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Morphology, germination, and geographic distribution of

Pentaclethra macroloba (Fabaceae): a hyperdominant Amazonian tree

Adelson Rocha Dantas

*, Marcelino Carneiro Guedes

, Caroline da Cruz Vasconcelos

Jaynna Gonar Lôbo Isacksson

, Dayane Nathália Barbosa Pastana

, Ana Cláudia Lira-Guedes

& Maria Teresa Fernandez Piedade

1. Programa de Pós-graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brasil;

adelson.dantas@yahoo.com.br, maua.manaus@gmail.com

2. Departamento de Recursos Florestais, Empresa Brasileira de Pesquisa Agropecuária, Macapá, Brasil;

marcelino.guedes@embrapa.br, ana-lira.guedes@embrapa.br

3. Programa de Pós-graduação em Botânica, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brasil;

cc_vasconcelos@hotmail.com

4. Grupo de Pesquisa em Ecologia Florestal, Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Brasil;

jaynnagonar@hotmail.com

5. Programa de Pós-graduação em Engenharia Florestal, Universidade Federal de Lavras, Lavras, Brasil;

dayanepastana@gmail.com

* Correspondence

Received 10-VIII-2020. Corrected 04-XI-2020. Accepted 13-XI-2020.

ABSTRACT. Introduction: Pentaclethra macroloba is a hyperdominant tree in the Amazon estuary of

great socioeconomic importance for the region because the oil from its seeds is a powerful herbal medicine.

Objective: We aimed to characterize the morphological structure, the morphological adaptations in response

to the daily flooding of the Amazon estuary and the biogeographic area of P. macroloba. Methods: Detailed

description of the external morphology, from germination to the adult tree, was obtained from individuals

located in floodplain forest, Northeast Amazonia. The occupation area and the geographical extension of P.

macroloba were determined from point of geographical coordinates of botanical samples deposited in the digital

collections of Mobot and SpeciesLink. Results: Adult individuals have adapted structures in response to daily

flooding, such as: adventitious roots to increase respiratory efficiency and lenticels in the trunk, serving as a

connection point for oxygen transport between the root and the aerial part. Dried fruit favours the activation of

the explosive dehiscence mechanism, allowing the seed to be expelled long distance. Deltoid shape of the seed

allows water fluctuation and more efficient dispersal. Seedling is phanerocotylar hypogeal and with one pair of

reserve cotyledons that provide the seedling an extra source of energy to escape the flood. Germination rate was

78 % and the speed was 0.2 seeds.day

-1

. Circular buffer method revealed the presence of 123 subpopulations of

P. macroloba distributed in a radius of 5 699 943 km² across the Neotropical region. Conclusions: Much of the

morphological structures of P. macroloba are adaptive and evolutionary responses to the periodically flooded

environment of the Amazon estuary, showing that these environments select the trees, best adapted, to inhabit

the flood. P. macroloba has a wide geographical area denotes the plasticity of adapting to different environments,

which may justify its monodominance in some regions.

Key words: morphological adaptation; tidal flooding; Neotropical tree; adventitious roots; pracaxi oil; manage-

ment, conservation.

Rocha Dantas, A., Carneiro Guedes, M., da Cruz Vasconcelos, C., Lôbo Isacksson, J.G.,

Barbosa Pastana, D.N., Lira-Guedes, A.C., & Fernandez Piedade, M.T. (2021).

Morphology, germination, and geographic distribution of Pentaclethra macroloba

(Fabaceae): a hyperdominant Amazonian tree. Revista de Biología Tropical, 69(1),

181-196. DOI 10.15517/rbt.v69i1.43446

ISSN Printed: 0034-7744 ISSN digital: 2215-2075

DOI 10.15517/rbt.v69i1.43446

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Some tree species in the Amazon region

have great dominance, occurring in a wide

area, others have isolated populations and

their distribution is restricted to a specific

environment (ter Steege et al., 2013). The

great challenge for many forest ecologists is to

understand the mechanisms and strategies that

trees develop over time to colonize the most

varied environments in the Amazon rainforest.

In the Amazon floodplain, the periodically

flooded environment can promote speciation

and adaptation processes in the trees that

inhabit this environment. Various adaptations

in the external morphology of the plants are

observed in response to the low availability of

oxygen in the rhizosphere and the constant ero-

sion of the soil, such as high density of lenticels

in the trunk and the presence of roots and aerial

structures: rhizophores, pneumatophores, haus-

toria and buttresses (Almeida, Amaral, & Silva,

2004; Parolin, 2012).

In Central Amazonia, flooding in the for-

est can last up to 243 days and reach a height

of up to 6 m on the tree trunk (Schöngart,

Piedade, Ludwigshausen, Horna, & Worbes,

2002). Trees respond to this long period of

flooding reducing metabolic activity, which in

many cases leads to leaf fall in the canopy (De

Simone, Junk, & Schmidt, 2003) and formation

of annual rings on the trunk (Schöngart et al.,

2004). However, in the Eastern Amazon, the

knowledge of the morphological and ecophysi-

ological adaptations of tree species that grow

under the regime of daily flooding and low

amplitude of the Amazon estuary (Junk et al.,

2011) is still quite modest.

