This article was downloaded by: [Ingenta Content Distribution (Publishing Technology)]On: 07 October 2014, At: 10:03Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office:Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

GranaPublication details, including instructions for authors and subscriptioninformation:http://www.tandfonline.com/loi/sgra20

Pollen morphology and systematics ofBurseraceaeMadeline M Harley a , Unsook Song b & Hannah I Banks aa Palynology Unit , Herbarium, Royal Botanic Gardens , Kew, Richmond,Surrey, TW9 3AE, UKb Unsook Song, Dept Forest Resources, College of Agriculture , ChonbukNational University , 561‐756, South Koreac Palynology Unit , Herbarium, Royal Botanic Gardens , Kew, Richmond,Surrey, TW9 3AE, UKPublished online: 18 Feb 2007.

To cite this article: Madeline M Harley , Unsook Song & Hannah I Banks (2005) Pollen morphology andsystematics of Burseraceae, Grana, 44:4, 282-299, DOI: 10.1080/00173130500477902

To link to this article: http://dx.doi.org/10.1080/00173130500477902

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”)contained in the publications on our platform. However, Taylor & Francis, our agents, and ourlicensors make no representations or warranties whatsoever as to the accuracy, completeness, orsuitability for any purpose of the Content. Any opinions and views expressed in this publicationare the opinions and views of the authors, and are not the views of or endorsed by Taylor &Francis. The accuracy of the Content should not be relied upon and should be independentlyverified with primary sources of information. Taylor and Francis shall not be liable for anylosses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilitieswhatsoever or howsoever caused arising directly or indirectly in connection with, in relation to orarising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any substantialor systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, ordistribution in any form to anyone is expressly forbidden. Terms & Conditions of access and usecan be found at http://www.tandfonline.com/page/terms-and-conditions

Pollen morphology and systematics of Burseraceae

MADELINE M. HARLEY, UNSOOK SONG and HANNAH I. BANKS

Harley, M. M., Song, U. & Banks, H. I. 2005. Pollen morphology and systematics of Burseraceae. –Grana 44: 282–299. ISSN 0017-3134.

The Burseraceae are a medium-sized family in which 18 genera are currently recognised. They are thesubject of a long-term project to describe the pollen morphology from light, scanning electron andtransmission electron microscopy. The pollen morphology of tribe Protieae has been published, as wellas an account of the pollen of the African taxa in the family. Pollen data for the other two tribes,Bursereae and Canarieae, are more or less complete. The pollen of all the genera have been examined,with the exception of the recently described Pseudodacryodes Pierlot for which, currently, there is nopollen material available. This paper summarises the results.

There is considerable variation in exine and aperture features between, and occasionally within, thegenera and 14 major pollen types are defined, including two previously undescribed types: ‘Canarium

oleiferum’ and ‘Canarium gracile’. The distribution of pollen characteristics throughout the family iscompared with previously published tribal and subtribal groupings, as well as with current ideas ofgeneric relationships from molecular analyses. Comparisons show notable congruence of pollen datawith molecular data. To some extent pollen morphology is different for each of the subtribes.Nevertheless, there are some notable exceptions, for example, the pollen of Garuga and Boswellia areremarkably similar, although Garuga has been included, somewhat tenuously, in tribe Protieae, andBoswellia is included in tribe Bursereae, subtribe Boswelliinae. In a recent molecular tree Garuga andBoswellia appear to be closely related, and this supports the conclusion, based on severalmacromorphological characters as well as pollen, that Garuga should be transferred to tribe Bursereae.

Madeline M. Harley* & Hannah I. Banks, Palynology Unit, Herbarium, Royal Botanic Gardens, Kew,

Richmond, Surrey, TW9 3AE, UK; Unsook Song, Dept Forest Resources, College of Agriculture,

Chonbuk National University, 561-756, South Korea.

*Corresp. Author

(Manuscript received 19 April 2005; accepted 28 October 2005)

The Burseraceae are a medium-sized pantropical family of

18 genera comprising shrubs and trees with prominent resin

ducts in the bark, as well as in other parts of the plant.

Economically, among the best-known members of Burser-

aceae are: Gaboon Mahogany (Aucoumea klaineana Pierre);

Indian White Mahogany (Canarium euphyllum Kurz),

Myrrh (Commiphora myrrha (Nees) Engl.) and Frankincense

(Boswellia species, notably B. sacra Flueck.). The resin from

Bursera, especially in Mexico, is extracted to make varnish.

The species are widely distributed in the Old and New

Worlds, but centred especially in Malesia, Africa, Meso- and

South America. This distribution is reflected in the widely

used tribal classification of Lam (1932) where genera of tribe

Protieae are predominantly South American, those of tribe

Bursereae predominantly African or Mesoamerican, while

those of tribe Canarieae are predominantly Malesian.

Systematically the family has been placed in various

orders by different authors (see Brummitt 1992): within

the Geraniales sensu Bentham & Hooker (1862), Dalla Torre

& Harms (1901); Rutales sensu Melchior (1964), Thorne

(1983); Dahlgren (1983), Young (1982), Takhtajan (1987);

Sapindales sensu Cronquist (1981). The Angiosperm Phylo-

geny Group (1998, 2003) also includes Burseraceae in their

circumscription of Sapindales. Of the 38 families that have,

at times, been placed in the same order as Burseraceae in

different systematic treatments, only three families have

consistently been placed with Burseraceae – Meliaceae,

Rutaceae and Simaroubaceae. Interestingly, in all recent

systematic treatments, a sister relationship between Burser-

aceae and Anacardiaceae has been recognised. This has been

further confirmed by molecular studies including Soltis et al.

(2000) and Savolainen et al. (2000).

Prior to the studies initiated (MMH) for the World Pollen

and Spore Flora, the pollen morphology of Burseraceae had

not been addressed in relation to the systematics of the

family. A long-term project to describe the pollen morphol-

ogy of each of the three widely accepted tribes, from light,

scanning electron and transmission electron microscopy, for

The World Pollen and Spore Flora (WPSF) is nearing

completion. The pollen morphology of tribe Protieae has

already been published (Harley & Daly 1995), and an

account of the pollen of the African taxa in the family

(Harley & Hall 1999). Pollen data for the other two tribes,

Bursereae and Canarieae, are more or less complete. The

pollen of all the genera have been examined, with the

exception of the recently described Pseudodacryodes Pierlot

(1997) for which, currently, there is no pollen material

available. In Harley & Daly (1995) there is a summary of

previously published accounts of pollen morphology for

some of the taxa included in the family. More recently

comprehensive pollen morphological accounts for the

species of each of the three tribes which occur in South

America have been published by Aguilar-Sierra & Melhem

(1998a, b, c).

Grana 44: 282–299, 2005

Grana 44 (2005) # 2005 Taylor & Francis. ISSN 0017-3134

DOI: 10.1080/00173130500477902

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

The pollen morphology of Anacardiaceae, Meliaceae,

Rutaceae and Simaroubaceae is more or less distinct from

that of Burseraceae. Pollen morphology of Meliaceae, and

references to, is summarised by Van der Ham (1995). Pollen

morphology has been described for about 60% of Rutaceae

genera, representative of all seven subfamilies (Engler 1931),

although the coverage is more comprehensive for some

subfamilies than for others; for example, within subfamily

Rutoideae pollen studies appear to be completely lacking in

tribe Boronieae, while in tribe Xanthoxyleae pollen studies

have been carried out for only four genera. Pollen accounts for

Rutaceae include: Arreguın-Sanchez et al. (1995), Barth 1980,

1982, 1983, 1985; Correa et al. (1992), Erdtman (1952), Grant

et al. (2000), Harley (1986), Lobreau-Callen et al. (1975),

Morton & Kallunki (1993), Mziray (1992), Rasolodimby

(1983), Victor & Van Wyk (1998, 1999a, b, 2001). The pollen of

the small, predominantly pantropical, family Simaroubaceae

has not been extensively studied. Probably the most compre-

hensive account remains that of Basak (1963) for Indian

members of the family. The pollen of Anacardiaceae is also

generally distinguishable from that of Burseraceae (Erdtman

1952, Baksi 1976, Ibe & Leis 1979). Notably, a distinctly striate

exine – which is not particularly common among colporate

edicots – is fairly common in the Sapindales, including:

Anacardiaceae, Rutaceae, Sapindaceae, Simaroubaceae, as

well as in Burseraceae.

MATERIAL AND METHODS

The pollen data presented are based on extensive sampling of all

currently recognised genera of Burseraceae with the exception of the

recently described Pseudodacryodes Pierlot (1987) for which no

pollen material is currently available (Pierlot: pers. comm.). Pollen

data for tribe Protieae (Crepidospermum, Garuga, Protium, Tetra-

gastris) are already published (Harley & Daly 1995), while accounts

of the pollen morphology of tribes Bursereae (Aucoumea, Beiselia,

Boswellia, Bursera, Commiphora, Triomma) and Canarieae (Canar-

ium, Dacryodes, Haplolobus, Pseudodacryodes, Rosselia, Santiria,

Scutinanthe, Trattinnickia) are in progress.

Pollen preparation methods for light microscopy (LM), scanning

electron (SEM) and transmission electron microscopy (TEM) follow

the protocols described in Harley & Daly (1995), including the

methods for calculating and defining endoaperture shape, endoa-

perture width and colpus length relative to overall pollen size.

Endoaperture shape index (ENSI) for lalongate endoapertures

(Table I) – the result of dividing the average polar length of the

endoaperture by the average equatorial width (E) of the pollen

grain. The endoaperture shape is interpreted: 3.6 or more, per-

lalongate; 2.6 – 3.5 average lalongate; 2.5 or less, brevi-lalongate.

