Schelpe (1979)

and Plants of southern Africa: names and distribution (Arnold & De Wet 1993).

UITTREKSEL

'n Taksonomiese verslag oor die genus Asterella, en vier van die plaaslike verteenwoordigers daarvan, A. muscicola, A.

bachmannii, A. marginata en A. wilmsii, subgenus Phragmoblepharis, word hier gegee. ’n Sleutel tot die spesies word verskaf.

Twee eksemplare, Collins 775 en Eyles CH 1175, wat deur Amell (1963) as Reboulia hemisphaerica gei'dentifiseer is, is in

werklikheid A. wilmsii: die teenwoordigheid van die genus Reboulia in Suider-Afrika is dus nie bevestig nie en dit behoort

geskrap te word van die geannoteerde kontrolelys deur Magill & Schelpe (1979) en van Plants of southern Africa: names and

distribution (Arnold & De Wet 1993).

Asterella P. Beauv. in Dictionnaire des sciences

naturelles 3: 257 (1805); A. Evans: 247 (1920); Frye &

L. Clark: 69 (1937); Hassel: 100 (1962); S.W. Amell: 59

(1963); Vanden Berghen: 169 (1972); R.M. Schust.: 224

(1992). Type: A. tenella (L.) P. Beauv. (= Marchantia

tenella L.), (lecto. designated by Long & Grolle 1992b).

Fimbraria Nees: 44 (1820); Gottsche et al .: 555 (1846);

Schiffn.: 33 (1893); Steph.: 84 (1899); Sim: 22 (1926); K.

Miill.: 353 (1952), nom. illeg. Lectotype: F. marginata Nees.

Hypenantron Corda: 648 (1829). Type: H. ciliatum

Corda.

Dictyochiton Corda ex Nees: 258 (1838) nom. inval.

Rhacotheca Bisch.: 12 (1844). Type: R. azotica Bisch.

Octokepos Griff.: 343 (1849). Type: O. khasyanum

Griff.

Thalloid, smallish to medium-sized to fairly large, flat-

tish to slightly concave proximally, firm or rarely some-

what spongy, lime green to bright green, in crowded

patches or dense mats; on soil at seepages and river banks

or in drier, rocky locations. Branches simple, rarely

once/twice pseudodichotomously furcate, or with latero-

ventral or apical innovations; thickened over midrib, thin-

ning toward margins, these from above somewhat scal-

loped, attenuate, frequently purple; apex slightly notched,

with ventral scales recurving over edge.

* National Botanical Institute, Private Bag XI 01 . Pretoria 0001 .

MS. received: 1993-11-19.

Dorsal epidermis hyaline, unistratose, cells mostly

thin-walled, lacking trigones, occasionally with a single

large oil body; air pores small, simple, slightly raised, sur-

rounded by 2 or 3 concentric rings of cells, 6-8 per ring,

walls rarely radially thickened and pores then stellate; as-

similation tissue with small, empty air chambers in several

irregular layers or tall and in one layer, cells in bounding

walls chlorophyllose but occasionally with an oil body;

storage tissue with rounded or angular cells closely packed

together; rhizoids both smooth and pegged. Scales mostly

purple or wine-red, in 2 forwardly directed ventral rows,

ovate to obliquely triangular, with one (rarely 2 or 3) lan-

ceolate or acuminate appendage, scattered oil cells

present, margins mostly entire.

Monoicous, paroicous or autoicous, rarely dioicous.

Androecia sessile; antheridia in paroicous species in a

cluster or a row immediately or somewhat further poste-

rior to insertion of stalk; in autoicous or dioicous species,

androecia well-defined, on reduced latero-ventral branches

or as a median oval disc on main branch. Archego-

niophores arising from apical notch, borne on stalk with

or without air chambers and with one rhizoidal furrow, at

the summit, with or rarely without paleae; head rounded

or umbonate, nearly smooth to distinctly papillose, its air

chambers opening via compound pores, below with (1-)

2^f(-5) lobes, each enclosing a capsule, the wall of the

latter lacking thickening bands; involucre membranous,

continuous with edges of lobes; pseudoperianth present,

mostly pendulous, conical or blunt, vertically split into

segments, but united at the tip, covering and projecting

beyond the capsule in southern African species. Spores

small to medium-sized to large, yellow, brown or fuscous,

triangular-globular and winged, distal face rounded, most-

ly with regular or irregular network of large, angular to

134

Bothalia 24,2 (1994)

FIGURE 1 . — Asterella muscicola. A, dorsal view of thallus; B, ventral view of thallus; C, carpocephalum raised on stalk and antheridia proximal to

foot of stalk; D, transverse section of thallus; E, scale with fimbriate apex; F, scale with acuminate apex; G, transverse section of air pore; H,

dorsal cells, air pore and oil cell from above; 1, transverse section of stalk; J, longitudinal section of young archegoniophore; K, capsule wall

cells. A-C, E, G, I, J, Perold & Koekemoer 2968\ D, F, H, Conch 13\ K, Anderson 1248. Scale bars: A-D, 2 mm; E, F, I. 250 pm; J, I mm;

G, H, K, 50 pm.

Bothalia 24,2 (1994)

135

rounded areolae, bordered by ridges and generally lined

with small subsidiary areolae; proximal face with

pronounced triradiate mark, its arms extending across un-

dulating wing, each of three facets also with network of

large and small areolae. Elaters short or of medium length,

with 1-3 spirals. Chromosome number, n = 9 or multiple

thereof, or 10.

Asterella is one of the larger genera of the Marchan-

tiales. It is classified in the family Aytoniaceae, subfamily

Reboulioideae. The genus Asterella has been divided into

three subgenera: Brachyblepharis, Asterella and Phrag-

moblepharis, the latter with three sections, namely Pap-

piae, Lindenbergianae and Saccatae (Grolle 1976). Aste-

rella species are easily recognized by the presence of a

basket-like pseudoperianth, which soon splits into narrow

segments. It occurs world-wide and has had a long and

controversial nomenclatural history, which is reviewed by

Long & Grolle (1992a). Long & Grolle (1992b) have also

submitted a proposal to conserve the generic name

Asterella with a conserved type.

The four southern African species of Asterella are all

placed in subgenus Phragmoblepharis Grolle (1976),

since the segments of the pseudoperianths remain coherent

at their tips for a long time, in contrast to those in sub-

genera Brachyblephar is and Asterella, where they separate

at maturity. The last two subgenera are not found in

southern Africa.

Key to the southern African species of Asterella

la Thalli spongy, with tall air chambers mostly in one storey, and then not subdivided by supplementary partitions, each opening

dorsally by a stellate pore; ventral scales occasionally fimbriate at single lanceolate appendage; carpocephalum round or

umbonate and lacking paleae at summit of stalk; pseudoperianth extending ± 300 |im beyond involucre and subdivided

into 12 or 13 segments; spores 75-95 pm in diameter, dark brown, ornamentation with irregular zigzagging ridges ....

1. A muscicola

1 b Thalli compact, firm, with small, low air chambers in several storeys, only some top ones opening above by a dorsal, non-stellate

pore; ventral scales with 1 (or 2) lanceolate or ovate appendages, margin ± entire; carpocephalum round or umbonate,

papillose or ± smooth, with paleae at summit of stalk; pseudoperianth extending more than 1000 pm beyond involucre

and subdivided into 14—16 segments; spores more than 100 pm in diameter, yellow or brown, ornamentation with larger

areolae generally containing subsidiary areolae:

2a Thalli smallish to large; carpocephalum covered with distinct papillae, projecting ± 200 pm; paleae at summit of stalk shaggy,

dense, pale mauve or colourless, up to 3000 pm long and 4 or 5 cells wide at base; ventral scales with lanceolate

appendage; spores elaborately ornamented with 6-8 areolae across distal face, 20-30 pm wide and ridges extending

across wing, containing numerous subsidiary areolae (common, mostly summer rainfall species) 2. A. bachmaimii

2b Thalli medium-sized to very large; carpocephalum ± smooth or with low papillae; paleae at summit of stalk colourless or

purple, length variable; ventral scales with lanceolate or ovate appendages, spores less elaborately ornamented:

3a Thalli medium-sized; carpocephalum with umbonate head; paleae at summit of stalk mostly colourless, some very long,

more than 8000 pm in length, ± 4 cells wide at base; ventral scales with 1 or 2 lanceolate appendages; spores on

distal face with (4— )6— 9 areolae across, ± 32 pm wide, very high ridges seldom extending across wing, usually

containing small subsidiary areolae (winter rainfall species) 3. A. nuirginata

3b Thalli large to very large; carpocephalum with rounded head, distinctly lobed below; paleae at summit of stalk almost

colourless to purple, 2000-3000 pm long, some up to 7 cells wide at base; ventral scales with single, large-celled,

ovate appendage, constricted at base; spores on distal face with 5-8 areolae across, 25-30 pm wide and extending to wing

margin, almost empty of subsidiary areolae and hollow (summer rainfall, mostly Afromontane species) 4. A wihnsii

1. Asterella muscicola (Steph.) S. W. Arnell: 60

(1963).

Fimbraria muscicola Steph.: 121 (1892); Steph.: 97 (1899), Sim: 22

(1926). Type: Transvaal, Spitzkop bei Lydenburg, Febr. 1888, leg. Dr

Wilms G 001664 , holo.! (G); G 024589 , iso.! (G).

Thallus medium-sized to fairly large, grooved toward

apex, slightly concave more proximally, dorsally bright

green, margins soon turning purple along edge, becoming

proximally wider (up to 1 mm) and pinkish purple (Figure

1A), polygonal outlines of subdorsal air chambers visible

from above, i.e. reticulate dorsally, median areolae small,

enlarging toward margins and then in parallel, radiating

rows, air pores tiny, slightly raised, white ‘specks’, ap-

parently solitary over each polygonal area, wet; thallus

margins clasped together, revealing deep purple, transver-

sely wrinkled underside of wings, dry; in crowded

patches, simple or once/twice pseudodichotomously fur-

cate. Branches 4— 7 (-13) mm long, total length up to 18

mm long, 2.5-3 .5(-6.5) mm wide, in section 1250 pm

thick over midrib, laterally thinning out into attenuate

wings, apex notched, with tips of 4—6 hyaline or purple-

red ventral scales recurving over edge; margins acute, thin,

scalloped, undulate, older parts dead, ventrally somewhat

striate across, shiny, deep purple, flanks sloping obliquely;

ventral face medianly keeled, green, midrib with row of

purple-red scales on either side (Figure IB).

Dorsal epidermis unistratose, hyaline, purplish toward

margins, cells thin-walled, without trigones at angles, from

above 4- or 5-(-7)-sided, (37.5-) 45.0-72.5 x 15.0-25.0

pm, in transverse section 25 pm thick, rarely containing

an oil body; marginal cells mostly 4-sided, variable in

size, (17.5-)25.0-50.0 x 15.0-40.0 pm; air pores very

slightly raised, simple, small, ± 7.5 pm wide, mostly 6-

sided (Figure 1H), up to 137.5 pm distant from each other,

bounded by innermost circle of collapsed cellular remains,

otherwise surrounded by 2 concentric rings of cells, each

generally with 6 cells: inner cells bluntly triangular, smal-

lest 12.5 x 7.5 pm at inner, narrower tip and 17.5 pm at

wider part, larger cells 22.5 x 25.0 pm, radial walls most-

ly thickened and pores thus stellate, outer row of cells

(22.5— )25.0— 32.5 x 25.0-37.5 pm. partly overlain by inner

cells; assimilation tissue up to 650 pm thick, with air

chambers long and empty, in one layer (Figure ID), or

sometimes in several layers, particularly if section not ex-

actly vertically cut and then seen in more than one

plane, 90-150 pm wide above, narrowing to ± 50 pm

wide below, vertical medianly, sloping obliquely toward

margins, unistratose walls composed of cells, (30. 0-)

136

Bothalia 24,2 ( 1994)

37.5 — 47.5 x 32.5 pm in transverse section, when viewed

from the front, 30.0-45.0 x 32.5-40.0 jam; occasionally

with somewhat smaller cells containing an oil body,

light brown to dark brown, smooth or finely warty,

round, diameter ± 30 (am, almost entirely filling cell;

storage tissue ± 600 |am thick, cells tightly packed

together, angular, 20.0-37.5 pm wide, some with oil

bodies, which are here more frequent than in air cham-

ber walls; rhizoids smooth, ± 17.5 pm wide, or pegged

and 22.5 pm wide. Scales wine-red to purple-red, ar-

ranged in 2 forwardly directed ventral rows, one on

either side of midrib, not extending to margins of tlial-

lus, except at apex, obliquely triangular, 1100-1250 pm

wide at curved base, above with acuminate appendage

tapering to a narrow tip (Figure IF), occasionally

toward apex fimbriate (Figure IE) and sometimes with

several one- or two-celled marginal papillae, up to 37.5

x 10.0 pm, total length ± 1050 pm, including 170-350

pm long appendage, 8 or 9 cells wide where it joins

body of scale, cells 5- or 6-sided, rarely rectangular,

57.5- 100.0 x 25.0-32.5 pm, occasionally interspersed

with scattered smaller, colourless cells (2—6 or 8), the

oil body having been lost.

Paroicous. Androecia with antheridia in a group or in

a short single or double row along midline of thallus and

generally immediately proximal to stalk, i.e. basiscopic

of archegoniophore (Figure 1C) or very rarely on sepa-

rate plant, immersed, 350 x 250 pm, each opening above

into a prominent, conical papilla, 220 x 100 pm. Ar-

chegoniophores single, rarely paired at apices of 2 fur-

cating branches, almost sessile when young (Figure 1 J),

domed, air pores compound, leading below into air cham-

bers, supported on and radiating outwards from central

core of parenchymatous tissue, containing numerous oil

cells, these also present in air chamber walls and epider-

mis. Carpocephala at maturity raised on stalk (Figure

1C) arising at bifurcation of branches, the latter continu-

ing in growth; stalk yellowish, shiny, erect or somewhat

bent, 5-8 mm long, stout, 675 pm wide at ± midlength,

becoming thicker toward base and tapering toward sum-

mit, in transverse section irregular in shape, with one

rhizoidal furrow, 175 x 137 pm, cortical cells in single

layer, thick-walled, brown, 12.5 x 12.5-15.0 pm, medul-

lary cells thin-walled, 20.0-32.5 x 12.5-25.0 pm, with

narrow to wide, open air chambers (Figure II); head

rounded to somewhat umbonate, 3 mm across, bearing 4

or 5 capsules, the wall brown with unistratose cells lack-

ing spiral thickenings, 4-6-sided, 50.0-57.5 x 20.0-25.0

pm; pseudoperianths extending obliquely downward and

outward and projecting ± 300 pm beyond involucre,

somewhat flattened sideways, in 12 or 13 cage-like,

hyaline segments, each of which 550 x 150 pm, connate

toward broad, blunt tips, at apex with small central nipple

penetrated by a pore, cells in segments 4-6-sided, 47.5

x 22.5 pm, thick-walled. Spores 75-95 pm in diameter,

triangular-globular, dark brown, opaque, wing somewhat

pleated, 5 pm wide, margin undulate, distal face (Figure

2A-C) convex, reticulate, with very irregular, mostly in-

complete areolae, the ridges forming an irregular, zig-

zagging maze; proximal face (Figure 2D E) with distinct

triradiate mark, facets also with irregular, incomplete

areolae, ranging from small and crowded to larger and

more widely dispersed. Elaters 150-175 pm long, 17.5

pm wide in centre, slightly tapering toward ends, doubly

spiral (Figure 2F), light brown. Chromosome number.

n = 10 (T. Bornefeld pers. comm.)

DISCUSSION

This species of Asterella has tall air chambers and was

initially placed in the group Spongiosae, together with A.

FIGURE 2. — SEM micrographs of Asterella muscicola. A-E, spore: A, distal face; B, distal side view; C, areolae on distal lace much enlarged; D,

proximal face; E, side view. F, elater. A, D-F, Perold & Koekemoer 2968\ B, C, Marais 832. A, D, E, x 490; B, x 320; C, x 952; F, x 460.

Bothalia 24,2(1994)

137

pilosa and A. tenera, by Stephani (1892). It was illustrated

by him in his leones (Microform 1985 seen by me). Later

on, Stephani (1899) proposed a new classification based

on the shape of the female receptacle and he then placed

it in group B, Capituli centrum hemisphaericum. Now-

adays it is classified in subgenus Phragmoblepharis

Grolle, (since the pseudoperianth segments remain at-

tached at their tips when mature), and in its section Sac-

catae, (since the summit of the stalks lack paleae).

Sterile specimens of A. muscicola have been confused

with Athalamia spathysii , since the dorsal air pores are

also stellate. The air chambers are likewise devoid of

chlorophyllose filaments, but oil bodies are more

numerous and their remains are present in the scales

which have cells half as wide as those in A. spathysii. It

differs from Athalamia species mainly in sporophyte char-

acters: the stalk arises at the bifurcation of the branches,

it is thicker and has a rhizoidal furrow, its cortical cells

differ from those in the medulla where air chambers are

present, it is devoid of scales both at the base and summit

(Amell (1963) erroneously refers to scales at the top), the

cells in the capsule wall lack annular or semi-annular

thickenings, pseudoperianths are present, the spores are

larger, dark brown and winged, their ornamentation is

reticulate (not papillose), the shape is triangular-globular

with a distinct triradiate mark on the proximal face and

the elaters are shorter and wider. Mycorrhiza are present

in the storage tissue, having entered via the rhizoids.

Vegetative reproduction is rarely by ventral stolons.

Quite a number of Asterella specimens held at PRE

had been incorrectly identified as A. muscicola, even by

Amell (1957), who also misnamed a Volk collection of

Athalamia spathysii from Namibia as Asterella muscicola

(Volk 1979). Sim (1931) also reported A. muscicola from

South West Africa [Namibia] but this has not been con-

firmed; in fact, according to Volk (1979), Grolle had in-

formed him (pers. comm.) that A. muscicola does not

grow in Namibia.

The type specimens consist of only a few fragments

and were collected east of Lydenburg, south of the present

town of Sabie, Eastern Transvaal. The species is probably

endemic to southern Africa and is known from Botswana,

the North-West (northeastern Cape & southeastern Trans-

vaal), Northern and Eastern Transvaal (type specimen),

KwaZulu/Natal, Orange Free State, Lesotho, and Eastern

Cape (Figure 3). Its range extends into Malawi (Kasunga

Nat. Park, Perold 2682) and Zimbabwe (Eyles 932, 933;

Miller 7869) from where it is also reported by Best (1990).

It frequently grows at high altitudes on soil overlying

sandstone or basalt outcrops in association with other

liverworts such as Plagiochasma spp. and Riccia spp.

2. Asterella bachmannii (Steph.) S. W. Amell,

Hepaticae of South Africa: 62 (1963). Type: Pondoland,

Port Grosvenor, Bachmann ( 13866 G, lecto.!; 13867 G!).

Fimbraria bachmannii Steph.: 7 (1894); Steph.: 105 ( 1899). Sim: 22

(1926).

TTtallus smallish to medium-sized to quite large, firm

and compact, dorsally flat, light green, rather crystalline

to shiny when fresh, margins turning purple on exposure

to sun (Figure 4A), crinkled outlines of small subdorsal

air chambers faintly or not visible from above, air pores

FIGURE 3. — Distribution of Asterella muscicola. •; A. wilmsii. □ , in

southern Africa and Zimbabwe; andA. marginata. ▲, in southern

Africa. Summer rainfall area: to the right of the solid line. Summer

and winter rainfall area: to the left of the solid line. Winter rainfall

area: to the left of the broken line.

tiny, slightly raised and scattered, wet; thallus margins

raised or inflexed, sometimes inrolled and tightly clasped

together, dry; in crowded, overlying mats, simple or oc-

casionally once, rarely several times pseudodichotomously

furcate, often with apical or latero-ventral innovations.

Branches broadly ligulate, widening rapidly from narrow

base, when simple up to 17 or 18 mm long, when

branched total length up to 25 mm, with terminal branches

3-4 mm long and moderately divergent, (1.9— )2.5— 4.0

(-4.9) mm wide, (450-)500-600(-775) pm thick over

midrib, laterally thinning out into attenuate wings, apex

slightly notched, with tips of a few ventral scales recurv-

ing over edge; margins acute, thin, slightly scalloped,

somewhat undulate; ventrally green or red to deep purple,

laterally somewhat striate across obliquely sloping flanks,

medianly keeled, midrib with row of purple scales on

either side (Figure 4B).

Dorsal epidermis unistratose, generally containing

chloroplasts, from above cells (4-)5- or 6-sided, thin-

walled, (30.0— )50.0—67.5(— 90.0) x 22.5-30.0 pm, their

orientation changing from apically directed medianly to

outwardly sloping laterally in transverse section, (20-)

25-35 pm thick, occasionally containing a round oil

body, 25 pm across, almost filling cell; marginal cells in

1 or 2 rows, long- or short-rectangular (Figure 4G), oc-

casionally 5-sided, 30.0-50.0 x (1 2.5-) 17.5-22.5 pm; air

pores slightly raised (Figure 4F), simple, small, oval, up

to 17.5 x 12.5 pm, 110-150 pm distant from each other

(Figure 4E), bounded by innermost circle of collapsed

cells, and outwardly surrounded by 2 intact, partly over-

lying concentric rings of 6— 8(— 10) cells in each, inner

ones smaller, ± 12.5 x 15.0-20.0 pm, outer ones bluntly

wedge-shaped, up to 15-20 x 25-35 pm. radial walls not

thickened; assimilation tissue up to 280 mm thick, with

small, empty air chambers (Figure 4D), 37.5-75.0 pm

wide, in 2-4 storeys, toward margins elongating and slop-

ing obliquely, chlorophyllose cells in bounding walls

rounded or oval, 25.0-30.0 x 22.5-32.5 pm; storage tis-

sue mostly confined to keel, ± 360 pm thick, cells an-

gular, isodiametric, ( 17. 5-)25. 0-35.0 pm wide, closely

packed together, walls thick and pitted, an occasional cell

138

Bothalia 24,2 (1994)

i i

FIGURE 4. — Asterellci bachmannii. A, dorsai view of thallus; B, venlral view of thallus, appendages of scales mostly not visible against dark purple

flanks; C, carpocephalum with papillose disc and two pseudoperianths; D, transverse section of thallus; E, air pore and surrounding cells

from above; F, transverse section of air pore; G, marginal cells; H, appendage and upper part of scale; I, transverse section of stalk; J, paleae.

A-D, I, Glen 2/50; E, G, H, .1, Perold & Koekemoer 2856\ F, Candy 7. Scale bars: A-D, I mm; E-G, 50 pm; H, 1, 250 pm; J, 100 pm.

Bothalia 24,2(1994)

139

with oil body; rhizoids arising from ventral surface

numerous, smooth, 15-20(-30) (4m wide, or pegged, 7.5-

17.5 |im wide. Scales (Figure 4H) red to deep purple,

arranged in 2 forwardly directed ventral rows, one on

either side of midrib, not extending to margins of thallus,

obliquely triangular, usually with a single lanceolate ap-

pendage, occasionally with two, 450-650(-800) |4m long,

constricted at base, 150-200 |4m wide, tapering above to

a conical apical cell, 50.0-87.5 x 7.5-17.5 pm, lower

cells 95.0-125.0 x 32.5-37.5 pm, body of scale up to

1000 pm long and 1500 pm wide at its crescentic base,

cells 4-6-sided, 50.0-77.5 x 25.0-35.0 pm, scale tapering

to narrow ‘tail' below, cells long and narrow, 82.5-122.5

x 12.5 pm, ± 8 smaller, colourless cells per scale, 35 x

35 pm, containing remains of oil body.

?Dioicous, rarely autoicous. Androecia extending back-

wards in median patch from apex of main branch, rarely

with a second one at a midlength constriction, or, some-

times on short apical or lateral innovations, antheridia im-

mersed in sessile, elongated or oval cushions, ± 3000 x

750 pm, lacking scales and opening above via stout,

raised, purple-red papillae, 150 pm long. Archego-

niophores proximal to apical notch of main branch or rare-

ly on short latero-ventral innovations, single, occasionally

paired at apices of 2 forking branches, almost sessile when

young, with numerous (± 75), long, pale, sometimes

purple, paleae arching over disc. Carpocephala at

maturity raised on stalk, arising 1.5 mm back from apex

of branch in apical notch, its foot sometimes in a shallow,

rounded depression proximally, its length variable, ( 1— )5—

1 3(— 20 ) mm long, whitish to purple, widening toward

base, in transverse section at ± midlength (Figure II) 550

x 450 pm, with single rhizoidal furrow, cortical cells in

a single layer, slightly thicker-walled. 17.5 x 12.5 pm.

medullary cells angular, ± 25.0 x 17.5 pm; at summit of

stalk ± 32 slender, shaggy paleae, white or purple, up to

3250 pm long, 4 or 5 cells wide at base, cells 120-137

x 25 pm, gradually tapering to conical apical cell, 67.5 x

20.0 pm (Figure 4J); disc rounded, ± 3 mm across when

bearing 4 or 5 capsules, but frequently with only 1 or 2

capsules (Figure 4C) and then smaller, above with

numerous prominent papillae, outwardly projecting ± 200

pm and enclosing air chambers which open above via

compound air pores; membranous involucre partly cover-

ing capsules below, the latter spherical, 1000 pm across,

the wall turning brown, unistratose, cells lacking spiral

thickenings, 4-6-sided, 62.5-80.0 x 27.5-37.5 pm, toward

apex of capsule cells shrinking and their walls thickening,

with trigones at corners, the wall dehiscing along well-

defined line and inner basal part remaining attached; pseu-

doperianths descending obliquely downward and

extending ± 1000 pm beyond involucre, generally split

into 14 cage-like segments, shiny white or purple-stained,

up to 2375 pm long and 750 pm wide at widest part,

tapering to narrow tips where coherent with other seg-

ments, the cells elongated, 175-258 x 37 pm, becoming

shorter toward tip. Spores 102.5-125.0 pm in diameter,

triangular-globular, mostly yellow, sometimes brown,

translucent, wing undulate, up to ± 20 pm wide, margin

crenulate, distal face (Figure 5A, B) convex, with network

of 6-8 angular areolae across, 20-30 pm wide, ridges 7.5-

10.0 pm high and laterally extending across wing, hollow

floor of areolae highly porate (Figure 5C) and generally

with smaller subsidiary areolae (Figure 5A), sometimes

with ornamentation becoming very elaborate (Figure 5B)

and always extending over crests of main ridges and

across wing to margin; proximal face with prominent

triradiate ridge (Figure 5D, E), its arms ± 15 pm high and

continuous from the pole across wing to margin, each of

FIGURE 5. — SEM micrographs of Asterella bachmannii. A-E, spore: A, distal face with primary and subsidiary areolae; B, distal face, seen slightly

from side, with more highly ornamented areolae; C, much enlarged areolae on distal face, lacking subsidiary areolae, but highly porate; D.

proximal face; E, side view. F, elater. A, Glen 2155 ; B, Dieterlen 1142; C, S.M. Perold 2703 ; D. Perold & Koekemoer 2917: E, Perold &

Koekemoer 2874; F, Perold & Koekemoer 2856. A, D, E, x 400; B, x 430; C, x 1000; F, x416.

140

Bothalia 24,2 (1994)

3 facets with areolae, ± 10 jim wide, also extending across

wing and containing numerous (Figure 5D) or fewer (Fig-

ure 5E), smaller, subsidiary areolae that cross over crests

of main areolae and onto wing to margin, which is finely

ornamented on both faces. Elaters 1 42— 1 65(— 1 80) pm

long, and 15 jam wide in centre, slightly tapering to the

ends, doubly spiral (Figure 5F), yellow. Chromosome

number, n = 9. (T. Bomefeld pers. comm.)

DISCUSSION

Asterella bachmannii is a variable species and can

range in size from smallish to quite large. The thallus

margins and ventral face can be very deeply pigmented

or hardly at all, depending on whether it is exposed to

intense sunlight or not. The ventral scales can likewise be

deeply pigmented and the appendages are then not clearly

discernible against the purple flanks as in Figure 4B. It

can be distinguished from A. muscicola by the compact-

ness of the assimilation tissue and from A. wilmsii, by its

smaller size and the lanceolate appendages (occasionally

double) of the purple or reddish purple ventral scales and

from A. marginata by its generally purple, not wide, black

thallus margins and by its mostly summer rainfall distribu-

tion. Sterile specimens with lanceolate scale appendages

that had been collected in the summer rainfall areas (Fig-

ure 3: area to the right of the solid line) have not been

named, although there can be little doubt that they should

also be placed under A. bachmannii. Asterella bachmannii

and A. marginata are, however, sympatric in the Western

and Eastern Cape, where the winter and summer rainfall

seasons overlap (Figure 3: area to the left of the solid

line), and here too only specimens with carpocephala have

been named. Fertile plants of A. bachmannii are easily

recognized by the mostly pronounced papillae on the disc

of the carpocephalum as well as by the dense, narrow,

stringy or shaggy paleae which are usually white, but oc-

casionally can be purple-stained. The spores are highly

ornamented with the main areolae containing numerous

smaller subsidiary areolae on both faces, giving it a lacey

appearance. Spores from all available sporulating material

were photographed by SEM and the spore ornamentation

proved to be the most consistently uniform character, ex-

cept in immature spores and in some old spores which

had become shrivelled.

The sexuality is difficult to determine, as the plants

form dense overlying mats with apical and latero-ventral

innovations; rarely xould it be conclusively ascertained

that an androecium grew on a short lateral innovation of

a main branch with a carpocephalum at the apex and even

more rarely, both a carpocephalum and an androecium

were found on lateral innovations of the same main

branch.

Asterella bachmannii is common and by far the most

frequently collected Asterella species in the summer rain-

fall areas of southern Africa. It is known from Botswana,

the North-West, Northern and Eastern Transvaal, the PWV

(central Transvaal), Swaziland, KwaZulu/Natal, Orange

Free State, Lesotho, Eastern and Western Cape (Figure 6).

It is mostly found on damp soil along stream banks, at

waterfalls or in shaded gulleys or kloofs, sometimes on

soil-covered vertical rock walls at seepages or on soil

overlying sandstone, in light shade or in full sunlight. It

FIGURE 6. — Distribution of Asterella bachmannii in southern Africa

(and Zimbabwe).

occasionally grows together with A. wilmsii , Sym-

phyogyna species and Fossombronia species. Its range ex-

tends into Zimbabwe (Eyles CH 776 , CH 1122 , CH 1276;

Miller CH 4250; Schelpe 4009 , 5359; Sim CH 1213, CH

1249) and Malawi ( Perold 2573 , Nyika Nat. Park). Best

(1990) has also reported it from Zimbabwe. It is thought

that the specimens from Zaire ( Schmidt 258, 7188 ) iden-

tified and described by Vanden Berghen (1972) as A. mar-

ginata should be placed here, since the carpocephalum

disc is markedly papillose and the ventral scale, as il-

lustrated by him, has two acuminate appendages, which

I also sometimes found in A. bachmannii. In A. marginata

most of the paleae are generally much longer and its dis-

tribution is moreover apparently confined to the winter

rainfall area (Figure 3: area to the left of the broken line)

of the Western Cape with outliers in the Eastern Cape.

3. Asterella marginata (Nees) S.W. Arnell,

Hepaticae of South Africa: 63 ( 1963). Type: Capite b. spei,

crescit iuxta viam in monte Leuwenstaart ad terrain, leg.

Bergius (BM).

Fimbraria marginata Nees: 44 (1820); Gottsche et a!:. 559 (1846);

Steph.: 104 (1899).

Thallus medium-sized, firm and compact, dorsally flat-

fish to somewhat concave, bright green, marginally with

narrow to mostly wide black or occasionally reddish

purple border (Figure 7A), shiny to dull, outlines of sub-

dorsal air chambers hardly visible from above, air pores

slightly raised and scattered, wet; thallus margins raised

to inrolled, dry; in crowded mats, simple or once, rarely

twice pseudodichotomously furcate, sometimes with api-

cal or latero-ventral innovations. Branches obovate to ob-

cordate, or ligulate, frequently widening rapidly from

narrow base, up to 23 mm long, with tenninal branches

10-15 mm long and moderately to widely divergent, 2.3-

5.0 mm wide, 550-565 pm thick over midrib, laterally

thinning out into attenuate wings, apex notched, with ap-

pendages of apical scales recurving over edge; margins

acute, thin, very wavy to almost frilly; ventrally green

over midrib, but partly covered by row of purple scales

on either side (Figure 7B), flanks purple to black and obli-

quely sloping (Figure 7D).

Bothalia 24,2 (1994)

FIGURE 7. — Asterella marginata. A. dorsal view of thallus with young carpocephalum raised on stalk and sessile androecium; B, ventral view of

thallus; C, carpocephalum with pseudoperianths; D, transverse section of thallus; E, transverse section of air pore; F, air pore and surrounding

cells from above; G, marginal cells; H, ventral scale with one appendage; I, ventral scale with 2 appendages; J, transverse section of stalk; K,

paleae. A, B, D-F, FI, I, S.M. Perold 2787\ C, Pillans 3991 ; G, Arnell 505 ; J, Arnell 206', K, Koekemoer 3 1 6. Scale bars; A-D, 1 mm; E-G,

50 pm; H-J, 250 pm; K, 100 pm.

142

Bothalia 24,2 (1994)

Dorsal epidermis unistratose, from above cells 5- or

6-sided, walls thin but slightly thickened at corners, 30.0-

45.0 x 17.5-20.0 jam, in transverse section 27.5-37.5 pm

thick; marginal cells in 1 or 2 rows (Figure 7G), short-

rectangular, 25 x 30 pm, or isodiametric, 27.5 x 27.5 pm,

or irregular in shape; air pores slightly raised (Figure 7E),

simple, oval, small, ± 10.0 x 7.5 pm and up to 1 17.5 pm

distant from each other, bounded by innermost ring of

collapsed cells, ± 5 pm wide, outwardly surrounded by 2

intact, partly overlying concentric rings of 5-7 cells in

each, inner ones smaller (Figure 7F), 10.0-12.5 x 12.5—

22.5 pm, outer ones 15.0-17.5 x (17. 5-) 25.0-35.0 pm;

assimilation tissue 200-250 pm thick, with small, empty

air chambers in top 2 or 3 storeys, 12.5-42.5 pm wide,

becoming larger in lowest storey, up to 75 x 50 pm,

chlorophyllose cells in bounding walls rounded to oval,

20.0-35.0 x 22.5-27.5 pm, quite frequently with round

oil body, ± 20 pm in diameter and almost tilling cell;

storage tissue confined to keel, ± 300 pm thick, cells an-

gular and closely packed together, 22.5^15.0 pm wide,

some containing an oil body, cell walls porate, thickened,

often with striate network of thickening bands; rhizoids

numerous, some pegged, 10-15 pm wide, others smooth,

15-22 pm wide. Scales (Figure 7H, I) deep purple to

lightly pigmented, in two forwardly directed ventral rows,

one on either side of midrib, not extending to thallus mar-

gins, triangular to obliquely triangular, with 1 or 2(3) lan-

ceolate, apically shortly acuminate appendages, equal in

length or not, 675-925 pm long, tapering to single apical

cell, ± 105 x 15 pm, lower cells ± 100.0 x 27.5 pm,

gradually becoming shorter, ± 40.0 x 22.5 pm, toward

unconstricted base, ± 375 pm wide, body of scale ± 675

pm long, 825-925 pm wide at crescentic base, cells 55-

125 x 27-32 pm, 5- or 6-sided, walls somewhat sinuate,

tapering below to narrow 'tail', where cells long-rectan-

gular, 70-150 x 10-12 pm, oil body remains in up to ±

20 cells per scale, colourless, rounded, 37.5 x 30.0 pm,

a few small mucilage papillae at lateral scale margin.

Autoicous or monoicous. Androecia in sessile cushions

on latero-ventral innovations or at base of main branches

(Figure 7A), antheridia immersed and opening above via

raised, purple papillae. Archegoniophores proximal to api-

cal notch of main branch, single, occasionally paired at

apices of two furcating branches, almost sessile when

young. Carpocephala at maturity raised on stalk, arising

± 1 mm back from apex of branch in apical notch, its

foot slightly wider than midlength dimensions of ± 575

x 600 pm, in transverse section (Figure 7J) with a single

rhizoidal furrow, 85 pm wide, cortical cells in one layer,

slightly thicker-walled on outside, small and rounded, ±

17.5 x 17.5 pm, medullary cells angular, 15-30 pm wide,

length of stalk variable, 2.5-18.0 mm, white or reddish

purple, at its summit (and along its length) with numerous

pale, occasionally purple paleae (Figure 7K), some of

them very long, up to 8400 pm, others 1250-2750 pm,

base ± 100 pm or 4 cells wide, tapering to single apical

cell, 95 x 30 pm, lower cells 125 x 27 pm; disc + 3 mm

across, umbonate (Figure 7C), air pores compound, slight-

ly raised amd sometimes quite conspicuous, ( 1 — )3— 5(— 6)

capsules borne below, each encased in pseudoperianth

which descends obliquely downward, extending ± 1100

pm beyond the involucre and divided into 15 segments,

these 2125 pm long and 550 pm wide at widest part,

tapering toward coherent tip, cells (4-)5- or 6-sided, 90.0-

137.5 x 25.0-37.5 pm, lower down smaller, ± 50 x 25

pm. Spores ( 102-) 125-140 pm in diameter, triangular-

globular, yellow, translucent, wing undulate, up to 20 pm

wide, margin crenulate, distal face (Figure 8 A, B) convex,

centrally with (4— )6-9 complete areolae, ± 32.5 pm wide,

outer areolae incomplete, the ridges up to 12.5 pm high,

seldom extending across wing, smaller, subsidiary areolae,

2. 5-5.0 pm wide (and occasionally even further divided

up), generally covering floor of larger areolae and extend-

ing over crests of main ridges (Figure 8C); proximal face

with prominent triradiate mark (Figure 8D, E), its arms

15 pm high and continuous from the pole across wing to

margin, each of 3 facets with complete or mostly incom-

plete areolae, main ridges sometimes extending across

wing, small subsidiary areolae covering floor and ridges

of main areolae, as well as arms of triradiate mark. Elaters

± 145 pm long, 12.5 pm wide in centre, slightly tapering

to the ends, doubly spiral (Figure 8F), yellow. Chromo-

some number: n = not known.

DISCUSSION

Asterella marginata has frequently been confused with

A. bachmannii, in fact, Amell (1963) stated that he could

find no real differences between them, basing his opinion

on their scale appendages, air pores, epidermal cells and

spores. The result is that many specimens held at PRE

and BOL, have been wrongly identified. Sterile collec-

tions of A. marginata are indeed difficult to place. In fer-

tile specimens, however, the umbonate head of the

carpocephalum, which lacks prominent papillae and the

frequently very long, pale paleae, as well as the spore

ornamentation mostly with numerous fine, ± regular, sub-

sidiary areolae contained within the highly ridged, larger

ones, which usually do not extend across the wing, make

it quite easily recognizable. Its distribution, moreover, ap-

pears to be confined to the winter rainfall areas of the

Western and Eastern Cape, the latter being the only area

where A. marginata (Figure 3) and A. bachmannii (Figure

6) occur together. Previous reports of A. marginata from

elsewhere (Stephani 1899; Arne! I 1963; Vanden Berghen

1972; Best 1990) should be treated with reservation. As

noted under A. bachmannii , Vanden Berghen’s (1972: fig.

75A) illustration of A. marginata , with prominent papillae

on the carpocephalum head, suggest it to be the fonner

species, and not the latter.

Asterella marginata grows in dense mats on clayey soil

or on weathered, soil-covered rocks at seepages or river-

banks, between rock crevices and under ledges, sometimes

in association with Fossombronia spp., Bryum spp. and

Riccia spp.

4. Asterella wilmsii (Steph.) S.W Amell , Hepaticae

of South Africa: 62 (1963). Type: Spitzkopf bei Lyden-

burg, Transvaal, leg. Dr Wilms (ex Herb. Jack, (001666

G, lecto. fide in litt. Grolle!) selected here; ex Herb. Steph.

024590 G!).

Fimbraria wilmsii Steph.: 122 (1892); ibid.: 103 (1899); Sim: 23

(1926).

F. angolensis Steph: 100 (1899); Asterella angolensis S.W. Amell:

64 (1963). Type: Angola, Huilla, waterfall, Newton 25a (001673 G,

holo.!) fide Grolle (on specimen packet).

Bothalia 24,2(1994)

143

FIGURE 8. — SEM micrographs of A sterella marginata. A-E, spore: A, distal face; B, distal face seen slightly from the side;C, much enlarged areolae

with inner subsidiary areolae; D, proximal face; E, side view. F, elater. A, Amell 267\ B, C, E, S.M. Perold 2418; D, Arnell 505; F, S.M.

Perold 2092. A, x 340; B, x 424; C, x 990; D. x 304; E, x 408; F, x 493.

Thallus large, thin but compact, dorsally flat to slightly

concave, yellowish green, margins gently scalloped, dark

red (Figure 9A), pigmentation becoming diffuse inwardly,

outlines of subdorsal air chambers not visible from above,

air pores hardly raised, wet; thallus margins slightly raised

to inflexed or sometimes inrolled, dry; in crowded, over-

lying mats, mostly simple or once pseudo-dichotomously

furcate, sometimes with apical or latero-ventral innova-

tions. Branches broadly ligulate, widening rapidly from

narrow base, 30-40(-75) mm long, if furcate, terminal

branches up to 10 mm long, narrowly to moderately diver-

gent, 4.7—7. 1 mm wide; 600-800(-950) pm thick over

midrib, laterally thinning out into attenuate wings (Figure

9D), apex notched with appendages of hyaline to deep

purple ventral scales recurving over edge; margins acute,

thin, somewhat undulate; ventrally reddish purple, lateral-

ly striate across, flanks sloping obliquely, medianly

keeled, green, midrib with row of purple-red scales on

either side (Figure 9B).

Dorsal epidermis unistratose, cells containing chloro-

plasts, from above 5- or 6-sided, elongated, thin-walled,

50-95 x 25-35 pm, toward wings up to 1 07 x 30 pm, in

transverse section (30.0-)37.5-47.5 pm thick, occasional-

ly with round oil body, 25-35 pm, almost filling cell;

marginal cells somewhat thicker-walled, especially on the

outer side, in 1 or 2 rows (Figure 9E). elongated, 30.0-

50.0 x 12.5-15.0 pm, inner cells 25-50 x 25 pm; air

pores (Figure 9F) very slightly raised, simple, oval, small,

17.5 x 8.0 pm and 125-250 pm distant from each other,

surrounded by 3 concentric rings of (6— )7— 9 cells in each,

innermost ring ± 5 pm wide, with cells collapsed, in the

next ring cells rounded to transversely oval or bluntly tri-

angular, 12.5-17.5 x 22.5 pm, partly overlying outer ring

of bluntly triangular or polygonal cells, 15-27 x 35-40

pm; assimilation tissue ( 150— )250— 3 20 pm thick over

midrib, air chambers medianly in several vertical storeys,

toward margins sloping obliquely, small and irregularly

shaped, (25— )35— 50 pm wide, mostly empty and only

rarely with 1 or 2 cells jutting into a chamber immediately

below an air pore (Figure 9G), bounding cells oval to

round, 45.0-52.5 x 27.5-37.5 pm, occasionally containing

an oil body; storage tissue 450-650 pm thick over midrib,

thinning out gradually and absent at margins, cells angular

and closely packed, 25.0-37.5(^10.0) pm wide, becoming

somewhat smaller lower down, walls thick, porate and

sometimes with a network of striations; rhizoids in

clumps, mostly smooth, 22.5-25.0 pm wide, pegged ones

10.0-12.5 pm wide. Scales hyaline or pink to purple-red,

arranged in two forwardly directed ventral rows, one on

each side of midrib, not extending to margins of thallus,

except at apex, obliquely crescentic with large, ovate or

roughly triangular appendage (Figure 9H), (850—) 1050—

1200 x 420-500 pm, cells long-hexagonal, 92-150 x 55-

62 pm, at apex ending in single cell forming an apiculus,

65-100 x 15 pm, at base constricted where joined to rest

of scale, 1000-1100 x 950-1050 pm, where cells smaller

and elongated, 60-100 x 35-42 pm, scale continuing into

long tail, ± 1200 x 200 pm, cells 1 05— 1 37(— 220) x (12-)

22-25 pm, ± 9 cells per scale, only 42-55 x 42-47 pm,

containing an oil body in each.

Autoicous. Androecia in raised cushions, oval or elon-

gated or heart-shaped, 1.0-3. 5 x 1.0 mm, extending back-

wards from apex of main branch, frequently on apical or

latero-ventral innovation, antheridia immersed and open-

ing above via conspicuous papillae. Archegoniophores

proximal to apical notch of main branch, single, oc-

casionally paired at apices of two forking branches, ± ses-

sile when young and surrounded by up to 70 purple

paleae, not arching over disc. Carpocephala at maturity

raised on stalk, arising ± 2 mm back from apex of branch

144

Bothalia 24,2 (1994)

FIGURE 9. — Asterella wilmsii. A, dorsal lace of thallus with stalk and carpocephaluin; B, ventral face of thallus; C, carpocephalum from below; D,

transverse section of thallus; E, marginal cells; F, air pore, dorsal cells and oil cell from above; G, transverse section of air pore and air

chamber; H, ventral scale; I, transverse section of stalk; J, paleae from summit of stalk. A, I, J, S.M. Perold 2632', B, C, H. Anderson, I219cr,

D, E, Perold & Koekemoer2836\ F, G, H, Perold & Koekemoer 2830. Scale bars: A- D, 1 mm; E-G, 50 pm; H, I, 250 pm; J, 100 pm.

