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An ongoing re-investigation of the early Miocene Saldanha Bay (South Africa) palynoflora, using combined light and scanning electron microscopy (single grain method), is revealing several pollen types new to the African fossil record. One of the elements identified is Loranthaceae pollen. These grains represent the first and only fossil record of Loranthaceae in Africa. The fossil pollen grains resemble those produced by the core Lorantheae and are comparable to recent Asian as well as some African taxa/lineages. Molecular and fossil signals indicate that Loranthaceae dispersed into Africa via Asia sometime during the Eocene. The present host range of African Loranthaceae and the composition of the palynoflora suggest that the fossil had a range of potential host taxa to parasitise during the early Miocene in the Saldanha Bay region.
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The rst Loranthaceae fossils from Africa
FRIÐGEIR GRÍMSSON
1
, ALEXANDROS XAFIS
1
, FRANK H. NEUMANN
2,3
,
LOUIS SCOTT
3
, MARION K. BAMFORD
4
& REINHARD ZETTER
1
1
Department of Palaeontology, University of Vienna, Vienna, Austria,
2
School of Agricultural, Earth and Environmental
Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa,
3
Department of Plant Sciences, University of the Free
State, Bloemfontein, South Africa,
4
Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South
Africa
Abstract
An ongoing re-investigation of the early Miocene Saldanha Bay (South Africa) palynoora, using combined light and
scanning electron microscopy (single grain method), is revealing several pollen types new to the African fossil record. One of
the elements identied is Loranthaceae pollen. These grains represent the rst and only fossil record of Loranthaceae in
Africa. The fossil pollen grains resemble those produced by the core Lorantheae and are comparable to recent Asian as well
as some African taxa/lineages. Molecular and fossil signals indicate that Loranthaceae dispersed into Africa via Asia
sometime during the Eocene. The present host range of African Loranthaceae and the composition of the palynoora
suggest that the fossil had a range of potential host taxa to parasitise during the early Miocene in the Saldanha Bay region.
Keywords: Santalales, diagnostic pollen, host plants, Miocene, palaeoecology, palaeophytogeography, parasitic plants,
pollen morphology
The Loranthaceae is a large family with c. 76 genera and
at least 1000 species divided into ve tribes (Nickrent
1997onwards; Nickrent et al. 2010). The family is
widely distributed and occurs in tropical to temperate
regions of Australasia, Asia, the Middle East, Africa,
Europe, and Central and South America (e.g. Barlow
1983; Polhill & Wiens 1998), showing a clear geo-
graphic split between a New World group (Psittacanthi-
nae Engl.) and Old World-Australasian lineages
(Elythrantheae Engl. and Lorantheae Rchb.; e.g. Nickr-
entetal.2010; Grímsson et al. 2017,2018). The c. 238
species and 21 genera occurring in Africa (Table I)are
considered to be the most derived in the family. Most of
the African genera/species are endemic, with only Helix-
anthera and Taxillus extending into Asia. Helixanthera,
occurring from Africa to Indonesia, is regarded as the
most primitive Lorantheae genus thriving in continental
Africa (Polhill & Wiens 1998). Even though Lorantha-
ceae are currently found all over Africa (except the
Sahara desert), it has been suggested that they dispersed
to the continent during the Cretaceous (Gondwanan
derivation) or Eocene times (Asian derivation) (Barlow
1983,1990; Polhill & Wiens 1998), however, no fossil
Loranthaceae have ever been reported from this part of
the world. The fossil record of Loranthaceae, recently
summarised by Grímsson et al. (2017,gures 10, 11,
and le S4), shows that the family already had a global
distribution during the Eocene, occurring on all conti-
nents except Africa and Antarctica. The Loranthaceae
have a fragmentary fossil record composed solely of
fossil pollen (Grímsson et al. 2017), most likely due to
the ecology and life cycle of Loranthaceae (small woody
plants, with relatively few leaves, their fruits are ingested
by birds, and seeds germinate immediately after regur-
gitation; see Polhill & Wiens 1998) . Therefore, the only
way to trace the origin and evolution of this family, in
Correspondence: Friðgeir Grímsson, Department of Palaeontology, University of Vienna, Althanstraße 14 (UZA II), A-1090 Vienna, Austria.
E-mail: fridgeir.grimsson@univie.ac.at
(Received 2 November 2017; accepted 13 December 2017)
Grana, 2018
Vol. 57, No. 4, 249259, https://doi.org/10.1080/00173134.2018.1430167
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Table I. African Loranthaceae genera and their hosts.
