Amber from western Amazonia reveals Neotropical diversity during the middle Miocene

Abstract

Tertiary insects and arachnids have been virtually unknown from the vast western Amazonian basin. We report here the discovery of amber from this region containing a diverse fossil arthropod fauna (13 hexapod families and 3 arachnid species) and abundant microfossil inclusions (pollen, spores, algae, and cyanophyceae). This unique fossil assemblage, recovered from middle Miocene deposits of northeastern Peru, greatly increases the known diversity of Cenozoic tropical–equatorial arthropods and microorganisms and provides insights into the biogeography and evolutionary history of modern Neotropical biota. It also strengthens evidence for the presence of more modern, high-diversity tropical rainforest ecosystems during the middle Miocene in western Amazonia.

• Pebas Formation
• Peru
• Hexapoda
• Arachnida
• microorganisms

Full text

Amber from western Amazonia reveals Neotropical
diversity during the middle Miocene
Pierre-Olivier Antoine*
†‡
, Dario De Franceschi
†§
, John J. Flynn
†¶
, Andre
´
Nel
†§
, Patrice Baby*
储
, Mouloud Benammi**,
Ysabel Caldero
´
n
††
, Nicolas Espurt*
储
, Anjali Goswami
‡‡
, and Rodolfo Salas-Gismondi
§§
*Laboratoire des Me´ canismes et Transferts en Ge´ ologie, Unite´ Mixte de Recherche–Centre National de la Recherche Scientifique 5563, 14 Avenue E
´
douard
Belin, F-31400 Toulouse, France;
§
De´ partement Histoire de la Terre, Muse´ um National d’Histoire Naturelle, Unite´ Mixte de Recherche–Centre National de la
Recherche Scientifique 5143, F-75231 Paris Ce´ dex 05, France;
¶
Division of Paleontology, American Museum of Natural History, Central Park West at 79th
Street, New York, NY 10024-5192;
储
Institut de Recherche pour le De´ veloppement, Miraflores, Lima 18, Peru´ ; **Laboratorio de Paleomagnetismo,
Universidad Nacional Autonoma de Mexico, Mexico City, Mexico;
††
Perupetro, Avenida Luis Aldana 320, San Borja, Lima 41, Peru´;
‡‡
Palaeontology
Department, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom; and
§§
Departamento de Paleontologı´a de Vertebrados,
Museo de Historia Natural Javier Prado, Universidad Nacional Mayor de San Marcos, Lima 11, Peru´
Communicated by W. A. Berggren, Woods Hole Oceanographic Institution, Woods Hole, MA, July 12, 2006 (received for review March 15, 2006)
Tertiary insects and arachnids have been virtually unknown from
the vast western Amazonian basin. We report here the discovery
of amber from this region containing a diverse fossil arthropod
fauna (13 hexapod families and 3 arachnid species) and abundant
microfossil inclusions (pollen, spores, algae, and cyanophyceae).
This unique fossil assemblage, recovered from middle Miocene
deposits of northeastern Peru, greatly increases the known diver-
sity of Cenozoic tropical–equatorial arthropods and microorgan-
isms and provides insights into the biogeography and evolutionary
history of modern Neotropical biota. It also strengthens evidence
for the presence of more modern, high-diversity tropical rainforest
ecosystems during the middle Miocene in western Amazonia.