Bothalia 24,2(1994)

145

in apical notch, its length variable, (2 — )4 — 1 ()(— 20) mm

long, often purple, widening toward base, in transverse

section at ± midlength (Figure 91) 600 x 525 fim, with

rhizoidal furrow ± 75 x 100 pm, cortical cells in a single

layer, thick-walled, especially on outside, rounded, 15.0-

27.5 x 12.5 pm, medullary cells with thinner walls, but

thickened at corners, up to 37.5 x 30.0 pm, at summit of

stalk and also protruding from notches of disc, dark purple

paleae (Figure 9J), occasionally pink or colourless, length

variable, up to 2000 pm long, rarely as much as 3250 pm

long, but then narrower, and only 3 cell rows wide, mostly

up to 7 cell rows or ± 325 pm wide at base, cells (4— )5

or 6-sided, ± 155.0 x 62.5 pm. gradually tapering to con-

ical apical cell, 100 x 25 pm; disc rounded, 3. 5-5.0 mm

across when bearing full complement of 4 or 5 capsules

(Figure 9C), but sometimes only 1 or 2 capsules present

and then smaller and asymmetric, above almost smooth

or with low papillae further down, from which compound

air pores lead to air chambers below; capsules spherical,

wall with cells 4-6-sided, 57.5-85.0 x 42.5-65.0 pm, thin-

walled and lacking spiral thickenings, but toward dehis-

cence line cells much thickened at corners, turning brown,

27.5- 47.5 x 27.5-32.5 pm; pseudoperianth extending up

to 1500 pm beyond involucre, generally with 16 seg-

ments, white or purple-stained, 2250 x 500 pm, tapering

to narrow tip where coherent with other segments, cells

100.0-137.5 x 40 pm, toward tip 62.5-75.0 x 27.5-37.5

pm. Spores 115.0-152.5 pm in diameter, triangular-

globular, mostly yellow, translucent, wing thin, somewhat

scalloped, 20.0-22.5 pm wide, margin crenulate, distal

face (Figure 10A, B) convex, with network of 5-8, ±

smooth, angular, complete or incomplete areolae across

and extending over wing to margin on both sides, 25-30

x 20-25 pm, small subsidiary areolae sometimes present

(Figure 10C), and extending over crests of main ridges,

7.5- 10.0 pm high; proximal face with prominent triradiate

ridge (Figure 10D, E), its arms up to 25 pm high and

continuous from the pole across wing to margin, each of

3 facets with rounded areolae, up to 20 x 20 pm, some

with small, subsidiary areolae, others appearing smooth

and hollowed out. Elaters (Figure 10F) 225-230 pm long,

17.5 pm wide in centre, slightly tapering to ends, 12.5

pm wide, sometimes branched, doubly spiral, yellow.

Chromosome number, not known.

DISCUSSION

Asterella wilmsii is the largest of the southern African

species in this genus. It can also be distinguished from

the others by the single, ovate or roughly triangular, large-

celled appendage of the ventral scales, by the distinctly

lobed disc of the carpocephalum, with purple paleae

protruding from the notches and by the paleae being

generally slightly broader based (up to 7 cells wide). The

young, almost sessile archegoniophore is surrounded by

purple paleae, which do not arch over it, as in A. bach-

mannii. The disc is less papillose and the spores are not

as highly ornamented as those of A. bachmannii, often

lacking smaller subsidiary areolae in the large areolae,

which then appear to be almost smooth and hollow and

extend across the wing. A. wilmsii is not as widespread

in southern Africa as A. bachmannii and it is far less fre-

quently collected. It is known from the PWV, Northern

and Eastern Transvaal, Swaziland and KwaZulu/Natal

(Figure 3). Its range extends northward into Zimbabwe

( Coates Palgrave 2524; Eyles 414. 786, CH 1175; Henkel

2558; Miller CH 4249; Schelpe 4063, 5650; Volk 00640),

from where it has also been reported by Best (1990), and

into Angola (the type specimen of A. angolensis ) as well

as Malawi (Bizot et al. 1976). It may also grow in Zaire,

a tentative conclusion based on the ovate scale appendages

FIGURE 10. — SEM micrographs of Asterella wilmsii. A-E, spore: A, distal face: B, distal face seen from the side; C, much enlarged areolae on distal

face, with some inner subsidiary areolae which also extend over their crests; D. proximal face; E, side view. F, elater. A, Sim CH 1269; B,

D, Doidge 3187; C, Sim CH 1274\ E, F, Perold & Koekemoer2836. A, B, x 316; C, x 1033; D, x 277; E, F, x 340.

146

Bothalia 24,2 (1994)

illustrated by Vanden Berghen (1972) in his fig. 74H, I

and the distal spore face in fig. 74K, which suggest this

species, although the material was merely designated as

Asterella sp. by him. Asterella wilmsii was also reported

from Mozambique by Amell ( 1963). The main distribution

pattern along the mountains of the eastern part of the sub-

continent suggests that it is an Afromontane species with

isolated western outliers. It grows on damp soil along

streambanks and waterfalls, sometimes in forested areas,

forming dense mats, occasionally in association with A.

bachmannii and Symphyogyna spp.

Two specimens of A. wilmsii , Collins 775 from Rus-

tenburg Kloof, and Eyles CH 1175 from Goromanzi in

Zimbabwe, had been misidentified and reported by Arnell

(1963) as Reboulia haemispherica. The presence of the

genus Reboulia has not been confirmed in southern Africa

and the species should accordingly be deleted from the

checklist of southern African bryophytes (Magill &

Schelpe 1979), as well as from Plants of southern Africa:

names and distribution (Arnold & De Wet 1993).

SPECIMENS EXAMINED

Alheit 54610 (3) BOL. H. Anderson CH 1219 (2), 1219a (4), 1248

(1) , 1262. CH 4504. CH 4505 (2), CH 12758 (4), CH 13288. CH 13587

(2) PRE. Amell 46. 206. 216, 239. 267. 505, 5359 (3) BOL.

Bachmann, G 13866 (lectotype), G 13867 (2). G. Bayer CH 1235 (2)

PRE. Bews CH 1229 (4), CH 1259. CH 1272 (2) PRE. Bosmari CH 208 ,

LI 3185 (2) PRE. Bottomley CH 172 (2), CH 263 (3), CH 1217, CH

2863 (4) PRE. Bottomley & Doidge CH 3565 (2), C'H 3591 (4) PRE.

Braun 714 (2) PRE.

• Coates Palgrave 2524 (4) BOL. Collins 775 (4) PRE. Condy 13 (1),

14, 17 (2) PRE.

Deal & Kiltick 78b (2) PRE. Dieterlen 793a & b (1), 794, 1119.

1120, 1142 (2) PRE. Doidge CH 17 (2), CH 170 p.p., CH 3187 (4) PRE.

Du Plessis 54613 (2) BOL. Dyer 863 (3) PRE.

Edwards CH 1270 (4) PRE. Ellis CH 13472 (1) PRE. Eyles 414 (4)

CH 776 (2), 786 (4) 932, 933 (1), CH 1122 (2), CH 1175 (4) CH 1240,

CH 1276, CH 1421 (2) PRE.

Garabedian CH 1218 (3), CH 1537 (2) PRE. Garside 6131, 6509,

6511, 6585 (3) BOL. Gilliland 215 (2) PRE. Glen 1674, 1675 (4) 1776,

2150, 2155, 2260, 2422, 2423, 2424, 2425, 3003, 3004, 3125 (2) PRE.

Glen & Reid 1724 (1) PRE.

Hardy 930 (4) PRE. Hardy et al. 5377C (2) PRE. He an 3660 (1)

PRE. Hendry 9 (2) PRE. Henkel CH 762, 2558 (4) PRE. Hepburn CH

1262 (2) PRE.

Jacot Guillarmod CH 3673 (2) PRE. Junod 794 (2) PRE.

Koekemoer 106 (2), 284a, 295, 316, 318, 757, 869 (3), 974 (4) PRE.

Kresfelder CH 163 (4) PRE.

Leighton CH 1216 (2) PRE. Liebenberg CH 2851 (4) PRE.

Magill 6370 (2) PRE. Malan 54611 (3) BOL. Marais 832 ( 1) PRE.

Michell 8 (3) PRE. Miller CH 4249 (4), CH 4250 (2), 7869 (1) PRE.

Mogg CH 158, CH 197, CH 1191, CH 1192, 4227, 4624 (2), 12557,

37642 (4) PRE. Mohle 315 (4) PRE. Morley 287, 297, 309 (3) PRE.

Mott 861 { 1 ) PRE.

Newton 25a (4) G.

Obenneyer TM 1940c, CH 3110 (4) PRE. Oliver 1474 (3) BOL,

7762 (2), 8854, 8877 (3) PRE.

Pegler 1356, 2150 (2) PRE. S.M. Perold 98, 100, 258 (2), 494, 509,

521, 522, 531, 610, 635, 646 (3), 685 (4) 686, 863 (2), 1457, 1603, 1899,

1909, 1934, 1992, 1997, 2040a, 2387, 2418 (3), 2482, 2487, 2488, 2572

(2), 2632, 2633 (4) 2703 (2), 2787, 2789 (3), 2800 (1), 2979, 2986 ( I ),

2986a, 3000 (2), 3001 (1) PRE. Perold & Koekemoer 2825 (2), 2830a,

2836 (4) 2848, 2855, 2856 (2), 2874 (4) 2877, 2898 (2), 2911 (4) 2913

(2), 2914 (4) 2916, 2917, 2919 (2), 2921 (4) 2934, 2946, 2947, 2951.

2960, 2968 ( 1 ), 2970, 2971 (2), 3030 (3) PRE. Phelan 375 (2) PRE.

Pieterse 16 (3) PRE. Pillans 3991 (3) BOL, PRE.

Reid 969, 1012 (1) PRE.

Schelpe 2043, 4009 (2), 4063 (4) 4735, 4918a (3), 5255 (1) BOL,

5359 (2) PRE, 5650 (4) 6028 (2) BOL, 7729, 7792, 8045 (3) BOL. Scott

24 (2) PRE. Sim. T.R., CH 1160, CH 1198 (2), CH 1205 (4) CH 1206,

CH 1208, CH 1210, CH 1213, CH 1215 (2), CH 1224 (4) CH 1226,

CH 1239, CH 1244, CH 1245, CH 1246, CH 1247, CH 1248, CH 1250

(2), CH 1251 (4) CH 1252, CH 1254, CH 1455 (2), CH 1260 (3), CH

1263, CH 1265, CH 1268 (2), CH 1269, CH 1273, CH 1274 (4) CH

1297, 8147 (2) PRE. Smook 6422, 8237 (1) PRE. Stirton 8967 (4) 8992

(2), 91 16 (3) PRE. Stoneman CH 1219 (2) PRE. Symons 8247 (2) PRE.

Thomas CH 947, CH 948 (2), CH 2869 (3) PRE.

University Durban-Westville 46, 49, 50 (2) PRE.

Van der Bijl 3, CH 1202, CH 1207, CH 1227 (2) PRE. Van der

Merwe CH 232 (4) PRE. Van der Schijff 5131, 5860 (4) PRE. Van Rooy

781 (2), 1088 (1), 1289, 1348 (2), 1389, 1630 (4) 1696, 1822, 1830 (1),

2461 (2), 2716, 2930 (1), 3134, 3139 (2), 3144, 3580, 3609 (1) PRE.

Van Vuuren 1476 (4) PRE. CM. Van Wvk 2561 (3) PRE. Veltman &

Potgieter 15 (4) 134 (2) PRE. Venter 8611 (2) PRE. VI ok 2675 (3) PRE.

Volk 00640 (4) Herb. Volk 84/651 (1) M, PRE.

Wagener CH 13241 (2) PRE. Wager Bequest CH 250, CH 251 (2),

CH 3691 (3), CH 3806 (4) PRE. West CH 3667 (2) PRE. Wilms G 1664

(1), G 001666 (lectotype), 02458 (1), G 024590 (4) G.

( Eyles 932, 933 and Miller 7869 are from Zimbabwe)

ACKNOWLEDGEMENTS

My gratitude to Dr R. Grolle and Mr D.G. Long for

refereeing this article and for their helpful suggestions. I

also wish to thank the curators of BOL and G for the loan

of specimens. Dr T. Bornefeld for the chromosome counts

of Asterella muscicola and A. bachmannii, the artist, Ms

A. Pienaar, the typists, Mesdames J. Mulvenna and J.

Veldman, and the photographer, Mrs A. Romanowski. My

colleagues at NBI are warmly thanked for collecting

specimens.

REFERENCES

ARNELL, S.W. 1957. Hepaticae collected in South West Africa by Prof.

Dr O.H. Volk. Mitteilungen der Botanischen Stoats sammlung,

Miinchen : 16: 262-272.

ARNELL, S.W. 1963. Hepaticae of South Africa. Swedish Natural

Science Council, Stockholm.

ARNOLD, T.H. & DE WET, C. (eds) 1993. Plants of southern Africa:

names and distribution. Memoirs of the Botanical Survey of South

Africa No. 62.

BEST, E.B. 1 990. The Bryophyta of Zimbabwe — an annotated checklist.

Kirkia 13: 293-318.

BISCHOFF, G.W. 1844. In M.A. Seubert, Flora Azorica.

BIZOT, M„ DURY, M.N. & POCS, T. 1976. East African biyophytes, II.

Acta Botanica Academiae Scientiarum Hungaricae 22: 1-8.

CORDA, A.K.J. 1829. Genera hepaticarum. Die Gattungen der Leber-

moose. Beitrdge zur Naturgeschichte 12: 643-655.

EVANS, A.W. 1920. The North American species of Asterella. Contribu-

tions from the U.S. National Herbarium 20: 247-312.

FRYE, T.C. & CLARK, L. 1937. Hepaticae of North America. University

of Washington Publications in Biology 6: 1-162.

GOTTSCHE, C.M., LINDENBERG, J.B.G. & NEES AB ESENBECK,

C.G. 1844—1847. Synopsis hepaticarum. Hamburg, Meissner.

GRIFFITH, W. 1849. On the higher cryptogamous plants. Notulae ad

Plantas Asiaticas, Part 2: 285-352. Calcutta.

GROLLE, R. 1976. Verzeichnis der Lebermoose Europas und benach-

barter Gebiete. Feddes Repertorium 87: 171-279.

HASSEL DE MENENDEZ, G.G. 1962. Estudo de las Anthocerotales y

Marchantiales de la Argentina. Opera Lilloana 7: 1-297.

LONG, D.G. & GROLLE, R. 1992a. Studies on the genus Asterella P.

Beauv. (Hepaticae). 1. Nomenclatural history. Taxon 41: 65-69.

LONG, D.G. & GROLLE, R. 1992b. Proposal to conserve Asterella

(Hepaticae: Aytoniaceae) with aconserved type. Taxon 41: 1 14.

MAGILL, R.E. & SCHELPE, E.A. 1979. The bryophytes of southern

Africa. Memoirs of the Botanical Survey of South Africa No. 43.

MULLER, K. 1951-1958. Die Lebermoose Europas. Dr L. Rabenhorst's

Kryptogamen- Flora 6:41 6-47 1 .

NEES AB ESENBECK, C.G. 1820. Horae physicae Berolinenses collec-

tae ex symbolis virorum.

Bothalia 24,2 ( 1 994)

147

NEES AB ESENBECK, C.G. 1 838. Naturgeschichte der europdischen

Lebermoose 4: 259.

PALISOT DE BEAUVOIS, A.M.F.J. 1805. Asterelle (Bot.), Asterella.

Dictionnaire des sciences naturelles 3. Paris.

SCHIFFNER, V.F. 1893. Hepaticae. Die natiirlichen Pflanzenfamilien 1:

3-38. Leipzig.

SCHUSTER, R.M. 1992. The Hepaticae and Anthocerotae of North

America Vol. 6: 1—937. Field Museum of Natural History.

SIM, T.R. 1926. The Bryophyta of South Africa. Transactions of the

Royal Society of South Africa 15: 1—475.

SIM. T.R. 1931 . South African Bryophyta. Further notes. Transactions of

the Royal Society of South Africa 20: 15, 16.

STEPHANI F. 1876-1907. leones hepaticarum. P. Geissler (ed.). IDC

Microform Publishers, Zug, Switzerland.

STEPHANI, F. 1892. Hepaticae africanae. Hedwigia 31 : 122.

STEPHANI, F. 1894. Hepaticarum species novae V. Hedwigia 33: 7.

STEPHANI, F. 1899. Species hepaticarum. Fimbriaria. Bulletin de T

Herbier Boissierl: 84—110.

VANDEN BERGHEN, C. 1972. Hepatiques et Anthocerotees. Resultats

scientifiques de T exploration hydrobiologique du Basin Lac

Bangweolo & Luapula 8: 1-202.

VOLK, O.H. 1979. Beitrage zur Kenntnis der Lebermoose (Marchan-

tiales) aus Siidwestafrika (Namibia) 1. Mitteilungen der Botani-

schen Staatssammlung, Miinchen 15: 223-242.

Bothalia 24,2: 149-152(1994)

Studies in the Marchantiales (Hepaticae) from southern Africa. 7. The genus

Cryptomitrium (Aytoniaceae) and C. oreades sp. nov.

S.M. PEROLD*

Keywords: Aytoniaceae, Cryptomitrium, C. oreades, Hepaticae, Lesotho, Marchantiales, Reboulia , Reboulioideae, taxonomy

ABSTRACT

As far as is known, the rare genus Cryptomitrium is reported here for the first time for the whole continent of Africa with the

description of a new species, C. oreades, from the mountain Kingdom of Lesotho in southern Africa. The specimen, attributed

to the genus Reboulia from southern Africa, was misidentified.

UITTREKSEL

Die seldsame genus Cryptomitrium word hier, sover bekend, die eerste maal vir die hele vasteland van Afrika vermeld met

die huidige beskrywing van 'n nuwe spesie, C. oreades, vanaf die bergagtige Koninkryk van Lesotho in suidelike Afrika. Die

eksemplaar wat aan die genus Reboulia vanuit suidelike Afrika toegeskryf is, is verkeerd geidentifiseer.

Cryptomitrium Austin ex Underw. in Bulletin Illinois

State Laboratory of Natural History 2: 36 (1884); Schiffn.:

33 (1893); Steph. 221 (1899); M. Howe: 43 (1899); A.

Evans: 45 (1923); Hassel: 120 (1963). Type species: C.

tenerum (Hook.) Austin.

Platycoaspis Lind, in Lind. & Amell: 11 (1889).

Thalloid, smallish to medium-sized, margins purple,

thin, medianly thicker and rather flat to slightly concave,

green, in loose patches; at seepage, on soil overlying rocky

outcrops. Branches simple or rarely once pseudo-

dichotomously furcate; thickened over midrib, thinning

toward scalloped or irregularly crenate margins, laterally

striate from above; apex slightly notched, dorsally not

grooved along midline. Dorsal epidermis hyaline, cell

walls thickened, especially at the comers, but not bulging,

some cells containing an oil body; air pores simple, small,

slightly raised, surrounded by 3 concentric rings of cells

without radial thickening of the walls and leading below

into topmost layer of individual empty air chambers, in 2

or 3(4) storeys, bounding walls unistratose, chlorophyl-

lose; storage tissue with angular cells, not restricted to

keel; rhizoids of both kinds, smooth as well as pegged.

Scales dark red or reddish pink, in 2 forwardly directed

ventral rows, not imbricate, roughly triangular to transver-

sely rectangular, with 1 or 2(3) filiform appendages.

Autoicous. Antheridia in groups, sunken into dorsal tissue

along midline and opening into projecting, conical papil-

lae above. Catpocephalum single, raised on stalk with one

rhizoidal furrow, lacking air chambers and arising dorsally

at apical notch of thallus or ventrally along margin, head

disciform-round, with 1 or 2 layers of air chambers,

separated from one another by unistratose cell plates and

opening above via compound air pores; 3-6 capsules

borne below, protruding between membranous lips of in-

* National Botanical Institute, Private Bag X101, Pretoria 0001 .

MS. received: 1993-03-26.

volucres; capsular wall apically bistratose, inner cells with

thickening bands, remainder of wall unistratose, cells thin-

walled. Spores triangular-globular, winged, distal face

with ± reticulate ornamentation, or thick sinuate ridges;

proximal face with high, thin, conspicuous triradiate mark,

each facet with incomplete areolae. Elaters long, tapering,

bispiral.

Cryptomitrium oreades Perold , sp. nov.

Thallus statura mediocri, late linearis vel ovatus, dorso

viridi, marginibus tenuibus, striatis, crenatis; ventraliter

atropurpureus, utrimque costae serie squamarum prorsum

versarum, deltoidearum, purpurearum vel rubescentium,

appendicibus filiformibus. Cavemulae vacuae. Autoicus.

Androecium grex antheridiorum immersorum, cervicibus

exsertis. Carpocephalum disciforme, stipitatum, ventraliter

sub latere thalli exoriens, lateraliter emergens, prope an-

theridia, cum sulco unico rhizoidali. Sporae (77.5 )— 85 .0—

95.0 pm diametro, deltoideo-globulares, alatae, superficie

distali plerumque cristis crassis sinuatis, superficie

proximali nota triradiata gracili, alta; superficiebus

minoribus cristis incompletis. Chromosomatum numerus

ignotus.

TYPE. — Lesotho: 1 km from New Oxbow Lodge on

road to Mokhotlong, ± */2 km from bridge to the left,

along Tiholohatsi River, at interface between basalt rock

slope and grassy fringe, under large boulder in wet

seepage area on soil, in alpine heath-grassland, alt. ±

2 900 m, April 1994, Perold & Duckett 3228 (PRE, holo.).

Thallus medium-sized, broadly linear (Ligure 1A) to

oblong, sometimes apically rather wider; dorsally flat to

slightly concave along centre, green, toward margins

striate across with deep purple of ventral face showing

through thin dorsal tissue, walls of air chambers beneath

faintly visible, when wet; margins irregularly crenate to

wavy, flanks ventrally deep purple, incurved and arched

over or clasped together above dorsal epidermis, when

150

Bothulia 24.2 (1994)

FIGURE 1 . — Cryptomitrium oreades. Morphology and anatomy of thallus. A, dorsal face of thallus with carpocephalum on stalk emerging at side

of thallus; B, ventral face of thallus; C, carpocephalum seen from below; D, ventral scale; E, transverse section of stalk; F, transverse section

of thallus; G, air pore and surrounding cells seen from above; H, transverse section of air pore and dorsal cells; I, thin, unistratose portion of

wall; .1, bistratose apical portion of capsule wall with thickenings, from above; K, transverse section of bistratose portion of capsule wall.

A-C, E, F, l-K, Van Rooy 305 /; D, G, H, Perold & Duckett 3228. Scale bars: A-C, F, 1 mm; D, 500 pm; E, 250 pm; G-K, 50 pm.

Bothalia 24,2 (1994)

151

dry; in loose patches, simple or once pseudodichotomous-

ly furcate. Branches mostly up to 12 x 3-5(-6) mm,

(450-)600-800 pm thick over midrib, laterally thinning

out into wings, apex slightly notched, purple filiform tips

of scale appendages reflexed over edge; margins thin,

acute; flanks sloping very obliquely upward and outward;

ventral face medianly rounded, on either side of midrib

with a row of apically directed, ± triangular to transversely

rectangular, purple or reddish scales (Figure IB).

Dorsal epidermis unistratose, cells hyaline, from above

oval or rounded or irregularly shaped, with trigones

prominent, but not bulging, walls slightly thickened, 25.0-

42.5 x 20.0-32.5 pm, in transverse section rectangular,

up to 35 pm high, vertical walls thick, with some cells

containing an oil body; marginal cells variable in shape,

27.5-30.0 x 32.5-50.0 pm; air pores simple, raised ± 25

pm above dorsal cells (Figure 1H), oval or round, up to

32.5 x 27.5 pm, surrounded by 3 concentric rings of cells,

walls not radially thickened (Figure 1G). innermost ring

consisting of 6-8 cells, thin-walled and wedge-shaped, ±

8.0 x 15.0 pm, collapsed and often fragmentary, next row

of cells transversely oblong, 15.0-17.5 x 27.5-35.0 pm.

partly overlying outer row of 6-8 cells, 17.5-25.0 x 27.5-

42.5 pm, these in turn partly overlying dorsal cells; as-

similation tissue 280^150 pm thick, medianly with 3

layers of vertical, empty air chambers (Figure IF), sloping

toward margins, 125-240 pm wide, Vi or more the thick-

ness of thallus, bounded by unistratose, chlorophyllose

walls, cells 20.0-37. 5(— 55.0) x 25.0-37.5 pm, occasional-

ly with an oil body; storage tissue 125-350 pm thick,

cells closely packed and angular, 35.0-62.5 pm wide, here

and there a few cells with an oil body, ± 30 pm wide,

almost filling cell; rhizoids arising from swollen, ventral

epidermal cells, mostly smooth and up to 25 pm wide,

others pegged, 10.0-22.5 pm wide. Scales dark red or

reddish pink, in 2 ventral rows on either side of midrib

(Figure IB), not imbricate, 300-410 x 600-750 pm,

roughly triangular (Figure ID) to transversely rectangular,

with 1 or 2(3) filiform appendages, 150-590 pm long, of

which basal cells in 2 rows, but soon just in a single

string, rectangular, ± 70 x 27 pm; cells along scale mar-

gins brick-shaped or polygonal, ± 27.5 x 62.5 pm, some-

times with slime papillae, 25.0 x 12.5 pm. projecting here

and there, cells in body of scale 5- or 6-sided, 50.0-75.0

x 22.5-37.5 pm, walls sometimes sinuous; 6-9 small clear

cells (the oil bodies no longer present), ± 17.5 x 22.5 pm,

scattered in between cells of scale.

Autoicous. Androecia in diffusely arranged groups of

antheridia (Figure 1 A) sunken into dorsal tissue, their con-

ical necks 200 pm wide at base and projecting ± 150 pm

above surface, each with an opening leading into an-

theridial cavity below. Carpocephalum raised on stalk,

mostly single, rarely two adjacent, disciform-round, not

lobed (Figure 1A), green, turning brown with age, 2. 5-4.2

mm in diameter, rather flattish on top. with one layer of

elongated air chambers, opening via compound air pores

encircled by 4 concentric rings of cells (2 above and 2

below surface), scattered oil cells present; 3-6 capsules

borne below (Figure 1C), each on short seta and initially

protruding only slightly through elongated radial clefts

which eventually widen, the lips becoming membranous

and functioning as an involucre; capsules globose, 1100

x 850 pm, basal %-3/4 um-shaped with delicate, hyaline.

unistratose wall, of which apical V4-V3 part bistratose

(Figure IK), forming an operculum that is shed at an an-

nulus by dehiscence, outer layer ± 37.5 pm thick, con-

tinuous with rest of thin-walled cells (Figure 1 1), 4- or

5-angled, ± 52.5-100.0 x 27.5M-0.0 pm, inner layer of

cells restricted to apical part, thicker- walled (Figure 1 J ),

smaller, 20.0-32.5 x 25.0-35.0 pm, with narrow,

brownish, rod-like thickenings (Figure 1 K); stalk of car-

pocephalum erect, arising ventrally from below flank of

thallus and emerging laterally, close to site of antheridial

group (Figure 1A), basally red and partly covered with

purple scales, otherwise yellowish, apically surrounded by

a few hyaline, filiform scales, with 1 rhizoidal furrow

(Figure IE), length 3-5 mm, diameter 400-490 pm, in

transverse section with cortical cells 12.5-17.5 x 12.5-

22.5 pm, outer wall rounded and slightly thickened,

medullary cells angular, closely packed ( 1 2.5— )25.0— 30.0

x 17.5-25.0 um. Spores light brown, semitransparent, tri-

angular-globular, (77. 5-)85. 0-95.0 pm in diameter, wing

7.5 pm wide, undulating and somewhat plicate (Figure

2D), margin irregular; distal face (Figure 2A-C) convex

with ornamentation hardly reticulate or with thick, sinuate

ridges up to 5 pm high, irregularly branched and wavy,

separated by deep fissures; proximal face (Figure 2D) with

conspicuous triradiate mark, thin, tortuous, ± 7.5 pm high,

extending onto wing, each facet with irregular, branching

ridges, forming incomplete areolae. Elaters light brown,

bispiral (Figure 2E, F), 210-275 pm long and 10 pm wide

at widest part, tapering to tips, 5 pm wide. Chromosome

number not known.

DISCUSSION

This species is characterized by a disciform-round car-

pocephalum. borne on an erect, uni-furrowed stalk which

arises ventrally at the margin and emerges laterally to the

thallus in close proximity to the dorsally situated an-

theridial group. Worldwide only two other species have

been described in this genus; firstly C. tenentm from

North America (Alameda, California, Washington and

Mexico) as well as from Costa Rica, Guatemala, Chile

and Argentina, and secondly C. himalayense (Kashyap

1915) from India (Mehra & Sokhi 1977). Cryptomitrium

oreades differs from the other two species mainly by the

lateral position of its stalk; in C. tenerum and C. hima-

layense the stalk is dorsally situated near the apex of the

thallus; their thalli are also thinner and more delicate than

those of our species. The genus Cryptomitrium is clas-

sified in the family Aytoniaceae and in the subfamily

Reboulioideae Grolle, together with Asterella, Mannia and

Reboulia. The genus Reboulia does not occur in southern

Africa (Perold 1994); Amelfs (1963) only record of it

from Rustenburg Kloof, Collins 775C, is a specimen of

Asterella wilmsii and was clearly misidentified. So far, C.

oreades is known from only two localities in Lesotho

(Figure 3), growing at high altitude in association with

the moss Gymnostomum aeruginosum J.E. Sm.

The specific epithet, oreades, is derived from the Greek

word 'oread', meaning 'mountain nymph' and was chosen

because of the mountainous location of this species.

152

Bothalia 24,2 (1994)

FIGURE 2. — Cryptomitrium oreades. A-D, spores: A, distal lace; B. distal face seen from side; C, proximal face; D, side view. E, elater; F, part of

elater. A,‘ B, E, F, Van Rooy 3051 ; C, D, Perold & Duckett 3228. A, B, x 470 ; C, x 77; D, x 493; E, x 324; F, x 1990.

SPECIMEN EXAMINED

(excluding the type specimen, already mentioned)

LESOTHO. — 2828 (Bethlehem): 6 km from New Oxbow Lodge to

Mokhotlong, basalt outcrops, alpine heath-grassland, on soil, (-DC), Van

Rooy 3051 (PRE).

ACKNOWLEDGEMENTS

I wish to sincerely thank Prof. J.G. Duckett, Queen

Mary and Westfield College, London, for finding the

specimen which has been selected as the holotype, when

we were together in the field; also Dr and Mrs D.J.B.

Killick for accompanying me. My thanks also to my col-

league at NBI, Mr J. van Rooy, for collecting the first

specimen of Cryptomitrium oreades ; and to Dr R. Grolle

for discussions about the affinities of this taxon, after it

FIGURE 3. — Distribution of Cryptomitrium oreades in southern Africa.

was forwarded to him by kind intercession of Prof. O.H.

Volk, Wurzburg, to whom I had sent it first. The specific

epithet was suggested to me by Dr H.F. Glen, who also

wrote the Latin translation. I extend my gratitude to him

for both these favours, also to Miss M. Koekemoer,

curator at PRE, for accompanying me to Lesotho in 1993

when we failed to find more material of C. oreades, to

the artists, Ms G. Condy and Ms J. Kimpton; to the typist,

Mrs J. Mulvenna, and to the photographer, Mrs A. Roma-

nowski, for their valued contributions.

REFERENCES

ARNELL, S.W. 1963. Hepaticae of South Africa. Swedish Natural

Science Council, Stockholm.

EVANS, A.W. 1923. In North American Flora. Sptwerocarpales — Mar-

chantiales 14: 1-66.

HASSEL DE MENENDEZ, G.G. 1963. Estudio de las Anthocerotales y

Marchantiales de la Argentina. Opera Lilloana 7: 1-297.

HOWE, M.A. 1899. The Hepaticae and Anthocerotes of California.

Memoirs of the Torres Botanical Club 7: 1-208.

KASHYAP, S.R. 1915. Morphological and biological notes on new and

little known west Himalayan liverworts. III. The New Phytologist

14: 1-18.

LINDBERG, S.O. & ARNELL, H.W. 1889. Musci Asiae Borealis. 1.

Lebermoose. Kongelige Svenska vetenskapsakademiens handlin-

gar 23: 1-69.

MEHRA. P.N. & SOKHI, J. 1977. Embryology of Cryptomitrium

himalayense Kash. Journal of the Hattori Botanical Laboratory

43: 157-190.

PEROLD, S.M. 1994. Studies in the Marchantiales (Hepaticae) from

southern Africa. 6. The genus Asterella and its four local species.

Bothalia 24: 133-147.

SCHIFFNER, V. 1893. Hepaticae. Die Natiirlichen Pflanzenfamilien 1:

3-141.

STEPHANI, F. 1899. Species hepaticarum. Bulletin de THerbier Boissier

7:221,222.

UNDERWOOD, L.M. 1884. Descriptive catalogue of the North

American Hepaticae, north of Mexico. Bulletin Illinois State

Laboratory of Natural History 2: 1-133.

Bothalia 24,2: 153-162 (1994)

A new serotinous species of Cliff ortia (Rosaceae) from the southwestern Cape

with notes on Cliff ortia arborea

E.G.H. OLIVER and A.C. FELLINGHAM

Keywords: Cliffortia, new species, serotiny, taxonomy

ABSTRACT

A remarkable new species, Cliffortia conifera E.G.H. Oliv. & Fellingham, from the Anysberg, Ladismith District, is

described and compared to its closest ally in the genus, Cliffortia arborea Marloth, which is widespread along the escarpment

of the Great Karoo from Calvinia in the north to Beaufort West in the southeast. It is unique in the genus for its serotinous

cone-like synflorescences which are borne on determinate lateral branchlets occurring in zones on the main branches. A similar

serotinous condition exists in C. arborea, but the inflorescence axis is the main branch. The serotinous inflorescences are

complex synflorescences consisting of numerous, highly condensed, double racemes (homoeothetic dibotrya). To date

serotinous inflorescences have not been recorded in Cliffortia. C. arborea and C. conifera are included in section Arboreae, the

description of which is emended here.

UITTREKSEL

’n Merkwaardige nuwe spesie, Cliffortia conifera E.G.H. Oliv. & Fellingham, van die Anysberg, distrik Ladismith, word

beskryf en vergelyk met sy naaste verwant in die genus, Cliffortia arborea Marloth, wat wydverspreid voorkom op die Groot

Karoo-platorand vanaf Calvinia in die noorde tot by Beaufort-Wes in the suidooste. Dit is uniek in die genus vanwee die

serotiniese, keelagtige bloeiwyses (synflorescences) wat gedra word op laterale takkies met beperkte groei, wat in sones op die

hooftakke voorkom. 'n Sooitgelyke serotiniese toestand bestaan by C. arborea maar die as van die bloeiwyse is die hooftak. Die

serotiniese bloeiwyses is komplekse ‘synflorescences’ wat uit vele, hoogs gekondenseerde dubbele raseme (homoeotetiese

dibotrya) bestaan. Serotiniese bloeiwyses is nog nie voorheen by Cliffortia aangeteken nie. C. arborea en C. conifera word

geplaas in seksie Arboreae die beskrywing waarvan hier hersien word.

INTRODUCTION

The genus Cliffotlia is a prominent element in the fyn-

bos vegetation of the Cape Floral Region. With a total of

110 species it is one of the largest genera, and the over-

whelming majority of its species is endemic. It is surpris-

ing that Cliffortia, for its size, is the only representative

of the Rosaceae in the fynbos.

The genus has been well researched by Weimarck in

a number of publications since his expedition to southern

Africa in 1930, the major one being his revision of the

genus (Weimarck 1934). Since Weimarck's work there has

been much collecting of fynbos elements, particularly on

the mountains by Elsie Esterhuysen of the Bolus Her-

barium. This has resulted in a large accumulation of

material in the Cape herbaria which has needed thorough

curation by the second author at the Stellenbosch Her-

barium (STE). It is showing that the collecting and record-

ing of male, female and fruiting material for every species

needs special attention for a complete understanding of

the species and their relationships. It has also resulted in

the detection of numerous species complexes and in the

uncovering of a number of new species.

Some unusual material with 'galled' branchlets (Van

Wyk 1072 ) was collected on a general collecting expedi-

* Stellenbosch Herbarium, National Botanical Institute, RO. Box 471,

Stellenbosch 7599.

MS. received: 1992-08-31.

tion of staff from the Stellenbosch Herbarium to the Anys-

berg near Ladismith in October 1982. The 'galled' branch

could not be identified at the time, so it was given to

Pauline Fairall (Bond) of the Compton Herbarium (NBG)

for an opinion. She suggested the genus Cliffortia and

noted that the ‘galls’ actually contained withered flowers.

The collection was placed in the Incertae in both herbaria.

Resulting from the current curation of Cliffortia, the first

author made a search in 1991 for fresh material of this

taxon and located a small population in the vicinity of

Van Wyk’s original locality.

An examination of this fresh material clearly showed

that we were dealing with a very distinct new species of

Cliffortia and a remarkable situation in which the female

flowers are borne in serotinous cone-like heads. This con-

dition had never before been recorded in the genus and

was very reminiscent of that occurring in the genus

Leucadendron R. Br. (Proteaceae) and Widdringtonia

Endl. (Cupressaceae). In old plants of Cliffortia the cone-

like heads are clearly retained on the plant for up to six

years after flowering (Figure 1 ).

In this paper we have followed the terminology used

by Weberling (1981, 1983) to describe the structure of the

inflorescences. The basic unit of flowers is a highly con-

densed raceme (botryum) of the third order, a second order

co-florescence. These racemes are aggregated into highly

condensed double racemes (dibotrya) which in turn are

clustered into a compact syntlorescence in the form of

either a cone-like head or a subterminal zone.

154

Bothalia 24,2 ( 1994)

FIGURE 1. — Photograph of female

synflorescences in Cliffortia

conifera (left) showing three

zones (years) of cones on

short, secondary flowering

branchlets, Oliver 10055 and

in C. arborea (right) showing

five years of conoid synflores-

cences on proliferating main

branch, three on upper half of

branch and two on lower half.

Oliver 10054.

TAXONOMY

Cliffortia conifera E.G.H. Oliv. & Fellingham, sp.

nov. in genere singularis et distinctissima propter flores

suas femineas in synflorescentibus strobilinis lignosis in

extremis ramulorum lateralium breviorum noninnovan-

tium praesentes, ad sectionem Arboreae pertinens sed a

specie unica C. arborea Marloth, strobilorum positione

structuraqne solum in ramulis secundariis determinatis,

strobilorum foliis involucratis lignosis semipermanen-

tibus, foliis latioribus interdum dentatis, indumento den-

siore brevioreque incano-floccoso differt.

Frutex erectus lignosus ad 4 m altus cortice griseo

desquamato. Rami incano-floccosi glabrescentes. Folia 3-

foliolata, vagina lata omnino vaginanti, incano-floccosa;

stipulae subulatae 0. 5-2.0 mm longae, base puberulae

glabrescentes; foliola ( 10—) 1 2— 1 7(— 1 8) x (2)3-6(-9) mm,

anguste elliptica vel anguste ovata ad ovata, integra inter-

dum [2]3[4]-lobata, marginibus abaxialiter parvum

revolutis, incano-floccosa, adaxialiter glabrescentia,

apicibus acutis subulatis subula 0.25-1.50 mm longa. /n-

florescentia mascula: racemosa condensata lloribus 3 vel

4(5) in extremis brachyblastorum in ramulis inferioribus.

Flores masculi brevissime pedicellati; bractea ad 1 .5 mm

longa, anguste triangularis ciliata; sepala 2. 8-3. 2 x 1 .8-3.0

mm, late elliptica vel subcircularia ad late obovata, apice

subacuto crasso, exteme lanata ad villosa; stamina 6-9;

filamenta 3. 5-5.0 mm longa, filiformia glabra; antherae

1.0 x 1.2 mm. Inflorescentia feminea: multa di bo try a in

syn-florescentias strobilinas obovoideas, interdum sphae-

roideas in extremo ramuli brevis lateralis, strobili juvenes

12 x 12-30 x 22 mm albo-flavovirentes, veteres plerum-

que 25 x 25 mm, griseovirides, omnes incani; folia

primaria strobili l(3)-foliolata, vagina latissima, stipulis

brevissimis lateralibus subulatis vel sine stipulis, ciliata,

dense lanata abaxialiter, glabra adaxialiter, foliolis 0.5-2.0

mm longis; folia secundaria strobili unifoliolata circum

florescentias (botrya) involucrata, 5-10 x 3-5 mm, initio

oblique obovoidea mollia demum elongato-ovoidea lig-

nosissima, subula apicali intro aspicienti, dense et breve

lanata, basaliter glabra ciliata; axis florescentiae truncatus

longe villosus floribus 5-18 in florescentiis capitulatis in

extremis planis axium tertiorum aggregatae his in dibot-

ryis 4-6 in extremis axium secundariorum aggregatis.

Flores feminei pro maxime parte occulti; bractea ad 1.5

mm longa vel absens, elongato-triangularis ciliata;

pedicellum 0. 1-0.2 mm longum; sepala 3 vel 4, 1. 7-2.0

x 0.3 mm, linearia subacuta ad obtusa, apicaliter externe

lanata aliter glabra, erecta ad parum patentia; recep-

taculum 0.9- 1.2 mm longum, obovoideum, 3^f cristis vel

alis angustis, glabrum; stigma 1 linearis planoconvexa

4.5-5 .0 x 0.2-0.25 mm, torta, in dimidio superiore ir-

regulariter dentata, alba marginibus rubris. Fructus 1.8-

3.5 x 0.8- 1.0 mm, irregulariter ellipsoideus ad ovoideus,

brunneus glaber, 3 vel 4 alis vel cristis angustis lon-

gitudinalibus pallide flavis. Figurae 2 & 3.

TYPE. — 3220 (Montagu): Ladismith Dist., Anysberg,

E end above Prinskloof, 1 300 m, (-BC), 4-06-1992,

Oliver 10055 (STE, liolotype; BOL, K, PRE, isotypes; all

male & female).

Bothalia 24,2 (1994)

155

Woody erect shrubs up to 4 m tall with main trunk up with crisped branched hairs submedially attached, the

to 150 mm in diameter with dark grey, flaking bark, plants hairs falling off with age. Leaves 3-foliolate with broad

regenerating from a lignotuber. Branches incano-floccose totally sheathing incano-floccose vagina remaining on

FIGURE 2. — Ctiffortiaconifera. A, branch with female cones in flower, x 1 ; B, male branchlet with flowers, x 1 ; C, leaf with lobed leaflets, adaxial

view, x 3; D, leaf with entire leaflets, adaxial view, x 3; E, leaflet, adaxial view, x 3; F, male flowers, x 3; G, trifoliolate primary cone leaf,

adaxial view, x 6; H, unifoliolate primary cone leaf, adaxial view, x 6; I, outer secondary cone leaf, lateral & adaxial views, x 6; J. innermost

secondary cone leaf, partially lateral adaxial view, x 6; K, bracts of female flowers, x 12; L, female flower, x 12; M, fruit, x 12. All drawn

from the type, Oliver 10055 (STE).

156

Bothalia 24,2 (1994)

branches after leaflets have been shed and giving seg-

mented appearance to branches; stipules subulate from 0.5

mm long in young leaves to 2.0 mm in old leaves, remain-

ing on vagina for some time after leaflets have been shed,

hairy in lower part becoming totally glabrous, cream to

reddish; leaflets ( 10— ) 12— 1 7(— 1 8) x (2)3— 6(— 9) mm, nar-

rowly elliptic or narrowly ovate to ovate, mostly entire,

occasionally [2]3|4]-lobed, with margins slightly revolute

abaxially, completely incano-floccose when young soon

becoming glabrous mostly on apical half of upper surface

and margins and remaining incano-floccose on lower sur-

face, all apices acute and subulate, subula 0.25-1.50 mm

long, colourless or reddish. Inflorescence (male): a con-

densed raceme of 3 or 4(5) flowers on a villous highly

reduced brachyblast in axil of a subapical leaf of lower

lateral branches situated well below apex of main

branches. Flowers (male) very shortly pedicellate, creamy

white; bract up to 1.5 mm long, narrowly triangular, long

ciliate, whitish soon turning brown; sepals 2.8-3.2 x 1.8-

3.0 mm, broadly elliptic or subcircular to broadly obovate

with apex subacute thickened, mostly reflexed, villous to

lanate outside; stamens 6-9; filaments 3. 5-5.0 mm long.