Genus
Number
of
species
African
species Occurrence in Africa Recorded host families in Africa See Table
Helixanthera c. 45 12 Tropical, scattered around edge
of continent
Anacardiaceae, Bignoniaceae, Boraginaceae,
Burseraceae, Combretaceae,
Euphorbiaceae,Fabaceae, Lauraceae*,
Loranthaceae, Malvaceae*, Moraceae,
Ochnaceae, Phyllanthaceae, Rhamnaceae,
Rubiaceae*, Rutaceae, Sapotaceae
S1
Plicosepalus 12 12 Eastern side of Africa to Angola
and South Africa
Anacardiaceae, Apocynaceae, Burseraceae,
Combretaceae,Fabaceae, Rubiaceae
S2
Emelianthe 1 1 Drier parts of E. and NE.
Africa
Anacardiaceae, Burseraceae,
Euphorbiaceae, Malvaceae
S3
Pedistylis 1 1 Southern Africa Anacardiaceae,Combretaceae, Ebenaceae,
Fabaceae, Meliaceae, Moraceae
S4
Actinanthella 2 2 SE. and S. Africa Capparaceae, Erythroxylaceae, Oleaceae S5
Oncocalyx 13 13 Drier forests and bushland of
eastern and southern Africa
Anacardiaceae, Apocynaceae, Boraginaceae,
Burseraceae, Cannabaceae, Capparaceae,
Celastraceae, Combretaceae, Ebenaceae,
Euphorbiaceae,Fabaceae, Malvaceae,
Pittosporaceae, Rhamnaceae, Salicaceae,
Salvadoraceae, Tamariaceae, Zygophyllaceae
S6
Spragueanella 2 2 E. and SC. Africa along coast
and extending into
mountains in dryer forest
Podocarpaceae, Putranjivaceae S7
Oliverella 3 3 Eastern and south-central
Africa in coastal and
deciduous bushland and
mixed woodland
Combretaceae,Euphorbiaceae,Fabaceae,
Malvaceae
S8
Berhautia 1 1 Senegal and Gambia Combretaceae S9
Englerina 25 25 Tropical Africa Achariaceae, Asteraceae, Bignoniaceae,
Boraginaceae, Buddlejaceae, Burseraceae,
Clusiaceae, Combretaceae, Ebenaceae,
Fabaceae,Loganiaceae, Malvaceae,
Oleaceae, Primulaceae, Proteaceae,
Rhamnaceae, Rubiaceae, Rutaceae*,
Sapindaceae
S10
Agelanthus 59 59 Africa south of the Sahara Anacardiaceae, Apocynaceae, Asteraceae,
Boraginaceae, Burseraceae, Cannabaceae,
Cappaeaceae, Celastraceae,
Chrysobalanaceae, Combretaceae,
Convolvulaceae, Erythroxylaceae,
Euphorbiaceae,Fabaceae, Iteaceae,
Juglandaceae*, Lamiaceae, Loranthaceae,
Lythraceae*, Malvaceae, Meliaceae,
Moraceae, Olacaceae, Oleaceae,
Phyllanthaceae, Plumbaginaceae,
Rhamnaceaee, Rosaceae*, Rutaceae*,
Proteaceae, Salicaceae, Salvadoraceae,
Santalaceae,Sapindaceae, Solanaceae*,
Ulmaceae, Urticaceae, Vitaceae
S11
Tapinanthus 30 30 Tropical and southern Africa Anacardiaceae, Apocynaceae, Asphodelaceae,
Asteraceae, Burseraceae, Celastraceae,
Combretaceae, Crassulaceae, Ebenaceae,
Euphorbiaceae,Fabaceae, Juglandaceae*,
Kirkiaceae, Lamiaceae, Loranthaceae,
Malvaceae, Meliaceae, Melianthaceae,
Moraceae, Myrtaceae, Ochnaceae,
Phyllanthaceae, Proteaceae, Rosaceae,
Rhamnaceae, Rutaceae, Salicaceae,
Salvadoraceae, Santalaceae,Sapotaceae,
Solanaceae, Tamaricaceae
S12
(Continued )
250 F. Grímsson et al.
time and space, is to study fossil Loranthaceae pollen in
relation to phylogeny. Grímsson et al. (2018) evaluated
the correlation of pollen morphology and molecular
phylogenetic relationships within Loranthaceae and dis-
covered that most pollen typesinthisfamilyarelinked
to a single genus or discrete evolutionary lineages. Since
pollen types produced by most extant members of the
Loranthaceae are distinct (Feuer & Kuijt 1978,1979,
1980,1985;Kuijt1988; Liu & Qiu 1993; Han et al.
