Studies of the pollen morphology and taxonomy of the ... · Candolle as a monotypic genus while others includ- ing Meikle (1977) and Schmidt (1978),(1979) have included Securigera

REVIEW OF

PALAEOBOTANY AND

PALYNOLOGY ELSEVIER Review of Palaeobotany and Palynology 94 (1996) 239 257

Studies of the pollen morphology and taxonomy of the tribes Loteae and Coronilleae (Papilionoideae; Leguminoseae). 3, Coronilla L. and related genera and systematic conclusions

M.J. Diez a, I.K. Ferguson b,,

a Departamento de Biologla Vegetal y Ecologia, Apdo. 1095., 41080, Sevilla, Spain b The Herbarium, Royal Botanic Gardens, Kew, Surrey, Richmond, TW9 3AE, UK

Received 31 July 1995; revision 3 April 1996; accepted 3 April 1996

Abstract

The pollen morphology of 48 taxa has been studied with light and electron microscopy. The pollen is three- zonocolporate, elliptical or more or less rectangular, sometimes circular, in equatorial outline and circular or triangular in polar outline; small or medium size, P x E =(14-30)x (9-26) Ixm. The colpi are long, the endoapertures lalongate. The ornamentation is perforate, microreticulate, granulate-verrucate, striate-rugulate perforate-granulate or finely granular. Exine is 0.5-2 ~tm thick at the mesocolpium. The endexine thickened at the equator, thinner at the poles, the foot layer very thin or absent, the infratectum columellate; the columellae are sometimes almost granular often widely spaced with expanded bases and the tectum thick. Ornamentation is the primary basis for the division into types.

Five pollen types are recognised. With the exception of Securigera, which has similar pollen to Coronilla, the types correspond well with the genera recognised in the group. The pollen morphology of Scorpiurus is distinct from that of the rest of the group.

Pollen morphology is discussed in relation to the taxonomy of the group and its significance to relationships and evolution of the tribes is considered.

It is concluded that there is little evidence from pollen morphological studies to support the separation of the Coronilleae and Loteae as two tribes. It is suggested that the group Loteae shows some affinities in pollen morphology with tropical tribes as for example Phaseoleae as well as with temperate herbaceous tribes.

1. Introduction

Coronilla and related genera comprising the tribe Coronil leae as circumscribed by Polhill (1981) has about 50 species primarily centred a round the Mediterranean, extending to the Atlantic Islands, Western Asia and Nor theas t Africa. The mono typ ic

* Corresponding author. Fax: +44 181 332-5278. E-mail: [email protected]

0034-6667/96/$15.00 © 1996 Elsevier Science B.V. All rights reserved PH 0034-6667(96)00014-0

genus Antopetitia A. Richard occurs in tropical Africa.

As discussed earlier (Diez and Ferguson, 1991,1994) the delimitation of the tribes Loteae and Coronil leae and the generic limits within the tribes has long been problematic, various authors adopt ing different limits. Polhill (1981) reviews the problems separating Coronil leae from Loteae by the jointed fruits but admits that there is no real practical reason why the two tribes should not be

240 M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239 257

amalgamated. Lassen (1989a) treats Coronilla and related genera as an assemblage within the tribe Loteae. Lock (1989) and Lock and Simpson (1991) have followed Lassen's treatment.

Some recent authors including Ball (1968) and Chamberlain (1970) have treated Securigera de Candolle as a monotypic genus while others including Meikle (1977) and Schmidt (1978),(1979) have included Securigera securidaca in Coronilla. Lassen (1989a) redefined the limits of the two genera recognising nine species in Coronilla and twelve species in Securigera. He clearly distinguishes these genera from Hippocrepis Linnaeus. At about the same time Lassen (1989b) transferred Coronilla emerus to Hippocrepis. This species had hitherto been retained in Coronilla by most authors including Ball (1968), Chamberlain (1970) and Meikle (1977).

Dominguez and Galiano (1974b) in revising the morphologically specialised Scorpiurus Linnaeus separate four species, however, most authors including Ball (1968) and Greuter et al. (1989) recognised only two.

Hammatolobium Fenzl, the remaining genus placed in Coronilleae by Polhill (1981) has been transferred to Tripodium Medicus and redefined by Lassen (1986) and this treatment is followed by Greuter et al. (1989). The pollen morphology of this genus is described and discussed by Diez and Ferguson (1991).

The pollen morphology of the Coronilla group has been studied by a number of workers especially of the species in the Iberian Peninsula. Ohashi (1971) examined the pollen of ten species in light microscopy including Antopetitia which he suggests is palynologically similar to Ornithopus. Pire (1974) included a number of species in the group in a study of the pollen of the tribe Hedysareae while Dominguez and Galiano (1974a) examined the pollen of Scorpiurus. The pollen of eleven of the annual species of Hippocrepis were investigated by Dominguez (1976). Ferguson and Skvarla (1981) as a part of a review of the pollen morphology of the subfamily Papilionoideae illustrate the pollen of Scorpiurus villosa with scanning and transmission electron microscopy and go on to suggest that in the tribe Coronilleae there is a little variation in the tectum which may prove to have some

taxonomic significance at generic level but the apertures are unspecialised.

The pollen of four species of Ornithopus was examined by Alsina Aser (1984) using light and scanning electron microscopy. Prados et al. (1985a),Prados et al. (1985b) studied the pollen of some eleven species from Coronilla, Hippocrepis, Ornithopus and Scorpiurus. They included these data in a numerical analysis, however, the results do not clarify relationships greatly.

Fern~indez (1987) has examined pollen of four species of Coronilla and placed these in a type of their own distinguished by rugulate ornamentation from the pollen of three species of Ornithopus. The latter are placed in a separate type with rectangular shaped pollen that is smooth at the poles and verrucate at the equator. She also investigated the pollen of five species of Hippocrepis and three species of Scorpiurus which she placed in a large and not well defined pollen type including species of Trifolium Linnaeus, Medicago Linnaeus and Anthyllis Linnaeus.

Recently, Crompton and Grant (1993) in an extensive review and numerical analysis of the pollen morphology of the genus Lotus concluded that the Old World species had less variable pollen than the New World taxa. They suggest that the pollen sculpturing pattern of some members of the Coronilleae differ from Loteae and described Ornithopus as having verrucate clusters with nano- processes, Scorpiurus as reticulate and Hippocrepis slightly reticulate. They do not describe the pollen of Coronilla.

The purpose of this paper, the last of a series (see also Diez and Ferguson, 1991, 1994) is to describe the pollen morphology of Coronilla and related genera and to see how much palynological characters can contribute to the understanding of relationships between the tribes Loteae and Coronilleae.

2. Material and methods

Pollen material was obtained from the Herbarium, Department of Botany, Faculty of Biology, University of Sevilla (SEV) and the Herbarium, Royal Botanic Gardens, Kew (K). Details of the specimens examined are given below.

M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257 241

Pollen was acetolysed in the standard way (Erdtman, 1960). For light microscopy (LM) slides were prepared by mounting the pollen in glycerol jelly. Twenty to thirty measurements of pollen grains (P and E) were made from each specimen.

The measurements shown in Table 1 represent the mean and range of all the samples examined of each taxon. Fewer (approximately five) measurements were made of the other characters.

For scanning electron microscopy (SEM) pollen was air dried on specimen stubs from 95% ethanol and examined with a Jeol T100 or a Hitachi 2400 SEM. For transmission electron microscopy (TEM) acetolysed exines were fixed with 2% osmium tetroxide, pre-stained with uranyl acetate and embedded in epon-araldite (Skvarla, 1966; Skvarla and Pyle, 1968). Sections were cut with a diamond knife and post-stained with uranyl acetate and Reynold's lead citrate using an LKB Ultrastainer and examined with a Hitachi H300 TEM.

The nomenclature used for the European species generally follows Tutin et al. (1968) but the most recent changes proposed by Lassen (1986),(19893),(1989b) and Greuter et al. (1989) are adopted and these changes are shown in the list of specimens examined. For any African or Asian species not included in Lassen (1989a) the nomenclature used by Lock (1989) and Lock and Simpson (1991) is followed. The terminology in general follows F~egri and Iversen (1975) and Punt et al. (1994).