FIGURE 3. — Clijforlia conifera. Photograph of female branch of

holotype prior to pressing, showing cones in flowering stage

(Oliver 10055), x 0.5.

filiform glabrous; anthers 1.0 x 1.2 mm. Inflorescence

(female): many condensed double racemes (homoeothetic

dibotrya) aggregated into an obovoid, occasionally sphae-

roid, cone-like synflorescence at end of a short lateral

branchlet, these cones ( 1— )4 — 1 0 in a subterminal zone on

main branches, rarely on secondary branches, young cones

12 x 12-30 x 22 mm whitish yellow-green and old mature

cones mostly 25 x 25 mm dull grey-green, all incanous,

older fruiting cones retained for up to 6 years, vegetative

region between zones 50-80 mm long, occasionally up to

300 mm; leaves of primary cone axis (primary cone

leaves) (3-)l-foliolate, with very broad vagina, with or

without short lateral subulate stipules, ciliate, densely and

shortly lanate abaxially, glabrous adaxially, leaflets 0.5-

2.0 mm long, reduced otherwise foliaceous, inner with an

expanded sheathing base; dibotrya of 4-6 co-florescences

of second order with axis 0.5-2. 0 mm long; leaves of

secondary cone axis (secondary cone leaves) unifoliolate,

arranged involucre-like around florescences (botrya), 5-10

x 3-5 mm, at first obliquely obovoid and soft, becoming

elongate-obovoid and very woody, reducing in size

towards axis, with inwardly pointing apical subula, ovoid,

attenuated into a long stout terminal subula, apically

greenish densely and shortly lanate, basally white glabrous

and ciliate; co-florescence (botryum) highly condensed

with 5-18 flowers in a capitulum-like arrangement, axis

very short, truncate, long villous. Flowers ( female ) mostly

hidden; bract up to 1.5 mm long or absent, very thin,

elongate triangular, long ciliate, brownish; pedicel 0. 1-0.2

mm long; sepals 3 or 4, 1 .7-2.0 x 0.3 mm, linear subacute

to obtuse, lanate outside apically otherwise glabrous, erect

to slightly spreading, colourless; receptacle 0.9-1. 2 mm,

obovoid, with 3-4 longitudinal narrow ridges or wings

ending in small apical bulges, glabrous; style 1, linear,

planoconvex, 4.5-5.0 x 0.2-0.25 mm, curled and twisted,

exserted from cone, white, edged in upper half with short

irregular red stigmatic teeth. Fruit 1. 8-3.5 x 0.8-1. 0 mm,

irregularly ellipsoid to ovoid, dark brown and glabrous

with 3 or 4 yellowish longitudinal narrow ridges or wings,

apically emarginate, retained within cone for several years

after flowering period. Figures 2 & 3.

The closest ally to C. conifera is C. arborea. C. con-

ifera possesses female flowers borne in condensed cone-

like structures, in a different position to those of C.

arborea. Herbarium material of C. arborea was rather in-

adequate for a thorough investigation and is also extreme-

ly difficult to handle due to its toughness and spikiness.

A trip was therefore made to collect fresh material of both

species in June 1992 in order to analyse and compare the

structures in detail.

Weimarck created the section Arboreae to provide a

place for the unusual tree-like species, C. arborea, which

had been described by Marloth in 1905. He noted that the

species possesses several unique morphological charac-

ters. He described the flowers as ‘closely clustered in

groups of 5-8 in the axils of simple leaves on very con-

tracted twigs’. These he noted were bunched together in

such a way as to give the impression of a ‘spadix’. This

clearly points to the elongated compact cone-like structure

that is present on those herbarium sheets which are fertile,

but does not fully reflect the situation in nature. All fertile

female herbarium material seen by us possesses a single

subterminal ‘spadix’ or ‘cone’ on a single branch. In the

Bothalia 24,2(1994)

157

wild, branches may possess only a single subterminal

cone, but others can have a series of cones spread along

their main axis (Figures 1 & 4A). Needless to say the former

are far easier to collect and press. The single cone situation

shown by Marloth and present on all the herbarium material

collected before our investigation, occurs only when an ac-

tively growing branch flowers for the first time. The spread

of cones along a stem clearly showed that the current, flower-

ing cone was subapically situated with the other cones lower

down in a series at close intervals with each successive cone

representing a previous year’s inflorescence. Weimarck was

therefore unaware of the retention of the inflorescences for

a number of years following their initial formation during

the flowering period. We therefore prefer to use the term

‘cone’ for C. arborea , particularly when C. conifera is taken

into account.

A detailed examination of the cones of both species

showed that they are very similar in their structure and

differ mainly in their position on the main branches. In

C. arborea the primary axis of the cone is the main rela-

tive branch which elongates beyond the cone and also

laterally via sterile, lateral, secondary branchlets within

the cone, whereas in C. conifera the primary axis of the

cone is a secondary lateral branch which is determinate

in growth and devoid of any lateral vegetative branching.

The development of lateral branches from the cones in

C. arborea is clearly shown in the photograph published

with the protologue by Marloth (1905) and in the upper-

most cone in Figure 1. His photograph shows numerous

very short, lateral, leafy branchlets which conceal the true

nature of the female compound inflorescence underneath.

The cones are complicated structures which require

careful dissection for analysis. A simplified diagram of

the cones from both species is summarized in Figure 4.

In this we have followed the terminology of Weberling

(1983). The order of branching refers only to the branch-

ing of the inflorescence and not to the rest of the plant.

The cones are polytelic synflorescences composed of

numerous, condensed, sessile, racemes (botrya), up to 50

per cone, the co-florescences (Figure 4C & D) which are

grouped together in highly condensed double racemes

(dibotrya) (Figure 4B & B'). The co-florescences resemble

capitula with up to 16 flowers all arising at the same level

from the truncated end of the very short, 3rd order, flores-

cence axis. The flattened end of this axis is covered by

long erect hairs from which the bracteoles just emerge.

The subtending secondary cone leaves on the 2nd order

axes are very different from the normal vegetative leaves

and are considerably thickened and eventually become

woody (Figures 21 & J; 5D). These enlarged, woody, in-

volucral leaves form the basic matrix of the cone and

almost completely cover the female flowers with only the

stigmas protruding in most cases. There is another type

of leaf in the cone and these we refer to as the primary

cone leaves (Figures 2G & H; 5C). They are situated on

the main or primary axis of the cone (1st order inflores-

cence branch) and subtend the lateral 2nd order dibotrya.

In C. conifera these primary cone leaves are unifoliolate,

occasionally trifoliolate, but they are always trifoliolate in

C. arborea. In the latter species some of the leaflets of

these primary cone leaves may be shed, but the scars in-

dicate that the original condition was trifoliolate.

Further differences in the cones occur between the

secondary cone leaves. In C. conifera they are mostly

obovoid in shape with a stiff, apical, adaxially pointing

subula. They are at first softish, but become woody and

remain intact in the cone for the life of the cone (± 6

years). In C. arborea they are widest at the middle with

the upper portion narrowing, foliaceous and reflexed and

with an apical, more or less erect subula. They are softish,

not becoming very woody and after several seasons

abscise at the top of the sheath. Thus in C. arborea the

old cones retain only the flattened bases of the secondary

cone leaves and are considerably narrower than the

flowering and fruiting cones.

Female cones are therefore found only in these two

species in the genus. The possibility of other species

having a similar character, but not recorded, was not dis-

counted. Clearly one is drawn to the species C. strobilifera

L. on account of its name. This is a common widespread

species which bears small ovoid ‘cones’ at various points

on the plant. These are just vegetative galls having no

connection with the position of flowers which are borne

singly over the normal branches. Another species that at-

tracts attention is C. heterophylla Weim. which has two

distinctly different types of leaves on the plant and these

are associated with the flowers. The majority of leaves

are linear-lanceolate whereas considerably broader ovate

leaves occur in long terminal zones. The female flowers

occur in the axils of these broader leaves. The whole ap-

pearance of the branches is rather cone-like but not com-

parable with those found in the section Arboreae.

Weimarck (1934: 170) drew attention to the existence

of a true inflorescence in only three species in the genus,

C. arborea, C. odorata L. f. and C. hirsuta Eckl. & Zeyh.

In the latter two species the flowers, 5-15, occur in con-

tracted racemes which he noted ‘approach the form of

heads’. He also noted that male and female flowers are

frequently found in the same inflorescence. However, in

a later review of the genus (Weimarck 1948) he placed

the two species in a division of his key which described

the flowers as ‘at least the male, fascicled in the leaf axils’.

He included two new species in this group, C. discolor

Weim. and C. viridis Weim., but made no mention of their

inflorescences in either the descriptions or the discussions.

The cone -bearing zones on the plants of C. conifera

vary considerably depending on how vigorously the

branches are growing. Most have 5-8 cones in the zones,

but there can be as few as one or as many as 1 1 (Figure

1). The vegetative region between the zones is usually

50-80 mm long with vegetative lateral branchlets

developed there, but it can be as short as 30 mm or as

long as 300 mm in vigorously growing branches. These

observations were made on the few, mature, cone-bearing

adult plants in the type population.

Apart from the differences in the cones, the leaves in

C. conifera are visibly very different from those in C.

arborea which are much wider and erect-spreading. The

appearance of the plants is remarkably similar to some

species in the genus Phylica L. in the Rhamnaceae. In C.

arborea the leaves are linear, needle-like and very

revolute, in fact very ericoid, and also falcate. The

recurved nature of these leaves is very marked on the

158

Bothalia 24,2 (1994)

FIGURE 4. — Longitudinal diagrams of architecture and structure of synflorescence. A, B, Cliffortia arborea: A, three conoid synflorescences on

main branch and two minor synflorescences on lateral branches; B, part of synflorescence showing three dibotrya. A', B', C. conifera: A',

two zones of four and five conoid synflorescences on lateral truncate branches; B', part of synflorescence showing four dibotrya. C, D, single

co-florescence or botryum (solid square) with its seven individual flowers (open circles). MA, main or primary axis; FB, flowering secondary

branches; VB, vegetative secondary branches; SN, synflorescence; DB, dibotryum; CoF', co-florescence or botryum; pci, primary cone leaf;

scl, secondary cone leaf; br, bract of single flower; zoned lines in synflorescences in A & A' represent dibotrya; dotted zigzag lines in B, B',

C & D represent expanded highly condensed axes; solid squares represent botrya, and circles, single flowers.

Bothalia 24.2 ( 1 994)

159

FIGURE 5. — Cliffortia arborea. A. leaf, adaxial view, x 3; B, leaf with foliaceous stipules from region just below synflorescence, abaxial view, x

6; C, primary cone leaf with third leaflet shed, adaxial view, x 6: D, secondary cone leaf, lateral/adaxial view, x 6; E, fruit, x 12. All drawn

from Oliver 10054 (STE).

main branches just below the young cones where even

the stipules become foliaceous and recurved (Figure 5B).

The leaves in C. conifera are, however, problematic in

that there is a clear difference between those of the col-

lections from the type population and those of Van Wyk

1072. The leaflets on the latter collection are mostly linear,

1 .0—1 .6[2.0J mm wide, and revolute with no broad open-

backed examples. Even a long period of softening by boil-

ing in water with softener added, does not render them

any broader. In the collections from the type population

the leaflets are mostly much broader, (2)3— 6(9) mm wide,

with only the occasional leaflet being more linear. The

width of the leaflets in the dried collections tends to be

slightly narrower than in the fresh state. This distinct dif-

ference is puzzling seeing that we have been unable to

relocate the site at which Van Wyk made her collection.

Until such time as this has been rediscovered and the

plants studied in the field, we are unable to assess this

clear disjunction and have therefore excluded it from the

type description.

Marloth described the hairs on C. arborea as Mal-

phigian hairs, i.e. hairs which are attached by their middle;

two-branched hairs according to Weimarck (1934). Both

species have these hairs on the branches and leaves. The

hairs are very flat in the middle portion where they are

very flimsily attached to the surface and are easily

removed when touched. The two ends are curled and

somewhat erect. In C. conifera the hairs are very closely

packed whereas in C. arborea they are longer and sparser.

The bracts of the female flowers in Cliffortia are usual-

ly well developed and amplexicaul, enveloping the base

of the flower (Weimarck 1934). In C. conifera and C.

arborea the bracts are much reduced to nonexistent and

are flat, only slightly curved in the largest examples. They

are placed on the flattened end of the axis of the co-flores-

cences (botrya) between the closely packed flowers in a

manner similar to that in the Asteraceae. Being surrounded

by long transparent hairs and being themselves covered

with long hairs, they are very difficult to locate and ex-

amine especially when they are reduced to mere vestiges.

Marloth ( 1905) described the female flowers of C. ar-

borea as having a solitary style with one white, non-

plumose stigma. Weimarck (1934) described the stigma

as linear and a little branched which is unique for the

genus in which most of the species have showy, plumose,

red stigmas. He regarded the basal nonplumose portion

as the style which in most species is very short. C. coni-

fera and C. arborea have identical style/stigma configura-

tions. The style/stigma is an elongate-linear, planoconvex,

white organ with very short irregular teeth on the edges

in the upper three-quarters to half and an acute, red apex

(Figure 2L). The actual position of the stigmatic surfaces

in these two species is not clear to us and so we refer to

the structure as a style/stigma. In the other species of

Cliffortia the lateral hairs are very well developed and

Weimarck refers to the region in which these occur as the

stigma. This problem will need careful examination of

fresh material of both species to ascertain the position of

trapped germinating pollen grains.

The type population of C. conifera consists of about

50 plants, most of which had been burnt off by a fire

some five years previously. There were only eight mature

plants which survived the fire and which were flowering.

The plants which had been burnt were all regenerating

from a basal lignotuber, but even though the strongest

growing one was already 1.5 m tall, none had produced

any cones. The oldest plant was growing protected among

large boulders and was about 4 m tall, or rather, long,

seeing that it was growing out diagonally from between

the boulders.

Cliffortia arborea Marloth in Botanische Jahr-

biicher 39: 318 (1905); Weim.: 91 (1934). Type: Africa

australis, in rupibus montium regionis Roggeveld dictae,

alt. 1 500 m. Oct., Marloth 3907 (Bt. holo.; BOL female!.

160

Bothalia 24,2 ( 1994)

K! male, P male [sec. Weimarck], STE! sterile). Lectotype

here designated, Marloth 3907 (BOL female).

Stipules 0-2, subulate or below synflorescences subu-

late to foliaceous. Inflorescence (male): a condensed

raceme of 2^4 flowers on a brachyblast in the axil of a

normal vegetative leaf. Male flowers: sepals 3, 4 x 3 mm

in the largest specimen seen, abaxially lanate, apex sub-

ulate; stamens 8-10. Inflorescence (female): an ellipsoid

cone-like synflorescence of condensed double racemes

(dibotrya) consisting of sessile capitulum-like co-flores-

cences (botrya), the synflorescence borne on the main

branch with continued apical growth, with 2nd order axes

continuing growth laterally and sometimes forming a

secondary cone or male florescences in subsequent

seasons; primary cone leaves trifoliate, stipules absent to

well developed and foliaceous; secondary cone leaves

unifoliolate, 12 mm long reducing in size towards axis of

dibotryum, basally sheathing, medially ovoid, shortly

lanate, distally cylindric, glabrescent, apex subulate,

abscising at top of basal sheath in third or fourth year.

Several points which are at variance with Weimarck’s

description and do not concern the conoid inflorescences

which have been dealt with in detail under C. conifera,

need some discussion. Most of the material examined was

devoid of stout subuloid stipules. In most cases there is

very little indication of any stipules, but when they are

present they can be prominent. However, below the cones

they are usually well developed and even foliaceous. The

male flowers are not borne singly in the axils of vegetative

leaves but in groups of 2-4 on highly reduced short shoots

and have more anthers, 8-10 per llower, than were

recorded by Weimarck. The female flowers can have 3 or

4 sepals not just 3.

Both Marloth and Weimarck noted that C. arborea had,

in addition to the branched hairs of the indumentum,

pedunculate glands which produced a strongly aromatic

oil. We have not been able to observe any of these glan-

dular hairs on the material at our disposal and the fresh

material from the Komsberg and the Nuweveld Mountains

was not aromatic. We believe that Marloth must have con-

fused the aromatic nature of some of the plants which he

collected on his Roggeveld trip and this was repeated by

Weimarck who never handled any fresh material.

The production of short, sterile, 2nd order branches

within the current flowering synflorescence is peculiar to

this species. During the flowering period these lateral

branchlets characteristically appear just beyond the boun-

daries of the cone. In the following season these branch-

lets elongate considerably, as shown in Figure 4A, and

clearly visible in Figure I (right). In herbarium material

these branches appear to be all sterile. However, fresh

material from our own collections showed some very in-

teresting features. The collection from Komsberg ( Oliver

10054) possessed some laterals with small female

synflorescences shown in the diagram in Figure 4A. These

appeared to have flowered at the same time as the

synflorescence above them on the main axis, the second

one from the apex. One of the collections from the

Nuweveld Mountains (Fellingham 1625) possessed in-

stead, numerous male florescences on these lateral

branches.

Marloth did not state where his type collection was

housed. Weimarck (1934) gave the location of several

specimens of Marloth 3907 with male and female material

in B and BOL and only male material in K and P. The

only female specimen appears to be the one in BOL, be-

cause the material in B was destroyed during the Second

World War. There is no male material of Marloth 3907

in BOL as cited by Weimarck. We have therefore selected

the female collection of Marloth 3907 in BOL as the lec-

totype.

Marloth also gave no exact locality for the type col-

lection. However, in the discussion on the species he noted

that it occurred only on the southern end of the Roggeveld

on the Komsberg. The lectotype in BOL has appended to

it the original print of the habit/habitat photograph which

was published with the protologue. On the reverse it is

labelled in Marloth's own handwriting as taken on the

Komsberg at 1 550 m and the specimen is labelled as

‘southwestern krantzes on the Komsberg, 1 550 m’. It is

therefore clear that the Komsberg is the type locality for

the species.

In his discussion of the species Marloth noted that the

appearance of the short branchlets, i.e. those protruding

from the young female inflorescence, caused the local

people to give the plant the common name of ‘Starboom

(= Sternbaum)’ or rather sterboom. This has been cor-

rupted subsequently to ‘sterkboom’ as indicated by the

naming of several localities at the southeastern end of the

Roggeveld escarpment as Sterkboomkloof, Sterkboom-

plaat on the Trigonometrical Survey maps (1:250 000 &

1:50 000). However, the correct name is still included as

the original farm name ‘Sterboom Hoek 8’ on the map

322 1CA in the 1:50 000 series.

Since the discovery of the species, the distribution

range has been considerably extended by further collec-

tions from as far north as the Hantams Mountain near

Calvinia to the Nuweveld Mountains above Beaufort West

in the east. Marloth quoted information from the local

farmers in 1905 that the species used to be very common

along the edge of the escarpment, but with there being

no other woody plants in the whole area the species was

being used in considerable quantities for firewood. It is

now reduced to a few small populations in the southern

Roggeveld. In the Hantams area it was fairly common on

dolerite screes and krantzes in 1 955 according to Acocks

18621 with the populations above Akkerendam now in a

nature reserve controlled by the Calvinia Municipality.

Shearing ( Shearing 893) records the species as fairly com-

mon locally at Mountain View on the Nuweveld Moun-

tains which the second author confirmed during a visit to

the area. Fortunately the very good populations on the

Nuweveld Mountains occur in an area that now falls

within the recently established Karoo National Park where

the species is assured of the best possible protection.

Section Arboreae

The addition of the new species to the section Arboreae

and the changes to the description of C. arborea neces-

sitate the emending of the sectional description. The diag-

Bothalia 24,2(1994)

161

nostic feature of the section is now the serotinous, triple

botryoid, conoid synflorescence.

Section Arboreae H. Weim. emend. E.G.H. Oliv. &

Fellingham

Shrubs or small trees. Leaves trifoliolate; stipules 0-2,

subulate to foliaceous; leaflets revolute or flat, entire to

dentately 2-4-lobed. Inflorescence (male): a condensed

raceme of 2-5 flowers on a lateral highly condensed short

shoot in axil of vegetative leaf. Male flowers: sepals 3 or

4; stamens 6-10. Inflorescence (female): a conoid

synflorescence subterminally on main branches with con-

tinued apical growth (C. arborea) or apically on deter-

minate lateral short shoots (C. conifera ), the synflorescences

composed of condensed double racemes (dibotrya) each

consisting of condensed co-florescences (botrya). Female

flowers: sepals 3 or 4; receptacle triangular narrowed to

base, narrowly 3-winged or 3-ridged; style/stigma single,

linear, edges irregularly and shortly dentate; achene single.

Species included: Cliffortia arborea Marloth (type

species), C. conifera E.G.H. Oliv. & Fellingham.

PHYTOGEOGRAPHY

C. conifera is known only from the eastern end of the

Anysberg in the western part of the Ladismith District

where it grows at 1 300 m on steep, east-facing, summit

slopes on sandstones of the Nardouw subgroup of the

Table Mountain Group in the Cape Supergroup (SACS

1980). The associated vegetation is Mesic Mountain Fyn-

bos (Moll et al. 1984). The area falls within the Anysberg

Nature Reserve of the Cape Department of Nature & En-

vironmental Conservation. The weather station nearby on

the mountain has recorded an annual rainfall in the region

of 450 mm per annum which occurs throughout the year

with peaks in mid-winter, late spring and early autumn.

The nearest locality of its closest ally, C. arborea , is

90 km due north on the Roggeveld escarpment at the

Komsberg. This species is considerably more widespread

from the Hantams Mountains at Calvinia in the north

along the edge of the Roggeveld escarpment and

eastwards to the Nuweveld Mountains above Beaufort

West (Figure 6). In all cases it grows near the edges of

escarpments or in kloofs below the escarpments which

are at high altitude ranging from 1 500-1 800 m and sub-

jected to harsh climatic extremes of heat and drought in

summer and intense cold with several annual falls of snow

in winter. From the rainfall maps and the rainfall figures

available for nearby towns, it seems likely that the species

receives in the vicinity of 300 mm of rain per annum,

mostly in the winter months but occasionally in summer.

In the Roggeveld the escarpment is composed of sand-

stones and mudstones of the Adelaide subgroup of the

Beaufort Group in the Karoo Sequence with the Hantams

and Nuweveld Mountains being dolerite intrusions (SACS

1980). The record at the northern end of the Hantams

Mountain (Oliver 8878) was in a sheltered kloof at a lower

altitude of only 1 300 m. In all its localities it grows

amongst Karroid Shrubland (Moll et al. 1984) with no

representatives of Fynbos in the area.

Other species occurring like C. arborea on the interior

mountains of the southern Cape Province are C. han-

tamensis Diels, only from the Hantams Mountain and the

Roggeveld at Uitkyk, both C. arborea localities, and C.

ramosissima Schltr. from the Hantams Mountain, to the

high mountains near Graaff-Reinet and as far north as the

northern Drakensberg. Marloth (1905) pointed to the iso-

lated taxonomic, as well as geographic, position of C. ar-

borea and suggested that it is a relic of a former wider

distribution of the genus during pluvial periods. With the

discovery of the closely related C. conifera occurring in

the nearby Cape Floral Region with numerous other

species of Cliffortia , the linkup with the rest of the genus

is substantiated.

PHENOLOGY

C. conifera and C. arborea are monoecious with uni-

sexual male and female flowers borne on separate

branches. The female flowers are borne in terminal or

subterminal cones near the ends of the main branches.

The male flowers are borne in small groups in the axils

of vegetative leaves on lateral normal branches. In C.

conifera these male lateral branches are situated below

the female cones mostly lower down on the plant. In C.

arborea it is clear from the herbarium material that they

are also borne on lower lateral normal branches in this

species. Both male and female inflorescences were at-

tached to the same main branch with the male flowers

just below a single subterminal female cone (Acocks

18621; Marloth 9730) or on lateral branches emanating

from the lower older cones (Fellingham 1625) (see below

under C. arborea). These two species are clearly wind-

pollinated which is the syndrome presumed for all other

species of Cliffortia (Koutnik 1987). The position of the

flowers would indicate that updraughts of air would be

responsible for transferring the pollen to the female

flowers. This would fit in well with the habit and habitats

observed in the field where winds would come up from

below the plants on the edges of the escarpment or at the

foot of summit cliffs or in steepish kloofs.

FIGURE 6. — Known distribution of Cliffortia conifera , •; and C. ar-

borea, O.

162

Bothalia 24,2 (1994)

The female flowers, except for the long, exserted,

strap-shaped style and stigma, are totally hidden from

view within the envelope of secondary cone leaves. After

pollination they remain in the cones protected by these

leaves which become quite woody in C. conifera. The

entire cone in this species may remain on the plant for as

long as six years after initial formation. At what stage the

fruits are shed is difficult to ascertain, but we believe that

this occurs during the second or third year following

flowering. In C. cirboreci the secondary cone leaves

abscise after about 3-4 years, apparently after the fruits

are shed. The flat-ended woody bases of the secondary

cone leaves remain on the main branch for several years

after that, indicating where the original ‘flowering’ cone

had been situated. It is clear that some additional monitor-

ing of the plants in the field is necessary to ascertain the

complete phenological cycle in both species.

The flowering in these species occurs at different times

of the year. In C. conifera the female and male flowers

are most prolific during the late summer and autumn

months from April to June with some of the female

flowers opening as late as August. In C. arborea we have

been able to examine freshly opened flowers ( Fellingham

1624, 1625), and deduce that the plants flower in late

spring and early summer from October to December. The

flowering of the latter species is therefore surprisingly

soon after the advent of warmer weather, seeing that it

occurs in the coldest regions of the southwestern Cape.

SPECIMENS EXAMINED

C. conifera

WESTERN CAPE. — 3320 (Montagu): Ladismith, Anysberg, E end

above Prinskloof, 1 300 m, (-BC), 23-09-1990, Oliver 9730 (PRE, S,

STE, all female); ibid. 10-08-1991, Fellingham 1531 (STE female); ibid.

4-06-1992, Oliver 10055 (BOL, K, MO, PRE, STE, all male & female);

Anysberg, E end, gully leading to Prinsberg, (-DA), 6-10-1982, M. van

Wyk 1072 (NBG, STE, both female).

C. arborea

NORTHERN CAPE. — 3119 (Calvinia): Akkerendam, dolerite screes

& krantzes of Hantamsberg, 1 372 m, (-BD), 14-1 1-1955, Acocks 18621

(BOL male & female, K male & female, NBG male); summit of Hantam

Peak, 1 660 m, (-BC), Wisura 3556 (NBG sterile); Hantamsberg, Voet-

padskloof, S-facing slope, renosterveld, 1 465 m, (-BD), 3-09-1986,

Oliver 8878 (STE sterile); upper E slope of Hantam Mtn, Vanrhynshoek

Farm, kloof near stream, (-BD), 7-10-1986, Thomas & Van Jaarsvehl

8961 (NBG sterile). 3220 (Sutherland): Roggeveld, Farm Uitkyk,

Sneeuwkrans, below krantz facing W, 1 730 m, (-AD), 10-1920, Marloth

9730 (PRE stem & bark only, STE male & female); Hottentotsbank near

Sneeukrans, W-facing scree slopes, 1 433 m, (-AD), 22-09-1981, Rourke

1728 (K sterile, NBG sterile); Roggeveld, southwestern krantzes on the

Komsberg, 1 550 m, (-DB), 04-1905, Marloth 3907 (BOL female, K

male, STE sterile); Roggeveld Mtns, Komsberg, 1 525 m, (-DB), 10-

1920, Marloth 9770 (PRE female, STE female); just W of road at top

of Komsberg Pass, sandstone escarpment, (-DB), 22-09-1977, Moffett

1463 (STE sterile); plateau at top of Komsberg Pass, E of road, 1 600

m, (-DB), 1-03-1986, Moffett & Steensma 4067 (STE male); Komsberg

Pass, lower slopes ENE of Skurwekop, 1 500 m, (-DB), 4-06-1992,

Oliver 10054 (BOL, K, MO, PRE, S, STE, all female). Without precise

locality: mountains near Sutherland, 12-1905, Du'Toit sub BOL 10057

(BM, BOL, K, all sterile); Sutherland, shady side of very inaccessible

kloofs, 13-10-1969, De Villiers s.n. (NBG immature female). 3221 (Mer-

weville): Sterkboomkloof near Vinkfontein, edge of kloof, 1 500 m, (—

CA), 28-02-1986, Moffett & Steensma 4060 (STE sterile).

WESTERN CAPE. — 3222 (Beaufort West): Nuweveldberge,

Karoo National Park, Mountain View area near FM tower, SW slope,

1 830 m, (-BA), 17-11-1992, Fellingham 1624 (MO, PRE, STE, all

female); Karoo National Park, Mountain View, top of mountain, 1 830

m (-BA), 3-01-1985, Shearing 893 (PRE female); Nuweveld Mtns, S

slopes above Beaufort West, 1 525 m (-BC), 07-1940, Esterhuysen 2759a

(BOL sterile); Nuweveldberge, Karoo National Park, Mountain View area

near the Look Out, 1 830 m, (-BC), 17-11-1992, Fellingham 1625 (BM,

PRE, STE, all male & female).

ACKNOWLEDGEMENTS

We appreciate the valuable comments received from

Prof. Focko Weberling, one of the referees, and the dis-

cussions with Prof. Dietrich Miiller-Dobhes. We acknow-

ledge the co-operation of Alan Martin, officer-in-charge

of the Anysberg Nature Reserve, in our botanical work in

the Anysberg area.

REFERENCES

KOUTNIK, D. 1987. Wind pollination in the Cape flora. In A.G. Rebelo,

A preliminary synthesis of pollination biology in the Cape flora.

South African National Scientific Programmes Report No. 141:

126-133.

MARLOTH, R.H. 1905. Eine neue interessante Cliffortia vom Rog-

geveld. Botanische Jahrbiicher 39: 318, 319.

MOLL, E.J., CAMPBELL, B.M., COWLING, R.M., BOSSI, L„ JAR-

MAN, M.L. & BOUCHER, C. 1984. A description of major

vegetation categories in and adjacent to the Fynbos biome. South

African National Scientific Programmes Report No. 83. CSIR,

Pretoria.

SOUTH AFRICAN COMMITTEE FOR STRATIGRAPHY (SACS)

1980. Stratigraphy of South Africa. Part I . Handbook of Geologi-

cal Survey of South Africa 8.

WEBERLING, F. 1981. Morphologie der Bliiten und der Bliitenstande.

Eugen Ulmer, Stuttgart.

WEBERLING, F. 1983. Fundamental features of modern inflorescence

morphology. Bothalia 14: 917-922.

WEIMARCK, A.H. 1934. Monograph of the genus Cliffortia. Lund:

Gleerupska.

WEIMARCK, A.H. 1948. The genus Cliffortia, a taxonomical survey.

Botaniska Notiser 1948: 167-203.

Bothalia 24,2: 163-166(1994)

FSA contributions 1: Aquifoliaceae

S. ANDREWS*

Trees or shrubs. Leaves alternate, rarely opposite,

simple, mostly evergreen; stipules minute. Inflorescences

in axillary cymes. Flowers unisexual, regular, small,

sepals and petals usually fused at base, rarely free. Sepals

4— 6(— 8 ), imbricate. Petals 3-5 (-8), imbricate, white.

Stamens 4— 5(— 8 ), usually adnate to petals; anthers 2-

thecous. Ovary superior (2)4-6(-22)-locular; style ter-

minal; stigma capitate or discoid. Fruit a globose or ovoid

berry, containing 2— 10(— 20) pyrenes. Seeds with copious

endosperm.

Found throughout the tropical, subtropical or temperate

regions of the world. Ilex and Nemopanthus are recog-

nised in the family, which is often placed in the

Celastrales. Other genera such as Phelline, Sphenostemon

and Oncotheca are now placed in separate families by

several authors.

4614 ILEX

Ilex L., Species plantarum 1: 125 (1753); L.: 60

(1754); Sond.: 473 (1860); Benth. & Hook, f.: 356 ( 1867);

Harv.: 51 (1868); Oliv.: 359 (1868); Marloth: 150 (1925);

Loes.: 53 (1942); H. Perrier: 1 (1946); Keay: 623 (1958);

A. Robyns: 110 (1960); Mendes: 353 (1966); Verde.: 1

(1968); Mendes: 1 (1973); R.A. Dyer: 331 (1975); Trou-

pin; 321 (1983); Verde.: 329 ( 1989). Type species: I. aqui-

folium L.

Description as for family but petals fused at the base

with adnate stamens.

A genus of about 400 species of which only one is

indigenous to southern Africa.

The name Ilex is derived from its resemblance to the

leaves of Quercus ilex , the evergreen oak.

Ilex mitis (L.) Radik, in Reports of the British As-

sociation for the Advancement of Science 1885: 1081

(1886); Loes.: 246 (1895); Loes.: 240 (1901); Baker f.:

43 (1911); Loes.: 463 (1912); Engl.: 218 (1921); Exell:

74 (1927); Burtt Davy: 445 (1932); Lebrun: 134 (1935);

Loes.: 65 (1942); H. Perrier: 2 (1946); Robyns 1: 493

(1948); Brenan: 58 (1949); Adamson: 569 (1950); Exell

& Mendonga 1: 348 (1951); Brenan: 235 (1953); Keay:

623 (1958); F. White: 215 (1962); Von Breitenbach: 611

(1965); Mendes: 353 (1966); Verde.: 1 (1968); Palmer &

Pitman: 1269 (1972); Mendes: 1, 2 (1973); Compton: 333

(1976); Palgrave: 492 (1977); Troupin: 322 (1983);

Verde.: 329 (1989). Type: South Africa, specimen 261.2

Herb. Linnaeus [LINN, lecto.!; fide Verde.: 243 (1967)].

* The Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9

3AB, England.

MS. received: August 1990.

var. mitis

Sideroxylon mite L. Systema naturae, edn 12,2: 178 (1767); Jacq.:

249 (1789); Willd.: 1089 (1798); Sims: t. 1858 (1816). Scleroxylum mite

(L.) Willd.: 249 (1809). Myrsine mitis (L.) Spreng.: 663 (1824); Pappe:

22 (1854).

Prinos lucidus Aiton: 478 (1789); Aiton: 313 (1811); Willd.: 226

(1799); Pers.: 388 (1805); DC.: 17 (1825); Roem. & Schult.: 61 (1829).

Type: not traced in BM.

Chrysophyllum millerianum Lam.: 45 (1797); Poir.: 447 (1810); Poir.:

17 (1812). Manglilla milleriana (Lam.) Pers.: 237 (1805); Roem. &

Schult.: 504 (1819). Type: South Africa, Cape of Good Hope, Mill. Fig.

pi. Gardeners' Dictionary 2: 199, t. 299 (1760).

Leucoxylon laurinum E. Mey. in Drege: 77, 79, 199 (1843), nom. nud.

Ilex capensis Sond.: 473 (1860); Pappe: 12 (1862); Oliv.: 359

(1868); Hiem: 143 (1896); Sim: 151 (1907); Eyles: 403 (1916). Types:

South Africa, Magaliesberg, Zeyher 1129 (K, SAM, isosyn.!); Uiten-

hage, Zeyher 3365 (SAM, isosyn.!); Zeyher 3366 (K, SAM, isosyn.!);

Winterhoeksberg and Nieuwekloof, Drege (K. isosyn.!) and many other

sheets and plates.

Rex mitis (L-) Radik, forma capensis (Sond.) Loes.: 242 (1901).

Celastrus sieberi Bemh. in Hb. Krauss., nom nud.

Densely crowned tree or shrub to 16 m tall, occasional-

ly to 33 m, evergreen; trunk up to 1 m in diameter, rarely

to 5.5 m. Bark smooth when young, whitish or grey, later

becoming pustulate and somewhat chunky or fissured,

(older Cape trees often have a pinkish red bark). Young

branchlets often puberulous, purplish. Leaves alternate,

glabrous, elliptic to elliptic-lanceolate, oblong-elliptic or

obovate-elliptic, 2.4-9. 5(-l 1.0) x 0.9— 2.5(— 3.5) mm,

acute, apiculate or rounded at apex, rarely acuminate

(often kinked when dried), obtuse or cunate at base, dark

green, often dull above, paler below; midrib pale, sunken;

entire or sometimes spiny near apex or in upper half of

leaf only, (young foliage olive or reddish green, spiny),

petiole 0.7-2.0 mm long, glabrous, channelled, usually

reddish purple; stipules semi-persistent. Inflorescence 1-

few-flowered cymes, pubescent. Calyx pubescent, lobes 5

or 6, 0.5-1 .0 mm long, ciliate. Petals white, glabrous, 2.3-

3.0 x 1. 5-2.0 mm, lobes 5 or 6, ciliate, fragrant. Stamens

5 or 6, 1.5-2. 5 mm long, staminodes shorter. Ovary

globose, 1.6 x 1.3 mm, stigma sessile, discoid, prominent;

rudimentary ovary conical. Fruit 4—6 mm in diam., glo-

bose, slowly ripening from greenish pink to dark crimson;

pyrenes 5 or 6, 3. 0-3. 5 x 1.0- 1.5 mm.

Widespread in Africa south of the Sahara, down to the

Cape. Does not occur in Namibia, Botswana and in the

drier parts of the Transvaal, Orange Free State and the

Cape. Most frequently growing beside rivers and streams,

in moist evergreen forests or low montane grassveld.

Flowering from September to February and fruiting from

December to June. Usually found between 7-600 m near

the coast and 1 000-2 1 30 m further inland. Ranges from

common to rare depending on locality. Figure 1.

Vouchers: Compton 32099 (PRE); Hemm 29 (PRE); Scheepers 772

(K, PRE): Strey 9880 (K. PRE); Williams 593 (K, PRE).

Has been used as an enema for colic in children

(southern Sotho); as a purgative (Kgatla); a lather is used

164

Bothalia 24,2 (1994)

for washing the bodies of influenza sufferers (Zulu) and

in witchcraft (Sotho). The wood is used for furniture and

ceilings, brake blocks, railway sleepers and for firewoord.

Common names: Litota, liBota (Swati); Munamiti

(Bakone Suto); Mutanzwa-Khamelo (Venda); Phukhu,

Motoo a phofu, Mofusata (S Sotho); iPhuphuma (Zulu);

monamane (N Sotho); unDuma (Xhosa, Zulu); phukgu,

phugile (S Sotho); waterboom, waterhout, without, wit-

waterhout (Afrikaans); Cape holly, wild holly, water tree,

African holly (English).

Cultivated in Europe as a glasshouse or stove plant before

1816.

Var. schliebenii Loes. is only known from the Moro-

goro District, Tanzania and differs from var. mitis in its

smaller, almost round leaves.

FIGURE 1. — Ilex mitis var. mitis. A-F,

male : A, flowering branch, x 1 ; B,

bud, x 4; C, flower, x 4; D, calyx,

opened out, x 4; E, corolla, opened

out to show stamens, x 4; F,

rudimentary ovary, x 4. G-J,

female: G, flower, x 4; H, corolla,

opened out to show staminodes, x

4; I, ovary and calyx, x 4; J, detail

from fruiting branch, x 1. A-F,

Jessel 61\ G-I, Battiscombe 643\

J.A.S. Thomas 2650 (Reproduced

from the Flora of tropical East

Africa, with permission of the

Director of the Royal Botanic Gar-

dens, Kew. Artist Dorothy Thomp-

son.).

Introduced species

Voucher specimens have been seen for the following

species which are cultivated. Other taxa are mentioned in

Hollies — underused trees and shrubs for cultivation in

southern Africa (S. Andrews in prep.).

Ilex aquifolium L. Common or English holly. Na-

tive of S & W Europe, North Africa and W Asia. Shrub,

evergreen. Bark grey. Leaves elliptic or ovate, dark glossy

green, undulate, entire or when spinose, divaricating.

Flowers white, rarely tinged pink. Fruits spherical, red.

In parks and gardens.

Vouchers: S. Andrews 956 (PRE); L.E. Codd 10449 (PRE); F. Venter

12107 (PRE).

Bothalia 24,2(1994)

165

Ilex cornuta Lindl. & Paxton. Homed holly. Native

of China and Korea. Shrub, evergreen, dense rounded

habit. Leaves rectangular, dull green, spines variable, from

5-9 on older plants. Flowers white. Fruits spherical, red.

In parks and gardens.

Voucher: S. Andrews 985.

I. cornuta ‘Burfordii’. Leaves with terminal spine

only. Female. In gardens.

Vouchers: S. Andrews 986 (PRE); L.D. du Toil 130 (PRE).

Hex x koehneana Loes. (I. aquifolium L. x /.

latifolia Thunb.). Evergreen tree or shrub. Leaves oblong

to elliptic, large, glossy mid-green, strongly spined.

Flowers white. Fruits globose, bright red. In gardens.

Voucher: S. Andrews 914 (K, PRE).

Dex paraguariensis A. St.-Hil. Mate, Yerba Mata,

Paraguay tea. Native of Paraguay, Brazil, Uruguay, Ar-

gentina. Evergreen tree to 12 m. Bark grey. Leaves oblong

to obovate-oblong, obtuse, serrate, dull mid-green.

Flowers greenish white. Fruits globose, glossy dark red.

Planted at Westfalia Estate, Duiwelskloof, probably for

economic beverage which is made from the dried leaves.

Voucher: J.J. Bos 1093 (K. PRE).

Dex pernyi Franch. Native of Central and W China.

Shrub, evergreen. Leaves nearly sessile, triangular. 5-

spined, squared at base, dark glossy green. Flowers yel-

lowish. Fruit spherical, red. Seen in gardens.

Voucher: 5. Andrews 983 (PRE).

Ilex vomitoria Aiton (/. cassine Walter non L.)

Yaupon. Native of SE United States and Mexico. Tree or

shrub to 7 m. evergreen. Leaves ovate or elliptic, obtuse,

crenate, dark glossy green. Flowers white. Fruit globose,

scarlet. Planted in Grahamstown Botanic Garden. Foliage

contains a caffeine used by the North American Indians.

Voucher: 5. Andrews 1162 (K. PRE).

REFERENCES

ADAMSON. R.S. 1950. Aquifoliaceae. In R.S. Adamson & T.M. Salter,

Flora of the Cape Peninsula. Juta, Cape Town.

AITON, W. 1789. Hortus kewensis, edn 1. George Nicol, London.

AITON, W. 1811. Hortus kewensis, edn 2. Vol. 2. Longman, London.

BAKER. E.G. 1911. Contribution to our knowledge of the flora of

Gazaland. Journal of the Linnean Society. Botany 40: 1-245.

BENTHAM, G. & HOOKER, J.D. 1867. Genera plantarum 1: 356.

Lovell Reeve, London.

BRENAN, J.P.M. 1949. Check lists of the forest trees and shrubs of the

British Empire 5.2, Tanganyika Territory. Imperial Forestry In-

stitute, Oxford.

BRENAN, J.P.M. 1953. Plants collected by the Vemay Nyasaland ex-

pedition of 1946. Memoirs of the New York Botanical Garden 8:

191-256.

BURTT DAVY, J. 1932. A manual of the flowering plants and ferns of

Transvaal and Swaziland , Vol. 2. Longmans Green, London.

COMPTON. R.H. 1976. The Flora of Swaziland. Journal of South

African Botany , Supplementary Volume 1 1 .

DE CANDOLLE, A.P 1825. Prodromus systematis naturalis regni

vegetabilis. Treuttel & Wiirtz, Paris.

DREGE, J.F. 1843. Zwei pflanzengeographische Documente. Flora,

Regensburg.

DYER, R.A. 1975. Genera of South African flowering plants, Vol. 1.

Government Printer, Pretoria.

ENGLER, H.G.A. 1921. Aquifoliaceae. Die Pflanzenwelt Afrikas 3,2:

218-220. Engelmann, Leipzig.

EXELL, A.W. 1927. Mr John Gossweiler’s Portuguese West African

plants. Journal of Botany, London 65: Suppl. Polypet. 74.

EXELL, A.W. & MENDON^A, F.A. 1951. Aquifoliaceae. Conspectus

florae angolensis 1 : 348. Junta de Investigafoes Coloniais, Lis-

bon.

EYLES, F. 1916. A record of plants collected in Southern Rhodesia.

Transactions of the Royal Society of South Africa 5: 273-564.

HARVEY, W.H. 1 868. Genera of South African plants, edn 2. Longman,

Green, Reader & Dyer, London.

HIERN, W.P. 1896. Catalogue of the African plants collected by Dr

Friedrich Welwitsch 1: 143, 144. British Museum (Natural His-

tory), London.

JACQUIN, N.J. 1789. Collectanea. Wappler, Vienna.

KEAY, R.W.J. 1958. Aquifoliaceae. Flora of West tropical Africa, edn 2,

1,2: 623. Crown Agents, London.

LAMARCK, J.B.A.P.M. 1797. Tableau encyclopedique et methodique,

Botanique. Pancoucke, Paris.

LEBRUN, J. 1935. Les Essences forestieres du Congo Beige 2: les

essences forestieres dies regions montagneuses du Congo orien-

tale. INEAC, Bruxelles.

LINNAEUS, C. 1753. Species plantarum. Salvius, Stockholm.

LINNAEUS, C. 1754. Genera plantarum, 5th edn: 60. Salvius, Stock-

holm.

LINNAEUS, C. 1767. Systema naturae, edn 12,2: 178. Salvius, Stock-

holm.

LOESENER. L.E.T. 1895. Aquifoliaceae. In H.G.A. Engler. Pflanzenwelt

Ost-Afrikas C: 245, 246. Reimer, Berlin.

LOESENER. L.E.T. 1901. Monographia Aquifoliacearum, pars 1. Vova

acta academiae caesareae Leopoldino-Carolinae 78: 8-500.

LOESENER, L.E.T. 1912. Botanik: Aquifoliaceae. Wissenschaftliche Er-

gebnisse der deutschen Zentral-Afrika Expedition 1907-1908. 2:

463,464.

LOESENER. L.E.T. 1942. Aquifoliaceae. Die Natiirlichen Pflanzen-

familien, edn 2, 20b: 36-86. Engelmann, Leipzig.

MARLOTH. H.W.R. 1925. Flora of South Africa. Darter, Cape Town.

MENDES, E.J. 1966. Aquifoliaceae. Flora zambesiaca 2: 353-355.

Crown Agents, London.

MENDES, E.J. 1973. Aquifoliaceae. Flora de Mozambique 47: 1, 2.

