J . Linn.Soc. (Bot.), 59, 3 7 7 , ~ . 111 Printed in Great Britain

111

The taxonomic significance of certain anatomical variations among Ericaceae

BY LESLIE WATSON, F.L.S.

Department of Botany, Manchester University* (Accepted for publication June, 1964)

INTRODUCTION

The universally accepted classification of Ericaceae is that of Drude (1889) in Engler’s Pjhnzenfamilien. His treatment is summarized in Table 1, and it rests on the features of floral and fruit morphology given there. It represents a modification by the usual processes of taxonomic devaluation, of the scheme laid down by D. Don in 1834, a substantial part of which dates back to A. L. de Jussieu.

Of the subfamilies, the Vaccinioideae are kept apart from the rest of the family entirely on the strength of their inferior ovaries and fleshy fruits: i t is well known that many of the species have anthers dehiscing by means of apical awns, but this feature is not universal in the group and is to be found elsewhere in the family (Matthews & Knox, 1926; Palser, 1951). However, scrutiny of the literature on ericaceous fruits and ovaries reveals that exclusive use of the inferior ovary and fleshy fruit does not allow any clear line of demarca- tion to be drawn. Thus in Chiogenes the ovary is described as half-inferior, and the decision to exclude that genus from the Vaccinioideae presumably rests on the upper half. Also there are among the Vaccinioideae some genera (e.g. Sophoclesia) where the fruit is dry and not fleshy, while Gaylussacia has a drupe. On the other hand, flet3hy fruits are well known elsewhere in the family, and Gaultheria in the Arbutoideae has a fleshy calyx.

The Rhododendroideae depend entirely on their septicidal capsules and the absence of stamen appendages for their subfamily status, for winged seeds are very far from universal there ; but similar capsules occur elsewhere (e.g. Calluna) and unappendaged stamens are of widespread occurrence in the other subfamilies. The extraordinarily vague definition of the Arbutoideae leaves one with the impression that this subfamily might prove merely a repository for divers genera which do not fit conveniently elsewhere. Of the subfamilies, in fact, only the Ericoideae inspire confidence : here there is an obvious correlation between the floral and fruit characters listed in Table 1 and the distinctive ‘ericoid’ habit (Watson, in press).

Table 1. Summary of the current chsijication of Ericaceae (from Drude, 1889) I. RHODODENDROIDEAE

Fr. a septicidal capsule; seeds often winged; C. deciduous; sta. without appendages.

1. Ledeae (polypet., seeds winged) :

2. Rhododendreae (gamopet., C. zygomorphic;

3. Phyllodoceae (C. actinomorphic; seeds not

Ellwttea, Cludothamnus, Bejaria, Ledum, Tripetaleia Rhododendron, Menziesia, Tm=Gophyllurn

Ledothamnus, Leiophyllum, Lobeleuria, Diplarehe, Rhodothamnus, Kalmia, Phyllodoce Bryanthzca, Daboeoia

seeds winged) :

winged) :

* Present address : Department of Botany, Southampton University.

112 LESLIE WATSON, F.L.S. Table 1 (cont.)

11. ARBUTOIDE~LE Fr. a berry or loculic. caps.; seeds not winged; C. gamopet., deciduous; sta, appendaged. 1. Andromedeae (fr. a dry capsule, smmll calyx Enkianthw, Cassiope, Leucothoe, Andromeda,

Epigaea, Chamaechphne, Pieris, Zenobia cfaultheria, Pernettya, Diplywsia, Chiogenes

Arbutus, Arctostaphylos, Arctowr

at the base): , Lyonia, Agauria, Oxydendron, Orphanidesia,

2. Gaultherieae (fr. capsule or berry; K. fleshy

3. Arbuteae (K. a small disc at base of berry or or leafy; anthers with short processes) :

drupe; anthers with long processes) :

111. VACCINIOIDEAE K. fused around fr., fleshy; G. 1. Vaccinieae (ovary sharply defined from Regwlepb, Gaylussacia, Vaccinium, Catanthera,

peduncle) : CoroUobotrys, Disterigma, Oxywccus 2. Thibaudieae (ovary decurrent with

peduncle) : Pe&apterygium, Agapetes, Paphia, Sphyrospermum, Sophoclesia, Oreanthes, Macleania, Anthopterus, Notopora, Pindlaya, Cavendishia, Psammisia, Hornemnnia, Thibaudia, Ceratostemma

IV. ERICOIDEAE Fr. usually loculic, capsule or nut; seeds not winged; C. persistent; sta. usually appendaged. 1. Ericeae (seeds more than 1 per loculus) : Macnabia, Calluna, Pentapera, Erica,

Bruckenthalia, Phdippia, Ekinella, Blaeria 2. Salaxideae (seeds 1 per loculus) : Eremia, Grbebachia, Simcheilus, Sympieza,

Scyphogyne, Salaxis.

Taking examples at the tribal level, there is a particularly unimpressive diagnosis for the Gaultherieae (Table 1, subfam. Arbutoideae) ; and that of the Andromedeae is hardly convincing.

The feeble definitions of his groups lead one to view Drube’s scheme with suspicion, and a superficial examination of the plants themselves immediately casts further doubts on it. Thus, the tribes Andromedeae and Phyllodoceae each include an enormous range of habit forms : genera with needle-like leaves occur alongside genera with broad flat ones; some consistently have bud scales while others do not, and so on. Furthermore, several of these universally accepted groups (notably the Arbutoideae, the Andromedeae and the Phyllodoceae) are remarkable for the unlikely geographical scatter of their constituent genera.

TAXONOMIC RESEARCH DURING THE TWENTIETH CEKTlJRY

It is curious that Drude’s system has never been challenged, because no evidence has accumulated to substantiate it. The likely explanation, as I have pointed out elsewhere (Watson, in press), is that most workers tackling the Ericaceae have confined themselves to certain of the accepted groups, making no serious effort to contrast these one with another.