The floodplains of the Amazon estuary

have several endemic and dominant species as

Pentaclethra macroloba. Species of the Faba-

ceae family, popularly known by name “pra-

caxi” (Dantas, Marangon, Guedes, Feliciano, &

Lira-Guedes, 2017). This species is hyperdomi-

nant Amazon (Ter Steege et al., 2013) and large

occurrence in Amazon estuary (Carim, Wit-

tmann, Piedade, Guimarães, & Tostes, 2016).

Among the three populations of P. macroloba

in Neotropical America, little is known about

the natural history of the population that lives

in the Amazon Basin (Hartshorn, 1983).

P. macroloba is an important non-timber

species in the local socioeconomic, source of

income for several riverside Amazon, due to

its multiple uses. The bark of the tree trunk has

triterpenoid saponins that have anti-haemor-

rhagic action against the venom of snakes of

the Bothrops genus (Silva et al., 2007). The oil

extracted from the seeds is a powerful natural

medicine, which is very common riverside

Amazon people to use this oil to treat muscle

pain and inflammation. The oil has a high con-

centration of fatty acids that moisturize the skin

(Costa et al., 2014), which is highly requested

by the cosmetics industry as raw material.

Despite the great arboreal biodiversity of

the Amazon, information on the basic morphol-

ogy of plant species is still lacking, difficult

to understand the evolutionary adaptations of

trees to the environment. In addition, studies

of plant morphology are important to ensure

the correct identification of trees and natural

regeneration (Melo, Mendonça, & Mendes,

2004), indispensable requirement in biodiver-

sity inventory.

Dispersion patterns of the trees has great

contribution to the diversification of the Ama-

zon rainforest (Gentry, 1981). The biogeo-

graphic patterns of trees are the result, in many

cases, of limited dispersion (Wiens, 2011)

and reveal characteristics of its ecology and

evolutionary biology (Gaston & Fuller, 2009),

important knowledge for conservation strate-

gies of species that have economic potential,

such as P. macroloba.

In this study, we evaluated the morpho-

logical adaptations of P. macroloba in response

to the daily flooding of the Amazon estuary. We

provide a detailed description of the external

morphology of P. macroloba and evaluate its

biogeographic area to assist in the management

and conservation of this species.

MATERIALS AND METHODS

Study area: Botanical material was

collected from individuals located in two

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floodplain areas: Mazagão Experimental Field

(CEM) and Fazendinha Environmental Pro-

tection Area (APA da Fazendinha hereafter),

State of Amapá, Brazil. CEM belongs to the

Brazilian Agricultural Research Corporation,

located in the city of Mazagão (00°02’33” S

& 51°15’24” W), it has 55.95 ha of floodplain

forest and is bathed by the tributary of the

Amazon River called “furo do Mazagão”. The

APA da Fazendinha is located in the city of

Macapá (00º03’04.24” S & 51°07’42.72” W),

it has 13 659 ha of floodplain forest and is

directly bathed by the Amazon River.

The climatic system of the region is Am

(Köppen classification), tropical rainy (Alva-

res, Stape, Sentelhas, Gonçalves, & Sparovek,

2013), and in the state of Amapá, the rainy

season begins in December, with the concentra-

tion of rainfall in the month of March where the

peak of precipitation is above 60 mm until the

month of August. The dry season starts in Sep-

tember when the monthly rainfall is below 60

mm (Vilhena, Silva, & Freitas, 2018). The soils

of the area are classified as typical Melanic

Gleysols Ta Eutrophic, with predominance of

silt. Both the sediment and the soil are formed

by smectite, illite, kaolinite, goethite, anatase

and quartz (Pinto, 2014).

The vegetation is classified as dense

alluvial ombrophilous forest (IBGE, 2012),

with predominance of species Mora par-

aensis, Astrocaryum murumuru, P. macroloba,

Carapa guianensis and Virola surinamensis

(Carim et al., 2016).

Data collection: Morphological descrip-

tion of the 34 adult trees (30 trees in APA and

4 trees in CEM) occurred in the field, observ-

ing their characteristics from the trunk base

towards the top of the crown. After the descrip-

tion of the tree adults, fertile branches contain-

ing flowers, fruits and seeds were collected

with the help of a pruning stick of 10 m and

the usual tree climbing technique according to

Laman (1995).

Branches were stored in moistened poly-

ethylene bags and sent to the Embrapa Seed

Laboratory, where the structures were measured

and morphological description was conducted,

through a specialized form with botanical

terms. After the description, exsiccates were

prepared for deposit in the Embrapa Herbarium

Amazônia Oriental - IAN, Belém, Pará (regis-

tration numbers IAN192676 and IAN192677).

Morphological structures of the trunk,

branches, leaves, flowers, fruits, seeds and

seedlings were recorded using a Canon® cam-

era (Model EOS Rebel T2i). Small structures

were recorded using a Leica stereomicroscope

(model EZ4D) with fixed camera.