3. Specimens investigated

Antopetitia abyssinica (L.) A. Richard. Nigeria, Daramola 6230 (K); Tanzania, Staples, 373 (K); Stolz, 207 (K)

Coronilla coronata L. Italy, Feoli Chiapella (SEV 75720) Coronilla juncea L. Portugal, B61iz and Guerra (SEV 12791); Spain, Aparicio (SEV 56786); Galiano et al. (SEV 119620); Devesa, Luque and Ubera (SEV 41831) Coronilla minima L. Spain, Loidi, Molina and Fernfindez Gonz~ilez (SEV 107847); Soriano (SEV 113977) Coronilla ramosissima (Ball) Ball (=Coronilla juncea L. subsp. ramosissima Ball). Morocco, Easton 16 (K); Lindberg 3612(K) Coronilla repanda (Poiret) Gussone subsp, dura (CaviUier) Coutinho. Spain, Cabezudo (SEV 17927); Cabezudo, Silvestre and Vald6s (SEV 37515); Fern~mdez Diez (SEV 25334); Gibraltar, Beususan, Talavera and Valdes (SEV 124736)

Coronilla scorpioides (L.) Koch. Spain, Galiano et al. (SEV 7935); Casaseca (SEV 3194); Dominguez and Gibbs (SEV 16313) Coronilla valentina L.

subsp, glauca (L.) Battandier (= C. glauca L.). Spain, Andr6s and Arroyo (SEV 87111); Mayor (SEV 24994)

subsp, pentaphylla (Desfontaines) Battandier. Algeria, Balansa 380 (K)Coronilla viminalis Salisbury. Morocco, Trethwey 227 (K)

Hippocrepis areolata Desvaux (=H. bicontorta Loiseleur- Deslongchamps). Qatar, Wilcox 106 (K); Saudi Arabia, Collenette 2496 (K) Hippocrepis atlantica Ball. Morocco, Ball s.n. (K) Hippocrepis biflora Sprengel (= H. unisiliquosa L. subsp, biflora (Sprengel) Bol6s and Vigo). Spain, Galiano and Dominguez (SEV 15138); Yugoslavia, Prior, s/n (K) Hippocrepis brevipetala (Murbeck) Dominguez. Algeria, Birch and Wolfe s.n. (K); Morocco, Blanch6 et al. (SEV 123535) Hippocrepis ciliata Willdenow. Spain, Galiano and Dominguez (SEV 13909); Peris and Stubing (SEV 121097) Hippocrepis commutata Pau. Spain, Ladero and Fuertes (SEV 93192); Nieto Feliner (SEV 123477) Hippocrepis comosa L. Spain, Loidi (SEV 101058) Hippocrepis constricta G. Kunze (= H. multisiliquosa L. subsp. constricta (Kunze) Maire). Saudi Arabia, Collenette 740 (K) Hippocrepis cyclocarpa Murbeck. Egypt, Palmer 69 (K) Hippocrepis emerus (L.) Lassen (= Coronilla emerus L.)

subsp, emeroides (Boissier and Spruner) Lassen (= Coronilla emeroides Boissier and Spruner; C. emerus L. subsp, emeroides Holmboe). Russia, Chechrstakov (SEV 43352)

subsp, emerus (= Coronilla emerus L.). Italy, Chiapella (SEV 75721) Hippocrepis eriocarpa (Boissier) Boissier (= Hippocrepis squamata (Cavanilles) Cosson subsp, eriocarpa (Boissier) Nyman). Spain, Castroviejo (SEV 125155) Hippocrepis glauca Tenore (=H. comosa L. subsp, glauca (Tenore) Bonnier and Layens). Spain, Fern~indez (SEV 25471) Hippocrepis minor Munby. Algeria, Birch and Wolfe s.n. (K) Hippocrepis multisiliquosa L. Spain, Cabezudo, Dominguez and Talavera (SEV 7831) Hippocrepis neglecta Lassen. Morocco, Balls 13 2456 (K) Hippocrepis salzmannii Boissier and Reuter. Spain, Luque, Talavera and Vald6s (SEV 117019) Hippocrepis scabra de Candolle (=H. comosa L. subsp, scabra (de Candolle) Bol6s and Vigo). Spain, Martinez (SEV 120619) Hippocrepis squamata (CavaniUes) Cosson (=H. comosa L. subsp, squamata (Cavanilles) Bol6s and Vigo). Spain, Charpin and Defferrand (SEV 91954); Asensi and Diez (SEV 108523) Hippocrepis unisiliquosa L.

subsp, bisiliqua (Forsskal) Bornmt~ller (=H. bisiliqua Forsskal). Iraq, Rami and Rechinger 17721 (K)

subsp, unisiliquosa. Jordan, Simpson 53249 (K) Hippocrepis valentina Boissier (=H. balearica Jacquin subsp. valentina (Boissier) Uhrov~i). Spain, Stfibing (SEV 110926)

Ornithopus compressus L. Spain, Diez, Pastor and Silvestre (SEV 73178)

242 M.J. Diez, I.K. Ferguson/Review o f Palaeobotany and Palynology 94 (1996) 239~57

Table 1 Showing taxa examined arranged in pollen types, with ornamentation, measurements (~tm) of the mean and ranges for the polar (P) and equatorial (E) axes and the shape index P/E

Types and taxa Ornamentat ion Polar axis Equatorial axis P/E

Type I Coronilla coronata striate-rugulate 19 (20.35) 22 15 (16.25) 18 C. juncea striate-rugulate 15 (18.27) 21 10 (14.37) 18 C. minima striate rugulate 17 (19.35) 22 15 (16.05) 18 C. ramosissima striate-rugulate 17 (19.25) 21 13 (14.87) 16 C. repanda subsp, dura striate rugulate 14 (18.10) 21 10 (13.39) 16 C. scorpioides striate rugulate 15 (17.20) 20 9 (12.16) 14 C. valentina subsp, glauca striate-rugulate 19 (22.50) 24 14 (16.92) 22 subsp, pentaphylla striate rugulate 19 (20.75) 22 15 (16.55) 18 C. viminalis striate-rugulate 23 (25.60) 29 18 (19.40) 21 Securigera atlantica striate-rugulate 23 (24.45) 26 18 (19.80) 21 S. cretica striate-rugulate 20 (22.37) 25 17 (18.70) 20 S. elegans striate rugulate 23 (25.15) 28 20 (21.50) 23 S. grandiflora striate rugulate 24 (24.35) 26 19 (19.35) 20 S. orientalis striate rugulate 20 (22.83) 25 16 (17.18) 18 S. parviflora striate-rugulate 21 (22.15) 23 17 (18.35) 19 S. securidaca striate-rugulate 20 (23.00) 26 18 (19.62) 22 S. varia striate rugulate 23 (26.45) 29 17 (22.30) 25

1.11 (1.25) 1.31 1.06 (1.27) 1.66 1.05 (1.20) 1.37 1.18 (1.29) 1.40 1.13 (1.35) 1.80 1.14 (1.41) 1.72 1.00 (1.28) 1.56 1.17 (1.25) 1.31 1.20 (1.31) 1.44 1.14 (1.23) 1.33 1.00 (1.23) 1.41 1.08 (1.16) 1.27 1.20 (1.25) 1.31 1.22 (1.32) 1.50 1.15 (1.20) 1.29 1.09 (1.17) 1.30 1.04 (1.18) 1.47

Type II Ornithopus compressus granulate verrucate 23 (23.80) 25 19 (19.60) 21 O. isthmocarpus granulate-verrucate 25 (28.25) 30 21 (23.37) 25 O. perpusillus granulate-verrucate 18 (20.25) 22 13 (15.55) 18 O. pinnatus granulate verrucate 23 (25.82) 30 17 (19.52) 22 O. sativus granulate verrucate 22 (25.62) 28 20 (21.72) 24 O. uncinatus granulate verrucate 23 (24.30) 26 17 (18.85) 23

1.15 (1.21) 1.31 1.12 (1.20) 1.30 1.11 (1.30) 1.46 1.09 (1.32) 1.58 1.00 (1.18) 1.35 1.08 (1.28) 1.46