Matthews t Knox (1926) described the stamen morphology for representatives from 13 genera. They showed that the ericaceous anther usually becomes inverted on the filament a t a very early stage during its development, and also that different mechanisms of anther dehiscence exist in the family. The Arbuteae emerged as being unusual in that their anthers become inverted only when the stamens are mature-i.e. at a later stage than usual. Apart from supporting the taxonomic soundness of the Arbuteae however, this study was insufficiently comprehensive to help much in evaluating the taxonomic categories.

Copeland (1944) studied the anatomy and morphology of the Rhododendroideae laying

Certain anatomical variations among Erimeae 113

special emphasis on their floral anatomy. He decided that the group ‘exhibits a pervading uniformity. . . (and) . . . is certainly natural’-a surprising conclusion, since he was un- able to contribute anything to its manifestly unsatisfactory definition. He proposed a classification of the genera, based on the dehiscence mechanisms of the anthers and the presence or absence of viscous threads amongst the pollen tetrads, which is a slight amend- ment of Drude’s : the Phyllodoceae remain intact, and the Rhododendreae and Ledeae are hardly changed except that Bejaria becomes a monogeneric tribe.

Cox (1948 a, b ) studied the wood structure of species from 18 genera of Rhododendroideae and 16 genera of Arbutoideae, and i t is interesting to notice that Drude’s tribes Andromedeae and Phyllodoceae proved particularly inconsistent in this respect. There was no attempt on the part of Cox to correlate his observations with other features of the plants concerned, and the new tribes which he based on them are not to be taken seriously. Palser (1951 ; 1954) has studied floral morphology in the tribes Andromedeae and Arbuteae, with special emphasis on the vascular anatomy. She found that the Arbuteae hold together well in this respect. The Andromedeae however exhibit considerable variation, and Palser classified the genera under 2 main groups* accord- ing to the kind of sepal vascular supply, with Epigaea, Enkianthus and Oxydendrum isolated in other aspects of floral structure. Palser’s groups however, do not correlate intelligibly with those of Cox, and the safest conclusion we can draw from these studies is that the Andromedeae and the Phyllodoceae are very heterogeneous assemblages.

Hagerup (1953) appears to have been the only modern worker to interpret his observa- tions on Ericaceae outside the limits prescribed by Drude, although his research on the group was not extensive. He published notes on leaf morphology, and suggested that all the genera with needle-like leaves should be placed together. His idea that Calluna is markedly different from other Ericoideae but similar to Cnssiope is readily confirmed (Watson in press).

OBSERVATIONS

Stomata1 structure, stomatal distribution and pith structure studies have proved so illuminating in the ta,xonomy of Epacridaceae (Watson, 1962, and in press) that it seemed worth while to examine the same features in Ericaceae. I have investigated 98 species from 50 genera, and the observations are recorded in Table 2 .

The 3 stomatal types previously described for the Epacridaceae (anomocytic, paracytic and cyclocytic) are all found in the Ericaceae, although the cyclocytic arrangement is again of very infrequent occurrence. Stomata on the leaves are nearly always confined to the abaxial surface, and the guard cells, as in the Epacridaceae, are always raised above the level of the surrounding epidermis. Sepal stomata are very widespread in the family, and may be confined to the adaxial or the abaxial surface; very rarely, they appear on both surfaces. Corolla stomata also occur, but have a more limited distribution among the genera; they are nearly always abaxial but were found on both corolla surfaces in 2 species.

The 2 pith types seen in Epacridaceae (homogeneous and heterogeneous, see Watson, 1962) are both widespread in Ericaceae. There is also a 3rd type, of rather infrequent occurrence, where t h e mature pith consists of a central core of relatively large, thin- walled cells with small, thick-walled ones a t the periphery: the term ‘Calluna type’ used in an earlier paper (Watson, in press) will be employed here also.

The structure of stomata on the leaves and their distribution patterns on leaves and sepals, as well as the pith structure, seem as in Epacridaceae to exhibit a high degree of constancy among the members of a genus in those cases where more than 1 species has been examined; but the occurrence of corolla stomata among the species in genera

* Leucothoe, Lyonia, Pieris and Chanzaedaphne usually have 3 sepal traces whlle Andrmeda, Cassiope and Harrinzanella have 1 ; but the classification is not very satisfactory because the condition can vary within a genus (e.g. Leucothod).

114 LESLIE WATSON, F.L.S.

Table 2 . Anatomical observations 0 7 ~ species of Ericaceae: s t o m d d structure (pzracylic, anomocytic or cyclocytic); pith structure (homogeneous, heterogenm or CaUuna-type); presence (+) or absence ( - ) of stomata on adaxial (ad) and abaxial (ab) surfaces of leaves,

s e p l s and corolla. Blanks indicate incomplete records

Species Vaccinioid group

1. Cavendkhia pubescens HemsI. 2. Ceratostemma ntadoni Britton 3. Pentapterygium rugosum Hook. 4. Agapetes obovata Benth. & Hook. 5 . Qaylussacia resinosa Torr. & Gray

G. dumosa Torr. & Gray 6. Vaccinium arboreum Marsh

V . witk-idaea L. V . myrtillus L. V . Uli$ino&U?n L,

7 . Oxycoccw. palwtris Pers. 8. Oxydendrum arbweurn DC. 9. Diplycosia luwnicu (Gray) Merril