The morphological stages of fruit and seed

maturation were determined monitoring 30

individuals, during the period from April 2018

to March 2019 in the APA da Fazendinha. It

was possible to observe the development of the

first fruits, as well as to determine the matura-

tion time and the morphological changes that

occurred over time. The fruits that showed

any significant change in shape or colour in

the crown were collected, measured, and pho-

tographed. A chronological sequence of the

maturation of fruits and seeds was built.

For the morphometric analysis, 54 fruits

and 114 seeds were collected to obtain fresh

mass (g), length (mm), width (mm) and thick-

ness (mm). Fruits and seeds were weighed

on analytical balance (Shimadzu® model

AUW22OD, Japan), with accuracy of 0.001 g.

The measures of length, width and thickness

were measured with a digital caliper (Carbo-

grafite® model 150, accuracy of 0.01 mm).

To evaluate the germination process and

seedling phases, 60 seeds (4 replicates x 15

seeds) were sown in plastic trays (45 x 28 x 7.5

cm), containing sand as substrate sterilized at

100 °C and vermiculite of medium particle size

(1:1 ratio). The germination phases and seed-

ling formation were monitored every two days

in a greenhouse, for a period of six months.

The dispersal pattern of the species was

analysed through the geographical coordinates

of the botanical samples deposited in the

digital repositories of the Missouri Botani-

cal Garden (Tropicos, 2019) and SpeciesLink

(CRIA, 2019).

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Data analysis: All descriptions of the

morphological characteristics of P. macroloba

followed a standardized form in botanical

terms, based on botanical literature (Barroso,

Morim, Pioxoto, & Ichaso, 2004; Gonçalves &

Lorenzi, 2011; Harris & Harris, 2001). Mean ±

standard deviation and coefficient of variation

(CV) of the morphometric data were calcu-

lated. The morphometric relationships between

fruits and seeds were evaluated using simple

linear regression. The significance of the rela-

tionship was assessed by analysis of variance

at 0.05 % probability. The percentage of germi-

nated seeds, average germination time and the

germination speed were determined (Maguire,

1962). Germinated seed was considered when

the cotyledons open emitting the epicotyl and

the seedling phase begins with the expansion

of the first pair of leaves (Camargo, Ferraz,

Mesquita, Santos, & Brum, 2008).

Geographic dispersal map of the species

was prepared in the software QGIS 2.18. The

extent of occurrence (EOO), area of occupation

(AOO) and number of subpopulations (IUCN,

2017) of P. macroloba were determined using

the statistical package ConR (Dauby, 2019).

The number of subpopulations was estimated

using the circular buffer method (Rivers, Bach-

man, Meagher, Lughadha, & Brummitt, 2010).

All statistical analysis were performed using

the R program (R core Team, 2019).

RESULTS

Description of adult trees in the field: P.

macroloba (Fig. 1A) has an average height of

13 m (maximum 37 m) and 26 cm of diameter

(maximum 59 cm). The base of the trunk (Fig.

1F) can be channelled or in buttresses, with

the tree stem (Fig. 1B) straight or inclined and

cylindrical shape. Rhytidome (outer bark) has

a rough texture and with a mixture of green

and grey colors (presence of lichen stains,

Fig. 1D), with abundant elliptical and blackish

green lenticels (Fig. 1C). The phloem (inner

bark) is reddish and the sapwood is yellow-

ish (Fig. 1E). The tree does not show exudate

when the rhytidome is injured However, one

day after, the tree exudes a colourless and vis-

cous liquid (Fig. 1I). During the flood period

of the Amazon estuary, P. macroloba produces

a large number of adventitious roots (Fig. 1H).

Individuals often show spread of branches at

the base of the trunk (Fig. 1G).

The leaves (21.3 ± 4.7 cm) are bipinnate

(Fig. 2A), paripinnate, with alternate spiral

phyllotaxy (Fig. 2C) and have 6-15 pairs of

leaflets (8.6 ± 2.8 cm). When new, the leaves

Fig. 1. Morphological characteristics of adult individuals of Pentaclethra macroloba in the Amazon estuary: A. Pentaclethra

macroloba tree, B. Straight trunk, C. Protuberant lenticels on the trunk, D. Moss and lichen stain, E. Red phloem and

yellow sapwood, F. Base of the trunk, G. Spread of branches at the base of the trunk, H. Adventitious roots and I. Exudate

on the trunk.

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have a light red colour (Fig. 2B) and when

ripe, they have a dark green colour (Fig. 2A).

The leaflets (8.6 ± 2.8 cm) are opposite or sub-

opposite, containing 28-45 pairs of pinnules.

The pinnules (11.7 ± 0.6 mm) are opposite,

oblong or linear, with an obtuse/asymmetric

base; acute apex, mucronate and with the entire

blade margin. The pinnules are coriaceous, dark

green on the adaxial side, light green abaxial

and glabrous on both sides. The petiole (32.6 ±

10.6 mm) varies from yellowish green to black-

ish brown, smooth to slightly rough, channelled

and covered by abundant trichomes (Fig. 2D).