Type III Subtype I l ia Hippocrepis areolata perforate 15 (18.17) H. biflora perforate 21 (21.89) H. ciliata perforate 16 (18.62) H. commutata perforate 16 (18.95) H. comosa perforate 18 (19.00) H. constricta perforate 15 ( 15.85 ) H. cyclocarpa perforate 16 (17.50) H. emerus subsp, emeroides perforate 19 (23.15) subsp, emerus perforate 22 (24.05) H. eriocarpa perforate 17 (20.20) H. glauca perforate 19 (21.25) H. minor perforate 19 (20.83) H. neglecta perforate 20 (20.30) H. salzmanni perforate 22 (23.75) H. scabra perforate 21 (22.05) H. squamata perforate 20 (22.82) H. unisiliquosa subsp, bisiliqua perforate 15 (16.00) subsp, unisiliquosa perforate 19 (20.65) H. valentina perforate 18 (20.60)

22 13 (14.41) 17 1.06 (1.26) 1.46 25 15 (17.74) 20 1.05 (1.23) 1.66 20 13 (14.47) 16 1.14 (1.28) 1.42 22 12 (14.82) 20 1.00 (1.27) 1.66 20 14 (14.70) 16 1.20 (1.29) 1.42 17 14 (14.60) 16 1.00 (1.08) 1.21 19 13 (14.30) 16 1.12 (1.22) 1.38 27 20 (23.30) 26 0.87 (0.99) 1.09 26 20 (22.10) 25 0.95 (1.09) 1.25 22 15 (16.90) 19 1.10 (1.19) 1.31 22 15 (16.60) 18 1.18 (1.27) 1.46 22 14 (15.25) 16 1.25 (1.31) 1.46 21 14 (15.15) 16 1.25 (1.33) 1.50 25 18 (18.35) 20 1.21 (1.29) 1.38 24 16 (18.05) 19 1.10 (1.22) 1.33 28 16 (17.92) 21 1.10 (l.27) 1.56

17 14 (14.50) 15 1.00 (1.10) 1.21 22 13 (14.70) 15 1.26 (1.40) 1.53 23 15 (17.00) 18 1.10 (1.20) 1.35

M.J. D&z, I.I( Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239~57 243

Table 1 (continued)

Types and taxa Ornamentation Polar axis Equatorial axis PIE

Subtype IIIb H. atlantica perforate-rugulate 18 (20.05) 21 16 (17.15) 20 1.05 (1.16) 1.31 H. brevipetala perforate-rngulate 17 (19.42) 22 14 (14.95) 16 1.20 (1.29) 1.46 H. multisiliquosa pefforate-rugulate 20 (22.65) 25 15 (17.15) 20 1.13 (1.21) 1.56

Type IV Antopetitia abyssinica finely granular 20 (23.35) 26 21 (23.45) 26 0.86 (0.99) 1.09

Type V Scorpiurus muricatus microreticulate 18 (21.60) 24 12 (13.85) 16 1.12 (1.56) 1.76 S. vermiculatus microreticulate 20 (22.47) 25 13 (14.05) 15 1.50 (1.60) 1.76

Ornithopus isthmocarpus Cosson (=Ornithopus sativus Brotero subsp, isthmocarpus (Cosson) Dostfil). Morocco, Trethwey, 21 (K); Trethwey, 230 (K) Ornithopus perpusillus L. England, Milne-Redhead, 5990 (K); Spain, Diez, Pastor and Silvestre (SEV 73178) Ornithopus pinnatus (Miller) Druce. Spain, Segura Subizarreta (SEV 41058); Segura Subizarreta (SEV 38689) Ornithopus sativus Brotero (=O. sativus Brotero subsp, roseus (Dufour) Dostfil). Spain, Cabezudo (SEV 21937); Cabezudo (SEV 80376) Ornithopus uncinatus Maire and Samuelsson. Morocco, Samuelsson 7239 (K)

Scorpiurus muricatus L. (=S. sulcatus L.; S. sulcatus subsp. muricatus (L.) Battandier; S. subvillosus L.). Greece, Atchley, s.n. (K); Spain, Galiano et al. (SEV 7956); Martin et al. (SEV 107488); Wales, Wade, 3771 (K) Scorpiurus vermiculatus L. Spain, Dominguez and Silvestre (SEV 7877); Rivera (SEV 46669)

Securigera atlantica Boissier and Reuter (=Coronilla atlantica (Boissier and Reuter) Boissier). Algeria, Durando 521 (K) Securigera cretica (L.) Lassen (=Coronilla cretica L.). Greece, Atchley 1639 (K); Yugoslavia, Huser s.n. (K) Securigera elegans (Pancic) Lassen (= Coronilla elegans Pancic). Greece, Alston and Sandwith 988 (K) Securigera grandiflora Lassen (= Coronilla grandiflora Boissier). Turkey, Kotschy 48 (K)Securigera orientalis (Miller) Lassen (= Coronilla orientalis Mil]er; Coronilla orientalis var. balansae Boissier). Turkey, Balls 13413 (K); Stainton 8193 (K); Stainton and Henderson 5934 (K). Securigera parviflora (Desvaux) Lassen (=Coronilla rostrata Boissier and Spruner; C. parviflora Willdenow; Artrolobium parviflorum Desvaux). Greece, Reverchon 38 (K) Securigera securidaca (L.) Degen (=Coronilla securidaca L.; Securigera coronilla de Candolle; Bonaveria securidaca (L.) Hal~csy). Greece, Shay 80/85 (K) Securigera varia (L.) Lassen (=Coronilla varia L.). France, Tarascon and Ledoux (SEV 22540); Switzerland, Wyatt, 31 (K)

4. Results

The pollen of Coronilla and related genera is generally three-zonocolporate, small in size, about 20-25 I.tm, with endoapertures lalongate and with exine stratification comprised of a thick endexine at the mesocolpium, foot layer thin or absent, an infratectum with short usually broad columellae, or sometimes more or less granular and a thick complete tectum.

4.1. Type I (Plate I, 1-15)

Elliptical or rectangular-elliptical in equatorial outline and more or less circular or triangular-circular in polar outline. Spheroidal to prolate, PIE = 1.00-1.80. Small to medium size, P x E = (14-29) x (9-25) ~tm. Colpi terminal, costate, membrane granular; endoapertures lalongate, more or less rectangular or elliptical in outline, constricted or nonconstricted in the middle, sometimes X-shaped, (2-6) x (5-14) ttm. Exine 1-1.5 ttm thick at the mesocolpium, with a thick endexine, more reduced at the poles, foot layer absent, short and widely spaced columellae and thick tectum. Ornamentation striate-rugulate.

The pollen of Securigera is a little larger than Coronilla, with the exception of C. viminalis, where the pollen size is similar to that of Securigera.

Taxa included: Coronilla coronata, C. juncea, C. minima, C. ramosissima, C. repanda subsp, dura, C. seorpioides, C. valentina subsp, glauca and subsp. pentaphylla, C. viminalis, Securigera atlantica, S. cretica, S. elegans, S. grandiflora, S. orientalis, S. parviflora, S. securidaca, S. varia.

244

PLATE I

M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239 257

I

4

G u IU

14

13 ~ *l.q ~


The ornamentat ion, outline in equatorial view and exine thickness varies. Five pollen types and two subtypes are recognised:

la. Ornamenta t ion striate-rugulate ................................................................................................................................. Type I b. Ornamenta t ion not striate-rugulate ......................................................................................................................... 2

2a. Ornamenta t ion finely reticulate .................................................................................................................................. Type V b. Ornamenta t ion perforate, perforate-rugulate, granulate-verrucate or perforate finely

granulate-rugulate ............................................................................................................................................................ 3 3a. Pollen with ornamenta t ion granulate-verrucate and rectangular in equatorial

outline .................................................................................................................................................................................. Type II b. Pollen with ornamenta t ion perforate, perforate-rugulate or perforate finely

granulate-rugulate and circular, elliptical or rectangular-elliptical in equatorial outline .................................................................................................................................................................................. 4

4a. Pollen with perforate-finely granulate-rugulate ornamentat ion, more or less circular in equatorial outline and exine 1.5-2 gm thick at mesocolpium .................................................................... Type IV

b. Pollen with perforate or perforate-rugulate ornamentat ion, elliptical or rectangular- elliptical in equatorial outline and exine 0.5-1.5 gm thick at mesocolpium .............................................. Type III (5)

5a. Ornamenta t ion perforate .............................................................................................................................................. Subtype I l i a b. Ornamenta t ion perforate-rugulate ............................................................................................................................ Subtype IIIb

The taxa examined are arranged in pollen types with measurements in microns of the mean and ranges for the polar (P) and equatorial (E) axes, the shape index PIE and the ornamenta t ion are shown in Table 1.

