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A review of Neotropical Burseraceae

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DOI: 10.1007/s40415-021-00765-1

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Brazilian Journal of Botany
https://doi.org/10.1007/s40415-021-00765-1

SYSTEMATICS, PHYLOGENY & FLORISTICS - REVIEW ARTICLE

A review of Neotropical Burseraceae

Douglas C. Daly1 · Ricardo O. Perdiz2 · Paul V. A. Fine3 · Gabriel Damasco4 ·
María Cristina Martínez‑Habibe5 · Laura Calvillo‑Canadell6

Received: 29 July 2021 / Revised: 9 November 2021 / Accepted: 10 November 2021

© The Author(s), under exclusive licence to Botanical Society of Sao Paulo 2021

Abstract
This review of Neotropical Burseraceae emphasizes developments since the last major review of the family in 2011. The
Burseraceae comprise a Laurasian group (represented by Eocene fossils in the Northern Hemisphere) that originally dispersed
through Central America into Amazonia. During cooling and drying events in the Oligocene, the frost-intolerant northern
American progenitors were likely driven extinct; subsequently, the family experienced several vicariant events and later
several long-distance dispersals across the Southern Hemisphere. From Amazonia, the family re-colonized Central America
and the Caribbean. The most rapid diversifications in the Americas for the Burseraceae occurred during the Miocene in
Protium and Bursera, much of it through geological events, dispersal, and habitat specialization. A number of taxonomic
advances were made in Neotropical Burseraceae since 2011; these included 59 published new species overall, re-drawn
generic limits in tribe Protieae, new genus records for Burseraceae in Central America and the Cerrado of Brazil, new taxa
that more than doubled the number of Neotropical Dacryodes, and a recently recognized center of diversity for Protium
in the Andes. Revised generic descriptions and a new key to the New World genera of Burseraceae are provided. Special
attention is given to the implications of leaf architecture for characterization of clades. Monoecy (rare) and parthenocarpy
(possibly frequent) are discussed, and the close relationship of dioecious trees and small bee pollination is highlighted. Most
Burseraceae are dispersed by birds or arboreal mammals that carry pyrenes relatively short distances away from the mother
tree; however, other modes are found in the family, including wind dispersal (rare in New World Burseraceae), clumped
dispersal of pyrenes by ants and lizards, and oilbirds that can disperse Dacryodes fruits more than 30 km; some dispersers
that ingest pyrenes also aid in germination. The diversity and abundance of Burseraceae in a number of regions and habitats
(but especially in moist forests of Amazonia and dry forests of Mexico) are striking. This, plus the fact that the taxonomy
and phylogeny of New World Burseraceae are relatively well-resolved, spotlights the Burseraceae as an important model
organism for researching mechanisms of diversification, species limits, cryptic species, and “hyperdominance” in tropical
forests. High chemical diversity and differences in biological activity make sense in the context of diversification and coex-
istence. Studies of chemical defenses support the idea of a “growth defense trade-off” and suggest that selection by different
natural enemies could be implicated in the speciation process; they also show that closely related species often display high
chemical divergence, and plants with the most chemical defenses have a lower number and diversity of insect herbivores.
The range of physical and chemical properties of Burseraceae resin is reflected in their cultural uses, which are diverse while
showing strong ethnobotanical convergence.

Keywords Cryptic species · Diversification · Hyperdominance · Leaf architecture · Model organisms

1 Introduction

New World Burseraceae comprise an excellent case of recip-

rocal illumination, in which a strong taxonomic foundation
has permitted development of a robust phylogeny, which in
turn has informed decisions regarding suprageneric as well
* Douglas C. Daly as infrageneric classification (e.g., Daly et al. 2001; Fine
ddaly@nybg.org et al. 2005, 2014; Daly and Fine 2018). This permits
Extended author information available on the last page of the article

13
Vol.:(0123456789)

highlighting the results of research in which Burseraceae
taxa or clades have served as model organisms for testing
hypotheses relating to diversification or to patterns of plant
diversity (Daly et al. 2012a; Lagomarsino and Frost 2020),
shedding light on the roles of habitat specialization, parapa-
tric speciation, herbivore pressure, and chemical defenses in
diversification and species coexistence.
Moreover, phylogenomic studies of recalcitrant species
complexes are proving highly relevant to two prominent
issues in tropical tree diversity, cryptic species and hyper-
dominance, with the former bringing a critical focus on the
latter.
This review of Neotropical Burseraceae is not meant to
replace that of the whole family that appeared in Kubitzki’s
magnum opus (Daly et al. 2011; Kubitzki 2011); rather, it
emphasizes developments since then and in fact some sec-
tions (e.g., pollen) have been omitted if there has been little
of substance to report since 2011. Discussions and genus
descriptions are tailored to focus on New World Burser-
aceae; this means that some sections are rather different
from the treatment in Kubitzki (2011) even if they do not
report significant research post-2011.
All of Bursera is treated because the genus comprises an
important part of New World Burseraceae diversity, and any
geography-based partial exclusion would be artificial. Some
species are truly tropical, some are technically subtropical
or warm-temperate; moreover, some occur at low latitudes
but high elevations.
2 Fossil‑calibrated phylogenetic results
of Neotropical Burseraceae
The crown age of the Burseraceae was estimated to be
78–106 Ma, with its stem dating to at least 115 Ma (Weeks
et al. 2014). A second analysis that included all of the Sap-
indalean families and fossils throughout the order (but
relatively few Burseraceae taxa) recovered a more recent
fossil-calibrated crown age of 64–85 Ma for Burseraceae
(Muellner-Riehl et al. 2016). In any case, both analyses
estimate the origin of the Burseraceae to be during the
Cretaceous.
Fossil wood of Upper Cretaceous age (73 ma) was
reported from the Olmos Formation in Coahuila, México
(Estrada-Ruiz et al. 2010) and described as a new genus
and species in the Sapindales, Coahuiloxylon terrazasiae
Estrada-Ruiz, Martínez-Cabrera & Cevallos-Ferriz. The
wood shares anatomical characteristics with Burseraceae
and Anacardiaceae, like the presence of indistinct growth
rings, simple perforation plates, and heterocellular rays. One
could infer that C. terrazasiae represents a period when the
two sister families were diverging, although it could also be
13
D. C. Daly et al.
an extinct lineage that was neither strictly Anacardiaceae or
Burseraceae.
The fossil record of the family from the Paleocene and
Eocene includes several macrofossils from North America
and Europe. From the London Clay Formation, there are
fruits described as Bursericarpum aldwickense Chandler
and Protocommiphora europea Reid & Chandler, com-
pared, respectively, with extant Protieae and Commiphora
(Chandler 1961, 1964; Reid and Chandler 1933; Collinson
1983; Harley and Daly 1995; Weeks et al. 2005, 2014; Friis
et al. 2011). Similarly, reports of fossil leaves and pollen of
Bursera of the Eocene from the Lagerstätte of the Floris-
sant Fossil Beds in the Rocky Mountains of Colorado sug-
gest a tropical (or frost-free) climate there (Meyer 2003).
Furthermore, Calvillo-Canadell et al. (2013) described two
Eocene fossil leaves, Bursera popensis Calvillo-Canadell,
Rodríguez-Reyes, Medina-Lemos, & Cevallos-Ferriz and
B. ezequieli Calvillo-Canadell, Rodríguez-Reyes, Medina-
Lemos, & Cevallos-Ferriz, from the La Carroza Formation
in the La Popa basin of Nuevo León, Mexico.
The phylogenetic analysis of Weeks et al. (2014) suggests
that the family originated in the Northern Hemisphere, in
the Laurasia megacontinent. After the major cooling and
drying that took place in the Oligocene, Burseraceae along
with other plant taxa lacking frost tolerance were extirpated
from freezing climates and this resulted in several vicari-
ant events, with lineages entering the tropics and becoming
separated during continental drift and the widening Atlan-
tic Ocean. Several Neotropical lineages of Burseraceae
(e.g., within Protieae and Canarieae s.l.) have relatives in
Africa, Madagascar, and Asia that likely are products of such
ancient vicariance (Weeks et al. 2014; Gostel et al. 2016).
Long-distance dispersal has also played an important role in
the historical biogeography of the family, with more recent
transitions across oceans in Protium and Commiphora being
facilitated by bird- or wind-dispersed seeds (Fine et al. 2014;
Gostel et al. 2016).
The Protieae radiated after they arrived in the Amazon
and then secondarily dispersed to Central America, the
Caribbean, the Brazilian Atlantic Forest and the Chocó bio-
geographic region. This surprising result may be explained
by the contraction of lowland rain forest habitat in Central
America during the Oligocene and early Miocene—meaning
that although the Protieae once lived in North America and
likely dispersed to South America via Central America and/
or the Caribbean, these progenitors must have gone extinct
soon afterward and thus all extant Caribbean and Central
American taxa come from Amazonian ancestors (Fine et al.
2014).
Most diversification in Burseraceae has occurred since
the Miocene, with two of the largest rate shifts occurring in
Neotropical Protieae (Fine et al. 2014; Weeks et al. 2014)
and Meso-American Bursera (De-Nova et al. 2012). This
A review of Neotropical Burseraceae
accumulation of Amazonian diversity during the Miocene
agrees with recent paleogeographic reconstructions that
indicate that this period involved major changes in the
Western Amazon, including Andean uplift, major changes
to the hydrology of the main rivers, and the formation of new
edaphic habitats (Fine et al. 2014). Radiations are thought
to be spurred by key innovations or the colonization of new
regions. In this case, we envision that arrival into the large,
contiguous rain forest habitats of Amazonia, coupled with
the propensity to evolve habitat specialization, represented
an opportunity for Protieae trees to spread their ranges and
diversify. Fine et al. (2014) found that habitat specializa-
tion into sandy soil and flooded forest habitats has occurred
many times independently in the Protieae, especially in the
Amazon.
Bursera is an important floristic element in Neotropical
dry forests. Its center of origin is Mesoamerica, where about
100 of its 125 species occur. As noted, most extant spe-
cies of Bursera arose in the Miocene (De-Nova et al. 2012),
when that region underwent its peak aridification (Graham
2010). Very similar to Bursera and sister to it is the almost
exclusively Old World genus Commiphora, represented in
the New World solely by C. leptophloeos (Mart.) J.B. Gillett.
The two genera are so similar that some authors in Cuba and
Dominican Republic transferred several species of Bursera
to Commiphora, but molecular studies confirmed that in fact
all of the taxa present in the Greater Antilles and the Baha-
mas belong in Bursera (Martínez-Habibe 2012).
Extant species of Bursera in the Greater Antilles and the
Bahamas are derived from two separate colonization events
from Central America, and no sister relationships exist
between any South American ancestor and extant Greater
Antilles and the Bahamas taxa. Speciation in this region
occurred on and among emergent islands between the mid-
Miocene and the Pleistocene (Martínez-Habibe 2012), an
evolutionary history that agrees with paleogeographic evi-
dence (Iturralde-Vinent and MacPhee 1999; MacPhee and
Iturralde-Vinent 2000).
Megafossil records of Canarium fruits have been identi-
fied from the Eocene in North America, the Eocene to Oli-
gocene in Europe, the Oligocene in Africa, the Oligocene
to Miocene in Asia, and the Pleistocene in Australia and
the Pacific islands. Recently, Han et al. (2018) described
Canarium guangxiensis Han & Manchester based on com-
puted tomography (CT) scans of fossil fruits from the late
Oligocene in China. The broad distribution of Canarium and
related lineages over the Northern Hemisphere contracted
during the Miocene as a result of its extinction in North
America and Europe.
Based on the fossils known so far, Han et al. (2018)
hypothesized that Canarium may have had a North Ameri-
can Eocene origin, with subsequent spread to Eurasia
and Africa, followed by dispersal across the Southern
Hemisphere. It is interesting to note that Federman et al.
(2015) showed Malagasy Canarium to be monophyletic and
hypothesized that it reached Madagascar via long-distance
dispersal from tropical Asia. As currently circumscribed,
the genus is highly diverse in both Asia and Madagascar but
is represented in continental Africa by a single, apparently
relictual species, C. schweinfurthii Engl.
3 Family description and morphology
Trees or shrubs, sometimes rupicolous, very rarely scan-
dent or epiphytic, with schizogenous resin canals in most
vascularized tissues. Leaves alternate, rarely stipulate or
pseudostipulate (Old World only), imparipinnately com-
pound or infrequently unifoliolate or apparently simple,
rarely bipinnate, often the petiole pulvinate at base, the
rachis sometimes winged, often the lateral or at least the
terminal petiolules pulvinulate at apex; leaflets (sub-)
opposite; primary vein framework pinnate, secondary
vein framework usually some form of brochidodromous
or semi-craspedodromous (see separate “Leaf architec-
ture of Burseraceae” section). Inflorescences (pseudo-)
terminal and/or axillary, rarely cauliflorous, structurally
a panicle of cymes but sometimes appearing spicate, fas-
ciculate, or racemose. Flowers actinomorphic, unisexual
(with either the androecium or gynoecium reduced or
rarely obsolete, see “Reproductive Morphology” sec-
tion) or less often bisexual; hypanthium sometimes pre-
sent; perianth 2-whorled and 3–5(6)-parted; calyx par-
tially synsepalous, valvate (less often imbricate or apert
(open)), sometimes slightly accrescent in fruit; petals
distinct or less often partially fused, when free usually
induplicate-valvate or sometimes imbricate in the middle;
flowers (meta-)obdiplostemonous, rarely haplostemonous
(the antepetalous series missing); filaments usually dis-
tinct, anthers sometimes continuous with the filaments
(not sagittate), dehiscence longitudinal and introrse or
latrorse; disk intrastaminal, usually annular, sometimes
adnate to the receptacle or apparently absent (taxa with
hypanthium); gynoecium syncarpous and 2–5(6–12)-car-
pellate and -locular, in staminate flowers the pistil reduced
or less often rudimentary or absent, sometimes the disk
and pistillode replaced by a parenchymatous ovariodisk;
ovary superior, rarely semi-inferior within a hypanthium;
most locules abortive in most genera; ovules 2 per locule,
epitropous, collateral or (in Beiselia) superposed, attached
laterally or (sub-)apically; style 1, erect, sometimes shortly
branched near the apex, stigmas or stigmatal lobes usu-
ally as many as carpels but sometimes the stigma capitate.
Fruit a fleshy or dry compound drupe or rarely a pseudo-
capsule (Beiselia); each seed contained in a pyrene, the
pyrenes fused and indehiscent (Dacryodes, Trattinnickia),
13

or separated by a columella and dehiscent, with the pyr-
ene (partly) enveloped in a pseudaril or rarely (sub-)alate
(Beiselia). Seeds exalbuminous, the embryo minute and
straight; cotyledons entire and plano-convex, or lobed and
contortuplicate, or palmatifid, rarely transversely twice-
folded. Germination epigeal or hypogeal, cryptocotylar
or phanerocotylar, with the first eophylls opposite or
alternate, simple or trifoliate or pinnately compound, the
leaf(let) margin entire or serrate.
In the New World, approximately 280 species in 6 gen-
era, in the tropics and subtropics, represented by few taxa in
some warm temperate areas (Fig. 1).
Vegetative morphology – Burseraceae are entirely
woody. Most taxa are small to large trees, but Commiphora
leptophloeos can be shrubby and species in Bursera can be
shrubby, pachycaulous, or caudiciform in arid conditions;
some of these can be effectively lithophytic. Bursera stand-
leyana L.O. Williams & Cuatrec. is a small, epiphytic cloud
forest tree in Costa Rica.
Buttresses are often present in moist forest taxa; these are
(sometimes branched) plank buttresses, rarely flying but-
tresses, and/or stilt roots. The bark is diverse; the color is
usually gray or brown but can be red, yellow, or green (e.g.,
many Bursera spp.). It is close in most genera but can be
Beiselia
0 500 1000 1500 2000 2500 3000 km
Dacryodes
Fig. 1  Generalized distributions of the six New World genera of Burseraceae. Specimen data from New York Botanical Garden database. Dots
represent specimen collections of each genus. Map generated in R environment 4.1 (R Core Team 2021) with R packages tmap (Tennekes 2018),
sf (Pebesma 2018), and shapefiles from R package rnaturalearth (South 2017)
13
D. C. Daly et al.
papery and exfoliating (e.g., most Bursera subgenus Bur-
sera); it can be thin and smooth (most Protium) to thick and
deeply fissured (e.g., Protium sect. Tetragastris).
Resin ducts are associated with virtually all vascularized
tissues. The resin is usually evident as an exudate and can
be clear, translucent, milky, or rarely reddish, and the con-
sistency can be watery or gummy; the clear and translucent
resins usually have a strong terpenoid odor. It can dry crys-
talline and powdery, or solid and translucent, or rubbery and
opaque. In most species the resin is flammable when dry, in
some when fresh as well.
Most taxa are unarmed, but some Commiphora and a very
few Bursera have thorns that terminate short shoots, some-
times on adventitious shoots from the trunk and boughs;
axillary thorns have been reported on seedlings of Protium
javanicum Burm.f. (Lam 1932b) and observed on the only
known specimen of Protium melinonis Engl. The persistent
swollen petiole bases of Beiselia are often cuspidate.
Cataphylls are sometimes present (persistent in some Bur-
sera subgenus Elaphrium (Jacq.) Triana & Planch.). The
leaves are evergreen or deciduous (Beiselia, most Bursera,
Commiphora) and alternate (sometimes appearing opposite
in Protium unifoliolatum Engl.), often conferted at branch
apices. New World Burseraceae are exstipulate; most are
imparipinnate, but a few Bursera species are bipinnate,
Bursera Commiphora
Protium Trattinnickia
A review of Neotropical Burseraceae
several Protium species are unifoliolate (with a distal pulvi-
nulus), and several species of Bursera appear to have simple
leaves, lacking pulvinuli.
The petiole is often basally pulvinate, the rachis winged
in some Bursera. Most Dacryodes, Protium, and Trattin-
nickia have a pulvinulus at least at the distal end of the ter-
minal petiolule and usually at both ends of the lateral peti-
olules. The leaflets are (sub)opposite. The leaflet apex can
be gland-tipped (e.g., some Bursera). The margin is entire
or variously crenate or toothed, the teeth rarely gland-tipped
(e.g., Beiselia and Protium cuneifolium (Cuatrec.) Byng &
Christenh.).
Leaflet architecture (following Ellis et al. 2009) is mod-
erately diverse (summarized here but see separate “Leaf
architecture of Burseraceae” section on this topic). Pri-
mary venation is always pinnate, the secondary framework
most often (festooned-) brochidodromous or less often
cladodromous (Beiselia, some Bursera), or as noted above
semi-craspedodromous (Protium sect. Crepidospermum,
many Bursera subgenus Elaphrium). Intersecondaries are
sometimes present, also usually epimedial tertiaries. The
intercostal tertiary fabric is variously percurrent, irregular-
reticulate, or admedially ramified (sometimes composite
admedial). In Trattinnickia sect. Burserifoliae the areoles
define papilla-filled abaxial laminar crypts. Freely ending
veinlets are usually present and then dendritic, and ranging
from unbranched to highly branched (the latter in some Pro-
tium clades and most Bursera and Dacryodes), sometimes
ending in tracheoid idioblasts (Beiselia, most Bursera, many
Protium) or highly branched sclereids (e.g., Protium sect.
Papilloprotium).
Punctate leaflets characterize Protium sect. Icicopsis but
are not restricted to that section. In the Neotropics, asperous
leaflets are found in some Trattinnickia and in Dacryodes
cuspidata (Cuatrec.) Daly.
Reproductive morphology – Inflorescences are often
initiated with leaf flush or, in the case of most arid-zone
taxa, beforehand. In New World taxa, they are axillary albeit
often pseudoterminal (e.g., Trattinnickia). Inflorescence
architecture is a panicle of cymes, as noted above, but a
great deal of morphological diversity is achieved through the
suppression or proliferation of axes or the pedicels, result-
ing in pseudoracemes, pseudofascicles, or pseudospikes,
the latter characteristic of some lineages (e.g., Protium sect.
Icicopsis). Some New World taxa show rather subtle sexual
dimorphism of inflorescences; in these cases, the male inflo-
rescences are somewhat longer, more slender and more laxly
branched, with more flowers. Inflorescence bracts subtend
inflorescence axis branches and cymules and may be cadu-
cous to persistent.
Burseraceae flowers are actinomorphic and unisexual or
less often bisexual. In dioecious taxa, flowers are usually
structurally bisexual, but with either a reduced pistillode
lacking stigmas or reduced staminodes lacking pollen. The
flowers of some taxa and lineages show sexual dimorphism,
the pistillate flowers being slightly larger and more robust.
Perigynous species occur in some Bursera.
The perianth is always 2-whorled and can be
3–5(6)-parted. The calyx is partially synsepalous (rarely
divided to the base) and lobed (rarely truncate), and the aes-
tivation is usually valvate (apert (open) in Bursera, imbri-
cate in Commiphora). The petals are distinct or less often
partly to mostly fused, and their aestivation can be valvate,
induplicate-valvate (including all Protium) or valvate at the
apex and slightly imbricate along the sides (some Commi-
phora and Dacryodes). In most taxa, there is an inflexed
apiculum. Petal color ranges from pale green to (greenish)
yellow, white, cream, pink, and red.
The flowers are usually obdiplostemonous (i.e., carpels
are antepetalous), but the two whorls often appear to form a
single cycle (metaobdiplostemony; Lam 1931, 1932a); some
taxa are haplostemonous, with the antepetalous series miss-
ing; the anthers are sometimes continuous with the filaments
(not sagittate; some Dacryodes and staminate flowers of
some Protium sect. Tetragastris), the dehiscence longitudi-
nal and introrse or latrorse. As noted, in pistillate flowers the
stamens are reduced and the anthers do not produce pollen.
In New World species, the disk is intrastaminal and annu-
lar, less often adnate to the receptacle or apparently absent
(some Bursera with a hypanthium); in several clades the disk
and pistillode are replaced by a parenchymatous ovariodisk
(e.g., Protium sect. Tetragastris). In staminate flowers the
pistillode is variously reduced: (1) most often resembling
a reduced pistil and parenchymatous or with locules and
rudimentary ovules, capped by a style; (2) consisting of a
parenchymatous cylinder (e.g., Protium sect. Sarcoprotium);
(3) obsolete (e.g., some Bursera); or (4) part of the aforesaid
ovariodisk.
The gynoecium is syncarpous, 2–5-locular or rarely
(Beiselia) 10–12-locular, the ovary usually superior or
sometimes the perianth epigynous when a hypanthium is
present (some Bursera), the placentation axile. The single
style is apical, erect, sometimes shortly branched near the
apex, usually the stigmas or stigmatal lobes as many as the
carpels, sometimes the stigma capitate. In most Burseraceae,
the gynoecium is synascidiate at least to the midpoint of
the ovary, and symplicate up to the base of the distinct stig-
mas, but in Beiselia the synascidiate region encompasses
the whole ovary and extends beyond the locules, and the
symplicate zone below the postgenitally united distinct
carpel tips is short. In the flower of Beiselia, the notable
massive remnant of the floral apex is uplifted to the base of
the distinct carpel tips (Bachelier and Endress 2009). The
ovules are 2 per locule, collateral or superposed, usually
bitegmic, slightly campylotropous, and they have a longer
13