10. Chiogems serpillijolia Salisb. 1 1. QaultJwia pocurnberw L.

G. acuminata Cham. & Schlecht. G. antip& Forst. f. c f . shallon Pursh. G. odoratu Willd. G. rupestris R. Br.

12. Pernettya pilosa G. Don P . angustijolia Lindl. P. ciliaris G. Don

13. Lyonia ferruginea Sutt. L. paniculata Kutt.

14. Pieris mariana Benth. 8;. Hook. P . nit& Benth. & Hook. P. phillyraefolia DC. P. fioribunda Benth. & Hook.

15 . Leucothoe racemosa Gray L. axillark D. Don L. acuminatu G. Don

16. Chanmedaphne calyculata Moench. 15. Zembia specwsa D. Don 18. Enkianihw japonicw. Hook. f.

E. campanulatw, Nichols. 3. himalaffizcs Hook. & Thoms.

A . salicijolia Hook. ex Oliver 19. Agauria buxifolia Baker

Ericoid group

20. Erica scoparia L. E. cinerea L. E. stricta Don E. u m b e l b L.

2 1. Penbapera siculu Klotzsch 22. Macnabia nwntccna Benth. 23. Bruckcenthalia spiculifolia Reicht. 24. Philippia abietina Klotzsch 2 5 . Salaxis rugosa Benth. 26. Sytnpieza c a p d e l b Licht. 27. Simocheilw multijorus Klotzsch

Stomata r L

Structure Leaf Sepal -- ad ab ad ab

para para para para para para para para para para Para para para para para para para para para anom para para para anom anom anom anom anom anom para para anom para anom anom anom anom anom anom

anom anom anom anom anom anom anom anom anom anom anom

+ + + + + + + + + + +

+ + + + + + + + + + +

Corolla <---*-, Pith ad 8b structure

- - homo - - homo - - homo

homo - + homo - + homo - + homo - + homo - - homo - - homo + + homo - + Calluna - - homo - - homo - + homo - + hetero

+ hetero - + hetero

+ hetero + hetero

- + hetero - + hetero - + hetero - - homo - + hetero - + homo - + homo - - hetero - + hetero - + homo - + Calluna - + Calluna - - homo - - hetero - + Calluna - + hetero - + hetero - - homo - - homo

- - -

homo homo homo homo homo homo homo homo homo homo homo

Certain anatomical variations among Ericaceae Table 2 (cont.)

Stomata

115

Structure Leaf Sepal -- ad ab ad ab

anom + + - anom + + + - anom + + + - anom + + + -

-

Pith structure

Calluna Calluna Calluna Calluna

Species Calluna group 28. Calluna vulgaris Salisb. 29. Cassiopejastigiata D. Don

C. tetragonu D. Don C. selaginoides Hook. 8: Thoms.

Epigaea group 30. Epigaea repeiw L.

Arbuteae group 31. Arbutus u n d o L.

A. canariensis Duham. A. andrachne L.

32. Arctostuphylos glauca Lindl. A . oflcinalis Wimm. 8: Grab. A. uva-ursi Spreng.

33. Arctous alpinn Siedenzu

Rhododendroid group (i) Ledeae 34. Cladothamnus pyrolifolius Bong. 35. Ledurn palwtre L.

L. glandulosum Sut t . L. latijoliurn Jacq.

E. bracteata B. & I3 . 36. Elliottea pnniculatn B. & H.

(ii) 37. Kalmia Zatijolia L.

K . hirsuta Walt. K . glauca Xit. K. angustifolia L.

38. d n d r o m d a polifoliic L. A . glaucophylla Link.

(iii) Rhododendreae 39. Menziesia globularis Salisb.

M . pentandm Maxim. M . jerruginea Sni.

40. Tsusiophyllum tannkac Maxim. 41. Rhododendron hirsutum L.*

Rh. calendulaceum Torr. Rh. anthopogon D. Don Rh. indicurn Sweet Rh. lapponicuin Wahlenb.

(iv) Bejarieae 42. Bejaria resinosa L.

B. mexicana Benth. B. vacemosa Vent. B. glauca Humb. et Bonpl.

Phyllodoceae group

43. Loiseburia procumbeiis Desf. 44. Leiophyllzcm buxijolium Ell. (ii) 45. Phyllodoce caerulea Bab.

P. empetrijormis D. Don 46. Bryanthus breweri A. Gray

B. taxijolius A. Gray

(i)

cyclo - + + - hetero

homo homo homo homo homo homo homo

anom anom anom anom anom anom anom

- + + - - + + - - + + - - + + - - + + - - + + - - + + -

hetero hetero hetero hetero hetero hetero

anom anom anom anom anom anom

- + - + - + - - + - - - + - + - + - + - + - +

-

anom - + + - anom - + + + anom - + - - anom - + - anom - + - anom - + -

- - -

hetero hetero hetero hetero hetero hetero

mom anom anom anom anom mom anom anom anom

- + - + - + - + - + - + - + - + - + - + - + - + - + - f - + - + - + - +

homo homo homo homo homo homo homo homo homo

cycle - + - + cpclo - + - + cycle + + - + cycle - + - +

homo homo homo homo

homo homo

mom - + + - anom - + + - anom - + + - anom - + + - anom - + + - anom - + + -

hetero hetero hetero hetero

116 LESLIE WATSON, F.L.S. Table 2 (cont.)

Stomata

Structure Leaf Sepal Corolla Species ,------- ,k-, Pith

Phyllodoceae group (contd.) ad ab ad ab ad ab structure (iii) 47. Rhodothamnus charnuecistus Reibch. anom + + hetero

(iv) Bejarieae 48. Ledothamnw sessiJorus N.E.Rr. anom - + + - - + hetero

49. Daboecia polijolia D. Don anom - + + + - - hetero

Diplarche group 50. Diplarche multijora Hook. & Thorns. anom - + - + - - homo

D. puucijora Hook. & Thoms. anom - + homo

* Pith structure in Rhododendron: Homogeneous in Rh. lepidotum Wall., Rh. nudijorum Torr., Rh. owidentale A. Gray, Rh. retusum Benn., Rh. rhodora J. F. Gmell. Heterogeneous in Rh. rnaddeni Hook. f., Rh. maximum L.