Junta de Investigates do Ultramar, Lisbon.

MILLER, P. 1760. Gardeners' Dictionary. London.

OLIVER. D. 1868. Ilex. Flora of tropical Africa 1: 359. Lovell Reeve,

London.

PALGRAVE, K.C. 1977. Trees of southern Africa. Struik, Cape Town.

PALMER, E. & PITMAN, N. 1972. Trees of southern Africa. Balkema,

Cape Town.

PAPPE, C.W.L. 1854. Silva capensis. Van de Sandt de Villiers, Cape

Town.

PAPPE, C.W.L. 1 862. Silva capensis, edn 2. Index.

PERRIER DE LA BATHIE, J.M.H.A. 1946. Aquifoliacees. Flore de

Madagascar et des Comores 115: 1—5.

PERSOON. C.H. 1805. Synopsis plantarum. Cramer, Paris.

POIRET, J.L.M. 1810. Encyclopedic methodique , Suppl. Agasse, Paris.

POIRET. J.L.M. 1812. Encyclopedic methodique 2,2. Agasse, Paris.

RADLKOFER, L.A.T. 1886. In Reports of the British Association for the

Advancement of Science 1885: 1081.

ROBYNS, A. 1960. Aquifoliaceae. Flore du Congo Beige 9: 109-112.

INEAC, Brussels.

ROBYNS, W. 1948. Flore des spennatoplvytes du Parc National Albert.

Tome 1 — Gymnospermes et Choripetales. Institut des Parcs

Nationaux du Congo Beige, Brussels.

ROEMER. J.J. & SCHULTES. J.A. 1819. Systema vegetabilium 4. Cotta,

Stuttgardt.

ROEMER, J.J. & SCHULTES, J.A. 1829. Systema vegetabilium 7.1.

Cotta. Stuttgardt.

SIM. T.R. 1907. The forests and forest flora of the Colony of the Cape of

Good Hope. Taylor & Henderson, Aberdeen.

SIMS, J. 1816. Sideroxylon mite. Curtis ’ Botanical Magazine 43: t. 1858.

SONDER, O. 1860. Ilex in W.H. Harvey & O. Sonder. Flora capensis 1:

472M74. Hodges Smith. Dublin.

SPRENGEL, K. 1824. Systema vegetabilium, edn 16. Dietrichiana,

Gottingen.

TROUPIN, G. 1983. Flore du Rwanda — Spenmtophytes 2: 321-323.

Musee Royale de l’Afrique Centrale, Tervuren.

VERDCOURT, B. 1967. Tropical African plants 28: Aquifoliaceae. The

typification of Ilex mitis (L.) Radik. Kew Bulletin 21 : 243.

166

Bothalia 24,2 (1994)

VERDCOURT, B. 1968. Aquifoliaceae. Flora of tropical East Africa.

Crown Agents, London.

VERDCOURT, B. 1989. Aquifoliaceae. Flora of Ethiopia 3: 329, 330.

National Herbarium, Addis Ababa.

VON BREITENBACH, F. 1963. Indigenous trees of southern Africa.

Government Printer, Pretoria.

WHITE, F. 1962. Forest flora of Northern Rhodesia. Oxford University

Press, London.

WILLDENOW, C.L. 1798. Species plantarum 1,2. Nauk, Berlin.

WILEDENOW, C.L. 1799. Spiecies plantarum 2. Nauk, Berlin.

WILLDENOW, C.L. 1809. Enumeratio plantarum horti regii botanici

Berolinensis. Libraria Scholae regalis, Berlin.

Bothalia 24,2 167-170(1994)

Notes on African plants

VARIOUS AUTHORS

PROTEACEAE

A NEW SPECIES OF LEUCOSPERMUM FROM THE SOUTHWESTERN CAPE

Since the last revision of Leucospermurn R. Br. was

published (Rourke 1972), undescribed taxa in this

prominent genus continue to be found (Rourke 1979;

1983). The singular species here described as Leucosper-

mum harpagonatum Rourke was discovered during

August 1993 at the northeastern end of the Rivier-

sonderend Mountains by Dr A.E. Rebelo of the Protea

Atlas Project.

Leucospermurn harpagonatum Rourke , sp. nov.

distinctissima, habitu prostrato conferto; foliis glabris

secundis integris; inflorescentia 8-10 floribus; 25-35 brac-

teis involucralibus; perianthio curto, tubo inflato distaliter

dense lanato; stylo distaliter retrorse hamato adaxialiter

valde arcuato, distinguitur.

TYPE. — Cape Province 3419 (Caledon): Groot Toren,

north slopes of Riviersonderend Mountains above

Olifantsdoom Farm on west side of a koppie NW of

Aasvoelkrans, (-BB), 20-10-1993, J.P. Rourke 2030

(NBG holo.!; B, BOL, E, K, MO, NSW, PRE, S, STE,

iso.!).

Prostrate sprawling shrublet forming dense mats 1-3

m in diam., 100-150 mm tall, with trailing branches

radiating horizontally along ground, arising from a single

main stem. Flowering branches usually produced at

perimeter of mat, 3-5 mm in diam.. puberulous initially,

soon glabrous, reddish flushed, bearing numerous pedun-

culate axillary inflorescences. Leaves secund, linear to nar-

rowly oblong, 55-110 x 2-10 mm, tapering in petiolar

region; apex entire, obtuse to rounded with a single amber

callosity; lamina broadly concave on upper surface, mar-

gins slightly incurved. Inflorescence 8— 10( 12)-flowered.

turbinate, 28-30 mm in diam.; pedunculate, peduncle 10-

20 mm long. Involucre prominent, 3-seriate; composed of

25-35 ovate to broadly ovate, densely sericeous, car-

tilaginous involucral bracts, 6-8 x 2-A mm; imbricate but

apices patent, acuminate. Receptacle obconic-flattened, 3-

5 mm diam. Floral bracts tightly clasping perianth, broad-

ly ovate, acute, 5 x 6-7 mm, very densely sericeous.

Perianth cream to pale carmine, very strongly adaxially

curved, utriculose, 1 0—15 mm long; tube prominently in-

flated, 9-10 x 5-6 mm distally, narrowed and glabrous

proximally, densely lanate distally; claws 4—5 mm long,

abruptly narrowed above tube, strongly deflexed on open-

ing, densely lanate, especially along margins, carmine in

live state; limbs lanceolate-acute, 3 mm long, recurved on

opening, densely villous. Anthers 4, sessile, 1 mm long.

Style 20-25 mm long, strongly adaxially cygneous, taper-

ing terminally, upper half retrorsely barbed, cream or red-

dish in live state, tapering to a narrow neck below pollen

presenter. Pollen presenter inwardly curved, conic-acute

1.5 mm long with a distinct proximal corona. Stigmatic

groove terminal. Ovary not differentiated from style,

minutely sericeous, 0.5 mm long. Hypogynous scales

linear-acute 2 mm long, yellow. Fruit a minutely

puberulous, cylindric, greyish-white achene, 8x5 mm,

broadly emarginate at apex. Figures 1 & 2.

Diagnostic characters

This species is clearly related to L. hamatum Rourke

on account of its few-flowered inflorescences, adaxially

curved styles beset with minutely retrorse barbs and in-

flated perianth tubes. It is distinguished from L. hamatum

by having linear to narrowly linear, entire leaves (usually

tridentate in L. hamatum) and by the utriculose perianth

tube, densely lanate in the upper half (glabrous in L.

hamatum). Another marked difference is that L. har-

pagonatum has a well-developed involucre of 25-35

bracts, whereas in L. hamatum the involucre consists of

3 or 4 bracts or is completely absent and is replaced by

a false involucre formed from 4 or 5 floral bracts. On

average there are more flowers in each inflorescence in

L. harpagonatum (8-10 flowers) and fewer (4—7 flowers)

in L. hamatum.

Relationships

Leucospermurn hamatum and L. harpagonatum are

clearly a pair of geographical vicariads, their distribution

areas separated by approximately 200 km. They share the

remarkable character of having styles beset with minutely

retrorse barbs. Their perianths are also similar in form,

having very reduced shortened claws and a large tube

prominently inflated distally to form a bladder-like nectar

reservoir. In this character they appear to be allied to

Leucospermurn section Tumiditubus and may even have

been derived from that section as a specialised offshoot.

However, the two species should be placed within a

distinct section of their own. With its well-developed in-

volucre and greater number of flowers in each inflores-

cence, L. harpagonatum represents a very much less

reduced stage than L. hamatum.

Distribution , habitat and biology

Present information suggests that L. harpagonatum is

endemic to a few hectares at the northeastern end of the

Riviersonderend Range near McGregor in the south-

western Cape. A single population of approximately 60

plants has been located on the farm Groot Toren above

Olifantsdoom homestead at an elevation of approximately

168

Bothalia 24,2 ( 1994)

FIGURE 1. — Leucospermum harpagonatum Rourke. A, flowering shoot:, B, lengthwise section through inflorescence; C, perianth in bud; D,

involucral bract; E, perianth at anthesis showing inflated tube region; F, floral bract; G, perianth limb and anther; H, gynoecium showing

retroresly barbed style, pollen presenter, ovary and hypogynous scales; I, mature achene. From the type material Rourke 2030.

Bothalia 24,2(1994)

169

FIGURE 2. — -Leucospermum harpa-

gonatum Rourke. A, flowering

branch; B, close-up view of

inflorescences about to open

(left) and fully open (right).

Rourke 2030. Photo by J.

Loedolff.

790 m, growing in a dry variant of Mesic Mountain Fyn-

bos (Figure 3).

Mature adult plants form dense mats 0.5-3. 0 m in

diameter which resemble Carpobrotus edulis when

viewed from a distance. Flowering takes place on short

shoots as well as on the long trailing branches produced

at the perimeter of the mats. These trailing branches are

particularly floriferous producing up to twenty-five axil-

lary inflorescences along their length. The flowers are

cream at first, changing to pink and carmine in the post-

pollination phase. They produce no perceptible odour and

open between late August and the end of November. Both

styles and perianths are chewed by rodents which gnaw

open the bladder-like perianth tube apparently to gain ac-

cess to the large volume of nectar which is produced in

each swollen perianth.

The specific epithet is derived from harpago — a grap-

pling iron and the suffix -atum indicating likeness or pos-

session. alluding to the distinctive form of the styles.

170

Bothalia 24,2 (1994)

Specimens examined

WESTERN CAPE. — 3419 (Caledon): above Olifantsdoorn, Rivier-

sonderend Range, (-BB), Aug. A.G. Rebelo s.n. Protea Atlas 9308121

(NBG); Groot Toren, north slopes of Riviersonderend Mountains above

Olifantsdoorn Farm on west side of a koppie NW of Aasvoelkrans, (-BB),

Oct., Rourke 2030 (B. BOL, E, K, MO, NBG. NSW, PRE, S, STE).

ACKNOWLEDGEMENTS

I am most grateful to Dr Tony Rebelo for drawing my

attention to this species, to Ellaphie Ward-Hilhorst who

prepared the line drawing and to Jeanette Loedolff for the

photographs.

REFERENCES

ROURKE, J.P. 1972. Taxonomic studies on Leucospennum R. Br. Jour-

nal of South African Botany , supplementary vol. No. 8.

ROURKE, J.P. 1979. Leucospennum winteri. The Flowering Plants of

Africa : t. 1781.

ROURKE, J.P. 1983. A remarkable new Leucospennum from the

southern Cape. Journal of South African Botany 49: 213-219.

J.P. ROURKE*

* Compton Herbarium, National Botanical Institute, Kirstenbosch, Private

Bag X7, Claremont 7735, Cape Town.

BORAGINACEAE

LOBOSTEMON REGULAREFLORUS — THE CORRECT NAME FOR L. GRAND1FLORUS

Levyns (1934) published Lobostemon grandiflorus

(Andrews) Levyns as a new combination. The basionym

is cited as Echium grandiflorum Andrews (1797). Salis-

bury (1796), however, described E. grandiflorum Salisb.

a year earlier. According to Article 64.1 of the ICBN

(Greuter et al. 1988) a combination based on a later

homonym is illegitimate.

However, Art. 72, Note 1 of the ICBN (Greuter et al.

1988) permits an author to use an illegitimate epithet

providing it is used in a ‘new position or sense’. This

means that Lobostemon grandiflorus Levyns is treated as

new having priority from 1934. Nonetheless, an older

specific epithet than Levyns’s grandiflorus exists and the

present combination is therefore rejected in favour of the

one given below.

Ker Gawler (1801) published the trinomial Echium

regulare florum, which cannot be regarded as a phrase in

the ablative. Therefore, in accordance with Art. 23.1 of

the ICBN (Greuter et al. 1988), the aforementioned epithet

is not to be rejected and must be united as below. Regard-

ing the epithet regulare, it is clearly an adverb and is

therefore not subject to the provisions of Recommendation

73G in respect to changing the ‘e’ to ‘i\

The illustration by Andrews (1797: t. 20) is chosen as

the lectotype because Ker Gawler (1801) refers solely to it.

Lobostemon regulareflorus (Ker Gawl.) Buys,

comb. nov.

Echium regulare florum Ker Gawk: 147 (1801). E. grandiflorum

Andrews: t. 20 (1797); Vent.: t. 98 (1805); Desf.: 177 (1809); Edwards:

t. 124 (1816); Aiton: 299 (1810); Mord. Laun. & Loisel.: t. 195 (1819);

Roem. & Schult.: 1 1 & 714 (1819); Link: 170 (1821); Drapiez: t. 235

(1830), non E. grandiflorum Salisb.: 1 15 (1796). E. formosum Pers.: 163

(1805); Lehm.: 418 (1818): DC.: 15 (1846); C.H. Wright: 44(1904). E.

lubiferum Poir.: 663 ( 1808). Type: Andrews: The Botanist’s Repository:

t. 20 (1797), (lecto., here designated).

Lobostemon formosus (Pers.) H. Buek: 132 ( 1837).

L. grandiflorus (Andrews) Levyns: 443 (1934).

REFERENCES

AITON, W. 1810. Hortus kewensis, edn 2,1: 299. Longman, London.

ANDREWS, H.C. 1797. The Botanist's Repository, t. 20. Bensely, Lon-

don.

BUEK, H.W. 1 837. Echia capensia. Linnaea 11: 132.

DE CANDOLLE, A.P. 1846. Prodromus systematis naturalis regni

vegetabilis 10: 15. Treuttel & Wiirtz, London.

DESFONTA1NES, R.L. 1809. Histoire des arbres et arbrisseaux qui

peuvent etre cultives en pleine terre sur le sol de la France 1 : 177.

Brosson, Paris.

DRAPIEZ, P.A.J. 1830. Herbier del’ amateur de fleurs, contenant, graves

et colorie’s, d’apres nature 4: t. 235. De Mat, Bruxelles.

DUMONT DE COURSET, G.L.M. 1814. Le Botaniste cultivateur, ou

description, culture et usages de la plus grande partie des plantes

etrangeres 2,7: 147. Deterville Goujon, Paris.

EDWARDS, S. 1816. The Botanical Register 2: t. 124. Ridgeway, Lon-

don.

GREUTER, W„ BURDET, H.M., CHALONER, W.G., DEMOULIN, V.,

GROLLE, R„ HAWKSWORTH, D.L., NICOLSON, D.H.,

SILVA, PC., STAFLEU, F.A., VOSS, E.G. & McNEILL, J. 1988.

International code of botanical nomenclature adopted by the

Fourteenth International Botanical Congress, Berlin, July-August

1987. Regnum vegetabile 1 18.

KER GAWLER, J.B. 1801. Recensio plantarum hue usque in repositorio

botanicarum depictamm : 11. White, London.

LEHMANN, J.G.C. 1818. Plantae e familiae Asperifoliantm nuciferae:

418. Dummler, Berlin.

LEVYNS, M.R. 1934. A revision of Lobostemon. Journal of the Linnean

Society 49: 393-451.

LINK, J.H.F. 1821. Enumeratio plantarum horti regii botanici berolinen-

sis altera 1: 170. Reimer, Berolini.

MORDANT DE LAUNAY, J.C.M. & LOISELEUR-DESLONG-

CHAMPS, J.L.A. 1819. Herbier general de Vamateur 3: t. 195.

Audot. Paris.

PERSOON, C.H. 1805. Synopsis plantarum, sen Enchiridium botanicum

complectens enumerationem systematicam specierum hucusque

cognitarum 1: 163. Cramerum, Paris.

POIRET, J.L.M. 1 808. Encyclopedic methodique . Botanique 8: 663. Chez

H. Agasse, Paris.

ROEMER. J.J. & SCHULTES. J.A. 1819. Systema vegetabilium 4: 1 1 &

714. Cottae, Stuttgardt.

SALISBURY, R.A. 1796. Prodromus stirpium in horto ad Chapel Aller-

ton vigentium: 115. London.

VENTENAT, E.P. 1805. Jardin de la Malmaison 2: t. 98. De Pimprimerie

de Crapelet.

WRIGHT, C.H. 1904. Flora capensis 4,2: 44. Lovell Reeve, London.

M.H. BUYS* and J.J.A. VAN DER WALT*

* Department of Botany, University of Stellenbosch, Private Bag X5018,

Stellenbosch 7599.

MS. received: 1994-01-25.

Bothalia 24,2: 171-185 (1994)

An overview of Aspergillus (Hyphomycetes) and associated teleomorphs in

southern Africa

A. LOUISE SCHUTTE*

Keywords: Aspergillus , Emericella, Eurotium, fungi, Hyphomycetes, mycotoxins, overview, pathology, southern Africa, taxonomy

ABSTRACT

An overview is given of literature concerning the genus Aspergillus Link and its teleomorphs, Chaetosartorya Subram,,

Emericella Berk. & Broome, Eurotium Link, Fennellia B.J. Wiley & E.G. Simmons, Neosartorya Malloch & Cain and

Sclerocleista Subram. encountered in the Republic of South Africa, Botswana, Lesotho, Mozambique, Namibia, Swaziland,

Transkei and Zimbabwe up to 1993. The information is grouped under headings that indicate the field of research, namely

general mycology, plant pathology, human pathology, animal and insect pathology, industrial relevance and secondary metabo-

lites and mycotoxins. An alphabetical list of recorded Aspergillus species is provided and the relevant host or substrate is given

together with a literature reference, while the fungal nomenclature has been updated. All the Aspergillus species that are

regarded as common have been reported from southern Africa. No in-depth research has been done here on this group, except

for chemical work on mycotoxins.

U1TTREKSEL

’n Oorsig van literatuur aangaande die genus Aspergillus Link en sy teleomorwe, Chaetosartorya Subram., Emericella Berk.

& Broome, Eurotium Link, Fennellia B.J. Wiley & E.G. Simmons, Neosartorya Malloch & Cain en Sclerocleista Subram.,

aangetref in die Republiek van Suid-Afrika, Botswana, Lesotho, Mosambiek, Namibie, Swaziland, Transkei en Zimbabwe tot

1993 word gegee. Die informasie word gegroepeer onder opskrifte wat die aard van die navorsing aandui naamlik mikologie,

plantpatologie, menslike patologie, dierlike- en insekpatologie, industriele toepassings en sekondere metaboliete en mikotok-

siene. ’n Alfabetiese lys van aangetekend e. Aspergillus spesies word verskaf en die relevante gasheer of substraat word saam met

'n verwysing gegee terwyl die swamnomenklatuur op datum gebring is. Die algemene Aspergillus spesies in suidelike Afrika is

almal aangeteken. Geen diepgaande navorsing is hier op hierdie groep gedoen nie, behalwe die chemiese werk op mikotoksiene.

INTRODUCTION

‘Species of the great group Aspergillus form a very

considerable percentage of all the mould colonies en-

countered in the cultural examination of foodstuffs, of soil

and of miscellaneous materials’ (Thom & Church 1926).

Economically and ecologically Aspergillus is a very

important group, not only because of its ubiquitous nature,

but it also has the ability to grow under a wide range of

conditions (Domsch et al. 1980). There are probably few

substrates that cannot be colonized and degraded. These

fungi also synthesize an extraordinary variety of metabo-

lites with biological activity (Raper & Fennell 1973).

Profitable and advantageous applications of Aspergillus

can be found in the production of antibiotics, antifungal

substances, vitamins and organic acids, in the preparation

of oriental foods, the use of various species in physiologi-

cal experiments and testing of fungicides as well as in

genetic work (Kozakiewicz 1989). Aspergilli also have a

deleterious impact: some members of the genus are plant

pathogens (Raper & Fennell 1973; Gorter 1977), there are

well-known human (Martin & Berson 1973) and animal

pathogens (Neitz 1965), many are mycotoxin producers

(Frisvad 1989) and they contribute greatly to spoilage

(Kozakiewicz 1989).

* Mycology Unit, Biosystematics Division, Plant Protection Research

Institute, Private Bag XI 34, Pretoria 0001, Republic of South Africa.

MS. received: 1993-10-15.

The genus name Aspergillus dates back to Micheli,

who used the term because of the similarity between the

conidial head and a holy water sprinkler called an aspergill

(Raper & Fennell 1973). The development of the

taxonomy of Aspergillus is described in detail by Raper

& Fennell (1973), Christensen & Tuthill (1985) and

Kozakiewicz (1989).

The first comprehensive work on the genus Aspergillus

was by Thom & Church (1926) and the second revision

of this work is the monograph currently used for Asper-

gillus identifications (Raper & Fennel 1973). These

authors recognised 132 species and separated them into

18 groups. In an update by Samson (1979), he accepted

another 34 taxa and nomenclaturally separated the asexual

from the sexual states.

A shortcoming of the work of Raper & Fennell (1973)

is the fact that both anamorph and teleomorph species are

treated under the anamorph genus, Aspergillus. The

nomenclatural separation of the anamorph from the

teleomorph, as incorporated by Benjamin (1955), was not

accepted by Raper & Fennell (1973). Benjamin (1955)

selected the previously published generic names, Eurotium

Link, Emericella Berk, and Sartorya Vuill. for the teleo-

morphic states. The typification of 190 taxa of Aspergillus

was investigated by Samson & Gams (1985) and adjust-

ments were made to meet the rules of the International

Code of Botanical Nomenclature, giving teleomorphic

names priority over anamorphic ones. The taxonomic

work of Horie (1980), Gams & Samson (1985) and

172

Bothalia 24,2 ( 1994)

Kozakiewicz (1989) further contributed to our knowledge

of the group.

Various authors have studied specific groups of the

genus: Al-Musallam (1980) did a revision of the black

Aspergilli, Christensen (1982) revised the A. ochraceus

group and Kurtzman et al. ( 1986) and Klich & Pitt ( 1988)

differentiated between species in the A. flavus group.

Horie ( 1980) and Kozakiewicz (1989) used ascospore and

conidial ornamentation as an aid to identification.

More sophisticated methods such as DNA relatedness

(Kurtzman et al. 1986), mycotoxin production (Klich &

Pitt 1988; Frisvad 1989), API-Zym strips (Jain & Lacey

1991) and genetic similarity studies (Peterson 1992) have

been used with success in Aspergillus identification. Sam-

son & Pitt (1985, 1990) described the use of nucleic acid

relatedness, serological methods, exocellular polysac-

charides, enzyme electrophoresis, ubiquinone systems and

DNA and RNA studies for the same purpose. Their find-

ings confirm the value of a multidisciplinary approach to

fungal taxonomy in general, including that of Aspergillus.

A major contribution to Aspergillus taxonomy has been

made by the workshops on Aspergillus and Penicillium

systematics (Samson & Pitt 1985, 1990) as well as the

formation of the Subcommission on Penicillium and

Aspergillus Systematics under the International Commis-

sion on Taxonomy of Fungi (Samson & Pitt 1990).

This paper is an overview of publications dealing with

all aspects of Aspergillus in South Africa, Botswana,

Lesotho, Mozambique, Namibia, Swaziland, Transkei and

Zimbabwe. Literature is grouped under headings indicat-

ing the scope of the research and is in chronological order.

A list of recorded species is appended in which isolates

in the dried collection (PREM) as well as the culture col-

lection (PPRI) of the National Collection of Fungi were

included. Culture collections donated to the Mycology

Unit as well as catalogues of international culture collec-

tions were consulted for additional information. No at-

tempt has been made to verify published data, the identity

of Aspergillus isolates or any other infonnation. Names

of fungi and hosts or substrates are given exactly as in

the original text.

OVERVIEW OF LITERATURE

General mycology

The first entry of an Aspergillus in the National Col-

lection of Fungi is A. glaucus Link (PREM 701 — see

checklist), collected by J.H.T. De Villiers from Nicoti'ana

tabacum in the Cape Colony, on 24 December 1909.

Eurotium herbariorum Link (PREM 833 — see checklist),

identified by R.N. Adlam and collected by Medley Wood

from Cephalanthus natalensis in Transvaal ( Wood 3920),

is the second entry. No author citation or date is given

but Medley Wood collected during the previous century

and died in 1915 (Doidge 1950). In all probability this

specimen represents the first record of an Aspergillus in

southern Africa.

Aspergillus isolates are often listed in general fungal

surveys. Cohen (1950) studied soil fungi and recorded

three Aspergillus species. Doidge (1950) listed 19 species

of Aspergillus. Many of these species names are no longer

in use. The mycological Herbarium of the Timber Re-

search Laboratory, connected to the Transvaal Chamber

of Mines, had a collection of over 1 400 timber-deteriorat-

ing fungi, mostly obtained underground. Many of these

isolates had been identified overseas by Thom and the

CBS (see checklist). Fortunately, Doidge (1950) listed

these fungi, including the Aspergilli. as the original infor-

mation and lists could not be traced.

Ascosporic Aspergillus spp. present in the collection

of the University of the Witwatersrand were discussed by

Swart ( 1 959). Five Aspergillus spp., four of which were

new records for South Africa, were isolated from forest

soil in Zululand (Eicker 1969). The majority of fungi iso-

lated from Zululand soil belonged to the Fungi Imperfecti,

with Aspergilli well represented (Eicker 1970a), and dis-

tributed evenly in vertical profiles of these soils (Eicker

1970b). In a paper dealing with the occurrence, isolation

and identity of thermophylic fungi, Eicker (1972) indi-

cated that A. fumigatus Fresen. can grow and sporulate at

temperatures ranging from 20°C to 50°C. A. japonicus

Saito was present in three of the four Eucalyptus leaf litter

horizons (Eicker 1973). From savanna soil of the

Transvaal 16 species of Aspergillus were isolated (Eicker

1974), and most of these were deposited in IMI (see

checklist). Few isolates of Aspergillus were found on litter

of Panicum coloration L. (Eicker 1976). In the western

Transvaal, seven species of Aspergillus were found in the

soil of an Acacia karroo community (Papendorf 1976).

Bezuidenhout (1977) found nine Aspergillus spp. among

Hyphomycetes associated with the grass, Cenchrus

ciliaris L. Hyaline amerospores, including those of Asper-

gillus, were found to make up 4.5% of the aerospora

above an Eragrostis curvula (Schrad.) Nees pasture (Van

der Merwe et al. 1979).

Gorier (1979) compiled a checklist of fungi recorded

in South Africa up to 1977: the original publications are

listed here. A. clavatus Desm. was found to be present in

45% of industrial malt samples, while A. flavus Link com-

prised about 25% of the fungi found on commercial malt

(Rabie & Eiibben 1984). Roux (1985) isolated five Asper-

gillus spp. from a Karoo pasture. A. carbonarius (Bainier)

Thom has been recorded on Eucalyptus (Lundquist &

Baxter 1985) and Aspergillus spp. were found on Pinus

(Lundquist 1987).

Aspergillus spp. were the dominant fungi isolated from

the bare patches on the Giribes plains in Namibia, making

up 21% of fungi isolated (Eicker et al. 1982), but no ex-

planation could be given for this phenomenon. Allsopp et

al. (1987) isolated fungi associated with roots of

proteaceous seedlings and recorded A. duricaulis Raper

& Fennell and A. unilateralis Thrower from South Africa

for the first time. A. ficuum (Reichardt) Hennings and A.

ustus (Bainier) Thom & Church were found to be en-

dophytes in grass (De Villiers 1989). Aspergillus spp. were

commonly isolated from indigenous stored seed (Isaacs

& Benic 1990). Watson et al. (1990) found among others,

A. terreus in the gut of dune dwelling lepismatids, but

neither the role nor the effect of these fungi could be

determined. Conidiogenesis of A. niger Tiegh. was studied

by Tiedt (1992).

Bothalia 24,2(1994)

173

Plant pathology and seed deterioration

Verwoerd (1929) indicated A. niger as the cause of

disease of onions and pomegranates in the winter rainfall

area. Rosselet (1953) used A. niger as test organism in

determining available potassium in lowveld soil, and later

(Rosselet 1955) to determine levels of potassium, mag-

nesium and phosphorus in citrus orchards as well as in

virgin soil. This method is based on the assumption that

elements available to micro-organisms will be available

to plants. These references possibly have more relevance

to plant nutrition than to plant pathology.

Doidge & Van der Plank (1936) indicated A. niger and

Aspergillus spp. as a cause of rot on stored citrus fruit. A.

carbonarius, A. niger and A. ochraceus group were listed

as plant pathogens by Doidge et al. (1953). A. niger was

found to comprise 6% of fungi in citrus orchard soil

whereas in virgin soils A. fumigatus was one of the

dominant species. The latter species was rarely isolated

from citrus soil (Martin 1960). Four species of Aspergillus

contributed to the decay of litchi fruit, according to Roth

(1963) whereas A. niger has been isolated from banana

hands (Roth & Loest 1965).

Van der Westhuizen & Bredell (1972) found several

Aspergillus species on high quality maize, A. flavus , A.

niger and A. sydowi (Bain. & Sart.) Thom & Church being

among the most prevalent ones. Stored lucerne seed was

found to yield only a few Aspergillus spp. and no increase

during storage was reported (Marasas & Bredell 1973).

An index of plant pathogens (Gorter 1977) listed A. flavus

and A. niger.

According to Bornman (1978) a large proportion of

seeds of Welwitschia mirabilis (Hook, f.) are sterile and

this situation is aggravated by A. niger. This fungus infests

the inflorescence, rendering more than 99% of all seeds

infertile. This same fungus has also been listed in con-

nection with post-harvest decay of mangoes (Wehner et

al. 1981). Aspergillus contamination of both stored seed

and seedlings of maize is high: members of the A. glaucus

group are often isolated and it is suggested that some

Aspergillus spp. may be seed-transmitted (McLean & Ber-

jak 1987).

Various Aspergillus species were isolated from the

roots of Medicago spp., but they were not pathogenic

(Lamprecht et al. 1988). Steinke et al. (1990) found that

Aspergillus spp. deteriorated both Avicennia and Bru-

guiera leaves but they made up less than 12% of isola-

tions. This group of fungi occurred in less than 10% of

sorghum grain (Bosman et al. 1991). A. niger commonly

occurred in citrus soil but did not have a pronounced an-

tagonistic effect on various fungal pathogens of citrus

(Botha & Wehner 1990). Four Aspergillus spp. were

recorded to be antagonistic to Rhizoctonia solani by

Weideman et al. (1990).

Aspergillus spp. did not pose problems on stored

homoiohydrous seeds (Mycock & Berjak 1990). Mycock

et al. (1990) found that A. flavus var. columnaris Raper

& Fennell can infect maize seedlings and survive in the

maturing plant, and Mycock & Beijak (1992) found that

hot water treatment of maize seed decreased internal

Aspergillus counts from 61% to 5%. Healthy chicory roots

were inoculated with Aspergillus spp. isolated from in-

fected roots, but the fungi had no detrimental effect

(Prinsloo et al. 1991).

Human pathology

Species of Aspergillus are indicated as pathogens

worldwide in various aspects in the pathology of humans

and of other mammals and insects. In the case of humans

information is grouped below according to the effect of

the fungus. Thiel (1986) as well as Marasas (1988) con-

sidered foodbome mycotoxins such as aflatoxin, produced

by A. flavus to be of great medical relevance.

Aspergilli as allergens

Members of this genus have allergenic qualities and

the first southern African report in this regard is a survey

done by Ordman & Etter (1956). They found that Asper-

gillus spp. made up only 0.7% of airborne fungi in Johan-

nesburg and showed no seasonal incidence. A later survey

(Ordman 1963) indicated the same tendencies, with

similar results obtained for Windhoek (Ordman 1970).

Patients with positive precipitins to Aspergillus had these

to either A. fumigatus or A. niger ; the antigens were

prepared locally (Benatar et al. 1980). Patients of certain

population groups were found to be more allergic to A.

fumigatus than others (Joubert et al. 1988). Ten per cent

of allergic children in the Western Cape were sensitive to

Aspergillus spp. when positive skin tests were done,

whereas 12% tested positive to this fungus when IgE

responses were used (Potter et al. 1991)

Aspergilli and cancer

In an appraisal of liver cirrhosis and hepatoma in the

local population, Isaacson (1966) came to the conclusion

that liver cell necrosis can be a result of A. flavus toxicosis

rather than of infective hepatitis. Purchase & Vorster

(1968) suggested that aflatoxin M found in milk also had

a carcinogenic effect.

Gilman (1972) conducted a comprehensive survey into

fungal contamination of food in the Eastern Transvaal and

Swaziland and the findings supported an association be-

tween mycotoxins in the diet and incidence of liver cancer.

Various Aspergillus spp. were recorded and aflatoxin was

found to be more prevalent in groundnut products than in

maize. Peers et al. (1976) found a significant correlation

between ingested aflatoxin and the incidence of primary

liver cancer in Swaziland. Aspergillus was present in 3.3%

of samples from the low rate area and 6.7% samples from

the high rate area of an oesophageal cancer area in

Transkei (Marasas et al. 1981). The correlation of high

risk of exposure to aflatoxin and the hepatitis B virus to

hepatocellular carcinoma has been indicated (Bressac et

al. 1991), but is beyond the scope of this overview. The

above-mentioned references are merely representative of

this subject; more were traced but they did not refer to a

specific fungus.

174

Bothalia 24,2 (1994)

Aspergillosis, keratitis and otitis

Cases of infection by Aspergillus are often associated

with degenerative disorders. Jacobs et al. (1965) found

that pulmonary aspergillosis was extremely rare in all race

groups in South Africa and they described a single case.

Martin & Berson (1973) gave a comprehensive account

of fungal diseases in southern Africa, listing cases of

aspergilloses: various Aspergillus spp. were considered

responsible for 69 cases of diseases of the ear.

Two cases of aspergillosis of the skin were recorded

by Findlay et al. (1971) and in both cases the organism

involved was A. fumigatus, while Caro & Dogliotti (1973)

described a similar case. Block & Young (1977) indicated

the value of early diagnosis of opportunistic fungal infec-

tions and again referred to A. fumigatus. They also found

that the use of membrane filter blood cultures gave better

results than serological methods. This same fungus was

responsible for four cases of pneumonia described by Kal-

lenbach et al. (1977). Bak & Wagenveld ( 1983) discussed

the treatment of otitis where one of the organisms causing

problems was A. niger. A. fumigatus as well as an uniden-

tified Aspergillus sp. was found to cause fatal fungal

pneumonia in heart transplant patients (Cooper et al.

1983). A case report of paranasal sinus aspergillosis was

given by Glass et al. (1984) but no fungus was indicated.

Pulmonary aspergillosis caused by A. fumigatus compli-

cated pneumonia and was the cause of death of an other-

wise healthy patient (Lewis et al. 1985).

Aspergillus spp. were identified in four cases of fungal

keratitis that responded well to miconazole treatment

(Fitzsimons & Peters 1986). In the area where Mseleni

joint disease is found, 41% of homegrown groundnuts

were contaminated by Aspergillus (Marasas & Van

Rensburg 1986). A. stromatoides Raper & Fennell was

found to cause a fatal sino-orbital infection (Sacho et al.

1987), while A. niger was isolated from a patient with a

fatal brain abscess (Berkowitz et al. 1987). Govender et

al. (1991) reported five cases of A. fumigatus infection of

the spine and found that the patients responded well to

antifungal drugs.

Animal and insect pathology

Prinsloo (1960) found that A. parasiticus Speare in-

fected brown locusts both in the laboratory and in the

field. Neitz (1965) indicated A. fumigatus as an enzootic

pathogen in various birds, having obtained some of this

information by personal communication. Prozesky et al.

(1971) gave an account of A. fumigatus infection of scaly

weavers. An outbreak in a colony of these birds kept at

Onderstepoort is described: fortunately, the indicated treat-

ment quickly put an end to the morbidity and deaths. Nes-

bit (1986) described aspergillosis of a piglet but no

causative organism could be isolated.

Industrial relevance

The first record of Aspergilli mentioned in an industrial

sense was by Van der Bijl (1920) who studied deteriora-

tion of sugar by fungi. Isolates were sent to Thom in

America and his full report is included in Van der Bijl's

publication. The production of the enzyme invertase by

micro-organisms such as A. niger and A. terreus Thom

was influenced by various factors and these were indi-

cated. In the dairy industry Aspergillus spp. were reported

by Davel & Neethling ( 1930) to be troublesome. Purchase

& Vorster (1968) tested milk samples for the presence of

aflatoxin M, as this mycotoxin may be carcinogenic: 21

samples were tested and five gave positive results. A prob-

lem with sticky molasses meal was addressed Try Roth

(1968) who tested many micro-organisms, among others

seven species of Aspergillus, to render the product more

free-flowing.

When fungi found on cheese were tested for toxicity,

all isolates of A. ustus were found to be toxic to ducklings,

but no mycotoxins were detected in the cheese (Liick et

al. 1976). Likewise, no aflatoxin was detected in cheese

or milk powder but 23% of milk samples tested positive

(Liick & Wehner 1979).

Aspergillus spp. were found to be more prevalent on

grapes infected by Botrytis than on healthy ones (Le Roux

et at. 1973). Using three different techniques, Eicker

(1977) isolated thermophylic fungi, including A. fumi-

gatus, from mushroom compost. Fungal growth on wet-

blue leather is a common occurrence and Russell (1981)

tested various fungicides by using fungi including Asper-

gillus spp. isolated from this substrate.

Relative cellulytic activity of 14 species of Aspergillus

was also determined, when mesophilic fungi on compost

was studied (Eicker 1980). Various casing materials for

mushroom production were evaluated by Smit (1984) and

Aspergilli were encountered during microbiological

evaluation. Thermotolerant fungi, namely A. fumigatus

and an Aspergillus sp., were grown on spent sulphite liq-

uor from a pulp mill (Pretorius 1993a, b, c). The potential

for single cell protein production, the growth charac-

teristics of these fungi and three reactor configurations

were discussed.

Secondary metabolites and mycotoxins

Species of Aspergillus and Penicillium are potent

secondary metabolite and mycotoxin producers (Frisvad

1989). The use of secondary metabolite profiles in the

identification of these species is well established and these

substances are the subject of ongoing research (Samson

& Pitt 1985; Frisvad 1989; Samson & Pitt 1990).

In the early 1960's aflatoxin, a metabolite of A. flavus

and A. parasiticus, was discovered and soon found to be

highly carcinogenic (Raper & Fennell 1973). Previously

Thom & Church (1926) had already indicated that grain

contaminated with A. flavus could be poisonous to cattle

and swine. As a result of these findings, research in secon-

dary metabolites and mycotoxins became a high priority

world-wide. Rabie et al. (1964) indicated that A.

amstelodami (L. Mangin) Thom & Church had a toxic

effect on poultry and rabbits. The fungus proved to be

lethal to rabbits and reduced the growth of ducks. The

work done subsequently by Scott (1965) attracted inter-

national attention. He investigated the toxigenicity of

fungi obtained from various commercial products: 46 fun-

gal strains belonging to 22 species caused the death of

ducklings in only 14 days. Of these, 12 species belonged

Bothalia 24,2(1994)

175

to the genus Aspergillus. Five of these Aspergillus spp.

also had a detrimental effect on mice and rats.

Rabie et al. (1965) found that A. wentii Wehmer was

toxic to experimental animals, but the toxin was not iden-

tified. Rabie & Terblanche (1967) compared the influence

of temperature on two A. wentii isolates with variable

toxicity. The toxins were characterized and found to be

mildly toxic to ducklings (Rabie et al. 1986).

Van Warmelo (1967) investigated the correlation be-

tween the incidence of toxicity of stock feeds and certain

fungal species. Aflatoxin was found in only five of the

39 samples in which A. flavus was detected. Van Warmelo

et al. (1968) found that aflatoxin can accumulate in maize

naturally infected with A. flavus and that moisture and

temperature affect this process.

Holzapfel et al. (1966) showed that sterigmatocystin

was produced by fungi other than A. versicolor (Vuill.)

Tiraboschi and found that three out of five strains of A.

nidulans (Eidam) Wint. caused rapid deaths in ducklings.

A. niger was the most frequent fungus found on dried

fruits and nuts. Wehner & Rabie (1970) indicated that

maize on which A. niger as well as A. flavus was grown

had a detrimental effect on ducklings.

The production of ochratoxin by A. ochraceus Wilhelm

is well documented (Kellerman et al. 1988). The structure

of the mycotoxin has been determined by Van der Merwe

et al. (1965a, b), and Purchase & Theron (1968) illustrated

the acute toxicity of this fungus to rats.

Rabie et al. (1976) grew A. versicolor on various media

and at various temperatures to determine optimum produc-

tion of sterigmatocystin: when Aspergillus isolates ob-

tained from international culture collections were tested

for production of sterigmatocystin, A. aurantio-brunneus

(Atkins, Hindson & Russel) Raper & Fennell, A. quad-

rilineatus Thom & Raper and A. ustus gave positive

results (Rabie et al. 1977). The latter was a local isolate,

producing a low quantity of sterigmatocystin. The effect

it had could have been partly due to other toxins such as

ausdiol, which were not tested for.

A. clavatus produced a tremorgenic substance which

had a lethal effect on cattle and sheep (Kellerman et al.

1976). This fatal substance was produced by the fungus

when it was grown on malt sprouts as well as on sorghum

beer residue (Kellerman et al. 1984). In both cases the

toxin involved was unknown. The mycotoxins cyto-

chalasin E and K were isolated from an isolate of A.

clavatus (Steyn et al. 1982). The tremorgenic and lethal

effect of A. clavatus was illustrated with photographs by

Coetzer et al. (1985) and a similar report was given by

Kellerman et al. (1988).

Dutton & Westlake (1985) tested agricultural com-

modities for fungi and their toxins. They found A. flavus

and A. parasiticus in 22% of the samples whereas 27.2%

of samples yielded aflatoxin B 1 and often also B2, G 1

and G2. Westlake & Dutton (1985) reported on the in-

cidence of mycotoxins in the broiler industry and found

that aflatoxin may depress growth rates and could play a

role in poultry diseases.

Rabie (1986) reviewed contamination of foods by

toxigenic fungi and mycotoxins and discussed law-enfor-

cement problems. Rheeder et al. (1990) warned that

Aspergillus on maize grain should be monitored as it poses

a mycotoxological threat. Liibben (1992) tested various

isolates of fungi obtained from oats and wheat for toxicity

and found that several Aspergillus isolates tested positive.

All isolates that proved to be toxic in the above research

are indicated in the appended checklist with an asterisk

(*) preceding the reference.

Mutagenic activity of various secondary metabolites of

Aspergillus spp. has been indicated by Wehner et al.

(1978), Wehner et al. (1979a, b) and Kfir et al. (1986).

Extracellular enzyme production of Aspergillus spp. was

studied by McLean et al. ( 1985): A. flavus and A. candiclus

Link were found to be prolific enzyme producers. HPLC

determinations of aflatoxin B and G in groundnut seed,

indicated a 79. 1 % presence of A. parasiticus and 20.9%

of A. flavus (Labuschagne & Wehner 1990). McLean et

al. (1990) found that aflatoxin B1 is toxic to callus tissue

of maize.

The large number of references concerning work of a

chemical nature, is beyond the scope of this overview.

However, the following works serve as general references.

A symposium on mycotoxins (Anon. 1965) treated various

aspects of aflatoxin. Purchase & Theron (1967) gave a

comprehensive review of work on mycotoxins in South

Africa. Steyn (1980) summarised studies on secondary

metabolism, highlighting contributions by South African

scientists. The sixth International IUPAC Symposium on

Mycotoxins and Phycotoxins (Steyn & Vleggaar 1986)

was held in South Africa and two local papers on aflatoxin

were included. An update on the mycotoxins produced by

Aspergillus spp., is included in the work of Frisvad (1989).

DISCUSSION

The 25 commonly encountered species of Aspergillus

(Domsch et al. 1980) have all been recorded from

southern Africa, although of the estimated 170-200

described Aspergilli (Christensen & Tuthill 1985), only

72 or about 40% of species with Aspergillus anamorphs

have been traced and included in the checklist. Forty per

cent of all described Aspergillus spp. have been recorded

from single locations or are restricted in geographic dis-

tribution (Christensen & Tuthill 1985); so many probably

do not occur here. This may explain why such a relatively

low percentage of Aspergillus species have been recorded

from southern Africa.

It may be concluded that southern Africa, with its

varied climatic regions and some of the oldest geological

formations in the world, may be a source of Aspergillus

species differing from those already known. Most records

of Aspergilli here have been from foodstuffs, and little

information is available concerning the ecological adap-

tation of members of this genus to the diverse conditions

in this country. It is significant that on the arid Giribes

Plain of Namibia, the dominant genus isolated from soil

in the perplexing bare patches has been Aspergillus (Eick-

er et al. 1982). Unfortunately there is no indication how

many, if any, of those isolates were difficult to identify

and were consequently lumped under the heading ‘ Asper -

176

Bothalia 24,2 (1994)

gillus spp.' The same may be true for other surveys such

as those of Eicker (1969, 1970, 1974) and Papendorf

(1976), where unidentified Aspergilli were listed. A survey

of various ecological niches may prove to be a taxonomi-

cally rewarding undertaking and may yield potentially

useful but as yet undescribed species.