Endoaperture width index (ENWI) for lalongate endoapertures

(Table II) – the average equatorial width of the endoaperture in

proportion to the average equatorial width of the pollen grain. The

average equatorial width of the endoaperture 63, is divided by two,

and the result divided into the average equatorial width of the

pollen grain. The endoaperture width index is interpreted: 1.45 or

less, very wide; 1.46 – 2.0, wide; 2.01 – 2.50, average; 2.51 – 3.00,

short; 3.01w, very short [NB. The reasoning for the first part of the

calculation is based on the equatorial width of the pollen grain, in

LM, being a planar dimension, whereas the width occupied by the

endoapertures, is effectively 3-dimensional. Dividing the sum total

of the three endoapertures by two provides a measurement which is

more compatible with the equatorial width of the pollen grain]. The

colpus length index (CLI) see Table III, is the result of dividing the

average colpus length into the average polar length of the pollen

grain (P). The colpus length is interpreted: v1.05 – 1.35, long;

1.36 – 1.69, average; 1.70 – 2.00w, short.

Terminology follows Segaar & Van der Ham (1993), Punt et al.

(1994 & the updated website version at: http://www.bio.uu.nl/palaeo/

glossary/ ), Harley & Daly (1995).

RESULTS

As well as our unpublished pollen data for tribes Bursereae

and Canarieae (MH, US, HB) we have drawn on the

following published sources for our morphological data:

Segaar & Van der Ham (1993), Forman et al. (1989, 1994),

Harley & Daly (1995), Harley & Hall (1999). The pollen

types described here focus on the major differences in pollen

morphology within the family. Some of these major types

include the more finely delimited types from the pollen

account of tribe Protieae (Harley & Daly 1995), where

species and collection data for all species studied for tribe

Protieae are given. Full lists of species and collections

studied will also be provided for tribes Bursereae and

Canarieae when the tribal pollen morphological accounts for

Bursereae (M. Harley: in prep.) and Canarieae (M. Harley:

in prep.) are published.

General pollen morphology (Tables IV & V)

Pollen grains usually isopolar, rarely heteropolar. Aperture

system tricolporate, rarely tricolporate lobed-vestibulate or

triporate projectate; aperture disposition usually fossapertu-

rate, angulaperturate less frequently planaperturate. Pollen

Table I. Endoaperture shape index (ENSI).

(Harley & Daly 1995).

Endoaperture shape Index

PER-LALONGATE 3.6 or moreAVERAGE LALONGATE 3.5 – 2.6BREVI-LALONGATE 2.5 or less

Table II. Endoaperture width index (ENWI).

(Harley & Daly 1995).

Endoaperture Width index

VERY WIDE 1.45 or lessWIDE 1.46 – 2.00AVERAGE 2.01 – 2.50SHORT 2.51 – 3.00VERY SHORT 3.01 or more

Table III. Colpus length index (CLI).

(Harley & Daly 1995).

Colpus Length index

LONG 1.35 – 1.05 or lessAVERAGE 1.36 – 1.69SHORT 1.70 – 2.00 or more

Pollen of Burseraceae 283

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

shape either suboblate, oblate-spheroidal, spheroidal, pro-

late-spheroidal, subprolate, prolate or, rarely, per-prolate;

outline in polar view circular, rounded triangular, triangular,

triangular-lobed, hexagonal or triangular projectate.

Pollen size: polar length (P) – 17 – 46 mm, rarely to

83 mm; equatorial width (E) – 14 – 40 mm, rarely to

73 mm. Endoapertures lalongate, circular, subcircular or,

rarely, lolongate; endoaperture shape (see Table I for

shape index) for lalongate endoapertures: per-lalongate,

average lalongate or brevi-lalongate; endoaperture width

(see Table II for width index) for lalongate endoapertures:

very wide, wide, average, short or very short; colpus

length (see Table III for length index): long, average or

short. Costae either absent or, more frequently, present

and either polar oriented and sickle-shaped or circular or,

less frequently, meridionally extended parallel to colpus

margines, and tapered toward apices; in light microscopy

they may appear indistinct, distinct, or very pronounced,.

Exine tectate or semitectate and either psilate, psilate-

perforate, foveolate, low relief rugulate, scabrate-rugulate,

perforate-rugulate, striate, striate-perforate, striate-reticu-

late, spinulose, micro-reticulate spinulose, reticulate or

foveolate-spinulose, supra-reticulate clavate, coarsely reti-

culate with shallow lumina and psilate rounded muri or

very coarsely reticulate with deep lumina and psilate

sharply angular muri. Apocolpial wall thickness: 1 – 5 mm;

infratectum columellate or granular or, occasionally,

granular-columellate; apocolpial ultrastructure: between

taxa the thicknesses of the ectexine layers (tectum,

infratectum and foot layer) vary relative to each

other (Table IV: 11a – c); endexine: generally thin or

absent in mesocolpial areas, present and thicker in

apertural areas, even thicker in endoapertural region,

rarely present at apocolpia.

The major pollen types (summarised in Tables IV – VI)

1. ‘Protium type’ (Fig. 1A, B, D – F, J – L, P, Q)

Isopolar, tricolporate and angulaperturate - fossaperturate;

prolate spheroidal, sub prolate, prolate or, rarely, per-

prolate; outline in polar view rounded triangular; pollen

size: P – 31.8 (22 – 46) mm, E – 24.5 (14 – 37) mm; colpus

length: short, average or long; endoapertures lalongate;

endoaperture shape: per, average or brevi; endoaperture

width: average, wide or very wide, sometimes almost

merging to form an endocingulum (Fig. 1E, F); costae

distinct, sickle-shaped, polar oriented; exine tectate and

psilate, or psilate-perforate; apocolpial wall thickness

1 – 2.5 mm, apocolpial ultrastructure: tectum and foot layer

thick, infratectum thin or very thin, infratectum granular-

columellate, no apocolpial endexine.

Taxa included. – Tribe Protieae: Protium (most spp.) – Tro-

pical S. America; Tetragastris (all) – Tropical N. & S.

America; Crepidospermum (all) – Tropical S. America;

Tribe Canarieae: Trattinnickia (most) – Tropical S. Amer-

ica; Dacryodes (some) – S. America, Africa & Asia; Haplo-

lobus (some) – Malesia & Pacific; Santiria (some) – OW

Tropics; Scutinanthe brevisepala – Sri Lanka to Sulawesi.Ta

ble

IV.

Su

mm

ary

of

no

n-a

per

tura

lch

ara

cter

isti

csfo

rea

chp

oll

enty

pe.

[gen

era

la

bb

rev

iati

on

use

din

mo

reth

an

on

eco

lum

n:

n/d

–n

od

ata

]1.

Po

llen

typ

e;2.

Po

lari

ty:

het

–h

eter

op

ola

r,is

o–

iso

po

lar;

3.

Ou

tlin

ein

po

lar

vie

w:

C–

circ

ula

r,H

X–

hex

ago

nal,

RT

–ro

un

ded

tria

ngu

lar,

T–

tria

ng

ula

r,T

L–

tria

ngu

lar

lob

ed,

TP

–tr

ian

gu

lar

pro

ject

ate

;4.

Len

gth

po

lar

axis

(P);

5.

Wid

theq

uato

rial

axis

(E);

6.

Sh

ap

e:O

S–

ob

late

sph

ero

idal,

P–

pro

late

,P

p–

per

pro

late

,P

S–

pro

late

sph

ero

idal,

S–

sph

ero

idal,

SO

–su

bo

bla

te,

SP

–su

bp

rola

te;

7.

Exin

ety

pe:

ST

–se

mi-

tect

ate

,T

–te

ctate

;8.

Exin

esu

rface

:b

r–

bre

vi,

cla

–cl

avae,

cor

–co

ars

e,fo

v–

foveo

late

,h

-rel

–h

igh

reli

ef,

l-re

l–

low

reli

ef,

mu

-an

g–

mu

rian

gu

lar,

mic

–m

icro

,m

u-r

o–

mu

riro

un

ded

,p

erf

–p

erfo

rate

,p

si–

psi

late

,re

t–

reti

cula

te,

rug

–ru

gu

late

,sc

a–

scab

rate

,sp

l–

spin

ulo

se,

str

–st

riate

,v-c

or

–ver

yco

ars

e;9.

Ap

oco

lpia

lw

all

thic

kn

ess;

10.

Ap

oco

lpia

lu

ltra

stru

ctu

re(i

nfr

ate

ctu

mco

mp

osi

tio

n):

col

–co

lum

ella

te,

gra

–

gra

nu

lar,

irr

–ir

regu

lar;

11a.

Ap

oco

lpia

lu

ltra

stru

ctu

re(i

nfr

ate

ctu

m):

vte

c–

thin

ner

than

tect

um

,wte

c–

thic

ker

than

tect

um

,vte

c–

sim

ilar

tote

ctu

m;1

1b

.Ap

oco

lpia

lult

rast

ruct

ure

(tec

tum

):v

fl–

thin

ner

than

foo

tla

yer

,

wfl

–th

ick

erth

an

foo

tla

yer

,vfl

–si

mil

ar

tofo

ot

layer

;11c.

ap

oco

lpia

lult

rast

ruct

ure

(fo

ot

layer

):v

inf

–th

inn

erth

an

infr

ate

ctu

m,w

inf

–th

ick

erth

an

infr

ate

ctu

m,v

inf

–si

mil

ar

toin

fra

tect

um

;12.A

po

colp

iale

nd

exin

e:A

–

ab

sen

t,P

–p

rese

nt.

12

34

(mm

)5

(mm

)6

78

9(m

m)

10

11

a11

b1

1c

12

1.

Pro

tium

typ

eis

oR

T,

T22

–46

14

–37

PS

,S

P,

P,

(Pp

)T

psi

,p

si-p

erf

1–

2.5

gra

-co

lv

tec

vfl

win

fA

2.

Canari

um

typ

eis

oT

,RT

,TL

18

–57

15

–44

SP

,PS

(P,O

S)

Tst

r-

l-re

l,h

-rel

,co

,b

r1

–3

col

vte

c/v

tec

vfl

vin

f/w

inf

A

3.

Pro

tium

sagoti

anum

typ

eis

oR

T26

–43

21

–34

SP

-PS

(P)

Tp

si-

co-p

erf/

fov

1.5

–2

.5co

lv

tec/

vte

cvfl

vin

f/w

inf

A

4.

Pro

tium

poly

botr

yum

typ

eis

oR

T-C

17

–39

18

–40

OS

-PS

ST

mic

-ret

,sp

i1

–4

col

wte

cvfl

vin

fA

5.