4.2. Type H (Plate II, 16-26)

R e c t a n g u l a r in e q u a t o r i a l ou t l i ne a n d m o r e or less t r i a n g u l a r - a n g u l a p e r t u r a t e in p o l a r out l ine . Sphe ro ida l to pro la te , P / E = l . O 0 - 1 . 5 8 . Smal l to

m e d i u m size, P x E = ( 1 8 - 3 0 ) × ( 1 7 - 2 5 ) gm. Co lp i m o r e o r less t e rmina l , costate , m e m b r a n e g ranu la r ; e n d o a p e r t u r e s l a longa te , m o r e or less el l ipt ical in ou t l i ne a n d cons t r i c t ed in the middle , ( 2 - 5 ) × ( 4 - 1 1 ) gm. Ex ine 1 - 2 g m th ick at the meso-

PLATE I

In 1-5, 7-11 and 13 scale bar equals 5 gin; in 6 and 12 scale bar equals 2 gin; in 14 and 15 scale bar equals 1 gm. 1-15. Type I. 1-4. Coronilla valentina subsp, pentaphylla (Balansa, 380). 1. LM equatorial view. 2. LM equatorial view. 3. LM endoaperture. 4. LM polar view. 5, 6. CoroniUa viminalis (Trethwey, 227). 5. SEM equatorial view and aperture. 6. SEM detail of ornamentation. 7, 8. Securigera securidaca (Shay 80/58). 7. LM equatorial view. 8. LM equatorial view. 9, 10. Securigera atlantica (Durando, 521). 9. LM Endoaperture. 10. LM polar view. 11, 12. Securigera grandiflora (Kotschy, 48). 11. SEM equatorial view. 12. SEM detail of ornamentation. 13 15. Securigera varia (Wyatt 31). 13. TEM equatorial section through whole pollen grain. 14. TEM exine stratification at apertural area. 15. TEM exine stratification at polar area.

246 M.J. D&z, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257

P L A T E II

16 1~ - k, 19


colpium, with a thick endexine, very reduced at the poles, foot layer absent, short, widely spaced irregular columellae, sometimes almost granular like and thick tectum. Ornamentation granulate-verrucate and perforate at the mesocolpium and more or less psilate at the apocolpia.

The endoapertures in Ornithopus perpusillus are a little smaller, (2-3) x (4-6) pm. typical of Type II.

Taxa included: Ornithopus compressus, O. isthmocarpus, O. perpusillus, O. pinnatus, O. sativus, O. uncinatus.

4.3. Type 111 (Plate 111, 27-37)

Elliptical or rectangular-elliptical in equatorial outline and more or less circular or tr iangular- circular in polar outline. Oblate-spheroidal to prolate, P/E=0.87-1.66. Small to medium size, P x E = ( 1 5 - 2 8 ) x (12-26) gm. Colpi more or less terminal, costate, membrane granular; endoapertures lalongate, elliptical or more or less rectangular in outline, slightly constricted or nonconstricted, sometimes circular in Hippocrepis unisiliquosa subsp, unisiliquosa, ( 3 - 5 ) x ( 5 - 1 1 ) I.tm. Exine 0.5-1.5 gm thick at the mesocolpium, with a thick endexine, very reduced at the poles, foot layer very reduced, columellae quite dense, short, broad, and thick tectum.

Two subtypes can be distinguished by ornamentation:

4.3.1. Subtype Ilia (Plate IlL 27-32, 35-37) Ornamentation perforate. The pollen of Hippocrepis constricta and H.

unisiliquosa subsp, bisiliqua is a little smaller in size, about 16 gin. In the rest of the species the pollen is 20 gm or more in size. The exine is a little less thick in H. bicontorta, 0.5-1 gm, and the endoapertures are smaller in H. bicontorta and H. comosa.

Taxa included: Hippocrepis areolata, H. biflora, H. ciliata, H. commutata, H. comosa, H. constricta, H. cyclocarpa, H. emerus subsp, emeroides and subsp, emerus, H. eriocarpa, H. glauca, H. minor, H. neglecta, H. salzmanni, H. scabra, H. squamata, H. unisiliquosa subsp, bisiliqua and subsp, unisiliquosa, H. valentina.

4.3.2. Subtype IIIb (Plate III, 33-34) Ornamentation perforate-rugulate on the meso-

colpium with some more or less distinct muri. There is a some similarity between the ornamen-

tation of this subtype and that of Type I. Taxa included: Hippocrepis atlantica, H. brevipet-

ala, H. multisilquosa.

4.4. Type IV (Plate IV, 38-46)

More or less circular or slightly elliptical in equatorial outline and circular in polar outline. Spheroidal, P/E = 0.86-1.09. Small to medium size,

PLATE II

In 16-21 and 23 scale bar equals 5 gm; in 22 and 24-26 scale bar equals 2 pm. 16-26. Type II. 16-21. Ornithopus isthmocarpus (16-19. Trethwey 230; 20, 21. SEV 26391). 16. LM equatorial view. 17. LM equatorial view. 18. LM endoaperture. 19. LM polar view. 20. SEM equatorial view and aperture. 21. SEM equatorial view. 22. Ornithopus pinnatus (SEV 38689), SEM detail of ornamentation. 23-26. Ornithopus perpusillus (Milne-Redhead, 5990). 23. TEM polar section through whole pollen grain. 24. TEM exine stratification at polar area. 25. TEM exine stratification at mesocolpium. 26. TEM exine stratification at apertural area.

248 M.J. Diez, ~ I~ Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257

P L A T E I I I

30

36 (for description see p. 250)

M.J. D&z, I. f~ Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257

PLATE IV

249

~ i i ~ ! ! ¸¸ iiiiiiiiiiiiiiiiiii!i ¸

" T |

48

40

(for description see p. 250)

250 M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239--257

P x E = ( 2 0 - 2 6 ) x (21-26) ~tm. Colpi more or less terminal, costate, membrane granular; endoapertures lalongate, elliptical or more or less rectangular in outline, slightly constricted or nonconstricted (7-10) ×(10-12) Ixm. Exine 1.5-2 ~tm thick at the mesocolpium with a thick endexine, reduced at the poles, foot layer thin, columellae short, irregular sometimes more or less granular, widely spaced, broad, expanded at base and fusing to form a foot

layer and thick tectum. Ornamentation perforate, finely granular-rugulate at the mesocolpium and more or less psilate at the apocolpium.

Taxa included: Antopetitia abyssinica.

4.5. Type V (Plate IV, 47-54)

Elliptical or rectangular-elliptical in equatorial outline and more or less circular in polar outline.

PLATE III (see p. 248)

In 27-31 and 35 scale bar equals 5 ktm; in 32-34 and 36 scale bar equals 2 ~tm; in 37 scale bar equals 1 ~tm. 27-37. Type III. 27-32 and 35-37 Subtype IIIa 27. Hippocrepis biflora (SEV 22668), LM equatorial view. 28. Hippocrepis glauca (SEV 25471), LM equatorial view. 29. Hippocrepis biflora (SEV 22668), LM endoaperture. 30. Hippocrepis emerus (SEV 43352), LM polar view. 31, 32. Hippocrepis glauca (SEV 25471). 31. SEM equatorial view. 32. SEM details of ornamentation and aperture. 33, 34. Subtype IIIb. Hippocrepis brevipetala (SEV 123.535). 33. SEM details of ornamentation. 34. SEM Details of ornamentation and aperture. 35 37. Hippocrepis biflora (Prior, s.n.). 35. TEM polar section through whole pollen grain. 36. TEM exine stratification at polar area. 37. TEM exine stratification at mesocolpium.