South African isolates of Aspergillus have been men-

tioned by authorities such as Thom & Church ( 1926), and

Raper & Fennel (1973) who described A. cristatus Raper

& Fennell on the basis of an isolate ‘received in 1954

from the CBS as H. Swart 168 isolated by H. Swart, S.

Africa’. Neither the authors of this fungus name, nor the

CBS catalogue (see checklist), indicated a substrate or

locality for this isolate. Swart’s (1959) writings however,

stated that his specimen No. 168 was isolated from

mangrove soil, collected on the island of Inhaca off

Maputo [Lourenfo Marques], Mozambique.

Although no local scientist has made a major contribu-

tion to the taxonomy of this group, much attention has

been paid to the detection and characterisation of

mycotoxins, and South Africans have become world

leaders in this field. A large number of references con-

cerning aflatoxin, a metabolite of A. flavus and A.

parasiticus, are available, but these have not been treated

here as they do not refer to specific fungal isolates. The

same goes for other mycotoxins such as austocystins,

ochratoxin and sterigrrlatocystin. It is of interest that

ochratoxin A, B, and C were characterised in South Africa

(Van der Merwe et al. 1965a, b), and their toxicity deter-

mined (Purchase & Theron 1968), but the toxins themsel-

ves have never been isolated here (Mantle & McHugh

1993).

Eicker (1975) found that A. aculeatus had an an-

tagonistic effect on both Staphylococcus and Candida.

Shortly afterwards a secondary metabolite of this fungus,

namely aculeacin A, was found to have strong activity

against filamentous fungi, as well as yeasts (Mizuno et

al. 1977). There may be other members of the group with

similar undetected beneficial characteristics.

Species of Aspergillus such as A. ochraceus K. Wilh.,

A. niger and A. terreus , but especially A. parasiticus, are

known insect pathogens (Domsch et al. 1980). Isolates

from arthropods have been recorded in southern Africa

(Prinsloo 1960), but their potential as agents in biological

control has not been investigated. Aspergillus spp. are

chemically very active and may even be valuable in the

control of plant pathogens.

The value of sophisticated chemical methods employed

by many Aspergillus taxonomists (Samson & Pitt 1985,

1990) as well as that of electron microscopy (Kozakiewicz

1989) has been indicated. They have become indispen-

sable in Hyphomycete taxonomy, but little attention has

been given to these methods in South Africa. Morphologi-

cal and physiological characteristics are almost the only

criteria by which Aspergillus is identified here. Although

this is still the most accessible way of taxonomic deter-

mination, the new techniques could become a powerful

tool in the hand of South African taxonomists.

It is clear that the field for workers on Aspergillus is

wide open, be it in industry, ecology, biological control,

biochemistry, the various pathology disciplines or by im-

plementing the modern methods available to the

taxonomist.

ACKNOWLEDGEMENTS

I thank Ms A. P. Baxter of the Plant Protection Re-

search Institute for kindly reviewing a draft of the

manuscript.

REFERENCES

ALLSOPP, N„ OLIVIER. D.L. & MITCHELL. D.T. 1987. Fungal

populations associated with root systems of proteaceous seedlings

at a lowland fynbos site in South Africa. South African Journal of

Botany 53: 365-369.

AL-MUSALLAM, A. 1980. Revision of the black Aspergillus species.

Ph.D. thesis, Utrecht.

ANON. 1965. Symposium on mycotoxins in foodstuff. Agricultural

aspects. Department of Agricultural Technical Services Technical

Communication No. 35: 1-60.

BAK, J.P. & WAGENFELD, D.J.H. 1983. Treatment of otitis externa

with miconazole nitrate. A comparative study involving 85 cases.

South African Medical Journal 63: 562, 563.

BENATAR, S.R. 1977. Aspergillus infection in the western Cape. South

African Medical Journal 5 1 : 297-305.

BENATAR, S.R., KEEN, G.A. & NAUDE, W. DU TOIT 1980. Aspergil-

lus hypersensitivity in asthmatics in Cape Town. Clinical Allergy

10:285-291.

BENJAMIN, C.R. 1955. Ascocarps of Aspergillus and Penicillium.

Mycologia 47 : 669-687.

BERKOWITZ, F.E. & JACOBS, D.W.C. 1987. Fatal case of brain

abscess caused by rooster pecking. Pediatric Infectious Disease

Journal 6: 941, 942.

BEZUIDENHOUT, H. 1977. 'n Ondersoek van die Hyphomycetes geas-

sosieer met Cenchrus ciliaris L. M.Sc. thesis. University of

Pretoria.

BLOCK, C.S. & YOUNG, C.N. 1977. Early diagnosis of opportunistic

systemic fungal and nocardial infections. South African Medical

Journal 52: 1056-1060.

BORNMAN, C.H. 1978. Welwitschia. Paradox of a parched paradise.

Struik Publishers, Cape Town.

BOSMAN, J.L., RABIE, C.J. & PRETORIUS, A.J. 1991. Fungi as-

sociated with high and low tannin sorghum grain in the Republic

of South Africa. Phytophylactica 23: 47-52.

BOTHA, W. & WEHNER, F.C. 1990. Biocontrol of citrus root pathogens

with induced fungal antagonists. Phytophylactica 22: 147

(Abstract).

BRESSAC, B„ KEW, M.. WANDS, J. & OZTURK, M. 1991. Selective

G to T mutations of p53 gene in hepatocellular carcinoma from

southern Africa. Nature 350: 429^43 1 .

CARO, I. & DOGLIOTTI. M. 1973. Aspergillosis of the skin. Report of

a case. Dennatologia 146: 244-248.

CHRISTENSEN, M. 1982. The Aspergillus ochraceus group: two new

species from western soils and a synoptic key. Mycologia 74:

210-225.

CHRISTENSEN, M. & TUTHILL. D.E. 1985. Aspergillus: an overview.

In R.A. Samson & .1.1. Pitt, Advances in Penicillium and Aspergil-

lus systematics. Plenum Press, New York.

COETZER, J.W.A., KELLERMAN, T.S. & NAUDE, T.W. 1985.

Neurotoxicoses of livestock caused by plants and fungi in South

Africa. Republic of South Africa Department of Agriculture and

Water Supply Technical Communication No. 199: 1-34.

COHEN, C. 1950. The occurrence of fungi in the soil, after different

burning and grazing treatments of the veld in the Transvaal. South

African Journal of Science 46: 260-264.

COOPER. D.K.C., LANZA, R.P., OLIVER, S„ FORDER, A.A., ROSE,

A.G., UYS, C.J., NOVITZKY, D. & BARNARD, C.N. 1983.

Infectious complications after heart transplantation. Thorax 38:

822-828.

DAVEL, H.B. & NEETHLING, H.L. 1930. Skimmels en Iml bestryding

in die melkery. Union of South Africa Department of Agriculture

Science Bulletin No. 80: 1-18.

Bothalia 24,2(1994)

177

DE VILL1ERS, J.C. 1989. Endofitiese fungusse teenwoordig in 'n aantal

Suid-Afrikaanse grasspesies. M.Sc. thesis, Potchefstroom

University for C.H.O.

DOIDGE, E.M. 1950. The South African fungi and lichens to the end of

1945. Bothalia 5: 1-1094.

DOIDGE, E.M., BOTTOMLEY, A.M., VAN DER PLANK, J.E. &

PAUER, G.D. 1953. A revised list of plant diseases in South

Africa. Union of South Africa Department of Agriculture Science

Bulletin No. 346: 1-125.

DOIDGE, E.M. & VAN DER PLANK, J.E. 1936. The fungi which cause

rots of stored citrus fruits in South Africa. Union of South Africa

Department of Agriculture and Forestry Science Bulletin No. 1 62:

1-23.

DOMSCH, K.H., GAMS, W. & ANDERSON, T-H. 1980. Compendium

of soil fungi. Academic Press, London.

DUTTON, M.F. & WESTLAKE, K. 1985. Occurrence of mycotoxins in

cereals and animal feedstuffs in Natal, South Africa. Journal of

the Official Analytical Chemists 68: 839-842.

EICKER, A. 1969. Microfungi from surface soil of forest communities in

Zululand. Transactions of the British Mycological Society 53:

381-392.

EICKER, A. 1970a. Ecological observations on soil fungi. South African

Journal of Science 66: 327-334.

EICKER, A. 1970b. Vertical distribution of fungi in Zululand soils.

Transactions of the British Mvcological Society 55: 45-57.

EICKER, A. 1972. Occurrence and isolation of South African ther-

mophilic fungi. South African Journal of Science 68: 150-155.

EICKER, A. 1973. The mycoflora of Eucalyptus maculata leaf litter. Soil

Biology and Biochemistry 5: 441^148.

EICKER, A. 1974. The mycoflora of an alkaline soil of the open-savan-

nah of the Transvaal. Transactions of the British Mvcological

Society 63: 281-288.

EICKER, A. 1975. A survey of the antimycotic and antibacterial activity

of soil microfungi from Transvaal. Journal of South African

Botany 41: 187-198.

EICKER. A. 1976. Non-parasitic mycoflora of the phylloplane and litter

of Panicum coloratum. Transactions of the British Mvcological

Society 61: 275-281.

EICKER, A. 1977. Thermophilic fungi associated with the cultivation of

Agaricus bisporus (Lange) Singer. Journal of South African

Botany AS: 193-207.

EICKER, A. 1980. Mesophilic fungi associated with cultivation of

Agaricus brunnescens. Transactions of the British Mvcological

Society 74: 465^-70.

EICKER, A„ THERON. G.K. & GROBBELAAR, N. 1982. ’n Mik-

robiologiese studie van ‘kaal kolle’ in die Giribesvlakte van

Kaokoland, S.W.A.-Namibie. South African Journal of Botany 1:

69-74.

FINDLAY, G.H., ROUX, H.F. & SIMPSON, I.W. 1971. Skin manifesta-

tions in disseminated aspergillosis. British Journal of Dermatol-

ogy 85, Supplement 7: 94—97.

FITZSIMONS, R. & PETERS, A.L. 1986. Miconazole and ketoconazole

as a satisfactory first-line treatment for keratomycosis. American

Journal of Opthalmology 101: 605-608.

FRISVAD, J.C. 1989. The connection between the Penicillia and Asper-

gilli and mycotoxins with special emphasis on misidentified iso-

lates. Archives of Environmental Contamination and Toxicology

18:452^167.

GAMS, W. & SAMSON, R.A. 1985. Typification of Aspergillus and

related teleomorphs. In R.A. Samson & J.I. Pitt, Advances in

Penicillium and Aspergillus systematics. Plenum Press, New

York.

GILMAN, G.A. 1972. Report of a survey of food storage and handling

techniques used in eastern Transvaal and Swaziland with special

reference to fungal contamination in the diet and the incidence of

liver cancer in man, Feb. 1968-Dec. 1971. R397: 1-126. Tropi-

cal Products Institute, Ministry of Overseas Developement, Lon-

don.

GLASS, R.B.J, HERTZANU. Y„ MENDELSOHN, D.B. & POSEN, J.

1984. Paranasal sinus aspergillosis. A case report with computed

tomogram findings. Journal of Laryngology and Otology 98:

199-205.

GORTER. G.J.M.A. 1977. Index of plant pathogens and the diseases they

cause in cultivated plants. Department of Agricultural Technical

Sevices Science Bulletin No. 329: 1-177.

GORTER, G.J.M.A. 1979. An annotated checklist and selected bibliog-

raphy of South African fungi for the period 1946-1977. Republic

of South Africa Department of Agricultural Technical Services

Technical Communication No. 163: 1-34.

GOVENDER, S„ RAJOO, R.. GOGA, I.E. & CHARLES, R.W. 1991.

Aspergillus osteomyelitis of the spine. Spine 16: 746-749.

HOLZAPFEL, C.W., PURCHASE, I.F.H., STEYN, PS. & GOUWS, L.

1966. The toxicity and chemical assay of sterigmatocystin, a

carcinogenic mycotoxin, and its isolation from two new fungal

sources. South African Medical Journal 40: 1100, 1101.

HOR1E, Y. 1980. Ascospore ornamentation and its application to the

taxonomic re-evaluation in Emericella. Transactions of the

Mycological Society of Japan 21: 483^193.

ISAACS, J. & BENIC, L.M. 1990. A study of the fungal mycoflora

associated with stored seeds of eight indigenous families.

Phytophylactica 22: 154 (Abstract).

ISAACSON, C. 1966. The aetiology of cirrhosis and hepatoma in the

bantu — an appraisal. South African Medical Journal 40: 1 1-13.

JACOBS. R, FRIEDBERG, E.C. & VAN NIEKERK, V. 1965. Pul-

monary aspergillosis in a white South African farmer. The Central

African Journal of Medicine 1 1 : 155-160.

JAIN, PC. & LACEY, J. 1991. Use of API-Zym strips and 4-nitrophenyl

substrates to detect and quantify hydrolytic enzymes in media and

grain colonized with Asperigillus, Eurotium and Penicillium

species. Mycological Research 95: 834—842.

JOUBERT, J.R., BRINK, S. & HENTZEN, G.M. 1988. Allergic asthma

in different population groups in the western Cape. Causative and

complicating factors. South African Medical Journal 73: 150-

154.

KALLENBACH, J., DUSHEIKO. J. BLOCH. C.S., BETHLEHEM, B„

KOORNHOF, H.J. & ZW1, S. 1977. Aspergillus pneumonia — a

cluster of four cases in intensive care unit. South African Medical

Journal 52: 919-923.

KELLERMAN, T.S., COETZER, J.A.W & NAUDE. T.W. 1988. Plant

poisonings and mycotoxicosis of livestock in southern Africa.

Oxford University Press, Cape Town.

KELLERMAN, T.S., NEWSHOLME, S.J., COETZER, J.A.W. & VAN

DER WESTHUIZEN, G.C.A. 1984. A tremorgenic

mycotoxicosis of cattle caused by maize sprouts infested with

Aspergillus clavatus. Onderstepoort Journal of Veterinary Re-

search S\: 21 \-21 A.

KELLERMAN. T.S., PIENAAR, J.G., VAN DER WESTHUIZEN,

G.C.A. , ANDERSON, L.A.P. & NAUDE, T.W. 1976. Highly

fatal tremorgenic mycotoxicosis of cattle caused by Aspergillus

clavatus. Onderstepoort Journal of Veterinary Research 43: 147—

154.

KFIR, R„ JOHANNSEN. E. & VLEGGAAR. R. 1986. Mutagenic ac-

tivity of austocystins — secondary metabolites of Aspergillus

ustus. Bulletin of Environmental Contamination and Toxicology

37: 643-650.

KLICH, M.A. & PITT, J.I. 1988. Differentiation of Aspergillus flavus

from A. parasiticus and other closely related species. Transac-

tions of the British Mycological Society 91 : 99-108.

KOZAKIEWICZ, Z. 1989. Aspergillus species on stored products.

Mycological Papers Ho. 161: 1-188.

KURTZMAN, C.P., SMILEY. M.J., ROBNETT. C.J. & WICKLOW,

D.T. 1986. DNA relatedness among wild and domesticated

species in the Aspergilus flavus group. Mycologia 78: 955-959.

LABUSCHAGNE, C.L.E. & WEHNER, F.C. 1990. The occurrence of

Aspergillus flavus and A. parasiticus on certified groundnut seed

in South Africa. Phytophylactica 22: 158 (Abstract).

LAMPRECHT, S.C., KNOX-DAVIES, PS. & MARASAS, W.F.O. 1988.

Fungi associated with root rot of annual Medicago spp. in South

Africa. Phytophylactica 20: 281-286.

LE ROUX, G„ ESCHENBRUCH, R. & DE BRUIN, S.I. 1973. The

microbiology of South African wine-making. Part 8. The

microflora of healthy and Botrytis cinerea infected grapes.

Phytophylactica 5: 51-54.

LEWIS, M., KALLENBACH, J., RUFF, P, ZALTZMAN, M„

ABRAMOW1TZ, J. & ZWI, S. 1985. Invasive pulmonary asper-

gillosis complicating influenza. A pneumonia in a previously

healthy patient. Chest 87: 691-693.

LUBBEN, A. 1992. Die insidensie en toksisiteit van fungi in koring- en

hawergraan in die RSA. M.Sc thesis, University of Pretoria.

LUCK, H. & WEHNER, F.C. 1979. Mycotoxins in milk and dairy

products. South African Journal of Dairy Technology 11: 169 —

176.

LUCK, H., WEHNER, F.C., PLOMP, A & STEYN, M. 1976.

Mycotoxins in South African cheeses. South African Journal of

Dairy Technology 8: 107-110.

LUNDQUIST, J.E. 1987. Fungi associated with Pinus in South Africa.

Part 2. The Cape. South African Forestry Journal 140: 4-15.

LUNDQUIST, J.E. & BAXTER, A.P 1985. Fungi associated with

Eucalyptus in South Africa. South African Forestry Journal 135:

9-19.'

178

Bothalia 24,2 (1994)

MANTLE, P.G. & McHUGH, K.M. 1993. Nephrotoxic fungi in foods

from nephropathy households in Bulgaria. Mycological Research

97: 205-212.

MARASAS, W.F.O. 1988. Medical relevance of mycotoxins in southern

Africa. Microbiologie Aliments Nutrition 6: 1-5.

MARASAS, W.F.O. & BREDELL, I.H. 1973. Mycoflora of South

African lucerne ( Medicago saliva L.) seed. Phytophylactica 5:

89-94.

MARASAS, W.F.O. & VAN RENSBURG, S.J. 1986. Mycotoxicological

investigations on maize and groundnuts from the endemic area of

Mseleni joint disease in Kwazulu. South African Medical Journal

69: 369-374.

MARASAS, W.F.O., WEHNER, F.C., VAN RENSBURG, S.J. & VAN

SCHALKWYK, D.J. 1981. Mycoflora of corn produced in

human oesophageal cancer areas in Transkei, southern Africa.

Phytopathology 71: 792-796.

MARTIN, J.P. I960. Fungi and nematodes in South African citrus orchard

soils in relation to the citrus replant problem. Soil Science Society

of America Proceedings 24: 469^472.

MARTIN, P.M.D. & BERSON, S.D. 1973. Fungus diseases in southern

Africa. Mycopathologia et Mycologia Applicata 50: 1-84.

MCLEAN. M, & BERJAK, P. 1987. Maize grains and their associated

mycoflora — a micro-ecological consideration. Seed Science and

Technology 15: 831-850.

MCLEAN, M„ MYCOCK, D.J. & BERJAK, P. 1985. A preliminary

investigation of extracellular enzyme production by some species

of Aspergillus. South African Journal of Botany 5 1 : 425^13 1 .

MCLEAN, M„ WATT. M.P., BERJAK. P. & DUTTON, M.F. 1990.

Maize callus — a tool for studying the effects of aflatoxin B1 on

plant cells. Phytophylactica 22: 150 (Abstract).

MIZUNO, K„ YAGI, A., SATOI, S„ TAKADA, M„ HAYASHI, M„

ASANO, K. & MATSUDA, T. 1977. Studies of aculeacin. 1.

Isolation and characterization of aculeacin A. The Journal of

Antibiotics 30: 297-302.

MYCOCK, D.J. & BERJAK, P. 1990. Fungal comtaminants associated

with several homoiohydrous (recalcitrant) seed species.

Phytophylactica 22: 413-418.

MYCOCK, D.J. & BERJAK, P. 1992. Intraseminal fungal location in

maize of selected seed storage fungi in relation to some

physiological parameters. South African Journal of Botany 58:

139-144.

MYCOCK, D.J., RIJKENBERG, F.H.J. & BERJAK, P. 1990. Infection

of maize seedlings by Aspergillus flavus var. columnaris var. nov.

‘Seed Science and Technology 18: 693-701.

NEITZ, W.O. 1965. A checklist and host-list of the zoonoses occurring in

mammals and birds in South and South West Africa.

Onderstepoort Journal of Veterinary Research 32: 189-374.

NESBIT, J.W. 1986. The pathology of pulmonary aspergillosis in a piglet.

Journal of the South African Veterinary Association 57: 125-127.

ORDMAN, D. 1963. The airborne fungi in Johannesburg. A second

five-year survey: 1955-1959. South African Medical Journal 37:

325-328.

ORDMAN, D. 1970. Seasonal respiratory allergy in Windhoek: the pol-

len and fungus factors. South African Medical Journal 44: 250-

253.

ORDMAN, D. & ETTER, K.G. 1956. The airborne fungi in Johannes-

burg. A five-year survey as a basis for the study of fungus allergy

in South Africa. South African Medical Journal 30: 1054—1058.

PAPENDORF, M.C. 1976. The soil mycoflora of an Acacia karroo

community in western Transvaal. Bothalia 12: 123-127.

PEERS, F.G., GILMAN, G.A. & LINSELL, C.A. 1976. Dietary

aflatoxins and human liver cancer. A study in Swaziland. Interna-

tional Journal of Cancer 17: 167-176.

PETERSON, S.W. 1992. Neosartorya pseudqfischeri sp. nov. and its

relationship to other species in Aspergillus section Fumigati.

Mycological Research 96: 547-554.

PITT, J.I. & SAMSON, R.A. 1990. Approaches to Penicillium and Asper-

gillus systematics. Studies in Mycology 32: 77-90.

PITT, J.I. & SAMSON, R.A. 1993. Species names in current use in the

Trichocontaceae (Fungi, Eurotiales). In W. Greuter, Names in

current use in the families Trichocomaceae, Cladoniaceae,

Pinaceae, and Lerrmaceae. Koeltz Scientific Books, Germany.

POTTER, PC., JURWITZ, J„ LITTLE, F„ McCALDIN, M. &

DOWDLE, E.B. 1991. Clustering of fungal allergen-specific IgE

antibody responses in allergic subjects. Annals of Allergy 66:

149-153.

PRETORIUS, W.A. & LEMPERT, G.G. 1993a. The selective cultivation

of the thermololerant Aspergillus sp. on spent sulphite liquor.

Water SA 19:69-72.

PRETORIUS, W.A. & LEMPERT, G.G. 1993b. Growth characteristics of

Aspergillus sp. grown on spent sulphite liquor. Water SA 19:

73-76.

PRETORIUS, W.A. & LEMPERT, G.G. 1993c. Biomass production of

Aspergillus fumigatus on spent sulphite liquor under non-aseptic

conditions. Water SA 19: 77-80.

PRINSLOO, G.C., BAARD, S.W. & FERREIRA, J.F. 1991. Organisms

associated with black root rot of chicory in South Africa.

Phytophylactica 23: 59-67.

PRINSLOO, H.E. 1960. Parasitiese mikro-organismes by die bruin-

sprinkaan Locustana pardalina (Walk.). South African Journal of

Agricultural Science 3: 551-560.

PROZESKY. O.P.M., BUYS, S.B., VAN DER MADE, H.N., DE WET,

P.J. & BROWN, J.J.M. 1971. Aspergillus fumigatus infection in

scaly weaver ( Sporopipes squamifrons). Journal of the South

African Veterinary and Medical Association 42: 175-178.

PURCHASE, I.F.H. & THERON, JJ. 1967. Research on mycotoxins in

South Africa. International Pathology 8: 3-6.

PURCHASE, I.F.H. & THERON, J.J. 1968. The acute toxicity of

ochratoxin A to rats. Food and Cosmetic Toxicology 6: 479- 483.

PURCHASE, I.F.H. & VORSTER, L.J. 1968. Aflatoxin in commercial

milk samples. South African Medical Journal 42: 219.

RABIE, C.J. 1986. Mikotoksienprobleme in Suid-Afrikaanse voed-

selkommoditeite. Suid-Afrikaanse Tydskrif vir Natuurwetenskap

en Tegnologie 5: 151-153.

RABIE, C.J., DE KLERK, W.A. & TERBLANCHE, M. 1964. Toxicity

of Aspergillus amstelodami to poultry and rabbits. South African

Journal of Science 7: 314-346.

RABIE, C.J. & LUBBEN, A. 1984. The mycoflora of sorghum malt.

South African Journal of Botany 3: 251-255.

RABIE, C.J., LUBBEN, A. & STEYN, M. 1976. Production of sterig-

matocystin by Aspergillus versicolor and Bipolaris sorokiniana

on semisynthetic liquid and solid media. Applied and Environ-

mental Microbiology 32: 206-208.

RABIE, C.J., STEYN, M. & VAN SCHALKWYK, G.C. 1977. New

species of Aspergillus producing sterigmatocystin. Applied and

Environmental Microbiology 33: 1023-1025.

RABIE, C.J., STEYN, P.S. & VAN HEERDEN, F.R. 1986. The isolation

and identification of some toxic constituents of Aspergillus wentii

Wehmer. Mycotoxin Research 2: 19-24.

RABIE, C.J. & TERBLANCHE, M. 1967. Influence of temperature on

the toxicity of different isolates of Aspergillus wentii Wehm.

South African Journal of Agricultural Science 10: 263-266.

RABIE, C.J., TERBLANCHE, M„ SMIT, J.D. & DE KLERK, W.A.

1965. Toxicity of Aspergillus wentii Wehmer. South African Jour-

nal of Agricultural Science 8: 875-880.

RAPER, K.B. & FENNELL, D.I. 1973. The genus Aspergillus. Krieger

Publishing Company, New York.

RHEEDER, J.P., MARASAS, W.F.O., VAN WYK, P.S., DU TOIT, W„

PRETORIUS, A.J. & VAN SCHALKWYK, D.J. 1990. Incidence

of Fusarium and Diplodia species and other fungi in naturally

infected grain of South African maize cultivars. Phytophylactica

22: 97-102.

ROSSELET, F. 1953. Aspergillus niger as a test organism for measuring

plant available potassium in lowveld soils. South African Journal

of Science 50: 344—347.

ROSSELET, F. 1955. Bio-assay of P, K and Mg in citrus fertilizer plots

using Aspergillus niger. South African Journal of Science 5 1 :

331-335.

ROTH, G. 1963. Post harvest decay of litchi fruit. Republic of South

Africa Department of Agricultural Technical Services Technical

Communication No. 11: 1-16.

ROTH, G. 1968. Biological treatment of molasses meal to reduce sticki-

ness. Proceedings of the South African Sugar Technologists' As-

sociation April: 57-64.

ROTH, G. & LOEST, F.C. 1965. Collar rot of banana hands and its

associated micro-organisms. Republic of South Africa Depart-

ment of Agricultural Technical Services Technical Communica-

tion No. 44: 1-14.

ROUX, C. 1985. The morphology and taxonomy of some fungi selected

from a survey of a natural Karoo pasture. Ph.D. thesis, Rand

Afrikaans University.

RUSSELL, A.E. 1981. Protection of wet-blue leathers against fungal

growth. Liri Research Bulletin No. 813: 1-14.

SACHO, H„ STEAD, K.J., KLUGMAN, K.P. & LAWRENCE, Z. 1987.

Infection of the human orbit by Aspergillus stromatoides.

Mycopathologia 97: 97-99.

SAMSON, R.A. 1979. A compilation of the Aspergilli described since

1965. Studies in Mycology No. 18: 1-38.

SAMSON, R.A. & GAMS. W. 1985. Typification of the species of

Aspergillus and associated teleomorphs. In R.A. Samson &

Bothalia 24,2 (1994)

179

J.l. Pitt, Advances in Penicillium and Aspergillus systemaiics.

Plenum Press, New York.

SAMSON, R.A. & PITT, J.l. 1985. Advances in Penicillium and Asper-

gillus systematics. Plenum Press, New York.

SAMSON, R.A. & PITT, J.l. 1990. Modem concepts in Penicillium and

Aspergillus classification. Plenum Press, New York.

SCOTT, D.B. 1965. Toxigenic fungi isolated from cereal and legume

products. Mycopathologia et Mycologia Applicata 25: 213-222.

SMIT, M. 1984. ’n Studie van verskdlende deklaagmateriale in die

kommersiele verbouing van Agaricus brunnescens Peck. M.Sc.

thesis. University of Pretoria.

STEINKE, T.D., BARNABAS, A.D. & SOMARU, R. 1990. Structural

changes and associated microbial activity accompanying decom-

position of mangrove leaves in Mgeni Estuary. South African

Journal of Botany 56: 39 — 48.

STEYN, P.S. 1980. The biosynthesis of mycotoxins. A study in secondary

metabolism. Academic Press, New York, London.

STEYN, P.S., VAN HEERDEN, F.R. & RAB1E, C.J. 1982. Cytochalasins

E and K, toxic metabolites from Aspergillus clavatus. Journal of

the Chemical Society Perkin 1 2: 541-544.

STEYN, P.S. & VLEGGAAR, R. 1986. Mycotoxins and phycotoxins.

Papers presented at the sixth International IUPAC Symposium.

Elsevier, Amsterdam.

SWART, H.J. 1959. Observations on fungus cultures from the collection

in the Botany Department of the University of the Witwatersrand.

2. Some ascosporic species of Aspergillus. South African Journal

of Science 55: 51-53.

THIEL, P.G. 1986. Mikotoksiene en gesondheidsrisiko's. Tydskrif vir

Natuurwetenskap en Tegnologie 5: 154-156.

THOM, C. & CHURCH. M.B. 1926. The Aspergilli. Baltimore, Williams

& Wilkins.

TIEDT, L.R. 1992. Conidiogenesis in Aspergillus niger. Thirtieth annual

congress of the South African Society for Plant Pathology.

Phytophylactica 24: 127 (Abstract).

VAN DER BIJL, P.A. 1920. Studies on some fungi and the deterioration

of sugar. Union of South Africa Department of Agriculture

Science Bulletin No. 18: 1-19.

VAN DER MERWE, K.J., STEYN, P.S. & FOURIE, L. 1965a.

Mycotoxins Part 2. The constitution of ochratoxin A, B and C,

metabolites of Aspergillus ochraceus Wilh. Journal of the Chemi-

cal Society December 1965: 7083-7088.

VAN DER MERWE, K.J., STEYN, P.S., FOURIE, L„ SCOTT, D.B. &

THERON, J.J. 1965b. Ochratoxin A, a toxic metabolite produced

by Aspergillus ochraceus Wilh. Nature 205: 1112, 1113.

VAN DER MERWE. W.J.J., EICKER. A., MARASAS, W.F.O. & KEL-

LERMAN, T.S. 1979. Aerospora of an Eragrostis curvula pasture

in South Africa. Onderstepoort Journal of Veterinary Research

46: 19-25.

VAN DER WESTHUIZEN, G.C.A. & BREDELL, I.H. 1972. The fungus

flora of high quality stored maize in South Africa, 1966-1972.

Final Report. Republic of South Africa, Department of Agricul-

tural Technical Services. Unpublished.

VAN WARMELO, K.T. 1967. The fungus flora of stock feeds in South

Africa. Onderstepoort Journal of Veterinary Research 34: 439-

450.

VAN WARMELO, K.T., VAN DER WESTHUIZEN, G.C.A. & MIN-

NIE, J.A. 1968. The production of aflatoxins in naturally infected

high quality maize. Republic of South Africa, Department of

Agricultural Technical Services, Technical Communication No.

71: 1-5.

VERWOERD, L. 1929. A preliminary checklist of diseases of cultivated

plants in the winter rainfall area of the Cape Province. Union of

South Africa, Department of Agricultural Science Bulletin No.

88: 1-18.

WATSON, R.T., ANELICH, R. & SCHUTTE, A.L. 1990. Fungi in the

gut contents of Namib Desert dune Lepismatidae (Thysanura:

Insecta). Madoqua 17: 53, 54.

WEHNER, F.C., BESTER, S„ KOTZE, J.M. & BRODRICK, H.T. 1981.

Fungi associated with post-harvest decay of mangoes in South

Africa. South African Mango Grower's Association Research

Report 2: 81-88.

WEHNER, F.C. & RABIE, C.J. 1970. The micro-organisms in nuts and

dried fruits. Phytophylactica 2: 165-170.

WEHNER, F.C., THIEL, P.G. & DU RAND. M. 1979a. Mutagenicity of

the mycotoxin emodin in the Salmonella/microsome system. Ap-

plied and Environmental Microbiology 37: 658-660.

WEHNER. F.C., THIEL, S.J., VAN RENSBURG, S.J. & DEMASIUS,

I. PC. 1978. Mutagenicity to Salmonella typhimurium of some

Aspergillus and Penicillium mycotoxins. Mutation Research 58:

193-203.

WEHNER, F.C., THIEL, P.G. & VLEGGAAR, R. 1979b. Mutagenicity

of 5,6-dimethoxysterigmatocystine, a metabolite from Aspergil-

lus multicolor, in the Salmonella! microsome system. Applied and

Environmental Microbiology 38: 1015-1017.

WEIDEMAN, H„ OPPERMAN, L. & WEHNER, F.C. 1990. Micro-

organisms antagonistic to Rhizoctonia solani causing crater dis-

ease of wheat in soils of the Springbok Flats. Phytophylactica 22:

154 (Abstract).

WESTLAKE, K. & DUTTON, M.F. 1985. The incidence of mycotoxins

in litter, feeds, and livers of chickens in Natal. South African

Journal of Animal Science 15: 175- 177.

CHECKLIST OF ASPERGILLUS, CHAETOSARTORYA, EMERICELLA, EUROPIUM, FENNELL1A. NEOSARTORYA (= SARTORYA)

AND SCLEROCLE1STA RECORDED IN SOUTHERN AFRICA

Aspergillus spp. recorded in southern Africa up to 1 993 are arranged alphabetically and the host and/or substrate from which each species was recorded

is given with the relevant literature reference. Species names as well as substrates are listed as cited in the original publications. To update the

nomenclature, cross references to names currently accepted are given and Samson (1979), Horie (1980), Samson & Gams (1985), Samson & Pitt

(1985, 1990), Kozakiewicz (1989) as well as Pitt & Samson (1993) were consulted. Aspergillus is essentially an anamorphic genus but until recently

anamorphic as well as teleomorphic states were grouped under this genus. These two states have now been separated and are therefore listed separately:

Aspergillus spp. followed by the teleomorphic genera in alphabetical order. In some cases there is more than one reference, or additional culture

collection numbers for the same isolate: these are given in square brackets.

The following abbreviations are used in the list:

CBS, South African isolates listed in the 1990 List of Cultures of the Centraalbureau voor Schimmelcultures, 32nd edition, Baam, The Netherlands.

IMI, cultures listed in the 1992 Catalogue of the Culture Collection, 10th edition, CAB International Mycological Institute, Kew, United Kingdom.

PPRI, isolates in the Culture Collection of the National Collection of Fungi. Isolates identified or verified by Z. Lawrence (nee Kozakiewicz) of the

IMI (pers. comm.) are indicated as ver. Z.L. IMI.

PREM, dried material in the National Collection of Fungi. Those specimens that were identified by the CBS are indicated.

The National Collection of Fungi has acquired additional fungal collections over the years. Aspergillus isolates in these collections (many no longer

viable) are listed under the following abbreviations:

CSIR, isolates listed in a collection received from the Council for Scientific and Industrial Research.

MCP, the collection of Papendorf (1979) received from the University of Pochefstroom for C.H.E. Isolates are listed under the substrate soil, but

some could have been from Acacia karroo litter.

TRL, a collection of the Transvaal Chamber of Mines, some isolates determined by Thom, as listed by Doidge (1950).

UCT, a collection obtained from the University of Cape Town containing isolates of Allsopp et aL (1987).

VdB, records in the Van der Bijl collection which is administered by the National Collection of Fungi; some are mentioned by Van der Bijl (1920).

# State of the fungus uncertain.

* Aspergillus species indicated as toxic.

180

Bothalia 24,2 ( 1994)

GENUS ASPERGILLUS

aculeatus (see A. japonicus)

allahabadii B.S. Mehrotra & Agnihorti

litter: Eicker (1973)

soil: Eicker (1969, 1970a, b)

alliaceus Thom & Church

aerospora: IMI 087 209

cereals and legume products: Scott (1965)

grass litter: PPRI 3638

Medicago spp.: Lamprecht et al. (1988) [PREM 48323, 48324]

soil: PPRI 3185 [PREM 49038]; CSIR 556

alutaceus (see A. ochraceus)

ambiguus Sappa

Zea mays : Van der Westhuizen & Bredell (1972)

amstelodami (see Eurotium amstelodami)

avenaceus G. Sm.

cereals and legume products: *Scott (1965)

cornmeal: CBS 237.65

soil: CSIR 826

awamori Nakaz.

aeropsora: PPRI 4098

grass hay: Van Warmelo (1967)

groundnut hay: Van Warmelo (1967)

lucerne hay: Van Warmelo (1967)

maize hay: Van Warmelo (1967)

swine meal: Van Warmelo (1967)

caespitosus Raper & Thom

Zea mays : Van der Westhuizen & Bredell (1972)

campestris M. Chr.

mouse nest material: PPRI 4080 [PREM 50885, ver. Z.L. IMI 344 489]

candidus Link

Avena sativa : *Liibben (1992)

cereals and legume products: Scott (1965)

cheese: Doidge (1950)

cotton wool: PPRI 3841

maize meal: Van Warmelo (1967)

man: Martin & Berson (1973)

mouse nest material: PREM 50887

pasture: Roux (1985)

peanut butter/meal/kemels: Gilman (1972)

peat: Smit (1984)

soil: PPRI 4081 [id. Z.L. IMI 344 490], 4518; CSIR 113, 114, 115,

116 [PREM 49364]

sorghum: CSIR 544

sorghum malt: Rabie & Liibben (1984)

swine meal: Van Warmelo (1967)

Zea mays'. Gilman (1972); McLean & Berjak (1985); Van der West-

huizen & Bredell (1972); Van Warmelo et al. (1968); PPRI

3713 [PREM 49889]

carbonarius (Bainier) Thom

Eucalyptus spp. Lundquist & Baxter (1985) |PPR1 3776, PREM 47143]

undetermined host: IMI 138 280 [CBS 111.80]

Vitis vinifera : Doidge (1950) [Doidge et al. (1953); Gorter (1977)]

cameus Blochwitz

cereals and legume products: *Scott (1965)

leather: PPRI 3635

peat: Smit (1984)

soil: Eicker(1974, 1975); Eicker et al. (1982); Papendorf (1976) |MCP

131, 133, PPRI 3636]; CSIR 239, 240, 241, 243

undetermined host: CSIR 1208, 1210, 1211 [PPRI 3570, PREM 49363]

cervinus Massee

litter: Eicker (1973)

soil: UCT [PPRI 3284]

chevalieri (see Eurotium chevalieri)

chevalieri var. intermedius (see Eurotium cristatum)

clavatoflavus Raper & Fennell

man: Martin & Berson (1973)

clavatus Desm.

Avena sativa: Liibben (1992)

cereals and legume products: *Scott (1965)

compost: Eicker (1980)

grass roots: PREM 49066

Hordeum vulgare: PREM 47911

maize sprouts: *Kellerman et al. (1984)

peanut butter/meal/kemels: Gilman (1972)

soil: CSIR 133; MCP 1302

sorghum: CSIR: 304, 519, 520

sorghum beer residue: *Coetzer et al. (1985); *Kellerman et al. ( 1 976);

PREM *44972, 45108

sorghum malt : Rabie & Liibben (1984); Steyn et al. (1982)

Zea mays: Van der Westhuizen & Bredell (1972); PREM 44702, 44708,

45046, 48598; CSIR 61, 519, 520

cremeus (see Chaetosartorya cremea)

cristatus (see Eurotium cristatum)

duricaulis Raper & Fennell

Hakea sericea roots: Allsopp et al (1987)

Leucospennum parile roots: Allsopp et al. (1987)

soil: All sop et al. (1987) [UCT]

eburneus (see Fennellia nivea)

echinulatus (see Eurotium echinulatum)

effusus (see A. oryzae)

elegans Gasperini

lucerne hay: Van Warmelo (1967)

maize hay: Van Warmelo (1967)

ficuum (see A. niger var. ticuum)

fischeri (see Neosartorya Fischeri)

fischeri var. glaber (see Neosartorya glabra)

fischeri var. spinosus (see Neosartorya spinosa)

tlavipes (see Fennellia flavipes)

flavus Link

aerospora: Doidge (1950); IMI 089 137

agricultural commodities: Dutton & Westlake (1985)

apricot: Klich & Pitt (1988)

Arachis hypogaea: Anon. (1965); Gorter ( 1977); Marasas & Van Rens-

burg (1986)

Avena sativa: *Liibben (1992)

Avicennia seeds: PREM 47526

barley: Klich & Pitt (1988)

beer: Martin & Keen (1978)

biltong: CSIR 1413 [PREM 47906], 1414 [PREM 47908]

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: *Scott (1965)

chicken feeds and litter: Westlake & Dutton (1985)

coconut matting: ; PREM 33293 [TRL det. CBS]

Cussonia paniculata seed: PPRI 3643

debris: PPRI 3200

face cream: PPRI 3273, 3274, 3275, 3276, 3277, 3278

fenugreek: Klich & Pitt (1988)

flannel bag: Doidge (1950) [TRL det. Thom]

fodder: PREM 43024, 47799

foodstuff: Marasas (1988); Purchase & Vorster (1968)

grapes: Le Roux et al. (1973)

grass hay: Van Warmelo (1967)

groundnut seeds/hay: Labuschagne & Wehner (1990); Van Warmelo

(1967)

insects (dead Chrysomelidae spp.): PPRI 5062

Litchi chinensis: Roth (1963)

litter: Eicker (1973)

lucerne hay: Van Warmelo (1967)

maize meal/silage: Van Warmelo (1967)

malt: Klich & Pitt (1988)

man: Martin & Berson (1973)

manure: PPRI 3475 [PREM 49335]

material: Doidge (1950)

molasses meal: Roth (1968)

natural gum: Roth (1968)

nuts/dried fruit: *Wehner & Rabie (1970)

Nicotiana tabacum: Doidge (1950)

Bothalia 24,2(1994)

181

oats: Klich & Pitt (1988)

paper: PPRI 3644

pasture: Roux (1985)

peanut: Klich & Pitt (1988)

peanut butter/meal/kemels: Gilman (1972)

sclerotia (Sclerotinia sclerotionim ): PREM 47228

soil: Allsop et al. (1987); Eicker (1969, 1970a, 1974, 1975) [PREM

44262]; Papendorf (1976); Weideman el al. (1990); CSIR, 203,

204. 205, 209, 211, 212, 213, 215, 216, 217, 222, 223, 224,

225, 229, 231, 237

sorghum: CSIR 299

sorghum malt: Rabie & Liibben (1984)

sugar cane cariopsis: PREM 47532

sunflower hay: Van Warmelo (1967)

sunflower seed: Klich & Pitt (1988)

swine meal: Van Warmelo (1967)

termite comb ( Macrotermes bellicosus ): Doidge (1950) [PREM 1 253 1

termites (dead Hodotermes mossambicus ): PPRI 3753

Triticum aestivum: Liibben (1992)

Zea mays: Gilman (1972); Marasas & Van Rensburg (1986); McLean

& Beijak (1985, 1987); Mycock et al. (1990); Van der West-

huizen & Bredell (1972); Van Warmelo et al. (1968); PREM

44927, 44952, 47530, 47552, 47553; CSIR 57, 63, 136, 146,

283, 500, 501, 508, 515, 776, 840, 843, 848, 851, 852, 856,

857

= flavus var. colwrmaris Raper & Fennell

compost: Eicker (1980)

cornmeal: CBS 242.65

soil; CSIR 147, 151; MCP 49

sorghum malt: Rabie & Liibben (1984)

Zea mays: Mycock et al. (1990): PREM 47529

flavus var. columnaris (see A. flavus)

foetidus Thom & Raper

Allium cepa: PPRI 4046 [PREM 49175]

leather: PREM 48031

fumigatus Fresen.

aerospora: Roth (1968)

antigen of: Benatar et al. (1980)

Avena sativa: Liibben (1992)

bagasse: PPRI 4975

birds: Doidge (1950)

‘blesbok’ dung (Damaliscus dorcas phillipsii): Eicker (1972)

cereals and legume products: *Scott (1965)

compost: Smit (1984); PPRI 3477 [PREM 49330], 3479 [PREM

42090]

duck (Anatidae spp.): Doidge (1950)

faeces of Cape sparrow ( Passer melanurus ): Eicker (1972)

fowl ( Gallus domesticus): Neitz (1967)

groundnut seeds: Van Warmelo (1967)

Hakea sericea roots: Allsopp et al. (1987)

jackass penguin (Sphenicus demursus): Doidge (1950); Neitz (1967)

king penguin (Aptenodites pathagonica): Neitz (1967)

Leucospermum parile roots: Allsopp et al. (1987)

litter: Eicker (1976)

lucerne hay: Van Warmelo (1967)

maize silage: Van Warmelo (1967)

man: Jacobs et al. (1965); Findley et al. (1971); Martin & Berson

(1973); Caro (1973); Block & Young (1977): Kallenbach et al.

