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Cretaceous African life captured in amber
Alexander R. Schmidt
a,1
, Vincent Perrichot
b,c,1
, Matthias Svojtka
d
, Ken B. Anderson
e
, Kebede H. Belete
f
,
Robert Bussert
g
, Heinrich Dörfelt
h
, Saskia Jancke
i
, Barbara Mohr
i
, Eva Mohrmann
i
, Paul C. Nascimbene
j
, André Nel
k
,
Patricia Nel
k
, Eugenio Ragazzi
l
, Guido Roghi
m
, Erin E. Saupe
c
, Kerstin Schmidt
n
, Harald Schneider
o
, Paul A. Selden
c,p
,
and Norbert Vávra
d
a
Courant Research Centre Geobiology, Georg-August-Universität Göttingen, 37077 Göttingen, Germany;
b
Centre National de la Recherche Scientifique, Unité
Mixte de Recherche 6118 Géosciences & Observatoire des Sciences de l’Univers de Rennes, Université Rennes 1, 35042 Rennes, France;
c
Paleontological Institute,
University of Kansas, Lawrence, KS 66045;
d
Department of Paleontology, Geozentrum, Universität Wien, 1090 Vienna, Austria;
e
Department of Geology,
Southern Illinois University, Carbondale, IL 62901-4502;
f
Golden Prospect Mining Company Ethiopia, Addis Ababa, Ethiopia;
g
Institut für Angewandte
Geowissenschaften, Technische Universität Berlin, 10623 Berlin, Germany;
h
Mikrobielle Phytopathologie and
n
Institut für Ökologie, Friedrich-Schiller-Universität
Jena, 07743 Jena, Germany;
i
Museum für Naturkunde zu Berlin, 10115 Berlin, Germany;
j
Division of Invertebrate Zoology, American Museum of Natural History,
New York, NY 10024;
k
Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7205, Entomologie, Muséum National d’Histoire Naturelle, 75005
Paris, France;
l
Department of Pharmacology and Anaesthesiology, University of Padua, 35131 Padua, Italy;
m
Institute of Geosciences and Earth Resources,
National Research Council and Department of Geoscience, University of Padua, 35137 Padua, Italy; and
o
Department of Botany and
p
Palaeontology Department,
Natural History Museum, London SW7 5BD, United Kingdom
Edited* by David L. Dilcher, University of Florida, Gainesville, FL, and approved March 3, 2010 (received for review January 23, 2010)
Amber is of great paleontological importance because it preserves
a diverse array of organisms and associated remains from dif ferent
habitats in and close to the amber-producing forests. Therefore,
the discovery of amber inclusions is important not only for tracing
the evolutionary history of lineages with otherwise poor fossil
records, but also for elucidating the composition, diversity, and
ecology of terrestrial paleoecosystems. Here, we report a unique
find of African amber with inclusion s, from the Cretaceous of Ethio-
pia. Ancient arthropods belonging to the ants, wasps, thrips, zor-
apterans, and spiders are the earliest African records of these
ecologically important groups and constitute significant discov-
eries providing insight into the temporal and geographical origins
of these lineages. Together with diverse microscopic inclusions,
these findings reveal the interactions of plants, fungi and arthro-
pods during an epoch of major change in terrestrial ecosystems,
which was caused by the initial radiation of the angiosperms.
Because of its age, paleogeographic location and the exceptional
preservation of the inclusions, this fossil resin broadens our under-
standing of the ecology of Cretaceous woodlands.
Arachnida
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Ethiopia
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Hexapoda
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microorganisms
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paleoecology
Ambers contain very important terrestrial taphocenoses.
Arthropods and other invertebrates, small reptiles, feathers,
mammal hairs, plants, and various microbes from different
habitats in and close to the amber forests are commonly pre-
served (1–6). Ambers and other fossil tree resins are found in
hundreds of Old and New World localities (7), with particular
abundance in the Cretaceous and the Eocene to Miocene. Until
now, most amber deposits have been discovered on the former
northern supercontinent Laurasia (SI Appendix,Fig. S1). With
the exception of the Cretaceous Lebanese and Jordanian ambers
(8, 9) and the Eocene Indian and Miocene Amazonian ambers
(10, 11), no fossiliferous amber deposit was known from the
southern continents that formerly formed Gondwana.