and thicker inner integument and an S-shaped or zigzag
micropyle. Additional details on the floral anatomy of the
family can be found in Narayana (1959, 1960) and Bachelier
and Endress (2009).
New World Burseraceae fruits are rarely dehiscent pseu-
docapsules or variations on a compound drupe, and the unit
of dispersal is the pyrene. The plants with pseudocapsules
(Beiselia in the New World) are dehiscent via dry valves,
releasing dry, compressed, winged pyrenes separated by a
persistent columella with as many lobes as the number of
valves; each pyrene is compressed parallel to radii of the
fruit axis (the columella lobes) and distally winged.
The compound drupes of New World Burseraceae are of
three types:
1. Fruits dehiscent septicidally and acropetally via valves,
the valves fleshy to leathery; pyrene 1 (including 1–2
connate or connivent abortive locules, rarely one or both
of these developing), basally attached to the receptacle,
and invested with a fleshy and brightly colored pseudaril
that partly or completely covers the pyrene (Bursera,
Commiphora).
2. Fruits dehiscent septicidally and acropetally via valves,
the valves fleshy to leathery (rarely sublignified), pyr-
enes 1–5, separated by a columella and enveloped in a
sweet, pulpy, white or rarely red pseudaril, on dehis-
cence tenuously suspended from the fruit apex by an
inverted V-shaped structure (Protium).
3. Fruits indehiscent, the exocarp thin and dry; the meso-
carp fleshy and oily or resinous or rarely dry; compound
pyrene (endocarp) of 2–3 connate locules, of which 1–2
are abortive; in Dacryodes the pyrenes are cartilaginous
and the undeveloped locules highly reduced and com-
pressed, forming an often separable articulated plate on
a margin of the developed locule; in Trattinnickia the
connate pyrenes are bony and tuberculate, the abortive
locules not reduced and not separable.
There is disagreement about the homology of the
pseudaril in the anatomy of the first two types. Van der Walt
(1975) considered it a zone of the mesocarp, and similarly,
Ramos-Ordoñez et al. (2013) interpreted it as being derived
from an inner mesocarp, while other authors associate it
with the endocarp; further developmental studies are needed.
In a phenomenon reported by Ramos-Ordoñez et al.
(2012) in Bursera species and frequently observed by the
current authors in Protium, the ovary develops and the
fruits reach their mature size and color well before the seeds
develop, and the locules are mostly empty; the seeds fully
develop and fill the locules just as the pseudarils are devel-
oping and just before the valves fall away. Ramos-Ordoñez
et al. (2012) also reported true parthenocarpy in Bursera, in
which the ovary and locules develop but no seeds develop.
13
D. C. Daly et al.
Both phenomena could be interpreted as effectively reduc-
ing the fitness of seed predators, which apparently invest a
great deal of energy opening empty fruits while the trees
economize on seed development.
The endocarp in all but one genus has a zone of weakness
(usually at the apex) where it splits open during germina-
tion. The testa in Burseraceae is thin but sometimes with
irregular thickenings and then infolded with contortuplicate
cotyledons, a morphology sometimes referred to as a “laby-
rinth seed” (van Heel 1970). The seed is exalbuminous, the
embryo straight, and the cotyledons account for most of the
seed volume. Cotyledon morphology in Burseraceae ranges
from entire and plano-convex and straight or variously
curved, to entire and plicate or contortuplicate, to pinnately
or palmately divided and folded, to 3-lobed and transversely
reverse-folded. Germination and seedling morphology in the
family are similarly diverse: germination can be epigeal or
hypogeal and cryptocotylar or phanerocotylar, and the first
eophylls can be opposite or alternate, simple or trifoliate or
pinnately compound, the margin entire or less often toothed.
4 Leaf architecture of Burseraceae
Leaves constitute an extremely rich and woefully under-
utilized source of characters for describing as well as dis-
tinguishing—or linking—angiosperms (Ellis et al. 2009),
revealing features of leaf architecture that will map onto
phylogenies at different ranks. Hickey (1973) expected that
leaf architecture will continue to grow in importance as an
integral part of any morphological study of dicots.
Recent work on the leaf architecture of Burseraceae and
Anacardiaceae has not only yielded insights into a number of
leaf characters (see below), it has also led to improvements
in protocols for leaf preparation (Vasco et al. 2014), which
in turn have made possible high-resolution images used in
studies quantifying connectivity in leaf vein networks (Ron-
ellenfitsch et al. 2015).
Paleobotanists need to be able to characterize the vein
patterns of leaf fossils, because that is most of what is avail-
able to them for study. The reality that leaf architecture is
the primary utensil for characterizing and identifying fossils
makes it essential for studies that help to re-construct ancient
floras and to understand how the plants of the past responded
to climate change (e.g., Carvalho et al. 2021).
Based on their fossil records as currently understood,
the Burseraceae and its sister family Anacardiaceae have a
long evolutionary history. Fossils of leaves, wood and fruits
attributed to various genera, especially of the Anacardi-
aceae, have been described from globally distributed fossil
localities, principally of Cenozoic age. Historical biogeog-
raphy depends heavily on plausible fossil identifications to
A review of Neotropical Burseraceae
formulate hypotheses about the origins and migrations of
extant groups; conversely, baseless taxonomic attribution
can misdirect those hypotheses. The present study thor-
oughly characterizes the leaves of many extant taxa repre-
senting many of the major lineages. Applying the same cri-
teria to ancient leaves will greatly facilitate a re-assessment
of key fossils that have formed the basis for prevailing sce-
narios of their historical biogeography.
As part of an initiative to develop an interpretive atlas of
the leaf architecture of the Burseraceae and Anacardiaceae, a
group of four collaborators has cleared, stained, and imaged
leaflets of 171 species of Burseraceae and scored them for 84
leaf characters (plus 10 tooth characters when appropriate),
plus nine geographic and ecological traits. This sampling
accounts for 12 of the 17 currently recognized genera in the
family and 111 of the estimated 193 species of tribe Protieae.
Leaf architecture and phylogeny of Burseraceae‑Pro‑
tieae – The most recent comprehensive phylogeny treat-
ing Burseraceae and Anacardiaceae is that of Weeks et al.
(2014). Sampling of major lineages in Burseraceae, espe-
cially in tribe Protieae, makes it possible to discern congru-
ences in leaf architecture within each of the nine published
sections in Protium, as well as in a number of unpublished
clades that can be recognized also by macromorphological
characters.
All Protieae have pinnate primary vein framework and
some form of brochidodromous secondary vein framework
(here including semi-craspedodromous). The venation is
usually highly organized, with strong areolation; for qua-
ternary and quintenary fabrics a very common combination
is irregular-reticulate and freely ramified. The great major-
ity of Protieae species sampled have a fimbrial vein, while
the marginal ultimate venation in some taxa is incomplete;
looping is rare.
Greater variation is found in the intersecondary veins,
including presence/absence, angle, length, and distal behav-
ior. Admedial tertiaries are quite diverse in origin (from
secondaries or their loops, intersecondaries, epimedial ter-
tiaries, costal tertiaries) and complexity (simple vs. com-
posite). Freely ending veinlets (FEVs) may be absent (i.e.,
areoles empty), or little-branched, or highly branched, and
termination can be simple, or tracheoid idioblasts, or highly
branched sclereids.
Unlike Bursera, less than ten percent of Protieae have
leaflets with teeth; some of these are only distally serrulate,
while others have teeth only on juvenile leaflets. Leaflets
of Protium sect. Crepidospermum always have teeth (some
glandular-tipped), while in the rest of the tribe some clades
include toothed and untoothed species, and a few species can
have toothed or untoothed individuals (e.g., Protium sub-
serratum (Engl.) Engl.). Some Protieae clades have leaflets
notable for non-vein characters, such as papillae (sect. Papil-
loprotium) or punctations (sect. Icicopsis).
Salient leaf architecture features of major clades
of Burseraceae‑Protieae – Protium sect. Crepidosper-
mum (1 of 6 species sampled). Secondary vein framework
semi-craspedodromous; intercostal tertiaries mixed oppo-
site-alternate percurrent and irregular-reticulate; FEVs
(freely ending veinlets) 0–2-branched; marginal ultimate
venation completely looped.
Protium sect. Icicopsis (8 of 21 species sampled). Epime-
dial tertiaries all perpendicular to midvein but also parallel
to secondaries in 2 species, all distally reticulating and in
7 spp also basiflexed; 6 species have intercostal tertiaries
mixed opposite-alternate-percurrent and irregular-reticulate;
all 8 sampled species have FEVs highly branched; 6 have
punctations visible.
Protium sect. Marignia (2 of 2 species sampled). Costal
secondary veins in 7–10 pairs, insertion (slightly) decurrent;
intersecondary veins 0–1 per intercostal space, long, adme-
dially branched; intercostal tertiary veins irregular-reticulate
and admedially branched; admedial tertiaries present, all off
intercostal tertiaries and composite from secondary loops;
quaternary veins all irregular-reticulate and freely ramified;
FEVs highly branched, terminating in tracheoid idioblasts.
Protium sect. Papilloprotium (5 of 5 species sampled).
Admedial tertiaries present in 4 of 5 species; quaternary
vein fabric irregular-reticulate and freely ramified; areolation
weak; FEVs highly branched, in 4 of 5 species terminating
in highly branched sclereids; some with serrate margin; 4 of
5 with dense papillae on abaxial surface.
Protium sect. Pepeanthos (5 of 8 species sampled). Cos-
tal secondary veins in 8–11 pairs; 4 species have alternate-
percurrent tertiaries in combination; all have quintenaries
irregular-reticulate and freely ramified (sextenary same in 2
of them); FEVs highly branched; 4 of 5 have a fimbrial vein.
Protium sect. Protium (3 of 4 species sampled, Old World
only). Epimedial tertiaries 1–2 per intercostal space, per-
pendicular to midvein, short and basiflexed or reticulating;
FEVs highly branched, in at least 2 species terminating in
tracheoid idioblasts; marginal ultimate venation with incom-
plete looping; inclusions in 2 species.
Protium sect. Sarcoprotium (4 of 9 species sampled).
Quintenary vein fabric irregular-reticulate and freely
ramified; FEVs highly branched, terminating in tracheoid
idioblasts.
Protium sect. Tetragastris (4 of 12 species sampled).
Quaternary and quintenary veins in 3 species are irregular-
reticulate and freely ramified; FEVs highly branched but
endings inconsistent.
Protium aracouchini complex (4 of 8 species sampled).
Epimedial tertiaries are perpendicular to midvein; 3 species
13

have quintenaries irregular-reticulate and freely ramified; 2
species have FEVs 0–1 branched, but 1 is unbranched or
1–3-branched.
Protium guianense (Aubl.) Marchand complex (3 spe-
cies sampled). Costal secondaries in 9–11 pairs; all 3 have
intersecondaries; epimedial tertiaries are perpendicular to
midvein; all are irregular-polygonal at quintenary or sex-
tenary; areoles empty or FEVs unbranched or 1-branched;
lamina appears punctate.
Protium hebetatum Daly complex (3 species sampled).
FEVs unbranched or 1-branched.
Protium heptaphyllum (Aubl.) Marchand complex (4 spe-
cies sampled). Tertiaries in 5 species are alternate-percurrent
in combination; 3 species have sextenaries irregular-polyg-
onal and freely ramified (1 has them irregular-reticulate and
freely ramified); 4 have FEVs unbranched or 1-branched, 2
species are unbranched to 2- or 3-branched.
Protium opacum Swart complex (4 species sampled).
Intercostal tertiaries in 2 species are alternate-percurrent
and irregular-reticulate and 2 species are mixed opposite-
alternate percurrent and irregular-reticulate; quaternaries all
alternate-percurrent and irregular-reticulate.
Diversity of tooth architecture in leaflets of Burser‑
aceae‑Protieae – Most species of Burseraceae and Anac-
ardiaceae have leaves or leaflets with entire margins, but
one also finds a number of taxa with margins that are ser-
rate, dentate, or crenate. The teeth described for these sister
families are diverse, and their morphological configurations
(including vasculature) may be linked to their evolutionary
history. Description of the distinct tooth types in their leaf
architecture brings new informative characters that per-
mit making taxonomic distinctions and in some instances
phylogenetic inferences. The work of Hickey and Wolfe
(1975) already recognized the importance of tooth charac-
ters for understanding angiosperm systematics (see Doyle
2007); they may also be understood as functional adaptive
responses in the context of climate studies, the leaf being the
organ that interfaces most with the environment in which the
plant grows (Xu et al. 2009; Hernández and Falcón 2014).
Teeth occur in at least five of the nine published sec-
tions and five unofficially recognized clades of Protium; the
margin may be crenate as in P. atlanticum (Daly) Byng &
Christenh. (sect. Crepidospermum); sparsely crenate as in
P. unifoliolatum (P. guianense clade); serrate as in P. pris-
tifolium Daly, or sparsely serrate as in most P. subserratum
(Engl.) Engl. (sect. Papilloprotium), P. dawsonii Cuatrec. (P.
heptaphyllum clade), and P. elegans Engl. (P. aracouchini
clade).
Irregular tooth spacing, angular sinus shape, and one
order of teeth predominate in tribe Protieae, although two
to three orders of teeth occur in Protium atlanticum and P.
pristifolium. The form and apex of teeth can vary among
13
D. C. Daly et al.
species and sections of Protium. For example, the tooth dis-
tal flank can be straight to concave (P. atlanticum), convex
(P. alvarezianum Daly & P. Fine, P. subserratum), or straight
(P. dawsonii); and the tooth proximal flank can be straight
to convex (P. alvarezianum, P. pristifolium, P. subserratum),
slightly convex (P. dawsonii), or convex (P. elegans, P. uni-
foliolatum, P. pilosum (Cuatrec.) Daly).
Leaf architecture and phylogeny of Bursera – To date,
sampling of Burseraceae outside of the well-sampled and
relatively highly resolved Protieae has been much more
uneven and incomplete. Of the major groups of Bursera
delimited by Espinosa et al. (2006), Andrés-Hernández et al.
(2012), De-Nova et al. (2012), and Martínez-Habibe (2012),
one (the B. copallifera (Sessé & Moc.) Bullock group) is
not yet represented in our samples and three groups are rep-
resented by only two samples each. Subgenus Elaphrium
(syn.: section Bullockia) is especially poorly sampled. Still,
some patterns can be observed.
Bursera simaruba (L.) Sarg. clade (7 species sampled).
All species sampled have festooned- brochidodromous sec-
ondary framework; in 5 the quintenaries are irregular-retic-
ulate and freely ramified; in 6 the FEVs are highly branched.
Caribbean clade (6 species sampled). Three have the leaf-
let apex tip glandular, 5 have admedial tertiaries (albeit with
different origins), all have the FEVs highly branched and
terminating in tracheoid idioblasts, and 4 have the marginal
ultimate venation with incomplete looping.
Bursera inaguensis Britton clade (3 species sampled).
All have admedial tertiaries, but with several combinations
of origins; all have the quaternaries irregular-reticulate and
freely ramified, and all have the FEVS highly branched and
terminating in tracheoid idioblasts.
Bursera fagaroides Engl. clade (2 species sampled). Both
species sampled show a cladodromous secondary frame-
work, decurrent insertion of secondary veins, admedial
tertiaries (also irregular-reticulate), and marginal ultimate
venation incompletely looped.
Bursera glabrifolia Engl. clade (2 species sampled). Both
species sampled have crenate margin, intercostal tertiaries
percurrent and irregular-reticulate, quaternaries alternate-
percurrent and irregular-reticulate, and quintenaries irreg-
ular-reticulate and freely ramifying. They also have very
similar tooth characteristics except the tooth principal vein
may be secondary or tertiary in rank and the sinus vascu-
larization is different.
Bursera fragilis S. Watson/B. microphylla A. Gray clade
(2 species sampled). Both have the secondary framework
cladodromous and intersecondaries that are parallel to the
secondaries and reticulating, but they differ in a number of
other respects.
A review of Neotropical Burseraceae
Discussion of leaf architectural characters – The
Manual of Leaf Architecture (Ellis et al. 2009) provides the
framework for leaf architectural studies. Working on the
Burseraceae-Anacardiaceae atlas has helped to refine con-
cepts and scoring of a number of leaf architectural character-
istics and indeed to make improvements in some of them and
to identify characters in the Manual needing improvement.
A character that has yet to be investigated in much depth
or taxonomic breadth is the Freely Ending Veinlets, or FEVs,
that occur within the areoles formed by leaf venation net-
works. The Manual and the scoring for the current Atlas in
preparation allow for type of branching (dendritic vs. dichot-
omizing), number of branches, and specialized endings
(tracheoid idioblasts and highly branched sclereids). Roth
(1996) realized that there are more character states related to
FEVs than had been reported but did not produce a coherent
framework for them. It will be important to examine them
in enough detail to study such characters as the number of
branching points within areoles and other qualitative aspects
of branching. It is also worth exploring possible correlations
between FEV type and habitat or phylogeny.
Hickey and Wolfe (1975) noted that the type and vascu-
larization of leaf teeth have a strong phylogenetic signal at
higher taxonomic ranks, but even a cursory examination of
the diversity of leaf(let) teeth in Anacardiaceae and Burser-
aceae highlights the fact that this feature of leaf architecture
is very poorly explored, indeed several patterns have yet to
be named, much less categorized.
5 Generic limits in New World Burseraceae
The most recent available overall phylogeny of Burseraceae
is that of Weeks et al. (2014), in which the monotypic Afri-
can genus Aucoumea is sister to Bursera + Commiphora.
The two major subgenera of Bursera are supported, as is
the placement of Commiphora leptophloeos firmly within
Commiphora.
The most recent available phylogeny that examined tribe
Canarieae s.l. in some depth (Federman et al. 2015) suggests
that Neotropical Dacryodes is sister to Trattinnickia; this
close relationship is evidenced by D. connata Daly & M.C.
Martínez, in which the petals are partially connate while
the rest of the genus is apopetalous. It is also suggestive of
that relationship that both D. cuspidata (Cuatrec.) Daly and
D. glabra (Steyerm.) Cuatrec. were originally published in
Trattinnickia.
The same phylogeny (Federman et al. 2015) shows the
Neotropical Dacryodes + Trattinnickia clade as sister to
African Dacryodes, and that clade in turn rather distantly
related to Asian Dacryodes + Santiria. It should be noted
that Neotropical Dacryodes was not well represented in the
sampling for the phylogeny.
Generic limits in Protieae were re-examined by Daly and
Fine (2018). Long-standing doubts about the monophyly of
Protieae genera (Daly 1989) were resolved by subsuming
Crepidospermum and Tetragastris under Protium in a mono-
generic tribe Protieae. The phylogeny showed strong sup-
port for the nine formally recognized sections of Protium,
most of which had been recognized as genera at some point;
the necessary new combinations were made, a diagnosis for
each section presented, and all the recognized species in
the genus assigned to sections. Still, Protium sect. Icica is
something of a “wastebasket” in that there is very little to
define it morphologically; moreover, it contains a good deal
of internal structure, some of which may eventually warrant
sectional status.
6 Taxonomic and floristic advances in New
World Burseraceae, 2011–2021
Research on Neotropical Burseraceae in the decade since
Kubitzki’s landmark synthesis of the angiosperms (Daly
et al. 2011) has resolved or greatly improved the taxonomy
of a number of clades in the family, including Protium sect.
Tetragastris, P. sect. Icicopsis, Trattinnickia, Bursera, and
Dacryodes. It has produced treatments of the family for
several flora catalogs. Fieldwork has revealed some striking
range extensions, and the results of taxonomic investiga-
tions have necessitated changes in ideas about dominance,
habitats, and geographic patterns of diversity and endemism.
A total of 59 new species were published in New World
Burseraceae in the decade since 2011.
Floras. Treatments were published for the catalogs of the
floras of Bolivia (Daly 2014a, b, c) and the Department of
Antioquia in Colombia (Daly 2011). New species of Bur-
sera have been published (Martínez-Habibe et al. 2013;
Martínez-Habibe and Daly 2016) in preparation for a treat-
ment of the family for the Flora of Cuba, which is as yet
unpublished.
Bursera. There were developments in the infrageneric
classification of this genus. Bursera subgenus Buntingia was
published to accommodate B. inversa Daly, which is distin-
guished from subgenera Bursera and Elaphrium by having a
milky resin, 15 staminodes (vs. 10), the stigma capitate (vs.
lobed), the abortive locules not reduced (vs. not), and the
cotyledons undivided with erose margin (vs. lobed, Castro-
Laportte 2013).
The Bursera species known colloquially as the quajiotes
have long been proposed as a distinct monophyletic group,
characterized by having a cladodromous secondary leaflet
vein framework, tracheoid idioblasts terminating the Freely
13