The pulvinus (7.5 ± 1.4 mm) varies from dark

green to black, rough and with trichomes. The

rachis (16.6 ± 5.8 cm) varies from yellowish

green to blackish brown colour, channelled and

with trichomes similar to the petiole. The pul-

vinule (1.7 ± 0.3 mm) is rough and varies from

yellowish green to blackish brown colour. The

rachilla has yellowish green or blackish brown

colour, smooth and with brownish trichomes.

Presence of a pair of linear stipules (Fig. 2E) at

the base of the pulvinus.

The inflorescence (17.1 ± 3.9 cm) is a ter-

minal spike of white colour, due to the presence

of numerous whitish staminodes (Fig. 3A). A

spike can have up to 411 flowers. The floral

Fig. 2. Morphological characteristics of the Pentaclethra macroloba leaf in the Amazon estuary: A. Ripe leaf, A. New leaf,

C. Alternate spiral phyllotaxy, D. Petiole channeled with trichomes and E. Pulvinus base stipule.

Fig. 3. Morphological characteristics of the Pentaclethra macroloba inflorescence in the Amazon estuary: A. Inflorescences

in the phase of floral bud and anthesis, A. Immature flower buds, C. Pentamer flower with their guiding lines [gl] of

pollinators, D. Gomosepalous calyx and E. Gland [g] in the anther.

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bud (4 ± 1.1 mm) is initially light green when

immature (Fig. 3B), becoming light green to

light brown with maturation. The flower (7.2 ±

1.3 mm) is pentamer (Fig. 3C), calyx gamose-

palous (Fig. 3D) and presenting up to 10 stami-

nodes. The stamen has a gland at the tip of the

anther (Fig. 3E). The petals have floral nectar

guide that direct the pollinator into the flower

(Fig. 3C).

Morphometry and characterization of

fruits and seeds: The fruit has an average

length of 33.7 cm (± 3.3 cm) and weight of

105.1 g (± 32.3 g) (Table 1). The average

number of seeds per fruit was four seeds (± 1

seed) (Table 1). Fruit length (mm) had a posi-

tive linear relationship between the measures of

fresh weight (F = 5.11; p = 0.031*; R² = 0.14;

Fig. 4A), length (F = 17.48; p = 0.0002***; R²

= 0.37; Fig. 4B), width (F = 59.2; p = 0.023*;

R² = 0.16; Fig. 4C) and thickness (F = 9.11; p =

0.005**; R² = 0.23; Fig. 4D) of the seeds.

The seed has an average length of 4.4 cm

(± 0.48 cm) and weight of 6.8 g (± 2.2 g) (Table

1). Fresh mass (g) of seeds has a positive lin-

ear relationship with its measures of length (F

= 116.23; p < 0.001***; R² = 0.67; Fig. 4E),

width (F = 53.01; p < 0.001***; R² = 0.48; Fig.

4F) and thickness (F = 56.48; p < 0.001***; R²

= 0.50; Fig. 4G).

The fruit is of the dry legume type (Fig.

5A), dehiscent, with 4-6 valves, light green

(immature) to dark brown (ripe), laterally flat-

tened and falcate, with an acute apex and with

cuneate or attenuate base. The ventral suture is

slightly flat. The pericarp is woody; externally

corrugated, glabrous, rare punctiform or ellipti-

cal lenticels; internally reddish brown, slightly

striate, glabrous and with diagonal cracks due

to the natural twist for opening and releasing

the seeds.

The seed is deltoid, rhomboid or obovoid

(Fig. 5B), with flat and irregular surface, dark

brown, opaque, striate and with thin grooves.

The coat (< 1 mm) varies from light brown to

dark brown and opaque. Cotyledons are fleshy,

light yellow to whitish colour and with chan-

nels that exude oil of rapid oxidation when

exposed to air. The seed embryo has a straight

embryonic axis, with well-developed plumule

and radicle (Fig. 5C). The seeds have an air

pocket between the cotyledons, which allows

floating in water (Fig. 5D).

The average time of the fruit and seed

maturation was 5 months (± 3 months) and 3

months (± 2 months), respectively. We recorded

the formation of up to five fruits per inflores-

cence. First fruit arise from the 22nd day after

flower fertilization (Fig. 6A). At this stage, it

is still possible to observe the persistence of

TABLE 1

Morphometric values of the measured variables in fruits (N = 22) and seeds

(N = 60) of Pentaclethra macroloba in the Amazon estuary

Average Standard deviation *CV % Minimum Maximum

Fruit

Fresh weight (g) 105.1 32.3 30.7 50.5 201.7

Length (cm) 33.7 3.3 9.9 22.4 40.8

Width (cm) 4.2 0.35 8.1 3.6 4.9

Thickness (mm) 1.4 0.25 17.1 0.99 1.8

Number of seeds 4.3 1.1 26.0 2 7

Seed

Fresh weight (g) 6.8 2.2 33.0 2.1 12.1

Length (mm) 4.4 0.5 10.8 3.3 5.7

Width (mm) 3.1 0.5 16.2 1.8 4.9

Thickness (mm) 1 0.16 16.3 0.6 1.3

*CV = coefficient of variation.

