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Biting midges (Diptera: Ceratopogonidae) from the Early Cretaceous El Soplao
amber (N Spain)
R. Pérez-de la Fuente
a
,
*
, X. Delclòs
a
, E. Peñalver
b
, A. Arillo
c
a
Departament d’Estratigrafia, Paleontologia i Geociències Marines, Facultat de Geologia, Universitat de Barcelona, Martí i Franqués s/n, E-08028 Barcelona, Spain
b
Instituto Geológico y Minero de España, Ríos Rosas 23, E-28003 Madrid, Spain
c
Departamento de Zoología y Antropología Física (Entomología), Facultad de Biología, Universidad Complutense, E-28040 Madrid, Spain
article info
Article history:
Received 26 May 2010
Accepted in revised form 10 May 2011
Available online 18 May 2011
Keywords:
Diptera
Ceratopogonidae
New species
Palaeoautoecology
Cretaceous amber
Spain
abstract
Three new species, Lebanoculicoides excantabris,Archiaustroconops borkenti, and Atriculicoides szad-
ziewskii are described from the Early Cretaceous (early Albian) El Soplao amber deposit (Rábago,
Cantabria, northern Spain). Protoculicoides skalskii Szadziewski and Arillo, found in the other Albian
Spanish ambers from Peñacerrada I (in Burgos) and San Just (in Teruel), and Austroconops sp., are
identified from this new outcrop. The find of a new species of Lebanoculicoides Szadziewski is especially
significant since this genus is considered the basalmost known among ceratopogonids. To date, the new
species of Atriculicoides Remm is the oldest occurrence for this genus. A general review of the taxonomy
and phylogeny of the family Ceratopogonidae, and the palaeoecological significance and palaeogeo-
graphic distribution of its basalmost lineages are given. The new data extend knowledge about biting
midges during the Early Cretaceous, a key period for understanding the phylogenetic relationships of the
ancient members of the family.
Ó2011 Elsevier Ltd. All rights reserved.
1. Introduction
Among Diptera, biting midges (Diptera: Ceratopogonidae) are
tiny to small nematocerous flies with a wide variety of feeding
strategies (haematophagy, predation, nectarivory, pollinivory, and
aphagy), and larvae which usually develop in semi-aquatic or moist
environments (Borkent, 1995). With nearly 6000 extant species
distributed worldwide, biting midges are especially plentiful as
amber inclusions, with around 250 extinct species (Borkent, 2011).
This abundance is related to the proximity of their habitat to the
resin sources, their minute size and their swarming behaviour
(Martínez-Delclòs et al., 2004; Grimaldi and Engel, 2005). The
abundant fossil diversity in widespread amber deposits, which
range from the Cretaceous to the Miocene, renders ceratopogonid
flies highly suitable organisms on which to carry out phylogenetic
studies and thus to extract evolutionary patterns (Borkent, 2000a,
Fig. 23).
A new Spanish amber deposit was recently discovered in El
Soplao, near the municipality of Rábago (Cantabria, northern
Spain) (Najarro et al., 2009). Notable features of this outcrop
include the plentiful presence of amber pieces with a blue-violet
glow, a fluorescence conferred by certain organic compounds
(Menor-Salván et al., 2009a, b, 2010), and its special richness in
amber formed by resin exuded under aerial conditions (stalactite-
shaped flows and other flows, like crusts). Amber pieces with
stalactitic or flow morphology and an inner banding pattern as
a result of succesive resin flows probably originated from aerial
polymerised resin. This kind of amber contains a large quantity of
bioinclusions, especially small flying insects, due to its high degree
of exposure (Martínez-Delclòs et al., 2004). Geological and
palaeobiological data indicate that the amber deposit had a para-
utochthonous origin in which wildfires promoted both resin
production and erosion (Najarro et al., 2010). Moreover,
biochemical data suggest that El Soplao amber was generated by
resin exuded by two different coniferous sources (Menor-Salván
et al., 2009a, 2010). Initial studies of El Soplao amber have
provided bioinclusions related to spiders and insects from 11
orders: Blattaria, Isoptera, Psocoptera, Thysanoptera, Hemiptera,
Raphidioptera, Neuroptera, Coleoptera, Hymenoptera, Diptera, and
Trichoptera. To date, the insects described include one new species
of the thysanopteran family Thripidae (Nel et al., 2010), one new
genus and species of the Jurassic-Cretaceous raphidiopteran family
Mesoraphidiidae (Pérez-de la Fuente et al., 2010), and one new
*Corresponding author.
E-mail addresses: perezdelafuente@ub.edu (R. Pérez-de la Fuente), xdelclos@ub.
edu (X. Delclòs), e.penalver@igme.es (E. Peñalver), aarillo@teleline.es (A. Arillo).
Contents lists available at ScienceDirect
Cretaceous Research
journal homepage: www.elsevier.com/locate/CretRes
0195-6671/$ esee front matter Ó2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cretres.2011.05.003
Cretaceous Research 32 (2011) 750e761
species of the hymenopteran family Serphitidae (Ortega-Blanco
et al., 2011).
Here, we describe three new ceratopogonid species from El
Soplao amber and report one genus and one species previously
known from other Cretaceous Spanish ambers. This paper also
discusses their likely habitats and feeding habits, giving an
overview of the taxonomy and phylogeny of the Ceratopogonidae,
as well as the palaeogeographic distribution of its ancient
lineages.
2. Geological setting
El Soplao is located on the north-west margin of the Basque-
Cantabrian Basin. The development of the basin during the Early
Cretaceous is related to the kinematics between the European and
Iberian plates (Malod and Mauffret, 1990; Olivet, 1996). The El
Soplao amber-bearing deposit, early Albian in age, is included
within the Las Peñosas Formation, in a unit of heterolithic
sandstones-siltstones and carbonaceous mudstones related to
broadly coastal delta-estuarine environments (Najarro et al., 2009).
In fact, the El Soplao deposit comprises part of the strip curve
formed from most of the previously known Spanish amber
outcrops, corresponding to the coastline during the Early Creta-
ceous (Delclòs et al., 2007). A 0.7e2.5 m thick level of organic-rich
clays contains the amber pieces, together with plant cuticle
remains mainly belonging to the conifer genera Frenelopsis
(Schenk, 1869) emend. Watson, 1977 and Arctopitys Bose and
Manum, 1990. Gingkoalean leaves of Eretmophyllum Thomas, 1913
(formerly cited for this outcrop as Nehvizdya) and Pseudotorellia
Florin, 1936 are found as well. Palinological information that
completes the overview of the palaeoforest is given in Najarro et al.
