A taxonomic survey of Guatteria section Mecocarpus including the genera Guatteriopsis and Guatteriella p . p . ( Annonaceae )

This paper deals with a group of species of the Neotropical genus Guatteria (Annonaceae) which are characterized by leaves with tiny warts (verruculae) on both surfaces and by elongate and short-stipitate monocarps (i.e., the length of the monocarp body surpassing the length of the stipe). These species were placed by Fries in Guatteria sect. Mecocarpus (Fries 1939) (the name derives from Ancient Greek µ???? = Poppy and ?a?p?? = fruit: fruit resembling that of Papaver species). All occur in South America, none having been found elsewhere so far. Although there is much doubt nowadays about the taxonomic significance of Fries's sections, we maintain sect. Mecocarpus at present for convenience's sake. Additionally, the former genus Guatteriopsis, united with Guatteria a short time ago (Erkens & Maas 2008b), is now also included in sect. Mecocarpus. The same applies to one of the two species attributed to Guatteriella (also merged with Guatteria by Erkens & Maas 2008b), namely Guatteriella tomentosa R.E.Fr. (not Guatteria tomentosa Rusby) which is put into synonymy with Guatteria trichocarpa Erkens & Maas. One new species is described, namely Guatteria griseifolia Maas & Westra. The two species complexes of G. guianensis and G. decurrens are now treated each as a single polymorphic species. The present study falls within the framework of a planned monograph of the whole genus Guatteria.

In 1939 Robert Fries published the last revision of the genus Guatteria as a whole, as part of his large-scale project 'Revision der Arten einiger Annonaceen-Gattungen' covering the period 1930 -1939 (followed in 1949 by a supplemental part on sect.Chasmantha).He divided the genus Guatteria into 30 sections, one of which was sect.Mecocarpus.That section was defined by him as having middle-sized to very large ('folia gigantea') leaves, which were characteristically 'verruculosapunctata', i.e. the surface of the leaves being covered with wart-like excrescences.Other features were the more or less distinct loops formed by the secondary veins in the lamina, thick petals and relatively large and mostly shortly stipitate monocarps.Fries distinguished 18 South American species in sect.Mecocarpus.
The first feature in his key to the species was the leaf size.On the base of that feature the section was divided by him into three groups: group 1 with middle-sized leaves less than 20 cm long and appressed sepals, and groups 2 and 3 with large to very large leaves, group 2 having appressed sepals, group 3 having reflexed sepals; some other features which were used by Fries in his key to the species were leaf shape and leaf base.
In his contribution to Die natürlichen Pflanzenfamilien (1959), Fries maintained the sect.Mecocarpus, recognizing the same species as in his 1939 treatment, but adding one more species, namely G. pastazae, described by him in 1947 (Fries 1947).
Molecular phylogenetic work on the genus Guatteria has been conducted by Erkens et al. (2007a, b).According to him (Erkens et al. 2007a) sect.Mecocarpus is a monophyletic group, also including 2 species of sect.Stenocarpus, namely G. inundata and G. riparia and G. megalophylla from the monospecific sect.Megalophyllum.Among morphological features characterizing sect.Stenocarpus are shortly stipitate and almost fusiform monocarps and leaves with often a distinct marginal vein, while the lack of verruculae on the leaves distinguishes sect.Stenocarpus from sect.Mecocarpus.(It is worth noting that sect.Stenocarpus is almost completely restricted to temporarily inundated forests.This is a rather exceptional habitat for Guatteria.)We cannot agree for the time being with Erkens's et al. (2007a) conclusion from his molecular studies that sections Mecocarpus s.l. and Stenocarpus should be united, as our morphological research shows considerable differences between both sections in leaves (texture, marginal vein, leaf base, presence or absence of verruculae), length of pedicels, length of stipes of monocarps, etc.Another point made by Erkens was that species of sect.Mecocarpus as described by Fries (1939) are easily recognizable and that monophyly of all its species was therefore to be expected.However, two accessions of Guat teria brevicuspis were found to form a separate clade (Erkens et al. 2007a, b).Though still poorly supported, these appeared more closely related to some species of Guatteriopsis (Guat teriopsis friesiana and G. kuhlmannii, now Guatteria friesiana and G. cryandra (Erkens & Maas 2008)) than to the remainder of sect.Mecocarpus (Erkens et al. 2007a).