Ending Veinlets, and distinctively multi-lobed cotyledons.
Espinosa et al. (2006) suggested recognition of a section to
be called Quaxiotea, and Andrés-Hernández et al. (2012)
reiterated the idea, but it has never been formally described.
One remarkable recent discovery was Bursera pereirae
Daly (2014c), the first new species of the genus described
from South America in the preceding 21 years, the first
record of Bursera for the Cerrado region, and the only spe-
cies of tribe Bursereae endemic to Brazil.
As noted, two species of Bursera were published for the
Flora of Cuba project still under way. Bursera gibarensis
M.C. Martínez, Daly & J. Pérez is a densely branching suf-
frutex with trifoliate leaves, and B. yaterensis M.C. Mar-
tínez, Daly & J. Pérez is a small shrub with unifoliolate
leaves. Both species are endemic to xeromorphic coastal
scrub in eastern Cuba. In addition, a taxonomic and phylo-
genetic analysis of Bursera subgenus Bursera in the Greater
Antilles and the Bahamas resulted in 15 accepted species,
including 5 species that had been transferred to Commiphora
but belong in Bursera (Martínez-Habibe 2012).
Dacryodes. Until 2011, Neotropical Dacryodes consti-
tuted a relatively small group of 23 species known from
the Caribbean and lowland northern South America, and
with the exception of the Caribbean D. excelsa Vahl, rare
where they occurred. In the decade since, 30 new Neotropi-
cal species have been published (29 by authors of the present
paper), totaling 53 recognized Neotropical species (Daly
and Martínez-Habibe 2016, 2019; Santamaria-Aguilar and
Aguilar 2017; Martínez-Habibe and Daly 2019). Dacryodes
patrona Daly (2014a, b, c) constituted a new genus record
for Central America, and D. uruts-kunchae Daly, M.C. Mar-
tínez & D.A. Neill (Daly et al. 2012a, b) is a dominant tree
on a number of sites in the northern Andes, some at eleva-
tions exceeding 2000 m. The major center of diversity for
neotropical Dacryodes is Amazonia, with minor centers in
the Andes and the Chocó floristic province.
Protium. The past decade has seen significant resolution
of the taxonomy of tribe Protieae. First, Protium sect. Pap-
illoprotium was published (Daly and Fine 2011), followed
later by an overhaul of generic limits in the tribe, such that it
now comprises a single genus, Protium, with nine published
sections. Two of these, Crepidospermum and Tetragastris,
had until recently been treated as distinct genera (Daly and
Fine 2018). Protium currently comprises 145 published and
accepted taxa, plus 60 as yet undescribed (Daly et al. 2020).
We have increased our understanding of geographic pat-
terns of diversity in Protium. Amazonia + Guianas continues
to be the most important center of diversity, with 97 pub-
lished and recognized taxa, some of them published only
recently (e.g., Daly 2018), plus a number of still unpublished
taxa. Meanwhile, examination of specimens from Mexico
and Central America had led to the recognition of 13 pub-
lished and accepted species from that region as of 2015,
13
D. C. Daly et al.
but then four new species were added to that number in the
following five years (Santamaría-Aguilar and Lagomarsino
2017; Perdiz et al. 2020); furthermore, eight species from
Central America remain undescribed.
Prior to 2011, only a handful of Protium species were
known from montane regions in the Andes and Venezuelan
Guayana, but that vision is changing. Several new Andean
species of Protium have been published recently (Daly 2020;
Daly et al. 2020), with a backlog of 25 undescribed species
from the region; a complicating factor is that ten of those are
known from only one collection.
Despite substantial advances in range extensions, habitat
extensions, and diversity of a number of clades in Neotropi-
cal Burseraceae, there are glaring gaps in documentation of
that diversity in regions where botanical activity has slowed
drastically in recent decades, including Venezuelan Guay-
ana, Panama, and montane elevations in general. Many of
the specimens representing undescribed diversity in these
regions as well as most of the Andes were collected in the
1980s and 1990s, reinforcing the pattern observed by Bebber
et al. (2010) that new taxa usually languish in herbaria for
many years before they are discovered and described.
Trattinnickia. With the publication of seven new species
since 2011, Trattinnickia now comprises 19 accepted spe-
cies, the great majority of them Amazonian and 12 of the
19 rare and poorly collected (Daly and Melo 2017; Melo
and Daly 2021).
7 Plant‑animal interactions and fungal
associates
Pollination and breeding systems – Neotropical Burser-
aceae are mostly dioecious, while the flowers of some Bur-
sera and Dacryodes are bisexual. Monoecy is rare, but one
example is Bursera linanoe (La Llave) Rzed., Calderón &
Medina in Guerrero, Mexico: in three populations, 77 trees
were found to be pistillate, 29 were staminate, and 44 were
predominantly staminate but still produced a few fruits
(Gutiérrez-Santiago et al. 2016).
Another strategy was displayed by Bursera morelensis
Ramírez in Mexico. Parthenocarpic fruits developed from
flowers that were not pollinated, and it was proposed that
this might serve to deceive insect seed predators (Ramos-
Ordoñez et al. 2008).
Dioecy often correlates with a woody habit and entomo-
phily (e.g., Matallana et al. 2005), notably with pollination
by small generalist insects (e.g., Bawa and Opler 1975); the
rather scant literature about pollination of Burseraceae sug-
gests that this is consistent in the family regardless of habi-
tat; examples are Trattinnickia peruviana Loes. (small bees,
van Dulmen 2001), Protium divaricatum Engl. and Com-
miphora leptophloeos (diverse small insects, van Dulmen
A review of Neotropical Burseraceae
2001 and Machado and Lopes 2004, respectively), Protium
subserratum (mostly Trigona spp. but some other Hymenop-
tera and Lepidoptera, Misiewicz et al. 2020), and Protium
spruceanum (Benth.) Engl. (Trigona sp. and Apis mellifera
Linnaeus, 1758, Vieira and Carvalho 2008).
In Central Amazonia, Burseraceae constituted the second
most-preferred family for two Melipona species (Souza et al.
2020). In the Yucatán of Mexico, Burseraceae comprised
the second most important source of nectar for the Mayan
Stingless Honey Bee Melipona beecheii Bennett, 1831 as
estimated by pollen volume (Villanueva-Gutiérrez et al.
2018). In Puebla, Mexico, Bursera copallifera received a
higher diversity of floral visitors on lower-disturbance sites
in dry forests (Rivas-Arancibia et al. 2015).
Individual flowers in Burseraceae are generally short-
lived (e.g., Bursera simaruba, Primack 1985). Both “Big
Bang” and “trapline” flowering strategies occur in the family
(sensu Gentry 1974), and at least in Protieae members of the
same clade tend to show the same syndrome (e.g., trapline
in Protium sect. Icicopsis as opposed to Big Bang in sect.
Sarcoprotium, pers. obs. Daly).
Sexual dimorphism in Burseraceae flowers is usually sub-
tle in Neotropical Burseraceae and visible only in dissected
flowers, because the non-functional organs are more often
reduced instead of obsolete; notable differences in flower
size between genders are found in only a few groups (e.g.,
Protium sect. Icicopsis).
The pollinator reward is nectar, secreted by the usually
annular disk. For example, in Central Brazil both flower
sexes of Protium spruceanum produced relatively abundant
nectar (~ 4 µl), with an average 30% concentration of sucrose
equivalents (Vieira and Carvalho 2008).
Dispersal – The two prevalent dispersal syndromes in
Burseraceae are zoochory (mostly endozoochory) and
anemochory. Winged pyrenes have arisen independently in
at least four distinct lineages, the Mexican endemic Beiselia
and the Paleotropical genera Aucoumea, Boswellia, and Tri-
omma (Canarieae). Hydrochory has not been recorded but
likely occurs in some of the rather few floodplain species.
The reward for dispersers differs among lineages. The
fruits of Protieae are dehiscent, and their pseudarils are
sweet, but they provide a low-energy resource, for exam-
ple, 6.5 kJ per pseudaril in Protium stevensonii (Standl.)
Daly (syn: Tetragastris panamensis) (see Howe 1980). The
fruits of Bursera are also dehiscent, but in contrast, the
pseudarils of Bursera simaruba and B. hindsiana Engl. are
fleshy and have high caloric content (32.8 ± 1.3 kJ ­g−1 and
27.4 ± 0.8 kJ ­g−1, respectively, Bates 1992).
Many Burseraceae show a generalist dispersal strat-
egy, and few visitor species are effective or important dis-
persers. In Panama, while 26 bird species were observed
feeding on Bursera simaruba fruits, only some of these
(notably oropendulas and caciques) swallowed the pyr-
ene and pseudaril and subsequently regurgitated the pyr-
ene remotely (Trainer and Will 1984). Also in Panama, 25
species were recorded as visiting Protium stevensonii (syn:
Tetragastris panamensis) fruits, and a number of mammal
and bird species removed the pyrenes, but monkeys were the
primary dispersers and the howler monkey Alouatta alone
accounted for 74% of seed removal; seeds deposited in the
feces of the mammals were viable (Howe 1980).
There are cases of strong (inter-)dependence. For the
oil-bird Steatornis on Trinidad, Burseraceae comprised
more than 25% of fruits consumed and was the second most
important family after palms; Dacryodes fruits often out-
numbered all other species in the samples (Snow 1962).
In Sonora, Mexico, the migratory gray vireo’s five-month
winter diet consists almost entirely of Bursera microphylla
fruits, and there is strong overlap between the vireo’s winter
range and that of B. microphylla (Bates 1992).
In Amazonia and the Guianas, bats have been observed
dispersing the fruits of several Protium species (Charles-
Dominique 1991; Parrado-Rosselli 2005; Lobova et al.
2009); it is worth noting that all have fruits that are green
or whitish both inside and out, whereas the fruits of many
Protium species show a sharp color contrast between the
outside and inside.
The “quality” of dispersal is extremely important. In a
study of Bursera longipes Standl. dispersal in a dry-forest
zone of southwestern Mexico, it was noted that birds that
functioned as legitimate dispersers by consuming whole
pyrenes and regurgitating or defecating intact pyrenes also
removed the pseudaril in the process, thereby facilitating
germination; the highest germination percentages were
recorded for seeds that passed through the digestive tract
of two migratory flycatchers (Almazán-Nuñez et al. 2016).
Dispersers may have different digestive systems. For
example, in Mexico, two bird species ingested pyrenes and
pseudarils of Bursera fagaroides, but 17% of those ingested
by Dumetella carolinensis (Linnaeus, 1766) germinated
(Ortiz-Pulido and Rico-Gray 2006), while those passed by
Vireo griseus (Boddaert, 1783) did not.
At Caparú Biological Station in Amazonian Colombia,
woolly monkeys (Lagothrix lagothricha (Humboldt, 1812))
dispersed the pyrenes of seven species of Protium and facili-
tated their germination (González and Stevenson 2014).
At the Cueva de los Guácharos in the Colombian Andes,
the oilbird Steatornis caripensis (Humboldt, 1817) ingested
the lipid-rich fruits of Dacryodes olivifera Cuatrec. and dis-
persed them up to 32.3 km (Stevenson et al. 2021). Prestoea
acuminata (Willd.) H.E. Moore (Arecaceae) and D. olivifera
accounted for the most biomass, and D. olivifera showed
the highest Seed Dispersal Effectiveness value (Cárdenas
et al. 2021).
13

In Bursera and especially Protium, when the valve(s) fall
from the dehiscing fruit, the exposed pyrene + pseudaril is
tenuously attached (at base and apex, respectively) and even-
tually falls if not animal-dispersed; that of Protium stevenso-
nii (syn: Tetragastris panamensis) can hang suspended for
72 h before dropping to the forest floor (Howe 1980).
Several lineages in Burseraceae display clump-dispersal,
in which frugivores defecate seeds in masses, and this often
corresponds to high seedling survival, something unexpected
considering density-dependent mortality and seed-shadow
effects. In Panama, 24% of ingested pyrenes of Protium
stevensonii (syn: Tetragastris panamensis) were dropped
in fecal clumps; droppings of howler monkey, white-faced
monkey and coatimundi contained 1–60, 6–45, and 4–9 pyr-
enes, respectively (Howe 1989). In the Colombian Ama-
zon, a relatively high proportion of seeds were viable under
and near the parent tree crown of Dacryodes chimantensis
Steyerm. & Maguire. Similarly, there was high survivorship
capacity close to (< 10–15 m) parent trees of Protium pan-
iculatum Engl., and overall seed predation of its fruits was
low compared to many other tropical species, suggesting a
need for only occasional longer-distance dispersal to found
new populations (“patches,” Parrado-Rosselli 2005).
In a Northeastern Brazilian forest, leaf-cutter ants
amassed numerous pyrenes of Protium heptaphyllum
3.4 ± 2.2 m from parent trunks; subsequently, they cut and
harvested the epicotyls of most seedlings but ultimately
effected short-distance dispersal of the survivors (Silva et al.
2007).
A study of Protium icicariba (DC.) Marchand in Eastern
Brazil observed dispersal by birds, but also workers of Atta
robusta ants removed the pseudarils or moved the pyrenes
to anthills; at the same time, Tropidurus torquatus lizards
ingested pyrenes with the pseudarils and defecated them
whole (Pereira et al. 2020).
Galls – Burseraceae are conspicuous in both the abundance
and diversity of galls. On three sites in Central Amazonia, a
species of Protium and Licania micrantha Miq. (Chrysobala-
naceae) were the host tree species that presented the high-
est number of gall morphospecies (ten morphotypes each,
Julião et al. 2014). In the Northeastern Brazilian state of
Bahia, Burseraceae hosted the second greatest number of
gall midge species (Maia and Silva 2020). In Costa Rica, a
new species of the braconid wasp genus Allorhogas crinitus
was described, reared from leaf galls on Protium panamense
(Rose) I.M. Johnst. (Centrella and Shaw 2013).
Fungal associates – In addition to galls, Burseraceae also
harbor fungal diversity. In the Brazilian Cerrado, a new
Puccinia-like genus, Neopuccinia, was discovered on Pro-
tium heptaphyllum (Martíns-Junior et al. 2019). In an area
of caatinga vegetation in Northeastern Brazil, 14 species of
13
D. C. Daly et al.
arbuscular mycorrhizae were found associated with Com-
miphora leptophloeos (Teixeira-Rios et al. 2018). In Minas
Gerais State, Brazil, a new species of Rosenscheldia (Doth-
ideomycetes) was discovered on branches of Protium warm-
ingianum Marchand, the first report of Rosenscheldia on
Burseraceae hosts in Brazil (Custódio et al. 2019).
Other relationships – Bark-boring weevils of the genus
Sternocoelus (Curculionidae) induce resin exudation by sev-
eral species of Burseraceae in eastern Amazonia, and the
hardened resin protects the developing larvae; the Tembé
and Ka’apor indigenous groups take advantage of this phe-
nomenon to collect resin and take it to market, where it is
bought and used for a number of practical and medicinal
purposes (Plowden et al. 2002).
8 Ecological importance
In the New World tropics and subtropics, the Burseraceae
comprise a significant component of the structure and diver-
sity of a number of regions and habitats, as borne out by
numerous studies published since 2011, some of them cited
here. The (sub-)tropical dry forests of Mexico are in many
locations the domain of Bursera; several species of Protium
are highly important in much of Amazonia; Commiphora
leptophloeos is abundant in parts of the Caatinga and Cer-
rado biomes of Brazil; and P. icicariba is an important part
of several areas of coastal restinga vegetation in Eastern Bra-
zil. As currently circumscribed, Protium heptaphyllum is a
dominant element in other restingas of Eastern Brazil, ripar-
ian forests of Northeastern and Southeastern Brazil, and dry
forests of parts of Central Brazil, but recent phylogenomic
studies suggest that some of these regional dominants com-
prise at least eight distinct species overall (see “Hyperdomi-
nant lineages in Burseraceae” section; Damasco et al. 2021).
In a study of tropical dry forest in the Siboney-Juticí
Ecological Reserve, Cuba, Bursera simaruba showed the
second highest density of all recorded tree species (Cardona
et al. 2017). In a biogeographical analysis of dry forests in
southern Mexico, multiple species of Bursera were endemic
to each of two floristic subprovinces of the Sierra Madre
del Sur province (Morrone et al. 2017). A study of the tree
flora in the Tenancingo-Malinalco-Zumpahuacán protected
area, state of Mexico revealed 19 species of Bursera, the
third most species-rich genus in the area (López-Patiño et al.
2012). And in a study of a remnant tropical dry forest in
central Veracruz, Mexico, three of the seven most dominant
species were Bursera species (Williams-Linera and Álvarez-
Aquino 2016).
In a study of the woody component of the flora of semi-
arid caatinga vegetation in Paraíba state, Commiphora lep-
tophloeos had the third-highest Importance Value (Guedes
A review of Neotropical Burseraceae
et al. 2012). In a study of the soil seed bank at different
depths and light conditions in a dry forest in northern Minas
Gerais, Brazil, seeds [pyrenes] of C. leptophloeos were the
most abundant (Menezes et al. 2019).
Amazonia is an important center of diversity and end-
emism for Burseraceae (Daly et al. 2012a, b; Daly 2018,
etc.). In a long-term inventory of 15 hectares of terra firme
dense forest in Central Amazonia, 36% of the species were
considered rare but the families Sapotaceae, Lecythidaceae
and Burseraceae together accounted for 39% of the total
number of individuals (Silva et al. 2011).
In an extensive study of niche determinism in the Colom-
bian Amazon, Burseraceae comprised two of the top ten
indicator species for the geological shield and three of the
top ten indicator species for Tertiary substrates (Cárdenas
et al. 2017). In a study of forest on an alluvial terrace in
Tambopata, Madre de Dios, Amazonian Peru, “Protium
altissimum” had the third-highest Importance Value (Agu-
irre and Pollito 2011), although given the location, the spe-
cies was probably P. acrense Daly (2020).
In Puerto Rico, Dacryodes excelsa is a dominant tree spe-
cies in moist tabonuco forests, as the species is popularly
known. This dominance is due in part to “unions” or clumps
of trees interconnected by root grafts. More than 60% of all
stems and basal area of tabonuco trees occur in these unions,
in which hurricane damage is significantly lower and the
trees are taller and have a smaller crown-DBH ratio (Basnet
et al. 1993).
A combination of ecological versatility and habitat spe-
cialization makes the Burseraceae an important part of
white-sand formations in Amazonia (Fine and Baraloto
2016). In a study of three forest formations on white-sand
soils in Viruá National Park, in the Rio Negro basin of north-
ern Amazonian Brazil, Burseraceae had the second highest
relative density and Protium stevensonii (syn.: Tetragastris
panamensis) was the species with the highest Importance
Value (Mendonça et al. 2017). In a study of forests on three
other areas of white-sand soils in central Amazonia, Burser-
aceae showed the third-highest Importance Value and the
second highest relative density (Demarchi et al. 2018).
For a study of ecological dominance in a sandy coastal
plain open scrub formation in Jurubatiba National Park, Rio
de Janeiro, Brazil, Protium icicariba had the second highest
Importance Value (Rosado and Mattos 2017). In Guarapari,
Espírito Santo state, Brazil, P. icicariba had the second high-
est Importance Value in both periodically flooded and non-
flooded shrubby restinga vegetation on white sand (Kuster
et al. 2019).
The Protium heptaphyllum complex has long been prob-
lematic (e.g., Daly 1987 and see “Hyperdominant lineages
in Burseraceae” section). It should be noted that while one
or another component of the complex may be a dominant
part of many regions and habitats, P. heptaphyllum is far
from being a single hyperdominant species (sensu ter Steege
et al. 2013), and the identities and abundance of the spe-
cies involved below will have to be re-examined (Damasco
et al. 2019, 2021). In a fragment of dry forest of the Serra
de Maracaju in the Pantanal region of Mato Grosso do Sul,
Brazil, “Protium heptaphyllum” showed by far the highest
Importance Value (Stavis et al. 2020). In an area of wood-
land savanna in the Brazilian Cerrado biome in Gurupi,
Tocantins state, “P. heptaphyllum” had the second highest
Importance Value (Cândido et al. 2016).
In a riparian forest in Sirinhaém, Pernambuco state,
Northeastern Brazil, “P. heptaphyllum” showed the highest
relative density and Importance Value (Silva et al. 2012).
“Protium heptaphyllum” showed the second highest rela-
tive density in both an area of moist Atlantic Forest in Per-
nambuco, Brazil (Lima et al. 2019) and in a study of woody
coastal restinga vegetation in Maranhão state (Machado
and Almeida Jr. 2019). “Protium heptaphyllum” showed
the highest Importance Value both in a study of coastal
dune vegetation in Itaúnas, northern Espírito Santo state in
Southeastern Brazil (Giaretta et al. 2013) and in a study of
the woody components of coastal plain restinga vegetation
in southern Bahia state (Santos et al. 2015).
The Protium heptaphyllum complex is not the only
Burseraceae that can dominate Cerrado sites. In a dry forest
fragment in Minas Gerais state, Brazil, Protium spruceanum
showed the highest density, and P. spruceanum and P.
widgrenii Engl. showed two of three highest Importance
Values (Silva et al. 2019a).
9 Ethnobotany and economic botany
Wherever Burseraceae occur, they are well known by local
cultures and they are easily found using the appropriate
regional names; some of the Neotropical examples are tabo-
nuco or encens (Caribbean Dacryodes), anime (Colombia),
isigo (eastern Bolivia), breu (Amazonian Brazil), tacama-
jaca (Venezuela), almêcego/almácigo/almiscar (Colombia,
Central and Southern Brazil), and copal (Mexico, Central
America, Colombia, Ecuador, Peru)(pers. obs.), not to men-
tion lesser-known indigenous names such as variations on
uruts-kunché (Shuar of Peru and Ecuador, Daly et al. 2012b).
The resins of Burseraceae can be so important culturally that
for example the Ka’apor of Maranhão, Brazil, have a spe-
cial purpose resin-based classification for them parallel to
a more standard morphology-based folk taxonomy (Balée
and Daly 1990).
There is remarkable congruence of uses for Burseraceae
resins; throughout the tropics, they are used as a sealant
(especially for caulking boats), as a fumigant, and for illu-
mination, among multiple other uses, but especially for
13