(2010), and extensive stratigraphical and sedimentological infor-
mation of the El Soplao amber-bearing outcrop is provided by
Najarro et al. (2009).
3. Material and methods
The ceratopogonid inclusions were found in amber collected
when the outcrop was discovered in 2007, and in three consecutive
excavations. Amber pieces containing the samples wereincluded in
synthetic Epoxy resin (EPO-TEK 301) and then polished (extensive
protocol is given in Corral et al., 1999).
The number ES-07-xx was assigned to those ceratopogonid
specimens provisionally housed at the “Museo Geominero”(IGME)
in Madrid (Spain), whilst those that will be housed at the future
El Soplao museum in Cantabria (Spain) were given the number
CES-xxx.
Fossils were examined with a Leica MS5 binocular microscope
and a Zeiss Axiophot optical microscope. General photographs
were taken using a Leica DFC420 camera. Microphotographs were
obtained with the aid of a Sony DXC-S500 digital camera attached
to the microscope. Drawings were made using a camera lucida.
Measurements were obtained using the Leica IM1000 programme.
Some images were reconstructed using Combine Z5 computer
software.
Terminology and criteria for measuring follow those of Borkent
(1995, 2000a).
4. Taxonomy and phylogeny of the Ceratopogonidae
The major lineages conforming the order Diptera, although still
controversial in some phylogenetic aspects, are nowadays
consistently defined (the most recent review of the high-level
phylogeny of Diptera is given in Yeates et al., 2007). The Cerato-
pogonidae form part of the lower Diptera, formerly known as the
suborder “Nematocera”, now that its paraphyletism has been
accepted (state of the art phylogenetic interpretations of lower
Diptera are given in Bertone et al., 2008). The nematocerous flies,
and thus the whole Diptera order, would have separated from
their mecopteroid ancestor around the Permo-Triassic boundary,
although the first true dipteran record is not reported until the
Lower/Middle Triassic of France (Krzemi
nski and Krzemi
nska,
2003). Moreover, biting midges are classified within the infra-
order (or suborder sensu Amorin and Yeates, 2006) Culicomorpha
Hennig, 1973, monophyletically grouping most of the blood-
feeding nematocerous dipterans (Grimaldi and Engel, 2005). The
oldest known culicomorphan, Aenne triassica Krzemi
nski and
Jarzembowski, 1999 comes from the Late Triassic of England
(Krzemi
nski and Jarzembowski, 1999). This Triassic genus belongs
to the Chironomidae (non-biting midges), which could be
considered the sister group of Ceratopogonidae (Beckenbach and
Borkent, 2003).
The patterns of diversification obtained with morphological
and molecular analyses of extant taxa have revealed a strong
correlation with the fossil record of Ceratopogonidae, the
monophyly of which is widely accepted (Borkent, 2000a;
Beckenbach and Borkent, 2003; Borkent and Craig, 2004). The
family is today divided into five subfamilies: Ceratopogoninae
Newman, 1834; Leptoconopinae Noé, 1907; Dasyheleinae Lenz,
1934; Forcipomyiinae Lenz, 1934, and Lebanoculicoidinae Bor-
kent, 2000 (Borkent, 2011). A first, basal group of lineages was
already established in the Old World during the Early Cretaceous,
but may possibly have started in the Late Jurassic (Fig. 1). It is
composed of genera mainly classified in the subfamily Lep-
toconopinae and the monogeneric subfamily Lebanoculicoidinae,
which is the only subfamily without extant representatives. The
genus Lebanoculicoides Szadziewski, 1996, hitherto exclusively
reported from the late BarremianeAptian Lebanese amber
(Szadziewski, 1996), is considered the sister group of all the
remaining Ceratopogonidae in that it is the only biting midge to
retain fully developed R
1
,R
3
and R
4þ5
wing veins. This important
feature justified the creation of its own subfamily (Borkent,
2000a). In turn, the subfamily Leptoconopinae includes six
genera that would have shared a common ancestor (Borkent and
Craig, 2004). Four of these are extinct, Minyohelea Borkent,
1995,Archiaustroconops Szadziewski, 1996,Fossileptoconops
Szadziewski , 1996,andJordanoconops Szadziewski, 2000;thetwo
remaining genera, Leptoconops Skuse, 1889, and Austroconops
Wirth and Lee, 1958, currently surviving as relicts (Szadziewski,
2008; more information in section 6), are today the only extant
representatives of the initial ancient diversity of the family.
However, there are some basal, Early Cretaceous genera with
uncertain phylogenetic position, e.g. Protoculicoides Boesel, 1937
and Atriculicoides Remm, 1976. Neither genus shows autapomor-
phies, and their diagnosis is mainly based on characters that are
highly subject to homoplasy (e.g. mid-dorsal separation/union
between the eyes and presence/absence of macrotrichia on the
wing membrane), which have therefore been discarded for
phylogenetic tests (Borkent, 1995, 2000a; Szadziewski, 1996;
Borkent and Craig, 2004). Thus, these cladistic inferences,
although consistent as a whole , have necessarily been based on t he
use of symplesiomorphies to locate Protoculicoides,andprimarily
on poorly conspicuous characters such as synapomorphies for
placing Atriculicoides, having been reported from a scarce fossil
diversity of the genus. However, Protoculicoides remains unclassi-
fied at subfamily level, and uncertainty exists as to whether
it belongs to the monophyletic Leptoconopinae or the
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761 751
[Forcipomyiinae þDasyheleinae þCeratopogoninae] clade
(Borkent and Craig, 2004). Atriculicoides has provisionally been
classified within the subfamily Forcipomyiinae since Borkent
(1995), and is the sister group to a clade grouping Forcipomyiinae
and Dasyheleinae (which would be tribes according to
Szadziewski, 1996). On the other hand, more derived lineages of
Ceratopogoni dae have successfully diversified world wide since the
Late Cretaceous. They mostly correspond to taxa classified within
the subfamily Ceratopogoninae, but also within the subfamilies
Dasyheleinae and Forcipomyiinae. An updated Ceratopogonidae
species catalogue is given in Borkent (2011).