In this study the species of the former genus Guatteriopsis are included (but with the exclusion of G. ramiflora -see Erkens & Maas 2008: 404).It should be noted that the species of Guatteriella, which was also merged with Guatteria (Erkens & Maas 2008), along with Guatteriopsis, share many features of Guatteria sect.Mecocarpus, notably the flowers on short pedicels and monocarps with short stipes, but G. campinensis lacks verruculae in the leaves.For that reason it is left out of this treatment.Erkens et al. (2007a) performed a molecular study on the genera Guatteriopsis and Guatteriella, studying Guatteriopsis blepharophylla, G. friesiana, G. hispida, G. kuhlmannii and Guatteriella tomentosa.According to them "the species of Guat teriopsis do not prove to be monophyletic, there are 3 lineages: 1. Guatteriopsis blepharophylla with G. hispida; 2. Guatteriopsis friesiana with G. kuhlmannii; and 3. G. ramiflora".In the same paper (Erkens et al. 2007a) it is concluded that all species of Guatteriopsis are nested within Guatteria and that generic status is unjustified.The merger was done, as mentioned above, in a subsequent paper (Erkens & Maas 2008).The present paper goes even further in bringing Guatteria brevicuspis under the synonymy of the type species of the former genus Guatteriop sis: Guatteria blepharophylla.As rightly stated by Erkens et al. (2007a), with only six out of 20 species of sect.Mecocarpus having been investigated, increased taxon sampling is needed to gain more insight in the phylogenetic relationships of the species of this almost monophyletic section.In Erkens's et al. (2007a, b) phylogenetic trees, there is one group with, among others, G. decurrens, G. multivenia (now put in the synonymy of G. guianensis), G. inundata, G. riparia (now put in the synonymy of G. inundata), G. excellens (now in the synonymy of G. guianensis), G. guianensis, G. cf.meliodora (now synonymous with G. decurrens, this paper, based on Maas 9231; unfortunately we were unable to retrace that collection when preparing the present text) and G. megalophylla.Several of these species fit very well in sect.Mecocarpus like G. decur rens, G. guianensis and G. meliodora.As already mentioned above G. inundata does, on morphological grounds, not belong here.The same holds true for G. megalophylla which shares the large leaves and the large and shortly stipitate monocarps with sect.Mecocarpus, but which totally lacks the verruculae on the leaves.
A note on the warts -Fig.1a -c As said in the introduction, Fries (1939) when describing Guat teria sect.Mecocarpus assigned great value to the presence of warty leaves ("feinwärzige Blätter").Warty (verruculose) leaves were found in all 18 species he described in this section.Fries did not explain the nature of these warts any further and it is only in some recent publications that some anatomical aspects possibly related to these structures have been dealt with.Van Setten & Koek-Noorman (1986) in their leafanatomical survey of Neotropical genera of Annonaceae observed sclereids occurring in the leaves of 50 % of the genera.They found three types of sclereids, namely brachysclereids (stone cells), osteosclereids (poorly branched sclereids with thick, multi-layered cell walls) and astrosclereids (branched to stellate sclereids, which are mostly longer and thinner than the osteosclereids and often connected with terminal veins).Among the genera investigated Guatteriella, Guatteriopsis and Guatteria were found to have osteosclereids as well as astrosclereids, with osteosclereids being dominant in Guatteriella and Guatteriop sis, while in Guatteria both types appeared to be common.It should be noted that these three (now united) genera include species with verruculose leaves and it is tempting to suspect a connection between warts and the presence of sclereids.Strong indications for this also come from two other genera with warty leaves, namely Pseudoxandra and Unonopsis.
In both genera Van Marle (2003, 2007) studied the leaf anatomy down to quite some detail.In Pseudoxandra Van Marle (2003) observed osteosclereids in most species, traversing the leaf blade from one side to the other and touching the epidermis both above and below.Shrinking could readily explain why warts are so well visible in dried leaves, but do not show in fresh or wetted leaves.In Unonopsis Van Marle (2007) could detect similar osteosclereids reaching from the adaxial to the abaxial side in part of the species.This further leads one to suspect the same type of sclereids to play a role in Guatteria, but anatomical proof for this has yet to be provided before a final conclusion can be drawn.
Habitat & Ecology -In non-inundated or inundated (restinga, tahuampa) forest, on clayey, rarely on sandy soil.At elevations of 0-800 m.Flowering and fruiting: throughout the year.
Vernacular names - Notes -Guatteria blepharophylla is recognizable by shortly pedicellate flowers (pedicels generally up to 10 mm long) and by petals which are densely covered with appressed, silvery hairs.