medicinal and ritual purposes (pers. obs.; also e.g., Walker
and Sillans 1961; Miller and Morris 1988; Daly et al. 2015).
The Yanomami of northern Brazil have many uses for
Burseraceae species (Albert and Milliken 2009; Yanomami
et al. 2014). As is common for Burseraceae across Amazo-
nia, they burn the resin of many Protium spp. and Dacryodes
spp. for illumination, and the wood is valued as excellent
firewood. The resin of Protium unifoliolatum and P. ama-
zonicum (Cuatrec.) Daly (the latter cited under the synonym
P. fimbriatum Swart) has been used to treat pulmonary dis-
orders. People consume the fruits of Dacryodes peruviana
(Loes.) H.J. Lam, D. roraimensis Cuatrec., P. altissimum and
P. polybotryum (Turcz.) Engl., and they recognize ten dis-
tinct entities within Dacryodes under the name mora mahi
(Milliken et al. 1999). They also eat the larvae of Nymphali-
dae collected in the trunks of P. amazonicum. Flowers of P.
amazonicum are visited by bees in the process of making
honeycombs. The wood of P. amazonicum is used to make
joists in house construction. Burned resin of Protium spp. is
mixed with an extract of crushed Bixa orellana L. seeds and
Copaifera sp. oil to produce a black dye for body-painting.
An unidentified species of Protium is used to treat diarrhea.
In moist forests of eastern Bahia, Brazil, Protium sp. trees
are wounded to produce resin used in candomblé ceremonies
(pers. obs., Daly), while P. catuaba (as Tetragastris) is used
locally as a sexual tonic (one of many species in various
families in Brazil used under that name; Daly 1990).
In tropical America, copal usually refers to species of
Bursera, Dacryodes, and Protium, but it is also applied in
some instances to non-Burseraceae like Hymenaea, Jat-
ropha, Pinus and Rhus. Ritual uses of copal have been
documented as far back as the seventh century A.D. on the
Mayan stelae (monuments) at the ceremonial site of Nim Li
Punit, showing copal (in this case, Protium copal (Schltdl.
& Cham.) Engl. used to make sacred fires by the Maya, with
the belief that this sacred essence is the manifestation of the
Maya gods (Freidel et al. 1993).
Most copal from the genus Bursera comes from two
widely distributed Mexican species, Bursera bipinnata Engl.
and B. copallifera (Linares and Bye 2008), although the
resin of up to 30 species of this genus has been harvested as
copal since pre-Hispanic times (Purata 2008). For example,
B. bipinnata and B. stenophylla Sprague & L. Riley were
used by the Aztecs on the site of the Templo Mayor as an
adhesive molding material for figurines representing deities
and as spiritual offerings (Lucero-Gómez et al. 2014).
Currently, copal species are cultural and economic
resources valued as non-timber forest products (NTFPs). In
Mexico, the resin is burned during the celebration of the Day
of the Dead and the quantity and quality of the harvested
resin in Mexico has led to the suggestion that Bursera spe-
cies were domesticated in the past (Abad-Fitz et al. 2020).
Unfortunately, in some rural areas in Mexico, populations
13
D. C. Daly et al.
of copal are being depleted by overexploitation (Cruz-León
et al. 2006).
Another NTFP is represented by the alebrijes, the pop-
ular and expensive painted wood carvings of fantastical
animals made in southern Mexico from the soft, workable
wood of Bursera glabrifolia (H.B.K.) Engl. Populations of
this resource too have been under heavy pressure, but for-
tunately it was the model for a scientifically and socially
sound approach to resource management that appeared to be
working to conserve the species (Peters et al. 2003).
A South American copal, Dacryodes olivifera Cuatrec.,
is abundant in the Sumaco Biosphere Reserve in Napo,
Ecuador, where its resin is considered a promising NTFP.
As with other Burseraceae in Amazonia and beyond, it has
been widely used for illumination and to seal wounds, and
it is still used in religious ceremonies. There is international
demand for this resin, in the form of dried resin or incense
sticks, but its future as a sustainable economic activity is still
uncertain (Getahun et al. 2014).
In Vaupés on the upper Río Negro in Colombia, the
Kubeo people make a beverage from the mesocarp of
another species of Dacryodes, D. belemensis Cuatrec.,
known locally as ibapichuna (“black fruit;“ Zarucchi 1980).
For the Aguaruna Jívaro of Peru, the folk generic kunchai
corresponds to Dacryodes and they recognize four species,
all with a thin, oil-rich, edible pseudaril that is eaten raw or
roasted: númi kunchái (D. peruviana), wáwa kunchái and
múun kunchái (D. kukachkana L.O. Williams), tsáju kunchái
(D. nitens Cuatrec.) and újuts (Dacryodes sp.)(Jernigan
2006).
10 Chemistry and biological activity
In the past 10 years, a substantial amount of research has
been conducted on Burseraceae chemistry in the Americas,
especially in Bursera and Protium. Bursera graveolens has
promising antiacaricidal effects against larvae of the cattle
tick Rhipicephalous microplus (Rey-Valeirón et al. 2017)
and inhibits amastigotes of Leishmania amazonensis (Mon-
zote et al. 2012). Bursera copallifera showed cytotoxic
effects on breast cancer cell lines (Domínguez et al. 2018),
and the resin and essential oil of B. schlechtendalii Engl.
have strong repellence against Aedes aegypti, while the inha-
lation of its vapors had anxiolytic effects in mice (Villa-
Ruano et al. 2018).
Within Protium, the most-studied species is the wide-
spread “P. heptaphyllum;” again it should be noted that
the P. heptaphyllum complex contains at least eight line-
ages deserving of specific rank (Damasco et al. 2019,
2021). A review of the pharmacological effects of α‐ and
β‐ amyrin in this taxon describes its analgesic, anti‐inflam-
matory, anticonvulsant, antidepressive, gastroprotective,
A review of Neotropical Burseraceae
hepatoprotective, antipancreatitic, antihyperglycemic, and
hypolipidemic effects (Nogueira et al. 2019). Specifically,
“P. heptaphyllum” is considered promising as a leishmani-
cidal (Houël et al. 2015; Cabral et al. 2021), acaricidal (Pon-
tes et al. 2007), gastroprotective (Araújo et al. 2011), vas-
orelaxant (Mobin et al. 2017), cytotoxic (Siani et al. 1999),
antimicrobial (Bandeira et al. 2006), and antinociceptive
(Rao et al. 2007).
Biological activity of other Protium species of interest
include the antibacterial properties of the fresh resin of
Protium neglectum Swart (Suárez et al. 2007); the essential
oil activity against Fusarium spp. in vitro of P. colombi-
anum Cuatrec. (Carvajal et al. 2016); the antiproliferative
properties of P. ovatum Engl. against cancer cells (Alves
et al. 2020) and Chagas Disease (Estevam et al. 2018); the
repellent and lethal activity against the red spider mite,
Tetranychus urticae, of the essential oils of Protium bahi-
anum Daly and “P. heptaphyllum” (Pontes et al. 2007); and
the larvicidal activity of Protium spruceanum leaf extracts
against the Asian blue mite (Rhipicephalous microplus, a
cattle parasite; Figueiredo et al. 2019). In vitro studies of
promastigotes and amastigote-infected macrophages showed
that the α-pinene, p-cymene and 1,8-cineole present in P.
hebetatum and P. altsonii Sandwith have in vitro leishmani-
cidal activity (Santana et al. 2020).
The only species of Commiphora in the Neotropics,
C. leptophloeos, has antimicrobial and anti-inflammatory
properties (Medeiros 2019), including inhibitory properties
against methicillin-resistant Staphylococcus aureus (MRSA)
(Pereira et al. 2017) and its application to treat subclinical
mastitis in ruminants (Silva et al. 2019a, b). This species
also has bioactive compounds including (E)-caryophyllene
and α-humulene, which have been reported as oviposition
deterrents and larvicidals against Aedes aegypti (Silva et al.
2015).
11 Ecological implications of chemical
defenses in Burseraceae
The decade since 2011 witnessed a major research focus
on the ecological and evolutionary significance of chemi-
cal investment in Protium. Protium species endemic to
nutrient-poor white-sand forests were found to have greater
investment in synthesis of defensive compounds and slower
growth rates than Protium species occurring in nutrient-
rich clay terra firme rain forests, consistent with the idea
of a growth defense trade-off (Fine et al. 2004, 2006). The
amount and types of chemical investment also were found
to differ among different ecotypes of Protium subserratum
adapted to different soils, suggesting that the growth defense
trade-off and selection by different natural enemies could
be implicated in the speciation process (Fine et al. 2013;
Lokvam et al. 2015).
Building on these results, Salazar et al. (2018) con-
ducted a larger more comprehensive study of the chemical
defenses and insect herbivores associated with 31 Protium
species co-occurring in the Allpahuayo-Mishana National
Reserve near Iquitos, Peru. Over 800 juvenile individu-
als were monitored for 64 weeks, and over 4000 feeding
records were documented from over 230 insect species;
from these same plants the authors characterized close to
600 putative secondary metabolites. Chemical investment
in secondary metabolites by Protium was high, averag-
ing 40% of leaf dry weight (22–58%), and the metabolites
identified belonged to two main categories: (1) phenolics
(including procyanidins, flavone glycosides and chlo-
rogenic acids); and (2) terpenoids (including saponins,
monoterpenes, sesquiterpenes, and triterpenes).
Different Protium species expressed different chemi-
cals, and phylogenetic similarity was not a good predic-
tor of defense chemistry—in other words, closely related
species often showed high chemical divergence, which is
consistent with results reported from other highly diverse
genera of tropical woody plants (e.g., Bursera, Piper, and
Inga)(Becerra 2007; Kursar et al. 2009; Richards et al.
2015; Salazar et al. 2016). What is more, Protium and Bur-
sera species that co-occur with their congeners are more
likely to have divergent chemical defenses, consistent with
the hypothesis that plant species compete for “enemy-free
space” and can more easily coexist when they have fewer
shared enemies (Becerra 2007; Vleminckx et al. 2018).
The insects associated with feeding on Protium were
mostly hemipterans, coleopterans, and lepidopterans, and
most insects were generalists that fed on a large number of
different Protium species (average 11 species). Neverthe-
less, all herbivore species showed strong preferences for or
avoidance of particular Protium species. Using statistical
machine learning techniques, Salazar et al. (2018) identi-
fied 81 different chemical compounds that were implicated
in repelling individual herbivore species. These “herbi-
vore active metabolites” or HAMs were found in each
Protium species and the plants that had the most of these
HAMs had a lower number and diversity of insect herbi-
vores (Salazar et al. 2018). These results suggest that the
rich chemical diversity found in plants evolves because
although many compounds are active, each one is effec-
tive against only a few herbivore species, and plants are
attacked by a multitude of different enemy taxa with differ-
ent metabolisms and evolutionary histories. Future studies
will investigate the associations between fungal pathogens
and Protium secondary metabolites to learn more about
defense strategies of the entire plant (roots, leaves, stems)
across its ontogeny.
13

12 Burseraceae as a model organism
After many years of a collective research effort including a
diverse network of research groups, it is safe to say that the
Burseraceae comprise one of the most-studied plant fami-
lies. With regard to the Amazonian flora, many advances
have been observed since it was suggested that the Burser-
aceae be used as a model organism (Daly et al. 2012a, b).
Recent studies have addressed (1) use of new techniques
and multiple datasets in species delimitation; (2) cryptic
species within lineages whose morphological variation
has been overlooked; and (3) processes responsible for
the diversification and demography of Burseraceae line-
ages. The latter include the evolution of chemical defenses,
discussed above. The sections below address these topics
and discuss how future research can contribute to improv-
ing the field of tropical botany and systematics.
Species limits – Species limits in Neotropical Burseraceae
have been inferred mainly using morphological data cou-
pled with geographic distributions (e.g., Daly and Fine 2011;
Daly and Melo 2017; Daly and Martínez-Habibe 2019).
Besides the traditional morphological characters that empha-
size reproductive structures, leaf venation characters have
been gaining more attention and for the past decade have
been commonly incorporated into taxonomic descriptions
and diagnoses (e.g., Daly and Fine 2011; Andrés-Hernández
et al. 2012; Daly et al. 2015; Mitchell and Daly 2015; Daly
2018, 2019, 2020; Daly and Martínez-Habibe 2019), leading
to better species delimitations.
In the past decade, integrative approaches have improved
the understanding of species limits in a diverse array of
Burseraceae. Weeks and Tye (2009) merged the traditional
morphological approach with DNA markers and amplified
fragment length polymorphisms (AFLPs) for assessing the
phylogeography and taxonomic boundaries of two Bursera
species. Misiewicz and Fine (2014) examined morphological
and genetic data to investigate populations of Protium sub-
serratum growing parapatrically in three different habitats,
and they suggested that these populations were diverging in
an incipient process of habitat-mediated speciation. Misie-
wicz et al. (2020) expanded this investigation among para-
patrically distributed P. subserratum populations by combin-
ing reproductive biology, population genetics, ecology, and
species distribution modeling, revealing more evidence of
reproductive isolation of these populations.
Damasco et al. (2019, 2021) combined data from mor-
phology, phylogenomics and leaf spectroscopy to clarify
species limits within the P. heptaphyllum species complex
and reestablished P. cordatum Huber. Similarly, Perdiz
(2020) investigated species limits in the P. aracouchini
13
D. C. Daly et al.
species complex, revealing five new species (Perdiz et al., in
prep.), one of which has been published (Perdiz et al. 2020).
Despite the amount of taxonomic research on Neotropical
Burseraceae that has been published in the past decade since
Daly et al. (2011), some groups still need further investi-
gation into their species boundaries. For example, Perdiz
(2020) investigated Protium calanense Cuatrec., which
contains morphologically distinguishable populations from
four different geographical areas, one of them in the Bra-
zil's Atlantic Forest while the rest are found in the Amazon,
and concluded that they have undergone recent speciation
(Perdiz 2020).
Cryptic diversity – Cryptic species are characterized as
such because they are difficult to distinguish morphologi-
cally, and often they are initially detected only with the aid
of molecular data (Bickford et al. 2007; Pinheiro et al. 2018).
One can expect to find numerous cases of cryptic diversity
in the highly diverse tropics, especially in groups like Ama-
zonian Protieae that have speciated recently and rapidly
(Weeks et al. 2014).
Some recent investigations have reinforced this expecta-
tion. Using morphological, geographical and habitat prefer-
ence data, Daly (2020) described three new species from
Protium sect. Tetragastris, two of which had been frequently
confused under P. altissimum (Aubl.) Marchand while the
other had been included within P. stevensonii (syn.: Tetra-
gastris panamensis) during the preceding 18 years. Simi-
larly, Perdiz et al. (2020) described P. santamariae Perdiz,
Daly & P. Fine, an entity that had been included within P.
aracouchini for more than 30 years.
Novel technologies are being developed and tested
to improve and accelerate the detection and diagnosis of
cryptic diversity in plant groups that have relatively well-
established baseline taxonomy. Near-infrared spectroscopy
(FT-NIR) has the potential to discriminate Amazonian tree
species through their spectral signatures (Durgante et al.
2013). Using Burseraceae-Protieae trees as a model, Lang
et al. (2015) concluded that FT-NIR has great potential for
identifying plant species in the field even at different ontoge-
netic stages. More recently, Draper et al. (2020) proposed
the use of artificial intelligence (AI) to generate an integra-
tive framework that includes several disparate data sources
(e.g., spectroscopy, DNA sequences, image recognition,
and morphological data). These technologies offer potential
solutions for improving and accelerating plant identifica-
tion techniques and the resolution of cryptic species (Draper
et al. 2020).
Although still scarce, explicit species delimitation studies
in an integrative framework have provided strong evidence
that the number of cryptic, unpublished species in Neo-
tropical Burseraceae is significantly greater than previously
thought, as evidenced by two studies cited above that alone
A review of Neotropical Burseraceae
revealed a total of 11 new species requiring description
(Damasco et al. 2019, 2021; Perdiz 2020). In addition, Daly
et al. (2020) estimated ca. 60 undescribed species of Protium
already represented in herbaria, a well-known phenomenon
for flowering plants in general (Bebber et al. 2010), and
ca. half of these species are Andean endemics from under-
collected montane forests (Daly et al. 2020). It is therefore
reasonable to expect that a more thorough inventory of the
Neotropical flora, coupled with more refined integrative
studies, will reveal many more new species “hidden in plain
sight” due to cryptic diversity.
Hyperdominant lineages in Burseraceae – Plant species
are not distributed evenly across space, and natural habitats
can harbor contrasting patterns of community structure and
species abundance. For instance, Amazonian forests harbor
greater plant diversity than most other forests across the
globe, nonetheless tree communities are structured in a way
that relatively very few species are extremely abundant (ca.
2% out of ~ 12,000 species), the so-called hyperdominants
(e.g., ter Steege et al. 2013), while the great majority are
rare. This unbalanced distribution of individuals across spe-
cies has captured the interest of many tropical ecologists, but
still the causes of the hyperdominance phenomenon in Ama-
zonian forests have not been fully examined, and in some
instances what appear to be single hyperdominants can prove
to be cryptic species complexes.
Patterns of hyperdominance have been extensively
described in Amazonia since Pitman et al. (2001) reported
“species oligarchy” in Peruvian and Ecuadorian forests (Pit-
man et al. 2013). In that first report, Burseraceae was listed
among the families with exceptional numbers of abundant
tree species. A synthetic study led by the ATDN (Amazon
Tree Diversity Network) analyzed ten years of data from
1430 tree-inventory plots distributed across the entire Ama-
zon Basin and highlighted the hyperdominance phenomenon
on a broader geographical scale (ter Steege et al. 2013). Of a
list of ca. 5000 confirmed species in the Amazon tree flora at
the time, Burseraceae was the seventh most abundant family,
accounting for approximately 24.2 billion trees, of which 11
species were ranked as hyperdominants. In addition, Protium
is listed among the top five most abundant genera, therefore
Burseraceae lineages are expressively relevant for future
research aiming to reveal the ecological and evolutionary
mechanisms that favor the unbalanced abundance of Ama-
zonian tree taxa.
Plant species could be successfully dominant for many
reasons, and they usually harbor an array of life history
traits that directly favors survival, reproduction and dis-
persal over other taxa. Members of the Burseraceae usu-
ally produce fruits that are attractive to a diverse group of
dispersers, including mammals and birds (see “Dispersal”
section), and many species are capable of producing a dense
number of seeds, which may optimize widespread dispersal
and enhance chances of habitat colonization. In addition, a
few widespread Burseraceae species maintain continuous
distributions over long distances via riparian forest habitats
(e.g., Protium spruceanum). None of these arguments serve
to distinguish hyperdominant Burseraceae from other abun-
dant lineages, however. More plausible arguments may well
not involve reproductive factors. Investment in synthesiz-
ing chemical defense compounds represents a fundamental
survival strategy against natural enemies. Previous results
on Protium lineages strongly supported the existence of a
growth defense trade-off, and chemical investment across
Burseraceae species is well-known to be high and diverse
(see “Ecological importance” section on Ecological Implica-
tions of Chemical Defenses). Future studies will investigate
whether the hyper-abundance of Burseraceae trees can be
linked to the presence of chemical compounds considered
active against herbivores and pathogens.
An important caveat must be reiterated here in relation
to the hyperdominance phenomenon. By the estimates of
the ATDN (ter Steege et al. 2013), Protium altissimum
(cited as Tetragastris altissima) was considered the sec-
ond most hyperdominant tree species in the entire Amazon
region (third most in Piva et al. 2020), but a recent study
revealed that it actually corresponds to three species, one
abundant in parts of central and eastern Amazonia and the
Guianas, one abundant in southwestern Amazonia, and one
native to the Cerrado of Central Brazil (Daly 2020). Simi-
larly, P. heptaphyllum, seemingly ubiquitous in many parts
of northern South America (see “Ecological importance”
section), has been shown to refer to at least eight species,
most geographically restricted and each apparently adapted
to distinct soil and climatic conditions; similarly, the abun-
dant P. aracouchini complex refers to at least five species
(Damasco et al. 2019, 2021; Perdiz 2020).
It is clear that a number of hyperdominants are not nearly
as dominant as proposed, still it is likely that many sites
across a number of Neotropical biomes are dominated by
one or a few taxa of hyperdominance complex. In the P.
heptaphyllum complex, for example, abundance values of
P. “aromaticum” Engl. sensu Damasco et al. (2021) were
extremely high relative to other tree species in different
fragments of seasonally dry forests in the Pantanal (Stavis
et al. 2020), woodland savannas in the Brazilian Cerrado
(Cândido et al. 2016), riparian and moist forests (Silva et al.
2012; Oliveira Junior et al. 2014; Lima et al. 2019), and
white-sand restingas of Brazil’s Atlantic forest (Giaretta
et al. 2013; Santos et al. 2015; Machado and Almeida Jr.
2019).
13