(4

Table 3. Constancy of features of stomatccl rnorlphology and distribution and pith structure within genera of Ericaceae (data from Table 2)

No. of genera No. of genera where constant where variable

Stomatal structure 21 Distr. of foliar stomata 22 Distr. of sepal stomata 19 Pith structure 17 Presence of corolla stomata 5

Table 4. Variation in foliar stomata.? structure, distribution of stomata and pith structure within genera of Ericaceae. Features known to vary are

indicated by (+). (Data from Table 2) Anatomical characters

Distr. of Distr. of Presence of Stomatal foliar sepal Pith corolla

Genera structure stomata stomata structure stomata Yaccimium Enkianthus Arctostuphylos Kulmia Bejuria Ledum Rhododendron Caultheria Leucothoe Lyonia Pieris

+ + + + +

\&ere they appear at all is more sporadic. These points are illustrated in Table 3, using the data from Table 2.

The 11 genera in which 1 or more of my characters has proved to be variable are listed :in Table 4, where each character is recorded as variable (-I-) or constant ( -) among the

Certain anatomical variations among Ericuceae 117

species examined. We see that in 5 of these genera, only 1 of the 5 characters is known to vary ; and ofthe others, in Rhododendron and Gaultheria certain combinations predominate among the species seen (Table 2, genera 11, 41). There are no reasons for suspecting any of these 7 genera of being taxonomically unsound, and the inconsistencies in them (and in Ledum) can be taken as a demonstration of the often overlooked principle, that taxo- nomic characters should be used in combination. The remainder of the genera listed in Table 4 (Pieris, Leucoth.oe and Lyonia) evidently constitute a taxonomically difficult ‘complex’, for the Index Kewensis reveals that the species have been freely shuffled among them by different authors. It is quite possible therefore, that variation in stomata1 structure and distribution and pith structure in these 3 genera reflects faulty generic delimitation or cases of mistaken identity in my material.

GROUPS EMERGING FROM THE OBSERVATIONS

In the light of what has been said about the existing classification, there is no need to be disheartened by a marked lack of agreement between the data presented in Table 2 and Drude’s scheme in Table 1. The groups of Table 2 represent what seem to me to be genuine relationships among the genera. The actual sequence of the groups is not intended to be meaningful.

The Vaccinioid group The Tables 5A, B and C are taken from the data presented in Table 2 . They show

positive associations among the species of Ericaceae examined between paracytic stomata on the leaves and sepal stomata confined to the abaxial surface; between paracytic stomata and the presence of corolla stomata; and between the presence of corolla stomata and the possession of only abaxial sepal stomata. When the characters are considered in terms of their occurrence in genera (Table 5 D) an additional association between paracytic

Table 5 . Analysis of data from Table 2 A. Correlation between the occurrence of paracytic foliar stomata and the possession of only abaxial sepal

stomata among the species. Sepal stomata

Abaxial only Other distributions I

Peracytic Stornatal structure

23 42

0 22

B. Correlation between the occurrence of paracytic foliar stomata and the possession of corolla stomata among the species.

Corolla stomata c--LL- Present Absent

Paracytic Stornatal structure

16 13

7 52

C . Correlation between the possession of corolla s tomta and only a b a k l sepal stomata among the species. Corolla stomata

Present Absent ,

Abaxial only stornate { Other distributions

28 1

37 22

D. Correlation between the occurrence of homogeneous pith and pracytic foliar stomata in the genera. Pith structure

Homogeneous Heterogeneous I

Paracytic Stomatal qtructure

12 22

4 19

118 LESLJE WATSON, F.L.S. stomata and homogeneous pith is revealed. In fact the Ericaceae include an assemblage in which combinations of paracytic leaf stomata, only abaxial sepal stomata, the possession of corolla stomata and a homogeneous pith seem to be more frequent than one would expect if the characters were randomly distributed.

It is interesting to consider the plants where these features predominate in com- bination: they constitute the Vaccinioid group of Table 2 (genera 1-16). They include all the members of Drude’s subfamily Vaccinioideae represented in the sample (genera 1-7), as well as several genera from his Arbutoideae; but a closer examination of them reveals so many common features that w0 must acknowledge them to be far more closely related than Drude would have us believe.

In these genera the leaves are nearly always broad with flat margins, although ‘ericoid’ needles and leaves with inrolled margins are common in the family as a whole. This is clearly seen in Table 6, which is based on the material examined for Table 2. The excep- tional case in the Vaccinioid group is Oxywccus plustm’s, which has narrow rolled leaves. 0. macrocarp however has flat ones.

Table 6. Leaf form and basic chrMnosonze number among the genera of Ericaceae Leaves Basic chromosome number

I I , Grooved, x = other

Broad, flat needle-like x = 12 than 12 Vaccinioid { Others

15 13

1 19

9 7

2 10

Bud-scales are universal among these Vaccinioid genera, although they are by no means universally present in the family: they are absent from Drube’s Ericoideae and from several genera in other groupings (notably in the Phyllodoceae). Nearly all of my Vaccinioid genera typically have an urceolate, actinomorphic corolla, although cam- panulate, hypocrateriform, polypetalous and zygomorphic ones are all widespread elsewhere; and the inflorescences are typically leafless (though bracteate) racemes or panicles, although this type does not predominate in the family as a whole. Cytological knowledge of the Ericaceae is rather fragmentary; but the available records (Darlington & Wylie, 1955) suggest that while the basic chromosome number among genera in the Vaccinioid assemblage is usually x = 12, basic numbers other than 12 predominate elsewhere. This is clearly brought out in Table 6. The exceptional basic numbers in the Vaccinioid group belong to the closely related Pernettya and Gaultheria. A number of x = 12 is recorded for some Gadtheria species however, and relatively few species from either genus are known cytologically.

All the ericaceous genera with inferior ovaries (i.e. the subfamily Vaccinioideae of Drude) fall in this Vaccinioid assemblage, and those genera where there i s a tendency to epigyny and a fleshy calyx (Chiogenes, DipZy&, GauZtJwia) are also there.

