Fig wasps in Dominican amber (Hymenoptera, Agaonidae)

2006·0.92 MB·English

by  Peñalver, Enrique

A tamerican museum
Novitates
PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3541, 16 pp., 9 figures December 7, 2006
Fig Wasps in Dominican Amber
(Hymenoptera: Agaonidae)
ENRIQUE PENALVER,1’2 MICHAEL S. ENGEL,1’3 AND DAVID A. GRIMALDI1
ABSTRACT
The fauna of fig wasps (Hymenoptera: Chalcidoidea: Agaonidae: Agaoninae) preserved in Early
Miocene (Burdigalian) amber from the Dominican Republic is reported. Three species are
described, representing both of the exclusively neotropical genera Tetrapus Mayr and Pegoscapus
Cameron: Tetrapus delclosi Penalver and Engel, new species, T. apopnus Penalver and Engel, new
species, and Pegoscapus peritus Penalver and Engel, new species. All are described and figured
based on females that are exquisitely preserved. The species are distinguished from each other as
well as from modern relatives.
INTRODUCTION cious) and varied syndromes in wasp biology
and anatomy depending on the host biology
Among the diverse array of specialized (e.g., Ramirez, 1974; Wiebes, 1979; Weiblen,
plant-insect interactions, the fig wasps 2002; Cook and Rasplus, 2003; Kjellberg et
(Agaonidae s.str.: see Rasplus et al., 1998) al., 2005). Recent studies on the phylogeny of
and the figs (Moraceae: Ficus spp.) they visit the fig wasps indicate that the fig-fig wasp
are one of the most renowned. The obligate association arose a single time (Machado et
pollination system between these wasps and al., 1996, 2001; Herre et al., 1996; Rasplus et
their fig hosts is remarkably complicated, al., 1998) and may be as old as 75-100 Ma as
involving differing breeding systems across derived from molecular estimates (Machado et
the diversity of Ficus species (functionally al., 2001; Ronsted et al., 2005). The oldest
monoecious versus functionally gynodioe- fossils recognizable as Ficus fruits, however,
1 Division of Invertebrate Zoology, American Museum of Natural History ([email protected]; [email protected]).
2 Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de Valencia, Apt. 2085, E-46071, Valencia, Spain
([email protected]).
3 Division of Invertebrate Zoology, American Museum of Natural History; Division of Entomology (Paleoentomology),
Natural History Museum, and Department of Ecology & Evolutionary Biology, 1501 Crestline Drive-Suite 140, University of
Kansas, Lawrence, Kansas 66049-2811 ([email protected]).
Copyright © American Museum of Natural History 2006 ISSN 0003-0082
2 AMERICAN MUSEUM NOVITATES NO. 3541
are from the Eocene of England (Collinson, flash unit (www.microptics.com). The speci¬
1989), from 20-45 Ma younger than the mens were drawn using a drawing tube
estimates for the origin of the fig—fig wasp attached to a Zeiss microscope. Specimens
mutualism, suggesting rather a Cenozoic di¬ are housed in the Amber Fossil Collection,
versification of the fig-fig wasp association. Division of Invertebrate Zoology, American
Unlike all other specialized, obligate pollina¬ Museum of Natural History, New York
tion systems where there is no fossil record (AMNH). Unless otherwise indicated, mea¬
(e.g., yucca-yucca moths), fig wasps have been surements, where provided, are of the holo-
discovered as fossils. Indeed, numerous inclu¬ types.
sions of fig wasps have been discovered in
Dominican amber and, as documented else¬ SYSTEMATIC PALEONTOLOGY
where (Penalver et al., in prep.), some are even
preserved in association with pollen from their Genus Tetrapus Mayr
fig hosts. Herein we provide a taxonomic
Of the three agaonid species in Dominican
account of this extinct fauna so as to make the
amber, two belong to the strictly Neotropical
names available for a forthcoming study of the
and basal genus Tetrapus. Today there are
paleobiology and paleoecology of fossil
presently recognized seven species of Tetrapus,
Agaoninae. Format for the descriptions gen¬
two of them unnamed (Wiebes, 1995), al¬
erally follows that employed by Wiebes (1995)
though this number shall most assuredly rise
for New World Agaoninae. interestingly, in
as the genus is more intensively studied and
the New World only two genera of agaonines
more thorough collections developed. Among
are native, Tetrapus Mayr and Pegoscapus
the modern species, Tetrapus costaricanus
Cameron. The systematics of neither has been
Grandi (recorded from Mexico, Costa Rica,
intensively studied, although a useful pre¬
and Panama) is the only species known in
liminary monographic treatment was pub¬
which the female’s third antennal article bears
lished by Wiebes (1995). Not surprisingly,
an external prominence, or projection.
the fossil agaonine fauna in Dominican amber
Interestingly, this distinctive trait is shared
includes representatives of both of these
with the two species described herein from
neotropical genera, establishing their native
Dominican amber, which is probably a notable
presence since the Miocene.
apomorphy uniting these species. Intensive
cladistic work on New World agaonines is
MATERIAL AND METHODS desperately needed as concepts of relation¬
ships within each genus are rudimentary.