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the calyx and corolla. On the 32nd day, the

perianth disappears, the fruit gains length and

falcate shape, presenting light red colour in

the centre and pale green colour at the edges.

(Fig. 6B). On the 53rd day, the fruit has a pale

green colour, membranaceous consistency and

the first light green seed appears (Fig. 6C). On

the 78th day, the fruit has a light green colour,

with slightly blackened edges, slightly woody

consistency and with protuberances (valves)

on the surface, due to the development and

expansion of the light beige seeds (Fig. 6D).

Fig. 4. Morphometric relationships of fruits and seeds

of Pentaclethra macroloba in the Amazon estuary.

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On the 110th day, the fruit has a dark green

colour, with blackening from the border to the

centre, woody consistency and the seed has

beige colour with light brown tones (Fig. 6E).

On the 144th day, the fruit has brown colour,

with some parts still green, woody consistency

and slightly dry and the seed has light brown

colour (Fig. 6F). On the 198th day, the fruit is

ripe, ready to disperse the ripe seeds (Fig. 6G).

Germination and initial seedling devel-

opment: The first seeds germinated on the

28th day (44 ± 27 days) after sowing and the

seedling phase on the 51st after sowing and

germination. Germination is hypogeal, pha-

nerocotylar and unipolar, with an axis between

the cotyledons. During germination, the seed

coat breaks, and the primary root emerges (Fig.

7A). The cotyledons open forming an acute to

right angle, with the epicotyl appearing (Fig.

7B). The epicotyl lengthens and the first pair

of leaves appearing (opposite or sub-opposite;

Fig. 7C), which soon produces the subsequent

leaves (Fig. 7D, Fig. 7E). Germination rate

Fig. 5. Morphological characteristics of fruits and seeds of Pentaclethra macroloba in the Amazon estuary: A. Immature

fruits, B. Ripe fruit with its valves, C. Ripe seeds, D. Seed embryo and E. Seeds floating in the water of the Amazon river.

Fig. 6. Maturation phases of fruits and seeds of Pentaclethra macroloba in the Amazon estuary. Evolution of shape, size

and colour: phase A. 22nd day after flower fertilization; phase B. 32nd day; phase C. 53rd day; phase D. 78th day; phase E.

110th day; phase F. 144th day; and phase G. 198th day of maturation.

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was 78 %, with average germination time of 54

days and the average germination speed was

0.2 seeds.day

-1

Seedling morphology: Seedling (Fig. 7D)

has hypocotyl not elongate; cotyledons with

reserves, asymmetrical, internally dark green

and externally brownish green, with longitu-

dinal grooves becoming rough over time. The

epicotyl (17.7 ± 3.7 cm) is initially green-

ish, becoming violet to brownish, smooth to

slightly rough, striate longitudinally, with yel-

low translucent trichomes and with abundant

circular and punctate lenticels. Presence of

11-13 triangular cataphylls (1.7 ± 0.6 mm)

along the epicotyl.

First pair of leaves (15.7 ± 4.4 cm) are

bipinnate, opposite, sub-opposite or alternate,

often paripinnate and rarely imparipinnate and

with 6-12 opposite leaflets. The pinnules (9.2

± 0.4 mm) are sessile, oblong, papyraceous,

with obtuse and asymmetric base, acute and

mucronate apex and margin of the entire and

ciliate blade (yellowish trichomes). The peti-

ole (3.8 ± 1.2 cm) is brownish green, with

trichomes, smooth or rough, with wing and flat

or channelled. Discolour leaf blade, with dark

green adaxial face and light green abaxial face.

The rachis (6.6 ± 2.4 cm) is brownish-green,

smooth to rough, apiculate and with trichomes

similar to the petiole, but more abundant. The

pulvinus (3.3 ± 0.8 mm) is dark green, rough,

with trichomes equal to that of the petiole and

with transverse fissures. Presence of a pair of

stipules at the base of the pulvinus (Fig. 8B).

Glands or extrafloral nectary at the base of the

pulvinus (Fig. 8C). The petiole is reduced to

pulvinule (0.6 ± 0.2 mm).

Subsequent leaves (10.4 ± 1.7 cm) are

equal to the first leaves, but smaller in size,

with alternate spiral phyllotaxy (Fig. 8A) and

have 9 to 16 leaflets. The pinnules (7.4 ± 2.1

mm) is equal to the first leaves, but larger.

The petiole (3.8 ± 1.2 cm) is equal to the first

leaves, but smaller. The rachis (6.6 ± 2.3 cm) is

equal to the first leaves. The pulvinus (3.2 ± 0.8

mm) is equal to the first leaves. The petiolule

is reduced to pulvinule. The pulvinule (0.6 ±

0.2 mm) is equal to the first leaves. Condupli-

cate prefoliation, from violet to reddish-brown

colour and with translucent trichomes. The

internodes have lenticels similar to the epi-

cotyl, but more abundant.