Pebas Formation 兩 Peru 兩 Hexapoda 兩 Arachnida 兩 microorganisms
A
mbers and other fossilized natural tree resins are com-
mon, documented in hundreds of Upper Paleozoic to
Recent localities from around the globe. In exceptional cases,
they can entomb pollen (1) or delicate and soft-bodied organ-
isms that are poorly sampled or absent in the fossil record
(2–4). Most of these amber-bearing deposits are restricted to
the Northern Hemisphere: Only three South American Ceno-
zoic localities have been reported, from the Eocene of Pat-
agonia, Miocene of eastern Brazil, and Pleistocene of French
Guyana (4, 5). We report the previously undescribed occur-
rence of fossil-bearing amber from the vast western Amazo-
nian basin, a region of extraordinary biological diversity today,
but whose fossil record has been virtually unknown for most
modern groups. Although the Miocene Pebas Formation of
northeastern Peru had long been investigated in paleontolog-
ical studies [mollusks, fishes, and pollen (6–10)], amber clasts
with organic inclusions are known from only a single level that
we discovered in 2004. This amber is especially noteworthy for
containing a diverse fossil arthropod fauna [at least 13 differ-
ent families of Hexapoda (in the Collembola, Coleoptera,
Diptera, Hemiptera, Hymenoptera, Orthoptera, Psocoptera,
and Trichoptera) and 3 arachnid species] and abundant mi-
crofossil inclusions [pollen, spores (30 morphotaxa, including
⬎20 fungi), algae, and cyanophyceae].
Results and Discussion
Three large and 25 smaller clasts (⬇150 g, in 50-g ⫹ 50-g⫹ 30-g
⫹ smaller clasts) were recovered, two of which include trapped
arthropods and pollen (see Figs. 2B, 3, and 4 and Tables 1 and
2). Others include spores or dispersed organs of cyanobacteria,
fungi, and freshwater algae, as well as a few unicellular organ-
isms (see Fig. 4 and Table 1). All of the amber clasts originate
from a single level of the Pebas Formation [18–10 million years
ago; ‘‘Solimo˜es Fm’’ in Brazil (10, 11)] in the Tamshiyacu locality
on the eastern bank of the Amazon River, ⬇30 km upstream of
Iquitos in northeastern Peru (Figs. 1 and 2). This outcrop has
been intensively studied for biostratigraphy and lithogenesis (7,
10, 11); it consists of two coarsening-upward parasequences,
together referred to the middle Miocene Crassoretitriletes Zone
(⬇15–12 Ma), based on the occurrence of C. vanraadshoovenii
pollen (7, 10, 11). The amber-bearing level corresponds to a
transgressive lag in the upper parasequence (TmB) (11), just
above bottom lignites (Fig. 2 A). ‘‘Rare detrital amber’’ was
already mentioned within this parasequence (11), but it was not
investigated further, and no fossil inclusions were reported. In
fact, it appears to be relatively abundant and of large size within
the locality. Even though the nature of the depositional envi-
ronments of Pebas strata has been widely debated throughout
the last decade (7, 10–14), with inferences ranging from fluvial,
Conflict of interest statement: No conflicts declared.
†
P.-O.A., D.D.F., J.J.F, and A.N. contributed equally to this work.
‡
To whom correspondence should be addressed. E-mail: poa@lmtg.obs-mip.fr.
© 2006 by The National Academy of Sciences of the USA
Fig. 1. Map of the Iquitos area (northeastern Peru) showing the geographic
location of the middle Miocene amber-bearing locality of Tamshiyacu (IQ 26),
denoted by an open circle. Map was redrawn from ref. 10.
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lacustrine, and brackish to tidal environments, most authors
acknowledge the occurrence of episodic marine incursions, most
likely of Caribbean origin (9–16).
Amber allows the fossilized preservation of delicate plant
structures [flowers or pollen (1, 17)], soft-bodied animals [e.g.,
nematodes, annelids, gastropods, arthropods, and small verte-
Fig. 3. Photographs of Euarthropoda in amber from the
Miocene of Iquitos (northeastern Peru). (A) Coleoptera:
Cucujoidea: Sphindidae. (Scale bar, 0.6 mm.) (B) Psocop-
tera, family undetermined. (Scale bar, 4 mm.) (C) Diptera:
Ceratopogonidae (female). (Scale bar, 0.7 mm.)
(D) Diptera: Chironomidae (male). (Scale bar, 1 mm.)
(E) Hemiptera: Aleyrodidae (male). (Scale bar, 0.8 mm.)
(F) Arachnida: Acarina (mite). (Scale bar, 0.2 mm.)
Fig. 2. Amber-bearing Tamshiyacu section (IQ 26, Iquitos area, northeastern Peru). (A) Middle Miocene amber-bearing level is indicated by black arrow.