13 Key to the new world genera
of Burseraceae
1 Branches and trunk Beiselia
armed with later-
ally compressed,
cuspidate protuber-
ances formed by
persistent swollen
petiole bases;
secondary leaflet
venation craspe-
dodromous; fruit
a pseudocapsule
with 10(12) narrow
valves dehisc-
ing to release as
many pyrenes, the
pyrenes com-
pressed and distally
winged, the wings
parallel to radii
of the fruit axis;
endemic to Micho-
acán, Mexico
– Branches and trunk 2 with 1 plurilocular
unarmed except
sometimes with
thorny short shoots
(Commiphora
leptophloeos, some
Bursera); second-
ary leaflet venation
diverse, only rarely
craspedodromous;
fruit a compound,
indehiscent or
dehiscent drupe,
the latter releas-
ing 1–5 pyrenes
slightly compressed
perpendicular to
radii of the fruit
axis; not restricted
to Michoacán
13
D. C. Daly et al.
2 Pulvinulus present 3
at least on terminal
petiolule, plants
evergreen
– Pulvinuli lacking 5
altogether, plants
deciduous or ever-
green
3 Flowers Protium pro maxima
(3–)4–5-merous, parte
when trimerous
the petals fleshy
and cucullate
(Protium sect. Sar-
coprotium); fruit
dehiscent, with 1–5
unilocular pyrenes,
each pyrene
overlain by a sweet,
spongy, white
or red pseudaril;
cotyledons plano-
convex or lobed,
often the latter
contortuplicate
– Flowers 3-merous; 4
fruit indehiscent
and drupaceous,
pyrene, 1–3 locules
developing; coty-
ledons palmatifid
or palmate (tribe
Canarieae)
4 Often one or both Trattinnickia
surfaces of leaflets
aspereous; flowers
3–5 mm long;
petals connate
more than half
their length, (sub)
erect, fleshy, the
abaxial surface
provided with
retrorse-appressed
hairs; stigmas (sub)
sessile, style mostly
obsolete; fruits
globose to ovoid
or umbonate, not
oblique, the endo-
carp bony, tubercu-
late, with 2–3 equal
lobes and horned
at apex, the locules
not separable
A review of Neotropical Burseraceae

– Leaflet surface only Dacryodes – Freely ending 6

rarely asperous; veinlets usually
flowers 1–2 mm highly branched,
long; petals free marginal ultimate
(fused at base in venation incom-
Dacryodes con- pletely looped;
nata), membrana- snail-shaped
ceous, retrorse glands absent;
hairs absent; style flowers sometimes
evident in flower; perfect, perianth
fruits ellipsoid 3–5-parted, very
(rarely globose) rarely haploste-
and usually slightly monous; ovary
oblique, the 2–3-locular and
endocarp cartilagi- stigma lobes 2–3;
nous and smooth, pyrenes 1(–2), very
not lobed nor rarely 3, connate,
horned, the aborted basifixed, pseudaril
locule(s) strongly fleshy and bright
compressed and red, yellow, or
forming an articu- orange; cotyledons
lated, separable palmatifid and
plate on periphery folded or contortu-
of pyrene plicate
5 Freely ending Protium sect. Crepi- 6 Branches often Commiphora
veinlets on leaflets dospermum thorny due to mod-
0–2-branched, ified short shoot
marginal ultimate apices; calyx cupu-
venation looped; lar to bell-shaped,
most surfaces lobes closed in
with snail-shaped bud, antepetalous
glands; flowers stamens usually
always unisexual, much shorter than
perianth 5-parted, antesepalous ones;
often haploste- pseudaril rarely
monous; ovary covering pyrene
5-locular and entirely, its arms or
stigmas (or stigma lobes (when pre-
lobes) 5; pyrenes sent) occurring on
1–5, separated by a sutures as well as
columella, covered on 1 or both faces;
with a white, in the Neotropics
spongy, sweet occurring in NE
pseudaril; after and C Brazil, E
dehiscence the Bolivia, Orinoco
pyrenes tenuously Basin of Venezuela
suspended from – Branches only rarely Bursera
fruit apex by an thorny; calyx
inverted V-shaped saucer-shaped to
structure; cotyle- shallowly cupular,
dons plano-convex the lobes open
and uncinately (apert) in bud, two
curved to form series of stamens
a J- or U-shaped (sub)equal; arillate
structure structures, when
not covering pyrene
entirely, with arms
on the sutures but
never on the faces;
Mexico and Carib-
bean south to Peru,
Ecuador, and N and
C Brazil

13
 D. C. Daly et al.

14 Genus descriptions for Neotropical
Burseraceae
Beiselia Forman (Fig. 2).
Beiselia Forman, Kew Bull. 42: 262 (1987).
Small dioecious trees or shrubs. Older bark gray and
peeling, trunk armed with laterally compressed, cuspidate
protuberances formed by persistent petiole bases. Leaves
deciduous, exstipulate, lateral leaflets sessile, leaflet
margin coarsely dentate to slightly serrate. Secondary
venation craspedodromous, strong intersecondaries often
present, opposed intercostal tertiaries freely branching and
meeting only at higher ranks. Inflorescences axillary, pseu-
doracemose, cymules on female inflorescences usually
reduced to solitary flowers. Flowers pedicellate. Perianth
5(–6)-parted, calyx apert (open) in bud, corolla valvate,
petals free. Androecium of 2 subequal series, stamens free
and inserted outside base of intrastaminal annular disk; in
staminate flowers the disk and pistillode fused to form a
broadly conical, parenchymatous ovariodisk; staminodes

Fig. 2  Beiselia mexicana Forman. A Leaf. B Leafless shoot with pendent infructescences, showing persistent spinose petiole bases. C Fruit with
valves falling away. D Fruit with valves fallen away and pyrenes in different stages of release, in lateral (above) and apical (below right) views. E
Pyrenes in lateral and dorsiventral views (A–E from Taylor 516, NY 4204148)

13
A review of Neotropical Burseraceae
in pistillate flowers present but significantly reduced.
Gynoecium 10(–12)-locular and slightly 10(–12)-lobed,
stigma subsessile, discoid, persistent. Fruit a pseudo-
capsule, ovoid-oblong, septicidal, each of 10(12) narrow
valves dehiscing acropetally to release a pyrene sepa-
rated by a wing of the columella, the pyrenes oblong and
compressed parallel to radii of the fruit axes and distally
winged. Cotyledons flat, entire, accumbent, radicle api-
cal and small. Germination epigeal, cotyledons opposite,
entire, first eophylls simple. N = 13.
One species endemic to dry forests in Michoacán,
Mexico.
Bursera Jacq. ex L. (Fig. 3).
Bursera Jacq. ex L., Sp. Pl. ed. 2, 1: 471 (1762), nom.
cons.
Elaphrium Jacq. (1760).
Terebinthus P. Browne (1756).
(Polygamo-)dioecious shrubs to large trees or suffrutices,
sometimes caudiciform, rarely (B. standleyana) epiphytic
or lithophytic. Bark papery and peeling (then usually red-
dish or yellowish, subgenus Buntingia and most of subge-
nus Bursera) or close (then (reddish-)gray, most Caribbean
Bursera and subgenus Elaphrium (syn: sect. Bullockia)).
Resin clear, translucent, or white (subgenus Buntingia).
Branchlets usually unarmed (rarely with thorns terminat-
ing short shoots). Cataphylls sometimes present (some sub-
genus Elaphrium). Leaves usually clustered near branchlet
apices, exstipulate, usually deciduous, often flushing dur-
ing or after anthesis; imparipinnately compound or some-
times unifoliolate or apparently simple, rarely bipinnate;
rachis often winged in subgenus Elaphrium; petiolules
lacking pulvinuli. Leaflet margin entire (subgenera Bursera
and Buntingia), crenate, or dentate (subgenus Elaphrium).
Secondary venation (festooned-)brochidodromous, (semi-)
craspedododromous, or cladodromous; intersecondaries
sometimes present (subgenus Bursera); intercostal tertiar-
ies alternate-percurrent or admedially ramified or random-
reticulate, rarely opposing tertiaries meeting only at higher
orders (e.g., B. kerberi Engl.); freely ending veinlets some-
times highly branched, often terminating in tracheoid idi-
oblasts or sometimes highly branched out of the plane of the
other veins. Inflorescence an axillary or subterminal pani-
cle of cymes, sometimes pseudospicate, pseudofasciculate,
or pseudoracemose. Flowers functionally unisexual or less
often bisexual. Staminate flowers (3–4)5-parted in subge-
nus Bursera, 4-parted in subgenus Elaphrium (unknown for
subgenus Buntingia). Pistillate and hermaphroditic flow-
ers 3-parted in subgenus Bursera, 4-parted in subgenus
Elaphrium, 5-parted in subgenus Buntingia. Receptacle flat
to saucer-shaped (rarely cup-shaped), sometimes forming
a hypanthium in staminate flowers. Calyx usually divided
almost to base, aestivation apert (open); petals free, indu-
plicate-valvate at apex but slightly imbricate along sides,
white, green, yellow, or rarely reddish, rarely cucullate (B.
schlechtendalii), usually with a thickened, inflexed apicu-
lum. Flowers either diplostemonous with the stamens and
staminodes in 2 usually subequal series (staminodes in 3
series in subgenus Buntingia). Pollen (most species): out-
line in polar view strongly triangular-lobed, shape spheroidal
or prolate-spheroidal. Disk intrastaminal, usually annular,
sometimes adnate to hypanthium when latter present. Pis-
tillode greatly reduced, with rudimentary locules and ovules,
or sometimes spindle-shaped and parenchymatous, occa-
sionally obsolete. In pistillate flowers, staminodes present
and reduced. Gynoecium 3-carpellate (subgenera Bursera
and Buntingia) or 2-carpellate (subgenus Elaphrium); style
usually short, stigmas or stigma lobes 3–2 (1 capitate stigma
in subgenus Buntingia), or the style shortly 3–2-branched;
the stigmas capitate, discoid, or elongate. Fruit a septicidally
dehiscent compound drupe, pericarp fleshy to coriaceous,
ellipsoid to ovoid (obovoid in B. inversa Daly) or subglo-
bose, often slightly oblique, maturing green or reddish(-
brown) or reddish; at dehiscence 2–3 valves (equaling the
number of developing locules) dehisce acropetally, expos-
ing the basifixed compound pyrene; pyrene cartilaginous
to bony, either fully enveloped by a brightly colored (red,
orange, or yellow), fleshy, arillate structure (subgenera Bur-
sera and Buntingia), or the arillate structure partially cover-
ing the pyrene from the base and extending arms or lobes
up the sutures (most of subgenus Elaphrium); 1 locule or
rarely 2(3) developing a seed, the other(s) abortive and either
developed but seedless (subgenus Buntingia) or compressed
and shorter, these not separable from fertile locule(s) but
often distinguishable by a ridge or furrow. Testa membrana-
ceous, cotyledons usually multi-lobed, otherwise unlobed
and erose (subgenus Buntingia) or palmately 3-lobed,
folded. Germination epigeal, phanerocotylar, first eophylls
alternate and simple or trifoliolate. N = 12.
Approx. 125 species, SW U.S., Mexico (center of diver-
sity), Central America, Caribbean, Colombia, Venezuela,
Trinidad, Guyana, SW Ecuador, NW Peru, N and C Brazil
(Roraima, Goiás), and possibly Vietnam (Bursera tonkinen-
sis Engl., incertae sedis).
Commiphora Jacq. (Fig. 4)
Commiphora Jacq., Pl. Hort. Schoenbr. 2: 66, t. 249
(1797), nom. cons.
Balsamodendrum Kunth (1824).
Hemprichia Ehrenb. (1829).
Heudelotia A. Rich. (1831).
Hitzeria Klotzsch (1861).
Spondiopsis Engl. (1895).
13
 D. C. Daly et al.

Fig. 3  Bursera pereirae Daly. A Habit and bark. B Branchlet with detail of rachis and leaflet bases. C Leafless flowering branchlet. D Bud. E
Staminate flower at anthesis; longisection of same with two petals and four stamens removed (at left) and pistillode (extreme left). F Adaxial
view of petal and ventral view of stamen (at left), lateral view of stamen (right). G Part of infructescence (above) and dehiscing fruit (A from
field photographs of Pereira & Alvarenga 3216, NY; B from Pereira & Alvarenga 3007, NY; C–F from Pereira & Alvarenga 3216, NY; G from
Pereira & Alvarenga 3658, NY)

13
A review of Neotropical Burseraceae

Fig. 4  Commiphora leptophloeos (Engl.) J.B. Gillett. A Papery bark. B Leaves. C Leafy branch with thorns. D flowering branchlet. E Flowering
branchlet with thorn. F Flower bud (left) and portion of inflorescence with open flower (right). G Longisection of staminate flower with stamens
from two series (left) and adaxial side of flower (right). H Fruiting branchlet. I Opened fruit in dorsiventral and lateral views. J Dorsiventral
view of pyrene (A from Zappi 3272, NY 02218629; B from Zappi & Harley 16309, NY 00608700; C from Parada 841 NY 04204147; D–G
from Pirani 1199, NY 00929435; H–I from Atkins 5090, NY 01016404; J from Pereira 3013, NY 00929360.)

(Polygamo-)dioecious shrubs or small trees. Bark papery branches often armed, the thorns modified axillary short
and peeling; resin usually aromatic and drying gummy; shoots or shoot apices. Leaves usually clustered near branch-
let apices, deciduous, exstipulate, often flushing during or

13
 D. C. Daly et al.

Fig. 5  Dacryodes amplectans Daly & M.C. Martínez. A Inflorescence and petiole. B Lateral view with 2 petal removed and view in plan of
staminate flower. C Longitudinal section of staminate flower with corolla removed, lateral view of staminate flower with perianth removed, and
(below) ovariodisk and one stamen. D Adaxial view of stamen. E Infructescence and immature fruits. F Adaxial view of petal and lateral view
of pistillate flower with one petal removed. G Lateral view of pistillate flower with perianth removed and longitudinal section of pistillate flower.
H Adaxial view of staminode. I Portion of infructescence (A–D from Daly et al. 6016, NY; E–H from Aymard & Delgado 6898, NY; I from
Treacy & Alcorn 289, F)

13
A review of Neotropical Burseraceae

Fig. 6  Protium hebetatum Daly. A Flowering branchlet. B Portion of pistillate inflorescence. C Pistillate flower. D Pistillate flower with three
petals removed, plus adaxial view of petal (upper left) and adaxial view of staminode (upper right). E Longisection of pistillate flower. F Stami-
nate flower (right) with adaxial view of petal (left). G Staminate flower with three petals removed. H Disk and pistillode (left), longisection of
staminate flower (center), and lateral and adaxial views of stamen (right). I Fruit. J Longisection of fruit. K Ventral and lateral views of pyrene
(A–D from Bernardi (tree no.) 2/1, NY; B–E from Clark et al. 7079, NY; F–H from Daly et al. 4100, NY; I–J from Daly et al. 5644, NY; K
from Bernardi (tree no.) 1/61, NY)

13
 D. C. Daly et al.

Fig. 7  Trattinnickia zickeliana M.F.F. Melo & Daly. A Leaf. B Portion of inflorescence and detail of leaflet margin (inset lower left). C Portion
of staminate inflorescence. D Staminate flower (right) and same with part of calyx and corolla removed. E Ovariodisk and four of the six sta-
mens. F Dorsal and ventral views of stamens. G Infructescence (A–F from Prance et al. 20,111, NY; G from Freitas 17, NY)

13
A review of Neotropical Burseraceae
after anthesis, imparipinnate or sometimes trifoliolate; rachis
unwinged (terete); petiolules lacking pulvinuli; leaflet mar-
gin entire or sparsely serrulate. Inflorescence an axillary or
subterminal panicle of cymes. Flowers unisexual or rarely
some flowers bisexual, 4-parted; calyx cupular to slightly
campanulate, closed in bud, partly synsepalous but lobed;
corolla (induplicate-)valvate at apex but often imbricate
along sides, usually with an inflexed apiculum; stamens in
two markedly unequal series, inserted outside base of or
on top of an intrastaminal annular disk, the disk forming a
shallow hypanthium with the calyx; pistillode rudimentary
or obsolete; gynoecium 2(rarely 3-)carpellate, style short,
stigma 2-lobed. Fruit a compound drupe with fleshy to coria-
ceous pericarp, septicidally dehiscent by 2 (sometimes 4,
very rarely 3) valves, exposing a basifixed compound pyr-
ene, enveloped basally by a brightly colored, fleshy, arillate
structure that extends lobes up the sutures and usually the
faces also; 1(–2) locule(s) developing a seed and usually
1 abortive. Testa membranaceous; cotyledons palmately
3-lobed or multi-lobed and flat or folded. Germination phan-
erocotylar, the first eophylls opposite and simple. N = 13.
One species in S Venezuela, C and NE Brazil, E Bolivia,
plus approx. 185 spp. in Africa, Madagascar, Arabia, penin-
sular India, Sri Lanka, Vietnam, Pakistan, and Iran.
Dacryodes Vahl (Fig. 5).
Dacryodes Vahl, Skr. Naturhist.-Selsk. 6: 115 (1810).
Pachylobus G. Don (1832).
Canarium sect. Africana Engl. in A. DC. & C. DC.
(1883).
Canarium sect. II, ser. 4 Tenuipyrena Engl. in A. DC. &
C. DC. (1883), pro parte.
Curtisina Ridl. (1920).
Hemisantiria H. J. Lam (1929).
Dioecious trees, sometimes with plank buttresses and less
often with stilt roots or flying buttresses. Outer bark tan to
(reddish) brown or (pale) gray, smooth or somewhat rough due
to scales or raised lenticels, relatively thin and shed in irregu-
lar plates; inner bark orange, yellowish-white or pink. Resin
clear or somewhat milky, drying as opaque, brittle globules,
often aromatic. Leaves evergreen, exstipulate, imparipinnately
compound, rachis often rhombic in cross-section, pulvinuli
apparent usually on terminal petiolules, sometimes on lateral
petiolules; leaflet margin entire; abaxial surface very rarely
asperous; leaflets drying black in some species; secondary
venation usually festooned-brochidodromous, intersecondar-
ies usually present (parallel to secondaries or perpendicular
to midvein), intercostal tertiaries alternate-percurrent or ran-
dom-reticulate; fimbrial vein usually present. Inflorescence
an axillary or sometimes (pseudo-)terminal panicle of cymes,
secondary axes reduced in some species. Flowers 3-parted,
calyx (shallowly) cupular to urceolate, truncate or 3-lobed,
sometimes divided nearly to base. Petals free (connate at
base in D. connata), aestivation induplicate-valvate at apex,
on sides valvate or slightly imbricate at anthesis, usually green
or pale yellow but sometimes red or whitish, with an inflexed
apiculum, spreading to patent at anthesis. In staminate flowers
the stamens in two subequal series, inserted outside base of
disk or on the sides or rim, anthers continuous with the fila-
ments or less often sagittate. Annular disk usually present;
pistillode either reduced but provided with locules and ovules,
or a variously shaped parenchymatous structure, or reduced
to a rudiment, or the disk and pistillode replaced by a coni-
cal ovariodisk. Staminodes reduced in pistillate flowers. Pis-
til 2–3-locular, style short and thick, stigma 2–3-lobed. Fruit
an indehiscent, compound drupe, variously colored, slightly
(oblique-)ovoid or ellipsoid or rarely subglobose, exocarp
thin and drying wrinkled, mesocarp thin and oily-resinous,
sometimes edible. Endocarp (thinly) cartilaginous, smooth,
not lobed; pyrenes 1(–2)- seeded, the 1–2 aborted locules
strongly compressed, forming an articulated, separable plate
on periphery of pyrene. Testa smooth, cotyledons palmate
or up to 13-palmatifid; folded or contortuplicate. Germina-
tion usually epigeal and phanerocotylar (rarely hypogeal and
cryptocotylar, e.g., D. excelsa), the first eophylls opposite or
alternate and simple or trifoliate.
As currently circumscribed (including African and Asian
species), ca. 1004 species in the moist tropics, of which 53
are Neotropical, usually lowland but some montane.
Protium Burm.f. (Fig. 6).
Protium Burm. f., Fl. Indica 88 (1768).
Icica Aubl. (1775).
Hedwigia Sw. (1788).
Tetragastris Gaertn. (1802).
Marignia Commers. ex Kunth (1824).
Crepidospermum Hook.f. in Benth. & Hook. f. (1862).
Icicopsis Engl. (1874).
Hemicrepidospermum Swart (1942).
Dioecious, unarmed (except Protium melinonis Engl. and
juvenile P. javanicum), small to large trees or rarely shrubs,
usually displaying Rauh's architectural model (Hallé et al.
1978), buttresses often present, bark usually smooth or less
often thick and fissured and shed in large irregular plates
on older trees (e.g., sect. Tetragastris). Resin translucent or
milky, usually aromatic, usually flammable when dry and
sometimes also when fresh. Leaves alternate (sometimes
appearing opposite in P. unifoliolatum), sometimes conferted
distally on branchlets (sect. Crepidospermum), evergreen,
exstipulate. Leaves imparipinnate or rarely unifoliolate, a pul-
vinulus present at the apex of the terminal petiolule (except
sect. Crepidospermum) and usually at distal or both ends of
lateral petiolules; leaflet margin entire or serr(ul)ate, rarely
with glandular-tipped teeth (Protium cuneifolium). Secondary
13

