Leonardoxa africana (Baill.) Aubrév.

Mckey, Doyle B., 2000, Leonardoxa africana (Leguminosae: Caesalpinioideae): a complex of mostly allopatric subspecies, Adansonia (3) 22 (1), pp. 71-109 : 96-102

1. Leonardoxa africana (Baill.) Aubrév. subsp.

africana (= group 4)

Tree to 14 m tall. Trunk (rarely) to 40 cm diam., usually under 15 cm diam. Young shoots produced in flushes consisting of only a single internode and young leaf at each branch tip. Internodes of young twigs (2.5-)3.5-7.5(-9) cm long, modified as myrmecodomatia, swollen,

with thick pith except at base; twigs 4.3-5.7 mm diam. at apex tapering to ca. 2 mm diam. at base of internode; ant-cavities each a single internode long. Swollen internodes present from the seedling stage (20 cm tall) onward. Prostoma of ant-domatia at apex of internode opposite leaf insertion, elliptic. Leaves (2-)3(-rarely 4)-jugate. Leaflets elliptic, falcate, apex long-acuminate, the smallest leaflets (proximal pair) (7.8-)13(-15) cm long and (3.5-)5(-6) cm broad, the largest ones (distal pair in 2-jugate leaves, next-to-distal pair in 3- and 4-jugate leaves) (9.5-)15(-20) cm long and (4-)5.5(-7) cm broad; nectary glands large (smooth gland surface oblong, about 1 × 0.75 mm, surrounded by a raised ring of tissue about 1mm broad), consistently present on abaxial surface of each leaflet, with (2-)3-5 glands on each proximal leaflet, (1-)2(-3) glands on each median leaflet, and (0-)1-2 glands on each distal leaflet. Racemes to 4 cm long, with 40-50 flowers, usually cauliflorous, borne on main trunk and on large branches, or ramiflorous on twigs of ca. 5 mm diam. and larger. Flowers 1.8-2.2 cm in diam.; pedicels 2-4 mm long; calyx green or red, sepals 0.5-0.8 cm long; petals violet, purple, mauve, pink or red, 0.6-1.0 cm long. Ovules 4-5. Fruit oblongobovate, 8-11 cm long, 2.5-4 cm broad.

Leonardoxa africana subsp. africana is a highly specialised myrmecophyte, differing from the other myrmecophytic subspecies in a number of traits: (1) Foliar nectaries ( Fig. 5C ) are larger, more numerous, and less variable in presence/absence and number than in the other subspecies; (2) only a single leaf-bearing intern- ode is produced in each flush of growth at a branch tip, so that each ant-cavity is a single internode long ( Figs. 6B , 7B ); (3) growth of different branch tips is not synchronised over the crown of the tree; (4) specialised swollen internodes appear much earlier (seedlings 20 cm tall) in plant ontogeny than in the other subspecies; (5) the prostoma is elliptic-oblong rather than spherical in shape ( Fig. 6D ). Also, while cauliflory on old branches, or even on the trunk, occurs in all three myrmecophytic subspecies, it appears to be especially frequent in subsp. africana ( Fig. 8B ).

DISTRIBUTION. — Leonardoxa africana subsp. africana is restricted to coastal forests of Cameroon ( Figs. 3 , 4 ). All the field sites are below 80 m elevation. Judging from collection localities and notes on labels, this subspecies appears rarely to occur above about 100 m. The northernmost known localities are from the Southern Bakundu Forest Reserve , and the southern boundary of its range appears to be near Campo , at the border with Equatorial Guinea. Within this coastal strip, it extends inland as far as Bipindi, on the eastern edge of the coastal plain .

ECOLOGY. — This subspecies, illustrated in AUBRÉVILLE (1970), is the one that has attracted most attention as a myrmecophyte. The studies by ELIAS (1980), MCKEY (1984), GAUME et al. (1997) and GAUME & MCKEY (1999) all concern this subspecies. Internodes are swollen and hollow, and these ant-domatia are present already in seedlings 20 cm tall (see Fig. 2B in LÉONARD [1993]). This subspecies is associated with two ant species that are completely restricted to this host, the formicine Petalomyrmex phylax and the myrmicine Cataulacus mckeyi ( MCKEY 1984) . Petalomyrmex is a mutualist of the plant, protecting its young leaves against phytophagous insects ( GAUME et al. 1997), while Cataulacus is a parasite, providing no protection to the plant and excluding Petalomyrmex from plants it occupies ( GAUME & MCKEY 1999). This subspecies was termed “ L. africana taxon T4” by CHENUIL & MCKEY (1996).