Here, we report a unique fossiliferous African amber. The
amber pieces were discovered within the Debre Libanos Sand-
stone Unit from the northwestern Plateau of Ethiopia (Fig. 1).
Because this geologic unit lacks index fossils (12, 13), we used
independent age-relevant information from the amber itself, its
inclusions, and the sporomorphs of the amber-bearing layer to
date the amber. Combined analysis of these physicochemical and
biological parameters revealed a Late Cenomanian age (≈93–95
million years old) for the amber (SI Appendix).
This fossil resin provides a unique window into a mid-Cretaceous
African woodland ecosystem and helps to elucidate the trophic
relationships within this environment. Diverse inclusions of
arthropods, microorganisms, and plant remains reveal manifold
interactions of plants, fungi, and animals during the early phase of
angiosperm evolution.
Results and Discussion
Amber Characteristics. The amber pieces are colorful and trans-
lucent (Fig. 2 Aand B). Chemical analysis of the Ethiopian amber
indicates that it is a Class Ic amber. This result suggests Cheir-
olepidiaceae did not produce the resin, despite the presence of
pollen grains of this Mesozoic conifer family in the amber-bearing
sediment. Infrared spectroscopy shows that this amber is unique
compared with all other fossil resins studied to date. Although we
do not have conclusive information regarding its botanical source,
the resin could have conceivably been produced by a previously
unknown Cretaceous gymnosperm or possibly even by a mid- to
late-Cretaceous angiosperm (SI Appendix).
Arthropods. Arthropod inclusions are abundant in this amber, with
30 fossil specimens preserved in nine of the studied pieces. These
fossils cover an impressive diversity, including the arachnid orders
Acari and Araneae, and at least 13 families of Hexapoda in the
orders Collembola, Psocoptera, Hemiptera, Thysanoptera, Zor-
aptera, Lepidoptera, Coleoptera, Diptera, and Hymenoptera (SI
Appendix,Table S1).
There is a large gap in the Mesozoic terrestrial arthropod
fossil record from the African continent. Compression fossils are
found in only one insect-bearing locality in the Triassic, one in
the Jurassic, and five in the Cretaceous (14). Thus, the Ethiopian
amber assemblage is of major significance for understanding the
biogeography and evolutionary history of African biota. Pre-
liminary identification of the inclusions has revealed noteworthy
discoveries: Most specimens represent a unique fossil record of
their group from Africa, and some are among the oldest records
in the world (Figs. 3 and 4, and SI Appendix,Fig. S10).
The most outstanding discovery is a complete, well-preserved
although enrolled, wingless female ant (Formicidae; Fig. 3A).
Visible characters preclude affinities with the extinct Spheco-
myrminae, which is the only subfamily recorded for contempora-
Author contributions: A.R.S., V.P., and N.V. designed research; A.R.S., V.P., M.S., K.B.A.,
K.H.B., H.D., S.J., B.M., E.M., P.C.N., A.N., P.N., E.R., G.R., E.E.S., H.S., P.A.S., and N.V. per-
formed research; A.R.S., V.P., M.S., K.B.A., R.B., H.D., B.M., P.C.N., A.N., P.N., E.R., G.R.,
E.E.S., H.S., P.A.S., and N.V. analyzed data; and A.R.S., V.P., K.B.A., B.M., P.C.N., E.R.,
E.E.S., K.S., P.A.S., and N.V. wrote the paper.
The authors declare no conflict of interest.
*This Direct Submission article had a prearranged editor.
1
To whom correspondence may be addressed. E-mail: alexander.schmidt@geo.uni-goettingen.
de or vincent.perrichot@univ-rennes1.fr.
This article conta ins supporting information online at www.pnas.org/ cgi/content/full/
1000948107/DCSupplemental.