Canari

um

ole

ifer

um

typ

eis

oR

T29

–32

29

–33

OS

ST

co-c

la4.5

n/d

n/d

n/d

n/d

n/d

6.

Garu

ga

typ

eis

oR

T36

–83

33

–73

SP

-PS

Tp

si-p

erf,

l-re

lst

r,ru

g2

–4

col/

gra

-irr

vte

cvfl

vin

fA

7.

Auco

um

eaty

pe

iso

T36

–40

37

–42

OS

Tp

si-p

erf

3.5

–4

col-

irr

vte

cv

flw

inf

A

8.

Co

mm

iph

ora

typ

eis

oC

(TL

,HX

)22

–38

23

–40

OS

-PS

ST

fov/r

et-s

pl

(sca

-sp

l)1

–4

col

wte

cvfl

vin

fA

9.

Tri

om

ma

typ

eis

oR

T-C

21

–27

23

–28

OS

Tsc

a-s

pl

1–

2.5

col

wte

cw

flv

inf

P

10.

Burs

era

typ

eis

oT

L17

–41

16

–39

OS

-PS

ST

str

1–

3co

lv

tec/

vte

cvfl

vin

f/w

inf

A

11.

Pro

tium

robust

um

typ

eis

oR

T19

–24

21

–25

OS

ST

co-r

et,

mu

-ro

-psi

1.5

col

vte

cvfl

win

fA

12.

Ross

elia

typ

eis

oR

T26

–30

26

–31

OS

-PS

ST

co-r

et,

mu

-an

g-p

si3

–4

col

vte

cw

flv

inf

A

13.

Canari

um

gra

cile

typ

eis

oT

P21

–30

28

–35

SO

Tsc

a-r

ug

1.5

–2

.5n

/dn

/dn

/dn

/dn

/d

14.

Scu

tinanth

ebru

nnea

typ

eh

etT

L24

–28

32

–39

SO

Tco

-per

f-ru

g1

–3

gra

vte

cw

flw

inf

A

284 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

Table V. Summary of aperture characteristics for each pollen type.

[general abbreviation used in more than one column: n/a – not applicable].1. Pollen type; 2. Aperture system: tric – tricolporate, tric-lo-ves – tricolporate, lobed-vestibulate, trip-pro – triporate projectate; 3.Aperture disposition: AN – angul-fossaperturate, PL – planaperturate; 4. Endoaperture shape: C – circular, LA – lalongate, LO –lolongate, SC – subcircular; 5. Costae: C – circular, D – distinct, Ind – indistinct, Mex – meridionally extended, parallel to colpusmargines, tapered towards colpus apices, Pol – polar oriented, Pro – very pronounced, Sic – sickle-shaped; 6. Colpus length: A – average,L – long, S – short; 7. Endoaperture shape: AL – average lalongate, BL – brevi-lalongate, PL – per-lalongate; 8. Endoaperture width: A– average, S – short; VS – very short, VW – very wide, W – wide.

1 2 3 4 5 6 7 8

1. Protium type tric AN LA D, Pro, Pol, Sic S, A, L PL, AL, BL A, W, VW2. Canarium type tric AN LA Ind/D, Pol, Sic A, L PL, AL, BL S, A, W (VS, VW)3. Protium sagotianum type tric AN LA D, Pol, Sic A, L PL, AL, BL S, A, W (VS, VW)4. Protium polybotryum type tric AN LA D, Pol, Sic A, L PL, AL, BL VS, S, A5. Canarium oleiferum type tric PL LA D, Pol, Sic A PL A6. Garuga type tric AN LA D, Pol, Mex S, A, L PL, AL, BL VS, S, A, W, VW7. Aucoumea type tric AN C, LA D, C S n/a VS8. Commiphora type tric AN C, LA, (LO) D, Pro, C S (L) BL S9. Triomma type tric AN C D, C S n/a VS10. Bursera type tric AN LA Pro, Pol, Sic S (A) PL, AL, BL A, W11. Protium robustum type tric AN LA D, Pol, Sic L AL VS12. Rosselia type tric PL LA D, Pol, Sic S BL VS13. Canarium gracile type trip-pro AN C/SC Pro, Pol, C n/a n/a n/a14. Scutinanthe brunnea type tric-lo-ves AN SC n/a S BL VS

Table VI. Tribal distribution of pollen types within Burseraceae.

POLLEN TYPE PROTIEAE BURSEREAE BURSEREAE CANARIEAEtribe Boswelliinae Tribe Burserinae

Type 1. ‘Protium’ Protium (most) Trattinnickia (most)Tetragastris (all) Dacryodes (some)Crepidospermum (all) Santiria (some)

Haplolobus (some)Scutinanthe brevisepala

Type 2. ‘Canarium’ Protium (few) Beiselia mexicana Trattinnickia (few)Dacryodes (some)Santiria (some)Haplolobus (some)Canarium (most)

Type 3. ‘Protium sagotianum’ Protium sagotianum Canarium polyphyllum

Protium tenuifolium Canarium sumatranum

Dacryodes rostrata

Type 4. ‘Protium polybotrum’ Protium carnosum Canarium acutifolium

Protium crassipetalum Canarium harveyi

Protium polybotryum Canarium paniculatum

Canarium trifoliolatumType 5. ‘Canarium oleiferum’ Canarium oleiferum

Type 6. ‘Garuga’ Garuga (all) Boswellia (all)Type 7. ‘Aucoumea’ Aucoumea klaineana

Type 8. ‘Commiphora’ Commiphora (all)Bursera glabrifolia

Bursera grandifolia

Bursera malacophylla

Type 9. ‘Triomma’ Triomma malaccensis

Type 10. ‘Bursera’ Bursera (most)Type 11. ‘Protium robustum’ Protium robustum

Type 12. ‘Rosselia’ Rosselia bracteata

Type 13. ‘Canarium gracile’ Canarium gracile

Type 14. ‘Scutinanthe brunnea’ Scutinanthe brunnea

Pollen of Burseraceae 285

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

286 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

WPSF pollen types included (Harley & Daly 1995). – Protium

cubense-type; Protium macgregorii-type; Protium strumo-

sum-type; Crepidospermum goudotianum-type; Tetragastris

mucronata-type.

2. ‘Canarium type’ (Fig. 1C, G – I, M – O, R)

Isopolar, tricolporate and angulaperturate; usually subpro-

late, sometimes prolate spheroidal, rarely, prolate or oblate

spheroidal; outline in polar view triangular, rounded

triangular or, sometimes, triangular lobate; pollen size: P

– 19.6 – 50.0 (18 – 57) mm, E. – 17.0 – 41.4 (15 – 44) mm;

colpus length: long or average; endoapertures lalongate;

endoaperture shape: brevi, average or per; endoaperture

width: wide, average, short, rarely, very short or very wide;

costae indistinct to distinct , sickle-shaped, polar oriented;

exine tectate with fine low or high relief striate to coarsely

striate, aligned or non aligned, occasionally brevi-striate,

striate-perforate or, rarely, striae transversely ridged;

apocolpial wall thickness 1 – 3 mm, apocolpial ultrastructure:

foot layer, tectum, infratectum columellate and similar in

thickness, or infratectum may be thinner, no apocolpial

endexine.

Taxa included. – Tribe Protieae: Protium (a few mainly OW

Tropics spp.); Tribe Bursereae: Beiselia mexicana – Mexico;

Tribe Canarieae: Dacryodes (some) – Tropical S. America;

Africa; Asia; Santiria (some) – OW Tropics; Haplolobus

(some) – Malesia and Pacific; Canarium (most) – OW Tro-

pics.

WPSF types included (Harley & Daly 1995). – Protium fimbria-

tum-type; Protium apiculatum-type; Protium connarifolium-

type; Protium serratum-type; Protium urophyllidium-type;

Protium javanicum-type; Protium madagascariense-type.

3. ‘Protium sagotianum type’ (Fig. 2A, D, G, J – L)

Isopolar, tricolporate and angulaperturate; prolate spheroidal,

subprolate or, less commonly, prolate; outline in polar view

rounded triangular; pollen size: P – 30.8 (26 – 43) mm, E – 25.8

(21 – 34) mm; colpus length: average or long; endoapertures

lalongate; endoaperture shape: per, average or brevi; endoa-

perture width: short, average or wide; costae distinct, sickle-

shaped, polar oriented; exine tectate and psilate with coarse

perforations or foveolae frequently denser and/or coarser in

apolcolpial area; apocolpial wall thickness 1.75 – 2.5 mm,

apocolpial ultrastructure: tectum, foot layer and columellate

infratectum more or less equal in thickness or, infratectum may

be thinner, no apocolpial endexine.

Taxa included. – Tribe Protieae: Protium sagotianum, P.

tenuifolium – Peru, Trinidad, Costa Rica; Tribe Canar-

ieae: Canarium polyphyllum, C. sumatranum – Sumatra,

Malay Peninsula; Dacryodes rostrata – Malesia.

WPSF type included (Harley & Daly 1995). – Protium sagotia-

num-type.

4. ‘Protium polybotryum type’ (Fig. 2B, E, H, I, M – O)

Isopolar, tricolporate and angulaperturate; oblate spheroi-

dal to prolate spheroidal; outline in polar view rounded

triangular to circular; pollen size: P – 26 (17 – 39) mm, E –

25.4 (18 – 40) mm; colpus length: average or long; endoa-

pertures: lalongate, endoaperture shape: brevi, average or

long; endoaperture width: average, short or very short;

costae distinct, sickle-shaped, polar oriented; exine semi-

tectate and micro-reticulate, spinulose; apocolpial wall

thickness: 1 – 2 mm or 3 – 4 mm; apocolpial ultrastructure:

tectum and foot layer similar in thickness, infratectum

columellate and wider, no apocolpial endexine.

Taxa included. – Tribe Protieae. – Protium carnosum,

P. crassipetalum, P. polybotryum – Brazil, Surinam;

Tribe Canarieae: Canarium acutifolium, C. harveyi, C.

paniculatum, C. trifoliolatum – Mascarenes, Mauritius,

Fiji, New Guinea, New Caledonia.