2004;Roldán&Kuijt2005;Caires2012;Cairesetal.
2012,2014,2017; Grímsson et al. 2017,2018)and
cannot be confused with pollen from other related
families, fossil Loranthaceae pollen give the potential
to trace modern lineages back in time.
Here we describe a new fossil Loranthaceae pollen
type from the earliest Miocene of Saldanha Bay, South
Africa. These fossils are the rst representatives of this
family in the fossil record of Africa. The diagnostic light
microscopy (LM)- and scanning electron microscopy
(SEM)-based features of the pollen provide sufcient
support to assign the fossils to a distinct lineage within
the Loranthaceae. Based on the taxonomic afliation to
extant taxa the palaeophytogeographic signals and
palaeoecological aspects of these fossil grains are dis-
cussed and potential host taxa are suggested from the
currently known palaeo-palynoora.
Material and methods
The sedimentary rock containing the fossil Lor-
anthaceae pollen is from core sample #114755 col-
lected at Saldanha Bay, South Africa. The sediments
are believed to be of earliest Miocene age. A Chat-
tian to early Miocene age for the Saldanha Bay
Table I. (Continued ).
Genus
Number
of
species
African
species Occurrence in Africa Recorded host families in Africa See Table
Moquiniella 1 1 Southern Namibia and the
Cape Province of South
Africa
Anacardiaceae, Apocynaceae, Ebenaceae,
Fabaceae, Hypericaceae, Malvaceae,
Moraceae, Rosaceae*, Salicaceae
S13
Globimetula 13 13 Tropical Africa Anacardiaceae*, Burseraceae,
Chrysobalanaceae, Combretaceae,
Fabaceae, Malvaceae*, Meliaceae,
Moraceae, Myrtaceae*, Phyllanthaceae,
Proteaceae, Rutaceae*
S14
Taxillus 35 1 Coast of Kenya Fabaceae S15
Vanwykia 2 2 Eastern and south-eastern
Africa
Fabaceae, Moraceae S16
Septulina 2 2 Western Cape Province of
South Africa and southern
Namibia
Aizoaceae, Anacardiaceae,Fabaceae,
Solanaceae, Tamaricaceae
S17
Oedina 4 4 Montane forests from Tanzania
to northern Malawi
S18
Oncella 4 4 Montane and coastal areas of
eastern Africa
Phyllanthaceae, Malvaceae, Meliaceae S19
Erianthemum 16 16 Eastern and southern Africa Anacardiaceae, Archariaceae, Asteraceae,
Bignoniaceae*, Burseraceae, Celastraceae,
Combretaceae, Ebenaceae,
Euphorbiaceae,Fabaceae, Lamiaceae,
Loganiaceae, Malvaceae, Meliaceae,
Myrtaceae*, Phyllanthaceae, Proteaceae,
Rhamnaceae, Rosaceae*, Rutaceae*,
Sapotaceae
S20
Phragmanthera 34 34 Tropical forests of Africa, few
extend into dry habitats in
south-central and southern
Africa
Anacardiaceae*, Annonaceae, Boraginaceae,
Burseraceae, Casuarinaceae*,
Combretaceae,Euphorbiaceae,
Fabaceae, Irvingiaceae, Lauraceae*,
Malvaceae*, Melianthaceae, Moraceae,
Myrtaceae*, Rhamnaceae, Rubiaceae,
Rutaceae*, Tamaricaceae, Phyllanthaceae,
Proteaceae,Sapotaceae
S21
Notes: Families with introduced host taxa are marked with asterisk*. Host families known from the fossil palyno-assemblage appear in bold.
Loranthaceae systematics and distribution summarised from Polhill and Wiens (1998), data on host taxa compiled from Wiens and Tölken (1979),
Visser (1981), Dean et al. (1994), Polhill and Wiens (1998, 1999), Dzerefos et al. (2003), Roxburgh and Nicolson (2005), Veste (2007), Didier et al.
(2008), Ogunmefun et al. (2013), Dlama et al. (2016) and Okubamichael et al. (2013, 2016). See also Tables S1S21 in Supplemental data.