(1977); Cooper et al. (1983); Lewis et al. (1985); Joubert et

al. (1988); Govender et al. (1991)

molasses meal: Roth (1968)

mushroom compost: Eicker (1977); PREM 42090

natural gum: Roth (1968)

onion seed: PREM 44770

ostrich ( Struthio camelus): Doidge (1950); Neitz (1967)

peat: Smit (1984)

scaly weaver ( Sporopipes squamifrons ): Prozesky et al. (1971)

sclerotia ( Sclerotinia sclerotionim ): PREM 47929

soil: Allsopp et al. (1987) [UCT[; Cohen (1950); Eicker (1974. 1975);

Eicker et al. (1982); Martin (1960); Papendorf (1976) [MCP

340]; PPRI 3283; CSIR 85, 86, 87, 88, 89, 94. 97, 98, 99

sorghum: CSIR 305 [PPRI 3290], 306

sorghum malt: Rabie & Liibben (1984)

spent sulphite liquor: Pretorius & Lempert (1993a, b, c)

straw: PPRI 3478 [PREM 49331]

sugar: Van der Bijl (1920) [VdB 906, Doidge 1950. PREM 14258]

swine meal: Van Warmelo (1967)

turkey ( Meleagris gallopavo): Neitz (1967)

undetermined host: CSIR 1203

Zea mays: Van der Westhuizen & Bredell (1972); CSIR 160, 552, 567

= fumigatus var. ellipticus Raper & Fennell

fodder: PPRI 4687

grass roots: PREM 49065

soil: PPRI 3210

fumigatus var. ellipticus (see A. fumigatus)

giganteus Wehmer

sorghum malt: Rabie & Liibben (1984)

glaucus (see Eurotium herbariorum )

heteromorphus Bat. & H. Maia

medical supplies: PPRI 4688

japonicus Saito

grapes: Le Roux et al. (1973)

litter: Eicker (1973)

soil: Eicker (1969. 1970a, 1975); PPRI 4070; PREM 44279

= aculeatus Iizuka

debris: PPRI 3842 [PREM 50884], 4097

grass roots: PPRI 3326 [PREM 49201, ver. Z.L. IMI 343 117]

soil: Eicker (1974, 1975); PPRI 4227, 4286 [PREM 50884],

4962

Trichilia seeds: PPRI 4854

Zea mays: PPRI 4858

mangini (see Eurotium herbariorum)

melleus Yukawa

citrus fruits: Doidge & Van der Plank (1936)

Medicago sativa seed: Marasas & Bredell (1973) [PREM 44411,

44495, 44518]; PPRI 4228 [PREM 50862]

= quercinus (Bain.) Thom & Church

Litchi chinensis: Roth (1963)

minutus (see A. ustus)

multicolor Sappa

debris: PPRI 3840 [id. Z.L. IMI 343 121]

nidulans (see Emericella nidulans)

nidulans var. echinulatus (see Eurotium echinulata)

nidulans var. latus (see Emericella nidulans)

niger (see A. niger var. niger)

niger var. ficuum (Reichardt) Kozak.

= ficuum (Reichardt) Henn.

Allium cepa: PPRI 3389 [PREM 49173], 3390 [PREM 49174],

3391 [PREM 49170], 3424 [PREM 49171], 3425

[PREM 49172]

compost: PPRI 3476 [PREM 49338]

grass endophyte: De Villiers (1989) [PPRI 3455, PREM 49280]

sand/soil: PPRI 3321 [PREM 49203], 3322 [PREM 49200],

3323 [PREM 49204, id. as A. niger Z.L. IMI 343 118]

niger Tiegh. var. niger

= niger Tiegh.

aerospora: Doidge (1950); Roth (1968)

Allium cepa: VdB 95 [Verwoerd (1929), Doidge (1950),

Doidge et al. (1953); Gorter (1977)]; PPRI 3253

[PREM 49169]; PPRI 5017

Allium sativum: PPRI 3388 [PREM 47499, ver. Z. L. IMI 343

119]

antigen of; Benatar et al. (1980)

Arachis hypogaea: Doidge (1950) [Doidge et al. (1953),

Gorter (1977)]; Marasas & Van Rensburg (1986)

Avena sativa: *Liibben (1992)

Avicennia marina: Steinke (1990)

banana: Roth & Loest (1965)

Bmguiera gymnorrhiza: Steinke (1990)

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: Scott (1965)

citrus fruits: Doidge & Van der Plank (1936)

Citrus limonia: Doidge (1950)

Citnts sinensis: Doidge (1950) [Doidge et al. (1953), Gorter

(1977)]

compost: Eicker (1980); Smit (1984)

contaminant on malt agar: PREM 25960

cowpea hay: Van Warmelo (1967)

182

Bothalia 24,2 (1994)

dairy: Davel & Neethling (1930)

debris: PREM 48974, 48982, 49202

dried sausage: *PREM 45524, *45525

flannel bag: Doidge (1950) (TRL)

fodder: PPRI 3618 [PREM 48029]

fruit (rotting): Doidge (1950); [Doidge et al. (1953)]

Gardenia fruits: Doidge (1950) [PREM 23647]

grapes: Le Roux (1973)

grass hay: Van Warmelo (1967)

groundnut hay: Van Warmelo (1967)

insect (dead Chrysomelidae sp.): PPRI 4966

leather (wet-blue): Russell (1981) |PPRI 3255]

Litchi chinensis : Roth (1963)

lucerne hay: Van Warmelo (1967)

Lycopersicum esculentum: Doidge et al. (1953)

maize meal/hay/silage: Van Warmelo (1967)

man: Doidge (1950); Martin & Berson (1973); Bak & Wagen-

feld (1983); Berkowitz & Jacobs (1987)

Mangifera indica : Doidge (1950)

mango: Wehner et al. (1981)

material: Doidge (1950)

Medicago sativa seed: Marasas & Bredell (1973)

Medicago spp.: Lamprecht et al. (1988) [PPRI 3739, PREM

48327]

molasses meal: Roth (1968)

nuts/dried fruit: *Wehner & Rabie (1970)

paper: PPRI 3640 [PREM 49877]

paper pulp: Smit (1984)

pasture: Roux (1985)

peanut butter/ meal/ kernels: Gilman (1972)

phylloplane: Eicker (1976)

pomegranate (Punica granatum ): Verwoerd (1929)

Pyrus malus: Doidge (1950)

soil: Allsopp et al. (1987) [UCT]; Botha & Wehner (1990);

Cohen (1950); Eicker (1974); Martin (1960); Rosselet

(1953, 1955); Weideman et al. (1990); PPRI 3328;

CSIR 170, 171, 172, 173; MCP 1012

sorghum malt: Rabie & Liibben (1984)

sugar: Van der Bijl (1920) [VdB 905, PREM 14260]

Triticum aestivum: Liibben (1992)

ventilation tubing: Doidge (1950) (TRL det. Thom)

Vitis vinifera : Doidge (1950) [Doidge et al. (1953), Gorter

(1977]

Welwitschia mirabilis: Bomman (1978); PREM 36987, 41961,

43736; CBS 139.54

Ximenia americana : PREM 5599

Zea mays : Doidge (1950); Gilman (1972); Marasas & Van

Rensburg (1986); McLean & Berjak (1987); Van der

Westhuizen & Bredell (1972); Van Warmelo et al.

(1968); PREM 47914; CSIR 56, 156, 334, 513, 550.

559, 628

= welwitschiae (Bres.) Hennings

Welwitschia bainesii: Doidge (1950) [VdB 2499]; Raper & Fen-

nell (1973); PREM^ 46296

niger var. tubengensis (Mosseray) Kozak.

= tubengensis Mosseray

compost: Eicker (1980)

debris: PREM 48979, 48981

soil: Eicker (1969, 1970) [PREM 44288]

sugar cane cariopsis: PREM 47531

Zea mays: PREM 47554, 48864

niveus (see FenneUia nivea)

nutans McLennan & Ducker

soil: Raper & Fennell (1973) [CBS 122.56]; UCT [PPRI 3227]

ochraceus K. Wilh.

Asclepias stem: PPRI 3764

Andropogon sorghum seed: *CSIR 806 [CBS 263.67]

Avicennia seed: PREM 47524, 47525

cereals and legume products: *Scott (1965)

Citrus limonia : Doidge et al. (1953)

contaminant on malt agar: PREM 25961

fodder: PPRI 4687

lucerne hay: Van Warmelo (1967)

Medicago sativa seed: Marasas & Bredell (1973) [PREM 44359]

peanut butter/meal/kemels: Gilman (1972)

soil: Eicker (1974, 1975); Eicker et al. (1982); Martin (1960); Papen-

dorf (1976) |MCP 337, 1013]; CSIR 101, 102, 140, 142, 144,

153, 154, 157, 161, 162, 163, 164, 167, 168, 169, 490, 516,

551

sorghum: *Van der Merwe et al. (1965b); CSIR 289, 291, 803, 804

Triticum aestivum : Liibben (1992) >•

unknown host: *Van der Merwe et al. ( 1965a, b); *IMI 132 429

Zea mays : Gilman (1972); McLean & Berjak (1987); Van der West-

huizen & Bredell (1972); Van Warmelo et al. (1968); PPRI

3854 [PREM 47920], 3855 [PREM 47534]; CSIR 60; MCP

[PPRI 3865]

omatus (see Sclerocleista ornata)

oryzae (Ahlb.) Cohn

cassava: Klich & Pitt (1988)

cattle pellets: PREM 47142

cereal and legume products: Scott (1965)

grass roots: PPRI 3151

manure: PPRI 3474 [PREM 49334]

Zea mays: Mycock & Beijak (1992); PPRI 3629 [PREM 47624];

PREM 47625, 47926

= effusus Tirab.

cereals and legume products: Scott (1965)

ostianus Wehmer

sorghum: CSIR 290

parasiticus Speare

aerospora: Doidge (1950)

agricultural commodities: Dutton & Westlake (1985)

Arena sativa: Liibben (1992)

com: Klich & Pitt (1988)

groundnut seed: Labuschagne & Wehner (1990)

insect (dead Chrysomelidae sp.): PPRI 5063

locust (Locustana pardalina): Prinsloo (1960)

man: Martin & Berson (1973)

Medicago spp. Lamprecht et al. (1988) [PREM 48325]

oats: Klich & Pitt (1988)

paper: PPRI 3641 [PREM 49873]

soil: Klich & Pitt (1988); CSIR 214

sunflower seed: Klich & Pitt (1988)

termites (dead Hodotennes mossambicus): PPRI 3754

Zea mays: Klich & Pitt (1988); CSIR 62

penicilloides Speg.

Arachis hypogaea: CBS 234.65

phoenicis (Corda) Thom

Welwitschia sp. inflorescence: PPRI 4110 (ver. Z.L.), 4111; IMI 056

824

proliferans G. Sm.

= sartoryi Syd.

gold mine: Thom & Church (1926), type of A. sartoryi

[Doidge 1950]

puniceus Kwon-Chung & Fennell

Cenchms ciliaris: Bezuidenhout (1977)

soil: Papendorf (1976) [MCP 46, 174, 236]

quadrilineatus (see Emericella quadrilineata)

quercinus (see A. melleus)

repens (see Eurotium repens)

restrictus G. Sm.

cereals and legume products: Scott (1965)

soil: CSIR 39, 40, 42

Zea mays: Van der Westhuizen & Bredell (1972); PPRI 4841

ruber (see Eurotium rubrum)

mgulosus (see Emericella rugulosa)

sartoryi (see A. proliferans)

sclerotiorum G.A. Huber

grass litter: PPRI 3678

insects (dead Chrysomelidae spp.): PPRI 5061

paper: PPRI 3304 (PREM 49209)

termites (dead Hodotennes mossambicus): PPRI 3305 [PREM 49205]

sparsus Raper & Thom

soil: PPRI 4082 [PREM 50863 ver. Z. L. IMI 344 491]

Bothalia 24,2 (1994)

183

stromatoides (see Chaetosartorya stromatoides)

subsessilis Raper & Fennell

compost: PPRI 4016 (id, Z.L. IMI 343 123)

sulphureus (Fresen.) Wehmer

Nicotiana tabacum: Doidge (1950)

sydowii (Bainier & Sartory) Thom & Church

cereals and legume products: Scott (1965)

compost: Eicker (1980)

grass hay: Van Warmelo (1967)

lucerne hay: Van Warmelo (1967)

maize silage: Van Warmelo (1967)

man: Martin & Berson (1973)

Medicago sativa seed: Marasas & Bredell (1973) [PREM 44470,

44471, 44481]

Melianthus comosus seed: PPRI 3810 [PREM 50888]

oats: Doidge (1950)

silage: CBS 170.63

soil: Eicker (1974); CS1R 122, 123, 124, 125, 126; UCT

sugar: Doidge (1950)

Watsonia marginata seed: PPRI 3839

Zea mays: Gilman (1972); Mycock & Beijak (1992); Van der West-

huizen & Bredell (1972); PREM 47555; CSIR 59

tamarii Kita

cereals and legume products: Scott (1965)

debris: PPRI 4018 [PREM 49064, ver. Z.L.]

dried beans: Klich & Pitt (1988)

peanut butter/meal/kemels: Gilman (1972)

soil: PPRI 4018; CSIR 127, 128, 129, 130, 131

sorghum grain: Bosman et al. (1991); CSIR 313

sunflower seed: Klich & Pitt (1988)

Zea mays'. Gilman (1972); PREM 47922

terreus Thom

aerospora: Roth (1965)

Avena sativa: *Liibben (1992)

Cenchms ciliaris: Bezuidenhout (1977)

cereals and legume products: Scott (1965)

debris: PPRI 3182, [PREM 49036]; PREM 48978, 48980

fishmoth gut ( Namibmormisma muricauda ): Watson et al. (1990) [PPRI

3614]

grass roots: PPRI 3613 [PREM 48975]; PREM 48976, 48978, 48980

groundnut seeds: Van Warmelo (1967)

leather (wet-blue): Russell (1981)

lucerne hay: Van Warmelo (1967)

maize meal/hay/silage: Van Warmelo (1967)

man: Martin & Berson (1973)

Melianthus comosus seed: PPRI 3615

natural gum: Roth (1968)

pasture: Roux (1985)

sclerotia ( Sclerotinia sclerotiorum ): PREM 47927

soil: Eicker et al. (1982); Weideman et al. (1990): PPRI 3180 [PREM

49037], 3613; CSIR 174, 175, 182, 183, 184, 185, 186, 187,

188, 189, 190, 191

sorghum: CSIR 307, 309

sorghum malt: Rabie & Liibben (1984)

straw: PPRI 3480 [PREM 49333]

sugar: Van der Bijl (1920) [VdB 904, Doidge (1950), PREM 14261]

Triticum aestivum : Liibben (1992)

Zea mays: Gilman (1972); McLean & Berjak (1987); Van der West-

huizen & Bredell (1972); Van Warmelo et al. (1968); PREM

47915, 47916, 47917, 47918, 47919; CSIR 159, 536, 539, 616

= terreus var. boedijni (Blochwitz) Thom & Raper

soil: CSIR 177, 178

= terreus var. floccosus Thom & Raper

soil: CSIR 175

terreus var. aureus Thom & Raper

compost: Eicker (1980)

millet seed: PPRI 4229 [PREM 50864]

terreus var. boedijni (see A. terreus)

terreus var. floccosus (see A. terreus)

terricola E.I. Marchal

Watsonia marginata seed: PPRI 3788

Zea mays: PREM 47551

tubengensis (see A. niger var. tubengensis)

umbrosus (see Eurotium herbariorum)

unilateralis Thrower

Hakea sericea roots: Allsopp et al. (1987)

Leucospemium parile roots: Allsopp et al. (1987)

soil: Allsopp et al. (1987)

ustus (Bainier) Thom & Church

aerospora: Roth (1968)

Arachis hypogctea: PPRI 3189 [PREM 49027]

Avena sativa: *Lubben (1992)

canvas ventilation tubing: IMI 089 359

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: Scott (1965)

cheese: Luck et al. (1976); Luck & Wehner (1979)

compost: Eicker (1980)

culture contaminant: Rabie et al. (1977)

debris: PPRI 3198 [PREM 49063], 3199, 3639

flannel bag: IMI 089 360

grass endophyte: De Villiers (1989) [PPRI 3456, PREM 49281]

grass roots: PREM 49063

insect (dead Chrysomelidae sp.): PPRI 3191 [PREM 49051], 3192

[PREM 49052], 3193 [PREM 49053]

lucerne hay: Van Warmelo (1967)

maize hay: Van Warmelo (1967)

Medicago sativa seed: PREM 44553

natural gum: Roth (1968)

soil: Eicker (1974, 1975); CSIR 117, 118, 119, 120, 121

sorghum malt: Rabie & Liibben (1984)

Zea mays: Van der Westhuizen & Bredell (1972); CSIR 8

= minutus E.V. Abbott

flannel bag: Doidge (1950) (TRL det. Thom)

variecolor (see Emericella variecolor)

versicolor (Vuill.) Tirab.

Avena sativa: *Liibben (1992)

canvas: Doidge (1950) (TRL det. Thom)

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: Scott (1965)

flannel bag: Doidge (1950) (TRL det. Thom)

grapes: Le Roux et al. (1972)

Leucospemium parile roots: Allsopp et al. (1987)

lucerne hay: Van Warmelo (1967)

man: Doidge (1950): Martin & Berson (1973)

Medicago sativa seed: Marasas & Bredell (1973) [PREM 44486]

Medicago spp.: Lamprecht et al. (1988) (PPRI 3502, PREM 48326]

paper: PPRI 3315 [PREM 49208]

peanut butter/meal/kemels: Gilman (1972)

Salvia stenophylla seed: PPRI 3519

soil: Martin (1960); Eicker (1974, 1975): Papendorf (1976) [MCP 339];

CSIR 179, 192, 193, 194, 196, 197, 198, 199, 201, 202; UCT

sorghum malt: Rabie & Liibben (1984)

undetermined host: Rabie et al. (1976); CSIR: 1365, 1367, 1370

wooden floor boards: PPRI 3890

Triticum aestivum: Liibben (1992)

Zea mays: Van Warmelo et al. (1968); Gilman (1972); McLean &

Beijak (1985, 1987); Van der Westhuizen & Bredell (1972);

PREM 47626, 47923; CSIR 478

viridinutans Ducker & Thrower

grass debris: PPRI 3327 |PREM 49206]

grass roots: PPRI 3208 [PREM 49067], 3209 [PREM 49068]

soil: PPRI 4976

welwitschiae (see A. niger var. niger)

wentii Wehmer

Avena sativa: Liibben (1992)

cereals and legume products: Scott (1965) [Rabie & Terblanche (1967)]

compost: Smit (1984)

groundnuts: *Rabie et al. (1965)

palm seed (Arega catechu): PREM 49026

peanut butter/meal/kemels: Gilman (1972)

soil: Eicker (1974); Weideman et al. (1990); CSIR 244, 245, 246, 247,

248, 249, 250, 251, 252, 254

sorghum: CSIR: 294, 295

sorghum malt: Rabie & Liibben (1984); *Rabie et al. (1986)

sugar cane cariopsis: PREM 47527

unknown host: Rabie & Terblanche (1967)

184

Bothalia 24,2 ( 1994)

Zea mays: Gilman (1972); McLean & Beijak (1987); Van der Wes-

thuizen & Bredell (1972); Van Warmelo et al. (1968); PPR1

3905; CS1R 155, 336, 357, 376, 418, 431; IMI 162 039

Aspergillus species undetermined

aerospora: Ordman (1963, 1970); Ordman & Etter (1956);

Potter et al. (1991); Van der Merwe et al. (1979)

agricultural commodities: Dutton & Westlake (1985)

Allium cepa: PREM 46375

Arachis hypogaea : Marasas & Van Rensburg (1986)

Avicennia marina: Mycock & Beijak (1990); Steinke et al. (1990)

banana: Roth & Loest (1965)

beer: Martin & Keen (1978)

Bruguiera gymnorrhiza : Steinke et al. (1990)

Camellia sinensis: Mycock & Berjak (1990)

Castanospermum australe: Mycock & Beijak (1990)

cereal and legume products: Isaacson (1966)

cheese: Luck & Wehner (1979)

chicken feeds and litter: Westlake & Dutton (1985)

Cichorium intybus: Prinsloo et al. (1991)

citrus fruits: Doidge & Van der Plank ( 1936)

Citrus sinensis: Doidge (1950) [Doidge et al. (1953)]

compost: Eicker (1980); Smit (1984)

corn: Marasas et al. (1981); Van Warmelo (1967)

cowpea hay: Van Warmelo (1967)

feedstuffs: Dutton & Westlake (1985); Van Warmelo (1967)

Ficus carica: Doidge (1950) [Doidge et al. (1953)]

grapes: Le Roux et al. (1973)

grass hay: Van Warmelo (1967)

groundnut hay: Van Warmelo (1967)

groundnuts: Marasas & Van Rensburg (1986)

indigenous seed: Isaacs & Benic (1990)

Landolphia kirkii: Mycock & Beijak (1990)

Lite hi chinensis: Mycock & Berjak (1990)

lucerne hay: Van Warmelo (1967)

man: Martin & Berson (1973); Cooper et al. (1983);

Fitzsimons & Peters (1986); Glass et al. (1984)

oranges: Doidge & Van der Plank (1936)

Passiflora quadrangularis: Doidge (1950)

pasture: Roux (1985)

piglet: Nesbit (1986)

Pinus sp.: Lundquist (1987)

Podocarpus henkelii: Mycock & Beijak (1990)

Prunus persica: Doidge et al. (1953)

Pyrus malus: Doidge et al. (1950)

Saccharum officinarum: Doidge (1950) [Doidge et al. (1953)]

scale: PREM 26137, 28447

Scadoxus membranaceus: Mycock & Berjak ( 1 990)

soil: Eicker (1974, 1975); Eicker et al. (1982); Papendorf (1976)

sorghum grain: Bosman et al. (1991)

spent sulphite liquor: Pretorius & Lempert (1993a, b, c)

sunflower hay: Van Warmelo (1967)

swine meal: Van Warmelo (1967)

Zea mays: Gilman (1972); Marasas & Van Rensburg (1986); Rheeder

et al. (1990); PREM 47913

GENUS CHAETOSARTORYA

cremea (Kwon-Chung & Fennell) Subram.

# A. cremeus Kwon & Fennell

Zea mays: Van der Westhuizen & Bredell (1972)

stromatoides B.J. Wiley & E.G. Simmons

# A. stromatoides Raper & Fennell

man: Sacho et al. (1987) [IMI 292 883)]

GENUS EMERICELLA

acristata (Fennell & Raper) Y. Horie

celery seed: PPRI 4961

echinulata (Fennell & Raper) Y. Horie

compost: PPRI 3465

# A. nidulans var. echinulalus Fennell & Raper

culture contaminant: PREM 48909

nidulans (Eidam) Vuill.

compost: PPRI 3466, 3467

# A. nidulans (Eidam) Wint.

aerospora: Roth (1968) >

Avena sativa: *Lubben (1992)

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: *Scott ( 1965)

compost: Eicker ( 1 980)

grass hay: Van Warmelo (1967)

groundnuts: *Holzapfel et al. (1966); Van Warmelo (1967)

litter: Eicker (1976)

lucerne hay: Van Warmelo (1967)

lupin seeds: Van Warmelo (1967)

maize hay/silage: Van Warmelo (1967)

Medicago sativa seed: PREM 44520, 44532

molasses meal: Roth (1968)

natural gum: Roth (1968)

pasture: Roux (1985)

soil: Eicker (1974, 1975); Eicker et al. (1982); CSIR 103, 104, 105,

106, 107, 108, 109, 110, 111, 997, 998

sorghum malt: Rabie & Liibben (1984)

Triticum aestivum: Liibben (1992)

Zea mays: *Holzapfel et al. (1966); Van der Westhuizen & Bredell

(1972); Van Warmelo et al. (1968); CSIR 835

# A. nidulans var. latus Thom & Raper

air-sac of penguin: CSIR 999

compost: Eicker (1980)

quadrilineata (Thom & Raper) C.R. Benj.

Arachis hypogaea: *CBS 235.65

compost: PPRI 3468

# A. quadrilineatus Thom & Raper

Medicago sativa seed: PREM 44514, 44515

Pisum sativum: PREM 44326

soil: CSIR 1000

sorghum: CSIR 295

rugulosa (Thom & Raper) C.R. Benj.

straw: PPRI 3469

# A. rugulosus Thom & Raper

Avena sativa: *Liibben (1992)

compost: Eicker (1980)

Pisum sativum: PREM 44327

soil: Eicker (1974, 1975)

variecolor Berk. & Broome

# A. variecolor (Berk. & Broom) Thom & Raper

Zea mays: Van der Westhuizen & Bredell (1972)

violacea (Fennell & Raper) Malloch & Cain

forest soil: CBS 314.89

GENUS EUROTIUM

amstelodami L. Mangin

aerospora: PPRI 4851

contaminant: PPRI 3429

lupin: PPRI 3720 [PREM 50889]

Melianthus comosus seed: PPRI 3869

Zea mays: PPRI 3836

# A. amstelodami (L. Mangin) Thom & Church

Arachis hypogaea: PREM 48049

cereals and legume products: Scott (1965)

grass hay: Van Warmelo (1967)

groundnut seeds: Van Warmelo (1967)

Litchi chinensis: Roth (1963)

lucerne hay: Van Warmelo (1967)

lupin seeds: Van Warmelo (1967)

mangrove soil: Swart (1959)

Medicago sativa seed: Marasas & Bredell (1973); PREM 44494,

44496

mine timber: Doidge (1950) |TRL det. Thom]

soil: CSIR 19, 20, 25, 28, 29, 31, 32, 36, 38

sugar: Doidge (1950)

swine meal: Van Warmelo (1967)

Triticum aestivum: Liibben (1992)

unknown substrate: *Rabie et al. ( 1964); Swart (1959); PREM 48049

Zea mays: Van der Westhuizen & Bredell (1972); CSIR 137, 841,

863

Bothalia 24,2(1994)

185

chevalieri L. Mangin

Zea mays'. PPRI 3847 [PREM 49437], 4908

# A. chevalieri (Mangin) Thom & Church

cereals and legume products: *Scott (1965)

compost: Eicker (1980)

soil: CS1R 52, 53, 54, 64, 65, 67, 78, 79, 82

Triticum aestivum : Liibben (1992)

unknown substrate: Swart (1959)

Zea mays'. Gilman (1972); Mycock & Berjak (1992); Van der West-

huizen & Bredell (1972); PREM 47921, 47924, 47925; CSIR

143

cristatum (Raper & Fennell) Malloch & Cain

horse feed: PPRI 4973

# -4. chevalieri var. intermedius Thom & Raper

soil: CSIR 975, 976

# A. cristalus Raper & Fennell

unknown substrate: Raper & Fennell (1973), type of A.

cristatus [CBS 123 53, IMI 172 278]

Zea mays: PREM 44574, 44575

echinulatum Delacr,

#A. echinulatus (Delacr.) Thom & Church

Zea mays: Gilman (1972); Van der Westhuizen & Bredell (1972)

herbariorum Link

Melianthus comosus seed: PPRI 3582

Pisum sativum seed: CBS 127 55

# A. glaucus Link

aerospora: Roth (1968)

Abrus precatorius seed: PREM 23617

Avena sativa: Liibben (1992)

Caryopemon cruciger: Doidge (1950) [PREM 23618]

Cenchrus ciliaris: Bezuidenhout (1977)

cheese: Doidge (1950)

contaminant on malt agar: PREM 25959 [id. CBS]

dairy: Davel & Neethling (1930)

Medicago sativa seed: PREM 44364

molasses meal: Roth (1968)

Nicotiana tabacum: Doidge (1950) [PREM 701]

nuts (Corylus avellana): PREM 23649

sorghum malt: Rabie & Liibben (1984)

sugar: VdB 902

Triticum aestivum: Liibben (1992)

unknown substrate: Doidge (1950)

Zea mays: McLean & Berjak (1985, 1987); Van Warmelo et al.

(1968); PREM 47529, 47535

# A. mangini Thom & Raper

cereals and legume products: *Scott (1965)

herbarium material: Swart (1959)

mangrove soil: Swart (1959)

soil: CSIR 45

= Eurotium umbrosum (Bainier & Sartory) Malloch & Cain.

Arachis hypogaea: CBS 232.65

# A. umbrosus Bainier & Sartory

Medicago sativa seed: Marasas & Bredell (1973)

soil: CSIR 43, 44, 46, 47

Zea mays: Van der Westhuizen & Bredell (1972); PREM 44570,

44576

repens De Bary

Cussonia paniculata seed: PPRI 3666

kiwi jam: PREM 47738

Melianthus comosus seed: PPRI 3665 [PREM 49891]

# A. repens (De Bary) Fischer

aerospora: Doidge (1950)

cereals and legume products: Scott (1965)

compost: Eicker (1980)

culture contaminant: Swart (1959)

dried sausage: *PREM 47101

peas: Swart ( 1959)

soil: CSIR 48, 50; MCP 1014

sorghum: CSIR 535, 537, 540

sugar: VdB 901

Triticum aestivum: Liibben (1992)

Zea mays: Gilman (1972); Van der Westhuizen & Bredell (1972)

rubrum J. Konig el al.

contaminant: PPRI 3609

# A. ruber (J. Konig et al.) Thom & Church

cereals and legume products: *Scott (1965)

compost: Eicker (1980)

Nicotiana tabacum: IMI 168 779

soil: CSIR 6, 7, 12, 21, 26, 27, 74

Triticum aestivum: Liibben (1992)

Zea mays: Gilman (1972); Van der Westhuizen & Bredell (1972);

CSIR 308, PREM 47534

GENUS FENNELLIA

flavipes B.J. Wiley & E.G. Simmons

# A. flavipes (Bainier & Sartory) Thom & Church

Cenchrus ciliaris: Bezuidenhout (1977)

cereals and legume products: *Scott (1965)

debris: PREM 48977

insect (dead Chrysomelidae sp.): PPRI 4965

Leucospermum parile roots: Allsopp et al. (1987)

soil: Martin (1960); Eicker (1974); PPRI 3181 [PREM 50865], 4226;

CSIR 134 [PREM 48046], 135; UCT

sorghum: CSIR 804

Zea mays: Van der Westhuizen & Bredell (1972); CSIR 1085 |PREM

48047]; PREM 48055

nivea (B.J. Wiley & E.G. Simmons) Samson

# A. niveus Blochwitz

cereals and legume products: *Scott (1965)

grass hay: Van Warmelo (1967)

soil: CSIR 132; IMI 161 651; UCT

# A. ebumeus Biourge

timber: Doidge (1950)

GENUS NEOSARTORYA

aurata (Warcup) Malloch & Cain

= Sartoiya aurata (Warcup) Subram.

soil: CSIR 977, 978 |PPRI 3418. PREM 49322, id. Z. L. IMI

343 120], 979. 980 [PPRI 3419], 981

fischeri (Wehmer) Malloch & Cain

face cream: PPRI 4230 [PREM 50867]

Leucospermum parile roots: Allsopp et al. (1987)

# A. fischeri Wehmer

litter: Eicker (1973)

peat: Smit (1984)

soil: Cohen (1950); Eicker (1969); CSIR 988, 996, 1050 [PPRI 3195,

PREM 49038]; PPRI 4975; IMI 332 643; CBS 317.89; UCT

glabra (Fennell & Raper) Kozak,

soil: UCT [PPRI 3247. PREM 49193]

# A. fischeri var. glaber Fennell & Raper

soil: CSIR 991, 992 [PPRI 3427, PREM 49319], 993

spinosa (Raper & Fennell) Kozak,

sterilised compost: PREM 47727

# A. fischeri var. spinosus Raper & Fennell

soil: CSIR 990 [PPRI 3428, PREM 49320]; IMI 332643

stramenia (R. Novak & Raper) Malloch & Cain

= Sartorya stramenia (Novak & Raper) Subram.

soil: CSIR 982, 983. 984, 985, 986

GENUS SARTORYA (see genus NEOSARTORYA)

GENUS SCLEROCLEISTA

ornata (Raper et al.) Subram.

= A. omatus Raper et al.

Zea mays: Gilman (1972)

Botha] ia 24,2: 187-194(1994)

The taxonomic value of epidermal characters in the leaf of Heteromorpha and

some related genera (Apiaceae)

P.J.D. WINTER* and B-E. VAN WYK*

Keywords: Apiaceae, epidermis, Heteromorpha , Polemannia, Polemanrtiopsis, stomata, taxonomy, trichomes, vestiture

ABSTRACT

All 17 species of Heteromorpha Cham. & Schltdl. (sensu Humbert 1956), all three species of Polemannia Eckl. & Zeyh. and

the monotypic Polemanniopsis B.L. Burtt were investigated for leaf epidermal characters. Stomatal type was anomocytic, with

an exception in only one Madagascar species, H. betsileensis. The distribution and density of stomata (on both leaf surfaces) are

diagnostic for some species. The number, size and outline of normal epidermal cells are different in juvenile and adult leaves

and these differences vary between species. Seven trichome types are recognized which, when combined with dispersion

pattern, also serve to characterise the various species and forms.

UITTREKSEL

A] 17 spesies van Heteromorpha Cham. & Schltdl. (sensu Humbert 1956), al drie spesies van Polemannia Eckl. & Zeyh. en

die monotipiese Polemanniopsis B.L. Burtt se blaar-epidermale kenmerke is ondersoek. Die stomata-tipe was anomosities, met

'n enkele uitsondering by een Madagassiese spesie, H. betsileensis. Die verspreiding en digtheid van stomata (op beide

oppervlakke) is diagnostics vir sommige spesies. Die aantal, grootte en buitelyn van gewone epidermisselle verskil by jeug- en

volwasse blare en hierdie verskille varieer tussen spesies. Sewe trigoomtipes word onderskei wat, saam met

verspreidingspatroon, kenmerkend is vir die verskillende spesies en vorme.

INTRODUCTION

Heteromorpha Cham. & Schltdl. ( sensu stricto) is a

genus of trees, shrubs or suffrutices occurring throughout

most of temperate and subtropical Africa. Seven species

are restricted to the African continent and Yemen. Hum-

bert (1956) broadened the generic concept to include eight

Madagascar species. The African contingent shares the

woody habit with the related Polemannia Eckl. & Zeyh.

from the Drakensberg region, and fruit characters with the

Western and Northern Cape genus Polemanniopsis B.L.

Burtt (Burtt 1988), which have been included here as

potential outgroups.

Most species are either glabrous or have trichomes

which are not readily visible to the naked eye. Phenotypic

variation as well as the broad species concepts employed

in past surveys (mostly Flora treatments and therefore of

a limited, regional nature), have tended to obscure the

taxonomic relevance of vestiture. However, trichome type

and trichome distribution have been used to distinguish

H. trifoliata from species with basally tuberculate

trichomes, and to characterise H. papillosa and H. goss-

weileri (Townsend 1985, 1989). Epidermal characters are

therefore clearly of taxonomic value in Heteromorpha ,

especially when the paucity of information on other char-

acters is considered.

Stomatal type has been recorded for only one of the

woody African Apiaceae, namely H. arborescens , which

was found to be anomocytic (Guyot 1971).

* Department of Botany, Rand Afrikaans University, RO. Box 524,

Auckland Park 2006, Johannesburg.

MS. received: 1993-02-09.

This investigation forms part of a complete revision of

the genus Heteromorpha. The formal taxonomic treatment

will be published elsewhere.

MATERIALS AND METHODS

Leaves from FAA material or from herbarium

specimens of all known species of Heteromorpha sensu

lato (including the Madagascan group), as well as the re-

lated genera Polemannia and Polemanniopsis , were

treated according to the method described by Ram & Nyar

(1974) to obtain epidermal peels of both leaf surfaces.

Specimens examined:

Heteromorpha (African species)

1A involucrata Conrath, typical form, sufffutex, Transvaal, Swaziland

& Natal, Winter 61. 68 (JRAU); Gerstner 3763 (PRE).

IB involucrata Conrath, ‘kassneri' form, sufffutex, Malawi & Zam-

bia, Quarre 5919 (PRE); Phillips 1295 (MO).

1C involucrata Conrath, ‘Zimbabwe’ form, sufffutex or weak shrub,

Zimbabwe & Angola, Jacobsen 2891 (PRE): Bayliss 10686 (PRE); Kers

3491 (S).

ID involucrata Conrath, ‘Malawi’ form, weak shrub, Malawi & SA,

Torre & Paiva 11897 (PRE); Winter 67 (JRAU).

2 pubescens Burtt Davy, suffrutex or weak shrub, Transvaal, Winter

66. 69 (JRAU); Junod 143 (PRE).

3 papillosa C.C. Towns., well-branched shrub, Namibia, Merxmiiller

& Giess 28004 (PRE); Dinter 3499 (PRE); Hanekom 135 (WIN).

4 gossweileti (Norman) Norman, suffrutex, Angola, Milne-Redhead

3981 (PRE); Mendes 2069 (PRE); Hundt 727 (PRE); Hooper &

Townsend 325 (K).

5 stenophylla Wolff ex Schinz, sufffutex, Namibia, Angola & Malawi,

Le Roux 295 (PRE); Giess 8602 (PRE); Dinter 5487 (PRE).

188

Bothalia 24,2 (1994)

6A arborescens (Spreng.) Cham. & Schltdl., tree, Cape, Van Wyk

3313 (JRAU); Vlok 2633 (JRAU); Ward 7538 (PRE).

6B trifoliata (Wendl.) Eckl. & Zeyh., typical form, tree, Eastern Cape

to Arabian Peninsula, Brink 128 (PRE); Winter 71 (JRAU); De Wilde

6041 (K); Semsei 4122 (PRE); Stolz 24699 (PRE); Pope & Muller 2075

(PRE).

6C trifoliata (Wendl.) Eckl. & Zeyh., frutescent form, shrub. Natal

to Malawi, Winter 51, 57 (JRAU); Rogers 22197 (PRE).

6D trifoliata (Wendl.) Eckl. & Zeyh., W African form, suffrutex,

Letouzey 5680 (K); Meurillon 1396 (K); Milne-Redhead 762 (K).

7 transvaalensis Schltr. & Wolff, suffrutex. Winter 50, 52, 55 (JRAU).

Heteromorpha (Madagascan species)

Ml laxiflora (Baker) Humb. var. alticola Humb., suffrutescent climb-

er, De la Bdthie 15168 (P); Humbert & Capuron 25031 (P); var. laxiflora ,

climber, Schatz 2655 (MO).

M2 marojejyensis Humb., thin-stemmed shrub, Humbert 22710 (P);

Miller & Lowry 4160 (MO); Herbier de 1'Alaotra 3475 (MO).

M3 tsaratananensis Humb., woody shrub, De la Bdthie 6806, 16411

(P); Humbert 18374 (P).

M4 coursii (Baker) Humb., woody shrublet, Humbert et al. 24702

(P); Herbier de 1'Alaotra 3825 (MO).

M5 betsileensis Humb., suffrutex, Humbert 3792 (P); De la Bdthie

6815 (P).

M6 andringitrensis Humb., herbaceous perennial, De la Bdthie 6809,

13741, 14430 (P).

M7 andohahelensis Humb., suffrutex, Humbert 6192, 6466, 13654 (P).

M8 bojeriana (Baker) Humb., suffrutex, Bojer s.n. (P); Dorr et al.

2889 (MO); Catat 332 (P).

Polemanniopsis (woody shrubs, NW Cape)

PO marlothii (Wolff) B.L. Burtt, Venter 8132 (PRE); Taylor 11384

(PRE); Van Jaarsveld 5457 (PRE).

Polemannia (woody shrubs, Drakensberg)

PI montana Schlecht. & Wolff, Smook 7181 (PRE); Schmitz 9077

(PRE); Jacobs 3097 (PRE).

P2 simplicior Hilliard & B.L. Burtt, Hoever 2016 (PRE); Pole Evans

19654H (PRE); Pentz sub PRE 48118 (PRE).

P3 gross ulariifolia Eckl. & Zeyh., Ratray 35 (PRE); Giffen 1296

(PRE); Gal pin 8359 (PRE).

Mean stomata] densities were determined under the

light microscope, by a minimum of six counts per

specimen over an area along the eyepiece scale bar.

Counts were not taken directly adjacent to the margin or

midvein, only in the secondary vein interstices. Dispersion

was scored according to patterns of local presence or con-

centration.

After germinating seeds of five African species | H. ar-

borescens, H. trifoliata, H. involucrata, //. pubescens and

H. transvaalensis ], juvenile leaves were available to in-

vestigate ontogenetic changes during leaf development.

Trichome types were studied by SEM on one specimen

of each taxon. To investigate the structure of each

trichome type, mature leaves were embedded in glycol

methacrylate (GMA) according to a modification (Tilney

1986) of the method of Feder & O’Brien ( 1968). Sections

were obtained with a Porter Blum MT-I ultramicrotome

and stained according to the so-called periodic acid —

Schiff/Toluidine Blue (PAS/TB) staining method. Draw-

ings were done with the aid of a camera lucida attachment

on a Zeiss compound light microscope. Vestiture

(trichome distribution) was studied on several specimens

with the aid of a dissecting stereomicroscope. The inves-

tigation was limited to the laminar region of the leaf.

RESULTS AND DISCUSSION

Five characters were chosen for analysis:

Stomata I apparatus

The stomatal apparatus proved difficult to interpret be-

cause cell boundaries were indistinct in the stomal region

and because cells adjacent to the stomata differed super-

ficially from the surrounding epidermal cells. The cuticula

appears to be much thicker in this region, making the

radial cell walls and guard cell boundary almost indiscer-

nible. This at first suggested a tetracytic or actinocytic

arrangement, but the number of surrounding cells was too

inconsistent for this to be the case. Stomata are juxtaposed

FIGURE 1 . — Stomatal apparatus types in Heteromorpha. A, H. betsi-

leensis'. anisocytic type. B. II. coursii: anomocytic type.

Bothalia 24,2(1994)

189

in some instances, or separated by one cell only (Figure

IB), confirming the perigenous anomocytic origin. Cells

surrounding the stomata sometimes differ from other

epidermal cells in their reaction to staining, but there is

no evidence of any structural difference, hence our inter-

pretation that these are not true subsidiary cells.

As found by Guyot (1971) for H. arborescens, the rest

of the genus — with one exception — as well as the related

genera, all possess the anomocytic type stomatal apparatus

(Figure IB). The stomata of the Apiaceae are generally

considered to be more or less intermediate between

anomocytic and anisocytic (Guyot 1971; Ostroumova

1987 in Baranova 1992).

The single exception, the Madagascan species H. bet-

sileensis , has an anisocytic type stomatal apparatus (Fig-

ure 1A). The radial cell walls of subsidiary cells are

shorter than the tangential walls, giving them a thinner

shape than the normal epidermal cells. The characteristic

clustering of the stoma with three surrounding cells sug-

gests a common origin from one stomatal initial cell

(mesogenous type), although it must be emphasized that

the ontogeny was not studied (see Baranova 1992 for a

detailed discussion of morphological vs. ontogenetic clas-

sification of stomata).

Stomatal dispersion

Stomata sometimes occur in crypts formed by the

prominently raised veins on the abaxial surface, as in H.

pubescens.

Four main patterns of stomatal dispersion over the

adaxial surface were identified. Stomata are either absent,

occur along margin and/or midrib only, occur mostly

along margin and veins, or occur throughout the entire

surface. These data are listed in Table 1. In the Madagas-

can species and the other genera stomata are either absent

or dispersed randomly across the entire surface. Hetero-

motpha sensu stricto by contrast, shows great variation.

H. stenophylla and H. gossweileri differ from the other

African species in their stomatal dispersion pattern which

is shared with all Polemanniopsis and Polemannia spe-

cies, but with only two Madagascan species (H. andoha-

helensis and //. bojeriana). In PI. papillosa this state

co-occurs with states 2 and 3 of Table 1 .

Stomatal distribution and density

The results of the stomatal density study are presented

in Figure 2. The data show that the variation in this char-

acter is independent of habit and also not logically corre-

lated with mesophytic or xerophytic habitats. Compared

to Heteromorpha, the other two genera are relatively in-

variant in terms of abaxial density (Figure 2A), having

values of around 110 per mm-. Across Heteromoipha ,

most species have between 100 and 200 stomata per mm2

on the abaxial surface. There are three Madagascan

species with much higher values. These are H. maroje-

jyensis (M2: mean = 279), H. tsaratananensis (M3: mean

= 293) and H. coursii (M4: mean = 265).

In the African Heteromorpha group, notable outliers

are H. involucrata ’ kassneri ’ form (IB: mean = 229), H.

gossweileri (4: mean = 220), and H. stenophylla (5: mean

= 88). The West African form of H. trifoliata — H. abys-

sinica sensu Jacques-Felix (1970) — is clearly distinguish-

able from all the central African forms of H. involucrata

(IB, 1C & ID; means = 229, 131 & 119 respectively).

Most species examined had none or virtually no adaxial

stomata (Figure 2B), whereas Polemannia has on average

just over 40 stomata per mm2, and a relatively high varia-

tion per species. Adaxial stomata are rare (mean less than

5 per mm2 or absent in most Heteromorpha species except

H. papillosa (3: mean = 16), H. gossweileri (4: mean =

88), H. stenophylla (5: mean = 27), H. andohahelensis

{Ml: mean = 8) and H. bojeriana (M8: mean = 17).

Epidermal ontogeny

As the leaves develop from the juvenile to the mature

stage, the proportion of stomata to normal epidermal cells

(Figure 3) remains constant in H. involucrata and H.

pubescens, whereas it decreases in both the typical and

the frutescent forms of H. trifoliata. This is not due to

fewer stomata being formed, but to a reduction in size of

the normal epidermal cells and thus a higher epidermal

cell density.

Trichome type

The variation in mature trichome types as well as their

distribution is summarized in Table 1 . Various types com-

prising seven character states were recognised and are

shown in Figure 4 and Figure 5. The papillate type

(Figures 4A; 5C2), which is also the juvenile type, has a

wide occurrence (present in all three genera), and is also

the only type for Polemanniopsis and Polemannia. Com-

pared to the Madagascan group where only the filamen-

tous, multicellular type is found in H. betsileensis alone,

the African species show a high diversity of form.