These characteristics of the Vaccinioid group, all of which are of distinctly limited distribution in the family as a whole, can be summarized as follows :

(1) Leaves usually broad and flat with paracytic stomata. (2) Inflorescences usually leafless, and racemose or paniculate. (3) Corolla usually urceolate, often bearing stomata. (4) Pith usually homogeneous in at least some members of a genus. (5) Basic chromosome number commonly x = 12. (6) Ovary frequently inferior or perigynous.

Zenobia, Enkianthus and Agauria. Two additional genera belong in the Vaccinioid

(i) Zenobia (Table 2, genus 17) has broad leaves, bud-scales, leafless racemes and an assemblage, although stomata1 and pith features are not clearly indicative of this.

Certain anatomical variations among Ericaceae 119

urceolate corolla; and in fact the genus has sometimes been considered synonymous with the Vaccinioid Leuwthoe, from which (using gross morphological criteria) it can be separated only with some diBculty.

(ii) Enkianthus (genus 18) agrees with the rest of the Vaccinioid genera on these same grounds, and in addition it has corolla stomata and a basic chromosome number ofn = 12. Although the leaves of species seen by me have anomocytic stomata, paracytic ones are found on the sepals. Sepal stomata of Ericales are usually of the same morphological type as those found on the leaves, but the situation in Enkianthus is paralleled in Gaultheria in the Vaccinioid group. G. rupestris, which is unusual in that genus for the anomocytic stomata on its leaves, has paracytic ones on the sepals.

The genus Agauria (genus 19) has broad flat leaves, leafless racemes and an urceolate corolla. It agrees with the Vaccinioid genera in these respects, and also in pith structure and in the distribution of sepal stomata. It is tentatively placed with the Vaccinioid assemblage in Table 2. The absence of corolla stomata and of paracytic stomata on the leaves however, combined with the geographical distribution of the genus (see later), suggest that its position needs further consideration. The material available to me was scanty.

Geography of the Vaccinioid group. The taxonomic soundness of the Vaccinioid group of Table 2, including Zenobia and Enkianthus (i.e. genera 1-18), gains support from phyto- geographical considerations. Their distribution is quite compatible with widely recog- nized floristic relationships between (i) N. America, E. Asia and Malaysia; and (ii) S. America and Australasia.

Fourteen of the genera are American. The most widespread are Gaultheria (America, West Indies, Indomalaysia to Tasmania) ; Pernettya (S. America, Mexico, Tasmania and New Zealand); and Vaccinium (N. America, the Andes, Europe and Madagascar). Other American genera also occur in Eastern and North Temperate Asia (Lyonia) and 1 species of the ditypic Chiogenes appears in N. America, the other in Japan. Few genera do not occur in America; t.hey are Agapetes (E. Asia, Malaysia, Fiji) ; Pentapterygium (E. Himalayas, Malaysia) ; Diplywlsia (Indomalaysia) ; and Enkianthus (Himalayas to Japan). The Vaccinioid group is virtually* absent from Africa, and only 3 of the genera (all American) occur in Europe.

The Eriwid group It has already been shown (Watson, in press) that studies on anatomical and gross

morphological characters confirm the main body of Drude’s Ericoideae as a sound taxo- nomic grouping. If we ignore Calluna, the floral and fruit characters used by Drude (Table 1) are correlated with the presence of the characteristic ‘ericoid’ habit : the leaves are small, needle-like and grooved and are usually borne in whorls, and there are no bud- scales or scale-leaves. The representatives examined (Table 2, genera 20-8) are constant with the exception of Calluna in stomatal morphology, stomatal distribution and pith structure. Geographically, Calluna again excepted, the group is clearly defined, being overwhelmingly Mediterranean and African with two main masses separated by the Sahara. There can be no doubt that the Ericoideae are a taxonomically sound grouping.

Calluna (genus 28) differs from the rest of Drude’s Ericoideae in many respects apart from the anatomical features listed, and I have discussed its relationship with Cmsiope in an earlier paper (Watson in press). These 2 genera undoubtedly merit a tribe of their

Epigaea group Drude placed Epigaeu (Table 2, genus 30) among his Andromedeae, but the genus is

remarkable among Ericaceae in having cyclocytic stomata on its leaves, and is further * Agauria, tentatively placed among the Vaccinioid group in Table 2, is corned to tropical Africa

and Madagascar. The widespread Vaccinium, which is overwhelmingly American, is also represented in Madagascar.

O W .

120 LESLIE WATSON, F.L.S.

distinguished from the rest of the Andromedeae by its adaxial sepal stomata. It proves on investigation to be very peculiar in other respects.

There are 2 species, 1 (E. repens) in North-east America and the other (E. asiaticu Maxim., not examined by me but said to be very similar to E . repem) in Japan. The plants of E . repens are functionally dioecious, a condition which seems to be unique in the family. The stamens of both species are unusual in being unappendaged and in having anthers which dehisce via longitudinal slits instead of the usual apical pores. The greatly expanded 5-lobed stigma is without parallel in the family and the densely pubescent ovary is another unusual feature. The broad cordate leaves are unique, and Palser (1951) lists other peculiarities : a double placenta in each locule of the ovary, instead of the usual single one; and large persistent bracts with an unusual vascular system. Whatever the merits of Drude’s Andromedeae, Epigaea evidently has little in common with the other members of that grouping. It is clearly very isolated and deserves a monogeneric tribe.

The Arbuteae Table 2 provides evidence to support the taxonomic soundness of the traditional

Arbuteae (genera 31-3) : for these genera regularly have sepals with only adaxial stomata, anomocytic foliar stomata and a homogeneous pith. Some species of Arctostaphylos (see Metcalfe & Chalk, 1950) have stomata on both leaf surfaces (an unusual condition in the family), but otherwise the genus seems to differ from Arbutus only in the number of seeds per loculus in the fruit.