PLATE IV (see p. 249)

In 38-42, 44 and 47-51 scale bar equals 5 ~tm; in 43, 45, 46 and 52 54 scale bar equals 2 ~tm. 38-46. Type IV. Antopetitia abyssinica (38-41 and 43, Daramola, 6230; 42, Stolz, 207; 44-46, Staples, 373). 38. LM equatorial view. 39. LM equatorial view. 40. LM endoaperture. 41. LM polar view. 42. SEM equatorial view. 43. SEM detail of ornamentation. 44. TEM polar section through whole pollen grain. 45. TEM exine stratification at polar area. 46. TEM exine stratification at apertural area. 47-54. Type V.47. Scorpiurus vermiculatus (SEV 46669), LM equatorial view. 48. Scorpiurus muricatus (SEV 7956), LM equatorial view. 49. Scorpiurus verrniculatus (SEV 46669), LM endoaperture. 50. Scorpiurus muricatus (SEV 7956), LM polar view. 51, 52. Scorpiurus muricatus (Atchley, s.n.). 51. SEM equatorial view. 52. SEM detail of ornamentation. 53, 54. Scorpiurus muricatus (Wade, 3771). 53. TEM exine stratification at apertural area. 54. TEM exine stratification at mesocolpium.


Prolate-spheroidal to prolate, P/E=1.12-1.76. Small to medium size, P × E = ( 1 8 - 2 5 ) x ( 1 2 - 1 6 ) ~tm. Colpi terminal, costate, membrane granular; endoapertures lalongate, more or less elliptical in outline, slightly constricted or nonconstricted, (2.5-3)×(3-6) ~tm. Exine ca. 1 pm thick at the mesocolpium, with a thick endexine, more reduced at the poles, foot layer absent, columellae short, comparatively thin, regular and dense, a little more widely spaced and irregular at the poles and thick tectum. Ornamentation microreticulate, lumina less 1 ~tm.

Taxa included: Scorpiurus muricatus, S. vermiculatus.

5. Discussion of pollen morphology of Coronilla and related genera

Pollen Type I is comprised of the genus Coronilla and the recently recircumscribed genus Securigera (Lassen, 1989a). The type is well defined and easily recognised by its striate-rugulate ornamentation which is very unusual in the pollen of the subfamily Papilionoideae. The pollen of the species placed in Securigera differs only from those of Coronilla by being slightly larger in size. In view of this, pollen morphology does not help with the delimitation of Seeurigera from Coronilla. It is noteworthy that the pollen of Securigera securidaca the only species placed in the genus Securigera by some workers including Ball (1968) and Chamberlain (1970), but transferred to Coronilla by Schmidt (1978), is also indistinguishable from that of Coronilla and from the other species recently transferred to Securigera.

The genus Ornithopus is macromorphologically well defined and it has very distinctive pollen ornamentation and comprises pollen Type II.

Pollen Type III is comprised of the genus Hippocrepis. Two more or less distinct subtypes are recognised. No clear macromorphological characters have been found which correlate with these subtypes. The perforate-rugulate subtype could be regarded as a link with the well developed striate-rugulate ornamentation of Type I. It is noteworthy that Lassen (1989a),Lassen (1989b) transferred Coronilla emerus and Coronilla emeroides to Hippocrepis and pollen morphology

provides additional evidence to support this re-arrangement.

The geographically isolated Antopetitia comprising pollen Type IV although quite distinct in a number of pollen characters shows a very slight similarity in its finely granular-rugulate ornamentation to the distinctive granulate-verrucate ornamentation of Ornithopus of pollen Type II. It is noteworthy that Ohashi (1971) links Antopetitia palynologically with Ornithopus and the pollen data may reflect the close macromorphological relationship reported between the two genera (Polhill, 1981 ). The macromorphologically specialised Scorpiurus comprises pollen Type V and this is the most distinct pollen type in the group. The reticulate ornamentation and the regularly arranged slender, short columellae in the infratectum make this stand out palynologically not only from the rest of the genera in the group but from the pollen of all the genera in tribes Coronilleae and Loteae.

6. A review of the pollen morphology of Loteae and Coronilleae, a key to pollen types and a table summarising the types

In general the apertures and ornamentation of the pollen of Anthyllis are very similar to Lotus and it is difficult to distinguish all the species in the two genera by pollen morphology. The ornamentation of the four-aperturate species of Lotus does differ slightly from Anthyllis species with four- aperturate pollen. Similarly Hymenocarpos with five-seven aperturate pollen can be distinguished from the palynologically somewhat anomalous North American Lotus strigosus. Pseudocolpi are only present in the Anthyllis vulneraria group.

Anthyllis tetraphylla stands out from the rest of the species with three-aperturate pollen by its comparatively very large pollen. It shows similarities to Tripodion (Hammatolobium) in having a much thicker exine than occurs in the pollen of the rest of the Loteae/Coronilleae group.

The striate-rugulate exine ornamentation distinguishes the pollen of Coronilla and Securigera as does the granulate-verrucate ornamentation of Ornithopus.

The pollen of a number of the genera that

252 M.J. D&z, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257

la. Pollen with 5-6(-7)aper tures ....................................................... 2 b. Pollen with 3-4(-5) apertures ...................................................... 3

2a. Ornamenta t ion psilate, finely perforate .................................... Hymenocarpus circinatus type (= Anthyllis I) b. Ornamenta t ion verrucate ............................................................... Lotus strigosus type (= Lotus I)

3a. Pollen with 4(-5) apertures ........................................................... 4 b. Pollen with 3(-4) apertures ........................................................... 7

4a. Ornamenta t ion psilate-finely perforate and fossulate ......... Anthyllis montana type (=Anthyll is II) b. Ornamentat ion striate-rugulate or rugulate-fossulate ........ 5

5a. Ornamenta t ion str iate-rugulate .................................................. Lotus denticulatus type (= Lotus IIc) b. Ornamenta t ion rugulate-fossulate ............................................. 6

6a. P = 21-29 ~tm ...................................................................................... Lotus argophyllus type (= Lotus IIa) b. P = 18-22 gm ...................................................................................... Lotus micrantus type (= Lotus IIb)

7a. P = 4 8 - 6 0 gm ...................................................................................... Anthyllis tetraphylla type (=Anthyll is III) b. P = 11-42 gm ...................................................................................... 8

8a. Exine 2-3 lam thick, circular in equatorial outline and P = 30-41 I.tm ...................................................................................... Tripodion lotoides type (=Anthyll is III)

b. Exine 0.5-2 ~m thick and elliptical, rectangular, rectangular elliptical and rarely circular in equatorial outline and P = 11-34 p.m .............................................................. 9

9a. Rectangular in equatorial outline ............................................... 10 b. Elliptical or rectangular-ell iptical (sometimes circular)

in equatorial outline ........................................................................ 12 10a. Ornamenta t ion granulate-verrucate .......................................... Ornithopus perpusillus type (=Coroni l la II)

b. Ornamentat ion psilate, perforate and/or fossulate ............... 11 l l a . P = 2 1 - 2 6 I.tm ...................................................................................... Anthyllis gerardii type (=Anthyll is IVa;

Dorycniopsis) b. P = 2 7 - 3 6 gm ...................................................................................... Cytisopsis dorycnifolia type (=Anthyll is IVb)

12a. Ornamenta t ion striate-rugulate .................................................. 13 b. Ornamentat ion reticulate, perforate-rugulate or

psilate-perforate and/or fossulate ............................................... 14 13a. Ornamenta t ion striate-rugulate over all the pollen and

endoaperture clearly lalongate, ( 2 - 6 ) x (5-14) ~tm ............... Coronilla varia type (=Coroni l la I) b. Ornamenta t ion striate-rugulate at the mesocolpium

and psilate perforate at the poles and endoaperture almost circular, ( 7 - 8 ) x (9-10) ~tm ............................................. Vermifrux abyssinica type (= Lotus IIIe)

14a. Ornamenta t ion finely reticulate ................................................... Scorpiurus muricatus type (=Coroni l la V) b. Ornamentat ion perforate, perforate-rugulate,

perforate-finely granulate rugulate, psilate-perforate and/or fossulate ................................................................................. 15

15a. With pseudocolpi .............................................................................. Anthyllis vulneraria type (= Anthyllis IVc) b. Without pseudocolpi ....................................................................... 16

16a. P = 32-38(X,> 34) p.m ..................................................................... Pseudolotus makranicus type (=Lotus llIa) b. P = l l - 3 5 ( X < 3 0 ) gm ..................................................................... 17

17a. With granules at colpus margin .................................................. Lotus crassifolius type (= Lotus IIId; Hosackia) b. Without granules at colpus margin ............................................ 18

18a. Endoapertures of (1-5) x (3-10) gm .......................................... Lotus creticus type (= Lotus IIIb) and Hippocrepis type (= Coronil la I l i a and Coronil la I l lb)

b. Endoapertures of ( 5 -10 )x (5-15) gm ....................................... Podolotus hosackioides type (=Lo tus IIIc), Anthyllis cytisoides type (=Anthyll is IVd) and Antopetitia (Coronilla IV)

The types are summarised in Table 2.