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neous and older ants in mid-Cretaceous Burmese and French
amber (15, 16). Regardless of the subfamily, this discovery is sig-
nificant because it is one of the oldest records of an ant and the
earliest from Gondwana. It has been suggested that ants arose in
Laurasia during the Early Cretaceous (16–18), but the present
discovery challenges this hypothesis. Ants evolved concurrent with
the rise of angiosperms but apparently remained scarce until
radiating into the world’s most diverse and ecologically dominant
eusocial organisms during the Paleogene (19). The discovery will
aid in resolving the phylogeny and timescale of ant lineages.
Other significant inclusions comprise a male spider that likely
belongs in the Linyphiidae (Fig. 3B), a family of small spiders
that weave sheet-webs (20). This specimen is the second-oldest
linyphiid discovered to date, the oldest being from Hauterivian–
lower Aptian Lebanese amber (21), and only the third fossil
spider species to be described from the African continent (22).
Extant linyphiids are globally distributed but most diverse and
common in mesic and hydric regions of the Northern Hemi-
sphere (23). A thrips (Fig. 3C) belonging to the Merothripidae is
only the second Cretaceous merothripid found to date, the other
one being a dubious specimen from Lebanese amber (24), and
only the third known fossil from this group. The merothripids are
a small but worldwide family, with most species residing in the
Neotropics and in North America; these tiny insects feed on
fungal mycelia on the forest floor or under the bark of decaying
trees. The only identifiable springtail (Fig. 3D) belongs to the
Isotomidae, which is known from one older record in Burmese
amber and a few younger Cretaceous and Cenozoic ambers (25).
Also identified is a zorapteran (Fig. 3E), an order of minute,
gregarious insects that are exceedingly rare in the fossil record,
with the oldest examples from Lower Cretaceous Jordanian and
Burmese ambers (9, 26). This order exhibits remarkable mor-
phological stability, because most Cretaceous representatives
belong to the extant genus Zorotypus. The fossil and extant dis-
tribution of this genus in virtually all tropical areas indicates a
great antiquity for the group. We found various wasps of the
cosmopolitan families Eulophidae, Mymaridae, Mymar-
ommatidae, and Trichogrammatidae (Fig. 3 F–Iand SI Appendix,
Fig. S10 Jand K), which are among the earliest fossils of these
small wasps that parasitize eggs and larvae of microlepidoptera,
beetles, various other insects, arachnids, and nematodes. Lep-
idoptera are evidenced by the presence of microscopic scales (SI
Appendix,Fig. S10F). Cretaceous ambers mostly fossilized
microlepidopterans such as Micropterigidae, but the preservation
of scales alone do not allow for a familial determination. Finally,
one leg and a partial head of a beetle were found fossilized in the
amber (SI Appendix,Fig. S10 Hand I), but it was not possible to
assign those fragments to any beetle lineage.
Microorganisms. Microinclusions of bacteria and fungi occur in
almost every studied amber piece, and a few nematodes were
also found (Fig. 2Cand SI Appendix,Fig. S11). Rod-shaped
bacteria are seen as chains of cells attached to detritus and
decayed arthropods (SI Appendix,Fig. S11 A–C).
Thousands of septate, mostly four-celled and slightly curved
fungal conidia, which are related to the extant anamorphic asco-
mycete genus Curvularia, are enclosed in the amber (Fig. 2Cand SI
Appendix,Fig. S11F). Extant species of this genus are common
parasites of vascular plants. The fossil spores are attached to sur-
faces of successive resin flows in the amber pieces, indicating that
they dropped down onto the liquid resin. The plethora of conidia
and the occurrence of the related conidiophores in the amber (SI
Appendix,Fig. S11E) suggest that this Cretaceous Curvularia-like
species sporulated plentifully at the site of the resin-bearing trees.
The Ethiopian amber also provides evidence of fungivory in the
Mesozoic. Many Curvularia-like conidia and possible remnants of
the perithecia of its teleomorph were found inside insect fecal pellets
of up to 800 ×250 μm(Fig.2Cand SI Appendix,Fig. S11 G–I); these
pellets are too large to have been produced by springtails and mites
trapped close to the fungi in the amber pieces. Instead, beetles or
their larvae are the most probable grazers of this Cretaceous fungus.