Geographic distribution: We analysed

210 points of geographical coordinates of

digital botanical collections. The centre of

occurrence of P. macroloba was throughout

Latin America, showing that it is a neotropical

species (Fig. 9). Data from digital repositories

Fig. 7. Phases of seedling development of Pentaclethra macroloba in the Amazon estuary: phase A. Primary root (pr)

formation; phase B. Opening of the cotyledons (cot) and formation of secondary roots (sr); phase C. Expansion of the

epicotyl (epi); phase D. Development of the first leaves (prot) and formation of cataphyll (cat) in the epicotyl; and phase E.

Ripe leaflets (fo) and apical bud (ag).

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show the presence of P. macroloba in Guate-

mala, Costa Rica, Panama, Colombia, Ven-

ezuela, Trinidad and Tobago, Guyana, French

Guyana Suriname, and Brazil. In Brazil, the

species is endemic to the Amazon biome and

its dispersion area comprises the states of Acre,

Amazonas, Roraima, North Mato Grosso,

Amapá and Pará.

The species has 123 subpopulations

(Fig. 9) distributed on a radius of 5 699 943

km² along its extent of occurrence. The area of

occupation of a species represents its suitable

habitat, for P. macroloba is 9 990 km².

DISCUSSION

The individuals described in this study

appear to be medium size compared to indi-

viduals of P. macroloba from Central America,

where populations are more robust (Hartshorn,

1983). In Costa Rica, adult individuals occupy

the canopy of the forest, reaching a height

of 25 to 35 m and with diameter reaching up

to 130 cm (Flores, 2003). In South America,

in the forests of the department of Chocó

(Colombia), the majority of individuals occupy

the sub-canopy forest, with a maximum diam-

eter of 65 cm (Hartshorn, 1983). In general,

the population of P. macroloba located in the

Amazon forest is of medium height (Harts-

horn, 1983), as presented the individuals in this

study with a maximum diameter of 59 cm. This

shows evidence that individuals in the Amazon

estuary invest more resources to gain height,

as the maximum height (37 m) found was

greater than other studies. According to Paro-

lin (2002), the trees of the Amazon floodplain

forests need to increase the maximum height to

escape the flood.

External morphological structures shown

by P. macroloba, evidence an adaptive relation-

ship to the periodically flooded environment of

the Amazon estuary. In response to flooding,

adventitious roots are produced during the

flood season in the Amazon river (from Janu-

ary to March influenced by the rainy season),

Fig. 8. Morphological characteristics of Pentaclethra macroloba seedling in the Amazon estuary: A. Phyllotaxy of the

subsequent leaves, B. Stipule at the base of the pulvinus and C. Gland at the lateral base of the pulvinus.

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decreasing in the dry season (from September

to December). This characteristic presented by

P. macroloba is a morphological adaptation to

the periodically flooded environment, because

the adventitious roots increase the energetic

and respiratory efficiency of the plant (Haase,

Simone, & Junk, 2003) when the rhizosphere

has low oxygen concentration. Individuals of

P. macroloba from some regions of Costa Rica

also have adventitious roots in flooded environ-

ments (Walter & Bien, 1989).

Reproductive strategies can also be

observed in P. macroloba. A characteristic that

calls attention in P. macroloba is the spread of

several branches at the base of its trunk (Fig.

1G). According to Gaddis, Zukin, Dieterich,

Braker, and Sork (2014), P. macroloba has a

high power of vegetative propagation (clonal

reproduction), even if the tree is down, there

are numerous sprouts of branches on the trunk

and roots. This strategy is efficient in peri-

odically flooded environments, because a faster

increase in height prevents the plant from being

submerged and has its productivity limited by

the flood (Parolin, 2002).

The species has nectar guides on its pet-

als to increase pollen efficiency. Nectar guides

are floral traits that some superior plants have

Fig. 9. Dispersion area (above) and number of subpopulations (below) of Pentaclethra macroloba in the Neotropical region

(Data source: tropicos.org and splink.cria.org.br).

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to attract the attention of effective pollinators

(Leonard, Brent, Papaj, & Dornhaus, 2013).

The nectar guide on the P. macroloba petal

attracts and directs pollinators into the corolla,

where is the nectar gland at the base of the

ovary (Barros, Pedersoli, Paulino, & Teixeira,

2017), increasing the chances of fertilization

of the ovule.

Morphological characteristics presented in

the fruits and seeds of P. macroloba are adaptive

evidence in search of greater efficiency in the

seed dispersal. The low moisture content that

the fruit has when ripe (dry fruit), favours the

activation of the explosive dehiscence mecha-

nism (the ventral suture and the valves) for

the seeds to be expelled (Williamson & Costa,

2000) at a distance of up to 10 m out of the

tree canopy (Hartshorn, 1983). The flattened

shape (deltoid), together with the accumulation

of air between the cotyledons (Soares, Santos,

& Silva, 2019) and the specific gravity of the

seed (Williamson & Costa, 2000), allows the

seed to float in the water of the Amazon estu-

ary, achieving greater efficiency in dispersion.