Few observations of flower visitors have been made, but on a few occasions sunbirds were seen visiting the pink to red flowers, which in this subspecies at least seem to have a somewhat longtubular corolla, compared to flowers of the non-myrmecophytic subspecies (see below).

ADDITIONAL SPECIMENS EXAMINED. — CAMEROON,

Southwest Province: Southern Bakundu Forest

Reserve, E.W. Jones in Brenan 9499 (K, P), FHI 29511 (K), 29672 (K), and 41007 (K); Southern Bakundu Forest Reserve, 1 km W Bombe Bakundu, Manning 1499 (MO); Southern Bakundu Forest Reserve, near Kindonge Camp, Manning 1517 (MO); Kumba (planted in forestry nursery), FHI 29369 (K). Littoral Province: 24 km E Douala, Breteler et al. 2580 (BR, K, P, YA); Douala, route Razel, Endengle 2105 (P, YA); Douala, forêt de Yelfoume, Fleury, in herb. Chevalier 33346 (P); 14 km E Douala, Douala-Edea Road, Mpom 303 in part (BR); Lake Tissongo, Douala-Edea Forest Reserve, McKey & Gartlan 120 (K), D.W. Thomas 167 (YA), Waterman & McKey 846 (K); stream Mangombe near Edea, Mpom 343 (YA). Central-South Province: near Bipaga II, km 40 from Kribi to Edea, de Kruif 994 (WAG); Lolodorf Road, 12 km E of Kribi, Bos 3630 (BR, WAG, YA); 5 km N of Lolodorf road, 19 km E of Kribi, Bos 3913 (BR, YA); Lolodorf Road, 18 km E of Kribi, Bos 4074 (BR, YA); km 30 from Kribi to Ebolowa, Bos 6233 (WAG); km 45 from Kribi to Campo, Bos 7315 (BR); 60 km S of Edea, S of Mboke, 11 km E of km 58 from Edea to Kribi, Leeuwenberg 5500 (BR, K, MO, P, WAG, YA); colline Nkoltsia, Villiers 775 (P); near Bella, Letouzey 4140 (P, YA); 2 km from Nkol-Bewa, Mpom 227 (P, YA); Edoudouma, Mpom 283 (YA); Bipindi, Farron 7181 (BAS, P, YA), Zenker, s.n. (BR, P), 52 (WAG), 1074 (K, MO, P, WAG), 2967 (BR, K, WAG), 4183 (BR, K, P), 4495 (BR, K, MO).

2. Leonardoxa africana subsp. letouzeyi McKey , subsp. nov. (= group 3)

Haec subspecies Leonardoxae africanae subsp. africanae arcte affinis, sed ab ea medullae loculo per internodia duo triave continuo, foliorum expansione simultanea ramunculi ad nodos terminales duos tresve, glandulis nectariferis crateriformibus minoribus ac quoad numerum plus variabilibus (ad foliola proximalia plerumque nullis ad duabus) atque foliolis usque ad 30 cm longis utroque rhachidis latere saepe quattuor distinguitur.

TYPUS. — D. W. Thomas et al. 7480, Cameroon, Southwest Province, roadside forest S of Baro Village , 5º14’N, 9º15’E, 250 m, 31 Mar. 1988 (holo-, MO; iso-, WAG).