vein framework some form of brochidodromous (here includ-
ing semi-craspedodromous); venation usually highly organ-
ized, with strong areolation; intersecondary veins sometimes
present; admedial tertiaries sometimes present, diverse in ori-
gin; freely ending veinlets (FEVs) may be absent (i.e., areoles
empty), or little-branched, or highly branched; termination
can be simple, or tracheoid idioblasts, or highly branched
sclereids. Inflorescence an axillary or subterminal panicle of
cymes, sometimes pseudofasciculate or pseudospicate (then
the flowers (sub-)sessile). Receptacle flat to shallowly cup-
shaped. Perianth 4–5-parted (most staminate flowers 3-parted
in Protium sect. Sarcoprotium). Calyx partially synsepalous
but lobed, valvate; corolla apopetalous or sometimes partially
sympetalous (consistently so in sect. Tetragastris), aestivation
induplicate-valvate, petals abaxially white to pale green or
yellow, rarely red. Flowers usually obdiplostemonous with
the two series of stamens subequal, or the stamens pentady-
namous or tetradynamous, or sometimes the flowers haploste-
monous (staminate flowers of some sect. Crepidospermum
or pistillate flowers of some sect. Icicopsis). Filaments free,
anthers usually sagittate (continuous with filaments in stami-
nate flowers of sect. Tetragastris). Pollen diverse. Receptacle
flat to shallowly cup-shaped. Disk usually intrastaminal and
annular, not adnate to calyx, green or yellow; pistillode usu-
ally present in staminate flowers, usually containing locules
and reduced ovules, sometimes reduced to a parenchymatous
cylinder (e.g., sect. Sarcoprotium) or the disk and pistillode
fused to form a conical or discoid ovariodisk (sects. Icicop-
sis, Tetragastris). Pistil 4–5-locular, style 1, sometimes with
4–5 short lateral branches, stigmas 4–5, sometimes spiculate
(sects. Pepeanthos, Sarcoprotium). Fruit a compound dehis-
cent drupe (nuculanum), pendent or horizontal at maturity,
obliquely ovoid to subglobose or ellipsoid, maturing red or
less often green, orange, gray, or brown, pericarp (exo- and
mesocarp) fleshy to coriaceous or rarely sublignified, sep-
ticidally and acropetally dehiscent by 1–5 valves (equal to
the number of pyrenes developed), the valves white or pale
red within. Pyrenes separated by a columella, each tenuously
suspended from the fruit apex by an inverted V-shaped struc-
ture, pyrene cartilaginous to bony or rarely papery (Protium
divaricatum subsp. fumarium Daly), enveloped in a spongy,
sweet, white (very rarely red) pseudaril, ventral side with a
usually raised funicular scar of diverse shape and size, often
embossed; cotyledons lobed and contortuplicate, or simply
plano-convex and straight or uncinately curved, or (Protium
sect. Icicopsis) plano-convex plus laterally reverse twice-
plicate and then sometimes uncinately folded. Germination
through the apex of the pyrene, epigeal or hypogeal, phanero-
cotylar or cryptocotylar, first eophylls opposite or alternate,
simple, the margin entire or distally serrulate. N = 11.
As presently circumscribed, the genus is estimated to
have 205 species in the Neotropics, plus 4 in tropical Asia,
and 2 in Madagascar and Mauritius.
13
D. C. Daly et al.
Trattinnickia Willd. (Fig. 7).
Trattinnickia Willd., Sp. Pl., ed. 4 [Willdenow] 4: 975
(1806).
Medium-sized to large dioecious trees, less often small
trees, rarely shrubby, usually displaying Rauh's architectural
model (Hallé et al. 1978), some species capable of stump-
sprouting; lacking proper buttresses but roots often broad or
swollen at base of trunk. Outer bark thin and smooth in some
taxa, in most of sect. Rhoifoliae rough and shallowly to deeply
fissured and shed in irregular plates; hoop marks frequently
present. Resin clear and watery or oily (rarely reported as
white), slightly sticky, drying yellowish or white and hard,
flammable in some species. Leaves evergreen, exstipulate,
rachis usually rhombic in cross section, pulvinuli usually
apparent on lateral petiolules and almost always on the termi-
nal ones, pulvinuli often galled; usually one or both leaflet sur-
faces asperous, the margin entire; Secondary vein framework
festooned-brochidodromous, intersecondaries sometimes pre-
sent and then perpendicular to the midvein, intercostal tertiar-
ies alternate-percurrent (sometimes also admedially ramified),
composite admedial tertiaries sometimes present; fimbrial
vein present. Often (sect. Burserifoliae Swart) the vein are-
oles on the abaxial side defining papilla-filled laminar crypts.
Inflorescence an axillary, pseudoterminal, or terminal panicle
of cymes. Perianth 3-parted, green or wine-red (rarely report-
edly white to yellow). Calyx cupular, partlyl synsepalous but
3-lobed, aestivation valvate, sometimes invested with retrorse
hairs abaxially, calyx not persisting in fruit and often shed
as a unit; corolla of 3 partly to mostly connate petals, fleshy,
aestivation induplicate-valvate, usually (sub)erect with an
inflexed apiculum, both surfaces always with at least some
retrorse trichomes, adaxial surface often densely invested with
minute capitate glandular trichomes. Flowers diplostemonous,
stamens of two subequal series, filaments free, usually strap-
shaped, anthers often continuous with the filaments (i.e., not
sagittate), sometimes red. Pollen endoapertures (per-)lalon-
gate. Pistillode reduced to a conical parenchymatous structure
either surmounting the intrastaminal disk or the two fused to
form an ovariodisk, the stamens inserted at or near the base. In
pistillate flowers staminodes reduced, inserted on rim of a thin
annular disk. Gynoecium 2–3-locular, style short, stigma 1,
2–3-lobed. Fruit a compound, indehiscent drupe, depressed-
globose to depressed-ovoid, maturing blue-black to (purplish)
black, mesocarp oily and resinous. Pyrene bony, 2–3-locular
and 2–3-lobed, tuberculate, with sutures between the lobes but
the carpels not separable, 2–3-horned at apex. Cotyledons pal-
matifid, germination epigeal, first eophylls simple, alternate,
and sparsely serrate.
A genus of 19 species, Costa Rica south to Brazil and
Bolivia (excluding the Caribbean).
A review of Neotropical Burseraceae
Acknowledgements D. C. Daly received general support from the Leo
Model Foundation, and fieldwork that contributed to this review of
the Burseraceae was supported by the National Science Foundation
(Grant No. 0918600), the Gordon and Betty Moore Foundation, the
Tinker Foundation, the Ford Foundation, the Overbrook Foundation,
the JRS Biodiversity Foundation, the Helmsley Charitable Trust, the
Beneficia Foundation, and the National Geographic Society. Herbarium
visits were generously hosted by ESALQ, GH, IAN, MEXU, RB, RON,
and SINCHI. P. V. A. Fine’s work on Burseraceae has been supported
by grants from the NSF (especially NSF DEB-0919567 and DEB-
1254214) and the National Geographic Society. PVAF would like to
thank fellow copaleros (besides the other coauthors) Italo Mesones,
Julio Sánchez, Tracy Misiewicz, Chris Baraloto and Diego Salazar for
sharing ideas and many good times in the field. R. O. Perdiz has been
supported by scholarships from the Coordenação de Aperfeiçoamento
de Pessoal de Nível Superior, Brazil (CAPES) (finance code 001) and
the Conselho Nacional de Desenvolvimento Científico e Tecnológico
(CNPq) (Process No. 142243/2015-9), and by the 2015 Alwyn H. Gen-
try Fellowship for Latin American Botanists, the 2016 Cuatrecasas
Fellowship Award, an ASPT Research Grant for Graduate Students
2017, and a 2018 IAPT Research Grant. Bobbi Angell executed the
superb botanical illustrations.
Author contributions DD contributed the study concept and design,
project administration, and supervision. All authors contributed to the
data curation, investigation, validation, and writing (both original draft
and editing).
Declarations
Conflict of interest The authors declare that they have no conflict of
interest.
References
Abad-Fitz I, Maldonado-Almanza B, Aguilar-Dorantes KM, Sánchez-
Méndez L, Gómez-Caudillo L, Casas A, Blancas J, García-Rod-
ríguez YM, Beltrán-Rodríguez L, Sierra-Huelsz JA, Cristians S,
Moreno-Calles AI, Torres-García I, Espinosa-García FJ (2020)
Consequences of traditional management in the production and
quality of Copal resin (Bursera bipinnata (Moc. & Sessé ex DC.)
Engl.) in Mexico. Forests 11:991. https://​doi.​org/​10.​3390/​f1109​
0991
Aguirre GA, Pollito PAZ (2011) Estructura y composición florística
de un bosque de terraza baja en Tambopata, Madre de Dios.
Biodivers Amaz 3:44–53
Albert B, Milliken W (2009) Urihi A: a terra-floresta Yanomami. Insti-
tuto Socioambiental & Institut de Recherche Pour le Développe-
ment, São Paulo
Almazán-Núñez RC, Eguiarte LE, Arizmendi MdC, Corcuera P (2016)
Myiarchus flycatchers are the primary seed dispersers of Bursera
longipes in a Mexican dry forest. Peer J 4:e2126. https://​doi.​org/​
10.​7717/​peerj.​2126
Alves CCF, Oliveira JD, Estevam EBB, Xavier MN, Nicolella HD,
Furtado RA, Tavares DC, Miranda MLD (2020) Antiproliferative
activity of essential oils from three plants of the Brazilian Cer-
rado: Campomanesia adamantium (Myrtaceae), Protium ovatum
(Burseraceae) and Cardiopetalum calophyllum (Annonaceae).
Braz J Biol 80:290–294. https://​doi.​org/​10.​1590/​1519-​6984.​
192643
Andrés-Hernández AR, Espinosa D, Fraile-Ortega ME, Terrazas
T (2012) Venation patterns of Bursera species Jacq. ex L.
(Burseraceae) and systematic significance. Plant Syst Evol
298:1723–1731. https://​doi.​org/​10.​1007/​s00606-​012-​0673-x
Araujo DAOV, Takayama C, Faria FM, Socca EAR, Dunder RJ, Manzo
LP, Luiz-Ferreira A, Souza-Brito ARM (2011) Gastroprotective
effects of essential oil from Protium heptaphyllum on experimen-
tal gastric ulcer models in rats. Rev Bras Farmacogn 21:721–729.
https://​doi.​org/​10.​1590/​S0102-​695X2​01100​50001​17
Bachelier JB, Endress PK (2009) Comparative floral morphology and
anatomy of Anacardiaceae and Burseraceae (Sapindales), with a
special focus on gynoecium structure and evolution. Bot J Linn
Soc 159:499–571. https://​doi.​org/​10.​1111/j.​1095-​8339.​2009.​
00959.x
Balée W, Daly DC (1990) Resin classification by the Ka’apor Indians.
Adv Econ Bot 8:24–34
Bandeira PN, Fonseca AM, Costa SMO, Lins MUDS, Pessoa ODL,
Monte FJQ, Nogueira NAP, Lemos TLG (2006) Antimicrobial
and antioxidant activities of the essential oil of resin of Protium
heptaphyllum. Nat Prod Commun 1:117–120. https://​doi.o​ rg/​10.​
1177/​19345​78X06​00100​207
Basnet K, Scatena FN, Likens GE, Lugo AE (1993) Ecological conse-
quences of root grafting in tabonuco (Dacryodes excelsa) trees
in the Luquillo Experimental Forest, Puerto Rico. Biotropica
25:28–35
Bates JM (1992) Frugivory on Bursera microphylla Burseraceae by
Wintering Gray Vireos (Vireo vicinior, Vireonidae) in the coastal
deserts of Sonora, México. Southwest Nat 37:252–258. https://​
doi.​org/​10.​2307/​36718​66
Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution
29:167–179. https://d​ oi.o​ rg/1​ 0.1​ 111/j.1​ 558-5​ 646.1​ 975.t​ b0082​ 4.x
Bebber DP, Carine MA, Wood JRI, Wortley AH, Harris DJ, Prance
GT, Davidse G, Paige J, Pennington TD, Robson NKB, Scotland
RW (2010) Herbaria are a major frontier for species discovery.
Proc Natl Acad Sci 107:22169–22171. https://​doi.​org/​10.​1073/​
pnas.​10118​41108
Becerra JX (2007) The impact of herbivore-plant coevolution on
plant community structure. Proc Natl Acad Sci 104:7483–7488.
https://​doi.​org/​10.​1073/​pnas.​06082​53104
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K,
Ingram KK, Das I (2007) Cryptic species as a window on diver-
sity and conservation. Trends Ecol Evol 22:148–155. https://​doi.​
org/​10.​1016/j.​tree.​2006.​11.​004
Cabral RSC, Fernandes CC, Dias ALB, Batista HRF, Magalhães LG,
Pagotti MC, Miranda MLD (2021) Essential oils from Protium
heptaphyllum fresh young and adult leaves (Burseraceae): chemi-
cal composition, in vitro leishmanicidal and cytotoxic effects. J
Essent Oil Res 33:276–282. https://​doi.​org/​10.​1080/​10412​905.​
2020.​18486​51
Calvillo-Canadell L, Rodríguez-Reyes OJ, Medina-Lemos R, Cevallos-
Ferriz SRS (2013) Eocene Bursera (Burseraceaea) in La Carroza
Formation, Mexico: a dry tropical flora member. Bol Soc Geol
Mex 65:631–643
Cândido JB, Lima DP, Teixeira PR, Souza PB (2016) Florística do
estrato arbustivo-arbóreo de uma área de Cerrado sensu stricto,
Gurupi, Tocantins. Encicl Biosf 13:1744–1752
Cárdenas D, González-Caro S, Duivenvoorden J, Feeley K, Duque A
(2017) Asymmetrical niche determinism across geological units
shapes phylogenetic tree communities in the Colombian Ama-
zonia. Perspect Plant Ecol Evol Syst 28:1–9. https://​doi.​org/​10.​
1016/j.​ppees.​2017.​06.​001
Cárdenas S, Echeverry-Galvis MÁ, Stevenson PR (2021) Seed dis-
persal effectiveness by oilbirds (Steatornis caripensis) in the
Southern Andes of Colombia. Biotropica 53:671–680. https://​
doi.​org/​10.​1111/​btp.​12908
Cardona LMF, Cantillo FA, Ojeda JB (2017) Composición florística
y estructura horizontal del bosque semideciduo micrófilo de la
13