(B) Large amber clast from the level in A (length ⬇ 70 mm) at natural size.
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brates (4, 17–19)], and microorganisms (20), which allows their
comparison with recent organisms. Contrary to what occurs in
Dominican amber, which preserves membrane structures, mus-
culature, and nerve tissue of arthropods (4), the amber clasts
from Iquitos only preserved cuticles. However, these organisms
are sufficiently well preserved to be identified precisely and used
as paleoenvironmental markers. In addition, this fossilized resin
from Iquitos preserves partial cell contents of some microor-
ganisms and pollen grains, as also observed in Baltic and Paris
basin ambers (21). Because it represents a previously unde-
scribed Neogene insect assemblage from western Amazonia, the
entomofauna is entirely unique and reflects only an initial
sample of what is likely to be a much more diverse assemblage,
necessitating broader taxonomic and phylogenetic analyses. Nev-
ertheless, preliminary identifications already reveal significant
taxonomic and ecological diversity, including two humid-
environment, ground-living Hexapoda (Collembola) and a
Trichoptera (Hexapoda with aquatic larvae). Among the
Diptera, the families Mycetophilidae, Chironomidae (Fig. 3D),
Ceratopogonidae (two specimens; Fig. 3C), Phlebotomidae, and
Phoridae are represented. The first four of these dipteran
families frequently live in humid environments. An adult Co-
leoptera (Cucujoidea: Sphindidae) is also present (Fig. 3A).
These beetles are myxomycophagous specialists, living in forests
on, or inside, mold sporocarps. There are also male and female
specimens of Hemiptera: Aleyrodidae (Fig. 3E), and two para-
sitoid Hymenoptera, one Chalcidoidea: Aphelinidae (which live
in Hemiptera [Aleyrodoidea, Aphidoidea, Auchenorrhyncha,
Psylloidea, and Coccoidea]), and one Scelionidae, plus four
undetermined insects, including a Psocoptera (Fig. 3B). Repre-
sentatives of the arachnids include at least three species of Acari
(Fig. 3F). The numerous microorganisms found in the other
amber clasts (Fig. 4) are fungi spores and conidia, cyanobacteria
cells (Fig. 4B), eubacteria (Fig. 4A), and a few freshwater green
algae. Among hundreds of individual spores and other micro-
structures, ⬎30 different morphotaxa could be identified (Table
1). These include many previously undescribed species, which
need to be studied comprehensively. The overall assemblage of
known spore species documents an early and兾or middle Miocene
age (22), confirming contemporaneity for both this amber and
the lithologic unit in which it is found (late early to early middle
Miocene age Pebas Formation). A previously undescribed spe-
cies of Frasnacritetrus (Staurosporea), a four-forked spore, is
related to the modern genus Tetraploa [usually associated with
Poaceae (grasses), Cyperaceae (sedges), or some tree species].
The rarity and fragility of these spores recovered from sediments
suggest that they could represent contamination by recent
Tetraploa (22). The presence of this specimen (Fig. 4G) within
Miocene amber testifies to definitive occurrence of this genus
in the early Neogene and could also indicate greater habitat
complexity than might be expected in the dense rainforest-do-
minated environment suggested by the other amber organisms.
Arthropods and microorganisms play an exceptionally impor-
tant role in modern terrestrial ecosystems (4), and amber-
Fig. 4. Microfossils in Miocene amber from western Amazonia (Iquitos, northeastern Peru) in photographs taken under a light microscope. (A) Eubacteria.
(B) Nostocaceae (Cyanobacteria). (C) Quilonia sp., pluricellate spores, specimens close to the modern Alternaria.(D) Polycellulaesporonites sp., also found in
modern Alternaria species. (E) Pluricellulaesporites sp. (F) Scenedesmus sp. (G) Frasnacritetrus sp., four-branched spore (only two are visible here in the microscope
focus). (H) Phragmothyrites sp., small subcircular ascostroma. (I) Hypoxylonites sp., fungal or algal spores. (J) Triporopollenites sp., pollen grain of a Proteaceae
(Eudicotyledons: Magnoliophyta).