5. Systematic palaeontology
Order: Diptera Linnaeus, 1758
Infraorder: Culicomorpha Hennig, 1973 (see also Amorin and
Yeates, 2006)
Family: Ceratopogonidae Newman, 1834
Subfamily: Lebanoculicoidinae Borkent, 2000
Genus Lebanoculicoides Szadziewski, 1996
Type species.Lebanoculicoides mesozoicus Szadziewski, 1996.
Range and locality. Early Cretaceous (late BarremianeAptian)
Lebanese amber (Jezzine).
Lebanoculicoides excantabris sp. nov.
2009 Lebanoculicoides sp. Najarro et al., p. 382, Fig. 13.
Material. Single female (holotype), ES-07-9. The specimen was
found together with two wasps (Hymenoptera), a mymar-
ommatid (ES-07-8) and a platygastrid (ES-07-10), as syninclu-
sions. Head and scutum are depressed and the thorax is
compressed. Unfortunate position of the legs prevents accurate
observation of the genitalia.
Fig. 1. Distribution among Early to Late Cretaceous ambers of the described Ceratopogonidae belonging to the most ancient lineages of the family, already present during
the Early Cretaceous. The palaeogeographic map (redrawn from Blakey, 2008), corresponds to middle Albian (w105 Ma). The framed area (Southwestern Europe) is
amplified at the bottom right of the figure. Early and Late Cretaceous ambers are indicated by dots and triangles respectively. The number of genera found for each amber
deposit is indicated in brackets. Data extracted essentially from Borkent (2011) and complemented by information in Borkent (1995), Szadziewski (1996, 2000, 2004),
Borkent (2000a, b), Szadziewski and Arillo (2003), Arillo et al. (2008), Poinar (2008) and this paper. Although ceratopogonids have been well reported from French
amber (Szadziewski and Schlüter, 1992; Perrichot, 2004; Perrichot et al., 2007), their detailed study has not yet begun, and thus they are under-represented in the figure.
Note also how the coincidence of biting midges has contributed to the correlation of Campanian Canadian ambers (McKellar et al., 2008). Early Cretaceous ambers.
(1) Austria (Hauterivian): Minyohelea casca. (2) Lebanon (late BarremianeAptian): Archiaustroconops ceratoformis,A.cretaceous,A.bocaparvus,A.hamus,andA.szadziewskii.
Archiculicoides acraorum ,A.schleei,andA.unus.Austroconops fossilis,A.gladius,A.gondwanicus,andA. megaspinus.Fossileptoconops lebanicus.Lebanoculicoides mesozoicus.
Leptoconops (Palaeoconops )amplificatus and L.(P.) antiquus.Minyohelea bacula,M. falcata,M.lebanica,M.minuta,M.schleei,andM.wirthi.Protoculicoides succineus and
P.punctus. (3) Jordan (Albian): Archiaustroconops sp. Jordanoconops weitschati.Spanish ambers. (4) El Soplao, Cantabria (early Albian): Archiaustroconops borkenti sp. nov.
Atriculicoides szadziewskii sp. nov. Austroconops sp. Lebanoculic oides excant abris sp. nov. Protoculicoides skalskii. (5) Peñacerrada I, Burgos (early Albian): Archiaustroconops
alavensis.Austroconops sp. Leptoconops zherikhini.Protoculicoides skalskii. (6) San Just, Teruel (middle Albian): Leptoconops zherikhini.Protoculicoides skalskii. (7) Myanmar
(late AlbianCenomanian): Archiaustroconops gracilis and A. kotejai.Atriculicoides swinhoei.Austroconops asiaticus.Leptoconops burmiticus,L.myanmar icus,L. nosopheris,
L.rossi,andL.subrossicus.Protoculicoides bur miticus.Late Cretaceous ambers. (8) Northwestern France (Cenomanian): Atriculicoides cenomanensis and A. incompletus.
Austroconops borkenti.Leptoconops sp. (9) Nizhnyaya Agapa, Taimyr (Cenomanian): Leptoconops boreus. (10) New Jersey (Turonian): Atriculicoides globosus and A.incom-
pletus.Leptoconops copiosus and L. curvachelus. (11) Yantardakh, Taimyr (ConiacianeSantonian): Atriculic oides macrophthalmus,A.da syheleis,A. sibiricus,andA.taimyricus.
Austroconops sibiricus.Leptoconops sibiricus and L. boreus.(12)Hungary(ConiacianeSantonian): Leptoconops clava.Canadian amber (Campanian). (13) Grassy Lake, Alberta:
Atriculicoides globosus.Minyohelea pumilis.Leptoconops primaevus.Protoculicoides depressus. (14) Cedar Lake, Manitoba: Atriculicoides globosus.Leptoconops primaevus.
Protoculicoides depressus.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761752
Fig. 2. Camera lucida drawings of Lebanoculicoides excantabris sp. nov., holotype ES-07-9. A, lateral habitus. B, head in lateral view. C, left wing. Scale bars ¼0.1 mm.
Fig. 3. Lebanoculicoides excantabris sp. nov., holotype ES-07-9. A, lateral habitus. B, lateral view of head. C, left wing. D, right foreleg tibio-tarsal articulation. E, left hindleg
tibio-tarsal articulation. F, left hindleg tarsal claws. Scale bars. AeC¼0.1 mm; DeF¼0.025 mm.
Derivation of name. Latin ex Cantabris, meaning “from the land of
Cantabria”.
Diagnosis.Male. Unknown. Female. Short flagellomeres (not
elongated); palpus 4-segmented; R
4þ5
terminating in a basal
position before reaching the wing apex.
Description. Female (Figs. 2A and 3A). Total length ¼0.98 mm.