WPSF type included (Harley & Daly 1995). – Protium polybo-

tryum-type.

5. ‘Canarium oleiferum type’ (Fig. 2C, F, P – R)

Isopolar, tricolporate and planaperturate; oblate spheroidal;

outline in polar view rounded triangular; pollen size: P – 30.7

(29 – 32) mm, E – 30.9 (29 – 33) mm; colpus length: average;

endoapertures lalongate; endoaperture shape: per; endoaper-

ture width: average; costae distinct, sickle-shaped, polar-

oriented; exine semitectate, coarsely and densely clavate;

apocolpial wall thickness c. 4.5 mm, apocolpial ultrastructure

unknown (embedded but not yet thin sectioned), however,

from light microscopy it appears that the clavae project from a

thin, finely reticulate tectum beneath which is a columellate

infratectum and a thin foot layer.

Taxon included. – Tribe Canarieae: Canarium oleiferum –

New Caledonia.

6. ‘Garuga type’ (Fig. 3A – F)

Isopolar, tricolporate and angulaperturate; prolate spher-

oidal or subprolate; outline in polar view rounded

triangular; pollen size: P – 55.5 (36 – 83) mm, E – 43.8

(33 – 73) mm [NB. Boswellia: P – 61.7 (43 – 83) mm, E – 44.9

(40 – 73) mm; Garuga: P – 49.3 (36 – 62) mm, E – 42.8

(33 – 57) mm]; colpus length: short, average or long;

endoapertures lalongate; endoaperture shape: brevi, average,

or per [per-lalongate apparently confined to Boswellia];

Fig. 1. Type 1. ‘Protium’ [A, B, D – F, J – L, P, Q] and Type 2. ‘Canarium’ [C, G – I, M – O, R]. (A, P) Protium copal: (A) equatorialmesocolpial view (SEM), (P) polar plane (TEM). (B, Q) Crepidospermum multijugum: (B) equatorial colporus view (SEM), (Q) polarplane (TEM). (C) Canarium denticulatum, mescolpial view (SEM). (D) Protium ferrugineum close up of aperture (SEM). (E, F, L) Cre-

pidospermum rhoifolium, different grains, equatorial views – note extreme width of endoapertures (LM): (E) high-mid focus, (F) midfocus, (L) low focus. (G) Canarium strictum, close up of exine surface and colporus (SEM). (H) Canarium sylvestre, close up of meso-colpium surface (SEM). (I) Canarium muelleri, close up of mesocolpium surface (SEM). (J, K) Protium opacum, different grains, equa-torial views, both high-mid focus (LM). (M – O) Canarium baileyanum (LM): (M) polar view mid-low focus, (N) equatorial view highfocus, (O) equatorial view mid focus, same grain as ‘N’. (R) Protium javanicum, polar plane (TEM). Scale bar – 2.5 mm (D, G – I);5 mm (A – C & N – R); 7.5 mm (J – M); 10 mm (E, F).

Pollen of Burseraceae 287

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

288 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

endoaperture width: variable: very short, short, average,

wide or very wide [very short and very wide apparently

confined to Garuga]; costae distinct, meridionally extended,

parallel to colpi, broad at equator and tapered to a point at

colpus apices (i.e. a very elongated triangle); exine tectate

and psilate-perforate, less frequently low relief striate or

rugulate mesocolpia [differentiation of mesocolpia more

common in Garuga]; apocolpial wall thickness 2 – 4 mm,

apocolpial ultrastructure: foot layer, tectum and irregularly

columellate infratectum similar in thickness, columellae

sometimes interspersed with granular elements, no apoc-

olpial endexine.

Taxa included. – Tribe Protieae: Garuga (all) – Himalayas,

Indo-Malaya to W. Pacific; Tribe Bursereae: Boswellia

(all) – OW Tropics.

WPSF type included (Harley & Daly 1995). – Garuga flori-

bunda-type.

7. ‘Aucoumea type’ (Fig. 4A – G)

Isopolar, tricolporate and angulaperturate; oblate spheroi-

dal; outline in polar view triangular; pollen size: P – 37.8

(36 – 40) mm, E – 39.6 (37 – 42) mm; colpus length: short;

endoapertures lalongate or circular; endoaperture shape:

Fig. 2. Type 3. ‘Protium sagotianum’ [A, D, G, J – L], Type 4. ‘Protium polybotryum’ [B, E, H, I, M – O] and Type 5. ‘Canarium olei-ferum’ [C, F, P – R]. (A, J – L) Protium tenuifolium var. sessiliflorum – (A, L) Tonduz 6989, (J – K) Tonduz 9952: (A) equatorial view(SEM), (J, K) same grain, equatorial view, high focus and mid focus, (L) polar view, high focus. (G) Protium tenuifolium, close up ofexine surface and colporus (SEM). (B) Protium polybotryum, equatorial mesocolpial view (SEM). (C, F, P – R) Canarium oleiferum: (C)equatorial mesocolpial view (SEM), (F) close up of exine surface and colporus (SEM), (P) polar view, high focus (LM), (Q) polarview, high focus (LM), (R) polar view, mid focus (LM). (D) Protium sagotianum, polar plane (TEM). (E, H) Protium crassipetalum:(E) polar plane (TEM), (H) close up of exine surface and colporus (SEM). (I) Canarium harveyi, close up of mesocolpium surface(SEM). (M – O) Canarium schweinfurthii (LM): (M) equatorial view, low-mid focus, (N) equatorial view, mid focus – different grain,(O) polar view, mid focus. Scale bar – 5 mm (A – E, J – R); 2.5 mm (F – I).

Fig. 3. Type 6. ‘Garuga’ [A – F]. (A) Boswellia papyrifera, equatorial mesocolpial view (SEM). (B) Garuga pierrei, equatorial colporusview (SEM). (C, D) Garuga pinnata (LM): (C) equatorial view, high-mid focus, (D) equatorial view, low focus, note elongate costae.(E) Boswellia dalzielii, close up of exine surface and colporus (SEM). (F) Garuga mollis, polar plane (TEM). Scale bar – 10 mm (A – B,D – I, K, M); 2.5 mm (C, J); 2 mm (L).

Pollen of Burseraceae 289

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

Fig. 4. Type 7. ‘Aucoumea’ [A – G] and Type 8. ‘Commiphora’ [H – M]. (A – G) Aucoumea klaineana: (A) polar plane (TEM), (B) equa-torial plane (TEM), (C) close up of exine surface and colporus (SEM), (D, E) same grain equatorial view, high and mid foci (LM), (F,G) same grain, polar view, mid and low foci (LM). (H – M) Commiphora: (H, I) C. sarandensis, equatorial view, high and mid foci(LM). (J) C. mossambicencis, close up of mesocolpial exine (SEM). (K) C. africana var. tubak, group of pollen grains in different orien-tations (SEM). (L) C. insisa, close up of exine surface and colporus (SEM). (M) C. mollis, polar plane (TEM). Scale bar – 5 mm (A –E, G – H); 10 mm (F, J – N); 2.5 mm (I).

290 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

brevi or circular; endoaperture width: very short; costae

distinct, circular; exine tectate and psilate-perforate; apoc-

olpial wall thickness 3.5 – 4.0 mm; apocolpial ultrastructure:

foot layer thick, tectum slightly thinner, infratectum very

thin irregular columellate, no apocolpial endexine.

Taxon included. – Tribe Bursereae: Aucoumea klaineana –

Trop. W. Africa.

8. ‘Commiphora type’ (Fig. 4H – M)

Isopolar, tricolporate and angulaperturate; oblate spheroi-

dal or prolate spheroidal; outline in polar view: circular,

less frequently lobed triangular or hexagonal; pollen size:

P – 26.5 (22 – 38) mm, E – 29.0 (23 – 40) mm; colpus length:

short or, rarely, long; endoapertures circular or lalongate,

less frequently lolongate; endoaperture shape: probably

brevi; endoaperture width: probably short; costae distinct,

or very distinct, more or less circular, less frequently sickle-

shaped, polar oriented; exine semi-tectate, foveolate or

reticulate spinulose, rarely scabrate-spinulose; apocolpial

wall thickness 1 – 4 mm; apocolpial ultrastructure: foot layer

and tectum thin, infratectum wide and columellate, no

apocolpial endexine.

Taxa included. – Tribe Bursereae: Commiphora (all) –

mostly subtropical and tropical Africa, Madagascar, a few

from Mexico, Cuba, Bahamas, Brazil; Bursera glabrifolia

(Mexico), B. grandifolia (Mexico), B. malacophylla (Ecua-

dor).

9. ‘Triomma type’ (Fig. 5A – C, H, J – L)

Isopolar, tricolporate and angulaperturate; oblate spheroi-

dal; outline in polar view rounded triangular to circular;

pollen size: P – 23.9 (21 – 27) mm, E – 25.05 (23 – 28) mm;

colpus length: short; endoapertures circular; endoaperture

width: very short; costae distinct, more or less circular; exine

tectate, exine topology scabrate-spinulose; apocolpial wall

thickness 1 – 2.5 mm; apocolpial ultrastructure: tectum thin,

foot layer very thin, infratectum columellate c. twice the

width of the tectum, distinct apocolpial endexine – thicker

than foot layer.

Taxon included. – Tribe Bursereae: Triomma malaccensis –

W. Malesia.

10. ‘Bursera type’ (Fig. 5D – G, I, M, N)

Isopolar, tricolporate, lobed and angulaperturate; oblate

spheroidal or prolate spheroidal; outline in polar view: lobed

triangular; pollen size: P – 26.3 (17 – 41) mm, E – 25.3

(16 – 39) mm; colpus length: short, less frequently average;

endoapertures lalongate; endoaperture shape: average or

per; endoaperture width: average or wide; costae very

distinct, sickle-shaped, polar oriented; exine semitectate,

distinctly striate – striae non-aligned or ‘woven’ or with

uni-directional alignment or striate-reticulate or striate

perforate; apocolpial wall thickness 1 – 3 mm; apocolpial

ultrastructure foot layer, tectal elements and columellate

infratectum similar in width or infratectum may be thinner,

no apocolpial endexine.