Loranthaceae Fossils from Africa 251
deposits is suggested on the base of the dinoagellate
indicator taxa Distatodinium craterum Eaton, Chirop-
teridium lobospinosum Gocht, Homotryblium plectilum
Drugg et Loeblich Jr. as well as Impagidinium para-
doxum (Wall 1967) Stover et Evitt 1978 (see details
in Roberts et al. [2017] including supplements). For
a full geological, stratigraphic, palaeontological and
palaeoenvironmental background of this locality/core
see Roberts et al. (2017). The sedimentary rock
sample was processed and fossil pollen grains
extracted according to the protocol outlined in
Grímsson et al. (2008). The fossil Loranthaceae pol-
len grains were investigated both by LM and SEM
using the single grain method as described in Zetter
(1989). The description of fossil Loranthaceae pol-
len includes diagnostic features observed both in LM
and SEM. Pollen terminology follows Punt et al.
(2007; LM) and Hesse et al. (2009; SEM). Lor-
anthaceae fossil material (SEM stubs) from Saldanha
Bay, South Africa, are stored in the collection of the
Department of Palaeontology, University of Vienna,
Austria under the accession numbers IPUW 7513/
211 and IPUW 7513/216.
Systematic palaeontology
The fossil pollen described here falls within the variation
of Pollen Type B denedbyGrímssonetal.(2018).
Pollen of this type is oblate (to various degrees), trian-
gular to trilobate in polar view and shows a ±psilate
sculpturing in LM. Usually, further sculpture details
are not observed in LM, but some pollen grains show
a clear exine thickening or thinning at the pole and along
the colpi or in the mesocolpium. The pollen is syn(3)
colpate, see gure 1 in Grímsson et al. (2018) for a
schematic drawing. Since the fossil pollen grains
described here show combining features known from
four extant Loranthaceae genera (see later), we classify
this fossil taxon as a morphotype (MT) named after the
locality where the pollen occurs.
Family Loranthaceae Juss.
Tribe Lorantheae Rchb.
Saldanha MT, aff. Lorantheae
Figures 13
Description.Pollen, oblate, concave-triangular to
trilobate in polar view, elliptic in equatorial view,
equatorial apices obcordate to T-shaped; size small,
polar axis 8.812.5 µm long in LM, equatorial dia-
meter 2025 µm in LM, 1522 µm in SEM; syn(3)
colpate; exine 0.81.0 µm thick, nexine thinner than
sexine (LM), triangular intercolpial nexine thicken-
ings in polar area (LM); tectate; sculpture psilate in
LM, nanoverrucate to granulate in area of mesocol-
pium in SEM, nanoverrucae 0.20.5 µm in diameter,
verrucae composed of conglomerate granula; margo
well developed, margo psilate or partly granulate,
margo with triangular protrusions in polar area
(SEM); colpus membrane nanoverrucate and gran-
ulate (SEM).
Remarks.Compared to extant pollen this fossil
MT shows a suite of features found only within the
tribe Lorantheae. This combination of outline, size,
colpi arrangement, thickening of nexine (LM), and
sculpture observed under SEM is typical for taxa
placed in the Subtribes Dendropthinae Nickrent &
Vidal-Russell (e.g. Tolypanthus, Dendrophthoe), Scur-
ullinae Nickrent & Vidal-Russell (e.g. Taxillus), and
partly Emelianthinae Nickrent & Vidal-Russell
(Phragmanthera). Both Tolypanthus maclurei (Merr.)
Danser and Dendrophthoe pentandra (L.) Miq. pollen
is very similar to the Saldanha MT (see Table II).
The Tolypanthus maclurei pollen (see gure 38 in
Grímsson et al. 2018) is usually larger than the fos-
sils, and the D. pentandra pollen (see gure 36 in
Grímsson et al. 2018) tends to have a slightly thicker
nexine, and wall peculiarities in the polar area are
hard to distinguish (LM). Otherwise the pollen of
these two taxa is almost identical to the Saldanha
MT. Pollen of Taxillus caloreas (Diels) Danser (see
gure 49 in Grímsson et al. 2018) has a more strik-
ing and larger, hexagonal in outline, thickening of
nexine in the polar area that differs from that
observed in the Saldanha MT. Most other features
are comparable to those observed in the fossils. Pol-
len of Phragmanthera rufescens (DC.) Balle (see gure
43 in Grímsson et al. 2018) is more or less identical
to the Saldanha MT, except the P. rufescens pollen is
slightly larger and the exine is thicker (LM).