Papillate trichomes, similar to those shown in Figure

4A and 5C. were observed on the juvenile leaf margins

of Heteromorpha. These were present on the juvenile

leaves in all forms of the five African species investigated.

This feature appears to be variously lost or modified by

means of apical and sometimes basal cell differentiation

in the ontogeny of the mature types.

Tuberculate trichomes occur either as simple tubercles

(Figure 5C) or with one (Figures 4C; 5 A, B & E) or many

(Figure 4E) trichomes of another type affixed apically.

This condition was described by Townsend (1985) as

papillose, and is characteristic of H. pubescens and most

forms of H. involucrata. The term ‘verruculose’ used by

Townsend (1985) to describe the vestiture in H. goss-

weileri suggests the simple tuberculate type of trichome

(Figure 5C1). Although the SEM survey showed only the

papillate type (Figure 4A), which does bear a superficial

resemblance to the tuberculate type, light microscopy con-

finned the presence of both types (Figure 5C).

The filamentous/filiform type (Figures 4E; 5E) is found

only in H. pubescens and H. betsileensis, and in addition

to distribution and density of hairs, characterizes these

species. Short cylindrical hairs (Figures 4B; 5D) are char-

TABLE 1. — Epidermal character state distribution for leaves of Heteromorpha, Polemannia, and Polemanniopsis

190

Bothalia 24.2 ( 1994)

Adaxial stomatal distribution: 1 , absent; 2, margin only; 3, mostly margin and veins; 4, across entire surface.

Trichome type: 5, papillate; 6, conical; 7, long cylindric; 8, short cylindric; 9, filamentous; 10, tuberculate; 11, multicellular.

Trichome distribution: 12, margin; 13, adaxial midrib; 14, adaxial lateral veins; 15, entire adaxial surface; 16, abaxial midrib; 17, abaxial lateral veins; 18, entire abaxial surface.

+. present; -, absent; F, few; R, rare; B, basal only; 1MV. intramarginal vein.

Bothalia 24,2(1994)

191

HETEROMORPHA POLEMANNIOPSIS HETEROMORPHA

FIGURE 2. — A, abaxial density, and B, adaxial density of stomata in the genera Heteromorpha, Polemanniopsis and Polemannia. Range and mean

values of specimens examined are indicated for each species/form; •, absence of stomata; single values (n = 1 ) are denoted by a horizontal

bar only. Taxa numbered and sampled as under Specimens examined.

acteristic of H. arborescens and H. trifoliata , but are also

found in H. papillosa, the West African form of H. tri-

foliata, and occasionally (with other types) in some forms

of H. involucrata.

Other types that can be identified are 1, a unicellular

conical hair (Figures 4F; 5A), usually present in all forms

of H. involucrata', and 2, a unicellular or multicellular

long cylindrical hair (Figures 4D; 5B), present in the

central African forms of H. involucrata.

Trichome distribution

Patterns of laminar distribution of trichomes are sum-

marized in Table 1. Hairs, when present, are usually lo-

cated at least on the adaxial midrib (Figure 6A). This is,

however, only rarely the case in H. involucrata , where

the abaxial midrib is usually more pilose than the adaxial

midrib. The presence of trichomes along the leaf margin

is the rule in H. involucrata (Figure 6B & C) and the

exception in H. trifoliata. The West African form of H.

trifoliata can be distinguished from the typical form by

the presence of small tubercles, albeit sparse in some

specimens, along the leaf margin. The leaf margin in typi-

cal H. trifoliata is usually glabrous, or if pubescent (com-

monly in young growth ), then with short cylindrical hairs.

Both forms have cylindrical trichomes along the adaxial

midrib.

H. involucrata is the only species with trichomes on

the areas between the veins (and not on the veins and

margin only, as in all other species). H. pubescens has

192

Bothalia 24,2 (1994)

FIGURE 3. — Variation in leaf epidermal ontogeny in Heteromorpha

indicated by differences in proportions of stomata to surrounding

cells between seedlings and mature leaves. This is a function of

the size and number of normal epidermal cells. 6B, H. trifoliata,

typical form. Winter 71; 6C, H. trifoliata , frutescent form.

Winter 57; I . //. involucrata. Winter 61; 2, H. pubescens. Winter

morphological features in common with H. involucrata,

and also shares the hairy abaxial midrib and presence of

hairs on the adaxial secondary venation (Townsend 1985)

in addition to those found elsewhere (Figure 6D).

H. gossweileri has a vestiture pattern, which for its

particular trichome type, is characteristic. The leaf margin,

midrib and major adaxial veins all have a variable number

of trichomes, often concentrated apically or basally

(Townsend 1985).

TAXONOMIC IMPLICATIONS

The anomocytic type of stomatal apparatus seems con-

servative, occurring throughout, with the exception of H.

betsileensis , suggesting a different position for this

species. This is also the only Madagascan species with

any degree of vestiture on the laminar region. The occur-

rence of a second stomatal type could indicate a

polyphyletic grouping of the Madagascan species, as this

feature appears to be rather conservative, and is a potential

character for tribal delimitation. A re-investigation of

generic limits is suggested. Abaxial stomatal density is a

potential grouping character within the Madagascan con-

tingent, and could support the division of the group into

two or more genera when these species are investigated

further.

The typical and frutescent forms of H. trifoliata, for

which seedlings were investigated, show an ontogenetic

feature not present in H. pubescens and H. involucrata,

namely a decrease in size of normal epidermal cells.

Three of the African species of Heteromorpha can be

distinguished from the others on the basis of the uniformly

dispersed adaxial stomata, a character which is shared

with Polemannia, Polemanniopsis and two Madagascan

species. This character may be logically correlated with

FIGURE 4. — Trichome types in

Heteromorpha sensu stricto.

A, H. gossweileri: papillate

hairs, resembling juvenile

state. B. West African form of

H. trifoliata: short cylindrical

hairs. C, H. involucrata, typi-

cal form: short conical hairs on

tuberculate base. D, H. in-

volucrata, ‘ kassneri ’ form: mul-

ticellular long cylindrical hairs.

E, H. pubescens: filamentous

trichomes on tuberculate base.

F, H. involucrata, 'Malawi'

form: conical trichomes. Scale

bars: 10 pm.

Bothalia 24,2(1994)

193

the high adaxial stomata] density in these species. H.

stenophylla , previously considered to be merely a form of

H. trifoliata (Schreiber 1967; Townsend 1985), is charac-

terized by having less than 100 abaxial stomata per mm2

and a substantially higher adaxial density than other

African species.

Papillate trichomes seem to be the primitive state from

which other states were derived. If the cell differentiation

in the development of the other trichome types were in-

vestigated, this could lead to a better understanding of the

phylogeny of Heteromorpha. The presence of small

tubercles (although sparse in some specimens) along the

leaf margin of the West African form of H. trifoliata raises

some doubt as to its present taxonomic position, and sug-

gests a closer affinity to the suffrutescent species H.

gossweileri , H. involucrata and H. pubescens. The abaxial

stomatal density distinguishes it from other suffrutescent

types with which it may be confused, namely some central

African forms of H. involucrata. The formal description

of this taxon has been indicated by other evidence, and

will be published elsewhere.

variation than the H. arborescens complex, and formal

recognition of infraspecific taxa may be useful.

CONCLUSIONS

Anomocytic stomata and papillate trichomes are con-

servative characters at the generic level. The density

and distribution of stomata are of limited value at this

level, but show some pattern at the species level.

Heteromorpha sensu stricto differs in the diversity of

trichome types, and this character is useful to distin-

guish some of the species.

Epidermal characters provide supporting evidence for

a less conservative treatment of the African species than

those of Cannon (1978) and Townsend (1985, 1989). The

degree of woodiness in Heteromorpha species is an im-

portant character and would seem to be correlated with

epidermal features. Without attention to habit, other char-

acters tend to be difficult to interpret.

H. pubescens and most forms of H. involucrata share,

along with other morphological characters, the distribution

of trichomes along abaxial midrib and venation, but are

distinguished on the basis of trichome type. Some forms

of H. involucrata exhibit deviation from the typical con-

dition of a hairy abaxial midrib. As currently cir-

cumscribed, this species shows as much if not more

ACKNOWLEDGEMENTS

Financial support from the Foundation for Research

and Development is gratefully acknowledged. We would

like to thank Dr W. Oldewage for his instruction and as-

sistance with the SEM.

FIGURE 5. — Structure of trichome

types, as seen in Figure 4, in leaf

transverse sections of Hete-

romorpha sensu stricto. A, ft.

involucrata , typical form: coni-

cal trichome on a tuberculate

base. B, H. involucrata, ‘ kass -

neri’ form: multicellular, long,

cylindrical trichome. C, H.

gossweileri: 1, tuberculate and

2, papillate trichomes. D, H. tri-

foliata, typical form: short,

cylindrical trichomes. E, H.

pubescens : filamentous

trichomes on a tuberculate base.

194

Bothalia 24,2 ( 1994)

FIGURE 6. — Some examples of trichome distribution in Heteromorpha sensu. stricto. A, H. trifoliata : adaxial midrib. B, H. involucrata: abaxial

view, margin only. C, H. involucrata, ‘ kassneri' form: margin and adaxial surface. D, H. pubescens : abaxial view, along entire venation.

Scale bars: A-C, 50 pm; D, 100 pm.

REFERENCES

BARANOVA, M. 1992. Principles of comparative stomatographic

studies of flowering plants. The Botanical Review 58: 49-99.

BURTT, B.L. 1988. A new shrubby genus of African Umbelliferae. Notes

from the Royal Botanic Garden Edinburgh 45: 493-501.

CANNON, J.F.M. 1978. Umbelliferae. Flora zambesiaca 4: 578-581.

Flora Zambesiaca Managing Committee, London.

FEDER, N. & O'BRIEN, T.P. 1968. Plant microtechnique: Some prin-

ciples and new methods. American Journal of Botany 55: 123-

142.

GUYOT, M. 1971. Phylogenetic and systematic value of stomata of the

Umbelliferae. In V.H. Heywood, The biology and chemistry of the

Umbelliferae: 157-176. (Supplement 1 to Botanical Journal of

the Linnean Society 64).

HUMBERT, H. 1956. Contributions a P etude de la Flore de Madagascar

et des Comores. Fascicle 5. Notulae Systematicae , Paris 15: 1 13—

134.

JACQUES-FELIX, H. 1970. Ombellales. Flore du Cameroun 10: 74-77.

Museum National d’Histoire Naturelle, Paris.

RAM, H.Y.M. & NAYYAR, V.L. 1974. A rapid method of obtaining

epidermal peels in plants by treatment with cupric sulphate and

hydrochloric acid. Stain Technology 49: 1 14—1 16.

SCHREIBER, A. 1967. Apiaceae. Prodromus einer Flora von Siidwest-

afrika 103: 1-9. Cramer, Lehre.

TILNEY, P.M. 1986. The taxonomic significance of anatomical and

morphological characters in the southern African species of Can-

thium Lam. (Rubiaceae). Ph.D. thesis. University of Pretoria.

TOWNSEND, C.C. 1985. Some notes on species of Heteromorpha (Um-

belliferae). Kew Bulletin 40: 843-850.

TOWNSEND, C.C. 1989. Umbelliferae. In R.M. Polhill, Flora of tropi-

cal East Africa: 37-41. Balkema, Rotterdam.

Bothalia 24,2: 1 95-202 ( 1 994)

Inflorescence morphology of Lachnaea and Cryptadenia (Thymelaeaceae)

J.B.P. BEYERS* and J.J.A. VAN DER WALT**

Keywords: Cryptadenia , inflorescence morphology, Lachnaea, Thymelaeaceae

ABSTRACT

The current delimitation of Lachnaea L. and Cryptadenia Meisn. is based on the inflorescence morphology. In Lachnaea

both indeterminate and determinate inflorescences occur, whereas in Cryptadenia only determinate inflorescences are present.

The indeterminate inflorescences in Lachnaea are capitate or umbellate. The determinate inflorescences in both genera

comprise a solitary, terminal flower. It is concluded that the two genera cannot be distinguished on inflorescence structure.

UITTREKSEL

Lachnaea en Cryptadenia word tans op grand van hul bloeiwyses onderskei. Beide onbepaalde en bepaalde bloeiwyses kom

by Lachnaea voor, terwyl by Cryptadenia net bepaalde bloeiwyses voorkom. Die onbepaalde bloeiwyses by Lachnaea is hofies

of skerms. Die bepaalde bloeiwyses by beide genera bestaan uit 'n enkel, terminale blom. Die gevolgtrekking word gemaak dat

die twee genera nie op grand van die struktuur van die bloeiwyses onderskei kan word nie.

INTRODUCTION

The Thymelaeaceae, which is regarded as a medium-

sized family comprising 50 genera and 720 species, occurs

in both temperate and tropical regions (Mabberley 1990).

Most genera belong to the subfamily Thymelaeoideae in-

cluding the genus Lachnaea L. and the genus Cryptadenia

Meisn. Both these genera are endemic in the Cape

Province.

In the classification systems of the Thymelaeaceae by

Endlicher (1847, sec. Domke 1934), Meisner (1857), Ben-

tham & Hooker (1880), Gilg (1894) and Domke (1934),

Lachnaea and Cryptadenia have always been placed next

to each other, reflecting their close affinity. Only one pre-

vious worker, Baillon (1880), did not regard Cryptadenia

as a separate genus but as a section of Lachnaea. In the

last taxonomic treatment of the two genera, Wright (1915)

followed the classification of Bentham & Hooker (1880).

The floral morphology of Lachnaea and its closest re-

lated genus, Cryptadenia, is similar. The Bowers are

bisexual, tetramerous, apetalous, with eight floral scales

inserted on the hypanthium below the insertion of the

eight stamens, which are arranged in two whorls of four

each. To distinguish between these two genera Wright

(1915) used the inflorescence structure. In Lachnaea he

regarded the flowers to be terminal, capitate or rarely

solitary, whereas in Cryptadenia he described them as

axillary, solitary and bibracteolate. A study of the descrip-

tions of the different taxa of both genera revealed that L.

axillaris Meisn., L. micrcintha Schltr. and L. ruscifolia

Compton have flowers which are axillary and solitary,

whereas the flowers of L. penicillata Meisn., according

to Wright (1915), are terminal and solitary. If one should

apply the criterion used by Wright (1915), the former three

* National Botanical Institute, RO.Box 471, Stellenbosch 7599.

**Department of Botany, University of Stellenbosch, Stellenbosch 7600.

MS. received: 1993-06-22.

species should rather be placed in Cryptadenia. Thus, the

criterion used by Wright does not hold.

A preliminary examination of herbarium specimens of

the Western Cape herbaria has brought to light numerous

misidentifications and incertae, illustrating the poor state

of our knowledge of Lachnaea and Cryptadenia. The con-

fusion which presently exists regarding the delimitation

of Lachnaea and Cryptadenia can be partly ascribed to

the inconsistencies in Wright’s interpretation of the in-

florescence morphology of these two genera (Wright

1915). As the inflorescence has been considered to be of

great taxonomic importance in the past, the study of the

inflorescence morphology was undertaken with the view

to improving our understanding of these two genera.

Meisner (1840) instituted three sections, Sphaero-

clinium Meisn., Conoclinium Meisn. and Microclinium

Meisn., within Lachnaea, based on the inflorescence mor-

phology. In his later publication of 1857 he followed the

same classification. In the section Sphaeroclinium he in-

cluded those taxa having a terminal, dense, many-

flowered capitulum, which was either involucrate or

evolucrate, the sessile flowers being arranged on a

moderately thick, globose receptacle. Meisner (1840,

1857) included L. buxifolia Lam. and L. filarnentosa

(Thunb.) Meisn. in this section. In the section Cono-

clinium he regarded the inflorescence as a terminal or sub-

terminal, few- to many-flowered, evolucrate capitulum.

Here the moderately thick receptacle was at first hemis-

pherical to conical but by later elongating, became sub-

cylindrical. From the regular arrangement of the flower

scars on the receptacle, he regarded the inflorescence as

a spike and not a capitulum. In this section he included

L. capitata (L.) Meisn. and L. densiflora Meisn. In the

section Microclinium he included those taxa having

flowers in sessile, terminal, subcapitate or subsolitary in-

florescences, or those rarely having axillary, solitary

flowers, namely L. axillaris, L. diostnoides Meisn., L.

ericoides Meisn. and L. penicillata Meisn. Meisner (1840)

196

Bothalia 24,2 (1994)

regarded the flowers of Cryptadenia as terminal, solitary

or geminate, or occasionally as axillary and solitary, but

in his later publication of 1857 he described the flowers

as being terminal and subsolitary.

Gilg (1894) regarded the inflorescences in Lachnaea

as usually being terminal, many-flowered heads, but oc-

casionally, when consisting of two flowers, as mostly axil-

lary. In Cryptadenia he regarded the flowers as solitary,

axillary, with two bracteoles.

Domke (1934) described the inflorescences in Lach-

naea as being usually terminal heads, which are basally

enclosed by an involucre, or congested heads without an

involucre. No mention was made of the solitary-flowered

inflorescence in his generic description of the genus. In

Cryptadenia he regarded the flowers as being solitary or

few, either terminal or axillary with two bracteoles.

Dyer (1975) followed Wright (1915) and also used the

inflorescence structure to distinguish between Lachnaea

and Cryptadenia. According to Dyer (1975) the flowers

in Lachnaea are arranged either in terminal, bracteate or

ebracteate heads or a congested spike, or are rarely

solitary, whereas in Cryptadenia the flowers are axillary

and solitary.

In the most recent publication on the inflorescence

morphology of the Thymelaeaceae, Weberling & Herkom-

mer (1989) regarded the inflorescences in Lachnaea as

being capitate or spicate, or having solitary, axillary

flowers borne on a proliferating spike as in L. axillaris.

In Cryptadenia they considered the flowers as being

solitary and terminal.

From the above literature survey there seems to be con-

sensus with regard to the terminal, many-flowered heads

but not with regard to the position of the single-flowered

inflorescences in Lachnaea. Similarly in Cryptadenia dif-

ferent views are expressed with regard to the position of

the inflorescence and the number of flowers in an inflores-

cence.

The aim of the present investigation was to determine

whether the inflorescence morphology could be used to

delimit the two genera.

MATERIALS AND METHODS

Material used in this study comprised herbarium

specimens and plants collected in the wild, with the ex-

ception of L. nervosa Meisn. of which fresh material was

unobtainable. Eighteen taxa were selected, 14 from Lach-

naea and four from Cryptadenia. The aim in selecting the

taxa was to have as broad a representation as possible of

all the taxa in the two genera. The criteria used for select-

ing the taxa were: 1, taxa representative of the three sec-

tions instituted by Meisner ( 1 840), taking in account the

variation in each section; and 2, taxa with solitary flowers.

Four of the five species of Cryptadenia currently

recognized were studied. Cryptadenia hreviflora Meisn.

was excluded as it is an intermediate taxon between Cryp-

tadenia grandiflora (L.f.) Meisn. and Cryptadenia uni-

flora Meisn. Levyns (1950) considered C. hreviflora as a

hybrid between the two species.

The 18 species studied were: Lachnaea aurea Eckl. &

Zeyh., L. axillaris , L. burchellii Meisn., L. buxifolia, L.

capitata , L. densiflora , L. diosmoides, L. ericoides, L.

eriocephala L., L. filamentosa , L. funicaulis Schinz, L.

nervosa , L. penicillata , L. ruscifolia , Cryptadenia filicaulis

Meisn., C. grandiflora , C. laxa Wright and C. uniflora

(nomenclature according to Arnold & De Wet 1993).

RESULTS

Inflorescence structure within Lachnaea

Both major types of inflorescences, as recognized by

Radford et al. (1974) and Cronquist (1988), namely in-

determinate and determinate, occur in Lachnaea.

Indeterminate inflorescences

Within the indeterminate inflorescences the capitulum

and the umbel are represented.

1. Species with capitula

L. buxifolia, L. capitata, L. densiflora and L. filamen-

tosa have terminal, multi-flowered, ebracteate capitula.

These capitula are borne singly at the ends of branches

on sericeous peduncles, which vary in length from 3-10

mm. The sessile flowers are arranged on a moderately

thick, convex receptacle, which elongates during the

flowering period, becoming narrowly conical or conical.

Different stages of flower development are present within

a capitulum. The fruiting stage may be present basally

while buds are still developing distally. An accurate num-

ber of flowers in an inflorescence is therefore not easily

determined. The number of mature flowers, at a given

time, varies from ± 50 in L. buxifolia, 20-50 in L. filamen-

tosa, ± 12 in L. densiflora and only 1-3 in L. capitata.

After flowering, vegetative growth is resumed by

lateral branches developing in the axils of the upper leaves

immediately beneath the capitulum. These will eventually

terminate in new capitula in the following flowering

period. However, some of these lateral shoots, as in L.

densiflora , may terminate in capitula within the same

flowering period. Lateral branches may also develop from

the axils of the leaves below the distal leaf on the main

flowering branches. These branches will, in the following

flowering period, be terminated by capitula (Figure 1).

2. Species with umbels

Two types of indeterminate umbels, namely bracteate

umbels as in L. eriocephala and ebracteate umbels as in

L. diosmoides, are recognized. The pedicels remain in the

old inflorescences for some time after the upper portion

of the flowers and the fruits have been shed. The number

of pedicels present indicates the number of flowers in each

inflorescence.

Bothalia 24,2 ( 1 994)

197

FIGURE 1. — Capitate inflorescences of Lachnaea species. A, capitulum of L. capitata, Beyers 128 , illustrating elongated receptacle after lower

flowers have been shed; B, capitulum of L. biixifolia , Beyers 122, with flowers partly removed. Diagrammatic illustration of branching pattern

of flowering branches: C, L. densiflora ; D, L. filamentosa: ■. remains of previous year's inflorescence; O, flowering capitulum; • ,

capitulum with fruits only; v, bud of new vegetative shoot.

2. 1 . Species with sessile bracteate umbels

Sessile, bracteate umbels occur in L. aurea , L.

eriocephala and L penicillata. In L. eriocephala (Figure

2) the inflorescence is comprised of about 40 shortly

pedicellate flowers, which are surrounded by a bracteate

involucrum consisting of four large bracts, in two whorls

of two. These bracts follow on the stem after the linear-

elliptic to lanceolate leaves. Similarly in L. aurea the ±

50-flowered umbel is surrounded by 8-10 bracts which

are spirally arranged. From the axils of the foliage leaves

immediately below the bracteate umbels, vegetative

growth is resumed by lateral branches in both species.

These lateral branches will eventually terminate in brac-

teate umbels in the following flowering period. Lateral

branching is not only restricted to the axil of the distal

leaf when the leaves are alternately arranged as in L.

aurea, or to the distal pair of leaves, when opposite as in

L. eriocephala, but may originate from the axils of the

other upper foliage leaves. These lateral branches are also

terminated by bracteate umbels in the following flowering

period. In both cases the lateral branches may elongate

considerably.

In L. penicillata (Figure 3) the inflorescence is also a

terminal bracteate umbel. The umbel, usually eight-

flowered, is surrounded by four bracts, in two whorls of

two each. Only the distal portion of a single mature flower

is visible at a time. Wright (1915) inadvertently regarded

the flowers as being ‘terminal, solitary, sessile7. The elon-

gated pedicels and buds enclosed by the bracts were ig-

nored by him. Lateral branching arises from the axils of

either the first or second pair of foliage leaves immedi-

ately below the inflorescence. These lateral branches may

elongate considerably or may be reduced to comprising

only one or two pairs of foliage leaves before being ter-

FIGURE 2. — L. eriocephala, Beyers 54. A, diagrammatic illustration of

branching pattern of flowering branches; B, bracteate umbel with

flowers and bracts removed; C, abaxial view of one of inner pair

of bracts; D, abaxial view of one of outer pair of bracts; ■.remains

of previous year’s inflorescence; V, umbel: b, scar of removed

bract; p. pedicel.

198

Bothalia 24,2 (1994)

FIGURE 3. — L. penicillata , Oliver &

Fellingham 9145. A, flower-

ing branch with a terminal

bracteate umbel; B, diagram-

matic illustration of branching

pattern of flowering branches;

■, remains of previous year's

inflorescence; V, umbel; b,

bract; fl, foliage leaf; v, new

vegetative shoot.

minated by an inflorescence. Up to three generations of

flowering branches may develop in one flowering period.

Vegetative growth is resumed by lateral branches develop-

ing from the axils of the upper foliage leaves of the last

flowering generation.

2.2. Species with sessile ebracteate umbels

In L. diosmoides, L. ericoides , L. junicaulis and L. ner-

vosa the flowers are borne in sessile, ebracteate umbels

at the tips of the branches. No bracts surround the in-

florescence as new vegetative growth arises from the axils

of the leaves immediately beneath the umbel (Figure 4).

The number of flowers per umbel varies among the dif-

ferent species and also within each species. In L. dios-

moides and L. junicaulis 6-20 flowers are present, where-

as in L. nerx’osa the number varies from 4—14 and in L.

ericoides from 2-8. As a result of the different develop-

mental stages of the flowers present in each umbel, only

a few mature flowers are present at a time. Lateral branch-

ing is resumed from the axil of the upper leaves below

the inflorescences but is not restricted only to the most

distal leaves immediately behind the inflorescence. In L.

nervosa (Figure 4) short, lateral branches also arise in the

axils of the leaves lower down on the main flowering

branch, which in the same flowering period are terminated

by inflorescences. Consequently the main flowering

FIGURE 4. — Diagrammatic illustration of branching pattern of flowering branches; A, L. ericoides ; B, L. nervosa. C, terminal ebracteate umbel in

L. nervosa, De Kock 152 , illustrating new vegetative shoot (v) in the axil of the distal foliage leaf (fl). ■. remains ot previous year's

inflorescence; V, umbel.

Bothalia 24,2 (1994)

199

branch has the appearance of a racemose inflorescence.

Similarly in L. diosmoides lateral vegetative shoots arising

in the axils of the leaves immediately below the inflores-

cence, may be terminated by inflorescences in the same

flowering period. Here they may overtop the umbel on

the main flowering branch, forming a dense cluster of

umbels, and at the same time reduced lateral shoots may

develop lower down in the axils of the foliage leaves of

the same main branch with a racemose appearance, as in

L. nervosa.

In L. ericoides (Figure 4) a first and second generation

of flowering shoots may occur. These shoots, as in the

previous taxa, develop from the axils of the leaves imme-

diately below the inflorescence. Below the most distal leaf

on the main flowering shoot, further lateral shoots may

develop which may terminate in inflorescences in the

same flowering period or in the next flowering period.

These flowering shoots are, unlike those in L. diosmoides ,

restricted to the upper leaves on the main flowering

branch. Vegetative shoots may also develop lower down

on the main flowering branches of the previous flowering

period which again will be terminated by inflorescences

in the following flowering period.

In L.funicaulis a pair of bract-like foliage leaves occurs

at the base of the umbels. These umbels appear bracteate

and resemble those of L. penicillata, but, unlike L. penicil-

lata, lateral vegetative growth develops in the axils of the

bract-like foliage leaves. These lateral vegetative shoots

will terminate in ebracteate umbels in the following

flowering period. Reduced lateral shoots also develop in

the axils of the upper leaves, behind the bract-like foliage

leaves on the main flowering branch, which may tenninate

in ebracteate umbels within the same flowering period,

forming a cluster of inflorescences towards the end of the

main flowering branch.

In L. burchellii (Figure 5), contrary to the interpretation

of Meisner (1840, 1857) and Wright (1925) who regarded

the inflorescences to be bracteate, the inflorescences are

terminal, sessile, ebracteate umbels. The umbels consist

of up to ten flowers, with 1 or 2 mature flowers at a time.

Vegetative growth is resumed from the axils of the leaves

immediately below the umbels. On some specimens the

inflorescences appear to be bracteate. These 'bracteate'

umbels are in fact reduced lateral branches, each ter-

minated by an ebracteate umbel. The leaves on these

branches differ in size and shape from the foliage leaves

on the rest of the plant. In the axil of the most distal leaf

FIGURE 5. — L. burchellii. A, diagrammatic illustration of branching pattern of flowering branches; B, terminal ebracteate umbel, Spreeth 155', C,

short lateral flowering shoot illustrating new vegetative shoot (v) in axil of bract-like leaf, Spreeth 155: D, short lateral flowering shoot, Oliver

9251: E, elongated lateral flowering shoot showing similar small prophylls (p) basally; s, scar of caducous bract-like leaves; V, umbel.

200

Bothalia 24,2 ( 1994)

FIGURE 6. — L. axillaris. A, dowering

shoot illustrating new vegeta-

tive shoot in axil of distal leaf,

Morley 174 ; B, diagrammatic

illustration of branching pattern

of flowering branches; ■, scar

of flower of previous year; ©,

flower bud; O, open flower; •,

fruit.

on one of these reduced flowering branches, a well-

developed bud of the new vegetative shoot was observed.

The lower two pairs of leaves on some of the elongated

lateral flowering branches, resemble those modified

foliage leaves of the reduced flowering branches. These

leaves are often caducous. Vegetative growth is resumed

by lateral branches developing from the axils of the upper

leaves immediately below the umbel and may also

originate from the leaf axils lower down on the main

flowering branch. These lateral branches will terminate in

umbels in the following flowering period. Flowering

branches may develop at random on the main flowering

branch, as in L. nervosa. These flowering branches arise

from the axils of the leaves behind the most distal leaf

pair during the same flowering period. The main flowering

branch thus has the appearance of a racemose inflores-

cence.

Determinate inflorescences

Meisner (1840) described the flowers of L. axillaris as

being axillary, opposite or scattered, always solitary, with

two intra-axillary bracteoles. In his later publication

(1857) he referred to the flowers as being subsolitary, axil-

lary or rarely terminal. Wright (1915) regarded the flowers

as being axillary and solitary. According to Weberling &

Herkommer (1989) the flowers of L. axillaris are solitary,

axillary with two transverse bracteoles.

The flowers of L. axillaris were found to be solitary

and terminal. A well-developed bud of the new vegetative

shoot occurs in the axil of one of the leaves of the pair

of foliage leaves immediately below the flower (Figure

6). Lateral branches, each terminated by a solitary flower,

develop at random on the main flowering branches within

the same flowering period. These flowering branches arise

from the axils of the foliage leaves below the leaf pair

immediately behind the terminal flower. These lateral

flowering branches vary in length and may even be

reduced to having one pair of opposite leaves. Conse-

quently the main flowering branch may have the ap-

pearance of a racemose or spicate inflorescence (Figure

6). Previous authors inadvertently regarded these leaves

immediately behind the solitary flower as transverse brac-

teoles. It was found that the new vegetative growth

originates in the axils of these leaves and terminates in

flowers in the following flowering period. This growth is

not always visible on herbarium material as specimens

are usually collected when they are in full flower.

The flowers of L. mscifolia were regarded by Compton

(1953) as being ‘solitary, axillary, sessile’. On studying

fresh material in the fruiting stage, well-developed vegeta-

tive buds were found in the axils of the bracteoles (Figure

7). These bracteoles are in fact bracteose foliage leaves

similar to those found on the short lateral flowering shoots

in L. burchellii. In L. ruscifolia the flowers are therefore

solitary and terminal on much reduced, lateral, flowering

shoots which develop at random in the axils of the foliage

leaves on the main flowering branches giving them a spi-

cate appearance (Figure 7). Occasionally the lateral

flowering shoot may consist of an additional pair of

foliage leaves between the bracteose leaves (prophylls)

and the flower (Figure 7). No terminal flower was ob-

served on the main branches probably due to the abortion

of the apical meristem. From the axil of the leaf behind

the aborted meristem new vegetative growth may resume

or a reduced flowering shoot may develop (Figure 7). Two

scarious prophylls which resemble the bracteose leaves

on the lateral flowering shoot, occur at the base of the

developing lateral vegetative shoot (Figure 7).

Thus, in both L. axillaris and L. ruscifolia the inflores-

cences are determinate, consisting of solitary, terminal

flowers.

Inflorescence structure within Cryptadenia

The inflorescences in Crytadenia are all cymose. In all

the taxa well-developed buds of the new proliferating

shoot develop in the axils of the upper leaf pair immedi-

ately behind the flower (Figure 8). These vegetative shoots

usually terminate in flowers in the following flowering

period, except in C. filicaulis and C. grandiflora where

they may terminate in flowers in the same flowering

period. Lateral branches may also arise at random from

the axils of the leaves beneath the distal pair below the

terminal flower on the main flowering branch. These

branches vary in length and may even be reduced to only

the terminal flower and a pair of foliage leaves as in C.

filicaulis (Figure 8). Consequently the main flowering

branch, as in L. axillaris, has the appearance of a racemose

Botha] ia 24,2(1994)

201

or spicate inflorescence. Lateral branches, each terminat-

ing in a solitary flower in the following flowering period,

may also develop from the axils of the leaves lower down

on the main flowering branches (Figure 8).

DISCUSSION

In the genus Lachnaea the flowers are arranged in ter-

minal, indeterminate, capitate or umbellate inflorescences,

or they are solitary and terminal. In Cryptadenia the

flowers are solitary and terminal. Determinate inflorescen-

ces occur in both Lachnaea and Cryptadenia, whereas

indeterminate inflorescences occur only in Lachnaea.

Table 1.

In both genera the differentiation of a long shoot/short

shoot system can be observed. In some taxa within Lach-

naea and Cryptadenia this system is more conspicuous

than in others. In both genera new vegetative growth

arises from the axils of the foliage leaves immediately

below the inflorescences, and this may terminate in an

inflorescence within the same flowering period. Thus two

generations of flowering branches may occur together on

a plant (Figures 4 & 8).

Weberling & Herkommer (1989) regarded the terminal,

single-flowered inflorescence found in Cryptadenia as a

monotelic inflorescence. The inflorescence in L. axillaris

and L. ruscifolia can therefore be regarded as monotelic.

The polytelic inflorescence on the other hand would, ac-

cording to their terminology, include the capitulum and

umbel in Lachnaea. According to Weberling (1983) the

polytelic type of inflorescence has probably been derived

repeatedly from the monotelic type during the evolution

of angiosperms by the reduction of the terminal flower

and specialization of the paracladia of the monotelic sys-

tem. The distal elements are reduced to single lateral

flowers or lateral cymes, which constitute elements of an

apical system composed of lateral flowers. Therefore the

floral axis, instead of terminating in a single flower, ter-

minates in a multi-flowered polytelic inflorescence.

According to Weberling & Herkommer (1989) Gony-

stylus Teijsm. & Binn. and Amyxa van Tiegh. of the Gony-

styloideae which is regarded as a relatively primitive

group, have monotelic synflorescences (synflorescence

according to Weberling 1983). Within the Thyme-

laeoideae, the Gnidioideae and probably the Aquila-

rioideae, certain taxa were also found to have monotelic

synflorescences. They came to the conclusion that, con-

sidering the other more or less primitive characters and

the different taxonomic evaluation of those combinations,

it was impossible to draw any taxonomic conclusions ex-

clusively from the existence of the monotelic synflores-

cences within those taxa.

FIGURE7. — L. ruscifolia. A, branch illustrating aborted apical meristem (a) being displaced by new lateral shoot developing from axil of distal

foliage leaf .Marshall 39; B, main branch with short lateral flowering shoot, Vlok 166; C, diagrammatic illustration of branching pattern

of flowering branches; D, flower bud with two bracteose leaves (p), Vlok 166 ; E, vegetative shoot (v) arising from axil of one of bracteose

leaves; f, flower; fl, foliage leaf; A, aborted apical meristem; ©, flower bud; O, open flower; •.fruit; ■. scar of flower of a previous

year.

202

TABLE 1. — Inflorescence characters of Cryptadenia and Lachnaea

Weberling & Herkommer (1989) regarded the ramifi-

cation type of the polytelic synflorescences in the Thyme-

laeaceae to be thyrsic. Within many genera, according to

them, these synflorescences have been reduced to

racemes, spikes or umbels and in some taxa, as in Lach-

naea, the umbel-like aggregation of flowers is combined

with the formation of an involucrum.

From the above one could conclude that within Lach-

naea the terminal, solitary flower is the primitive state

and that the bracteate umbel is the advanced state.

CONCLUSION

The inflorescence morphology revealed determinate and

indeterminate inflorescences in Lachnaea and only deter-

minate inflorescences in Cryptadenia. In both genera the

determinate inflorescence comprises a solitary, terminal

llower. No distinct differences with regard to the inflores-

cence morphology could be found between these two genera.

Therefore the inflorescence structure can not, as in the past,

be used to distinguish between the two genera.

REFERENCES

ARNOLD, T.H. & DE WET, B.C. 1993. Plants of southern Africa: names

and distribution. Memoirs of the Botanical Survey of South Africa

No. 62.

BAILLON, H. 1880. The natural history of plants, Vol. 6. Reeve, London.

BENTHAM, G. & HOOKER, J.D. 1880. Genera plantarum, Vol. 3.

Reeve, London.

COMPTON, R.H. 1953. Lachnaea ruscifolia. Journal of South African

Botany 19: 132.

CRONQUIST, A. 1988. The evolution and classification of flowering

plants, 2nd edn. New York Botanical Garden, Bronx, New York.

DOMKE, W. 1934. Untersuchungen liber die systematische und

geographische Gliederung der Thymelaeaceen nebst einer

Neubeschreibung ihrer Gattungen. Bibliotheca Botanica 27: 1-

151.

DYER, R.A. 1975. The genera of southern African flowering plants,

Vol. I . Department of Agricultural Technical Services, Pretoria.

G1LG, E. 1894. Thymelaeaceae. In A. Engler & K. Prantl, Die Natiir-

lichen Pflanzenfamilien T.III Abt. 6a: 216-245. Leipzig.

Bothalia 24,2 (1994)

FIGURE 8. — Inflorescence structure and branching patterns of Cryp-

tadenia species. A, flowering shoot in C. laxa. Bodkin sub Guthrie

3585. Diagrammatic illustration of branching pattern of flower-

ing branches: B, C. filicaulis; C, C. uniflora; ©, flower bud; O,

open flower; •, fruit; ■, scar of flower of a previous year.

LEVYNS, M.R. 1950. Thymelaeaceae. In R.S. Adamson & T.M. Salter,

Flora of the Cape Peninsula. Juta, Cape Town.

MABBERLEY, D.J. 1990. The plant-book. Cambridge University Press,

Cambridge.

MEISNER, C.F. 1840. Synopsis Thymelaearum, Polygonearum et

Begoniarum Africae Australis, imprimus a cl. J.J.Drege lectarum.

Linnaea 14: 385-516.

MEISNER, C.F. 1857. Thymelaeaceae. In A.P. de Candolle, Prodromus

systematis naturalis regni vegetabilis 14: 573-580. Victoris Mas-

son. Paris.

RADFORD, A.E., DICKISON, W.C., MASSEY, J.R. & BELL, C.R.

1974. Vascular plant systematics. Harper & Row, New York.

WEBERLING, F. 1983. Fundamental features of modem inflorescence

morphology. Bothalia 14: 917-922.

WEBERLING, F. & HERKOMMER, U. 1989. Untersuchungen zur In-

floreszenz-Morphologie der Thymelaeaceen. Tropische und Sub-

tmpische Pflanzenwelt 68: 1-124.

WRIGHT, C.H. 1915. Thymelaeaceae. In W.T. Thiselton-Dyer, Flora

capensis 5,1: 1-80. Reeve, London.

WRIGHT, C.H. 1925. Thymelaeaceae. In W.T. Thiselton-Dyer, Flora

capensis 5,4: 583, 584. Reeve, London.

Bothalia 24,2: 203-210(1994)

Morphological and ultrastructural variations in Schizaea pectinata

(Schizaeaceae: Pteridophyta)

B.M. PARKINSON*

Keywords: exospore structure, morphology, perispore formation, Schizaeaceae, Schizaea pectinata, sporogenesis, tapetal organisation, ultrastructure

ABSTRACT

Schizaea pectinata (L.) Sw. was collected from the extreme ends of its geographical range in South Africa for a study of

sporangial development, sporogenesis and tapetal organisation. Differences were noted in the gross morphology, in sporangium

size, spore size and in the patterning of the outer exospore from the two sites. Coiled structures were associated with the

development of the inner perispore in spores collected from the Transvaal, whereas dense, heterogeneous bodies were associated

with the formation of this layer in spores from the Cape. Differences were also noted in the organisation of the tapetum. A

cellular, parietal tapetum and a plasmodial tapetum were present in the Cape material when the spores had developed the

sculptured outer exospore. In sporangia from the Transvaal, however, only a plasmodial tapetum was present at the same stage

of sporoderm development. A detailed study of S. pectinata throughout its distribution is required to determine the taxonomic

importance of these findings.

UITTREKSEL

Schizaea pectinata (L.) Sw. is in die twee uithoeke van sy verspreidingsgebied in Suid-Afrika versamel vir ’n ondersoek van

sporangiumontwikkeling, sporogenese en tapetumorganisasie. Verskille in algehele morfologie, sporangiumgrootte,

spoorgrootte en in die versiering van die buitenste eksospoor, is in die twee versamelplekke aangeteken. By spore wat in die

Transvaal versamel is, is gekrulde strukture met die ontwikkeling van die binneste perispoor geassosieer, terwyl digte,

heterogene strukture met die vorming van hierdie laag by Kaapse spore, geassosieer is. Verskille in die organisasie van die

tapetum is ook waargeneem. 'n Sellulere, parietale tapetum en ’n plasmodiese tapetum het in die Kaapse materiaal voorgekom

by spore waar die versierde buitenste eksospoor ontwikkel het. By sporangiums wat in die Transvaal versamel is, was daar teen

dieselfde stadium van sporodermontwikkeling egter slegs ’n plasmodiese tapetum teenwoordig. ’n Breedvoerige ondersoek van

5. pectinata , regdeur die organisme se verspreiding, word benodig om die taksonomiese belang van hierdie bevindings te bepaal.

INTRODUCTION

An investigation of sporangial development, sporo-

genesis and tapetal organisation in Schizaea pectinata (L.)

Sw. was carried out on material collected from Ysterkroon

in the Northern Transvaal (2429BB Zebediela) and from

the Cape of Good Hope Nature Reserve (341 8AD

Simonstown). The Transvaal material was collected at an

altitude of 2 046 m in an area of vegetation described as

Northeastern Mountain Sourveld (Acocks 1988). The

plants were small, approximately 80 mm high, and were

found in well-protected sites at the bases of outcrops of

Black Reef quartzite. The plants were obscured by large

tussocks of Themeda triandra Forssk. and other coarse

grasses. Plants from the Western Cape were collected from

several sites, at altitudes below 150 m, all of which had

well-drained, highly leached, shallow sandy hthosols in

areas of Mesic Mountain Fynbos (Macdonald, Clark &

Taylor 1989). These plants regenerated quickly after fire,

becoming fertile after about four months of growth in

open situations. They gradually became overgrown and

shaded as other fynbos plants regenerated. In the second

and subsequent years following fire they produced few

new fronds. Voucher specimens (Cape J 06727 3, Trans-

vaal J067274) are housed in the C.E. Moss Herbarium

* Department of Botany, University of the Witwatersrand, Private Bag 3,

WITS 2050.

MS. received: 1992-11-26.

(J). In studying the ontogeny of the sporoderm, several

features were noted which differed in the specimens from

the two sites. These included variations in the sculpturing

of the outer exospore and in structures involved with the

development of the inner perispore. This led to a closer

study of the material to ascertain whether the differences

were constant features.

MATERIALS AND METHODS

Material was fixed in the field in 2% paraformaldehyde

and 3% glutaraldehyde in 0.08 M Pipes buffer at pH 8.0

(Colhoun & Steer 1981), washed in ice-cold buffer and

post-fixed on ice using 2% OsOq followed by washing

and dehydration through a graded acetone series.

Specimens were transferred into propylene oxide, in-

filtrated with resin using mixtures of propylene oxide and

resin and finally embedded in Epon (Luft 1961).

Sections 1 pm thick were stained in toluidine blue for

light microscopy and 60 nm ultra-thin sections were

stained in uranyl acetate and lead citrate for viewing in a

Jeol 100S transmission electron microscope at 80 Kv.

Specimens for scanning electron microscopy were

selected from material in primary fixative but were not

post-fixed. They were washed in buffer, passed through a

graded ethanol series, transferred to propylene oxide and

dried by the critical point method in a Balzers Union CPD

model 020. The specimens were mounted onto aluminium

204

Bothalia 24,2 (1994)

stubs coated with pressure sensitive adhesive and coated

with gold-palladium prior to viewing in a Jeol JSM-840

microscope at 15 Kv.

Sporal features were observed on fixed and processed

material from the two sites and a quantitative survey was

also carried out on fixed material.

Measurements of the sporangia and the spores from

each of the collection sites was based on a sample size

of 50 specimens. Sporangium length was measured from

the base of the capsule to the top of the annulus and the

width was measured at the widest point. The length and

width of spores complete with perispore were recorded.

RESULTS AND DISCUSSION

Gross morphology

Plants from the Transvaal were small, approximately

100 mm high with only a few fronds which had

regenerated after fire (Figure 1A). Between seven and

nine pairs of modified pinnae were supported on a straight

rachis held at an angle of about 100° from the photosyn-

thetic stipe.

Plants collected from the Cape (Figure IB) were

robust, about 200 mm high and formed extensive clumps

with large numbers of fronds (± 50) which had

regenerated after fire. The pinnae pairs numbered between

14 and 18. The rachis passed through a straight phase

during the unfolding of the crozier but was distinctly

curved at maturity.

Variations in the gross morphology of the plants from

the two sites which are approximately 2 000 km apart,

were initially thought to indicate ecotypes of S. pectinata.