Drude’s Arbuteae can be supported on other grounds. The tribe is unquestionably sound, and appears to be an isolated one in the family as a whole. Thus, the anthers of all 3 genera are peculiar in that they are versatile, becoming inverted at maturity by means of an articulation of the filament; in the rest of the family they are not versatile, the inversion taking place a t a very early stage in stamen ontogeny (Matthews & Knox, 1926). Palser (1954), who studied floral morphology and floral vascular anatomy in particular, noted that the Arbuteae ‘show considerably more consistency in organo- graphical features than do . . . most of the tribes of the Ericaceae’.

All the Arbuteae have broad flat leaves, and bud scales. The inflorescences are leafless and racemose, and the corolla is urceolate. In these respects they resemble the vaccinioid genera; but the basic chromosome number of all 3 of them is n = 13, by contrast with the n = 12 typical of the Vaccinioid group. They differ further in their adaxial sepal stomata, and they do not seem to exhibit the corolla stomata and paracytic leaf stomata which are so common among the Vaccinioid genera.

The Rhododendroad group Drude’s tribes Ledeae (minus Bejaria) and Rhododendreae are placed together in Table 2 and presented as the main body of the Rhododendroid group. The genera of these tribes consistently have anomocytic stomata (which are abaxial only) on the leaves and sepals, and they are almost alone outside the Vaccinioid group in exhibiting corolla stomata.

The Ledeae and Rhododendreae also have in common their septicidal capsules, un- appendaged anthers and (nearly always) winged seeds (see Table 1). These features occur sporadically elsewhere in the family, but here in the Rhododendroid group they are correlated with zygomorphic flowers and (nearly always, Copeland, 1944) fine viscous threads amongst the pollen tetrads. Neither of these characters is recorded elsewhere in the family. In addition, the inflorescences are usually terminal racemes or corymbs and the buds are always provided with scales. Thus the Rhododendroid genera seem to constitute a useful grouping. The main bulk of the group is split between North America and Eastern Asia ; but there are well-known floristic connexions between these regions and in fact one of the genera (Menziesia) is discontinuous between North America and North Temperate

C'erta i 1% anatomico I wuriations nmmig Er 1 wicccz e 121

Asia. Rhododendrou is the most 11 idespread, extendmg from Temperate Sor th -4merica via Mediterranean Europe to Japan, South China and the Himalayas to Seir Guinea, n it11 a single species In -lustraha. Ledum is Sorth Temperate. Arctic and circumpolar

The 2 tribes nere %eparated by Drude on their corolla structiire. the Ledeae being polypetalous and the Rliododendreae spnpetalous Copeland ( 19-14) shoved that they further differ i n the niechanism of anther dehiscence, and Table 2 reveals that while all the Ledeae examined have a heterogeneous pith the Rhododeridreae usually have a homogeneous one

Bejaria. Rejcirw. 11 hich Drude placed in the Lecleae. is markedly distinct and seem.; well \Torthy of a monogeneric tribe. It is the only ericaceous genus apart from Epzgatc~ n here cyclocytic stomata have been seen (Table 2 , genus 42). and B rucemo3a lias qtomata on both surfaces of tlie leaf I n the family as a whole the presence of stomata on both leaf surfaces is usually associated nith sepal stomata confined to the adaxial surface B. racemom in fact i b the only knonn exception, and as such is interesting iince it demon- strates that the oiie condition is not a necessary consequence of tlie other

Winged seed. cornhined 11 ith the presence of tnbcous threads among the pollen, 1111- appendaged stamens and septicidal capsules suggest that Bejnnri i i related to the Khodo- dendroid genera Copeland noted hon ever that the anthers have a peculiar deliircence mechanism unknonii elsen here in the family, n hereby the resorption tissue does not involve the epidermis: and for t h s reasoii he proposed the monogmeric tribe Bejarieae He also described it trilacunar vascular supply to the sepalz, remarking that this is unusual among the Rhododendroideae, and recorded tlie presence in Bejar ia of uniseriate branched trichomez. nhich are probably very rare in the family Cox found the nood structure to be different from that of the other Rhododendroideae seen hy him The flon-ers are nearly alnaj-s heptamerous in a family where pentamer>- 1s usual The leaves of all the species listed in Table 2 hare a very thick coating of wax nhich has to be remowd before the stomata can be detected, and in my experience the thickness of thiq layer is quite unparalleled among other Ericales

Bejaria is confined to South and Central America, n hile no other Rhododendroid genus occurs in that region The genus is therefore an isolated one both geographically and morphologically. the, C'opeland's tribe Bejarieae seems 1% ell justified

Kalmia and Andromeda. Table 2 shows that in the whole family, sepal stomata are recorded as absent from only 9 species representing 6 genera. Of these, Diplycosia (genus 9) is otherir ise typically Taccinioid, and C'aZZu)tu is undoubtedly related to C'assiope The other genera distinguished by species lacking sepal stomata are Ledicm, Khododendroli, Kalmia aiid diidromedn (genera 33, 41. 37. 38)

Ledurn and Rhododendron hare the TI inged seeds, zygomorphic corolla. unappendaged stamens and other features characteristic of the Rhododendroid group, where they certainly belong Kalmza also has unappendaged stamens. aiid is remarkable as the only genus outside Drucle's Ledeae and Rhododenclreae knon n to produce winged seeds (Copeland, 1942). I t does not hare the viscous threads among the pollen tetrads n hich are usual in Rhododenclroid genera, and the mature flowers are actinomorphic. but Ledum is also 1% ithout viscous threads, and its floners are markedly zpgomorphic only in the bud. The vegetative buds of Knlmia are like those of the Rhododendroid group in bearing scale-leal eq, and the inflorescences are often in typicall>- Rhododendroid terminal corymbs

d n d r o n t i d n corresponds n ith Knlmia (and Ledum) in haring a heterogeneous pith. The seeds are not ninged. but Bentham and Hooker describe them as compressed The floral formula of both Andromeda and Kalmia is K ( ~ ) C ~ ~ ) A l s + G ' ~ 5 ~ admittedly a common one in the Ericaceae, but the carpellary and stamina1 whorls are often reduced The leaves of Anrlromcdn are narron 11 itli revolute margins and are cloqely similar to those of Knlmia ylauca and L e d u m , and the buds also correspond with those of Knlmia and the Rhododendroid genera in haring bud-scales The genus also has the terminal cor-mbs