M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239~57 253

have been segregated from Anthyllis including Dorycnopsis and Cytisopsis can be distinguished by shape and size.

Vermifrux has pollen with distinct striate- rugulate ornamentation at the equator and psilate- perforate ornamentation at the poles.

Scorpiurus has very distinctive pollen with reticulate ornamentation. While Pseudolotus is distinguished by its comparatively large three- aperturate pollen.

The differences in the pollen morphology between the North American species of Lotus (subgenus Hosackia) with three apertures and the majority of the Old World species of Lotus and also Acmispon roudairei, the Anthyllis cytisoides group, Hippocrepis, Podolotus and the tropical African Antopetita are very small as can be seen summarised in the general key to pollen types of the whole Loteae/Coronilleae group that follows.

The pollen types described for the Anthyllis group (Diez and Ferguson, 1991), the Lotus group (Diez and Ferguson, 1994) and the Coronilla group are combined together into a single key.

7. General discussion and systematic conclusions

The pollen morphology of the majority of the genera placed in the tribes Loteae and Coronilleae of Polhill (1981) is relatively distinctive, particularly the exine stratification where there is a well development endexine, foot layer very reduced or absent, short, irregularly spaced columellae or large granules in the infratectum and a complete and thick tectum. This type of stratification is regarded as rather specialised by Ferguson and Skvarla (1981),Ferguson and Skvarla (1983) and Guinet and Ferguson (1989). The frequently occurring psilate ornamentation especially but also the striat- e-rugulate and fossulate-rugulate or even granulate-verrucate ornamentation found in Ornithopus are also distinctive and this combination of exine stratification and ornamentation type does not occur in other groups of the subfamily Papilionoideae. Psilate ornamentation does occur in the tribe Phaseoleae especially in the subtribe Diocleinae where it is regarded as a "derived" character (Kavanagh and Ferguson, 1981).

Within the Loteae/Coronilleae aperture number and exine ornamentation are the most useful pollen characters for dividing the group (see the key to pollen types). In Anthyllis and related genera there is a trend towards increase in aperture number from three-colporate to three-colporate with pseudocolpi to four-colporate and to six-seven colporate. A similar trend occurs in Lotus and closely related genera. Three-colporate pollen is wide- spread but most of the western North American species have four-colporate, or less commonly six- colporate pollen. Only those North America taxa that have been put into subgenus Hosackia have three-colporate pollen. This parallel in increas- ing aperture number between the primarily Mediterranean Anthyllis group and the North American Lotus group is noteworthy. Guinet and Ferguson (1989) have suggested than an increase in aperture number in the pollen of Leguminosae is indicative of specialisation and it would appear that the trend has evolved independently in the geographically and taxonomically separate lines in the tribe Loteae of Polhill (1981).

It is perhaps remarkable that there is no variation in aperture number in the Coronilla group (tribe Coronilleae of Polhill, 1981). However, there is far more variation in the exine ornamentation in this group than in the Loteae. The striate-rugulate ornamentation in Coronilla and Securigera is very rare in the subfamily Papilionoideae. Apart from occurring in a few North American species of Lotus and in Vermifrux it is only found in the taxonomically very remote tribe Swartzieae (Ferguson and Skvarla, 1991).

The striate-rugulate exine ornamentation in the three closely related North American species of Lotus, L. denticulatus, L. humistratus and L. wrangelianus is somewhat paralleled in the African genus Vermifrux. The pollen of the North American species of Lotus subgenus Hosackia is three-colporate which is distinguishable from the pollen of the Old World species of Lotus only by the presence of granules at the colpus margins. It is noteworthy that Crompton and Grant (1993) believe that the pollen of the Hosackia group is more closely related to that of the North American species than to the Old World taxa. However, these problems highlight the need for a complete taxonomic review

254 M.J. Diez, I.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239 257

Table 2 Summary of the major pollen characters used to distinguish all the types and subtypes recognised in the Loteae and Coronilleae (see Diez and Ferguson, 1991,Diez and Ferguson, 1994) and listing the taxa included. The arrangement of the types follows the order of the key to pollen types. Similar pollen types are placed adjacent to each other using aperture number and exine ornamentat ion as the primary distinguishing characters. Measurements are in ktm and only the ranges for the polar (P) and (E) are given and P/E indicates the shape index

Anthyllis I (Hymenocarpos circinatus type) Apertures 6 G7), ornamentat ion psilate, finely perforate. P x E=(21 32)x (18-34); P/E=0.82-1.36, suboblate to subprolate rarely prolate Taxa included: Anthyllis cornicina, A. lotoides, Hymenoearpos circinatus Lotus I (Lotus strigosus type) Apertures 5 6 ~7) , ornamentat ion verrucate. P x E = ( 2 2 33)x (24 38); P/E=0.81 1.00, suboblate to spheroidal Taxa included: Lotus strigosus Anthyllis II (Anthyllis montana type) Apertures 4 (-5), ornamentat ion psilate, finely perforate and fossulate. P x E = (20-33) x (20-34); P/E =0.75-1.28, suboblate to subprolate Taxa included: Anthyllis barba-jovis, A. hamosa, A. henoniana, A. hermanniae, A. montana, subsp, hispanica, subsp, jacquinii, subsp. montana Lotus IIc (Lotus denticulatus type) Apertures 4, ornamentat ion striate rugulate. P × E=(21 26)x (18 23); P/E= 1.04 1.26, spheroidal to subprolate Taxa included: Lotus denticulatus, L. humistratus, L. wrangelianus Lotus Ila (Lotus argophyllus type) Apertures 4 (-5), ornamentat ion rugulate fossulate. P × E = (21-29) x ( 19- 30); P/E = 0.86-1.20, suboblate to subprolate Taxa included: L. argophyllus, L. argyraceus, L. benthamii, L. grandiflorus, L. hermannii, L. junceus, L. nevadensis, L. rigidus, L. salsuginosus, L. scoparius, L. strigosus vat. tomentellus, L. wrightii Lotus IIb (Lotus micranthus type) Apertures 4, ornamentat ion psilate perforate. P x E = ( 1 8 22)x (17 23); P/E=0.86 1.11, suboblate to spheroidal Taxa included: Lotus haydonii, L. micranthus, L. purshianus Anthyllis III (Anthyllis tetraphylla type) Apertures 3 (-4), ornamentat ion psilate perforate. P x E = ( 3 0 - 6 0 ) × (30-60); P/E=0.79-1.18, suboblate to spheroidal. Exine 2-3 ~tm thick Taxa included: Tripodion (Anthyllis) tetraphylla, T. (Hammatolobium) kremerianum, Z (Hammatolobium) graecum Coronilla II (Ornithopus perpusillus type) Apertures 3, ornamentat ion granulate, verrucate and perforate. P x E = ( 1 8 30) x (17-25); P/E= 1.0 1.58, spheroidal to prolate. Exine I -2 ~tm thick Taxa included: O. compressus, O. isthmocarpus, O. perpusillus, O. pinnatus, O. sativus, O. uncinatus Anthyllis IVa (Anthyilis gerardii type) Apertures 3, ornamentat ion psilate, perforate and fossulate. P x E=(21 26)x (21 26); P/E=0.95-1.18, _+spheroidal Taxa included: Anthyllis gerardii Anthyllis IVb (Cytisopsis dorycnifolia type) Apertures 3, ornamentat ion psilate fossulate. P x E = ( 2 7 - 3 6 ) × (23-34); P/E= 1.00-1.20, spheroidal to subprolate Taxa included: Cytisopsis ahmedii, C. dorycnifolia Coronilla I (Coronilla varia type) Apertures 3, ornamentat ion striate rugulate. P x E = ( 1 4 - 2 9 ) x (9-25); P/E= 1.0-1.8, spheroidal to strongly prolate. Endoapertures lalongate (2-6) x (5-14) ~tm Taxa included: Coronilla coronata, C. juncea, C. minima, C. ramosissima, C. repanda subsp, dura, C. scorpioides, C. valentina, subsp. glauca, subsp, pentaphylla, C. viminalis, Securigera atlantica, S. cretica, S. elegans, S. grandiflora, S. orientalis, S. parviflora, S. securidaca, S. varia Lotus IIIe (Vermifrux abyssinica type) Apertures 3, ornamentat ion striate rugulate on mesocolpium, psilate on poles. P × E = ( 2 0 27) x (20 25); P/E=0.9-1.13, _+spheroidal. Endoapertures circular (7-8) × (9-10) ~tm Taxa included: Vermifrux abyssinica Coronilla V (Scorpiurus muricatus type) Apertures 3, ornamentat ion finely reticulate. P × E = ( 1 8 - 2 4 ) × (12 16); P/E= 1.12 1.76, spheroidal to strongly prolate Taxa included: Scorpiurus muricatus, S. vermiculatus Anthyllis Ivc (Anthyllis vulneraria type)