Head. Eye separation poorly visible. Antenna with 13 separate
flagellomeres ovoidal to subspherical towards the apex, terminal
flagellomere elongated (Figs. 2B and 3B). Mouthparts elongated;
mouthpart length/length of fifth tarsomere of foreleg ¼3.6. Palpus
4-segmented; segment 3 slightly swollen; segments 3/4 þ5¼1. 6
(Figs. 2B and 3B). Thorax. Scutum setose. Scutellum rounded, with
a few long thick setae along its margin. Wing. Length ¼0.92 mm,
costal ratio ¼0.76. Without macrotrichia; microtrichia present in
the entire wing membrane. Costa (C) not extending beyond apex of
radial veins 4 þ5(R
4þ5
). Two radial cells well-developed; first
radial cell 1.5 times longer than the second. R
4þ5
well-developed,
reaching wing margin well before the wing apex (Figs. 2C and
3C). Transverse vein r-m oblique, not subperpendicular to C. Media
(M) petiolate. Vein M
2
basally absent. Legs. Slender. Foreleg tibiae
with a pectinated tibial spur (Fig. 3D); midleg tibiae with apical
spur; hindleg tibiae with single transverse row of apical spines
(¼tibial comb, Fig. 3E). Hindleg 1st tarsomere with scattered spines
(Fig. 3E). Thick, paired spines in apex of tarsomeres 1e4. Tarsal ratio
of foreleg ¼1.9, hindleg ¼1.2, foreleg/hindleg ¼1.6. Claws short,
simple, similar in all legs (Fig. 3F). Genitalia. Cerci elongated, about
twice as long as wide.
Remarks.AfterSzadziewski (1996) described the genus based
on one female, Borkent (2000a) reported the male and simplified
the diagnosis to one unique character: the presence of a fully
developed R
1
,R
3
,andR
4þ5
.WhereasinLebanoculicoides meso-
zoicus R
4þ5
is concave and almost reaches the wing tip, in Leb-
anoculicoides excantabris sp. nov. it is convex and clearly ends
some distance from the wing tip. In addition to the diagnostic
characters, a quite low hindleg tarsal ratio and the cerci length
also differentiate these two species. It is noteworthy that the
elongated cerci of L. excantabris should recall those of Leptoconops
Skuse, 1889.
Subfamily indet.
Genus Protoculicoides Boesel, 1937
Type species.Protoculicoides depressus Boesel, 1937.
Range and locality. Early to Late Cretaceous (late Barre-
mianeCampanian). Protoculicoides succineus Szadziewski, 1996,
and Protoculicoides punctus Borkent, 2000 from late Barre-
mianeAptian Lebanese amber; Protoculicoides skalskii Szadziewski
and Arillo, 1998 from early Albian Peñacerrada I amber (Spain);
Protoculicoides burmiticus Szadziewski and Poinar, 2005 from late
AlbianeCenomanian Burmese (Myanmar) amber; Protoculicoides
depressus Boesel, 1937 from Campanian Canadian amber.
Protoculicoides skalskii Szadziewski and Arillo, 1998.
Material. Single female, ES-07-18.
Description. Female (Fig. 4). Total length ¼1.35 mm. Head.
Compound eyes separated mid-dorsally. Single vertex seta not
visible. Antenna with 13 separate flagellomeres; flagellomeres
9e13 more elongated than those preceding them, gradually
increasing in length towards the apex. Mouthparts very elongated,
about twice as long as the eye height; mouthpart length/length of
fifth tarsomere of foreleg ¼6.4. Palpus 5-segmented; segment 3
very elongated, cylindrical; segments 4 and 5 subequal in length.
Thorax. Scutum and scutellum with elongated setae. Scutellum with
rounded apex. Wing. Length ¼1.15 mm, costal ratio ¼0.84. Single
row of macrotrichia at dorsal margins of C and radius (R). Wing
Fig. 4. Protoculicoides skalskii Szadziewski and Arillo, 1998, ES-07-18. A, camera lucida drawing. B, photograph. Scale bar ¼0.1 mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761754
membrane without macrotrichia, microtrichia distinct. C ending at
tip of vein R
3
. Two well-developed radial cells present, rounded;
second radial cell longer than the first. Transverse vein r-m oblique.
M petiolate. Vein M
2
basally absent. Legs. Slender. Pair of thick setae
not visible on fore- and midleg trochanter. Foreleg tibiae with two
slender tibial spurs; midleg tibial spur not present; hindleg tibiae
with single transverse row of apical spines (¼tibial comb). Mid-
and hindleg first and second tarsomeres with scattered, stout
spines (better defined in first tarsomere). Thick, paired spines at
apex of tarsomeres 1e4 conspicuous only in mid- and hindlegs.
Tarsal ratio of foreleg ¼1.9, hindleg ¼2.1, foreleg/hindleg ¼0.9.
Claws short, simple, similar in all legs, somewhat basally widened.
Genitalia. Barely visible.
Remarks. The specimen ES-07-18 is a member of the genus
Protoculicoides on the basis of the presence of two well-developed
radial cells, the absence of a well-defined R
4þ5
, a wing membrane
devoid of macrotrichia, a costal ratio >0.7, and a foreleg/hindleg
tarsal ratio <1.3 (Borkent, 2000a).
It is assigned to P. skalskii by the following characters: (a) the
very elongated mouthparts, (b) the cylindrical morphology of the
palpal segment 3, and (c) a C not extending beyond apexof R
3
. This
species was described from Peñacerrada I but was also reported
from San Just (Arillo et al., 2008), both localities in Spain (Alonso
et al., 2000; Peñalver et al., 2007). Although genitalia are not
clearly visible in this specimen owing to amber fractures, it is
interpreted as a female because of antennal features that have been
observed repeatedly within the fossil diversity of the genus (and
also other ancient Cretaceous genera such as Atriculicoides): the last
five flagellomeres are elongated (instead of the last three or four in
males) and the well-developed plume of setae typical of males is
not present. The ES-07-18 specimen has a relatively higher costal
ratio than the holotype, which could be interpreted as intraspecific
variability (0.84 vs. 0.73).
Subfamily: Leptoconopinae Noé, 1907 (¼Austroconopinae
Borkent and Craig, 2004)
Genus Archiaustroconops Szadziewski, 1996
Type species.Archiaustroconops ceratoformis Szadziewski, 1996.