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preserved specimens provide key paleoenvironmental informa-
tion for the middle Miocene ecosystems of the western
Amazonian Basin. Resin entombment of an organism is a rapid
preburial process (4). Further, amber is insoluble in water (3) but
with a density close to it (1.04–1.10; Iquitos clast density ⫽ 1.06),
which allows its long-distance transportation in running water
and preservation in various proximal and downstream deposi-
tional environments (often associated with wood debris), includ-
ing delta-plain and兾or tidal environments (4). Occurrence of
amber containing terrestrial organisms is consistent with previ-
ous reconstructions of the depositional environment of the
Tamshiyacu sedimentary series (11, 14), accumulating near the
shore of a tidally influenced ‘‘marine-like megalake’’ (10). Some
amber deposits (notably Baltic amber) are known to be re-
worked, depending on both their density and the salinity of the
transporting water. The Iquitos amber clasts are unlikely to be
reworked from much earlier deposits because of the following:
(i) the Iquitos resin flows have kept their original shape (Fig.
2B); (ii) several trapped spore taxa have an early to middle
Miocene stratigraphical range, indicating contemporaneity with
the surrounding sedimentary matrix (Pebas Fm.); and (iii) the
composition and aspect of this Amazonian amber precludes the
occurrence of any subsequent tectonic deformation and兾or
sediment burial effect, such as that often observed in reworked
ambers (23, 24).
Many recent families of conifers and angiosperms generate
resins (25), but only a few of them have been documented to
be amber producers (4) through anatomical studies of associ-
ated amber and wood specimens [Pinaceae (17, 26); Caesal-
piniaceae (27)]. It is currently impossible to identify the
specific amber-producing tree(s) for the Iquitos specimens, but
the presence of fossil wood and excellent and laterally exten-
sive outcrops suggest that intensive sampling should permit
recovery of such connected specimens in the near future. In
the interim, however, infrared spectrometry (26), solubility,
and chemical properties indicate that the Iquitos amber orig-
inates from an angiosperm tree. Resin production is known to
have both seasonal and diurnal fluctuations [resin exudations
are more frequent during the warm season and in higher daily
temperatures (4)]. The alternating bands observed in the
Iquitos amber clasts can be inferred to represent successive
resin flows, as proposed for similarly banded ambers (18).
Periods of intensive amber production have been interpreted
to be due to either frequent storm damage to source trees or
intense forest fires [notably in relation to periods of drastic
paleoenvironmental changes (28)] or to the abundance of
mature trees in surrounding forests (23). The preliminary
sample is too small to provide unequivocal conclusions re-
garding which of these causes might have been responsible for
the resin exudation forming the Iquitos ambers.
The available insect sample (14 specimens) is sufficiently large to
provide several additional paleoecological inferences. As in all
other known amber insect associations, Hymenoptera and Diptera:
‘‘Nematocera’’ dominate. This dominance relates to a probable bias
of attraction of these insect groups to the resin, particularly with
respect to the position of the exudate in the tree or to the behavior
Table 1. Microorganisms entrapped in amber from the middle Miocene of Tamshiyacu, nearby Iquitos (northeastern Peru)
Binomen Higher-level taxon
Mycophyta
Psiamasporites fusiformis (Salard-Cheboldaeff & Locquin, 1980) Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Inapertisporites clarkei (Kalgutkar & Jansonius, 2000) Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Inapertisporites spp. Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Monosporites cf. magnus (Kalmghutkar, 1993) Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Monosporites sp. Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Hypoxylonites spp. Amerosporae (‘‘Fungi imperfecti’’ fungal or algal spore)
Dicellaesporites sp. Didymosporae (‘‘Fungi imperfecti’’ ⫽ Deuteromycetes)
Dicellaesporites cf. obnixus (Norris, 1986) Didymosporae (Deuteromycetes)