M.J. Diez, 1.K. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239-257 255

Table 2 (continued)

Apertures 3, ornamentation psilate, finely perforate. P x E=(24-42)x (23-38); P/E=0.96-1.33, spheroidal to subprolate or prolate. Pseudocolpi present Taxa included: Anthyllis cherleri, A. polycephala, A. ramburii, A. tejedensis, A. vulneraria, subsp, maura, subsp, vulneraria Lotus Ilia (Pseudolotus makranieus type) Apertures 3, ornamentation psilate perforate. P × E=(32-38)× (30-37); P/E=0.94-1.12, +_ spheroidal Pseudocolpi absent Taxa included: Pseudolotus makranicus Lotus IIId (Lotus crassifolius type) Apertures 3, ornamentation psilate perforate with granules around the colpus margin. P ×E=(18-23)×(16-20); P/E=I.O0 1.35, spheroidal prolate Taxa included: Lotus crassifolius, L. oblongifolius, L. stipularis Coronilla IIIa and Coronilla IHb (Hippocrepis type) Apertures 3, ornamentation perforate or perforate rugulate. P × E=(15-28)×(12 26); P/E=0.87-1.66, spheroidal to _+strongly prolate Taxa included: Hippocrepis areolata, H. atlantica, 14. biflora, H. brevipetala, H. ciliata, H. commutata, H. comosa, H. constricta, H. cyclocarpa, H. emerus, subsp, emeroides, subsp, emerus, H. eriocarpa, H. glauca, H. minor, H. multisiliquosa, H. neglecta, H. salzmanni, 14. scabra, H. squamata, H. unisiliquosa, subsp, bisiliqua subsp, unisiliquosa Lotus IIIb (Lotus creticus) type Apertures 3, ornamentation psilate, perforate. P x E = ( l l 31)× (7-31); P/E=0.95-1.90, spheroidal to strongly prolate Taxa included: Dorycnium broussonetii, D. fulgurans A, D. fulgurans B, D. graecum, D. hirsutum, D. pentaphyllum subsp, gracile, subsp. herbaceaum, subsp, pentaphyllym, D. rectum, D. spectabile, Lotus alpinus, L. angustissimus, L. arabicus, L. arenarius, L. australis, L. benoistii, L. berthelotii, L. biflorus, L. campylocladus, L. conimbrecensis, L. conjugatus, L. corniculatus, L. creticus, L. cruentus, L. cytisoides, L. discolor, L. dumetorum, L. edulis, L. garcinii, L. gebelia, L. glaber, L. glareosus, L. glinoides, L. goetzei, L. halophilus, L. hebecarpus, L. hispidus, L. jacobaeus, L. jolyi, L. krylovii, L. lalambensis, L. lancerottensis, L. lanuginosus, L. longisiliquosus, L. maculatus, L. maritimus, L. mascaensis, L. namubensis, L. ononopsis, L. ornithopodioides, L. parviflorus, L. pedunculatus, L. sessifolius, L. spartioides, L. tetragonolobus, L. tetraphyllus Lotus IIIc (Podolotus hosackioides type) Apertures 3, ornamentation psilate perforate and fossulate. P × E=(23-34)× (24-29); P/E=0.88-1.21, suboblate to subprolate Taxa included: Acmispon roudairei, Podolotus hosackioides Anthylfis IVd (Anthyllis cytisoides type) Apertures 3, ornamentation psilate perforate or finely fossulate. P × E = (24-3)5 × (20-32); P/E= 0.93-1.50, spheroidal to prolate Taxa included: Anthyllis aurea, A. cytisoides, A. terniflora Coronilla IV (Antopetitia type) Apertures 3, ornamentation perforate, finely granular-rugulate at mesocolpium and more or less psilate at apocolpium. P × E = (20-26) × (21-26); P/E=0.86-1.09, suboblate-spheroidal Taxa included: Antopetitia abyssinica

of relationships in Lotus and its closely related genera.

Although there have been many studies of the group, workers since Bentham (1865) have tended to focus their attention primarily on regional studies often at species level and below and there is a need to evaluate the similarities and differences that occur in a wide range of characters in both the Old World and the New World taxa before generic boundaries can be firmly established. This has been pointed out to same extent by Isely (1981) and more recently Lassen (1989a; pers. commun.) who is currently revising much of the group.

Hippocrepis with two types of pollen ornamentation is somewhat intermediate; one group of the

species with rugulate-fossulate ornamentation slightly resembles Coronilla while the other group with a perforate tectum is more similar to Lotus.

The pollen morphology of Scorpiurus is rather anomalous in the tribes both in ornamentation and stratification. The pollen is of a more general- ised type and it could point to need to re-evaluate the position of the genus in the Loteae/Coronilleae.

Ferguson and Skvarla (1981) have suggested that there is some evidence from pollen morphology for keeping separate the tribes Coronilleae and Loteae. They based this view on results from the pollen of Hymenocarpos, Lotus and only Scorpiurus from the Coronilla group. The latter genus has been shown to have atypical pollen. Overall there

256 M.J. Diez, LK. Ferguson/Review of Palaeobotany and Palynology 94 (1996) 239 257

appears to be little evidence from comparative pollen morphological studies to support upholding two distinct tribes. The data from the present investigation, especially from the exine stratification, suggest a broad interpretation of the tribe Loteae as adopted by Lassen (1989a) and followed by Lock (1989) and Lock and Simpson (1991) would be more appropriate.

The Coronilleae/Loteae are placed near to other temperate tribes including Cicereae, Trifolieae and Vicieae (Polhill, 1981). The pollen of these tribes shows similarities to Loteae/Coronilleae in size, shape, thin exine, exine thinner at the poles in comparison with the equator and also differences between the ornamentation on the poles and the equator (Clarke and Kupicha, 1976). The exine stratification of the Vicieae, particularly the well developed endexine, sometimes granular infratec- turn and often complete tectum (Ferguson, 1985) does resemble Loteae but the foot layer is rarely completely absent and as also occurs in Trifolieae where the tectum is usually reticulate or reticulate-rugulate. Some species of Trifolium do have a more or less psilate perforate tectum (Mufioz Rodriguez, 1990) but the exine stratification appears to differ having regular, distinct columellae (Ferguson and Skvarla, 1981). Cicer has pollen with reticulate ornamentation and exine stratification with distinct regular columellae (Ferguson and Skvarla, 1981).

Doyle et al. (1995) have shown from molecular systematic studies that the Loteae/Coronilleae group show unexpected results in having similarities with predominantly tropical tribes including Phaseoleae and Millettieae and not with those tribes with temperate distribution and herbaceous habit with which they have long been considered to be related. It has been pointed out in the present palynological investigation that many of the pollen characters in Loteae/Coronilleae are "derived" and in many ways the data from pollen morphology are not inconsistent with the molecular systematic findings. The similarities in pollen between some tropical tribes, particularly Phaseoleae, and the Loteae/Coronilleae could be considered as indicative of as much phylogenetic relationship between these groups as there is with the temperate tribes

with which Loteae/Coronilleae have been tradi- tionally placed.

However, as Doyle et al. (1992) point out only when more characters are investigated and homol- ogies more fully analysed can the phylogenetic relationships between Loteae/Coronilleae and temperate and tropical group be understood.

Acknowledgements

We are grateful to Dr. R.M. Polhill (Kew), Dr. J.M. Lock (Kew) and Mr. P. Lassen (Lund) for comment and advice. We thank Judith Sheldon and Hannah Banks for technical assistance.