Despite the number of fossil Loranthaceae pollen
reported so far only few grains/types have been studied
using SEM (see Grímsson et al. 2017). Of those stu-
died using SEM only two MTs, the Changchang MT
form the middle Eocene of China, and the Altmitt-
weida MT from the late Oligoceneearly Miocene of
Germany (Table II; see also Grímsson et al. 2017),
indicate a possible lineage relation (Lorantheae) with
the African fossils. The broadly rounded apices, the
rhombic structures covering equatorial apertures, and
the merely granulate sculpture clearly distinguishes the
Chinese Changchang MT from the African Saldanha
MT (see Table II). Still, the minute sculpture and the
basic form of the Changchang MT also link it to the
Lorantheae, especially to the Scurrulinae (Taxillus,
Scurulla) and Amyeminae (Amyema), and Grímsson
et al. (2017, p. 21) described this pollen MT as a
Scurrulinae pollen with an Amyema-like margo.
Therefore, the Changchang MT most likely belongs
to an extinct or ancestral Lorantheae lineage related to
252 F. Grímsson et al.
the core Lorantheae. The emarginate outline in equa-
torial view, the reduced sexine in the polar area, the
microverrucate sculpture in SEM, and the pollen size
clearly distinguishes the German Altmittweida MT
from the African Saldanha MT. Extant pollen very
similar to the Altmittweida MT can be found in two
Figure 1. LM (A) and SEM (B) micrographs of fossil Loranthaceae pollen from the early Miocene of Africa. A. Saldanha morphotype (MT)
pollen grains in equatorial and polar view. Note triangular intercolpial nexine thickenings in polar area. B. Saldanha MT pollen grains in
polar view. Equatorial apices are obcordate to T-shaped and the margo is psilate or partly granulate and with triangular protrusions in polar
area. Scale bars 10 µm (A, B).
Loranthaceae Fossils from Africa 253
Figure 2. SEM micrographs of fossil Loranthaceae pollen from the early Miocene of Africa. AD. Close-ups of central polar area showing
margo with triangular protrusions in polar area. EH. Close-ups of apex showing obcordate to T-shaped apices, and psilate or partly
granulate margo. Scale bars m(AH).
254 F. Grímsson et al.
extant species of Lorantheae, Amyema gubberula Dan-
ser and Helixanthera kirkii (Oliv.) Danser. It is there-
fore also likely that the Altmittweida MT belongs to a
lineage related to the core Lorantheae.
Discussion
The African Lorantheae fossils in a global (time and
space) context
The fossil pollen record of Loranthaceae (e.g. Gotha-
nipollis) recently summarised by Grímsson et al.
(2017) shows that the family had a worldwide dis-
tribution already during the Eocene, with represen-
tatives found in South America, North America,
Europe, East Asia, and Australasia. Based on this
palaeo-phytogeographic pattern it is most likely that
Loranthaceae were also present in Africa during that
time. The lack of fossil Loranthaceae pollen in the
African record should be considered an artefact
caused primarily by preparation techniques and
study methods, or palynologists working on African
material not knowing this typical Gothanipollis type.
Accepting this, the dispersal of Loranthaceae into
Africa might have occurred in the Southern Hemi-
sphere before the nal phases of the Gondwana
breakup (Late Cretaceous) or in the Northern Hemi-
sphere via Asia (early Eocene). Unfortunately, the
majority of Eocene fossil Loranthaceae pollen
found in the Southern Hemisphere (South America,
Australasia) has mostly been studied using LM only
(e.g. Romero & Castro 1986; Raine et al. 2011) and
is therefore of very limited use for interfamilial seg-
regation. In a molecular phylogenetic context (see
gure 2 in Grímsson et al. 2018) the present African
Loranthaceae show a closer relation to South, South-
east and East Asian lineages than any other, and are
clearly most distantly related to American Lorantha-
ceae. It is interesting, based on pollen morphology,
that the earliest Miocene fossils from Saldanha Bay
suggest the same close relation to Asian taxa
(Table II) and norelation to any of the American
lineages. Grímsson et al. (2017) established that sev-
eral major lineages of Loranthaceae were present
during Eocene in the Northern Hemisphere, with
records including representatives of extinct or ances-
tral lineages with afnities to both root-parasitic gen-
era (Nuytsia/Nuytsieae) and epiphytic lineages
Figure 3. SEM micrographs of fossil Loranthaceae pollen from the early Miocene of Africa. AD. Close-ups of mesocolpium showing
nanoverrucate to granulate sculpture (SEM). Scale bars m(AD).