9

122 LESLIE WATSON, F.L.S.

and the long slender pedicels which typify Kalmia and the Rhododendroid genera but which are very rare elsewhere in the family. Andromeda has awned anthers and loculicidal capsules, and differs in these respects from Kalmia and the other Rhododendroid genera of Table 2 . Since it bears a marked resemblance to these in other features, however, it is placed with them in the table.

Morphological similarities between Kalmia, Andromeda and the Rhododendroid genera are especially interesting in the light of records on the distribution of toxic substances in the family. The poisonous ‘andromedo-toxin’ is recorded so far only from Andromeda, Kalmia and Rhododendron (Forsyth, 1954)’ but the leaves of Ledum are also known to contain a narcotic principle. In the present connexion it is significant that all these poisonous Ericaceae have Rhododendroid afhities ; and it would evidently be worth while from an economic point of view to examine other Rhododendroid genera with this in mind, for hive bees have been known to incorporate Andromeda pollen in their honey and horses die after eating Rhododendron leaves.

T h e Phyllodoceae Table 2 indicates that 7 of the 9 genera from Drude’s Phyllodoceae (genera 43-9)

resemble one another but differ from the Rhododendroid group in having adaxial sepal stomata. Use of the name Phyllodoceae is here restricted to these 7 genera. Of the others, Kalmia has already been dealt with and Diplarche provides a special case to be mentioned presently. The Phyllodoceae as thus d e h e d have in common their septicidal capsules, unappendaged anthers and adaxial sepal stomata, and in the absence of further evidence it seems reasonabIe to keep them together. Nevertheless they are a distinctly hetero- geneous grouping both geographically and morphologically, and the variations in pith structure shown in Table 2 prove to be correlated with other distinguishing features. Ny view of Drude’s version of the tribe is summarized in Table 7 .

Table 7 . Relationships of Drude’s Phyllodoceae Phyllodoceae proper : (i) Lewphyllum and Loiseleuria

(ii) PhyUodoce and Bryanthus (iii) Rhodothamnus (iv) Ledothnmnus (v) Daboecia

Kalmk Rhododendroid ’ Isolated genus (Diapensisceae?) : Diplarche

Leiophyllum and Loiseleuria. Leiop?Lyllum and Loiseleuria (Atlantic U S . and Korth circumpolar respectively) have homogeneous pith. They are undoubtedly very closely related. Both have opposite leaves, and they have only 2 or 3 locules in the ovary where most Ericaceae have 4 or 5. Their anthers dehisce via longitudinal slits, by contrast with the usual ericaceous apical pores. The flowers of both genera are borne in terminal racemes, and Cox ( 1 9 4 8 ~ ) found that the two correspond, but differ from most other Rhododen- droideae, in details of wood structure. Neither genus produces bud scales. The leaves are small, ovate and evergreen; those of Leiophyllum are flat, and differ in this respect from the leaves of Loiseleuria, which have rolled margins.

Phyllodoce and Bryanthus. Ph yllodoce (Korth circumpolar) and Bryanthus (Eastern Siberia) have a heterogeneous pith, and also correspond in having needle-like grooved leaves and an urceolate or campanulate corolla. The leaves are usually needle-like and rolled, like those of the Ericoideae; but the habit is not strictly ericoid, since the leaves are alternate instead of whorled, the bud-scales are present. The flowers are solitary in the leaf axils, and Cox found that the 2 genera correspond with one another, but are dis- tinguishable from other Rhododendroideae, in details of wood anatomy. They are evidently closely related.

Certain anatomical variations among Ericaceue 123

Rhodothamnus. Rhodothamnus is a monotypic genus, endemic in the Alps. The long corolla lobes are rotate-an unusual feature in a family where they are usually imbricate. The broad flat leaves, with ciliate margins, are another peculiar feature. Bud-scales occur, and the flowers are solitary in the leaf axils.

Ledothamnus. This is another monotypic genus, endemic in Guiana : and it has proved to be remarkable as the only known case where corolla stomata occur in combination with adaxial sepal stomata (Table 5 C ) . The terminal solitary flowers of Ledothamnus have free spreading petals: there is no other example of this inflorescence t-ype in the family, and nearly all other Ericaceae are gamopetalous. The habit is thoroughly ericoid, with an absence of bud-scales and the rolled. needle-like leaves are arranged in whorls. In other respects however (stomata1 distribution, unappendaged anthers, septicidal capsules, polypetaly, inflorescence, geographical distribution) it has nothing in common with the Ericoideae. It does share adaxial sepal stomata, fruit structure and unappend- aged stamens with the other Phyllodoceae, but the genus is evidently a very isolated one.

Daboecia. Table 2 reveals an unusual feature in Daboecin (genus 49) : stomata on both sepal surfaces (seen elsewhere only in a species of Kalmia). The genus is ditypic and confined to Atlantic Europe. The floral formula K4C(4)X4+4G(4) is probably unique in a family where the flon-ers are basically pentamerous and frequently anisomerous. There are no bud-scales and the foliage leaves, which are broad with recurved margim, are remark- able for their densely tomentose under-surface. Natthews S: Knox (1926) showed that the anthers of Daboecia have a vascular trace pattern not known elsewhere in the family, and Cox (19483) proposed a monogeneric tribe on account of its unusual wood structure. There is no doubt that this too is an isolated genus.