References

Alsina Aser, M., 1984. Estudio palinol6gico de Ornithopus L. (Leguminosae) en la Peninsula Ib6rica. Anal. Asoc. Pal. Lengua Esp., 1: 15-20.

Ball, P.W., 1968. Securigera D.C., Coronilla L., Ornithopus L., Hippocrepis L., Scorpiurus L., Hammatolobium Fenzl. In: T.G. Tutin, V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Val- entine, S.M. Walters and D.A. Webb (Editors), Flora Euro- paea, 2. Cambridge Univ. Press, Cambridge, pp. 177--185.

Bentham, G., 1865. Leguminosae. In: G. Bentham and J.D. Hooker (Editors), Genera Plantarum 1. pp. 434 600.

Chamberlain, D.F., 1970. Securigera L., Coronilla L., Hip- pocrepis L., Ornithopus L. In: P.H. Davis (Editor), Flora of Turkey, 3. Edinburgh Univ. Press, Edinburgh, pp. 537 547.

Clarke, G.C.S. and Kupicha, F.K., 1976. The relationships of the genus Cicer L. (Leguminosae). The evidence from pollen morphology. Bot. J. Linn. Soc., 72:35 44.

Crompton, C.W. and Grant, W.F., 1993. Pollen morphology in Loteae (Leguminosae) with particular reference to the genus Lotus L. Grana, 32: 129-153.

Diez, M.J. and Ferguson, I.K., 1991. Studies of the pollen morphology and taxonomy of the tribes Loteae and Coronilleae (Leguminosae: Papilionoideae). 1. Anthyllis L. and related genera. Lagascalia, 16: 77-94.

Diez, M.J. and Ferguson, I.K., 1994. The pollen morphology of the tribes Loteae and Coronilleae (Papilionoideae: Legumin- osae). 2. Lotus L. and related genera. Rev. Palaeobot. Paly- nol., 81:233 255.

Dominguez, E., 1976. Revisi6n de las especies anuales del g6nero Hippocrepis L. Lagascalia, 5: 225-261.

Dominguez, E. and Galiano, E.F., 1974a. Revisi6n del gdnero Scorpiurus L. I. Parte experimental. Lagascalia, 4: 61-84.

Dominguez, E. and Galiano, E.F., 1974b. Revisi6n del g6nero Scorpiurus L. II. Parte sistemfitica. Lagascalia, 4:259 280.

Doyle, J.J., Lavin, M. and Bruneau, A., 1992. Contributions of


molecular data to Papilionoid legume systematics. In: P.S. Soltis, D.E. Soltis and J.J. Doyle (Editors), Molecular Sys- tematics of Plants. Chapman and Hall, New York, NY, pp. 223-251.

Erdtman, G., 1960. The acetolysis method. A revised description. Sven. Bot. Tidskr., 54: 561-564.

F~egri, K. and Iversen, J., 1975. Textbook of Pollen Analysis. Munksgaard, Copenhagen.

Ferguson, I.K., 1985. The role of the pollen morphology in plant systematics. An. Asoc. Pal. Lengua Esp., 2: 5-18.

Ferguson, I.K. and Skvarla, J.J., 1981. The pollen morphology of the subfamily Papilionoideae (Leguminosae). In: R.M. Polhill and P.H. Raven (Editors), Advances in Legume Sys- tematics. R. Bot. Gard. Kew, pp. 859-896.

Fergusou, I.K. and Skvarla, J.J., 1983. The granular interstitium in the pollen of the subfamily Papilionoideae (Leguminosae). Am. J. Bot., 70:1401 1408.

Ferguson, I.K. and Skvarla, J.J., 1991. Pollen morphology of the tribe Swartieae (subfamily Papilionoideae: Leguminosae). 2. The genera Aldina Endlicher and Swartzia Schreber and systematic conclusions. Rev. Palaeobot. Palynol., 67: 153-177.

Fernandez, I., 1987. Fabaceae. In: B. Vald6s, M.J. Diez and I. Fermindez (Editors), Atlas Polinico de Andalucia Occidental. Sevilla, pp. 185-200.

Greuter, W., Burdet, H.M. and Long, G., 1989. Med-Checklist, 4. Leguminosae. Cons. Jard. Bot. Gen6ve, pp. 2-214.

Guinet, Ph. and Ferguson, I.K., 1989. Structure, evolution and biology of pollen of Leguminosae. In: C.H. Stirton and J.L. Zarucchi (Editors), Advances in Legume Biology. Mon. Syst. Bot. Mo. Bot. Gard., 29:77 103.

Isely, D., 1981. Leguminosae of the United States. III Subfamily Papilionoideae: Tribes Sophoreae, Podalyrieae, Loteae. Mem. NY Bot. Gard., 25:1 264.

Kavanagh, T.A. and Ferguson, I.K., 1981. Pollen morphology and taxonomy of the subtribe Diocleinae (Leguminosae: Papilionoideae: Phaseoleae). Rev. Palaeobot. Palynol., 32: 317-369.

Lassen, P., 1986. In: W. Greuter and T. Raus (Editors), Med- Checklist Notulae, 13. Willdenowia, 16: 109-114.

Lassen, P., 1989a. A new delimitation of the genera Coronilla, Hippocrepis and Securigera (Fabaceae). Willdenowia, 19: 49-62.

Lassen, P., 1989b. Om Kroniller, sl/iktet Coronilla, i Norden. Sven. Bot. Tidskr., 83:83 86.

Lock, J.M., 1989. Legumes of Africa. A checklist. R. Bot. Gard. Kew, pp. 339-348.

Lock, J.M. and Simpson, K., 1991. Legumes of West Asia. A checklist. R. Bot. Gard. Kew, pp. 172-176.

Meikle, R.D., 1977. Flora of Cyprus, 1. Leguminosae. R. Bot. Gard. Kew, pp. 372-606.

Mufioz Rodriguez, A.F., 1990. Estudio taxon6mico del g6nero Trifolium en la Peninsula Ib6rica. Ph.D. Thesis. Univ. Sevilla, Sevilla, pp. 1-690.

Ohashi, H., 1971. A taxonomic study of the tribe Coronilleae (Leguminosae) with special reference to the pollen morphology. J. Fac. Sci. Univ. Tokyo. III, 11: 25-92.

Pire, S.M., 1974. Estudio palinol6gico de la tribu Hedysareae (Leguminosae). Bonplandia, 3: 143-169.

Polhill, R.M., 1981. Loteae DC. In: R.M. Polhill and P.H. Raven (Editors), Advances in Legume Systematics. R. Bot. Gard. Kew, pp. 271 375.

Prados, A., Dominguez, E. and Ubera, J.L., 1985a. Estudio pali- noldgico de la tribu Hedysareae DC. en Andalucia Occiden- tal. Anal. Asoc. Pal. Lengua Esp., 2: 43-54.

Prados, A., Porras, A., Ubera, J.L. and Dominguez, E., 1985b. Relaciones dentro de la subfamilia Papilionoideae a la luz de los datos palinoldgicos. Anal. Asoc. Pal. Lengua Esp., 2: 55-66.

Punt, W., Blackmore, S., Nilsson, S. and Le Thomas, A., 1994. Glossary of pollen and spore terminology. Lab. Palaeobot. Palynol., Utrecht, LPP Found. Contrib. Ser. 1, 71 pp.

Schmidt, B., 1978. Securigera securidaca (L.) Degen and D6rfler eine Spezies der Gattung Coronilla L. Feddes Repert. Bot. Taxon. Geobot., 89: 597-600.

Schmidt, B., 1979. Beitr~ge zur Kenntnis der Sippenstrukur der Gattung Coronilla L. Feddes Repert., 90: 257-361.

Skvarla, J.J., 1966. Techniques of pollen and spores electron microscopy. Part. 1: Staining, dehydration and embedding. Okla. Geol. Notes, 26: 179-186.

Skvarla, J.J. and Pyle, C.C., 1968. Techniques of pollen and spores electron microscopy. Part II. Ultramicrotomy and associated techniques. Grana Palynol., 8: 255-270.

Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valen- tine, D.H., Waiters, S.M. and Webb, D.A., 1968. Flora Euro- paea 2. Leguminosae. Cambridge Univ. Press, Cambridge, pp. 80-191.

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