Dominican amber, which is excavated Within the West Indies today there is
mainly from mines in the mountains north documented only T. antillarum Ashmead,
and northeast of Santiago, is a fossil resin a species of dubious status and known only
originating from an extinct species of from its type material collected on St. Vincent
Hymenaea tree (Leguminosae: Caesalpi- Island (Wiebes, 1995). The fact that the fossil
nioidea). This amber has been dated as mid- Tetrapus fauna shares putatively derived
Miocene (Grimaldi, 1995; Iturralde-Vinent features with T. costaricanus from the Recent
and MacPhee, 1996). All of the agaonid of Mesoamerica suggests that the origin of the
specimens known in Dominican amber are paleofauna was via dispersal from or direct
females, an expected outcome, since males are geological connection with Mesoamerica, fol¬
restricted to the cavity of the fig and most of lowed by later extinction of the insular fauna
them are apterous. and a second, later introduction of T. antillar¬
The material studied herein was acquired um from either South or Central America.
through purchase, but authenticity was con¬ Only a new monographic treatment of
firmed in all instances. The pieces were Tetrapus and cladistic analysis of relationships
prepared according to the protocol of Nascim- within the genus (along with a critical test of
bene and Silverstein (2000). Photomicro¬ the monophyly of Tetrapus and Pegoscapus)
graphy employed an Infinity K-2 long-dis¬ can further refine potential biogeographic
tance microscope and a MicrOptics fiber-optic patterns for this group of fig wasps.
2006 PENALYER ET AL.: DOMINICAN AMBER FIG WASPS 3
The only fossil record of Tetrapus, indeed species of this genus in amber, T. apopnus
the sole description of a fossil fig wasp prior to (see below), by the more numerous setae of the
present study, is a compression of dubious distalmost antennal article (fig. 3a), the barrel¬
identity from the Eocene-Oligocene shales of shaped flagellomeres (fig. 3a; cylindrical in T.
Florissant, Colorado: T. mayri Brues (1910). apopnus, cf. fig. 3b), the smaller number of
The species was largely placed in Tetrapus outer (i.e., lateral) denticles on the mandibular
based on habitus, and the original description appendage (6-8 in T. delclosi', compared with
lacks critical details, so the holotype of T. at least 11, perhaps 13, in T. apopnus [see
mayri should be critically reevaluated. The below]), smaller number of ventral, or lamel¬
only other records lack descriptions or formal lar, serrate ridges (11 in T. delclosi, compared
identifications; these are the figures of with 16 in T. apopnus), elongate protibial setae
Dominican amber agaonines by Poinar in distal position (versus medial position in T.
(1993), Wu (1997), Poinar and Poinar (1999), apopnus', cf. fig. 4a, 4c), and differences in the
and Grimaldi and Engel (2005) (the first of structure of the apical spines of the protibia
these figuring a Pegoscapus, apparently the (cf. figs. 4b and 4c, see also Description).
new species Pegoscapus peritus, described Tetrapus delclosi also differs from all other
herein, below; the latter three figuring the Tetrapus species (living and fossil) in the
new species T. delclosi, described herein, complete development of the parastigma. In
below). T. apopnus and modern species the submar¬
The host figs of Tetrapus species belong to ginal vein does not reach the anterior margin
Ficus (Pharmacosycea) Section Pharmaco- of the forewing, usually not turning anterior
sycea. As such, the presence of these fossils to form even an incomplete parastigma. In T.
in Dominican amber indicates the occurrence delclosi the submarginal vein reaches the wing
of figs of this section in the paleoflora of the margin but terminates there, thereby creating
Miocene of Hispaniola. a complete parastigma, but not forming
a marginal vein.