Taxon included. – Tribe Bursereae: Bursera (most) – Meso-

and tropical South America.

11. ‘Protium robustum type’ (Fig. 6A – E, J, K)

Isopolar, tricolporate and angulaperturate; oblate spheroidal;

outline in polar view rounded triangular; pollen size: P – 21.4

(19 – 24) mm, E – 22.5 (21 – 25) mm; colpus length: long;

endoapertures lalongate; endoaperture shape: average; endoa-

perture width: very short; costae distinct, sickle-shaped, polar

oriented; exine semi-tectate, and coarsely reticulate, lumina

shallow and bases sparsely granular, muri psilate and rounded;

apocolpial wall thickness c. 1.5 mm; apocolpial ultrastructure:

thick muri and foot layer, infratectum slightly thinner and

columellate, no apocolpial endexine.

Taxon included. – Tribe Protieae: Protium robustum –

Brazil.

WPSF type included (Harley & Daly 1995). – Protium robus-

tum-type.

12. ‘Rosselia type’ (Fig. 6F – I, L – N)

Isopolar, tricolporate and planaperturate; oblate spheroidal

to prolate spheroidal; outline in polar view rounded

triangular; pollen size: P – 28.2 (26 – 30) mm, E – 29.0

(26 – 31) mm; colpus length: short; endoapertures lalongate;

endoaperture shape: brevi; endoaperture width: very short;

costae distinct, sickle-shaped, polar oriented; exine semi-

tectate and very coarsely reticulate, lumina deep with

granular bases, muri psilate and angular; apocolpial wall

thickness 3 – 4 mm, apocolpial ultrastructure: muri thin and

pointed, supported by columellae of similar height and

width, foot layer thinner than the columellar layer or the

muri, no apocolpial endexine.

Taxon included. – Tribe Canarieae: Rosselia bracteata –

New Guinea (Rossel Island).

13. ‘Canarium gracile type’ (Fig. 7A, D, G, H)

Isopolar or subisopolar, triporate projectate, and angula-

perturate; suboblate; outline in polar view, triangular

projectate; pollen size: P – 25.9 (21 – 30) mm, E – 31.3

(28 – 35) mm; costae very pronounced, polar oriented, slight

meridional elongation; exine tectate, exine topology sca-

brate-rugulate; apocolpial wall thickness 1.5 – 2.5 mm, apoc-

olpial ultrastructure unknown.

Taxon included. – Tribe Canarieae: Canarium gracile Engl.

– Philippines.

14. ‘Scutinanthe brunnea type’ (Fig. 7B, C, E, F, I, J)

Heteropolar, tricolporate lobed vestibulate (rarely dicolpo-

rate lobed vestibulate) and angulaperturate, frequently (c.

75%) with radial asymmetry of polarisation for each

aperture lobe; suboblate; outline in polar view triangular

lobate; pollen size: P – 26.4 (24 – 28) mm, E – 34.5

(32 – 39) mm; colpus length: short; endoapertures subcircu-

lar, endoaperture shape: brevi; endoaperture width: very

short; costae not present; exine tectate, and coarsely

perforate-rugulate, aperture lobes more or less psilate with

Pollen of Burseraceae 291

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

Fig. 5. Type 9. ‘Triomma’ [A – C, H, J, K] and Type 10. ‘Bursera’ [D – G, I, M, N]. (A – C, H, J – L) Triomma malaccensis – (A – C, H, J)Yong 94742; (L) Kedah KFN27479: (A) equatorial view (SEM), (B) polar plane, endexine (arrows) underlies a very thin foot layer (TEM),(C) equatorial plane (TEM), (H) polar view (SEM), (J) equatorial view, high focus (LM), (K) equatorial view, mid focus (LM), (L) polarview, high-mid focus (LM). (D – G, I, M, N) Bursera: (D) B. confusa, equatorial view (SEM), (E – G, I) B. kerberi: (E) polar plane (TEM),(F) polar view (SEM), (G) equatorial plane (TEM), (I) close up of mesocolpial exine surface (SEM). (M – N) B. discolor: (M) equatorialview, high-mid focus (LM), (N) polar view, high-mid focus (LM). Scale bar – 5 mm (A – H); 2 mm (I); 10 mm (J – N).

292 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

Fig. 6. Type 11. ‘Protium robustum’ [A – E, J & K] and Type 12. ‘Rosselia’ F – I, L – N]. (A – E, J & K) Protium robustum: (A) equatorial col-porus view (SEM), (B) polar view (SEM), (C) close up of exine surface and colporus (SEM), (D) polar plane (TEM), (E) equatorial plane(TEM), (J) equatorial view, mid focus (LM), polar view, mid focus (LM). (F – I, L – N) Rosselia bracteata: (F) equatorial colporus view(SEM), (G) close up of mesocolpial reticulum (SEM), (H) polar plane (TEM), (I) equatorial plane (TEM), (L – M) different pollen grainsmid foci: (L) equatorial view, (M) alternative equatorial view, (N) polar view. Scale bar – 5 mm (A – B, D – F, H – N); 2.5 mm (C); 2 mm (G).

Pollen of Burseraceae 293

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

a few scattered indentations or perforations; apocolpial wall

thickness 1 – 3 mm, apocolpial ultrastructure: tectum very

irregular, at its thickest three times width of foot layer,

infratectum very thin, no apocolpial endexine.

Taxon included. – Tribe Canarieae: Scutinanthe brunnea -

Sri Lanka to Sulawesi.

KEY TO MAJOR TYPES IN BURSERACEAE

1a. Suboblate ………………………………………………2

1b. Not suboblate ……………………………………………4

2a. Apertures porate projectate … … … … … … … … …

… … … … … … … … … … … 3. ‘Canarium gracile type’

2b. Apertures not porate projectate ……………………… 3

3a. Apertures colporate, lobed vestibulate…………………

…………………… ……………4. ‘Scutinanthe brunnea type’

3b. Apertures colporate, not lobed vestibulate … … … 4

4a. Endoapertures with distinct, meridionally extended

costae, parallel to colpi … …………………6. ‘Garuga type’

4b. Endoapertures not as above … ………………………5

5a. Exine semi tectate, coarsely and densely supra-reticulate

clavate … ……………………5. ‘Canarium oleiferum type’

Fig. 7. Type 13. ‘Canarium gracile’ [A, D, G – H] and Type 14. ‘Scutinanthe Brunnea’ [B, C, E, F, I & J]. (A, D, G & H) Canarium

gracile: (A) group of grains in different orientations (SEM), (D) tilted equatorial view (SEM), (G) equatorial view, high-mid focus(LM), (H) polar view mid focus (LM). (B, C, E, F, I & J) Scutinanthe brunnea: (B) equatorial view with apertural lobe centre front(SEM), (C) section through apertural lobe, polar plane (TEM), (E) polar plane (TEM), (F) polar view (SEM) with lobes similarlypolarised, (I) equatorial view, mid focus (LM), (J) polar view, mid focus (LM) lobes asymmetrically polarised. Scale bar – 10 mm (A,I & J); 5 mm (B – H).

294 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

5b. Exine not as above … …………………………………6

6a. Exine coarsely reticulate ……………………………… 7

6b. Exine not as above …………………………………… 2

7a. Lumina very wide, and deep with angular muri

……………………………………8. ‘Rosselia bracteata type’

7b. Lumina wide, and shallow with rounded muri …

……………………………………11. Protium robustum type’

8a. Exine striate …………………………………………… 9

8b. Exine not striate ………………………………………10

9a. Outline in polar view strongly lobed-triangular, shape

spheroidal or prolate spheroidal …………10. ‘Bursera type’

9b. Outline in polar view triangular, or rounded triangular,

shape usually subprolate … ……………2. ‘Canarium type’

10a. Exine tectate, and psilate-perforate or foveolate …11

10b. Exine not as above ……………………………………13

11a. Shape oblate spheroidal, outline in polar view

distinctly triangular … …………………7. ‘Aucoumea type’

11b. Shape subprolate, prolate-spheroidal to prolate,

outline in polar view rounded triangular ………………12

12a. Psilate, usually finely perforate in mesocolpia, psilate

apocolpia …………………………………1. ‘Protium type’

12b. Coarsely perforate or foveolate, frequently more

pronounced in apocolpia ……3. ‘Protium sagotianum type’

13a. Exine spinulose, tectate ……………9. ‘Triomma type’

13b. Exine spinulose, semitectate … ……………………14

14a. Foveolate or reticulate, colpi usually short ……………

…………………………………………8. ‘Commiphora type’

14b. Microreticulate, colpi average to long…………………

………………………………4. ‘Protium polybotryum type’

DISCUSSION

The pollen types described are based on combinations of

varying aperture and exine morphology, as well as shape

and size. Of the 14 pollen types described 13 are

tricolporate, and range from oblate spheroidal to

prolate, characteristics frequently encountered in other

eudicotyledous families. Nevertheless, there are only four

pollen types where the overall combination of characteristics

is not obviously diagnostic to family level, these are,

‘Canarium type’, ‘Protium sagotianum type’, ‘Garuga type’

and ‘Protium robustum type’.

The pollen of Rosselia, originally described in Forman

et al. (1994), is not only unique within Burseraceae, it is also

unusual outside the family. In particular, the appearance of

the reticulum and the granulae in the bases of the lumina are

very similar to the reticulate pollen exine in some species of

Ruellia (Acanthaceae). However, the exine of Rosselia pollen

has a clearly defined foot layer while, in Ruellia, pollen with

a similar exine has no foot layer. Furthermore, in Ruellia

pollen there are 3, rarely 5, pores or, occasionally a short

colporus (Furness & Grant 1996).