Characteristically, G. blepharophylla has long-attenuate, densely to rather densely verruculose leaves.It occurs in Brazil (Amazonas, Mato Grosso, Pará, Rondônia and Roraima) and Venezuela (Amazonas and Bolívar).In Ecuador and Peru the leaves tend to have a shortly attenuate, acute, or even obtuse base.Specimens from Jenaro Herrera, Loreto, Peru are very variable in leaf shape, particularly the leaf base which shows the whole variation range between long-attenuate and obtuse.brown below, glabrous above, sparsely covered with appressed hairs below, the primary vein rather densely so, base obtuse to rounded, apex acuminate (acumen 15 -25 mm long), primary vein flat to slightly raised above, secondary veins indistinct, 17-25 on either side of primary vein, slightly raised above, not or indistinctly loop-forming, smallest distance between loops and margin 1-4 mm.Flowers in 1-2-flowered inflorescences in axils of leaves or on leafless branchlets; pedicels 1-5 mm long, 1-2 mm diam, fruiting pedicels up to 5 mm long and 3 mm diam, densely covered with appressed, brown hairs, articulated at c. 0.2 from the base, number of bracts not countable with certainty, one bract seen: broadly ovate-triangular, outer side densely covered with appressed, brown hairs; flower buds broadly ovoid; sepals basally connate, broadly ovate-triangular, 5-6 by 5 -6 mm, appressed, outer side densely covered with appressed hairs; petals yellow to golden yellow in vivo, ovate, 10 -15 by 8 -10 mm, outer side densely covered with appressed, brown hairs; stamens c. 2 mm long, connective shield not seen.Monocarps 10 -30, red to red-orange when ripe in vivo, blackish in sicco, ellipsoid, young ones 10-12 by 5-6 mm, sparsely covered with appressed hairs, apex apiculate (apiculum 0.5 -1 mm long), wall not measurable, stipes 1-3 by 1 mm.Seed not seen.Distribution -Brazil (Amapá, Pará).
Habitat & Ecology -In non-inundated forest, one specimen growing along river, often on clayey soil.At elevations of up to 250 m.Flowering: March, June, November; fruiting: August, September.
Habitat & Ecology -In non-inundated forest (from lowland rainforest to premontane forest), sometimes in periodically inundated forest.At elevations of 150 -2200 m.Flowering: throughout the year; fruiting: May to November.
Vernacular names -Bolivia: Piraquina, Oyshobo (Yuracare) (Thomas & Agustin 2024).Peru: Atzmiriqui.Note -Guatteria duodecima can at first glance be distinguished by relatively narrow and verruculose leaves which are usually narrowed both toward the base and toward the apex and also are densely to rather densely covered with appressed, almost silvery hairs on the lower side.Other distinctive features of this species are found in the shortly pedicellate flowers and monocarps which are always longer than the stipes.Tree or shrub 2.5-30 m tall, 5-50 cm diam; young twigs densely covered with appressed to half-appressed hairs 1-2 mm long, soon glabrous.Leaves: petiole 5-10 mm long, 3-4 mm diam; lamina elliptic to obovate or narrowly so, 12-28 by 5-12 cm (leaf index 1.6-4), coriaceous, densely and coarsely verruculose (the verruculae often tending to form strings), dull above, brown on both sides, glabrous above, rather densely to sparsely covered with appressed to half-appressed hairs 1-2 mm long below, base acute and often slightly attenuate, apex shortly acuminate (acumen 5-10 mm long), primary vein impressed above, secondary veins distinct, 12-18 on either side of primary vein, flat to slightly impressed above, smallest Distribution -Colombia (Amazonas), Venezuela (Amazonas), Peru (Loreto), Bolivia (Beni) and Brazil (Amazonas, Mato Grosso).
Habitat & Ecology -In periodically inundated or sometimes in non-inundated forest or in scrub savanna, often on clayey soil.At elevations of up to 175 m.Flowering: January, February, June, August to November; fruiting: March, April.
Notes -Guatteria dura is easily recognizable by densely and coarsely verruculose leaves, in which the large verrucae often form strings of 2 or 3.
Guatteria dura resembles G. meliodora in many aspects, among others by the thick leaves which completely lack the marginal vein so often found in this section; G. dura differs, however, by the densely verruculose lamina, the warts often forming strings of 2 or 3, vs the sparsely verruculose lamina with warts never forming strings in G. meliodora.The distinction between both species requires further study.
There is quite some variation in petal size and shape in G.Note -Guatteria friesiana can be recognized by its leaves with a cordate base, obscure secondary veins, a velutinous indument on young twigs and shortly pedicellate flowers.Habitat & Ecology -In non-inundated forest (cloud forest with abundant epiphytes, "bosque perennifolia", forest on limestone derived soil, locally with thick humus layer).At elevations of 900-2400 m.Flowering: January, July, November, December; fruiting: March, June, October to December.

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Habitat & Ecology -In non-inundated, often caatinga forest, on sandy soil.At elevations of up to 270 m.Flowering: March, April, July, October; fruiting: January, February, April, October, November.