reserva ecológica Siboney-Juticí, Cuba. Rodriguésia 68:315–
324. https://​doi.​org/​10.​1590/​2175-​78602​01768​203
Carvajal D, Alvarez R, Osorio E (2016) Chemical variability
of essential oils of Protium colombianum from two tropi-
cal life zones and their in vitro activity against isolates of
Fusarium. J Pest Sci 89:241–248. https://​d oi.​o rg/​1 0.​1 007/​
s10340-​015-​0667-x
Carvalho MR, Jaramillo C, de la Parra F, Caballero-Rodríguez D,
Herrera F, Wing S, Turner BL, D’Apolito C, Romero-Báez M,
Narváez P, Martínez C, Gutierrez M, Labandeira C, Bayona G,
Rueda M, Paez-Reyes M, Cárdenas D, Duque Á, Crowley JL,
Santos C, Silvestro D (2021) Extinction at the end-Cretaceous
and the origin of modern Neotropical rainforests. Science
372:63–68. https://​doi.​org/​10.​1126/​scien​ce.​abf19​69
Castro-Laportte M (2013) Propuesta de un nuevo subgénero para
el género Bursera Jacq. ex L. (Burseraceae), con comentarios
sobre Bursera inversa Daly. Ernstia 23:67–82
Centrella ML, Shaw SR (2013) Three new species of gall-associated
Allorhogas wasps from Costa Rica (Hymenoptera: Braconidae:
Doryctinae). Int J Trop Insect Sci 33:145–152. https://​doi.​org/​
10.​1017/​S1742​75841​30001​43
Chandler MEJ (1961) The lower Tertiary floras of southern England.
I. Paleocene floras, London Clay flora (supplement). British
Museum (Natural History), London
Chandler MEJ (1964) The lower Tertiary floras of southern England.
IV. A summary and survey of findings in the light of recent
botanical observations. British Museum (Natural History),
London
Charles-Dominique P (1991) Feeding strategy and activity budget of
the frugivorous bat Carollia perspicillata (Chiroptera: Phyllos-
tomidae) in French Guiana. J Trop Ecol 7:243–256. https://​doi.​
org/​10.​1017/​S0266​46740​00054​0X
Collinson ME (1983) Fossil plants of the London Clay. Oxford Uni-
versity Press, Oxford
Cruz León A, Salazar Martínez L, Campos Osorno M (2006) Anteced-
entes y actualidad del aprovechamiento de copal en la Sierra de
Huautla, Morelos. Rev Geog Agrícola 37:97–115
Custódio FA, Firmino AL, Pereira OL (2019) A new species of Rosen-
scheldia (Dothideomycetes) from Brazil. For Pathol 49:e12472.
https://​doi.​org/​10.​1111/​efp.​12472
Daly DC (1989) Studies in Neotropical Burseraceae. II. Generic lim-
its in New World Protieae and Canarieae. Brittonia 41:17–27.
https://​doi.​org/​10.​2307/​28075​83
Daly DC (1990) The genus Tetragastris and the forests of Eastern Bra-
zil: studies in Neotropical Burseraceae III. Kew Bull 45:179–194.
https://​doi.​org/​10.​2307/​41144​46
Daly DC (2011) Burseraceae. In: Idárraga Á, Ortiz R del C, Callejas
R, Merello M (eds) Flora de Antioquia: Catálogo de las Plantas
Vasculares, vol 2. Listado de las plantas vasculares del depar-
tamento de Antioquia. Editorial D’Vinni, Bogotá, pp 378–381
Daly DC (2014a) Burseraceae. In: Jørgensen PM, Nee MH, Beck SG
(eds) Catálogo de las plantas vasculares de Bolivia. Monographs
in systematic botany from the Missouri Botanical Garden. Mis-
souri Botanical Garden Press, St. Louis, pp 441–443
Daly DC (2014b) Dacryodes patrona, a new and endangered species
and new generic record for Central America. Studies in Neotropi-
cal Burseraceae XIX. Brittonia 66:307–310. https://​doi.​org/​10.​
1007/​s12228-​014-​9334-4
Daly DC (2014c) Bursera pereirae, a new species and generic record
for the Cerrado complex of Brazil. Studies in Neotropical
Burseraceae XVIII. Brittonia 66:186–190. https://​doi.​org/​10.​
1007/​s12228-​014-​9333-5
Daly DC (2018) Notes on the Burseraceae in central Amazonia,
including four new taxa. Studies in Neotropical Burser-
aceae XXVI. Brittonia 70:427–444. https://​doi.​org/​10.​1007/​
s12228-​018-​9537-1
13
D. C. Daly et al.
Daly DC (2019) A new identity for Tetragastris panamensis. Stud-
ies in Neotropical Burseraceae XXIX. Brittonia 71:345–346.
https://​doi.​org/​10.​1007/​s12228-​019-​09577-w
Daly DC (2020) New species of Protium sect. Tetragastris from the
Andes, the Brazilian Cerrado, and Amazonia. Studies in Neo-
tropical Burseraceae XXVIII. Brittonia 72:290–302. https://​
doi.​org/​10.​1007/​s12228-​020-​09616-x
Daly DC, Fine PVA (2011) A new Amazonian section of Protium
(Burseraceae) including both edaphic specialist and general-
ist taxa. Studies in Neotropical Burseraceae XVI. Syst Bot
36:939–949. https://​doi.​org/​10.​1600/​03636​4411X​604958
Daly DC, Fine PVA (2018) Generic limits re-visited and an updated
sectional classification for Protium (tribe Protieae) Studies in
Neotropical Burseraceae XXV. Brittonia 70:418–426. https://​
doi.​org/​10.​1007/​s12228-​018-​9533-5
Daly DC, Martínez-Habibe MC (2016) Seven new species of Dacry-
odes from western Colombia. Studies in Neotropical Burser-
aceae XXI. Brittonia 68:120–137. https://​d oi.​o rg/​1 0.​1 007/​
s12228-​015-​9405-1
Daly DC, Martínez-Habibe MC (2019) Ten new species of Dacryo-
des from Amazonia and the Guianas. Studies in Neotropical
Burseraceae XXIII. Brittonia 71:201–224. https://​doi.​org/​10.​
1007/​s12228-​018-​09564-7
Daly DC, Melo MF (2017) Four new species of Trattinnickia from
South America Studies in Neotropical Burseraceae XXII. Brit-
tonia 69:376–386. https://​doi.​org/​10.​1007/​s12228-​017-​9473-5
Daly DC, Cameron KM, Stevenson DW (2001) Plant systematics in
the age of genomics. Plant Phys 127:1328–1333
Daly DC, Harley MM, Martínez-Habibe MC, Weeks A (2011)
Burseraceae. In: Kubitzki K (ed) Flowering plants. Eudicots.
The families and genera of vascular plants, vol 10. Springer,
Berlin, pp 76–104
Daly DC, Fine PVA, Martínez-Habibe MC (2012a) Burseraceae: a
model for studying the Amazon flora. Rodriguésia 63:21–30.
https://​doi.​org/​10.​1590/​S2175-​78602​01200​01000​02
Daly DC, Neill D, Martínez-Habibe MC (2012b) An ecologically
significant new species of Dacryodes from the northern Andes
Studies in Neotropical Burseraceae XV. Brittonia 64:49–56.
https://​doi.​org/​10.​1007/​s12228-​011-​9206-0
Daly DC, Raharimampionona J, Federman S (2015) A revision of
Canarium L. (Burseraceae) in Madagascar. Adansonia 37:277–
345. https://​doi.​org/​10.​5252/​a2015​n2a2
Daly DC, Reynel-Rodríguez CA, Fernández-Hilario R (2020) A new
Andean species of Protium. Studies in Neotropical Burser-
aceae XXIX. Brittonia 72:419–423. https://​doi.​org/​10.​1007/​
s12228-​020-​09636-7
Daly DC (1987) A taxonomic revision of the genus Protium (Burser-
aceae) in eastern Amazonia and the Guianas. Ph.D. thesis, City
University of New York
Damasco G, Daly DC, Vicentini A, Fine PVA (2019) Reestablish-
ment of Protium cordatum (Burseraceae) based on integrative
taxonomy. Taxon 68:34–46. https://​doi.​org/​10.​1002/​tax.​12022
Damasco G, Baraloto C, Vicentini A, Daly DC, Baldwin BG, Fine
PVA (2021) Revisiting the hyperdominance of Neotropical
tree species under a taxonomic, functional and evolution-
ary perspective. Sci Rep 11:9585. https://​d oi.​o rg/​1 0.​1 038/​
s41598-​021-​88417-y
Demarchi LO, Scudeller VV, Moura LC, Dias-Terceiro RG, Lopes A,
Wittmann FK, Piedade MTF (2018) Floristic composition, struc-
ture and soil-vegetation relations in three white-sand soil patches
in central Amazonia. Acta Amazon 48:46–56. https://d​ oi.o​ rg/1​ 0.​
1590/​1809-​43922​01603​523
De-Nova JA, Medina R, Montero JC, Weeks A, Rosell JA, Olson
ME, Eguiarte LE, Magallón S (2012) Insights into the histori-
cal construction of species-rich Mesoamerican seasonally dry
tropical forests: the diversification of Bursera (Burseraceae,
A review of Neotropical Burseraceae
Sapindales). New Phytol 193:276–287. https://​d oi.​o rg/​1 0.​
1111/j.​1469-​8137.​2011.​03909.x
Domínguez F, Maycotte P, Acosta-Casique A, Rodríguez-Rodríguez
S, Moreno DA, Ferreres F, Flores-Alonso JC, Delgado-López
MG, Pérez-Santos M, Anaya-Ruiz M (2018) Bursera copallif-
era extracts have cytotoxic and migration-inhibitory effects
in breast cancer cell lines. Integr Cancer Ther 17:654–664.
https://​doi.​org/​10.​1177/​15347​35418​766416
Doyle JA (2007) Systematic value and evolution of leaf architec-
ture across the angiosperms in light of molecular phylogenetic
analyses. Cour Forschungsinst Senck 258:21–37
Draper FC, Baker TR, Baraloto C, Chave J, Costa F, Martin RE, Pen-
nington RT, Vicentini A, Asner GP (2020) Quantifying tropical
plant diversity requires an integrated technological approach.
Trends Ecol Evol 35:1100–1109. https://​doi.​org/​10.​1016/j.​tree.​
2020.​08.​003
Durgante FM, Higuchi N, Almeida A, Vicentini A (2013) Species
spectral signature: discriminating closely related plant species
in the Amazon with Near-Infrared Leaf-Spectroscopy. For Ecol
Manag 291:240–248. https://​doi.​org/​10.​1016/j.​foreco.​2012.​10.​
045
Ellis B, Daly DC, Hickey LJ, Johnson KR, Mitchell JD, Wilf P, Wing
SL (2009) Manual of leaf architecture. Cornell University Press,
Ithaca
Espinosa D, Llorente J, Morrone JJ (2006) Historical biogeographical
patterns of the species of Bursera (Burseraceae) and their taxo-
nomic implications. J Biogeogr 33:1945–1958. https://​doi.​org/​
10.​1111/j.​1365-​2699.​2006.​01566.x
Estevam EBB, Alves CCF, Esperandim VR, Cazal CM, Souza AF,
Miranda MLD (2018) Chemical composition, anti-Trypanosoma
cruzi and cytotoxic activities of the essential oil from green fruits
of Protium ovatum (Burseraceae). Rev Bras Frutic 40:e-794.
https://​doi.​org/​10.​1590/​0100-​29452​018794
Estrada-Ruiz E, Martínez-Cabrera HI, Cevallos-Ferriz SRS (2010)
Upper Cretaceous woods from the Olmos Formation (late
Campanian–early Maastrichtian), Coahuila, Mexico. Am J Bot
97:1179–1194. https://​doi.​org/​10.​3732/​ajb.​09002​34
Federman S, Dornburg A, Downie A, Richard AF, Daly DC, Dono-
ghue MJ (2015) The biogeographic origin of a radiation of trees
in Madagascar: implications for the assembly of a tropical for-
est biome. BMC Evol Biol 15:216. https://​doi.​org/​10.​1186/​
s12862-​015-​0483-1
Figueiredo JCG, Nunes YRF, Vasconcelos VO, Arruda SR, Morais-
Costa F, Santos GSC, Alvez FS, Duarte ER (2019) Effects of leaf
extracts of Protium spruceanum against adult and larval Rhipi-
cephalus microplus. Exp Appl Acarol 79:447–458. https://​doi.​
org/​10.​1007/​s10493-​019-​00447-4
Fine PVA, Baraloto C (2016) Habitat endemism in white-sand forests:
insights into the mechanisms of lineage diversification and com-
munity assembly of the Neotropical flora. Biotropica 48:24–33.
https://​doi.​org/​10.​1111/​btp.​12301
Fine PVA, Mesones I, Coley PD (2004) Herbivores promote habitat
specialization by trees in Amazonian forests. Science 305:663–
665. https://​doi.​org/​10.​1126/​scien​ce.​10989​82
Fine PVA, Daly DC, Villa Muñoz G, Mesones I, Cameron KM (2005)
The contribution of edaphic heterogeneity to the evolution and
diversity of Burseraceae trees in the western Amazon. Evolu-
tion 59:1464–1478. https://​doi.​org/​10.​1111/j.​0014-​3820.​2005.​
tb017​96.x
Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM, Stevens MHH,
Sääksjärvi I, Schultz JC, Coley PD (2006) The growth-defense
trade-off and habitat specialization by plants in Amazonian
forests. Ecology 87:S150–S162. https://​doi.​org/​10.​1890/​0012-​
9658(2006)​87[150:​TGTAHS]​2.0.​CO;2
Fine PVA, Metz MR, Lokvam J, Mesones I, Zuñiga J, Lamarre
G, Pilco MV, Baraloto C (2013) Insect herbivores, chemical
innovation, and the evolution of habitat specialization in Ama-
zonian trees. Ecology 94:1764–1775. https://​doi.​org/​10.​1890/​
12-​1920.1
Fine PVA, Zapata F, Daly DC (2014) Investigating processes of Neo-
tropical rain forest tree diversification by examining the evolu-
tion and historical biogeography of the Protieae (Burseraceae).
Evolution 68:1988–2004. https://​doi.​org/​10.​1111/​evo.​12414
Freidel D, Schele L, Parker J (1993) Maya Cosmos: three thousand
years on the Shaman’s path. William Morrow, New York
Friis EM, Crane PR, Pedersen KR (2011) Early flowers and Angio-
sperm evolution. Cambridge University Press
Gentry AH (1974) Flowering phenology and diversity in tropical
Bignoniaceae. Biotropica 6:64–68. https://​d oi.​o rg/​1 0.​2 307/​
29896​98
Getahun A, Hernández V, Gering E, Velasco C (2014) Resina de copal
en la Amazonía ecuatoriana: Oportunidades económicas para las
comunidades de la Reserva de Biosfera Sumaco, Ecuador. Huel-
las Del Sumaco 12:11–16
Giaretta A, Menezes LFT, Pereira OJ (2013) Structure and floristic
pattern of a coastal dunes in southeastern Brazil. Acta Bot Bras
27:87–107. https://​doi.​org/​10.​1590/​S0102-​33062​01300​01000​11
González M, Stevenson PR (2014) Seed dispersal by Woolly Monkeys
(Lagothrix lagothricha) at Caparú Biological Station (Colom-
bia): quantitative description and qualitative analysis. In: Defler
TR, Stevenson PR (eds) The Woolly Monkey. Springer, New
York, pp 147–165
Gostel MR, Phillipson PB, Weeks A (2016) Phylogenetic reconstruc-
tion of the myrrh genus, Commiphora (Burseraceae), reveals
multiple radiations in Madagascar and clarifies infrageneric
relationships. Syst Bot 41:67–81. https://​doi.​org/​10.​1600/​03636​
4416x​690598
Graham A (2010) Late Cretaceous and Cenozoic history of Latin
American vegetation and terrestrial environments. Missouri
Botanical Garden Press, St. Louis
Guedes RS, Zanella FCV, Costa Júnior JEV, Santana GM, Silva JA
(2012) Caracterização florístico-fitossociológica do componente
lenhoso de um trecho da caatinga no semiárido Paraibano. Rev
Caatinga 25:99–108
Gutiérrez-Santiago J, Jasso-Mata J, Queenborough SA, Soto-Hernán-
dez M, Rzedowski J, Jiménez-Casas M, Castillo-Martínez
CR (2016) Clasificación sexual de Linaloe (Bursera linanoe,
Burseraceae) e implicaciones productivas de aceite esencial, en
tres poblaciones naturales de Guerrero, México. Agro Product
9:66–72
Hallé F, Oldeman RAA, Tomlinson PB (1978) Tropical trees and for-
ests: an architectural analysis. Springer, New York
Han M, Manchester SR, Wu Y, Jin J, Quan C (2018) Fossil fruits of
Canarium (Burseraceae) from Eastern Asia and their implica-
tions for phytogeographical history. J Syst Palaeontol 16:841–
852. https://​doi.​org/​10.​1080/​14772​019.​2017.​13496​24
Harley MM, Daly DC (1995) Angiospermae, Burseraceae: Protieae. In:
World Pollen Spore Flora. Taylor & Francis, Oxford
Hernández M, Falcón B (2014) Variabilidad inter e intra específica en
la morfología foliar de las especies cubanas de Morella (Myri-
caceae). Biológica 16:43–52
Hickey LJ (1973) Classification of the architecture of Dicotyledonous
leaves. Am J Bot 60:17–33. https://​doi.​org/​10.​2307/​24413​19
Hickey LJ, Wolfe JA (1975) The bases of Angiosperm phylogeny: veg-
etative morphology. Ann Missouri Bot Gard 62:538–589. https://​
doi.​org/​10.​2307/​23952​67
Houël E, Gonzalez G, Bessière J-M, Odonne G, Eparvier V, Deharo E,
Stien D (2015) Therapeutic switching: from antidermatophytic
essential oils to new leishmanicidal products. Mem Inst Oswaldo
Cruz 110:106–113. https://​doi.​org/​10.​1590/​0074-​02760​140332
Howe HF (1980) Monkey dispersal and waste of a Neotropical fruit.
Ecology 61:944–959. https://​doi.​org/​10.​2307/​19367​63
13

Howe HF (1989) Scatter- and clump-dispersal and seedling demog-
raphy: hypothesis and implications. Oecologia 79:417–426.
https://​doi.​org/​10.​1007/​BF003​84323
Iturralde-Vinent MA, MacPhee RDE (1999) Paleogeography of the
Caribbean region: implications for Cenozoic biogeography.
Bull Am Mus Nat Hist 238:1–95
Jernigan KA (2006) An ethnobiological exploration of sensory and
ecological aspects of tree identification among the Aguaruna
Jívaro. University of Georgia
Julião GR, Venticinque EM, Fernandes GW, Price PW (2014) Unex-
pected high diversity of galling insects in the Amazonian upper
canopy: the savanna out there. PLoS ONE 9:e114986. https://​
doi.​org/​10.​1371/​journ​al.​pone.​01149​86
Kubitzki K (ed) (2011) Flowering plants. Eudicots: Sapindales,
Cucurbitales, Myrtaceae. The families and genera of vascular
plants, vol 10. Springer, Berlin
Kursar TA, Dexter KG, Lokvam J, Pennington RT, Richardson JE,
Weber MG, Murakami ET, Drake C, McGregor R, Coley PD
(2009) The evolution of antiherbivore defenses and their con-
tribution to species coexistence in the tropical tree genus Inga.
Proc Natl Acad Sci 106:18073–18078. https://​doi.​org/​10.​1073/​
pnas.​09047​86106
Kuster VC, Possatti L, Marbach PAS, Martins MLL (2019) Atributos
florísticos e ecológicos de formações arbustivas da Restinga em
área-chave para conservação da biodiversidade, Guarapari, ES,
Brasil. Hoehnea 46:e1002018. https://​doi.​org/​10.​1590/​2236-​
8906-​100/​2018
Lagomarsino LP, Frost LA (2020) The central role of taxonomy in
the study of Neotropical biodiversity. Ann Missouri Bot Gard
105:405–421. https://​doi.​org/​10.​3417/​20206​01
Lam HJ (1931) Beiträge zur Morphologie der dreizähligen Burser-
aceae-Canarieae. Ann Jard Bot Buitenzorg 42:25–56
Lam HJ (1932a) Beiträge zur Morphologie der Burseraceae, insbe-
sondere der Canarieae. Ann Jard Bot Buitenzorg 42:97–226
Lam HJ (1932b) The Burseraceae of the Malay Archipelago and
Peninsula. Bull Jard Bot Buitenzorg III:281–561
Lang C, Costa FRC, Camargo JLC, Durgante FM, Vicentini A (2015)
Near infrared spectroscopy facilitates rapid identification of
both young and mature Amazonian tree species. PLoS ONE
10:e0134521. https://​doi.​org/​10.​1371/​journ​al.​pone.​01345​21
Lima RBA, Marangon LC, Freire FJ, Feliciano AL, Silva RKS (2019)
Structure and diversity in ombrophilous forest in the Zona da
Mata of Pernambuco. Floresta e Ambiente 26:e20170602.
https://​doi.​org/​10.​1590/​2179-​8087.​060217
Linares E, Bye R (2008) El Copal En México CONABIO. Biodi-
versitas 78:8–11
Lobova TA, Geiselman CK, Mori SA (2009) Seed dispersal by bats
in the Neotropics. The New York Botanical Garden Press, New
York
Lokvam J, Metz MR, Takeoka GR, Nguyen L, Fine PVA (2015)
Habitat-specific divergence of procyanidins in Protium subser-
ratum (Burseraceae). Chemoecology 25:293–302. https://​doi.​
org/​10.​1007/​s00049-​015-​0198-1
López Patiño EJ, Szeszko DR, Pérez JR, Retis ASB (2012) The Flora
of the Tenancingo-Malinalco-Zumpahuacán Protected Natural
Area, State of Mexico, Mexico. Harvard Pap Bot 17:65–167.
https://​doi.​org/​10.​3100/​025.​017.​0113
Lucero-Gómez P, Mathe C, Vieillescazes C, Bucio-Galindo L, Belio-
Reyes V-A (2014) Archaeobotanic: HPLC molecular profiles
for the discrimination of copals in Mesoamerica. Application
to the study of resin materials from objects of Aztec offerings.
ArcheoSciences 38:119–133. https://​d oi.​o rg/​1 0.​4 000/​a rche​
oscie​nces.​4204
Machado MA, Almeida EB Jr (2019) Spatial structure, diversity, and
edaphic factors of an area of Amazonian coast vegetation in
13
D. C. Daly et al.
Brazil. J Torrey Bot Soc 146:58–68. https://​doi.​org/​10.​3159/​
TORREY-​D-​18-​00025.1
Machado IC, Lopes AV (2004) Floral traits and pollination systems in
the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–
376. https://​doi.​org/​10.​1093/​aob/​mch152
MacPhee RDE, Iturralde-Vinent MA (2000) A short history of Greater
Antillean land mammals: biogeography, paleogeography, radia-
tions, and extinctions. Tropics 10:145–154. https://​doi.​org/​10.​
3759/​tropi​cs.​10.​145
Maia VC, Silva BG (2020) Checklist of the gall midges (Diptera, Ceci-
domyiidae) in the state of Bahia (Northeastern Brazil). Braz J
Anim Environ Res 3:3991–4013. https://​doi.​org/​10.​34188/​bjaer​
v3n4-​096
Martínez-Habibe MC, Daly DC (2016) A taxonomic revision of Bur-
sera subgen. Bursera in the Greater Antilles and the Bahamas,
including a new species from Cuba. Brittonia 68:455–475.
https://​doi.​org/​10.​1007/​s12228-​016-​9441-5
Martínez-Habibe MC, Daly DC (2019) Nine new species of Dacryo-
des from Andean South America. Studies in Neotropical Burser-
aceae XXIV. Brittonia 71:325–344. https://​doi.​org/​10.​1007/​
s12228-​019-​09574-z
Martínez-Habibe MC, Daly DC, Pérez-Camacho J, Herrera-Oliver
P (2013) A new species of Bursera (Burseraceae) from Cuba.
Brittonia 65:62–65. https://​doi.​org/​10.​1007/​s12228-​012-​9262-0
Martínez-Habibe MC (2012) Systematics, biogeography and leaf anat-
omy and architecture of Bursera subgen. Bursera (Burseraceae)
in the Greater Antilles and the Bahamas. Ph.D. thesis, Claremont
Graduate University
Martins Júnior AS, Sakuragui CM, Hennen JF, Carvalho Júnior AA
(2019) Neopuccinia (Pucciniales): a new Puccinia-like genus
from the Brazilian Cerrado. Phytotaxa 406:169–179. https://​doi.​
org/​10.​11646/​phyto​taxa.​406.3.3
Matallana G, Wendt T, Araujo DSD, Scarano FR (2005) High abun-
dance of dioecious plants in a tropical coastal vegetation. Am J
Bot 92:1513–1519. https://​doi.​org/​10.​3732/​ajb.​92.9.​1513
Medeiros RD (2019) Commiphora leptophloeos (Mart.) J.B. Gillett
(Burseraceae): Estudo fitoquímico, toxicidade e avaliação do
potencial anti-inflamatório e antimicrobiano. Ph.D. thesis, Uni-
versidade Federal do Rio Grande do Norte, Centro de Ciências da
Saúde, Programa de pós-graduação em Ciências Farmacêuticas
Melo MFF, Daly DC, Santos JUM, Silva KC (2021) Three new species
of Trattinnickia. Studies in Neotropical Burseraceae XXX. Brit-
tonia 73:343–352. https://​doi.​org/​10.​1007/​s12228-​021-​09666-9
Mendonça BAF, Fernandes-Filho EI, Schaefer CEGR, Vasconcelos
BNF (2017) Soil-vegetation relationships and community struc-
ture in a “terra-firme” white-sand vegetation gradient in Viruá
National Park, northern Amazon, Brazil. An Acad Bras Cienc
89:1269–1293. https://d​ oi.o​ rg/1​ 0.1​ 590/0​ 001-3​ 76520​ 17201​ 60666
Menezes JC, Cruz Neto OC, Azevedo IFP, Machado AO, Nunes YRF
(2019) Soil seed bank at different depths and light conditions
in a dry forest in Northern Minas Gerais. Floresta e Ambiente
26:e20170314. https://​doi.​org/​10.​1590/​2179-​8087.​031417
Meyer HW (2003) The Fossils of Florissant. Smithsonian Books,
Washington
Miller AG, Morris M (1988) Plants of Dhofar, the southern region
of Oman, traditional, economic and medicinal uses. The Office
of the Adviser for Conservation of the Environment, Diwan of
Royal Court, Sultanate of Oman
Milliken W, Albert B, Gómez GG (1999) Yanomami: a forest people.
Royal Botanic Gardens, Kew
Misiewicz TM, Fine PVA (2014) Evidence for ecological divergence
across a mosaic of soil types in an Amazonian tropical tree:
Protium subserratum (Burseraceae). Mol Ecol 23:2543–2558.
https://​doi.​org/​10.​1111/​mec.​12746
A review of Neotropical Burseraceae
Misiewicz TM, Simmons TS, Fine PVA (2020) The contribution of
multiple barriers to reproduction between edaphically divergent
lineages in the Amazonian tree Protium subserratum (Burser-
aceae). Ecol Evol 10:6646–6663. https://​doi.​org/​10.​1002/​ece3.​
6396
Mitchell JD, Daly DC (2015) A revision of Spondias L. (Anacardi-
aceae) in the Neotropics. PhytoKeys 55:1–92. https://​doi.​org/​10.​
3897/​phyto​keys.​55.​8489
Mobin M, Lima SG, Almeida LTG, Silva Filho JC, Rocha MS,
Oliveira AP, Mendes MB, Carvalho FAA, Melhem MSC, Costa
JGM (2017) Gas chromatography triple-quadruple mass spec-
trometry analysis and vasorelaxant effect of essential oil from
Protium heptaphyllum (Aubl.) March [sic]. BioMed Res Int
2017:1928171. https://​doi.​org/​10.​1155/​2017/​19281​71
Monzote L, Hill GM, Cuellar A, Scull R, Setzer WN (2012) Chemical
composition and anti-proliferative properties of Bursera graveo-
lens essential oil. Nat Prod Commun 7:1531–1534. https://​doi.​
org/​10.​1177/​19345​78X12​00701​130
Morrone JJ, Escalante T, Rodríguez-Tapia G (2017) Mexican biogeo-
graphic provinces: map and shapefiles. Zootaxa 4277:277–279.
https://​doi.​org/​10.​11646/​zoota​xa.​4277.2.8
Muellner-Riehl AN, Weeks A, Clayton JW, Buerki S, Nauheimer L,
Chiang Y-C, Cody S, Pell SK (2016) Molecular phylogenet-
ics and molecular clock dating of Sapindales based on plastid
rbcL, atpB and trnL-trnF DNA sequences. Taxon 65:1019–1036.
https://​doi.​org/​10.​12705/​655.5
Narayana LL (1959) Microsporogenesis and female gametophyte in
Boswellia serrata Roxb. Curr Sci 28:77–78
Narayana LL (1960) Studies in Burseraceae. I. J Indian Bot Soc
39:204–209
Nogueira AO, Oliveira YIS, Adjafre BL, Moraes MEA, Aragão GF
(2019) Pharmacological effects of the isomeric mixture of alpha
and beta amyrin from Protium heptaphyllum: a literature review.
Fund Clin Pharmacol 33:4–12. https://d​ oi.o​ rg/1​ 0.1​ 111/f​ cp.1​ 2402
Oliveira Junior SB, Cerqueira RM, Gil ASB, Vilhena NQ (2014) Com-
posição florística e estrutural de uma mata ciliar em um frag-
mento urbano no município de Capão Bonito - SP. Enciclopédia
Biosfera 10:2059–2077
Ortiz-Pulido R, Rico-Gray V (2006) Seed dispersal of Bursera faga-
roides (Burseraceae): the effect of linking environmental fac-
tors. Southwest Nat 51:11–21. https://​doi.​org/​10.​1894/​0038-​
4909(2006)​51[11:​SDOBFB]​2.0.​CO;2
Parrado-Rosselli A (2005) Fruit availability and seed dispersal in terra
firme rain forests of Colombian Amazonia. Ph.D. thesis, Univer-
sity of Amsterdam
Pebesma E (2018) Simple features for R: standardized support for spa-
tial vector data. R Journal 10:439–446. https://​doi.​org/​10.​32614/​
RJ-​2018-​009
Perdiz RO (2020) Delimitação específica e filogeografia do complexo
Protium aracouchini (Aubl.) Marchand (Burseraceae). Ph.D.
thesis, Programa de pós-graduação em Ciências Biológicas
(Botânica), Instituto Nacional de Pesquisas da Amazônia
Perdiz RO, Daly DC, Vicentini A, Fine PVA (2020) A new species of
Protium (Burseraceae) from the Pacific Coast of Costa Rica. Phy-
totaxa 434:183–194. https://​doi.​org/​10.​11646/​phyto​taxa.​434.2.4
Pereira JJS, Pereira APC, Jandú JJB, Paz JA, Crovella S, Correia MTS,
Silva JA (2017) Commiphora leptophloeos: phytochemical and
antimicrobial characterization. Front Microbiol 8:52. https://​doi.​
org/​10.​3389/​fmicb.​2017.​00052
Pereira IF, Costa APF, Srbek-Araujo AC, Guimarães LJ, Merencio AF,
Silva AG (2020) The dispersion of diaspores of Protium icicar-
iba (Burseraceae): a networked or multifactorial system? J Chem
Ecol 46:163–175. https://​doi.​org/​10.​1007/​s10886-​019-​01140-x
Peters CM, Purata SE, Chibnik M, Brosi BJ, López AM, Ambrosio M
(2003) The life and times of Bursera glabrifolia (H.B.K.) Engl.
in Mexico: a parable for ethnobotany. Econ Bot 57:432–441.
https://​doi.​org/​10.​1663/​0013-​0001(2003)​057[0432:​TLATOB]​
2.0.​CO;2
Pinheiro F, Dantas-Queiroz MV, Palma-Silva C (2018) Plant species
complexes as models to understand speciation and evolution: a
review of South American studies. Crit Rev Plant Sci 37:54–80.
https://​doi.​org/​10.​1080/​07352​689.​2018.​14715​65
Pitman NCA, Terborgh JW, Silman MR, Núñez VP, Neill DA, Cerón
CE, Palacios WA, Aulestia M (2001) Dominance and distribution
of tree species in upper Amazonian terra firme forests. Ecol-
ogy 82:2101–2117. https://​doi.​org/​10.​1890/​0012-​9658(2001)​
082[2101:​DADOTS]​2.0.​CO;2
Pitman NCA, Silman MR, Terborgh JW (2013) Oligarchies in Ama-
zonian tree communities: a ten-year review. Ecography 36:114–
123. https://​doi.​org/​10.​1111/j.​1600-​0587.​2012.​00083.x
Piva LRO, Sanquetta CR, Wojciechowski J, Corte APD (2020) Fitosso-
ciologia em comunidades florestais do projeto RADAMBRASIL
no bioma Amazônia. BIOFIX Sci J 5:264–271. https://​doi.​org/​
10.​5380/​biofix.​v5i2.​73668
Plowden C, Uhl C, Oliveira FA (2002) Breu resin harvest by Tembé
Indians and its dependence on a bark-boring beetle. In: Stepp JR,
Wyndham FS, Zarger RK (eds) Ethnobiology and biocultural
diversity: proceedings of the seventh international congress of
ethnobiology. International Society of Ethnobiology/University
of Georgia Press, Athens, Georgia, pp 365–380
Pontes WJT, Oliveira JCS, Camara CAG, Lopes ACHR, Gondim
Júnior MGC, Oliveira JV, Schwartz MOE (2007) Composition
and acaricidal activity of the resin’s essential oil of Protium
bahianum Daly against two spotted spider mite (Tetranychus
Urticae). J Essent Oil Res 19:379–383. https://​doi.​org/​10.​1080/​
10412​905.​2007.​96993​10
Primack RB (1985) Longevity of individual flowers. Ann Rev Ecol Syst
16:15–37. https://​doi.​org/​10.​1146/​annur​ev.​es.​16.​110185.​000311
Purata SE (ed) (2008) Uso y manejo de los copales aromáticos: resinas
y aceites. CONABIO/RAISES, Mexico
R Core Team (2021) R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna
Ramos-Ordoñez MF, Márquez-Guzmán J, Arizmendi MC (2008) Par-
thenocarpy and seed predation by insects in Bursera morelensis.
Ann Bot 102:713–722. https://​doi.​org/​10.​1093/​aob/​mcn153
Ramos-Ordoñez MF, Arizmendi MC, Márquez-Guzmán J (2012) The
fruit of Bursera: structure, maturation and parthenocarpy. AoB
PLANTS 2012:pls027. https://​doi.​org/​10.​1093/​aobpla/​pls027
Ramos-Ordoñez MF, Arizmendi MC, Martínez M, Márquez-Guzmán
J (2013) The pseudaril of Bursera and Commiphora, a foretold
homology? Rev Mex Biodivers 84:509–520. https://​doi.​org/​10.​
7550/​rmb.​32114
Rao VS, Maia JL, Oliveira FA, Lemos TLG, Chaves MH, Santos FA
(2007) Composition and antinociceptive activity of the essential
oil from Protium heptaphyllum resin. Nat Prod Commun 2:1199–
1202. https://​doi.​org/​10.​1177/​19345​78X07​00201​201
Reid EM, Chandler MEJ (1933) The London Clay flora. British
Museum (Natural History), London
Rey-Valeirón C, Guzmán L, Saa LR, López-Vargas J, Valarezo E
(2017) Acaricidal activity of essential oils of Bursera graveolens
(Kunth) Triana & Planch. and Schinus molle L. on unengorged
larvae of cattle tick Rhipicephalus (Boophilus) microplus (Acari:
Ixodidae). J Essent Oil Res 29:344–350. https://​doi.​org/​10.​1080/​
10412​905.​2016.​12784​05
Richards LA, Dyer LA, Forister ML, Smilanich AM, Dodson CD,
Leonard MD, Jeffrey CS (2015) Phytochemical diversity
drives plant-insect community diversity. Proc Natl Acad Sci
112:10973–10978. https://​doi.​org/​10.​1073/​pnas.​15049​77112
Rivas-Arancibia SP, Bello-Cervantes E, Carrillo-Ruiz H, Andrés-
Hernández AR, Figueroa-Castro DM, Guzmán-Jiménez S
(2015) Variaciones de la comunidad de visitadores florales de
Bursera copallifera (Burseraceae) a lo largo de un gradiente de
13