The remaining nine pollen types are unique to Burser-

aceae, ‘Protium type’, ‘Protium polybotryum type’, ‘Canar-

ium oleiferum type’, ‘Aucoumea type’, ‘Commiphora type’,

‘Triomma type’, ‘Bursera type’, ‘Canarium gracile type’ and

‘Scutinanthe brunnea type’. Of these seven are represented by

only one species, ‘Canarium oleiferum type’, ‘Aucoumea

type’, ‘Triomma type’, ‘Protium robustum type’ ‘Rosselia

type’, ‘Canarium gracile type’ and ‘Scutinanthe brunnea

type’. The last two types represent extremely unusual

dicotyledonous pollen aperture morphologies. The distribu-

tion of pollen morphological types across the three most

widely accepted tribes of Burseraceae (Table VI) is inter-

esting, as it draws attention to some of the often debated

relationships within the family (Harley & Daly 1995).

Protium (147 species) is the largest genus of tribe Protieae

and Canarium (75 species) is the largest genus of tribe

Canarieae. The ‘Protium type’ (Fig. 1A, B, D – F, J – L, P,

Q) and the ‘Canarium type’ (Fig. 1C, G – I, M – O, R) share

some basic characteristics which are frequently encountered

in eudicot pollen: tricolpory, and a prolate spheroidal to

prolate shape, with a tectate exine. However, in the ‘Protium

type’ the often unusually wide endoapertures (Fig. 1E, F,

J – L), and a thin granular-columellate infratectum (Fig. 1P,

Q) are less commonly encountered than the smaller

endoapertures (Fig. 1N, O) and columellate infratectum

(Fig. 1P) of the ‘Canarium type’. Notably, however, with the

exception of the pollen of Beiselia mexicana, neither of these

pollen types occurs in tribe Bursereae.

In tribe Protieae all species of Tetragastris and Crepidos-

permum, as well as most Protium species have ‘Protium type’

pollen. A few species included in ‘Protium type’, particularly

in Crepidospermum, are distinguished by very wide endoa-

pertures which more or less form an endocingulum around

the equator of the grain (Fig. 1E, F & L); in all other

respects the pollen conforms to the ‘Protium type’. In

Protium there are a few Old World species: P. connarifolium

Merrill, P. javanicum Burm. f., P. madagascariense Engl., P.

obtusifolium Marchand, P. serratum (Wall. ex Colebr.) Engl.

and a few New World species: P. apiculatum Swart, P.

amazonicum (Cuatrec.) Daly (syn. P. fimbriatium Swart), P.

urophyllidium Daly which have pollen with a striate

‘Canarium type’ exine. In tribe Canarieae most species of

Trattinnickia and Scutinanthe brevisepala, have ‘Protium

type’ pollen, while in Dacryodes, Santiria and Haplolobus

some species have ‘Protium type’ pollen, and some species

have ‘Canarium type’ pollen. However, the majority of

Canarium species have striate ‘Canarium type’ pollen. It is

difficult to make clear distinctions between striate Protium

pollen, and the striate pollen in tribe Canarieae. Never-

theless, there are characters which, in a more refined

treatment of the ‘Canarium type, would probably support

the circumscription of one or two subtypes; for example,

shape – 60% of the Protium species included in ‘Canarium

type’ has prolate pollen, while in 97% of the Canarieae

species included the pollen is either prolate-spheroidal or

sub-prolate.

The coarsely perforate ‘Protium sagotianum type’

(Fig. 2A, D, G, J – L) and the microreticulate, spinulose

‘Protium polybotryum type’ (Fig. 2B, E, H, I, M – O) are also

represented only in tribes Protieae and Canarieae, albeit the

number of species in each case is few. The original ‘Protium

polybotryum type’ (Harley & Daly 1995) included three

Protium species, but now four species of Canarium are also

included. However, the exine surface and infratectum of the

New World Protium species are slightly different (cf.

Pollen of Burseraceae 295

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

Fig. 2H with Fig. 2I) and probably justify the distinction of

a subtype for the Canarium species included in this type.

The pollen of Canarium oleiferum (Fig. 2C, F & P – R) is

described here for the first time. It is one of the seven pollen

types in Burseraceae represented by only one species. The

clavate exine has not yet been thin-sectioned but, from light

microscopy, it appears that the clavae arise from a thin,

finely reticulate tectum beneath which is a columellate

infratectum and a thin foot layer; endexine also appears to

be present away from aperture areas.

The two genera included in the ‘Garuga type’ (Fig. 3A – F)

are usually placed in separate tribes, Garuga in Protieae, and

Boswellia in Bursereae, although a clearly defined suite of

characters which justify two distinct tribes has never been

fully resolved (Harley & Daly 1995). Both genera are from

the Old World: Garuga – Himalayas, Indomalaya to

western Pacific; Boswellia – Old World tropics, especially

Africa and India. The pollen is strikingly similar in the two

genera, and of a type commonly encountered in the

eudicotyledons, although within Burseraceae it is unique

to these two genera. The pollen type is based partly on size,

but mainly on the configuration of the colporate apertures

which have meridionally extended, tapering costae

(Fig. 3D). Notably, a DNA study of Burseraceae (Clarkson

et al. 2002) resolves Garuga and Boswellia as sister taxa.

The pollen of the monospecific genus Aucoumea

(Fig. 4A – G) is very distinctive both within and outside

the family. However, the characteristics of circular endoa-

pertures and circular costae are shared with two other

genera of Burseraceae: Triomma and Commiphora. All three

genera are in tribe Bursereae, although Triomma is in

subtribe Boswelliinae, and Commiphora is in subtribe

Bursereae (Table VI). Interestingly the ultrastructure of

Aucoumea pollen, thin infratectum, thick tectum and thick

foot layer is very similar to the ultrastructure of ‘Protium

type’ (cf. Fig. 1P, Q with Fig. 4A) but in other respects the

pollen is notably dissimilar.

‘Triomma type’ pollen (Fig. 5A – C, H & J – L) is

apparently unique in the family; in no other species of

Burseraceae is there pollen with an endexine which extends

across the apocolpial region (Fig. 5B). Furthermore, with

one rare exception in Commiphora – C. erosa Vollesen, it is

the only example of tectate spinulose pollen in the family.

Commiphora is the largest genus in the family with almost

200 species. Its pollen is distinctive and characteristic of the

genus (Fig. 4H – M). However, a few tropical American

species of the mainly Mexican genus Bursera, which is

considered to be closely related to the predominantly

African Commiphora, have been transferred to Commiphora:

C. leptophloeus (Mart.) Gillett (Gillett 1980), C. sarcopoda

(Paul G. Wilson) Rzed. & R. Palacios, C. tecomaca (DC.)

Rzed. & R. Palacios (Rzedowski & Palacios-Chavez 1985),

C. angustata (Griseb.) Moncada, C. glauca (Griseb.)

Moncada and C. inaguensis (Britton) Moncada (Moncada-

Ferrera 1989). Apart from the situation in C. inaguensis,

where two of the three collections which have been

examined have Bursera-like pollen, the pollen data strongly

supports the transfer of these species to Commiphora. The

DNA study by Clarkson et al. (2002) also supports a close

relationship between Commiphora and Bursera. In addition

there are other Bursera species which have Commiphora-type

pollen: B. glabrifolia Engl, B. grandifolia Engl. and B.

malacophylla Robinson.

The ‘Bursera type’ (Fig. 5D – G, I, M, N), like the

‘Canarium type’, has a striate exine. However, the striae

are more strongly pronounced in Bursera pollen and often

have a distinctly reticulate underlying structure (cf. Fig. 1H,

I with Fig. 5F, I). Furthermore, the striae, combined with a

triangular, trilobate outline in polar view, short colpi

(usually) and pronounced costae give the pollen of Bursera

a characteristic and unique appearance.

In ‘Protium robustum type’ (Fig. 6A – E, J & K) the colpi

are very long with a small apocolpial area (Fig. 6B). A

coarsely reticulate exine is rare in the family, the only other

example being the pollen of ‘Rosselia bracteata type’.

However, the reticulum and ultrastructure are strikingly

different between the two species. In P. robustum (Fig. 6C)

the lumina are small and shallow, the muri wide and

rounded, and the columellae short, while in R. bracteata

(Fig. 6F – I, M & N) the lumina are large and deep, the muri

narrow and angular and the columellae long.

‘Canarium gracile type’ (Fig. 7A, D, G & H) is the second

of two previously undescribed Burseraceae pollen types,

both are in Canarium. The three sub equatorial, porate,

projectate apertures are probably unique among extant

angiosperms, and it is all the more remarkable for occurring

in a large (c. 75 spp.) genus where all other species have

pollen which is isopolar and tricolporate. The best known

examples of tri-projectate pollen are those produced by

some members of the Loranthaceae (Feuer & Kuijt 1979);

these appear to have some affinity with the fossil pollen

genus Aquilapollenites Rouse (Rouse 1957). However, the

Loranthaceous examples are extreme triprojectate, syncol-

pate, and decidedly unlike the pollen of Canarium gracile.

Pollen of some species of Persoonia (Proteaceae) (Feuer

1986) has greater similarity to the pollen of C. gracile, but

there are two important differences: the porate projections

are strongly oriented towards one pole, and not visible when

viewed from the opposing pole which is not the case with C.

gracile. Secondly, in C. gracile pollen the porate projections

have very distinct costate thickenings (Fig. 7G, H) which are

not present in Persoonia pollen (Feuer 1986).

The pollen morphology of Scutinanthe brunnea (Fig. 7B,

C, E, F, I & J) is also very unusual, and this is amplified by

the simple, isopolar and tricolporate pollen of the only other

species of the genus: S. brevisepala Leenh. A detailed

description and discussion of the curious heteropolar pollen,

frequently with radially asymmetric polarisation of each

aperture lobe, was provided by Segaar & Van der Ham

(1993). There is no comparable pollen in extant angios-

perms. However, Segaar and Van der Ham (1993) discuss

the ‘‘shift’’ of the ecto- and endoaperture to opposite non

equatorial positions, and cite the example of the fossil

Normapolles group, where this unusual irregularity is also

known to occur (see Batten & Christopher 1981). The

Normapolles group was first proposed by Pflug (1953) to

include fossil pollen grains distinctly different from pollen

produced by living angiosperms. The first representatives are

noted from the middle Cenomanian, followed by rapid

diversification throughout the remainder of the Cretaceous

296 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

and early Tertiary, but by the end of the Eocene they have

become virtually extinct. There a number of examples of

Normapolles pollen bearing notable similarity to ‘Scuti-

nanthe brunnea type’, for example, some species of

Emscheripollis Krutsch, Trudopollis Pflug (Pacltova 1981)

and Plicapollis Pflug (Mikhelis 1981). A great many genera

have been described for dispersed pollen assigned to the

Normapolles group (see for example, Batten & Christopher

1981). So far, however, fossil flowers with in situ

Normapolles type pollen (see Friis et al. 2003 for summary)

have been associated with the Fagales (sensu APG 1998,

2003). The fossil flowers are very small and usually bisexual.

