Berberidaceae

Review of Palaeobotany and Palynology, 42 (1984): 7--21

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Elsevier Science Publishers B.V., Amsterdam -- Printed in The Netherlands

The Northwest European Pollen Flora, 30 BERBERIDACEAE

S. B L A C K M O R E

and G.L.A. H E A T H

Department of Botany, BritishMuseum (NaturalHistory),Cromwell Road, London S W 7 5 B D (GreatBritain)

LITERATURE Archangelsky (1973), Beug (1961), Erdtman (1952), Faegri and Iversen (1975), Heusser (1971), Kurnazawa (1936), Kuprianova and Alyoshina (1972), Mitroiu (1963, 1970), Nowicke and Skvarla (1979, 1981), Roland (1967).

INTRODUCTION

Of the three members of this family occurring in Northwest Europe only Berberis vulgaris is native. Epimedium alpinurn, which grows naturally in Southern Europe, and Mahonia aquifoliurn, a native of western North America, are often cultivated in Northwest Europe and have become naturalized locally. These three species belong to two tribes of the subfamily Berberoideae; Berberis andMahonia to tribe Berberideae and Epirnedium to tribe Epimedieae (Prantl, 1888; Janchen, 1949). Kumazawa (1936, 1938) stated that pollen characters are amongst the most striking differences between the two tribes, a view confirmed by recent investigations (Nowicke and Skvarla, 1979, 1981). Pollen grains of Berberis and Mahonia were found to be very susceptible to damage during acetolysis. After the usual 5-rain treatment with acetolysis mixture the majority of grains had disintegrated along their apertures leaving a number of rounded or angular fragments. Plate I illustrates pollen grains treated in this way since it is possible that such fragments might be encountered during pollen analysis. No reports of Berberidaceae pollen have been found in published pollen analyses and the fragility of Berberis and Mahonia pollen grains may be a contributing factor. To prepare slides with intact pollen grains of these two genera the anther contents were sieved very gently prior to acetolysis for the reduced time of 3 min with little or no agitation at any stage. This may have affected the size of the pollen grains but the measurements obtained agree quite closely with published data (Beug, 1961; Kuprianova and Alyoshina, 1972).

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© 1984 Elsevier Science Publishers B.V.

SPECIMENS EXAMINED All the specimens listed are housed in the herbarium of the British Museum (Natural History) except for those based on fresh material.

Berberis vulgaris L. -- Austria: Armiti s.n., Denmark: Dahl D45b; France: Brewar s.n., Heard s.n. ; Germany: Launert s.n.; Ireland: Herb. Pugsley s.n. ;Sweden: Kindlund s.n.

Epimedium alpinum L. -- England: Painter s.n. ; France: Herb. Hansen s.n., Ambrosi 142, Morynier s.n. ; Sweden: Foggitt 52.

Mahonia aquifolium (Pursh) Nuttall -- England: Blackmore (fresh material) 1981, Heath (fresh material) 1981, Herb Redgrove s.n., Frose s.n.; Sweden: Albani-Mellblom s.n. KEY TO THE POLLEN TYPES 1. a. Pollen 3-colpate, m i c r o r e t i c u l a t e . . . . . . . . . . . Epimedium alpinum t y p e b. Pollen s y n c o l p a t e , psilate with p e r f o r a t e t e c t u m . . . . . . . . . . . . . . . . . . 2 2. a. A p e r t u r e s spiral or consisting o f sinuous parts o f i n c o m p l e t e spirals, grains o f t e n breaking during acetolysis into e l o n g a t e d spiral f r a g m e n t s ....................................... Berberis vulgaris t y p e b. P a n t o c o l p a t e , t h e a p e r t u r e s dividing the exine into 4--8 r o u n d e d t o angular plates, grains o f t e n breaking into t h e f r a g m e n t s d e l i m i t e d b y the apertures . . . . . . . . . . . . . . . . . . . . . . . . . . Mahonia aquifolium t y p e DESCRIPTIONS OF THE POLLEN TYPES

Berberis vulgaris t y p e (Plate I, 1; Plates II--IV) Pollen class: S y n c o l p a t e . Apertures: Colpus, long, varying greatly, even w i t h i n a single specimen, f r o m a single spiral t o irregular, sinuous, i n c o m p l e t e spirals; slightly s u n k e n ; margins irregular, indistinct in places; m e m b r a n e s thin and readily breaking during acetolysis. Exine: Sexine and n e x i n e indistinguishable, s c a t t e r e d small cavities w i t h i n t h e e x i n e are just visible with light m i c r o s c o p y . Ornamentation: Psilate, with o r w i t h o u t s c a t t e r e d o r fairly dense puncta. Outline: R o u g h l y spherical. Measurements: G l y c e r i n e jelly -- d i a m e t e r 40-(43.5)-46 a m ; e x i n e 1--2 u m thick. Silicone oil -- d i a m e t e r 36-(40.1)-41 u m .