Diplarche group

Table 2 shows that Diplarche (genus 50) differs from the rest of Yrude’s Phyllodoceae in having only abaxial sepal stomata.

There are only 2 species, and the genus is confined to the Himalayas, It differs from all other Ericaceae in the structure of the androecium: 10 stamens, with 5 epipetalous and alternating with the corolla lobes and 5 hypogynous and opposite them. S o t only are the epipetalous stamens unique amongst Ericaceae, but their relative positions seem peculiar. Ericaceae are generally supposed to be obdiplostemonous, with the stamens of the outer whorl opposite the corolla lobes ; but in Diplarche the epipetalous members presumably represent the outer whorl (unless we invoke morphological gymnastics) and they alternate with the petals. The genus further differs from most Ericaceae in having capitulate inflorescences and serrate leaves, and the unappendaged stamens have anthers dehisuing by longitudinal slits instead of the usual ericaceous pores. Airy Shaw has recently sug- gested (Kew Bull., in press) that Diplarche really belongs in the family Diapensiaceae; and there is no doubt that it is very much a genus anomalum in its present position. Few collections hare been made, and the material available to me (duplicates of the original collection distributed by Hooker and Thomson) was poor.

TAXONOMIC COXCLUSIONS

The tribes

If the groups outlined in Table 2 are accepted the effect on the traditional classification of the family is iconoclastic. Of the 10 tribes only the Arbuteae, Rhododendreae, Ledeae and a modified version of the Phyllodoceae actually gain support. Most of the genera making up Drude’s Andromedeae turn out to be Vaccinioid; and of the rest Cmsiope belongs elsewhere with Calluiza and Epigaea is an oddity very distinct from all other

124 LESLIE WATSON, F.L.S.

Ericaceae. The sole survivor, Andromeda itself, seems to have Rhododendroid affinities, and thus the Andromedeae disappear as a useful taxonomic grouping.

The other tribes gain no support from the present study, but are not split asunder. It is significant that they all depend on solitary features. Thus the Vaccinieae and Thibaudieae are separated by Drude according to whether or not the pedicel is con- tinuous with the calyx. Sleumer (1960) however claims that this character is inconsistent within well-established genera, so that the separation is not even practicable, let alone taxonomically sound. Similarly the Ericeae and the Salaxideae are kept apart because of a difference in the structure of the ovary which has yet to be correlated with any other distinguishing feature.

The subfamilies Of the subfamilies, only the Ericoideae (if we exclude Callurn) and to some extent the

Rhododendroideae represent meaningful groupings. The latter seem to be a very sound assemblage if we exclude the Phyllodoceae, i.e. if limited to the Rhododendroid group of Table 2 .

The Phyllodoceae differ from the Rhododendroid genera in their adaxial sepal stomata. They also differ in having actinomorpbic flowers, wingless seeds and in having no viscous threads among the pollen. In these features they resemble all the Ericaceae not included in the Rhododendroid group. The Rhododendroid genera all produce bud-scales and hare broad flat leaves, but of Drude’s Phyllodoceae 5 genera are without bud-scales and 5 have tightly-rolled leaves. Their position alongside the Rhododendroid genera of Table 2 in the traditional Rhododendroideae depends on two common features: the possession of septicidal capsules and unappendaged anthers. Septicidal capsules occur elsewhere in Callum and certain Ericoideae however, and unappendaged stamens appear in various genera scattered throughout the family. These two features alone provide a weak excuse for so close an association of the Phyllodoceae with genera from which they differ in so many other respects ; and their inclusion destroys the Rhododendroideae as a well-defined, apparently natural taxonomic grouping.

It was emphasized in the Introduction that Drude’s Vaccinioideae are separated from other Ericaceae because of their inferior ovaries and fleshy fruits, a distinction which proves to be an arbitrary one. The Vaccinioid group of Table 2 include all the Vaccinioideae examined and a substantial part of the Arbutoideae as well; and the genera concerned have so many features in common that it seems absurd to separate them at the subfamily level. The absurdity is magnified in treatments (e.g. Hutchinson, 1959) where Drude’s Vaccinioideae are awarded full family status. This is the kind of situation we can expect TV hen taxonomic groups founded on single characters are uncritically accepted : sooner or later they are promoted within the taxonomic hierarchy.

The fault of Drude’s treatment of the Vaccinioideae lies in the narrowness of his interpretation, for the conventional Vaccinioideae certainly consist of closely related genera. The Arbutoideae on the other hand stand revealed as a hotch-potch of distantly related genera. The Gaultherieae and most Andromedeae are Vaccinioid ; the Arbuteae constitute a distinct little group the relationships of uhich are obscure; Cassiope belongs with Callunu and has little in common with other Arbutoideae: Epigaea is a genus anomalum which merits a monogeneric tribe and is not closely comparable with any of the recognized groups ; and Andromeda itself is closer to the Rhododendroid genera than to any of Drude’s Arbutoideae.

There is an overwhelming case for conserving wherever possible the main outlines of well-known families and genera, the names of which are in everyday botanical usage. But there is no point whatever in perpetuating such fanciful hierarchies of unnatural groupings as Drude’s treatment of the Ericaceae. Drastic changes are needed, and a scheme based on the groups outlined in Table 2 would undoubtedly represent a vast improvement.

C'crtrriii mntomicul vnrintions amony Ericucealz 12.5

ACK?iO\VLEDGEMESTS

Thanks are extended to the Keeper of the Herbarium for the use of specimens and facilit'ies a t the IIIanchester hliiseum ; and to the Department of Scient5fic and Industrial Research for financial support.

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METCALFE, C . R. 8- C ' H . u x , L., 1930. Sys temat ic Anntomy of the Dicotyledom. Oxford. P.ALSER, B. F., 1951. Studies on floral morphology in Ericales. I. Organography and vascular anatomy

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