Epiphytic fungi with globular, dark-colored hyphae are also
enclosed (SI Appendix,Fig.S11 J–L). They belong to the sooty molds,
Fig. 1. Location of the Ethiopian amber deposit. The white rectangle on the
geologic map indicates the area shown in detail. The red asterisk designates
the locality of the outcrop (10°08’45’’ N latitude, 38°57’56’’ E longitude).
Area map redrawn from Assefa (12).
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an ecological group of saprophytic fungi that are mostly assignable to
the Capnodiales (Ascomycota), which produce colonies on the sur-
face of living plants. Sooty molds typically obtain their nutrients from
the excretions of aphids, scale insects, and other producers of hon-
eydew, or from plant exudates. The discovery of mid-Cretaceous
epiphytic sooty molds is an example of the morphological stability or
stasis of taxa that, once adapted to particular microhabitats, preserve
their morphological features over some 100 million years.
Plant Remains. Remnants of plants are preserved in the form of
spores from homosporous ferns and lycophytes, pollen grains likely
belonging to the gymnosperm family Podocarpaceae and leaf cuticles
that are probably remnants from some early diverging angiosperm
families such as the Lauraceae, Chloranthaceae, or Proteaceae (SI
Appendix,Fig. S12 A–C). Some of the more remarkable minute plant
remnants are abundant stellate hairs (Fig. 2 Dand Eand SI Appendix,
Fig. S12 D–F). Comparison of these hairs to modern plants excludes
any relation to angiosperms and instead suggests ferns as the likely
source, e.g., the tree fern family Cyatheaceae and the mostly epiphytic
filmy fern family Hymenophyllaceae. As in the fossils, the stellate
hairs of extant representatives of these fern families are composed of
flat rays with margins that curve upward when drying and later drop
from the fronds.
Paleoecology. The onset and evolutionary success of angiosperms
led to a reorganization of terrestrial ecosystems in the middle
Cretaceous (27, 28). Coevolutionary events of plants and animals
provided a basis for radiation and speciation. Archaic gymno-
sperms declined and modern gymnosperm and fern families
diversified in the shadow of the angiosperms. As a result, there
was tremendous macroscopic change in terrestrial ecosystems
that influenced many groups of insects, fungi, and liverworts, and
probably also amphibians and mammals (28–31). In the Cen-
omanian, angiosperms were no longer restricted to early suc-
cession stages but became dominant in woodlands worldwide. In
this time of change, the Ethiopian amber forest represents an
ecosystem in which both conifers, such as members of the extinct
Cheirolepidiaceae and the extant Podocarpaceae families, and
early angiosperms co-occurred. The sporomorphs of the amber-
bearing sediment show that other conifers, different angiosperms
and diverse fungi, mosses, lycophytes, and ferns were also
abundant in this amber forest (SI Appendix,Fig. S9 and Fig. S12).
An epiphytic community comprising ferns and fungi developed.
Ascomycetes played a role not only as decomposers but also as
parasites and served as a food source for insects. Although an-
giosperms were present in the Ethiopian amber forest, no insects
were found that would have pollinated their early flowers. Many
hexapods trapped by the tree resin occupy other functional
niches in extant forests, such as small aerial parasitoids (wasps)
and fungivores or detritivores (springtails, merothripid, pso-
copteran, zorapteran) living among the leaf litter or under tree
bark. Predators are represented only by the ant, which was
probably foraging on the soil and on plants, and the linyphiid
spider, whose extant relatives typically construct webs close to
the ground in leaf litter, although some build webs in bushes or
other vegetation.
The Ethiopian amber is of great importance for improving our
knowledge of the evolutionary history of terrestrial arthropods,
Fig. 2. Ethiopian amber and its microinclusions. (A) Large translucent piece of amber of ≈1150 g (NHMW, N3881). (B) Color of amber pieces (MB. Pb. 2009/205).
(C)Curvularia-like fungal spores in an insect fecal pellet (MB. Pb. 2009/201). (D) Stellate hair resembling those of modern tree ferns of the family Cyatheaceae
(NHMW, N6964). (E) Stellate hair resembling those of the modern epiphytic filmy fern family Hymenophyllaceae (MB.Pb. 2009/206). (Scale bars: A, 1 cm, B, 1 mm;
C–E, 100 μm.)