Species: Berberis vulgaris. Comments This p o l l e n t y p e , a l t h o u g h variable, can be distinguished f r o m t h e Mahonia aquifolium t y p e b y its partial o r i n c o m p l e t e spiral apertures, Less t h a n 5% o f grains in each specimen e x h i b i t a p e r f e c t spiral a p e r t u r e (Plate II, 2). A m o r e c o m m o n t y p e o f grain has a single a p e r t u r e which divides the grain i n t o t w o equal i n t e r l o c k i n g parts, r a t h e r like a tennis bail (Plate II, 1). In o t h e r grains

the apertures are less regular and may occasionally have several anastomosing apertures so that they are similar in places to the Mahonia aquifolium type although retaining their spiral character elsewhere on their surface. Faegri and Iversen (1975), in their key, distinguished Berberis from Mahonia on the basis of differences in sculpturing; Berberis being described as "distinctly perforate or perfossulate" and Mahonia as "pitted". In the present study too much variation was encountered to permit reliable application of these characters.

Epimedium alpinum type (Plates V--VI) Pollen class: 3-Zonocolpate. P/E ratio: Suberect to semi-erect. Apertures: E c t o a p e r t u r e - colpus, long to very long, width medium to broad, sunken; margins granular and indistinct; ends tapering and acute; membrane delicate, often rupturing, scabrate. Exine: Sexine and nexine equal, thickness uniform throughout the grain; sexine 1 of short simple columellae, sexine 2 a perforate, incomplete tectum. Ornamentation: Microreticulate, with some grains appearing faintly striate. Outlines: Equatorial view -- elliptic, ends subacute. Polar v i e w - circular to slightly angular, the colpi indented. Measurements: Glycerine jelly -- P 28-(33.7)-36 #m; E 23-(26.1)-30 Urn; P/E ratio 1.2-(1.23)-1.26; exine 1.5 um thick. Silicone oil -- P 26-(30.6)-33 #m; E 21-(23.7)-27 um. Species: Epimedium alpinurn. Comments Nowicke and Skvarla (1979, 1981) described similar pollen from other species of Epimedium and throughout most members of the Epimedieae, although some species were said to have striate-reticulate pollen. Mahonia aquifolium type (Plate I, 2; Plates VII--IX) Pollen class: Syncolpate. Apertures: Irregularly syncolpate, with furrow-like apertures which divide the exine into 4--8 rounded or angular plates, narrow, sunken; margins variable, distinct or indistinct; membranes thin and often rupturing during acetolysis, sometimes scabrate. Exine: Sexine and nexine indistinguishable; small cavities within the exine are visible with light microscopy. Ornamentation: Psilate, usually punctate. Outline: Roughly spherical. Measurements: Glycerine jelly -- diameter 30-(36)-40.5 /~m; exine 1.5/zm thick. Silicone oil -- 27-(33)-40/zm. Species: Mahonia aquifolium.

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Comments T h e Mahonia aquifolium t y p e is m o r e c o n s t a n t in a p p e a r a n c e t h a n t h e Berberis vulgaris t y p e since the a p e r t u r e s a l w a y s t a k e the s a m e f o r m a l t h o u g h t h e n u m b e r o f a p e r t u r e s , a n d e x i n e p l a t e s t h e y delimit, varies. N o w i c k e and Skvarla ( 1 9 7 9 ) f o u n d n o d i f f e r e n c e b e t w e e n t w o N o r t h A m e r i c a n species o f Berberis a n d Mahonia a n d c o n s i d e r e d t h a t the u n i f o r m and distinctive pollen o f t h e t w o g e n e r a s u p p o r t e d the t r e a t m e n t o f t h e B e r b e r i d a c e a e b y H u t c h i n s o n ( 1 9 5 9 ) w h o i n c l u d e d o n l y these t w o g e n e r a in t h e family. ACKNOWLEDGEMENT T h e a u t h o r s w o u l d like to t h a n k Dr. G.C.S. Clarke f o r his c o m m e n t s o n the manuscript. REFERENCES Archangelsky, D.B., 1973. Palynological taxonomy of Berberidaceae. In: L.A. Kuprianova (Editor), Pollen and Spore Morphology of Recent Plants. Nauka, Leningrad, pp.18--21 (in Russian). Beug, H.-J., 1961. Leitfaden der Pollenbestimmung, 1. Lieferung. G. Fischer, Stuttgart, 63 pp. Erdtman, G., 1952. Pollen Morphology and Plant Taxonomy. Angiosperms 1. Almqvist and Wiksell, Stockholm, 538 pp. Faegri, K. and Iversen, J., 1975. Textbook of Pollen Analysis. Munksgaard, Copenhagen, 3rd ed., 295 pp. Godwin, H., 1975. History of the British Flora. Cambridge University Press, London, 2nd ed., 541 pp. Heusser, C.J., 1971. Pollen and Spores of Chile. University of Arizona Press, Tucson, AZ, 167 pp. Hutchinson, J., 1959. Families of Flowering Plants. Vol. 1. Dicotyledons. Oxford University Press, London, 510 pp. Janchen, E., 1949. Die systematische Gliederung der Ranunculaceen und Berberidaceen. Denkschr. Akad. Wiss. Wien, 108: 1--82. Kumazawa, M., 1936. Pollen grain morphology in Ranunculaceae, Lardizabalaceae and Berberidaceae. Jpn. J. Bot., 8: 19--46. Kumazawa, M., 1938. Systematic and phylogenetic consideration of the Ranunculaceae and Berberidaceae. Bot. Mag. (Tokyo), 52: 9--15. Kuprianova, L.A. and Alyoshina, L.A., 1972. Pollen and Spores of Plants from the Flora of the European Part of the U.S.S.R., I. Izv. Akad. Nauk S.S.S.R., Leningrad, 171 pp. ( in Russian). Mitroiu, N., 1963. Contributii la studiul palinologic al unor familii dintre Polycarpaceae (Ranales). Stud. Cerc. Biol., Set. Biol. Veget., 15: 239--250. Mitroiu, N., 1970. I~tudes morphopoUiniques et des aspects embryologiques sur les "Polycarpiceae" et Helobiae avec des considerations phylog~netiques. Lucraile Grad. Bot., Bucuresti, 243 pp. Nowicke, J.W. and Skvarla, J.J., 1979. Pollen morphology: the potential influence in higher order systematics. Ann. Mo. Bot. Gard., 66: 633--700. Nowicke, J.W. and Skvarla, J.J., 1981. Pollen morphology and phylogenetic relationships of the Berberidaceae s.1. Smithson. Contrib. Bot., 50: 1--83. Prantl, K., 1888. Berberidaceae. In: Engler, die N atiirlichen Pflanzenfamilien, 3 (2): 72--77. Roland, F., 1967. t~tude de l'ultrastructure des apertures: III, Compl6ments fournis par le microscope electronique ~ balayage. Pollen Spores, 11(3): 475--498.