While the inflorescences of Scutinanthe brunnea have small

(c. 3 – 5 mm long) unisexual flowers; the male flowers have

8 – 10 stamens and the female flowers have 2-celled ovaries

and one-seeded fruits. Unisexual fossil flowers with

Normapolles type pollen are rare, they include Bedellia

(Sims et al. (1999) and Endressianthus (Friis et al. 2003). The

suggested affinity for both genera is with Betulaceae (Sims

et al. (1999, Friis et al. 2003).

CONCLUSIONS

The pollen morphology of Burseraceae is extremely varied in

both exine and aperture variants, and includes a number of

pollen types unique to the family. Of 14 major pollen types

seven of the more unusual types are represented by only one

taxon; three of the taxa represent monospecific genera. It is

particularly remarkable that the family has two outstanding

examples of pollen with highly modified aperture systems.

One, Scutinanthe brunnea, shares similarities with some taxa

in the extinct Normapolles group, while the other, Canarium

gracile, occurs in a genus with generally unspecialised

tricolporate pollen. A substantial number of taxa in tribes

Protieae and Canarieae share the characteristics of pollen

types 1 to 4, and these are morphologically the least

specialised pollen types in the family. With the exceptions of

the pollen of Beiselia mexicana and Boswellia spp. the pollen

of tribe Bursereae is highly distinctive, and unique to the

tribe. Nevertheless, tribe Canarieae also includes four very

distinctive, monospecific pollen types. Pollen morphology

and DNA data support the long held opinion of a close

relationship between Bursera and Commiphora (Bursereae)

and, perhaps most interestingly, pollen morphology and

DNA data suggest a relationship between Garuga and

Boswellia which supports Daly’s comment (in Harley &

Daly 1995) that ‘‘Garuga is a morphological outlier in the

Protieae and should probably be transferred to the

Bursereae.’’

ACKNOWLEDGEMENTS

We thank the staff of the Leiden and Utrecht Herbaria for

permitting MMH to remove pollen samples from their Herbarium

collections, especially for tribe Canarieae. We also thank Dr Andrea

Weeks, University of Texas at Austin, for sending us samples of

Bursera pollen; as well as our reviewers Dr Raymond Van der Ham

and Dr Douglas Daly for their helpful comments on the submitted

manuscript.

SPECIMENS ILLUSTRATED

Aucoumea klaineana Pierre, Klaine 100, Gabon (K)

Boswellia dalzielii Hutch., Dalziel 279, Nigeria (K)

Boswellia papyrifera (Del.) Hochst., Eggeling 1238, Uganda (K)

Bursera confusa (Rose) Engl., Hinton 7772, Mexico (K)

Bursera discolor Rzed., Hinton et al. 7736, Mexico (K)

Bursera kerberi Engl., Hinton 10429, Mexico (K)

Canarium baileyanum Leenh., Kew Herbarium No. 227, Australia

(K)

Canarium denticulatum Blume, Parkinson 19, Andaman Isls. (K)

Canarium gracile Engl., Ramos 1130, Philippines (U)

Canarium harveyi Seem., A.C. Smith 1151, Fiji (K)

Canarium muelleri F.M. Bailey, Herbarium Lugd. Bat. 401390,

Australia (L)

Canarium oleiferum Baill., de Alleizette s.n., New Caledonia (L)

Canarium paniculatum Benth. ex Engl., Vaughan 12515, New

Guinea (K)

Canarium strictum Roxb., Venkata Reddi 99026, India (L)

Canarium sylvestre Gaertn., Robinson 878, Philippines (L)

Commiphora africana (A. Rich.) Engl. var. tubuk (Sprague)

Gillett, Carter 886, Somalia (K)

Commiphora incisa Chiov., Carter & Stannard 595, Kenya (K)

Commiphora mollis (Oliv.) Engl., Menezes 888, Angola (K)

Commiphora mossambicencis (Oliv.) Engl., Burtt 4589, Tanzania

(K)

Commiphora sarandensis Burtt, Burtt 3979, Tanganyika (K)

Crepidospermum multijugum Swart, Klug 2284, Peru (K)

Crepidospermum rhoifolium (Benth.) Tr. & Pl., Palacios 3021,

Ecuador (K)

Garuga floribunda Decne., Koorders VIB89, Celebes (K)

Garuga pierrei Guillaumin, Collins 73, Thailand (K)

Garuga pinnata Roxb., Drummond 3112, India (K)

Protium copal (Schltdl. & Cham.) Engl., Borgeau 2058, Mexico (K)

Protium crassipetalum Cuatrec., Campbell et al. P21923, Brazil (K)

Protium ferrugineum (Engl.) Engl., Pipoly et al. 6725 (K)

Protium javanicum Burm., f. Kostermans 18001, Indonesia (K)

Protium opacum Swart, Krukoff 4911, Brazil (K)

Protium polybotryum (Turcz.) Engl., Hostman 1268, Surinam (K)

Type

Protium robustum ( Swart) D.M. Porter, Daly et al. 1166, Brazil (K)

Protium sagotianum Marchand, Daly et al. 5124, Peru (K)

Protium tenuifolium (Engl.) Engl., Rogers 10117, s.l. Trinidad (K)

Protium tenuifolium (Engl.) Engl. var. sessiliflorum (Rose)

D.M. Porter, Tonduz 6989 (K - Type); 9952 Costa Rica (K)

Rosselia bracteata Forman, Katik et al. LAE70973, New

Guinea: Rossel Island (L)

Scutinanthe brunnea Thwaites, Endert 25 E IP 513, Indonesia:

Sumatra (K)

Triomma malaccensis Hook. f., Yong 94742 (K); Kedah Kepong

Field no. 27479, Malysia: Malay Penins. (K)

REFERENCES

Aguilar-Sierra, C. I. & Melhem, T. S. 1998a. Morfologia polınica da

tribo Bursereae (Burseraceae) na America do Sul. – Rev. Bras.

Bot. Reg. (Sao Paulo) 21: 17 – 26.

Aguilar-Sierra, C. I. & Melhem, T. S. 1998b. Morfologia polınica da

tribo Canarieae (Burseraceae) na America do Sul. – Rev. Bras.

Bot. Reg. (Sao Paulo) 21: 27 – 34.

Aguilar-Sierra, C. I. & Melhem, T. S. 1998c. Morfologia polınica da

Pollen of Burseraceae 297

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

tribo Protieae (Burseraceae) na America do Sul. – Rev. Bras.

Bot. Reg. (Sao Paulo) 21: 35 – 63.

Angiosperm Phylogeny Group (APG) 1998. An ordinal classifica-

tion for the families of flowering plants. – Ann. Mo. Bot. Gard.

85: 531 – 553.

Angiosperm Phylogeny Group (APG) 2003. An update of the

Angiosperm Phylogeny Group classification for the orders and

families of flowering plants: APG II. – Bot. J. Linn. Soc. 141:

399 – 436.

Arreguın-Sanchez, M. L., Palacios-Chavez, R. & Quiroz-Garcıa, D.

L. 1995. Morfologıa de los granos de polen de las familias

Rutaceae y Zygophyllaceae de la Estacion de Biologıa Chamela,

Jalisco, Mexico. – In: Mems 8o Coloq. Int. Paleobot. Palinol.,

Jalisco 1994, pp. 95 – 106. – Mexico DF.

Baksi, S. K. 1976. Pollen morphology of the genera Gluta Linnaeus

and Melanorrhoea Wallich (Anacardiaceae). – In: The evolu-

tionary significance of the exine (ed. I. K. Ferguson & J. Muller),

pp. 379 – 405. – Linn. Soc. Symp. Ser. I. Acad. Press, London/

New York.

Barth, O. M. 1980. Pollen morphology of a Brazilian Rutaceae:

Zanthoxylum (Fagara). – Pollen Spores 22: 425 – 436.

Barth, O. M. 1982. Variacoes polinicas em especies Brasileiras da

familia Rutaceae. – Bol. Inst. Geosci., Univ. Sao Paulo 13:

129 – 134.

Barth, O. M. 1983. Pollen morphology of Brazilian Rutaceae:

Dictyoloma and Hortia. – Pollen Spores 25: 409 – 420.

Barth, O. M. 1985. Pollen morphology of Brazilian Rutaceae:

Pilocarpus. – Pollen Spores 27: 145 – 153.

Basak, R. K. 1968. Studies on the pollen morphology of

Simaroubaceae. – Bull. Bot. Surv. India (1967) 9: 63 – 67.

Batten, D. J. & Christopher, R. A. 1981. Key to the recognition of

Normapolles and some morphologically similar pollen genera. –

Rev. Palaeobot. Palynol 35: 359 – 383.

Bentham, G. & Hooker, J. D. 1862. Geraniales: 49. Rutaceae, 50.

Simaroubaceae, 52. Burseraceae, 53. Meliaceae. – In: Genera

Plantarum. Vol. 1, P. 1, (ed. G. Bentham & J. D. Hooker),

pp. x – xi, 278 – 316 & 321 – 340. – A. Black, W. Pamplin, L,

Reeve, Williams & Norgate, London.

Brummitt, R. K. 1992. Vascular plant families and genera. – R.

Bot. Gards, Kew.

Clarkson, J. J., Chase, M. W. & Harley, M. M. 2002. Phylogenetic

relationships in Burseraceae based on plastid rps16 intron

sequences. – Kew Bull. 57: 183 – 193.