Loranthaceae Fossils from Africa 255
Table II. African fossil morphotype (MT) compared to similar extant pollen and fossil MTs.
Tolypanthus maclurei Dendrophthoe pentandra Taxillus caloreas
Phragmanthera
rufescens (s.l.)
a
Saldanha MT (this
study) Changchang MT Altmittweida MT
Age/epoch Recent Recent Recent Recent Early Miocene Middle Eocene
(Lutetian-
Bartonian)
Late Oligocene-
early Miocene
(Chattian-
Aquitanian)
Distribution/
locality
East Asia South, East and Southeast
Asia
East Asia Tropical Africa Saldanha Bay, South
Afruca, core sample
#114 755
Changchang Basin,
close to Jiazi
Town, Qiongshan
County, Hainan,
China
Altmittweida,
Saxony,
Germany
P/E ratio oblate oblate oblate oblate oblate oblate oblate
Outline p.v. trilobate to straight-
triangular
concave-triangular to
trilobate
concave-triangular concave-
triangular
concave-triangular to
trilobate
concave-triangular
to broadly
trilobate
convex-triangular
Outline eq. v. elliptic elliptic elliptic elliptic elliptic emarginate
Equatorial apices obcordate obcordate obcordate T-shaped obcordate to T-shaped broadly rounded broadly obcordate
P in LM (µm) 8.315.8 13.315 11.715 1518.3 8.812.5 4.45.5
E in LM (µm) 2530 21.725.8 23.330 26.731.7 2025 21.124.4 14.417.8
Aperture syn(3)colpate syn(3)colpate syn(3)colpate syn(3)colpate syn(3)colpate syn(3)colpate syn(3)colpate
Exine thickness in
LM (µm)
0.81.3 1.11.3 1.01.3 1.11.4 0.81.0 0.91.1 0.91.1
Wall peculiarities triangular intercolpial
thickening of nexine
in polar area
sexine partly reduced in
polar area, colpi
widening to a small eld
hexagonal nexine
thickening in
polar area
triangular
intercolpial
thickening of
nexine in
polar area
triangular intercolpial
thickening of nexine
in polar area
rhombic structures
(opercula)
covering
equatorial apices
intercolpial nexine
thickening at
pole, sexine
partly reduced in
polar area
Sculpture (SEM) nanoverrucate to
granulate
nanoverrucate to granulate nanoverrucate to
granulate
nanoverrucate
to granulate
nanoverrucate to
granulate
granulate nano- to
microverrucate to
granulate
Type and size of
sculpture
elements (µm)
verrucae 0.20.5
(0.8)
verrucae 0.20.6 verrucae 0.10.5 verrucae 0.1
0.6
verrucae 0.20.5 verrucae 0.21.3
Margo (SEM) well developed, psilate
or partly granulate,
with triangular
protrusions in polar
area
well developed, psilate or
partly granulate to
nanoverrucate, with
triangular protrusions in
polar area
well developed,
psilate with few
nanoverrucae or
granula in polar
area
well
developed,
psilate or
partly
granulate
well developed, psilate
or partly granulate,
with triangular
protrusions in polar
area
well developed,
psilate
psilate to
microverrucate,
granulate
Colpus membrane
(SEM)
nanoverrucate and
granulate
nanoverrucate and
granulate
nanoverrucate and
granulate
nanoverrucate
and
granulate
nanoverrucate and
granulate
granulate nanoverrucate and
granulate
Note: Distribution of extant taxa from Qui and Gilbert (2003) and Polhill and Wiens (1998). Pollen morphology of extant taxa summarised from Grímsson et al. (2018). Pollen morphology of
fossil mophotypes summarised from Grímsson et al. (2017).
a
Phragmanthera rufescens has been widely applied as an aggregate for tropical African Phragmanthera. According to Polhill and Wiens
(1998) P. rufescens is only known from Guinée and the Casamance region of southern Senegal, but the sample gured in Grímsson et al. (2018) is from Cameroon and might therefore represent P.
kamerunensis or another Phragmanthera species.
256 F. Grímsson et al.
(Lorantheae, Psittacantheae, Notanthera, Ely-
trantheae). In this scenario, it seems more likely
that the ancestor(s) of the fossils described here
and the current African lineages dispersed into
Africa from Asia (northern route) during the Eocene.