Range and locality. Early Cretaceous (late BarremianeCenoma-
nian). Archiaustroconops ceratoformis Szadziewski,1996,A. cretaceous
(Szadziewski, 1996), A. bocaparvus Borkent, 2000, A. hamus Borkent,
2000 and Atriculicoides szadziewskii Borkent, 2000 from late
BarremianeAptian Lebanese amber; Archiaustroconops alavensis
Szadziewski and Arillo, 1998 from early Albian Peñacerrada I amber
(Spain); Archiaustroconops gracilis Szadziewski and Poinar, 2005 and
A. kotejai Szadziewski and Poinar, 2005 from late AlbianeCenoma-
nian Burmese (Myanmar) amber.
Archiaustroconops borkenti sp. nov.
2009 Archiaustroconops sp. Najarro et al., p. 381, Fig. 12E.
Material. Single female (holotype), ES-07-17. The specimenis well-
preserved, but the thoraxis ventrally compressed and theabdomen is
strongly deformed and partially burst on the left side. A globular
artefact (probably a gas bubble) connects with the abdomen.
Derivation of name. The species name is dedicated to Dr Art
Borkent, in recognition of his prominent contribution to the
knowledge of biting midges.
Diagnosis. Male. Unknown. Female. Eyes separated mid-dorsally;
elongated flagellomeres; palpus 5-segmented with segment 3
greatly swollen and laterally flattened; C extending beyond apex of
R
3
along almost the total wing length, elongated first radial cell.
Fig. 5. Camera lucida drawing of the ventral habitus of Archiaustroconops borkenti sp. nov., holotype ES-07-17. Scale bar ¼0.1 mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761 755
Description. Female (Figs. 5 and 6A). Total length ¼1.18 mm.
Head. Compound eyes separated mid-dorsally by a distance of 3e4
ommatidia, single vertex seta present (Fig. 6B). Antenna with 13
separated flagellomeres gradually increasing in length towards the
apex (Fig. 6C); basal flagellomeres with sensilla trichoidea.
Mouthparts moderately elongated; mouthpart length/length of
fifth tarsomere of foreleg ¼2.8. Palpus 5-segmented; palpal
segment 3 greatly swollen and laterally flattened, ovoidal in lateral
view; palpal segment 4 small, much shorter than palpal segment 5
(Fig. 6D). Thorax. Scutum with elongated setae; scutellum not
visible in dorsal view. Wing. Length ¼0.91 mm, costal ratio ¼0.97.
Stylised wing shape (Fig. 6E). Wing membrane without macro-
trichia, microtrichia distinct. C distinctly extending beyond R
3
. Two
well-developed radial cells, very elongated; second radial cell
slightly longer than the first one. Transverse vein r-m oblique, not
subperpendicular to C. M petiolate. Vein M
2
basally absent. Legs.
Slender. Foreleg with two thick tibial spurs (Fig. 6F); midleg
possibly with slender apical spur. Thick, paired spines at apex of
tarsomeres 1e4 conspicuous only in mid- and hindlegs. Tarsal ratio
of foreleg ¼2.6, hindleg ¼1.3, foreleg/hindleg ¼2. Claws short,
simple, similar in all legs (Fig. 6G). Genitalia. Cerci very short
(Fig. 6H).
Remarks. The specimen ES-07-17 can be placed in the genus
Archiaustroconops in that it shows: (a) two well-developed radial
cells, (b) an oblique tranverse vein r-m, and (c) a foreleg/hindleg
tarsal ratio >1.4 (Borkent, 2000a).
Archiaustroconops borkenti sp. nov. shares most of its features
with A. alavensis and A. szadziewskii. Unlike the other
Archiaustroconops species, all three have a 5-segmented palpus
where the palpal segment 4 is much shorter than segment 5, and
equal and simple tarsal claws (not basally toothed). A. borkenti
displays a wing morphology similar to A. szadziewskii (high costal
ratio, first radial cell long, and Cu-A bifurcating distally; Borkent,
2000a), but its eyes are separated mid-dorsally and its palpal
segment 3 is greatly swollen and laterally flattened, as occurs in
A. alavensis (Szadziewski and Arillo, 1998; Szadziewski and Poinar,
2005) (eyes broadly abutting dorsally and palpal segment 3 slightly
swollen in A. szadziewskii).
A recent examination of the ceratopogonid collection from the
“Museo de Ciencias Naturales de Álava”revealed one specimen
from Peñacerrada I amber with antennal and wing characters
which coincided with those of A. borkenti.
Genus Austroconops Wirth and Lee, 1958
Type species.Austroconops mcmillani Wirth and Lee, 1958.
Range and locality. Early Cretaceous (late BarremianeAptian) to
Recent. Austroconops fossilis Szadziewski, 1996,A. gondwanicus
Szadziewski, 1996,A. gladius Borkent, 2000 and A. megaspinus
Borkent, 2000 from late BarremianeAptian Lebanese amber;
Austroconops asiaticus Szadziewski, 2004 from late AlbianeCenoma-
nian Burmese (Myanmar) amber; A. borkenti Szadziewski and
Schlüter, 1992 from Cenomanian Bezonnais amber (NW France);
Austroconops sibiricus Szadziewski, 1996 from ConiacianeSantonian
Yantardakh amber (Taimyr, northern Russia); A. mcmillani Wirth and
Lee, 1958 and A. annettae Borkent, 2004 from Western Australia.
Fig. 6. Archiaustroconops borkenti sp. nov., holotype ES-07-17. A, ventral habitus. B, frontal (left) and lateral (right) views of dorsal part of head. Arrow points to the separation
between composite eyes which bears the single vertex seta. C, flagellomeres 2e13 of the left antenna. Arrows show sensilla trichoidea in the basad flagellomeres. D, right palpus in
lateral view. Silhouette of the palpal segment 3 has been partially highlighted. Arrow shows the separation between palpal segments 4 and 5. E, left wing. F, right foreleg tibio-tarsal
articulation. G, tarsal claws of left hindleg. H, cerci. Scale bars. A, E ¼0.1 mm; B, C, H ¼0.05 mm; D, F, G ¼0.025 mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761756
Austroconops sp.
Material. Two females, CES-008 and CES-017.1. The latter spec-
imen is in a reconstructed stalactite-shaped amber piece, together
with a platygastrid (Hymenoptera) as syninclusion (CES-017.2). It is
well-preserved, though the right midleg is apparently missing.