Dicellaesporites cf. perelongatus (Kalgutkar & Jansonius, 2000) Didymosporae (Deuteromycetes)
Dicellaesporites africanus (Salard-Cheboldaeff, 1980) Didymosporae (Ascomycetes)
Dicellaesporites inequabilis (Martinez-Hernandez & Tomasini-Ortiz, 1989) Didymosporae (Deuteromycetes)
Dicellaesporites longus (Trivedi & Verma ex Kalgutkar & Jansonius, 2000) Didymosporae (Deuteromycetes)
Dyadosporites cf. minor (Salard-Cheboldaeff & Locquin, 1980) Didymosporae (Ascomycetes)
Kumarisporites sp. Phragmosporae (Deuteromycetes)
Reduviasporonites sp. Phragmosporae (Deuteromycetes)
Multicellites sp. Phragmosporae (Deuteromycetes)
Pluricellulaesporites sp. Phragmosporae (Deuteromycetes)
Quilonia spp. Phragmosporae (Deuteromycetes, 1 sp. cf. Alternaria)
Multicellaesporites sp. Phragmosporae (Deuteromycetes)
Diporicellaesporites fusoides (Salard-Cheboldaeff & Locquin, 1980) Dematiaceae (Phragmosporae)
Diporicellaesporites (Elsik, 1968) sp. Dematiaceae (Phragmosporae)
Dictyosporites (Felix, 1894) sp. Dictyoporeae (Deuteromycetes)
Polycellulaesporonites (Chandra, Saxena, & Setty, 1984) sp. Dictyoporeae (Deuteromycetes)
Frasnacritetrus spp. Staurosporae (Deuteromycetes)
Trilobites sp. Staurosporae (Deuteromycetes)
Phragmothyrites sp. Microthyriales (Phragmothyrium, Ascomycetes)
Lichen
Gen. et sp. indet. Incertae sedis
Chlorophyta
Scenedesmus sp. Scenedesmaceae
Magnoliophyta
Triporopollenites sp. Proteaceae
List is sorted by morphographic order for spores (22). Identification was by D.D.F.
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and local habitat of the trapped organisms (2, 4, 29). However, the
insects in the Iquitos amber seem to be associated with a humid
terrestrial environment, probably in a forest, which is consistent
with the identified fern spores and the large amount of unidentified
lignitic plant remains from the same layers (11). Unfortunately, the
lignitic fragments are partly transformed into vitrinite, which pre-
cludes any infrafamiliar identification of the associated trees. The
high diversity (13 different families for 14 specimens) and ecological
disparity (presence of parasitoids, phytophagous, myxomycopha-
gous, blood feeding, and detritivorous taxa) observed in even just
this preliminary sample suggest a rich and complex entomofauna
for the middle Miocene of western Amazonia (Table 2), consistent
with broader continental and global conditions associated with the
high Miocene floral diversity (30) and the Miocene Climate Opti-
mum (12). In addition, the Iquitos amber yields some Hexapoda
with aquatic affinities (Trichoptera, whose larvae are strictly
aquatic) and a small ground soil fauna (Collembola), as also occurs
in Baltic amber (28).
Light microscopy also revealed a preserved microcenosis. The
abundance of fungus spores and other microorganisms and the
comparative rarity of pollen (one pollen grain only) reveal that
these small resin flows most likely formed in the closed under-
growth of a moist forest, on the bark of the trunk or branches of the
amber-producing tree(s). Some of the fungal spores belong to
parasite or saprophyte groups found on wood, which could have
colonized tree injuries (broken branches or insect attacks) and
might have been trapped in the resin flow during cicatrization. The
occurrence of epiphytous predators, such as spiders, may also
promote carcass concentrations, as observed in the amber clast that
contained several spider webs (4, 18).
The Cenozoic history and evolution of terrestrial arthropods
and microorganisms is poorly documented in South America; for
instance, fossil insects were previously known only from three
lacustrine Oligocene Brazilian basins (31). Later in the Ceno-
zoic, nothing has been recorded from the Amazon area before
Holocene copal from Santander (Colombia), ⬍1,000 years old
(32). Comparisons with the entomofaunas of the Oligocene–
Miocene Dominican and Oligocene Chiapas amber (Mexico)
shall be of great palaeobiogeographical interest, because Do-
minican and Mexican ambers represent mid-Cenozoic faunas of
the two main transitional areas between North and South
America. Direct comparisons should be possible because the
potential taphonomic biases related to the chemical nature of the
ambers would be very similar in the three cases, because they
have comparable angiosperm origins.