For now, dispersal into Africa in the Southern Hemi-
sphere during the nal phases of the Gondwana
breakup cannot be ruled out. If some Loranthaceae
were dispersed via a southern route then those
lineages became extinct in Africa during the Caino-
zoic.
Time of origin and divergence of African Loranthaceae
lineages
Fossil constrained molecular dating by Grímsson
et al. (2017) suggests that Tupeia (A-type pollen)
and Loranthaceae with B-type pollen diverged in
the early Eocene (~50 Ma). A primary radiation is
believed to have followed shortly thereafter involving
the formation of both New World(root parasites,
Elytrantheae, Psittacantheae) and Old World(Lor-
antheae) clades. Crown group radiation in the Lor-
antheae is then believed to have started at the latest
in the late Eocene (38 Ma), with a second major
radiation taking place ~10 million years later (latest
in the Oligocene) involving among others the Old
Worldcore Lorantheae (Grímsson et al. 2017).
Unfortunately, there are no current African records
from the Eocene or Oligocene so far, but one could
expect to nd Loranthaceae pollen showing mor-
phology characteristic for the core crown Lorantheae
(e.g. Amyeminae, Dendropthinae) in such samples.
Still, the Saldanha MT suggests that until the earliest
Miocene pollen producing Loranthaceae in Africa
(at least southern Africa) still had the basal Lor-
antheae pollen form. More diverged lineages/genera
must therefore have evolved no earlier than during
the latest part of the early Miocene. The age and
pollen morphology of the Saldanha MT t perfectly
with the suggested core crown group radiation of
Lorantheae and the alleged formation of extant
lineages/modern genera lasting until the middle Mio-
cene (9 Ma; see gure 9 in Grímsson et al. 2017).
Fossil pollen showing derived features within the
Lorantheae, e.g. Emelianthinae and Tapinanthinae,
are most likely to be found in sediments younger
than earliest Miocene.
Ecology and potential hosts of the Saldanha MT
Loranthaceae are currently found in all parts of Africa
except the Sahara desert where there is little vegetation.
They occur in various habitats, ranging from sea-level to
mountain tops, in grasslands as well as rainforests and
semi-deserts. Their only requirements seem to be the
presence of suitable host plants and dispersal mechan-
isms (e.g. birds) to carry them between hosts (e.g. Visser
1981; Polhill & Wiens 1998). It is hard to pinpoint the
preferred host of a fossil taxon and if it had a narrow
(specialist) or wide (generalist) host range. Based on the
available host ranges of recent African Loranthaceae
(Table II;TablesS1S21 in Supplemental data) it
seems that most of the genera are generalists and para-
sitising many species/genera/families. The fossil palyno-
assemblage containing the Saldanha MT is extremely
taxon rich (Roberts et al. 2017) and composing pollen
from at least 150 different angiosperms veried using
SEM (Grímsson et al. unpublished data). Many of the
fossil pollen types belong in families that are known to
be parasitised by recent African Loranthaceae. These
include Anacardiaceae, Asteraceae, Casuarinaceae,
Euphorbiaceae, Fabaceae, Myrtaceae, Oleaceae, Pro-
teaceae, Santalaceae, Sapindaceae, Sapotaceae, and
the gymnosperm family Podocarpaceae. Based on the
recorded host families listed in Table II, it is likely that
every recent Loranthaceae genus would nd a suitable
host plant in the palaeo-vegetation at Saldanha Bay
during the earliest Miocene. The palaeo-vegetation
units in the Saldanha Bay region are believed to have
been very diverse (Roberts et al. 2017), composed, e.g.
of various lowland wetland and marshland forests (man-
grove, riparian/swamp) and different mixed evergreen
broad-leaved and/or coniferous forests stretching into
the surrounding highlands (see gure 13 in Roberts
et al. 2017). All potential vegetation units (habitats)
recorded by Roberts et al. (2017) would be suitable for
Loranthaceae based on the current vast habitat range of
the family in Africa (e.g. Polhill & Wiens 1998).