perturbación antropogénica. Rev Mex Biodivers 86:178–187.
https://​doi.​org/​10.​7550/​rmb.​44620
Ronellenfitsch H, Lasser J, Daly DC, Katifori E (2015) Topological
phenotypes constitute a new dimension in the phenotypic space
of leaf venation networks. PLOS Comput Biol 11:e1004680.
https://​doi.​org/​10.​1371/​journ​al.​pcbi.​10046​80
Rosado BHP, Mattos EA (2017) On the relative importance of CSR
ecological strategies and integrative traits to explain species
dominance at local scales. Funct Ecol 31:1969–1974. https://​
doi.​org/​10.​1111/​1365-​2435.​12894
Roth I (1996) Microscopic venation patterns of leaves and their impor-
tance in the distinction of (tropical) species. In: Encyclopedia
of plant anatomy. Gebrüder Borntraeger Verlagsbuchhandlung,
Stuttgart, pp 1–196
Salazar D, Jaramillo MA, Marquis RJ (2016) Chemical similarity and
local community assembly in the species-rich tropical genus
Piper. Ecology 97:3176–3183. https://​doi.​org/​10.​1002/​ecy.​1536
Salazar D, Lokvam J, Mesones I, Vásquez Pilco M, Zuñiga JMA, de
Valpine P, Fine PVA (2018) Origin and maintenance of chemical
diversity in a species-rich tropical tree lineage. Nat Ecol Evol
2:983–990. https://​doi.​org/​10.​1038/​s41559-​018-​0552-0
Santamaría-Aguilar D, Aguilar R (2017) Dacryodes talamancensis
(Burseraceae), la segunda especie del género para América Cen-
tral. Phytoneuron 11:1–6
Santamaría-Aguilar D, Lagomarsino LP (2017) Two new species and
a new combination in Protium (Burseraceae) from Costa Rica.
PhytoKeys 76:89–113. https://​doi.​org/​10.​3897/​phyto​keys.​76.​
10298
Santana RC, Rosa AS, Mateus MHS, Soares DC, Atella G, Guimarães
AC, Siani AC, Ramos MFS, Saraiva EM, Pinto-da-Silva LH
(2020) In vitro leishmanicidal activity of monoterpenes present
in two species of Protium (Burseraceae) on Leishmania amazon-
ensis. J Ethnopharmacol 259:112981. https://​doi.​org/​10.​1016/j.​
jep.​2020.​112981
Santos VJ, Zickel CS, Almeida EB Jr (2015) Composição estrutural
do estrato arbustivo-arbóreo de uma floresta de restinga no sul
da Bahia, Brasil. Pesquisas Botânica 68:257–269
Siani AC, Ramos MFS, Menezes-de-Lima O Jr, Ribeiro-dos-Santos
R, Fernandez-Ferreira E, Soares ROA, Rosas EC, Susunaga GS,
Guimarães AC, Zoghbi MGB, Henriques MGMO (1999) Evalu-
ation of anti-inflammatory-related activity of essential oils from
the leaves and resin of species of Protium. J Ethnopharmacol
66:57–69. https://​doi.​org/​10.​1016/​S0378-​8741(98)​00148-2
Silva PD, Leal IR, Wiurth R, Tabarelli M (2007) Harvesting of Protium
heptaphyllum (Aubl.) March. [sic] seeds (Burseraceae) by the
leaf-cutting ant Atta sexdens L. promotes seed aggregation and
seedling mortality. Rev Bras Bot 30:553–560. https://​doi.​org/​10.​
1590/​S0100-​84042​00700​03000​19
Silva KE, Martins SV, Ribeiro CAAS, Santos NT, Azevedo CP, Matos
FDA, Amaral IL (2011) Floristic composition and similar-
ity of 15 hectares in Central Amazon, Brazil. Rev Biol Trop
59:1927–1938
Silva RKS, Feliciano ALP, Marangon LC, Lima RBA, Santos WB
(2012) Estrutura e síndromes de dispersão de espécies arbóreas
em um trecho de mata ciliar, Sirinhaém, Pernambuco, Brasil.
Pesqui Florest Bras 32:1. https://​doi.​org/​10.​4336/​2012.​pfb.​32.​
69.​01
Silva RCS, Milet-Pinheiro P, Silva PCB, Silva AG, Silva MV, Navarro
DMAF, Silva NH (2015) (E)-Caryophyllene and α-Humulene:
Aedes aegypti oviposition deterrents elucidated by gas chro-
matography-electrophysiological assay of Commiphora lep-
tophloeos leaf oil. PLoS ONE 10:1–14. https://​doi.​org/​10.​1371/​
journ​al.​pone.​01445​86
Silva IF, Guimarães AL, Amorim VS, Silva TMG, Peixoto RM, Nunes
XP, Silva TMS, Costa MM (2019a) Antimicrobial activity of
ethanolic extracts from Commiphora leptophloeos (Mart.) J.B.
13
D. C. Daly et al.
Gillett against Staphylococcus spp. isolated from cases of mas-
titis in ruminants. Ciênc Anim Bras 20:e57228. https://​doi.​org/​
10.​1590/​1089-​6891v​20e-​57228
Silva TMC, Carvalho WAC, Terra MCNS, Santos RM, Santos ABM,
Souza CR (2019b) Anthropic disturbances as the main driver
of a semideciduous seasonal forest fragment in Minas Gerais.
Rodriguésia 70:e03352017. https://​d oi.​o rg/​1 0.​1 590/​2 175-​
78602​01970​065
Snow DW (1962) The natural history of the Oilbird, Steatornis
caripensis, in Trinidad, W.I. Part 2: Population, breeding ecol-
ogy and food. Zool Sci Contrib N Y Zool Soc 47:199–221
South A (2017) Rnaturalearth: world map data from natural earth. R
package version 0.1.0. https://​CRAN.R-​proje​ct.​org/​packa​ge=​
rnatu​ralea​r th
Souza RR, Pimentel ADA, Nogueira LL, Abreu VHR, Novais JS
(2020) Resources collected by two Melipona Illiger, 1806
(Apidae: Meliponini) species based on pollen spectrum of
honeys from the Amazon Basin. Sociobiology 67:268–280.
https://​doi.​org/​10.​13102/​socio​biolo​gy.​v67i2.​4617
Stavis VK, Machado PJR, Fina BG (2020) Estrutura de fragmento
de floresta estacional em área de ecótono, Mato Grosso do
Sul. Braz J Dev 6:59197–59213. https://​d oi.​o rg/​1 0.​3 4117/​
bjdv6​n8-​366
ter Steege H, Pitman NCA, Sabatier D, Baraloto C, Salomão RP, Gue-
vara JE, Phillips OL, Castilho CV, Magnusson WE, Molino J-F,
Monteagudo A, Núñez Vargas P, Montero JC, Feldpausch TR,
Coronado ENH, Killeen TJ, Mostacedo B, Vasquez R, Assis
RL, Terborgh J, Wittmann F, Andrade A, Laurance WF, Lau-
rance SGW, Marimon BS, Marimon B-H, Guimarães Vieira
IC, Amaral IL, Brienen R, Castellanos H, Cárdenas López D,
Duivenvoorden JF, Mogollón HF, Matos FD de A, Dávila N,
Garcı́a-Villacorta R, Stevenson Diaz PR, Costa F, Emilio T,
Levis C, Schietti J, Souza P, Alonso A, Dallmeier F, Montoya
AJD, Fernandez Piedade MT, Araujo-Murakami A, Arroyo L,
Gribel R, Fine PVA, Peres CA, Toledo M, Aymard C. GA, Baker
TR, Cerón C, Engel J, Henkel TW, Maas P, Petronelli P, Stropp
J, Zartman CE, Daly D, Neill D, Silveira M, Paredes MR, Chave
J, Lima Filho D de A, Jørgensen PM, Fuentes A, Schöngart J,
Cornejo Valverde F, Di Fiore A, Jimenez EM, Peñuela Mora MC,
Phillips JF, Rivas G, Andel TR van, Hildebrand P von, Hoffman
B, Zent EL, Malhi Y, Prieto A, Rudas A, Ruschell AR, Silva N,
Vos V, Zent S, Oliveira AA, Schutz AC, Gonzales T, Trindade
Nascimento M, Ramirez-Angulo H, Sierra R, Tirado M, Umaña
Medina MN, Heijden G van der, Vela CIA, Vilanova Torre E,
Vriesendorp C, Wang O, Young KR, Baider C, Balslev H, Fer-
reira C, Mesones I, Torres-Lezama A, Urrego Giraldo LE, Zagt
R, Alexiades MN, Hernandez L, Huamantupa-Chuquimaco I,
Milliken W, Palacios Cuenca W, Pauletto D, Valderrama San-
doval E, Valenzuela Gamarra L, Dexter KG, Feeley K, Lopez-
Gonzalez G, Silman MR (2013) Hyperdominance in the Ama-
zonian tree flora. Science 342:1243092. https://​doi.​org/​10.​1126/​
scien​ce.​12430​92
Stevenson PR, Cardona L, Cárdenas S, Link A (2021) Oilbirds disperse
large seeds at longer distance than extinct megafauna. Sci Rep
11:420. https://​doi.​org/​10.​1038/​s41598-​020-​79280-4
Suárez AI, Compagnone RS, Acosta D, Vásquez L, Diaz B, Canelón
DJ (2007) Chemical composition and antimicrobial activity of
the essential oil from oleoresin of Protium neglectum S. [sic]. J
Essent Oil Bear Plants 10:70–75. https://​doi.​org/​10.​1080/​09720​
60X.​2007.​10643​521
Teixeira-Rios T, da Silva DKA, Goto BT, Yano-Melo AM (2018) Sea-
sonal differences in arbuscular mycorrhizal fungal communities
in two woody species dominating semiarid caatinga forests. Folia
Geobot 53:191–200. https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 12224-0​ 18-9​ 314-7
Tennekes M (2018) tmap: thematic maps in R. J Stat Softw 84:1–39.
https://​doi.​org/​10.​18637/​jss.​v084.​i06
A review of Neotropical Burseraceae
Trainer JM, Will TC (1984) Avian methods of feeding on Bursera
simaruba (Burseraceae) fruits in Panama. Auk 101:193–195
Van der Walt J (1975) The fruit of Commiphora. Boissiera 24:325–330
van Dulmen A (2001) Pollination and phenology of flowers in the can-
opy of two contrasting rain forest types in Amazonia, Colombia.
Plant Ecol 153:73–85. https://d​ oi.o​ rg/1​ 0.1​ 023/A:1​ 01757​ 73051​ 93
van Heel WA (1970) Some unusual tropical labyrinth seeds. Proc Kon
Ned Akad Wet C 73:288–301
Vasco A, Thadeo M, Conover M, Daly DC (2014) Preparation of sam-
ples for leaf architecture studies: a method for mounting cleared
leaves. Appl Plant Sci 2:1400038. https://​doi.​org/​10.​3732/​apps.​
14000​38
Vieira FA, Carvalho D (2008) Genetic structure of an insect-polli-
nated and bird-dispersed tropical tree in vegetation fragments
and corridors: implications for conservation. Biodivers Conserv
17:2305–2321. https://​doi.​org/​10.​1007/​s10531-​008-​9367-7
Villanueva-Gutiérrez R, Roubik DW, Colli-Ucán W, Tuz-Novelo M
(2018) The value of plants for the Mayan stingless honey bee
Melipona beecheii (Apidae: Meliponini): a pollen-based study
in the Yucatán Peninsula, Mexico. In: Vit P, Pedro SRM, Roubik
DW (eds) Pot-pollen in stingless bee melittology. Springer,
Cham, pp 67–76
Villa-Ruano N, Pacheco-Hernández Y, Becerra-Martínez E, Zárate-Reyes
JA, Cruz-Durán R (2018) Chemical profile and pharmacological
effects of the resin and essential oil from Bursera slechtendalii [sic]:
a medicinal “copal tree” of southern Mexico. Fitoterapia 128:86–92.
https://​doi.​org/​10.​1016/j.​fitote.​2018.​05.​009
Vleminckx J, Salazar D, Fortunel C, Mesones I, Dávila N, Lokvam J,
Beckley K, Baraloto C, Fine PVA (2018) Divergent secondary
metabolites and habitat filtering both contribute to tree species
coexistence in the Peruvian Amazon. Front Plant Sci 9:836.
https://​doi.​org/​10.​3389/​fpls.​2018.​00836
Walker A, Sillans R (1961) Les plantes utiles du Gabon. Editions Paul
Lechevalier, Paris
Authors and Affiliations
Douglas C. Daly1 · Ricardo O. Perdiz2 · Paul V. A. Fine3 · Gabriel Damasco4
María Cristina Martínez‑Habibe5 · Laura Calvillo‑Canadell6
Ricardo O. Perdiz
ricoperdiz@gmail.com
Paul V. A. Fine
paulfine@berkeley.edu
Gabriel Damasco
gabriel.damasco@ufrn.br
María Cristina Martínez‑Habibe
mhabibe@uninorte.edu.co
Laura Calvillo‑Canadell
laura.calvillo@ib.unam.mx
1 Universidad Nacional Autónoma de México, Circuito Zona
Institute of Systematic Botany, The New York Botanical
Garden, 2900 Southern Blvd., Bronx, NY 10458, USA
2
Luz da Floresta, Rua Xiriana, 311, Aparecida, Boa Vista,
Roraima 69306‑320, Brazil
View publication stats
Weeks A, Tye A (2009) Phylogeography of palo santo trees (Bursera
graveolens and Bursera malacophylla; Burseraceae) in the Galá-
pagos Archipelago. Bot J Linn Soc 161:396–410. https://d​ oi.o​ rg/​
10.​1111/j.​1095-​8339.​2009.​01008.x
Weeks A, Daly DC, Simpson BB (2005) The phylogenetic history and
biogeography of the frankincense and myrrh family (Burser-
aceae) based on nuclear and chloroplast sequence data. Mol
Phylogenet Evol 35:85–101. https://​doi.​org/​10.​1016/j.​ympev.​
2004.​12.​021
Weeks A, Zapata F, Pell SK, Daly DC, Mitchell JD, Fine PVA (2014)
To move or to evolve: contrasting patterns of intercontinental
connectivity and climatic niche evolution in “Terebinthaceae”
(Anacardiaceae and Burseraceae). Front Genet 5:409. https://​
doi.​org/​10.​3389/​fgene.​2014.​00409
Williams-Linera G, Álvarez-Aquino C (2016) Vegetative and reproduc-
tive tree phenology of ecological groups in a tropical dry forest
in central Veracruz, Mexico. Bot Sci 94:756–756. https://d​ oi.o​ rg/​
10.​17129/​BOTSCI.​682
Xu F, Guo W, Xu W, Wei Y, Wang R (2009) Leaf morphology cor-
relates with water and light availability: what consequences
for simple and compound leaves? Prog Nat Sci 19:1789–1798.
https://​doi.​org/​10.​1016/j.​pnsc.​2009.​10.​001
Yanomami MI, Yanomami E, Albert B, Milliken W, Coelho V (eds)
(2014) Manual dos remédios tradicionais Yanomami, vol 2.
Instituto Socioambiental & Hutukara Associação Yanomami,
São Paulo
Zarucchi JL (1980) Ibapichuna: an edible Dacryodes (Burseraceae)
from the Northwest Amazon. Bot Mus Leafl Harvard Univ
28:81–85
Publisher's Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
·
3
Department of Integrative Biology and Jepson and University
Herbaria, University of California, Berkeley, 3040 and 1005
Valley Life Sciences Bldg. #3140, Berkeley, CA 94720‑3140,
USA
4
Department of Botany and Zoology, Universidade Federal
do Rio Grande do Norte, Campus Universitário Lagoa Nova,
Natal, RN 59078‑970, Brazil
5
Departamento de Química y Biología, Universidad del
Norte, Km. 5 vía Puerto Colombia, Barranquilla, Atlántico,
Colombia
6
Departamento de Botánica, Instituto de Biología,
Deportiva s.n., Ciudad Universitaria, Apartado Postal
70‑233, 04510 Mexico City, Mexico
13