Previous studies suggested that the Miocene of the Amazon
Basin sheltered high-diversity ecosystems, which were supposed
to have originated from climatic change (30), island biogeogra-
phy (33), or variable habitat (34). Yet, throughout Neogene
times northern South America is likely to have formed a single
floristic province, of which western Amazonia was a part [based
on pollen studies (7)]. The same palynostratigraphic data (7)
indicated that the regional vegetation already was a tropical
rainforest, with dominant swamp, alluvial plain, and aquatic
elements, with intermittent mangrove systems, throughout the
Crassoretitr iletes Zone [middle Miocene (7, 30)]. At the same
time, open habitats occurred, as revealed by typical floristic
elements, such as Poaceae (grasses).
The amber sample testifies both to high annual rainfall [with
marked seasonality (10)] and to exceptionally high plant and animal
diversity (30), providing more robust inferences about the timing of
establishment of high biodiversity and more modern ecosystems
and climate regimes in western Amazonia. For example, the diverse
animals, plants, fungi, and cyanobacteria entrapped in this initial
small amber sample substantiate that humid and densely forested
environments in a tropical climate must have been present by the
middle Miocene in western Amazonia. Future work on this assem-
blage should more widely elucidate the pattern of changes in biotic
diversity, palaeoenvironment, and paleoecology of an area that
experienced drastic environmental changes (7, 8) throughout the
Miocene (12, 30).
Materials and Methods
The amber clasts were hand-picked directly within the amber-
bearing level, for a width of ⬇200 m along a vertical riverbank.
This preliminary sampling method may have introduced a bias in
the frequency of arthropods within the amber inclusions (with-
out screening, we could not collect enough small fragments that
might contain more arthropods). Systematic screening of the
amber-bearing level is needed. The amber clasts and prepara-
tions are temporarily housed in the Muse´um d’Histoire Naturelle
(Paris, France) and belong to the collections of the Museo de
Historia Natural (Lima, Peru).
We thank Michel Lemoine and Gae¨l De Ploe¨g for their help in specimen
preparation, Laurent Marivaux for improving a previous version of the
manuscript, and George Poinar and Bruce MacFadden for helpful com-
mentary. This work was supported by the Environnements et Climats du
Passe´: Histoire et Evolution (ECLIPSE) Program of France, the Centre
National de la Recherche Scientifique, the Institut de Recherche pour le
De´veloppement, the National Aeronautics and Space Administration, the
Field Museum (Chicago, IL), and the American Museum.
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Table 2. Taxonomy of Hexapoda entrapped in amber
from the middle Miocene of Tamshiyacu, nearby Iquitos
(northeastern Peru)
Amber sample兾slide Entrapped Hexapoda
IQ 26IA1 (6) Diptera: Phoridae (female)
IQ 26IA (4) Coleoptera: Cucujoidea: Sphindidae
IQ 26IA (1) Diptera: Brachycera: Cyclorrhapha, family
undetermined
IQ 26IA2B Diptera: Chironomidae subfamily
Orthocladiinae (male)
IQ 26IA1 (7 and 9) two Diptera: Ceratopogonidae (female)
IQ 26IA (5) Hemiptera: Aleyrodidae (male)
IQ 26IA2 (10) Diptera larva, family undetermined
IQ 26IA2 Psocoptera, family undetermined
IQ 26IA3 Orthoptera wing fragments, family
undetermined (?) ⫹ Hemiptera
Aleyrodidae (female)
IQ 26IA3 Hymenoptera: Ichneumonidae (?)
IQ 26IA1 Hymenoptera: Chalcidoidea: Aphelinidae
Unlabeled Diptera: Phlebotomidae (female)
Unlabeled Diptera: Mycetophilidae ⫹ Hymenoptera:
Scelionidae
Unlabeled Hexapoda: Collembola
Unlabeled Hexapoda: Trichoptera
Identification was by A.N.
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