Correa, A. M. S., Watanabe, H. M. & Melhem, T. S. 1992. Flora

polınica da reserva do Parque estadual das Fontes do Ipiringa

(Sao Paulo, Brasil). Famılias: 44. Tiliaceae e 116. Rutaceae. –

Hoehnea 19: 117 – 124.

Cronquist, A. 1981. An integrated system of classification of

flowering plants. – Columbia Univ. Press, New York.

Dahlgren, R. M. T. 1983. General aspects of angiosperm evolution

and macrosystematics. – Nord. J. Bot. 3: 119 – 149.

Dalla Torre, C. G. de & Harms, H. 1901. 137. Rutaceae, 138.

Simaroubaceae, 139. Burseraceae, 140. Meliaceae. – In: Genera

Siphonogamarum ad systema Englerianum conscripta. 4. (ed. C.

G. Dalla Torre, C. G. de & H. Harms, H.), pp. 250 – 262. – W.

Engelmann, Lipsiae (Leipzig).

Engler, A. 1931. Rutaceae. – In: Die naturlichen Pflanzenf-

Familien. 2 Aufg, 19a. Pandales, Geraniales (ed. A. Engler, A.

& K. Prantl), pp. 405 – 456. – W. Engelmann, Leipzig.

Erdtman, G. 1952. Pollen morphology and plant taxonomy.

Angiosperms. – Almqvist & Wiksell, Stockholm.

Feuer, S. 1986. Pollen morphology and evolution in the Persoo-

nioideae, Sphalmioideae and Carnarvonioideae (Proteaceae). –

Pollen Spores 28: 123 – 156.

Feuer, S. & Kuijt, J. 1979. Fine structure of Mistletoe pollen II.

Pollen morphology and evolution in Psittacanthus (Lorantha-

ceae). – Bot. Not. 132: 295 – 309.

Forman, L. L., Brandham, P. E., Harley, M. M. & Lawrence, T. J.

1989. Beiselia mexicana (Burseraceae) and its affinities. – Kew

Bull. 44: 1 – 31.

Forman, L. L., van der Ham, R. W. J. M., Harley, M. M. & Lawrence,

T. J. 1994. Rosselia, a new genus of Burseraceae from the Louisade

Archipelago, Papua New Guinea. – Kew Bull. 49: 601 – 621.

Friis, E.-M., Pedersen, K. R. & Schoneneberger, J. 2003. End-

ressianthus, a new Normapolles-producing plant genus of

Fagalean affinity from the Late Cretaceous of Portugal. –

Int. J. Pl. Sci. 164(5 Suppl.): 201 – 223.

Furness, C. A. & Grant, M. C. 1996. Pollen morphology of some

Ruellia species (Acanthaceae) from Africa and Madagascar. –

Grana 35: 231 – 239.

Gillett, J. 1980. Commiphora (Burseraceae) in South America and its

relationship to Bursera. – Kew Bull. 34: 569 – 587.

Grant, M., Blackmore, S. & Morton, C. 2000. Pollen morphology

of the subfamily Aurantoideae (Rutaceae). – Grana 39: 8 – 20.

Harley, M. M. 1986. Pollen of Haplophyllum, Ruta and Thamnosma

(Rutaceae). – In: Taxonomic revision of the genus Haplophyllum

(Rutaceae) by C.C. Townsend – Hooker’s Icones Plant. 40: 6 – 11.

Harley, M. M. & Hall, D. 1999. Pollen morphology of the African

Burseraceae and related genera. – Palaeoecol. Africa & Sur. Isls

26: 225 – 242.

Harley, M. M. & Daly, D. 1995. Burseraceae: Protieae. – World

Pollen Spore Flora 20. Scand. Univ. Press, Stockholm/Oslo/

Copenhagen.

Ibe, R. A. & Leis, R. A. 1970. Pollen morphology of the

Anacardiaceae of northeastern North America. – Bull. Torrey

Bot. Club 106: 140 – 144.

Lam, H. J. 1932. The Burseraceae of the Malay Archipelago and

Peninsula. – Bull. Jard. Bot. Buitenzorg 3e Ser 12: 281 – 561.

Lobreau-Callen, D., Oltmann, O. & Straka, H. 1975. Rutaceae. –

Palynologia Madagassica et Mascarenica. Fam. 104. (ed. H.

Straka). Pollen Spores 17: 24 – 27.

Melchior, H. (Ed.) 1964. 27. Rutales. – In: Syllabus der

Pflanzenfamilien. 12 ed. Bd 2 (ed. A. Engler), pp. 262 – 277. –

Gebr. Borntraeger, Berlin.

Mikhelis, A. A. 1981. Normapolles pollen in Cretaceous/Palaeogene

boundary deposits of the Priazov’ye (Azov Sea area). – Rev.

Palaeobot. Palynol. 35: 209 – 229.

Moncada Ferrera, M. 1989. Reporte del genero Commiphora Jacq.

(Burseraceae) para Cuba. – Rev. Jard. Bot. Nacl. 10: 3 – : 10.

Morton, C. M. & Kallunki, J. A. 1993. Pollen morphology of the

subtribe Cuspariinae (Rutaceae). – Brittonia 45: 286 – 314.

Mziray, W. 1992. Taxonomic studies in Toddalieae Hook. f. (Rutaceae)

in Africa. – Symb. Bot. Upsal. 30, Uppsala Univ., Uppsala.

Pacltova, B. 1981. The evolution and distribution of Normapolles

pollen during the Cenophytic. – Rev. Palaeobot. Palynol. 35:

175 – 208.

Pflug, H. D. 1953. Zur Enstehung und Entwicklung des angios-

permiden Pollens in der Erdgeschichte. – Palaeontographica B

95: 60 – 171.

Pierlot, R. 1997. Pseudodacryodes Pierlot genre nouveau de

Burseraceae de l’est de la Rep. dem. du Congo. – Bull. Jard.

Bot. Natl Belg. 66: 175 – 186.

Punt, W., Blackmore, S., Nilsson, S. & Le Thomas, A. 1994.

Glossary of Pollen and Spore Terminology. – LPP Contr. Ser.

1. LPP Found., Utrecht. (updated – http://www.bio.uu.nl/

palaeo/glossary/).

Rasolodimby, J. F. C. 1983. Contribution palynologique a la

connaissance des Rutaceae de Madagascar. – These 3eme cycle.

131pp.

Rouse, G. E. 1957. The application of a new nomenclatural

298 M. M. Harley et al.

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014

approach to Upper Cretaceous plant microfossils from western

Canada. – Can. J. Bot. 35: 349 – 375.

Rzedowski, J. & Palacios-Chavez, R. 1985. La presencia de

Commiphora (Burseraceae) en Mexico. – Taxon 34: 207 – 210.

Segaar, P. J. & van der Ham, R. W. J. M. 1993. Pollen of

Scutinanthe brunnea compared with other burseraceous pollen

types: a remarkable case of divergence. – Rev. Palaeobot.

Palynol. 79: 297 – 334.

Sims, H. J., Herendeen, P. S., Lupia, R., Christopher, R. A. &

Crane, P. R. 1999. Fossil flowers with Normapolles pollen from

the Upper Cretaceous of southeastern North America. – Rev.

Palaeobot. Palynol. 106: 131 – 151.

Soltis, D. E., Soltis, P. S., Chase, M. W., Mort, M. E., Albach,

D.C., Zanis, M., Savolainen, V., Hahn, W. H., Hoot, S. B., Fay,

M. F., Axtell, M., Swensen, S. M., Prince, L. M., Kress, W. J.,

Nixon, K. C. & Farris, J. A. 2000. Angiosperm phylogeny

inferred from 18S rDNA, rbcL, and atpB sequences. – Bot. J.

Linn. Soc. 133: 381 – 461.

Savolainen, V., Fay, M. F., Albach, D. C., Backlund, A., van der Bank,

M., Cameron, K. M., Johnson, S. A., Lledo, M. D., Pintaud, J-C.,

Powell, M., Sheahan, M. C., Soltis, D. E., Soltis, P. S., Weston, P.,

Whitten, W. N., Wurdack, K. J. & Chase, M. W. 2000. Phylogeny of

the eudicots: a nearly complete familial analysis based on rbcL gene

sequences. – Kew Bull. 55: 257 – 309.

Takhtajan, A. 1987. Systema Magnoliophytorum. – USSR Acad.

Sci. Press, Leningrad (St. Petersburg).

Thorne, R. F. 1983. Proposed new realignments in the angiosperms.

– Nord. J. Bot. 3: 85 – 117.

Van der Ham, R. W. J. M. 1995. Palynology. – In: Flora

Malesiana, Ser. 1. Spermatophyta. Vol. 12 P. 1. Meliaceae

(ed. D. J. Mabberley, C. M. Pannell & A. M. Sing), pp. 6 – 7.

– Found. Flora Males. Herb. Neerl. Natl. Bot. Gard., Leiden.

Victor, J. & Van Wyk, A. E. 1998. Palynology of Acmadenia

(Diosminae: Rutaceae) and its taxonomic implications. – Grana

37: 143 – 154.

Victor, J. & Van Wyk, A. E. 1999a. Palynology of Diosma and

Coleonema (Rutaceae: Diosminae) and its taxonomic implica-

tions. – Grana 38: 12 – 19.

Victor, J. & Van Wyk, A. E. 1999b. Palynology of Adenandra

(Rutaceae: Diosminae) and its taxonomic implications. – Grana

38: 1 – 11.

Victor, J. & Van Wyk, A. E. 2001. Palynology of Euchaetis and

Macrostylis (Diosminae - Rutaceae) and its taxonomic implica-

tions. – Grana 40: 105 – 110.

Young, D. A. 1982. Proposal. – In: Amended outlines and indices

for six recently published systems of angiosperm classification

(ed. H. G. Bedell & J. L. Reveal). – Phytologia 51:

65 – 156.

Pollen of Burseraceae 299

Grana 44 (2005)

Dow

nloa

ded

by [

Inge

nta

Con

tent

Dis

trib

utio

n (P

ublis

hing

Tec

hnol

ogy)

] at

10:

03 0

7 O

ctob

er 2

014