A gas bubble at the end of the abdomen, and a thread of a spider’s
web adhering to the thorax and the left midleg can be seen. CES-
008 has been affected by a tangential fracture of the amber piece,
having lost a part of the cephalic region. As a result, neither
antennae are preserved, but one palpus and the distal half of the
mouthparts can be seen in detail.
Description. Female (Fig. 7). Total length ¼0.99e1.20 mm. Head.
Compound eyes probably separated mid-dorsally by a short
distance. Single vertex seta not evident. Antenna with 13 separate
flagellomeres; flagellomeres 9e13 slightly more elongated than
those preceding them; last flagellomere subconical in shape.
Mouthparts moderately elongated; mouthpart length/length of
fifth tarsomere of foreleg ¼2.6e2.8. Palpus 4-segmented; segment
3 slender, slightly swollen, ca. 3 times as long as its greatest width;
segment 4 þ5 ca. 2.5 times as long as its greatest width; segments
3/4 þ5¼1.6 e1.8 (Fig. 7C). Thorax. Scutum setose. Scutellum with
rounded apex. Wing. Length ¼0.73e0.80 mm, costal ratio ¼0.99.
Single row of macrotrichia at dorsal margins of R and C. Wing
membrane without macrotrichia, microtrichia distinct. Subcosta
(Sc) absent. C extending beyond apex of vein R
3
. Two well-
developed radial cells present, elongated, subequal in length.
Transverse vein r-m long, parallel to R
1
. M petiolate. Veins M
1
and
M
2
basally absent, completely absent in specimen CES-008. Legs.
Slender. Pair of thick setae not visible on fore- and midleg
trochanter. Foreleg tibiae with two slender, short tibial spurs;
midleg tibial spur not present; hindleg tibiae with single transverse
row of apical spines (¼tibial comb). Hindleg first tarsomere with
scattered setae. Thick, paired spines at apex of tarsomeres 1e4
poorly conspicuous. Tarsal ratio of foreleg ¼2e2.6, hindleg ¼1.3,
foreleg/hindleg ¼1.5e2. Claws simple, slender, similar in all legs.
Genitalia. Cerci short, rounded.
Remarks. Both specimens can be placed in the genus Austro-
conops in accordance with two well-developed radial cells and the
very diagnostic vein r-m parallel to R
1
(Borkent, 2000a). A
combination of important characters supports the exclusion of the
two El Soplao specimens from most of the species within the
genus: (a) a foreleg tibial spur not especially enlarged, (b) a C
almost reaching the total wing length (costal ratio almost 1) and
(c) two radial cells subequal in length. In fact, the two specimens
strongly resemble A. borkenti Szadziewski and Schlüter, 1992,
mainly in the following characters: (a) palpus 4-segmented, with
a palpal segment 3 slender in shape (ca. 3 times as long as its
greatest width) and 1.6e1.8 longer than the segment 4 þ5
(Szadziewski and Schlüter, 1992, Fig. 21), (b) flagellomeres 9e13
only slightly more elongated than those preceding them (visible
only in CES-017.1), and (c) simple claws, not basally toothed
(Szadziewski and Schlüter, 1992). A. borkenti was described as
a single female from Cenomanian Bezonnais amber (north-west
France), which is partially preserved, lacking the distal wing half
and some leg segments (Szadziewski and Schlüter, 1992). Its
preserved proximal wing portion seems to show an elongated first
radial cell (Szadziewski and Schlüter, 1992, Fig. 24), which within
the known diversity of the genus would mean that both radial
cells are subequal in length or, at least, the second is not much
more elongated than the first. Two differences have been noted
between the two Austroconops sp. specimens from El Soplao and
the A. borkenti holotype: the lack of Sc and a palpal segment 4 þ5
slightly less elongated.
We have recently re-examined the ceratopogonid collection
from Peñacerrada I amber in the “Museo de Ciencias Naturales de
Álava”.Austroconops proved to be very abundant, including two
well-preserved male specimens from more than 30 inclusions
belonging to this genus. The female specimens from Álava appear to
show very constant antennal, palpal and wing characters, similar to
those of A. borkenti. We prefer not to relate the specimens from El
Soplao to A. borkenti until this abundant material has been studied
further.
On the other hand, although the antennae of CES-008 are not
preserved, the other diagnostic characters such as the palpal shape
and the simple claws are sufficient to relate it to CES-017.1. In
addition, there are some minor differences between the two El
Soplao specimens that should be noted. Besides a certain difference
in size and foreleg tarsal ratios, whereas CES-017.1 lacks the basal
part of M
1
and M
2
, CES-008 entirely lacks these two veins. More-
over, CES-017.1 has a palpus somewhat more gracile than CES-008.
Lastly, only CES-017.1 presents an r-m vein where the most
Fig. 7. Austroconopssp., CES-017.1.A, camera lucida drawing. B, photograph.C. detail of the mouthparts, showingthe left palpal segments 3and 4 þ5 in the foreground. Scale bar ¼0.1mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761 757
proximal stretch is markedly transversal, and then drastically
changes its angle, rapidly reaching a continuous, nearly parallel
trajectory to R
1
. This exact r-m morphology has previously been
drawn in A. gladius and A.fossilis females (Borkent, 2000a, Fig. 12h,
13c), and seems to be absent in the A. borkenti holotype. It is
significant to note that the vein r-m shows a certain graduation of
parallelness within the genus. This fact could be interpreted as an
intermediate state between a transverse r-m, present in supposedly
more ancestral forms, and the parallel one characteristic of
Austroconops.
Subfamily: Forcipomyiinae Lenz, 1934
Genus Atriculicoides Remm, 1976
Type species.Atriculicoides macrophthalmus Remm, 1976.
Range and locality. EarlyeLate Cretaceous (late AlbianeCampa-
nian). Atriculicoides swinhoei (Cockerell, 1919) from late
AlbianeCenomanian Burmese (Myanmar) amber; Atriculicoides
cenomanensis Szadziewski and Schlüter, 1992, and A. incompletus
Szadziewski and Schlüter, 1992 from Cenomanian French
amber; Atriculicoides macrophthalmus Remm, 1976,A. dasyheleis
Szadziewski, 1996,A. sibiricus Szadziewski, 1996, and A. taimyricus
Szadziewski, 1996 from ConiacianSantonian Yantardakh amber
(Taimyr, Russia); Atriculicoides globosus (Boesel, 1937) from
Campanian Canadian amber.