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ECOLOGYGEOLOGY
plants, and fungi during the initial radiation of angiosperms in
the Cretaceous. Additional discoveries of unique amber deposits
will aid in closing the large gap in the Mesozoic record of ter-
restrial arthropods from the African continent.
Materials and Methods
Locality. The unique amber deposit was discovered near the town of Alem
Ketema in the eastern part of the northwestern Plateau of Ethiopia (Fig. 1). The
amber pieces occur in a siltstone within the Debre Libanos Sandstone Unit,
exposed along the slopes of the Wenchit River valley (SI Appendix,Fig. S2). A
few hundred pieces of amber have been recovered so far; we had access to 62
of them for investigation. Most of the pieces are 1–5 cm in size, but single
pieces of up to 25 cm were also found (Fig. 2Aand SI Appendix,Fig. S3 Aand B).
Preparation and Microscopy. The pieces of amber were ground and polished
manually with a series of wet silicon carbide abrasive papers [grit from FEPA
P 600–4000 (25.8 μmto5μm particle size), firm Struers] to remove the
weathered opaque surface and to minimize light scattering for the inves-
tigation. The original amber pieces were sometimes separated to isolate
inclusions for investigation. The inclusions were studied by using incident-light
microscopes (Carl Zeiss Stemi 2000 and Olympus SZH-ILLD) and transmitted-
light microscopes (Carl Zeiss AxioScope A1 and Olympus BX50) equipped with
Canon 450D and Olympus Color View IIIu digital cameras. In some instances,
incident and transmitted light was used simultaneously. To better illustrate
the three-dimensional inclusions, some photomicrographs were combined by
using the software package HeliconFocus 4.45. Fig. 3 C–Iand SI Appendix,Fig.
S9 A,C,Dand H–N,Fig. S10 Aand C–L,Fig. S11 B,D, and E, and Fig. S12 A–Cand
E, were obtained from several optical sections.
Fig. 3. Assorted arthropods fossilized in CretaceousEthiopian amber. (A) A worker ant (Hymenoptera, Formicidae; NHMW, N6976). (B) A male sheet-web weaver
spider (Araneae ,L inyphiidae; MB. A 1664). (C) A thrips (Thysanoptera, Merothripidae;NHMW, N6974a). (D)A springtail (Collembola,Isotomidae; NHMW,N6969). (E)
A Zoraptera (NHMW,N6991). (F) A wasp of the Eulophidae(Hymenoptera;NHMW, N6966a).(G) A fairy wasp (Hymenoptera,Mymaridae; NHMW,N6970). (H)Afalse
fairy wasp (Hymenoptera, Mymarommatidae; NHMW, N6965a). (I) A representative of the Trichogrammatidae (Hymenoptera; MB. I 5654). (Scale bars: 500 μm.)
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Repository. The amber pieces are deposited in the Museum für Naturkunde
zu Berlin, (MB. Pb. 2009/200 to MB. Pb. 2009/211, MB Pb. 2009/313 to MB Pb.
2009/341, MB. I 5654 to MB. I 5657, and MB. A 1664), in the Department of
Mineralogy and Petrography, Naturhistorisches Museum Wien, (NHMW,
N3881 and NHMW, N6964 to NHMW, N6991) and in the American Museum
of Natural History, New York (three pieces, sine numero). Please note that
some of the original 62 amber pieces were divided to investigate the
inclusions; each obtained fragment now has a separate collection number.
ACKNOWLEDGMENTS. We thank S. and H. Kaiser (Maria Enzersdorf, Austria)
for providing amber pieces for this study, A. Beran (Vienna), A. Chilin (Padua,
Italy), A. Giaretta (Padua, Italy), V. M. F. Hammer (Vienna), S. Salzmann
(Berlin), E. Stenzel (Berlin), and M. Weber (Vienna) for technical support and B.
Kosmowska-Ceranowicz (Warsaw), C. Pott (Stockholm), and E. Schrank (Berlin)
for discussion. This is contribution number 35 from the Courant Research
Centre Geobiology that is funded by the German Initiative of Excellence, and a
contribution to the project AMBRACE (BLAN07-1-184190) of the French
National Research Agency.
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