Note -Guatteria insculpta can be recognized by very densely and minutely verruculose leaves and by young twigs covered with a velutinous indument of erect red-brown hairs.Furthermore, this species stands out by the dense cover of erect brown hairs on the lower side of the leaves.Small tree c. 6.5 m tall, diam not recorded; twigs (no growth tip seen) glabrous.Leaves: petiole c. 10 mm long, 3-4 mm diam; lamina narrowly elliptic-ovate, 16-27 by 5-8.5 cm (leaf index 3-4), chartaceous to thinly coriaceous, rugulose above, not or sparsely verruculose along primary vein only, slightly shiny and brownish green above, dull brownish green below, glabrous on both sides, base shortly attenuate, apex acuminate (acumen c. 10 mm long), primary vein flat above, secondary veins indistinct, 15-18 on either side of primary vein, raised above, smallest distance between loops and margin 1-2 mm.Vernacular names -None.
Habitat & Ecology -In non-inundated or periodically inundated forest (várzea, igapó), on clayey soil.At elevations of up to 300 m.Flowering: April, May, July, August, October; fruiting: June to February.
Habitat & Ecology -In non-inundated (terra firme) forest, sometimes campinarana forest or campina forest, on sandy soil.The collection from Guyana (Clarke et al. 7132) is found in seasonally flooded forest on grey sand with Eperua, Clusia and Oenocarpus.At elevations of 125-240 m.Flowering: March, May, June, August, September; fruiting: August, December.
Notes -The label of the type collection of G. meliodora mentions that the yellow flowers have a strong odour resembling honey (hence the specific name).
Guatteria meliodora is well distinct from other species of sect.Mecocarpus by its thick, sparsely verruculose and often shortly acuminate and shiny leaves.It is noteworthy that the primary vein is keeled below in part of the material.For differences with G. dura see under the latter.
Pereira INPA/WWF 2303.6161(U) from Brazil, Amazonas, Fazenda Dimona, 90 km N of Manaus, may belong here, but this sterile collection is aberrant in having a strongly attenuate leaf base.
15. Guatteria novogranatensis R.E.Fr.-Fig.18; Map 3 Note -Guatteria novogranatensis was collected from a very large tree 30 m tall and with a diameter of 1.2 m!It looks quite similar to the Amazonian species G. longicuspis, both being cauliflorous and sharing most leaf characters.G. novograna tensis differs by a dense indument on large leaf veins below (vs mostly sparsely so) and by larger sepals (10 -13 mm long vs 5-7 mm long).It should not be ruled out that future research will prove the two taxa to be conspecific.
Habitat & Ecology -In premontane and montane forest, rarely in lowland rainforest, on soils derived from sandstone substrate or on red clay.At elevations of 0-1800 (-2200)  Notes -Guatteria pastazae can be recognized by having verruculose leaves with obscure venation and by an attenuate leaf base, combined with shortly pedicellate flowers and shortly stipitate monocarps.
Guatteria pastazae shows some features of G. modesta Diels but it differs by its much shorter stipes (stipes shorter than to almost equalling monocarp length) vs stipes longer than monocarp.
Habitat & Ecology -In non-inundated forest and along river banks.At elevations of 125-580 m.Flowering: August; fruiting: September.
Vernacular names -None.Note -Guatteria peruviana is united here with G. macro carpa, since the features given by Fries (number of secondary veins and leaf base) are highly variable in the genus Guatteria and can therefore hardly be used for specific distinction.
Habitat & Ecology -In non-inundated forest, on clayey to sandy soil.At elevations of up to 300 m.Flowering: July, November; fruiting: January.
Vernacular names -Colombia: Buruchicu (Muinane) (Van Andel et al. 161), Carguero (Muinane), Duj+ku (Uitoto), J+d+ra (Uitoto) (Cárdenas et al. 4064), Ñaajeku (Muinane) (Murillo A. et al. 510).Notes -This as yet undescribed species looks similar to G. hispida as to the leaf shape and the dense indument of stiff, erect hairs.It differs from the latter by the presence of a distinct marginal leaf vein, while in G. hispida the leaves do not show a marginal vein.There is scanty flowering material, only representing flowers in young stage.Murillo A. & Restrepo described fruiting material as well, but we did not see that.Altogether, it seems wisest at the moment not to formally publish a new species.Murillo A. & Restrepo (2000) attribute the collection Stein et al. 4002 (MO, U) from Loreto, Peru, to this as yet undescribed species as well.Actually, it is the type collection of G. grandipes.
Maas et al. 8186 (U)from Peru the ripe fruit has a sweet, edible pulp.