Small tree, (rarely) to 14 m tall. Trunk to 30 cm diam. Young shoots produced in flushes consisting of (1-)2-3 internodes plus young leaves at each branch tip (in adult trees). Internodes of young twigs (2.8-)7(-13) cm long, modified as myrmecodomatia, swollen, with thick pith; twigs (4-)5.5(-6.1) mm diam. at apex tapering to ca. 2.5-4 mm diam. at base of internode; enlarged pith extending throughout section of twig produced in a single growth flush; ant-cavities each 2-3 internodes long (in adult trees). Swollen internodes absent in seedlings, present only in plants ≥ 60 cm tall. Prostoma of ant-domatia at apex of terminal internode of each flush of growth, opposite leaf insertion, roughly spherical in shape. Leaves (2-3-)4(-5)-jugate. Leaflets elliptic, falcate, apex long-acuminate, proximal ones (13.2-)17(-22) cm long and (4.5-)6(-8) cm broad, largest leaflets (next-to-distal pair) (14.5-) 21(-32) cm long and (5-)7.5(-12) cm broad. Nectary glands absent from some individuals; when present, appearing intermediate in size (smooth gland surface oblong, about 1 × 0.75 mm, not surrounded by a raised ring of tissue) and few in number, usually 0-2 (very rarely up to 5) on proximal leaflets and usually absent on other leaflets. Racemes short (axis 3-5 cm long), with 40-60 flowers, axillary on twigs of up to 1 cm diam., also sometimes cauliflorous. Flowers 1.8-3 cm diam.; pedicels 0.3-0.5 cm long; calyx pale lilac, sepals 0.8-1.1 cm long; petals usually violet, sometimes pink, 0.9-1.3 cm long. Ovules 4-5. Fruit to 15 cm long, 5 cm broad.

The most distinctive trait of L. africana subsp. letouzeyi is the large size of its stems and leaves ( Fig. 9C ). Young twigs are much more robust than those of corresponding age of plants of any of the other subspecies, leaflets are larger, and 4- jugate leaves predominate on most adult trees, in contrast to the 2-or 3-jugate leaves which characterise the other subspecies. Another trait distinguishing the subspecies letouzeyi from all other subspecies is the great variation among individual trees of the same population in the number of foliar nectaries. This subspecies shares with subsp. rumpiensis several traits that together distinguish them from subsp. africana : (1) Antcavities are first produced in juveniles over 50 cm tall; (2) ant-cavities in adult trees extend over 2-3 internodes, corresponding to the units of growth produced in flushes; (3) vegetative growth is synchronised over the crown of the tree; (4) the prostoma is roughly spherical in shape ( Fig. 6C ).

DISTRIBUTION. — This subspecies occurs in the wettest forests of Africa, the lowland forests near the Bight of Biafra ( Figs. 3 , 4 ). It is found from Uwet Division, Calabar Province, Nigeria, through Korup National Park on Cameroon’s border with Nigeria, and throughout the Mamfe Plain and Cross River area. Its range extends northward at least to the Takamanda Forest Reserve north of Mamfe. The eastern limit of its distribution is uncertain.

ECOLOGY. — This subspecies is a myrmecophyte in which swollen stems may first appear in juveniles about 60 cm tall (but more commonly in saplings 1 m or taller). While saplings are associated with small colonies of any of several species of twig-nesting ants, mature individuals are occupied solely by the formicine ant Aphomomyrmex afer , which protects young leaves of the host tree against insect herbivores (GAUME 1998; GAUME & MCKEY 1998). This subspecies was termed “ L. letouzeyi ” by MCKEY (1991) and “ L. africana taxon T3” by C HENUIL & M C K EY (1996), GAUME et al. (1998) and GAUME & MCKEY (1998). The ant occupants of this subspecies tend scale insects and mealybugs inside the hollow stems of the host (GAUME et al. 1998), in contrast to the ants associated with the subspecies africana , which never tend homopterans. (For the subspecies rumpiensis, more information is required on this point.) As argued by GAUME et al. (1998), this dependence on homopterans is related to the low and variable number of foliar nectaries in this subspecies.

PARATYPES. — NIGERIA, Uwet Division: Calabar River, Latilo 35 ( BR, K, P) ; Oban, Talbot 1440 ( K) . — CAMEROON, Southwest Province: Bamenda Road, Mile 43 from Mamfe , 1,500 ft (460 m), Coombe 191 ( BR, K) ; Akpasang River, Korup National Park, McKey 72 ( P, YA) ; Korup National Park, between Mana River bridge and Camp 1, Manning 1714 ( MO) ; disturbed forest near Ndian Oil Palm Plantation , 50 m, D. W. Thomas 4269 ( BR, US) ; Takamanda Forest Reserve, near Matene , 170 m, D. W. Thomas 4527 ( MO) .