Positive linear relationship between the

length of the fruit and the measures of weight,

length and thickness of the seeds, give clue that

P. macroloba invests in resources to produce

seeds with high energy content. This strategy

allows the seedlings to survive the adverse

conditions of the flooded environment. Accord-

ing to Primack (1987), bulky seeds have high

reserve content in their cotyledons, allowing

the seedling to obtain an extra energy source

for a long period.

This study showed that the size of the

fruit is a good predictor for selecting seeds

with higher fresh weight, this characteristic is

important for the management of oil extrac-

tion from Pracaxi. The experience of riverine

people in oil extraction shows that larger

seeds yield a greater amount of oil, compared

to smaller seeds (in conversation with some

riverine people from the Bailique community,

Amapá, Brazil). This linear trend to produce

larger fruits and have larger seeds, can be

related to a more lasting source of nutrients for

the plants. Large seeds have greater amounts

of nutritive reserves for the development of the

plant and help to supply the lack of photosyn-

thetic tissue in the early stages of the seedling’s

life (Parolin, 2002).

The germination rate of P. macroloba

shows variability in different flooded environ-

ments in the Amazon. In this study, estuarine

floodplain forest, the germination rate found

was 78 %. In the igapó forest of Central Ama-

zonia, Parolin, Ferreira, and Junk (2003) found

a germination rate for P. macroloba of 45 %.

The two environments differ, among other fac-

tors, by the nutritional status of the soil. The

Amazon estuary is bathed by a river contain-

ing high load of sedimentary and nutritional

material, which are deposited in the soil of this

environment. The igapós of the Amazon are

of older geological origin and are bathed by

rivers of black water, with a high load of plant

material in decomposition, of low nutritional

fertility (Junk et al., 2011).

Hypogeal germination presented by P.

macroloba is common among Amazonian

floodplain species (Parolin et al., 2003) and

among native Amazonian legumes (Moreira

& Moreira, 1996). This type of germination is

related to the size of the seedling. Species with

hypogeal germination have seedlings eight

times larger than species of epigeal germi-

nation, both types of germination help the

seedlings to survive long periods of flooding

(Parolin et al., 2003). Melo, Franco, Silva,

Piedade, & Ferreira (2015) emphasize that the

germination of the type epigeal phanerocotylar

is an adaptive strategy for obtaining light and

in a short period of time.

Seedlings of P. macroloba produce numer-

ous lenticels in the epicotyl, fact also observed

by Parolin (2001) in floodplain seedlings in

the Central Amazon. Lenticels are essential in

flooded environments seedlings, due to these

structures facilitate the entry of oxygen and

improve the internal diffusion of gas between

the plant’s organs (Parolin, 2012). When locat-

ed above the surface of the water, lenticels are a

connection point between the aerial organs and

the root of the tree (Haase & Gudrun, 2010).

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Seedlings that manifest reserve cotyledons

in a flooded environment have great chances of

survival in this type of environment. Cotyledon

reserves guarantee rapid growth in height and

the seedling can escape total submersion in its

initial growth stages (Maia, Maia, & Parolin,

2005). This strategy is efficient in the Amazon

estuary, because most pracaxi seeds germinate

at the end of the flood period (period that the

waters recede from the interior of the forest)

and develop in the drought period (dry season

from September to December, where river

water does not reach the interior of the for-

est), being sufficient for the seedling to use the

cotyledon reserves and gain height to escape

the flood of next year.

Dispersion area of P. macroloba is quite

wide in the Neotropical region, allowing the

species to colonize various habitats. In Costa

Rica, the species is found in ancient alluvial

soils of virgin or secondary forests (Hartshorn,

1983), in annual precipitation regime above

4 300 mm and average temperature of 25 °C

(Eaton et al., 2011). On the island of Trinidad,

the species inhabits seasonal perennials forests

with high content of clay and sand (Greig-

Smith, 1952). In the Amazon region, the spe-

cies can colonize in flooded and non-flooded

environments. Dense populations of the species

can be found in clayey latosolic soils of the

dense non-flooded ombrophilous forest (Condé

& Tonini, 2013). In Central Amazonia, P. mac-

roloba is not dominant, but it tolerates lasting

flooding up to 14 m in height and poor soils in

the igapó forests (Ferreira & Parolin, 2007).

P. macroloba dominates estuarine floodplain

forests (Carim et al., 2016), areas with high

sedimentary load, rich in nutrients and low

amplitude of flooding (Junk et al., 2014).

The circular buffer method detected the

presence of 123 subpopulations of P. mac-

roloba widely distributed in the Neotropical

region. Hartshorn (1983) considers the pres-

ence of three large populations of P. macroloba

distributed in Latin America. According to the

author, the first population, widely studied,

occurs initially in the coastal region of Western

Nicaragua, passing through Costa Rica and

taking the Western part of Panama. The second

population occurs in the West of the depart-

ment of Chocó, Colombia and in the humid part

adjacent to the Darien province of Panama. The

third population is found in Northeast Venezu-

ela, the island of Trinidad, the Guianas and the

Amazon Basin. The author considers the neces-

sity for further studies aimed at the population

of the Amazon Basin, since this population is

little known in the scientific community.