Conclusion and outlook
Despite the numerous palaeopalynological investiga-
tions on African Cretaceous to Miocene microora
there are no comprehensive high resolution SEM-
based studies so far. Even though the potential for
studying pollen using combined LM and SEM from
African sediments was already established by Coetzee
in the 1980s (Coetzee 1981,1983;Coetzee&Muller
1984; Coetzee & Praglowski 1984,1988), she only
presented a handful of fossil taxa using SEM and no
other African palynologist has used this combined
method since. Based on the current Loranthaceae fos-
sil record it is very unlikely that the family should be
absent from Eocene and Oligocene sediments in
Africa. It is more likely that the preparation methods
(including sieving) and study techniques (counting up
to 300 grains in LM) biased the outcome, or/and when
present, the palynologist did not know this distinct
pollen type and disregarded it or simply misidentied
it. Our combined LM and SEM based study shows
that the early Miocene South African Loranthaceae
Loranthaceae Fossils from Africa 257
fossils resemble the core Lorantheae (Dendrophae,
Scurullae) and the more derived lineages (Tapi-
nanthae, Emelianthae) were not present in this area at
the time of accumulation. Molecular and fossil signals
suggest that Loranthaceae dispersed into Africa via
Asia (northern route) during the Eocene. Also, the
recent host range of African Loranthaceae and the
palaeo-palynological spectrum suggest that the fossil
would have no problems nding a host plant during the
early Miocene in the Saldanha Bay region. To fully
enlighten the African palaeophytogeographic history
of this family, including a more precise time of origin
in both time and space for the derived lineages, Eocene
to Pliocene sediments in other parts of Africa as well as
middle Miocene to Pleistocene sediments in South
Africa must be screened for Loranthaceae pollen and
studied using SEM. Upper Cretaceous to Paleocene
sediments (e.g. McLachlan & Pieterse 1978;Partridge
1978;Scholtz1985; Sandersen et al. 2011)shouldalso
be screened for Loranthaceae-type pollen to establish if
South American/Australasian basal lineages dispersed
into Africa via a southern route, but went extinct dur-
ing the early Cainozoic.
Disclosure statement
No potential conict of interest was reported by the
authors.
Funding
This study was funded by the Austrian Science Fund
(FWF) with a grant to FG, project number P29501-
B25. FN was funded by a post-doctoral fellowship at
the UKZN/UFS and LS by the National Research
Foundation, South Africa.
Supplemental data
Supplemental data for this article can be accessed
here.
ORCID
Friðgeir Grímsson http://orcid.org/0000-0002-1874-6412
Alexandros Xashttp://orcid.org/0000-0001-5528-3106
Frank H. Neumann http://orcid.org/0000-0002-3620-
2742
Louis Scott http://orcid.org/0000-0002-4531-0497
Marion K. Bamford http://orcid.org/0000-0003-0667-
130X
Reinhard Zetter http://orcid.org/0000-0002-0220-6921
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Loranthaceae Fossils from Africa 259
... Following the last comprehensive assessment of host associations in African mistletoes by Polhill and Wiens (1998, 1999a, 1999b) and a number of regional studies (see Table S1 for the reference list), Grímsson et al. (2018) have recently compiled the continent-wide published host species records for the African Loranthaceae. In contrast, the island mistletoe taxa (from the Madagascar and neighboring islands) have remained virtually unaddressed in terms of host associations since Balle (1964aBalle ( , 1964b and Philcox (1982), except for occasional studies dealing with individual mistletoe taxa (Albert et al., 2017). ...
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Host specificity has been investigated for centuries in mistletoes, viruses, insects, parasitoids, lice and flukes, yet it is poorly understood. Reviewing the numerous studies on mistletoe host specificity may contribute to our understanding of these plants and put into context the dynamics at work in root parasitic plants and animal parasites. The mechanisms that determine host specificity in mistletoes are not as well documented and understood as those in other groups of parasites. To rectify this we synthesised the available literature and analysed data compiled from herbaria, published monographs and our own field studies in South Africa. As for other groups of parasites, multiple factors influence mistletoe host specificity. Initially, pollination affects gene flow. Subsequently, seed dispersal vectors (birds and marsupials), host abundance and compatibility (genetic, morphological, physiological and chemical), history and environmental conditions affect the interaction of mistletoes and their hosts and determine host specificity. Mistletoe-host network analyses and a geographic mosaic approach combined with long-term monitoring of reciprocal transplant experiments, genetic analyses of confined mistletoe populations and comparative phylogenetic studies could provide further insights to our understanding of host specificity. Some of these approaches have been used to study animal-plant interactions and could be adopted to test and evaluate host specificity in mistletoes at local and larger geographic scales.
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