3. Leonardoxa africana subsp. rumpiensis McKey , subsp. nov. (= group 2)

Haec subspecies Leonardoxae africanae subsp. letouzeyi perarcte affinis, sed ab ea glandulis nectariferis crateriformibus majoribus ac quoad numerum plus constantibus (ad foliola proximalia plerumque nullis ad duabus) atque foliolis utroque rhachidis latere plerumque duobus distinguitur.

TYPUS. — Letouzey 14577, Cameroon, Southwest Province, Dikome Balue, 4°55’N, 9°15’E, 35 km NNW Kumba, 1200 m, 24 Mar. 1976 (holo-, P; iso-, K, YA).

Small tree, to 14 m tall. Trunk to 35 cm diam. Young shoots produced in flushes consisting of (1-)2-3 internodes plus young leaves at each branch tip (in adult trees) ( Fig. 7 ). Internodes of young twigs (3-)5.5(-11) cm long, modified as myrmecodomatia, swollen, with thick pith; twigs (3-)4(-5) mm diam. at apex tapering to ca. 2-3 mm diam. at base of internode; enlarged pith extending throughout section of twig produced in a single growth flush; ant-cavities each 2-3 internodes long (in adult trees). Swollen internodes absent in seedlings, present only in plants ≥ 50 cm tall. Prostoma of ant-domatia at apex of terminal internode of each flush of growth, opposite leaf insertion, roughly spherical in shape. Leaves 2 (-3)-jugate ( Fig. 9 ). Leaflets elliptic, falcate, apex acuminate to long-acuminate, smallest ones (proximal pair) (6.5-)16(-28) cm long and (2.7-) 6.5(-11) cm broad, largest leaflets (second pair) (7-)17.5(-30) cm long and (3-)7(-12) cm broad. Nectary glands of intermediate size (smooth gland surface oblong, about 1 × 0.75 mm, not surrounded by a raised ring of tissue), usually 2(0-5) on proximal leaflets ( Fig. 5 ), (0-)1(-2) on other leaflets. Racemes short (axis 3-5 cm long), with> 40-60 flowers, axillary on twigs 4-5 mm diam., also sometimes cauliflorous (on trunk up to 10 cm diam.). Flowers 1.8-3 cm diam.; pedicels 0.3-0.5 cm long; calyx colour unknown, sepals 0.8-1.1 cm long; petals mauve-pink to purple, 0.9-1.3 cm long. Ovule number unknown. Size of mature fruit unknown.

This subspecies is also a myrmecophyte; all trees possess swollen hollow internodes occupied by ants. As mentioned above, L. africana subsp. rumpiensis shares a number of traits with subsp. letouzeyi that distinguish these two from subsp. africana . It is distinguished from subsp. letouzeyi by its usually 2-jugate leaves ( Fig. 9 ), the smaller size of its leaflets and stems, the constancy in nectary number, and its restriction to piedmont and submontane forest (above 500 m and probably more commonly above 800 m).

DISTRIBUTION. — This taxon occurs in the Rumpi Hills ( Figs. 3 , 4 ), where it was studied in 5 field sites. Herbarium specimens from three other sites in the Rumpi Hills (see below) also appear to belong here. Material of myrmecophytic L. africana collected from submontane forest on another hill in the Southwest Province (Letouzey 13632 [K, P, YA], from a 960 m hill 55 km southwest of Mamfe) is tentatively placed in this subspecies.

ECOLOGY. — This myrmecophyte, in contrast to the two preceding subspecies, is restricted to submontane forest (and lowland forest transitional to it: “piedmont” [ THOMAS 1995]). As in the other myrmecophytes, internodes are hollowed and occupied by ants, and each adult tree is occupied by a single ant colony. In contrast to the two preceding subspecies, each of which is principally associated with one (or two) ant species, a diverse array of ant species occupy trees in populations of the subspecies rumpiensis (D. MCKEY and R. SNELLING, unpubl. results). Nature of the interactions with ants has not been studied in this subspecies. This subspecies was termed “ L. africana taxon T2” by CHENUIL & MCKEY (1996).