Considering the Amazon region, P. mac-

roloba presents a pattern “centered in the Ama-

zon” proposed by Gentry (1981). The pattern

centered in the Amazon is characterized by

having a high density of species in the Ama-

zon Basin, while the pattern centered in the

Andes has its centre of diversity on the border

of Central America with North-western South

America (Antonelli & Sanmartín, 2011). Gen-

try (1981) explains that the centre of endemism

for some species in the Amazon was influenced

by changes that occurred in the Pleistocene

(theory of Pleistocene forest refuges). Drastic

climate fluctuations in the Pleistocene period

caused the fragmentation and coalescence of

tropical forests, resulting in the isolation and

speciation of large forest populations (Connor,

1986). Several theories emerged to explain the

diversity and distribution pattern of tropical

species (Antonelli & Sanmartín, 2011), howev-

er, some knowledge gaps remain unanswered,

requiring in-depth studies on the topic.

External morphological characteristics of

P. macroloba shows evolutionary and adap-

tive evidence of the species in response to the

dynamics and the varied flooding amplitudes of

the Amazon floodplain forests. The plasticity

of adaptation to different habitats may explain

the dominance of this species and its centre of

diversification in the Amazon. The result of

this study is essential to assist in management

strategies, allowing, among others, a more pre-

cise identification of productive trees to order

the collection of seeds. In the scope of public

policies, the results reinforce the valorisation

of non-wood forest products, orienting towards

the better use of pracaxi seeds, a non-wood

product of local socioeconomic importance and

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that inhabits the fragile estuarine floodplains of

the Amazon.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we

followed all pertinent ethical and legal proce-

dures and requirements. All financial sources

are fully and clearly stated in the acknowled-

gements section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank Programa de Pós-graduação em

Ecologia (PPGEco/INPA), Instituto Nacional

de Pesquisas da Amazônia (INPA), Consel-

ho Nacional de Desenvolvimento Científico

e Tecnológico (CNPq) (doctoral scholarship

142316/2016-4) and Empresa Brasileira de

Pesquisa Agropecuária (Embrapa Amapá). This

work was supported by the Empresa Brasileira

de Pesquisa Agropecuário do Amapá through

Kamukaia III project [02.13.07.007.00.00].

RESUMEN

Morfología, germinación y distribución geográfica

de Pentaclethra macroloba (Fabaceae): árbol amazónico

hiperdominante. Introducción: Pentaclethra macroloba

es un árbol hiperdominante en el estuario del Amazonas,

de gran importancia socioeconómica para la región, pues el

aceite de sus semillas es un poderoso medicamento natural.

Objetivo: Nuestro objetivo fue caracterizar la estructura

morfológica, las adaptaciones morfológicas en respuesta

a las inundaciones diarias del estuario del Amazonas y

el área biogeográfica de P. macroloba. Métodos: Una

descripción detallada de la morfología externa, desde la

germinación hasta el árbol adulto, se obtuvo de individuos

ubicados en el bosque periódicamente inundado, al noreste

de la Amazonia. El área de ocupación y la extensión geo-

gráfica de P. macroloba se determinaron a partir del punto

de coordenadas geográficas de muestras botánicas deposi-

tadas en las colecciones digitales de Mobot y SpeciesLink.

Resultados: Los individuos adultos tienen estructuras

adaptadas en respuesta a las inundaciones diarias, tales

como: raíces adventicias para aumentar la eficiencia res-

piratoria y lenticelas en el tronco, que sirven como punto

de conexión para el transporte de oxígeno entre la raíz y

la parte aérea. Los frutos secos favorecen la activación

del mecanismo de dehiscencia explosiva, permitiendo

que la semilla sea expulsada a larga distancia. La forma

deltoidea de la semilla permite la fluctuación en el agua y

una dispersión más eficiente. La plántula es hipogel fane-

rocotiledones y con un par de cotiledones de reserva que

proporcionan a la plántula una fuente extra de energía para

escapar de la inundación. La tasa de germinación fue del 78

% y la velocidad fue de 0.2 semillas día

-1

. El método Circu-

lar buffer reveló la presencia de 123 subpoblaciones de P.

macroloba distribuidas en un radio de 5 699 943 km² a lo

largo de la región neotropical. Conclusiones: Gran parte de

las estructuras morfológicas de P. macroloba son respues-

tas adaptativas y evolutivas al ambiente periódicamente

inundado del estuario del Amazonas, lo que demuestra que

estos ambientes actúan como filtro ambiental seleccionado

las especies mejor adaptadas al medio. Su amplia área

geográfica denota la plasticidad de adaptarse a diferentes

ambientes, lo que puede justificar su monodominancia en

algunas regiones.

Palabras clave: adaptación morfológica; inundaciones

por mareas; árbol neotropical; raíces adventicias; aceite de

pracaxi; manejo, conservación.

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