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Plate descriptions (all figures × 2000, except where otherwise stated) PLATE I (p. 12)

Berberis vulgaris L. (Kindlund s.n.) 1. Pollen grain, acetolysed for 5 min, which has broken along a spiral aperture. Mahonia aquifolium (Pursh) Nuttall (Blackmore s.n.) 2. Fragments of pollen grains acetolysed for 5 min. PLATE II (p. 13)

Berberis vulgaris L. (Pugsley s.n.) 1. Spiral aperturate grain in high focus. 2. Spiral aperturate grain, cross-section. PLATE III (p. 14)

Berberis vulgaris L. (Dahl D45b) 1. Pollen grain divided into segments by an irregular aperture, high focus. 2. Same pollen grain, lower focus. PLATE IV (p. 15)

Berberis vulgaris L. (Armiti s.n.) 1. Scanning electron micrograph, overall view of pollen grain divided into two segments by a single aperture. 2. Scanning electron micrograph; overall view of spiral aperturate pollen grain. 3. Scanning electron micrograph; detail of ornamentation (× 10 000). PLATE V (p. 16)

Epimedium alpinum L. (Herb. Hansen s.n.) 1. Polar view; ornamentation at pole. 2. Polar view; lower focus. 3. Polar view; cross-section. 4. Equatorial view; ectoaperture. 5. Equatorial view; lower focus. 6. Equatorial view; cross-section. PLATE VI (p. 17)

Epimedium alpinum L. (Ambrosi s.n.) 1. Scanning electron micrograph; overall shape in equatorial view. Epimedium alpinum L. (Foggitt s.n.) 2. Scanning electron micrograph; overall shape, polar view. 3. Scanning electron micrograph; colpus in equatorial view. 4. Scanning electron micrograph; part of colpus showing granular colpus membrane (X 10 000). 5. Scanning electron micrograph; detail of ornamentation near pole (X 10 000). Epimedium alpinum L. (Ambrosi s.n.) 6. Scanning electron micrograph; fractured pollen grain.

12 PLATE I (Berberis vulgaris type: B. vulgaris, 1; Mahonia aquifolium type: M. aquifolium, 2)

13 PLATE II (Berberis vulgaris type: B. vulgaris)

14 PLATE III

(Berberis vulgaris type: B. vulgaris)

Z

PLATE IV (Berberis vulgaris type: B. vulgaris)

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16 PLATE V (Epimedium alpinum type: E. alpinum)

17 PLATE VI (Epimedium alpinum type: E. alpinum )

18 PLATE VII (p. 19) Mahonia aquifolium (Pursh) Nuttall (Herb. Redgrove s.n.) 1. Pollen grain; high focus. 2. Pollen grain;lower focus showing five exine plates, in optical section. PLATE VIII (p. 20) Mahonia aquifolium (Pursh) NuttaU (Herb. Redgrove s.n.) 1. Pollen grain divided by apertures into five plates, high focus. 2. Same grain ; lower focus. PLATE IX (p. 21) Mahonia aquifolium (Pursh) Nutall (Herb. Redgrove s.n.) 1. Scanning electron micrograph; overall view. 2. Scanning electron micrograph; detail of ornamentation (× 10 000). 3. Scanning electron micrograph; overall view. 4. Scanning electron micrograph; detail of ornamentation and part of aperture (× 10 000).

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PLATE VII (Mahonia aquifolium type: M. aquifolium)

20

PLATE VIII (Mahonia aquifolium type: M. aquifolium )

21 PLATE IX (Mahonia aquifolium type: M. aquifolium )