PARATYPES. — CAMEROON, Southwest Province : Steep hillside, 400-850 m, 5 km W of Esukutang Village, D. W . Thomas et al. 7988 ( MO); forest, 500 m, near Masaka- Batanga, D. W . Thomas & Namata 7746 ( MO); forest, 500 m, near Meta village , Nemba et al. 753 ( MO); colline, 960 m (près côte 897) E of piste Abakpa-Mbiofong , 55km SW Mamfe, Letouzey 13632 ( K, P, YA) .

Figures

Fig. 5. — Foliar nectaries of the Leonardoxa africana complex, all shown at the same scale: A, L. africana subsp. gracilicaulis (Zingui hill site); B, L. africana subsp. rumpiensis (Dikomé Balué site); C, L. africana subsp. africana (Akanga site). Nectaries of L. africana subsp. letouzeyi (not pictured) are similar in size to those of subsp. rumpiensis.

Fig. 6. — Internodes of the Leonardoxa africana complex, showing variation in specialisations for housing ants. Bar = 2 cm in all photos. A, apex of internode (note point of attachment of the paripinnately compound leaf) of L. africana subsp. gracilicaulis (Mbalmayo site), showing absence of swelling in this non-myrmecophytic subspecies; B, longitudinal section of internode of L. africana subsp. africana (Bombé Bakundu site) showing the strongly swollen ant-domatium, which in this subspecies is a single internode long.— C and D, prostoma of two myrmecophytic subspecies, located in both cases at the apex of the internode opposite the point of leaf insertion; the diagonally cut structure at the top of each photo is the leaf rachis: C, circular prostoma of L. africana subsp. letouzeyi (Rengo Rock site); prostoma of L. africana subsp. rumpiensis (not shown) is roughly similar in size and shape; D, elongate prostoma of L. africana subsp. africana (Bombé Bakundu site). Both are on internodes produced by plants growing in a greenhouse at the University of Miami, on cuttings uninhabited by ants. The structures are not holes, but are scars produced by the spontaneous drying of the unlignified prostoma in mature internodes.

Fig. 7. — Examples of variation in the unit of growth within the Leonardoxa africana complex. A, a branch tip of L. africana subsp. rumpiensis (Dikome Balue site) showing two recently matured internodes and leaves produced in a flush of growth; these leaves are bright green (shiny in this photograph) and distinct from the older mature leaf (dark green, not shiny) produced in a previous growth flush; arrow marks the base of this flush. Bar = 10 cm. B, a branch tip of L. africana subsp. africana (Bombe Bakundu site) showing the one-leaf and internode unit of growth typical of all populations of this subspecies. Bar = 2 cm.

Fig. 8. — Variation in floral traits within the Leonardoxa africana complex. Bar = 2 cm in both photos. A, inflorescence axillary on a young twig (vertical object just behind the inflorescence) in L. africana subsp. gracilicaulis (Mbalmayo site); hypanthium white, corolla and filaments of stamens lilac, anthers yellow. B, trunciflorous inflorescences in L. africana subsp. africana (Grand Zambi); hypanthium and corolla pink.

Fig. 3. — Geographic distribution of field localities of members of the Leonardoxa africana complex: L. africana subsp. gracilicaulis = Group 1; L. africana subsp. rumpiensis = Group 2; L. africana subsp. letouzeyi = Group 3; L. africana subsp. africana = Group 4.

Fig. 4. — Geographic distribution of herbarium collections of the Leonardoxa africana complex examined in this study: L. africana subsp. gracilicaulis = Group 1; L. africana subsp. rumpiensis = Group 2; L. africana subsp. letouzeyi = Group 3; L. africana subsp. africana = Group 4.

Fig. 2. — Representation of the contribution of different characters to the first three dimensions of the principal components analysis of field populations of the Leonardoxa africana complex.

Fig. 9. — Typical leaves of the Leonardoxa africana complex, all drawn at same scale. Bar = 10 cm. A, L. africana subsp. gracilicaulis; B, L. africana subsp. rumpiensis; C, L. africana subsp. letouzeyi; D, L. africana subsp. africana.