Variation in size of specimens collected at different al-

titudes had been commented on by Roux (1979). There

are known cases of exceptional morphological variability

within populations in other ferns from disjunct parts of

their range, as in Thelypteris palustris Schott (Tryon &

Lugardon 1991). Tryon & Tryon (1982) stated that the

systematics of the tropical American Schizaea Sm. are not

adequately known, largely due to a lack of field studies

necessary to establish the extent of variation within the

species and that there may be greater morphological diver-

sity than is currently recognised. The latter comment

probably also applies to the southern African members of

the genus, as confirmed by the anomalous results obtained

in this material.

Spore and sporangium size

Minimum and maximum dimensions of spores and

sporangia are presented in Table 1 and sample mean

values and standard deviations are presented in Table 2.

All measurements were statistically analysed by the

Student’s two sample t test (Parker 1979) and the differen-

ces were found to be statistically significant.

In the Cape sample, 76% of the spores were found in

a narrow range between 84 pm and 88.5 pm in length

FIGURE 1. — Gross morphology of plants of Schizaea pectinata. A,

J067274 from Ysterkroon in the Wolkberg, Transvaal; B,

.1067273 from the Cape of Good Hope Nature Reserve.

Bothalia 24,2 (1994)

205

TABLE 1 . — Spore and sporangial size in S. pectinata (pm )

while 80% of the Transvaal spores lay in a range between

105.5 pm and 115 pm.

A narrow range of variation in width was also found

in the Cape spores where 72% measured between 55.2

pm and 60 pm and 66% of the spores from the Transvaal

population measured between 60 pm and 67.2 pm. When

individual measurements of spore length and width were

plotted, the scattergram (Figure 2A) showed that there was

no overlap between the two populations with respect to

spore size.

A similar trend was seen in dimensions of sporangia

from the Cape sample where 84% of the sporangia lay

within a relatively narrow range between 580 pm and 650

pm in length, and in the Transvaal sample 76% of the

sporangia were found in the range between 698 pm and

744 pm.

Outer exospore sculpturing

The exospore in 5. pectinata consists of two layers

(Parkinson 1991). The inner exospore is a smooth layer

approximately 85 nm wide. The outer exospore which

forms the bulk of the exospore is sculptured and reaches

a maximum thickness of between 4 pm and 5 pm. The

sculpturing differs in the Transvaal and Cape material

(Figures 3 & 4). Spores from the Transvaal site (Figures

3A, C; 4A) have indentations (punctae) which are ap-

proximately 1 pm in diameter with ridges of the same

dimension separating them. The ridges have an uneven

but continuous surface and the inner surface of the punctae

is smooth. Spores from the Cape site (Figures 3B, D; 4B)

are also punctate. The punctae however, are 1.5 pm to

2.0 pm in diameter with uneven, 1 pm to 2 pm wide

ridges separating them. The whole surface is uneven, con-

sisting of irregular, juxtaposed granules.

Sporangial width showed a greater degree of variation

than sporangial length with 60% of the sporangia from

the Cape measuring between 372 pm and 418 pm and

78% of the sporangia from the Transvaal sample ranged

from 442 pm to 512 pm wide.

When length and width of individual sporangia were

plotted (Figure 2B) the scattergram revealed only a min-

imal amount of overlap between the two populations.

The systematic potential of spores with respect to size

and spore morphology has long been recognised (Wood

1973). Differences in spore size in the two Schizaeci

samples could indicate a difference in ploidy between the

two populations. Tryon & Lugardon (1991) found spores

of diploid Polystichum Roth species to have smaller

spores than tetraploids but they also found that spores

from disjunct populations of Thelypteris palustris showed

significant variation in size. It will be necessary to inves-

tigate the ploidy of the two populations and also to sample

populations from the entire distribution range before the

full significance of the present findings may be assessed.

TABLE 2. — Statistical analysis of spore and sporangial size in S. pec-

tinata (pm). For pairs of data within columns p< <0.01 % by two

sample t test

The differences in exospore structure could be the

result of the differences in the habitats of the two popula-

tions sampled. It has been suggested that the surface com-

plexity of spores of Pyrrosia Mirb. and Asplenium L. may

135

130

125

120

115

f 110

i 105

o>

i ioo

95

90

85

80

O

O

o

o ©

o

+ Cape spores

O Transvaal spores

50 55 60 65 70 75 80

Width in pm

Cape sporangia

Transvaal sporangia

FIGURE 2. — Scattergrams derived from measurements of 5. pectinata.

A, spore size; B, sporangial size.

206

Bothalia 24,2 (1994)

FIGURE 3. — Comparison of spore

size and features of outer exo-

spore sculpturing in S. pec-

tinata. A, C, spore surface of

Transvaal material; some of

surface debris is a preparation

artefact. B, D, spore surface of

Cape material; surface debris

consists of spherical particles

which may be associated with

early development of inner

perispore. Scale bars: A, B, 10

pm; C, D, 2 pm.

be related to ecological specialisations, i.e. whether the

plants are epiphytic, lithophytic etc. (Tryon 1990). Plants

of S. pectinate i at both sites were terrestrial. Correlations

between spore morphology and overall morphology in the

Thelypteridaceae have been shown to follow the

taxonomic groupings of other authors based on purely

morphological grounds (Wood 1973). However, since

there have been few studies on the ultrastructure of the

exospore in this genus or in the ferns as a whole, it is

difficult to assess the taxonomic significance of the varia-

tion in exospore structure in S. pectinata without further

study.

Formation of the inner perispore

In the spores from both the Cape and the Transvaal,

the inner perispore consisted of a darkly staining, discon-

tinuous and heterogeneous layer which was laid down on

the ornamented surface of the outer exospore. In the

material from the Cape (Figures 4B; 5A) the deposition

of the inner perispore was associated with dense,

heterogeneous spherical bodies. In the spores from the

Transvaal at the same stage of development (Figure 4A)

coiled structures were found in close proximity to the

developing inner perispore. There is some evidence

(Parkinson 1991) that these bodies are derived, at least in

part, from the plasmodial tapetum which disappears at

about this time. They are thought to contain some

sporopollenin as the perispore has been shown to be

acetolysis resistant (Parkinson 1991 ). These structures also

differ structurally and functionally from the spheroids in

Psilotum nudum (L.) P. Beauv. (Parkinson 1988) and

spherical structures in 5. pectinata (Figure 5B) termed

composite bodies (Parkinson 1990) which are present

during the formation of the outer perispore. I suggest that

the coiled and dense bodies are vehicles for the transport

of materials, particularly sporopollenin or its precursors,

from the plasmodial tapetum to the developing inner

perispore.

Outer perispore

The junction between the inner and outer perispore

layers was clearly demarcated in section, by an electron

lucent area. The inner perispore was a narrow, darkly

staining, heterogeneous layer, whereas the outer perispore

Bothalia 24,2 (1994)

207

FIGURE 4. — Structures associated with the formation of inner perispore in S. pectinata. A, section through part of spore wall of Transvaal

material. Sculptured outer exospore (E) with deep indentations, covered by narrow, heterogeneous layer of greater electron density, the

inner perispore. Large bodies (arrowed) have convoluted or coiled appearance. Smaller globules (arrow-heads) found attached to or close

to developing spore wall. B, section through part of spore wall of Cape material. Sculpturing of outer exospore (E) with shallowly rounded

projections covered by narrow, heterogeneous layer of greater electron density, the developing inner perispore. Spherical bodies ( arrowed)

dense, but show some substructure or heterogeneity and are attached to developing spore wall. Scale bars: A. B. 0.5 pm.

FIGURE 5. — A, rounded protrusions of outer exospore (E) of spore from Cape material during development of inner perispore. Note large size of

dense bodies in sporangial loculus associated with this development. B, composite bodies from sporangial loculus from Transvaal material

occur during final stages of spore wall development when outer perispore is being deposited. Similar structures also occur in the Cape material.

Scale bars: A, 2 pm; B, 0.5 pm.

208

Bothalia 24,2 ( 1994)

was not so darkly stained and often had a striated ap-

pearance in section (Parkinson 1991). Composite bodies

were associated with its development in both the Cape

and the Transvaal material (Figure 5B). The outer

perispore and the composite bodies were shown to contain

silicon (Parkinson 1990) and phenolics (Parkinson 1992).

The outer perispore was frequently displaced from the un-

derlying layers during handling of the material. There

were no observable differences between the outer

perispore of spores from the Transvaal and the Cape.

The structure of the perispore in ferns and fern allies

has been discussed by Hennipman (1970), Lugardon

(1974), Schraudolf (1984) and Uehara & Kurita (1989a

& b) but the ontogeny of the perispore layer is poorly

known. The dense bodies and the coiled structures

reported here are not the globules scattered on the spore

surface in species with a thin perispore (Lugardon 1981)

and which were regarded as the counterpart of orbicules

or Ubisch bodies in pollen. Fern spores used to be

described as perinous or non-perinous but work at the

electron microscope level (Lugardon 1971, 1974) has

shown that whereas the perine/perispore may be difficult

to detect with light microscopy, genera which were

originally described as being without a perispore have

now been shown to possess this layer. Tryon & Tryon

(1982) called for a re-examination of distinctions between

genera based on the presence or absence of a perispore

and characteristics of its formation and final structure, as

it may be taxonomically important.

Tapetal organisation

Tapetal organisation has been well studied in the an-

giosperms and Goebel (1905) recognised two types of

tapeta, secretory and plasmodial, between which transition

forms occur (Foster & Gifford 1959). The range of tapetal

types and structural variations in the Embryophyta is large

(Pacini, Franchi & Hesse 1985) but there have been few

studies dealing with tapetal ontogeny and structure in the

lower vascular plants.

A detailed, ontogenetic study of the tapetum has been

carried out on S. pectinata from the Cape (Parkinson

1991) and this work will form the basis of a separate

publication (in preparation). Essentially, what has been

determined is that a central, tetrahedral, archesporial initial

cell is responsible for the formation of a tapetal initial

layer. These cells then divide periclinally initiating the for-

mation of an inner and an outer tapetal layer. The inner

layer differentiates into a periplasmodial tapetum as-

sociated with the developing archesporial tissue and the

outer layer differentiates into a cellular, parietal tapetal

layer (Parkinson 1991). A complete ontogenetic study of

FIGURE 6. — Sections through sporangia: A, showing sculptured nature of outer exospore in S. pectinata from Transvaal material. Spores associated

with last remnants of periplasmodial tapetum (arrow-heads). No evidence of cellular, parietal tapetum which would be situated at position

marked by asterisks (*) adjacent to cells of sporangium wall. B, from Cape material. Sculptured outer exospore has developed and spores

associated with periplasmodial tapetum (arrow-heads). Attenuated, cellular, parietal, tapetal layer (*) adjacent to cells of sporangium wall.

Scale bars: A, B, 10 pm.

Bothalia 24,2(1994)

209

the tapetum from material from the Transvaal has not been

completed. In sections through sporangia from the

Transvaal material, at the stage when the outer exospore

was fully developed but perispore development was not

yet complete (Figure 6A), only a periplasmodial tapetum

was present. In sections of the Cape material at the same

stage of development (Figure 6B) both a cellular, parietal

tapetal layer and a periplasmodial tapetum were present.

The presence of a cellular, parietal tapetum and a plas-

modial tapetum existing concurrently in S. pectinata from

the Cape is similar in some respects to the condition pre-

viously reported in Psilotum nudum (Parkinson 1987). The

condition also exists in other members of the Schi-

zaeaceae, namely Anemia phvllitidis (L.) Sw. (Schraudolf

1984) and Lygodium Sw. (Binford 1907), as I have de-

duced from illustrations in these papers. It almost certainly

exists in Schizaea tenella Kaulf. (Parkinson 1991).

There are examples in the literature where a parietal

tapetum breaks down and becomes invasive during later

stages of pollen development as in Pinus banksiana Lamb.

(Dickinson & Bell 1972, 1976) and Beta vulgaris L.

(Hoefert 1971). There are also descriptions of an invasive

but non-syncytial type of plasmodium in Canna L. (Tiwari

& Gunning 1986a, b) which is regarded by these authors

as being intermediate between the secretory and plas-

modial forms. The tapetal condition in S. pectinata from

the Cape is interpreted as being dimorphic (Parkinson

1991) and the present author considers it to be a more

truly transitional form between the secretory and plas-

modial condition than the one described in Canna.

The significance of the differences noted in the condi-

tion existing in the material from the Cape and from the

Transvaal, at the stage when outer exospore development

has been completed, lies in the fact that in studies carried

out on the angiosperms, the timing of events in the

tapetum at specific stages of microspore development is

noted as reflecting family- or genus-specific differences.

The change from one type to another within families or

genera was interpreted as being a significant evolutionary

trend (Pacini, Franchi & Hesse 1985).

CONCLUSIONS

The statistically significant differences in sporangium

and spore size, the differences in the outer exosporal or-

namentation, the differences in the formation of the inner

perispore and the variation in tapetal organisation indicate

that what has always been considered to be a single

species may constitute more than one element. S. pec-

tinata and S. tenella are the only species currently recog-

nised in southern Africa (Sim 1915; Schelpe 1970; Roux

1979; Jacobsen 1983; Schelpe & Anthony 1986; Burrows

1990).

Tapetal origin and form was a basis for suggesting

phylogenetic relationships within members of the

Embryophyta which have been studied more completely,

particularly the angiosperms and gymnosperms (Pacini,

Franchi & Hesse 1985). Tapetal organisation in the ferns

and fern allies may supply information which could be

applied to phylogenetic problems within these groups. It

will be interesting to see whether work by Roux (1992)

on certain Schizaeaceae, particularly Mohria , will support

the present findings based on ultrastructural details.

ACKNOWLEDGEMENTS

I wish to thank J.P Roux of the Compton Herbarium,

Kirstenbosch, for reading the first draft of the manuscript,

for useful discussions and for his constructive criticism.

To P. Tshabalala for photographic printing and to M.A.S.

Coetzee for the Afrikaans translation, my sincere thanks.

Grants from the University of the Witwatersrand Research

Committee are gratefully acknowledged.

REFERENCES

ACOCKS, J.P.H. 1988. Veld types of South Africa, 3rd edn. Memoirs of

the Botanical Survey of South Africa No.57.

BINFORD. R. 1907. The development of the sporangium of Lygodium.

Botanical Gazette 44: 214-224.

BURROWS. J.E. 1990. Southern African ferns and fern allies. Frandsen,

Sandton, South Africa.

COLHOUN, C.W. & STEER, M.W. 1981. Microsporogenesis and the

mechanism of cytoplasmic male sterility in maize. Annals of

Botany 48: 417 — 424.

DICKINSON, H.G. & BELL, RR. 1972. The role of the tapetum in the

formation of sporopollenin-containing structures during

microsporogenesis in Pinus banksiana. Planta 107: 205-215.

DICKINSON, H.G. & BELL. P.R. 1976. The changes in the tapetum of

Pinus banksiana accompanying formation and maturation of the

pollen. Annals of Botany 40: 1 101-1 109.

FOSTER, A.S. & GIFFORD, E.M. Jr 1959. Comparative morphology of

vascular plants. Freeman, San Francisco.

GOEBEL. K. 1905. Organography of plants. Part 2. English edn by B.

Balfour, Clarendon Press, Oxford.

HENNIPMAN. E. 1970. Electron and light microscopical observations

on the perine of the spores of some Bolbitis species (Filices). Acta

Botanica Neerlandica 19: 671-680.

HOEFERT, L.L. 1971. Ultrastructure of tapetal cell ontogeny in Beta.

Protoplasma 73: 397^-06.

JACOBSEN, W.B.G. 1983. The ferns and fem allies of southern Africa.

Butterworths, Durban.

LUFT. J.H. 1961. Improvements in epoxy embedding methods. Journal

of Biophysics and Biochemical Cytology 9: 409.

LUGARDON, B. 1971. Contribution a la connaissance de la morpho-

genese et de la structure des parois sporales chez les Filicinees

isosporees. Ph.D. thesis, Universite Paul Sabatier, Toulouse,

France.

LUGARDON, B. 1974. La structure fine de l'exospore et de la perispore

des Filicinees isosporees. II. Filicales. Pollen et Spores 16: 161 —

226.

LUGARDON, B. 1981. Les globules des Filicinees, homologues des

corps d'Ubisch des spermatophytes. Pollen et Spores 23: 93-124.

MACDONALD, I.A.W., CLARK, D.L. & TAYLOR, H.C. 1989. The

history and effects of alien plant control in the Cape of Good Hope

Nature Reserve, 1941-1987. South African Journal of Botany 55:

56-75.

PACINI, E„ FRANCHI, G.G. & HESSE, M. 1985. The tapetum: its form,

function and possible phylogeny in Embryophyta. Plata Svs-

tematics and Evolution 149: 155-185.

PARKER, R.E. 1979. Introductory statistics for biology, 2nd edn. The

Institute of Biology 's Studies in Biology No. 3. Edward Arnold,

U.K.

PARKINSON, B.M. 1987. Tapetal organization during sporogenesis in

Psilotum muium. Anttals of Botany 60: 353-360.

PARKINSON, B.M. 1988. Atapetal membrane in Psilotum nudum (L.) P.

Beauv. Annals of Botany 61 : 695-703.

PARKINSON, B.M. 1990. Silicon detected in the perispore and as-

sociated structures in Schizaea pectinata (Schizaeaceae). Electron

Microscopy Society of Southern Africa Proceedings 20: 87, 88.

PARKINSON, B.M. 1991. An investigation of sporangial development,

sporogenesis and tapetal organisation in Schizaea pectinata (L)

Sw. (Schizaeaceae). Ph.D. thesis, University of the Wit-

watersrand, South Africa.

210

Bothalia 24,2 (1994)

PARKINSON, B.M. 1992. The development of the spore wall in Schizaea

pectinata (Schizaeaceae). Electron Microscopy Society of

Southern Africa Proceedings 22: 79, 80.

ROUX, J.P. 1979. Cape Peninsula ferns. National Botanic Gardens of

South Africa, Kirstenbosch. Cape Province, South Africa.

ROUX, J.P. 1992. Systematic studies in the genus Mohria (Pteridophyta:

Anemiaceae) I. Comparative morphology and anatomy of the

rhizome and frond. South African Journal of Botany 58: 83-89.

SCHELPE, E.A.C.L.E. 1970. Pteridophyta. In A.W. Exell & E. Launert,

Flora Zambesiaca. Crown Agents for Oversea Governments and

Administrations, London.

SCHELPE, E.A.C.L.E. & ANTHONY, N.C. 1986. Pteridophyta. In O.A.

Leistner, Flora of southern Africa. Botanical Research Institute,

Department of Agriculture and Water Supply, Pretoria.

SCHRAUDOLF, H. 1984. Ultrastructural events during sporogenesis of

Anemia phyllitidis (L.) Sw. I. Spore wall formation. Beitrage zur

Biologie der Pflanzen 59: 237-260.

SIM, T.R. 1915. The ferns of South Africa , 2nd edn. Cambridge Univer-

sity Press.

TIWARI, S.C. & GUNNING, B.E.S. 1986a. Development of tapetum and

microspores in Canna L.: an example of an invasive but non-syn-

cytial tapetum. Annals of Botany 57: 557-563.

TIWARI, S.C. & GUNNING, B.E.S. 1986b. Development and cell sur-

face of a non-syncytial invasive tapetum in Canna: ultrastructural,

freeze-substitution, cytochemical and immuno-fluorescence

study. Protoplasma 134: 1-16.

TRY ON, A.F. 1990. Fern spores: evolutionary levels and ecological

differentiation. Plant Systematics and Evolution , Supplement 5:

71-79.

TRY ON, A.F. & LUGARDON, B. 1991. Spores of the Pteridophyta.

Springer- Verlag, New York, Heidelberg, Berlin.

TRYON, R.M. & TRYON, A.F. 1982. Ferns and allied plants with

special reference to tropical America. Springer- Verlag, New

York, Heidelberg, Berlin.

UEFLARA, K. & KURITA, S. 1989a. An ultrastructural study of spore

wall morphogenesis in Equisetum arvense. American Journal of

Botany 76: 939-95 1 .

UEFLARA, K. & KURITA, S. 1989b. Ultrastructural study of spore wall

morphogenesis in Ophioglossum thermale Kom. var. nipponicum

(Miyabe et Kudo) Nishida. Botanical Magazine. Tokyo 102: 413-

427.

WOOD, C.C. 1973. Spore morphology in the Thelypteridaceae. Botani-

cal Journal of the Finnean Society 67, Supplement No. 1: 191—

203.

Bothalia 24,2: 211-215(1994)

Plant defences against mammalian herbivores: are juvenile Acacia more

heavily defended than mature trees?

R. BROOKS* and N. OWEN-SMITH*

Keywords: Acacia , browsers, defence, tannins, polyphenols, thorns

ABSTRACT

Juvenile trees are expected to be more heavily defended against browsing mammals than mature plants. Juvenile and mature

trees of Acacia tortilis and A. nilotica occurring at Nylsvley, Northern Transvaal, were quantitatively compared in terms of some

potential chemical and physical defences. Neither species showed any significant difference between juvenile and mature trees

in terms of total polyphenol content, condensed tannin content, protein precipitating ability or protein content in leaves. Both

species showed age-class differences in spinescence. In A. nilotica , thorns on branch tips were longer and more closely spaced

and leaves were smaller in juveniles than in adults. Hence juveniles of this species appear to be physically more heavily

defended than mature plants. In A. tortilis , curved thorns were longer, but straight thorns were shorter than in mature trees. There

was no difference between age classes in overall thorn density, but juveniles had a higher curved to straight thorn ratio. It is not

obvious what the effects of these differences might be on mammalian browsers.

UITTREKSEL

Na verwagting is jong borne beter as volwasse plante teen blaarvretende soogdiere beskerm. Jong en volwasse borne van

Acacia tortilis en A. nilotica by Nylsvley, Noord-Transvaal, is kwantitatief vergelyk in terme van etlike potensiele chemiese en

fisiese verdedigingsmeganismes. Nie een van die spesies het enige beduidende verskil tussen jong en volwasse borne getoon in

terme van totale polifenolinhoud, gekondenseerde tannieninhoud, proteinpresipiteringsvermoe of prote'ieninhoud in blare nie.

Albei spesies het ouderdomsklasverskille in doringagtigheid getoon. By A. nilotica, was dorings op punte van takke langer en

digter opmekaar en blare was kleinerby jong borne as by volwassenes. Dit blyk dus dat jong borne van hierdie spesie fisies beter

beskerm is as volwasse plante. By A. tortilis, was krom dorings langer, maar reguit dorings was korter as in volwasse borne. Daar

was geen verskil in algehele digtheid van dorings tussen ouderdomsklasse nie, maar jong borne het 'n hoer verhouding krom tot

reguit dorings gehad. Dit is nie duidelik wat die uitwerkings van hierdie verskille op soogdierblaarvreters is nie.

INTRODUCTION

Woody plants that are browsed by mammals when still

juvenile may show retarded growth and increased time to

reach reproductive maturity (Bryant et al. 1983; Bryant

et al. 1991b). Hence, woody plant defences against mam-

malian herbivores could be expected to be expressed more

strongly in juveniles than in mature trees (Bryant &

Kuropat 1980; Bryant et al. 1983; Bryant et al. 1991a, b,

c). This has been documented in Alaskan paper birch

( Betula resinifera) browsed by snowshoe hare (Lepits

americanus) (Reichardt et al. 1984) and quaking aspen

(Populus tremuloides) browsed by beaver ( Castor cana-

densis) (Basey et al. 1990). The objective of this study

was to assess whether some potentially defensive traits

were expressed more strongly in juvenile Acacia trees

than in mature trees. No studies comparing anti -herbivore

defences of juvenile and mature Acacia trees have yet

been reported.

Defences can take the form of either chemical com-

pounds or physical stmctures. Chemical defences include

secondary metabolites (Freeland & Janzen 1974; Bryant

& Kuropat 1980; Cooper & Owen-Smith 1985; Cooper

et al. 1988; Bryant et al. 1991c), high fibre contents (Bell

1983) or low nutrient levels (Lundberg & Astrom 1990).

* Department of Zoology, University of the Witwatersrand, Johannesburg

2050.

MS. received: 1993-09-02.

Physical defences include thorns and spines (Cooper &

Owen-Smith 1986; Milewski et al. 1991).

Polyphenols, including condensed and hydrolysable

tannins are widespread among woody plant species

(Swain 1979) and are commonly implicated as quan-

titative defences against herbivory (Rhoades & Cates

1975; Van Hoven 1984; Cooper & Owen-Smith 1985;

Cooper et al. 1988; Teague 1989b; Du Toit et al. 1990;

Furstenburg & Van Hoven in press). A. tortilis trees have

low amounts of condensed tannins in their leaves,

whereas A. nilotica is relatively high in total polyphenol

content (Cooper & Owen-Smith 1985). Both species are

relatively palatable to browsing ungulates (Owen-Smith

& Cooper 1987).

There is circumstantial evidence for longer thorns

being more effective as defences against browsers than

shorter thorns in several Acacia species (Foster & Dagg

1972; Young 1987; Milewski et al. 1991). Cooper &

Owen-Smith (1986) noted that thorns were more effec-

tive in restricting leaf losses to browsers when leaves

were small. In Acacia karroo , the rate of intake of

browse by goats was positively related to leaf mass per

unit length of shoot (Teague 1989a). Thus leaf size and

thorniness might act together in defence of trees against

browsing ruminants. A. nilotica has paired, straight

thorns, while A. tortilis has both 'hooked' thorns and

straight thorns.

212

Bothalia 24,2 (1994)

MATERIALS AND METHODS

The study area was the Nylsvley Nature Reserve in

northern Transvaal, South Africa (24° 39' S, 28° 42' E).

Acacia tortilis and A. nilotica occur in the woodlands

flanking the floodplain and in disturbed sites of former

human habitation (Coetzee et al. 1976; Cooper & Owen-

Smith 1986).

Ten pairs of trees comprising a juvenile and a mature

plant no more than 50 m apart, were sampled for each

species. Sampling was restricted to the disturbed Acacia

woodland, and samples were paired to control for spatial

differences in soil nutrients and browsing pressure. Adult

trees were defined as those showing evidence of reproduc-

tive maturity (i.e. presence of flowers or seed pods). No

trees taller than 1.7 m were considered for the juvenile

class.

All collections took place on two consecutive days in

March 1992, because during late summer all leaves are

mature but not yet senescent. For each plant, leaves were

taken from the terminal 250 mm of five branches on the

northern side of the canopy at a height of between 0.75

and 1.7 m (within the browsing reach of impala and/or

kudu). All leaf collecting took place between 06h00 and

09h00. Leaves of each pair of juvenile and mature trees

were collected consecutively, with no more than 15

minutes between collection for members of any pair, to

eliminate the effects of short time-scale fluctuations in leaf

chemistry. Analysis of leaf nitrogen content provides a

check for differences in leaf age between the juvenile and

mature trees sampled.

Collected leaves were placed in plastic bags, and kept

in a cooler box with ice blocks until the end of the col-

lecting session (maximum 3 hours). At the end of the ses-

sion, leaves were frozen in a deep freeze at - 4° C. They

were kept frozen until used for weighing and extraction

for chemical analysis.

Physical defences

The length of all thorns within 250 mm of the branch

tip on the same branches from which leaves were col-

lected was measured to the nearest millimetre. The density

of thorns was measured by counting the number of thorns

or thorn pairs within 250 mm of the branch tip.

The frozen leaves from each tree were weighed to the

nearest 10 g. From these measurements, the mean fresh

leaf mass for each tree was calculated to give an index

of leaf size for each tree. The leaf matter used in extraction

and for protein analysis (about 2.0 g) was weighed out

from frozen leaf material. Several leaves were later dried

in order to determine the relationship between dry mass

and the mass of fresh leaf material so that chemical

parameters could be reported in terms of ‘percentage of

dry mass’.

Chemical analyses

Phenol ics were extracted according to the method

described by Hagerman (1977). Approximately 2.0 g leaf

matter was frozen with liquid nitrogen and ground in a

mortar. The crushed material was then centrifuged three

times at 2500 rpm using 20 ml of 70% acetone as solvent

in each iteration. The supernatant was poured off each

time and stored at 4° C until needed for chemical analysis.

Condensed tannin content was measured using the acid

butanol assay (Porter et al. 1986). The absorbances at 550

nm were standardised against purified sorghum tannin.

The total polyphenol content was determined using the

Prussian blue assay (Price & Butler 1977). Absorbance

was read at 720 nm. The standard was commercial tannic

acid made up from powder form in the laboratory with

70% acetone.

The protein precipitating ability of the chemicals in the

leaves was determined by means of radial diffusion using

the method described by Hagerman (1977). The diameter

of the ring of precipitated BSA in an agarose gel was

measured, the square of the diameter being proportional

to the amount of tannin in the sample (Hagerman 1977).

Protein content was estimated by determining nitrogen

content by Kjeldahl oxidation using sulphuric acid and a

selenium catalyst (Keeney 1982). The amount of am-

monium in the digest was determined colorimetrically fol-

lowing the method of Cataldo et al. (1975) and absorbance

was read at 655 nm. The absorbances were compared to

a standard curve plotted from the absorbances of dilutions

of an ammonium sulphate solution. Crude protein content

equals 6.25 x nitrogen concentration.

For each species, each variable was compared by

means of a Wilcoxon paired summed-ranks test (Siegel

& Castellan 1989) because it was not possible to confi-

dently assume normality in any of the parameters. The

alpha level of acceptance for significant results was 5 per-

cent. Tests were one-tailed tests of the hypothesis that

juveniles are more heavily defended than mature trees.

RESULTS

Heights of juvenile trees sampled (mean and range)

were as follows: Acacia nilotica 1.24 m (0.89-1.60 m),

A. tortilis 1.16 m (0.79-1.58 m).

Chemical measures

The total polyphenol content of leaves of juvenile A.

nilotica did not differ significantly from that of leaves of

the mature plants (Table 1). The protein precipitating

ability (as measured by radial diffusion) of the extracts

from juvenile and mature A. nilotica did not differ sig-

nificantly, and neither did the protein contents of juvenile

and mature plants. A. nilotica did not show any sign of

containing condensed tannins, in that the extracts did not

turn purple (indicative of condensed tannin) in the acid

butanol test.

The polyphenol and condensed tannin contents for

juvenile A. tortilis trees did not differ significantly from

those of mature plants, nor did crude protein content or

protein precipitating capacity (Table 1).

Bothalia 24,2(1994)

213

TABLE 1. — Comparative levels of potential chemical defences of juvenile and mature Acacia nilotica and A. tortilis. N = 10 trees

A. nilotica A. tortilis

Mean ± S.D. Sig. Mean ± S.D. Sig.

juv., juvenile; mat., mature; sig., significance.

Physical parameters

Thoms of juvenile A. nilotica were significantly longer

(P = 0.042) than those of mature trees (Table 2). The

thorns of juveniles were, on average one and a half times

as densely spaced as those of mature trees due to shorter

intemode lengths (P = 0.003). Leaves of juvenile A.

nilotica weighed only 75 % of the mass of those of mature

trees (P = 0.003).

Comparison of the physical defences of juvenile and

mature A. tortilis trees was complicated by the fact that

this species bears both short, recurved ('hooked’ or

'curved') thorns and long, ‘straight’ thorns. The overall

density of thorns on juvenile trees did not differ sig-

nificantly from that on mature trees (Table 2).

The ratio of straight to curved thorns was significantly

higher in juveniles (P = 0.016) than in mature plants.

Curved thorns were significantly longer on juvenile than

on mature trees (P = 0.003), whereas straight thorns were

longer on mature trees than on juveniles (P = 0.05). Leaf

mass did not differ significantly between juveniles and

mature trees of this species.

DISCUSSION

Chemical defence

The results of this study indicate that for both Acacia

nilotica and A. tortilis , juvenile plants did not differ from

those of adult trees in total polyphenol, condensed tannin

or crude protein content. Hence juveniles of these two

Acacia species did not appear to be more heavily defended

chemically, at least at the time of year when samples were

collected. This is in contrast to the findings of Reichardt

et al. (1984) with regard to surface resins on twigs of

paper birch. This may be related to differences in the way

leaves and twigs are defended. Bryant et al. (1992: 345)

note that 'In every case that has been studied, the low

palatability of the juvenile phase has been related to in-

creased concentrations of antifeedants in inte modes ’ (our

emphasis).

Carbon-based secondary metabolites, such as tannins,

would be costly defences during periods of rapid growth

such as the juvenile stage (Bryant et al. 1991b, c, 1992).

Juveniles of both of these Acacia species show high in-

trinsic growth rates (Bryant et al. 1989).

It is also possible that polyphenols, condensed tannins

and protein precipitating compounds do not play a defen-

sive role in these species, since Owen-Smith & Cooper

(1987) classed both species as palatable to browsing

ruminants. Our results confirm that A. tortilis has relative-

ly low concentrations of condensed tannins in leaves, and

that A. nilotica has high total polyphenol contents, but no

measureable condensed tannins, as found by Cooper &

Owen-Smith (1985) and Cooper et al. (1988). Further-

more, our findings indicate that despite having a high

polyphenol content, A. nilotica leaf extracts have a protein

precipitating ability that is scarcely higher than that of A.

tortilis. This suggests that the polyphenols found in the

leaves of A. nilotica are mostly not tannins or other protein

binding compounds.

Physical defence

Juvenile A. nilotica specimens have significantly

longer and more densely spaced thorns and their leaves

TABLE 2. — Comparison of potential physical defences in juvenile and mature Acacia nilotica and A. tortilis. N = 10 trees

juv.. juvenile; mat., mature; sig., significance.

214

Bothalia 24,2 ( 1994)

are smaller than those of mature trees. Working in the

same study area. Cooper & Owen-Smith (1986) compared

scrub (< 1 m high) and mature trees of this species in

terms of thorn length and density. They reported thorn

densities of 91 nr1 for scrub and 59 nr1 for trees, which

are very similar to those found for juveniles and mature

trees respectively in this study. However A. nilotica scrub

showed a somewhat shorter mean thorn length (13 mm)

than found for juveniles in this study, and trees had longer

thorns (26 mm) on average than mature plants in this

study. The juvenile plants sampled in this study were

somewhat taller (mean = 1.24 m) than the scrub category

(all individuals less than 1 m) of Cooper & Owen-Smith.

Also, Cooper and Owen-Smith measured thorns over a

longer portion of the branch than the terminal 250 mm

used in this study.

Thoms retard mammalian browsing by restricting bite

size (Cooper & Owen-Smith 1986; Teague 1989a), but

the relative importance of thorn length and thorn density

in defence is not clear. Heavy browsing can induce longer

thorns in regrowth than are seen in unbrowsed plants

(Foster & Dagg 1972; Young 1987; Milewski et al. 1991),

suggesting that longer thorns might be more effective

browsing deterrents. The measurements presented here in-

dicate that juvenile Acacia nilotica are physically better

defended than mature trees only if two conditions hold.

Firstly, it must be shown that greater thorn length and/or

density provides better defence against browsers than

shorter or less dense thorns. Secondly, the pattern shown

by juveniles under one metre in height ( Cooper & Owen-

Smith 1986) must be explained. The smaller leaves of

juveniles in our study may assist in further restricting

feeding rates of browsers.

In A. tortilis, curved thorns are less dense but longer,

and straight thorns more dense but shorter, in juveniles

than in mature trees. Leaf size did not differ between clas-

ses. Curved thorns retard biting rates of kudu and impala

(Cooper & Owen-Smith 1986). The longer, less densely

spaced curved thorns in the juvenile trees do not neces-

sarily indicate heavier juvenile defence because it is not

known how (if at all) the length and density of curved

thorns contribute to their effectiveness as defences. Dif-

ferences in the lengths and relative densities of both thorn

types in Acacia tortilis cannot be said to support an

hypothesis of heavier juvenile defence until the defensive

roles played by the two thorn types is properly understood.

ACKNOWLEDGEMENTS

Dr Mary Scholes provided laboratory facilities and ad-

vice regarding laboratory techniques. Wendy Wolhuter

and three anonymous reviewers greatly improved this

manuscript with their suggestions. The Nature Conserva-

tion division of the Transvaal Provincial Administration

gave permission to work in and take samples from the

Nylsvley Nature Reserve. Gary Marnoweck helped with

arrangements at Nylsvley. This study was conducted as a

B.Sc. Honours project (RB) and funding and financial

support was obtained from the Zoology Department of

the University of the Witwatersrand, the Foundation for

Research Development and the University of the Wit-

watersrand senior bursary program.

REFERENCES

BASEY, J.M., JENKINS, S.H. & MILLER, G.C. 1990. Food selection by

beavers in relation to inducible defenses of Populus tremuloides.

Oikos 59: 57-62.

BELL, R.H.V. 1983. The effect of soil nutrient availability on com-

munity structure in African ecosystems. In B.J. Huntley & B.H.

Walker, Ecology of tropical savannas: 193-216. Springer- Ver-

lag, Berlin.

BRYANT, J.R & KUROPAT, P.J. 1980. Selection of winter forage by

subarctic browsing vertebrates: the role of plant chemistry. An-

nual Review of Ecology and Systematics 1 1: 261-285.

BRYANT, J.P., CHAPIN, F.S. & KLEIN, D.R. 1983. Carbon/nutrient

balance of boreal plants in relation to vertebrate herbivory. Oikos

40: 357-368.

BRYANT, J.P., DANELL, K„ PROVENZA, F„ REICHARDT. P.B.,

CLAUSEN, T.A. & WERNER, R.A. 1991a. Effects of mammal

browsing on the chemistry of deciduous woody plants. In D.W.

Tallanty & M.J. Raupp, Phytochemical induction by herbivores.

Wiley, New York.

BRYANT, J.P., KUROPAT, P.J., COOPER, S.M., FRISBY, K. & OWEN-

SMITH, N. 1989. Resource availability hypothesis of plant an-

tiherbivore defence tested in a South African savanna ecosystem.

Nature 340: 227, 228.

BRYANT, J.P., KUROPAT, P.J., REICHARDT. P.B. & CLAUSEN, T.P

1991b. Controls over the allocation of resources by woody plants

to chemical antiherbivore defense. In T.R. Palo & C.T. Robbins,

Plant defenses against mammalian herbivory. CRC Press, Boca

Raton.

BRYANT, J.P., PROVENZA, F.D., PASTOR, J„ REICHARDT, P.B.,

CLAUSEN, T.P. & DU TOIT, J.T. 1991c. Interactions between

woody plants and browsing mammals mediated by secondary

metabolites. Annual Review of Ecology and Systematics 22:

431-436.

BRYANT, J.P.. REICHARDT, P.B., CLAUSEN, T.P, PROVENZA, F.D.,

KUROPAT, P.J. 1992. Woody plant-mammal interactions. In

G.A. Rosenthal & M.R. Berenbaum, Herbivores: their interac-

tions with secondary plant metabolites, 2nd edn. Vol. 2: evolution-

ary and ecological processes. Academic Press.

CATALDO, D.A., HAROON, M„ SCHRADER, L.E. & YOUNGS, V.L.

1975. Rapid colorimetric determination of nitrate in plant tissue

by nitration of salicylic acid. In J.M. Anderson & J.S.I. Ingram

1989, Tropical soil biology and fertility: a handbook of methods.

CAB International. Originally in Communication in Soil Science

& Plant Analysis 6: 71-80.

COETZEE, B.J., VAN DER MEULEN, F„ ZWANZIGER, S„ GONSAL-

VES, P. & WEISSER, P.J. 1976. A phytosociological classifica-

tion of the Nylsvley Nature Reserve. Bothalia 12: 137-160.

COOPER, S.M. & OWEN-SMITH, N. 1985. Condensed tannins deter

feeding by browsing ruminants in a South African savanna.

Oecologia 67: 142-146.

COOPER, S.M. & OWEN-SMITH, N. 1986. Effects of plant spinescence

on large mammalian herbivores. Oecologia 68: 446-455.

COOPER, S.M., OWEN-SMITH, N. & BRYANT, J.P. 1988. Foliage

acceptability to browsing ruminants in relation to seasonal chan-

ges in the leaf chemistry of woody plants in a South African

savanna. Oecologia 75: 336-342.

DU TOIT, J.T., BRYANT, J.P. & FRISBY, K. 1990. Regrowth and

palatability of Acacia shoots following pruning by African savan-

na browsers. Ecology 71:1 49- 154.

FOSTER. J.B. & DAGG, A.I. 1972. Notes on the biology of the giraffe.

East African Wildlife Journal 10: 1-16.

FREELAND, W.J., & JANZEN, D.H. 1974. Strategies in herbivory by

mammals: the role of plant secondary compounds. American

Naturalist 1 08: 269-289.

FURSTENBURG, D. 1991. Die invloed van tanniene in plante op die

voedingsekologie van kameelperde Giraffa kamelopardalis. M.Sc.

thesis. University of Pretoria.

FURSTENBURG, D. & VAN HOVEN. W. 1992. Condensed tannin as

anti-defoliate agent against browsing by giraffe in the Kruger

National Park. Comparative Biochemistry and Physiology 101 A,

2:381-385.

HAGERMAN, A. 1977. Radial diffusion method for determining tannin

in plant extracts. Journal of Chemical Ecology 13: 437^149.

Bothalia 24,2(1994)

215

KEENEY, D.R. 1982. Nitrogen. In A.L. Page, R.H. Miller & D.R.

Keeney, Methods of soil analysis. Part 2. American Society of

Agronomy, Wisconsin.

LUNDBERG, P. & ASTROM, M. 1990. Low nutritive quality as a

defense against optimally foraging herbivores. American

Naturalist 135: 547-562.

MILEWSKI, A.V., YOUNG, T.P. & MADDEN, D. 1991. Thoms as

induced defences: experimental evidence. Oecologia 86: 70-75.

OWEN-SMITH, N. & COOPER, S.M. 1987. Palatability of woody

plants to browsing ruminants in a South African savanna. Ecology

68:319-331.

PRICE, M.L. & BUTLER, L.G. 1977. The prussian blue assay for poly-

phenols. Journal of Agriculture and Food Chemistry 25: 1268-1273.

PORTER, L.W., HRS ITCH, J. & CHAN, C. 1986. The conversion of

procyanidins and prodelphinidins to cyanidin and delphinidin.

Phytochemistry 25: 223-230.

REICHARDT, P.B., BRYANT, J.P., CLAUSEN, T.P. & WIELAND, G.D.

1984. Defense of winter-dormant Alaska paper birch against

snowshoe hares. Oecologia 65: 58-69.

RHOADES D.F. & CATES R.G. 1975. Toward a general theory of plant

antiherbivore chemistry. Recent Advances in Plant Phytochemistry

10: 168-213.

SIEGEL, S. & CASTELLAN, N.J. 1989. Nonparametric statistics. Mc-

Graw-Hill, New York.

SWAIN, T. 1979. Tannins and lignins. In G.A. Rosenthal, & D.H. Janzen,

Herbivores: their interactions with secondary plant metabolites:

657-682. Academic Press, New York.

TEAGUE, W.R. 1989a. Patterns of defoliation of Acacia karroo by goats

and changes in tannin levels and in vitro digestibility following

defoliation. Journal of the Grassland Society of Southern Africa

6: 230-235.

TEAGUE, W.R. 1989b. The response of Acacia karroo plants to defolia-

tion of the upper or lower canopy. Journal of the Grassland

Society of Southern Africa 4: 225-229.

VAN HOVEN, W. 1984. Trees’ secret warning system against browsers.

Custos 13: 11-17.

YOUNG, T.P. 1987. Increased thorn length in Acacia drepanolobium —

an induced response to browsing. Oecologia 71 : 436-438.

Bothalia 24,2:217-222(1994)

The saltmarsh vegetation of Langebaan Lagoon

M. O’CALLAGHAN*

Keywords: Langebaan Lagoon, saltmarsh, species distribution, zonation

ABSTRACT

The saltmarshes of Langebaan Lagoon are the most extensive in southern Africa. These marshes, as sampled along six

transects, are described. A general marsh, consisting of three species assemblages, was recognized and elevation above mean sea

level (MSL) is discussed as a probable determinant of species distributions. However, minor variations in species distributions

have been induced by changes in soil characteristics, the effects of wind on inundation depth and differences in water salinity.

UITTREKSEL

Langebaan se soutmoerasse is die mees uitgebreide in suidelike Afrika. Hierdie moerasse, soos bestudeer langs ses

lynopnames, word beskryf. ’n Algemene soutmoeras, bestaande uit drie spesiegroepe, kan herken word. Hoogte bo seevlak

(MSL) is waarskynlik bepalend vir die verspreidingspatrone van spesies. Nietemin kan klein variasies van hierdie patrone

veroorsaak word deur veranderinge in grondeienskappe, die effek van wind op waterdiepte en verskillende watersoutgehaltes.

INTRODUCTION

The saltmarshes of Langebaan Lagoon are the most

extensive in the temperate zone of southern Africa. At

5 700 ha, this Lagoon contains over 30% of South

Africa’s saltmarsh areas (O’Callaghan 1990). Most of the

Langebaan marshes have been protected since 1988 as

part of a nature reserve.

These saltmarshes have developed under unique con-

ditions as there is no riverine flow into the Lagoon. All

other saltmarsh development along the South African

coast occurs in estuaries where salinity and tidal charac-

teristics result from interactions between marine and

riverine water bodies. There is, however, an extensive

fresh water seepage into Langebaan Lagoon at the

southeastern comer (Shannon & Stander 1977) and the

wetland vegetation in this area is different from the true

saltmarshes. These less saline wetlands were excluded

from this study. They have been described by Boucher &

Jarman (1977) and Boucher (1987).