Atriculicoides szadziewskii sp. nov.
Fig. 8. Camera lucida drawings of Atriculicoides szadziewskii sp. nov., holotype ES-07-12. A, lateral habitus. B, wing reconstruction based on the visible preserved parts of both wings.
The total wing width has been estimated. Scale bars ¼0.1 mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761758
Material. Single female, ES-07-12, in a preparation containing
fragments of a leg and wings of a cockroach (ES-07-13) as synin-
clusions. The specimen was found together with three more syn-
inclusions, a beetle indet. (ES-07-14), and two platygastrid wasps
(ES-07-15, ES-07-16). The specimen is well-preserved, although
both wings are folded and unpreserved around the union between
C and R
3
(left wing shows this contact, right wing does not). The
distal part of the right antenna is poorly conspicuous due to its
proximity to the body. The right hindleg tarsus is not preserved. A
spider’s web thread adheres to the C of the right wing andthe right
hindleg tibia.
Derivation of name. The species is named in honour of Dr
Ryszard Szadziewski, in recognition of his valuable dedication to
the study of biting midges.
Diagnosis.Male. Unknown. Female. Mouthparts elongated; 5-
segmented palpus with segment 3 swollen at mid length and
segment 4 slightly shorter than segment 5, both elongately ovate;
wing with macrotrichia only sparsely covering the basal radial cell
plus the distal half of the wing membrane; cubital vein bifurcating
below the distal part of the basal radial cell.
Description. Female (Figs. 8A and 9A). Total length ¼1.31 mm.
Head. Compound eyes broadly abutting mid-dorsally. Single vertex
seta not visible. Antenna with 13 separated flagellomeres; flag-
ellomeres 9e13 more elongated than those preceding them; last
flagellomere especially elongated and widened in the shape of
a paintbrush-like club (could be an artefact; see remarks), with
a single seta at the pointed apex (Fig. 9B). Clypeus convex.
Mouthparts elongated; mouthpart length/length of fifth tarsomere
of foreleg ¼5.5. Palpus 5-segmented; segment 3 stout, swollen at
mid length, possibly with capitate sensilla in an apparently small
sensory pit at apex (Fig. 9C); segment 4 slightly shorter than
segment 5, both elongately ovate and exceeding mouthpart length;
segments 3/4 ¼3.2. Thorax. Scutum very raised and setose, with
some long thick setae in the posterior area. Scutellum rounded,
with a few long setae at the margin. Wing. Total length and costal
ratio unknown. C and R with macrotrichia. M with single row of
macrotrichia. Macrotrichia only covering the distal part of the
preserved wing membrane plus the basal radial cell (Figs. 8B and
9D); microtrichia distinct. C ending at tip of vein R
3
. Two well-
developed radial cells present, long, similar in length (second
radial cell 1.2 times longer than the first one). Transverse vein r-m
oblique, not subperpendicular to C. M petiolate, bifurcating below
the base of the second radial cell. Vein M
2
basally absent. Presence
of a supplementary evanescent vein that begins at r-m base and
runs parallel along M root until it bifurcates (conspicuous only in
the left wing) (Fig. 8B). Cubital bifurcation below the distal part of
the basal radial cell. Legs. Moderately slender. Pair of thick setae not
visible on fore- and midleg trochanter. Tibial comb not visible. First
and second tarsomeres of each leg with scattered, stout spines.
Thick, paired spines at apex of tarsomeres 1e4. Tarsal ratio of
Fig. 9. Atriculicoides szadziewskii sp. nov., holotype ES-07-12. A, lateral habitus. B, flagellum of the left antenna. C, left palpus. Arrow points to possible capitate sensilla in the distal
part of the palpal segment 3. Limits of the palpal segment 5 have been partially drawn. D, preserved portion of the right wing. E, tarsal claws of right midleg. F, cerci. Scale bars.
A¼0.1 mm; B, D, F ¼0.05 mm; C, E ¼0.025 mm.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761 759
foreleg ¼1.7, hindleg ¼1.8, foreleg/hindleg ¼0.94. Claws short,
simple, similar in all legs, angularly widened at their base (Fig. 9E).
Genitalia. Cerci short, rounded, highly setose (Fig. 9F).
Remarks. The specimen ES-07-12 is placed within the genus
Atriculicoides by (a) eyes broadly abutting mid-dorsally, (b) two
well-developed radial cells, (c) an oblique tranverse vein r-m, and
(d) the presence of macrotrichia on the wing membrane. An
especially enlarged terminal flagellomere is also common for this
genus. Macrotrichia covering only the distal half of the wing have
been reported for males of A.cenomanensis and A.macrophthalmus
(Remm, 1976; Szadziewski and Schlüter, 1992), although the pres-
ence of macrotrichia in the basal radial cell, as in A.szadziewskii sp.
nov., has hitherto been noted only in those wing membranes fully
covered by macrotrichia (Remm, 1976; Borkent, 1995; Szadziewski,
1996, 2004).
Within Atriculicoides, the last flagellomere tends to be enlarged
in relation to those preceding it in length and thickness. In fact,
when Remm (1976, p. 345) established the etymology of this genus
he noted the coincidence of this character, described as a “small
club at the apex of the antenna”, with Culicoides Latreille, 1809.
Subsequently, this character has been observed to a different
degree in most of the described Atriculicoides species. Although
both final flagellomeres of A. szadziewskii sp. nov. are undoubtely
enlarged, that of the left antenna shows a distinctive paintbrush-
like morphology (Fig. 9B). Nevertheless, this specific morphology
could reflect an artefact of preservation since the last flagellomere
of the right antenna, though distinctly swollen, appears more
cylindrical, but is poorly visible because it is very close to the body.
As this character is not clearly resolved, it has been excluded from
the diagnosis.
6. Palaeoecological remarks
The genera Leptoconops Skuse, 1889, and Austroconops Wirth
and Lee, 1958, are the only living representatives of the ancient
Early Cretaceous lineages of the Ceratopogonidae. Whereas
nowadays ca. 140 Leptoconops species show a pantropical distri-
bution and the only two known recent species of Austroconops are
restricted to Western Australia, during the Late Cretaceous both
genera were widely distributed in the Northern Hemisphere and
Eurasia, respectively (see Szadziewski, 2008,Fig. 6, 7B). Larval
stages of the two extant genera today burrow mostly within moist
soils, often on or near the sea-shore, in beach sands or coastal
marsh muds (Downes and Wirth, 1981; Borkent, 2001; Borkent and
Craig, 2004). According to this particular larval habitat, it has been
reported that the presence of Leptoconops sp. in the Cretaceous
amber record reflects the proximity of amber producing trees tothe
sea-shore (Szadziewski, 2004), in keeping with the delta-estuarine
scenario generally displayed by the main Cretaceous amber
deposits (Alonso et al., 2000; Cruickshank and Ko, 2003; Perrichot
et al., 2007). The genera Leptoconops and Austroconops have always
been found together, sometimes as syninclusions, and also together
with the genera Archiaustroconops and Protoculicoides, in the main
Early Cretaceous ambers: late BarremianAptian of Lebanon
(Borkent, 2000a, b, 2001), early Albian of Spain (Szadziewski and
Arillo, 1998, 2003), and late AlbianCenomanian of Myanmar
(Szadziewski, 2004; Szadziewski and Poinar, 2005). Therefore,
although a future find of the genus Leptoconops in El Soplao is
highly probable, the mere presence of the genus Austroconops
enables us to interpret that resin source forests would have
developed close to marine coasts in El Soplao as well. This is also
suggested by the sedimentological, taphonomical, and other
palaeontological data (Najarro et al., 2009, 2010).
On the other hand, females of both genera are today diurnal
blood feeders of mammals, birds, and reptiles (Downes and Wirth,
1981; Borkent, 2001; Borkent and Craig, 2004). Blood provides the
high protein supply necessary to promote egg development in
females, which in derived non-haematophagous biting midges can
be achieved by other protein-rich meals such as insect haemo-
lymph or pollen (Grimaldi and Engel, 2005). However, whereas the
plesiotypic condition of haematophagy within Culicomorpha is still
not clear (Lukashevich and Mostovski, 2003), cladistic analyses
indicate that it would have been well established in the basal
lineages of Ceratopogonidae (Borkent, 1995; Szadziewski, 1996).
Furthermore, despite the fact that finely toothed mandibles and
lacinia with retrorse teeth were not observed in the new fossil
ceratopogonid taxa ea typical vertebrate blood-feeding indicator
reported for some species of Atriculicoides and Protoculicoides
(Borkent, 1995, 2000a, b)enone of them bears enlarged or toothed
tarsal claws, an absence strongly correlated with vertebrate blood-
feeding in Ceratopogonidae (Szadziewski and Schlüter, 1992). It
should be noted that mouthpart length is not a deciding factor for
ceratopogonid haematophagous condition since extant blood-
feeding Leptoconopinae representatives often show short or very
short mouthparts (ibid.). Thus, haematophagy can be assumed not
only for the two specimens assigned to Austroconops sp. but also for
the rest of the El Soplao biting midges.
Moreover, it is highly plausible that haematophagous biting
midges would have fed on dinosaur blood during the Cretaceous
Period. Dinosaurs would have been preferentially bitten on
exposed, heavily vascularised areas, such as the eyelids, as indi-
cated by Borkent (1995). This author reviewed several studies
carried out on extant Culicoides species, demonstrating the indirect
correlation between number of CO
2
host-tracking sensilla in palpal
segment 3 and host size, a general tendency also existing in other
culicomorphan families. Thus, he concluded that host size of
Cretaceous Culicoides would have coincided with that of dinosaurs.
Furthermore, as supported in some fossil evidence in amber, it
has been hypothesised that the role played by haematophagous
biting midges today, acting as vectors of vertebrate pathogens such
viruses, nematodes, and protozoa, was also present in the first
stages of their evolutionary history during the Early Cretaceous
(Poinar and Poinar, 2005; Poinar, 2008), although the majority of
these reports should be viewed with caution.
7. Conclusions
Previous reports have demonstrated that the genera Archiaus-
troconops,Atriculicoides,Austroconops and Protoculicoides had
an expanded palaeogeographical distribution throughout the
Northern Hemisphere during, at least, the Early Cretaceous. Our
new record of the genus Lebanoculicoides also reveals a relatively
wide palaeogeographic distribution of what is thought to be the
basalmost genus of the Ceratopogonidae. The find of A. szadziewskii
sp. nov. represents the oldest record for this genus to date. The co-
occurrence of P. skalskii in Peñacerrada I, San Just, and now in El
Soplao, provides relevant palaeoentomological evidence in support
of a similar palaeoecology for these three Spanish amber localities.
The presence of biting midges in El Soplao amber, although not
surprising, has great palaeoenvironmental significance, since it
suggests the proximity of resin producing forests to marine coastal
areas during the earlyemiddle Albian. In addition, the five taxa
discussed here would have fed on vertebrate blood, possibly acting
as vectors and therefore spreading pathogens. Indeed, dinosaurs
may have been their hosts, as has been indicated previously for
other amber records.
The preliminary study of El Soplao amber has already provided
a strikingly diverse record of Ceratopogonidae dipterans, suggest-
ing that, as is customary for amber deposits, this group will be one
of the most prevalent.
R. Pérez-de la Fuente et al. / Cretaceous Research 32 (2011) 750e761760
Acknowledgements
We express our gratitude tothe “Consejería de Cultura, Turismo
y Deporte”, of the Government of Cantabria, SIEC S.A., and El Soplao
Cave in Cantabria for their interest in the study of El Soplao amber
and loaning us some studied samples. We are also grateful to
J. Alonso, director of the “Museo de Ciencias Naturales de Álava”in
Vitoria-Gasteiz, for allowing us to review the amber ceratopogonid
collection, and to D. Batten for his corrections on the advanced
version of the manuscript. We are indebted to R. López-del Valle for
the careful preparation of samples. This paper will be included in
the first author’s PhD thesis, funded by an APIF grant from the
University of Barcelona. This study is a contribution to the projects
CGL2008-00550/BTE: “The Cretaceous amber of Spain: a multidis-
ciplinary study”of the Spanish Ministry of Science and Innovation,
and 491-CANOA 35015 “Investigación científica y técnica de la
Cueva de El Soplao y su entorno geológico”of the IGME.
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