Tetrapus delclosi Penalver and Engel, Description: Female. Total body length
new species 1.90 mm, without ovipositor; forewing length
figures 1, 2a, 3a, 4a, b 1.62 mm, width 0.68 mm (as measured in
paratype AMNH DR-11-3). Integument faint¬
Agaonidae sp., Wu, 1997: 207 [figured two speci¬
ly imbricate and dark brown. Head slightly
mens].
longer than wide (length 0.62 mm, width
Agaonidae sp., Poinar and Poinar, 1999: 30, 33
[figured, with nematodes]. 0.30 mm), breadth much greater than com¬
Agaonidae sp., Grimaldi and Engel, 2005: 423 pound eye length; gena narrower than com¬
[figured, with nematodes and pollen grains]. pound eye width (figs. 1, 2a). Scape enlarged,
Diagnosis: As previously noted, among rectangular in form, with small external,
living species T. delclosi has a similar, albeit medial tubercle; third antennal article with
slightly larger, process on the third antennal prominent external projection bearing a stiff
article as that observed in T. costaricanus. apical seta; fifth to eleventh antennal articles
Tetrapus delclosi differs from T. costaricanus bear one whorl of sensilla lineara, distalmost
by the bidentate mandibular apex (among antennal article with dense setae (fig. 3a);
living species only T. ecuadoranus Grandi has flagellomeres barrel-shaped (fig. 3a). Man¬
a bidentate mandibular apex), the smaller dible with two acutely pointed, apical teeth;
number of outer denticles on the mandibular mandibular appendage with six to eight outer
appendage (6-8 in T. delclosi, compared with (i.e., lateral) denticles (referred to as “outer
15 in T. costaricanus), the first protarsomere row of teeth” by Wiebes, 1995), with 11
has 9-13 ventral spines (T. costaricanus and T. ventral serrate ridges (referred to as “inner
americanus Mayr have approximately 30 row of teeth” by Wiebes, 1995); two palplike
ventral spines, T. mexicanus Grandi has 40, appendages bearing a single, robust, apical
whereas T. ecuadoranus has 25), and the seta anteriorly on labiomaxillary complex
slightly more elongate head. Tetrapus delclosi (fig. 2a). Profemur distinctly swollen relative
can be distinguished from the only other to other femora; protibia with two elongate,
4 AMERICAN MUSEUM NOVITATES NO. 3541
valves
ovipositor
2006 PENALYER ET AL.: DOMINICAN AMBER FIG WASPS 5
distal setae (fig. 4a, b); protibial apical spines hesitation to formally designate this individual
depicted in figure 4a-b; outer surface with as a paratype. However, the mandibular
three spines, two at apex largest and well appendage is visible laterally and could be
defined, third in sub apical position and satisfactorily reconstructed, suggesting that
somewhat smaller but with well-defined apex; the specimen is T. delclosi.
internally with a single, prominent, apical Etymology: The specific epithet is a pat¬
spine and a series of weak, apical knobs along ronym honoring Dr. Xavier Delclos, special¬
margin; ventral surface of probasitarsus with ist on fossil insects at the University of
9-13 conical spines (fig. 4a); mesosoma slight¬ Barcelona.
ly longer than metasoma. Venation of fore¬
wing reduced, with submarginal vein and
Tetrapus apopnus Penalver and Engel,
parastigma; marginal, postmarginal, and ptero-
new species
stigmal veins absent; various spectral lines
figures 2b, 3b, 4c, 5, 6
in remigium of wing; hind wing with three
hamuli. Spiracular peritremata of eighth Diagnosis: Like T. delclosi, T. apopnus
urotergite prominent and slightly enlarged; has a slightly larger process on the third
protruding terminal, prominent pygostyles antennal article as that in T. costaricanus.
(cerci; 0.054 mm in length), with two apical, Tetrapus apopnus can be distinguished from T.
elongate setae; external portion of ovipositor costaricanus by the more elongate head, which
0.86 mm in length (visible portion 1.06 mm in is 2.11 times longer than wide (ca. 1.33 times
length); ovipositor valves slightly longer than longer than wide in T. costaricanus), and the
metasoma (0.92 mm in length), without ap¬ smaller number of outer denticles and ventral
parent pilosity (fig. la). Male. Unknown. serrate ridges on the mandibular appendage.
Holotype: Female, AMNH DR-14-576, The species can be distinguished from T.
Early Miocene (Burdigalian) amber from the delclosi, the only other species of the genus
Dominican Republic. The specimen is associ¬ in amber, by the features discussed in the
ated with fig pollen grains and parasitic diagnosis for that species (see above).
nematodes, and all occur in a small, clear Description: Female. Total body length
piece of amber measuring 15 mm in length X 2.06 mm, without ovipositor; forewing length
12 mm in width X 5 mm in depth (thickness). 1.59 mm, width 0.60 mm; hind wing length
The holotype is in the Amber Fossil 0.83 mm, greatest width 0.18 mm. Integument
Collection, Division of Invertebrate Zoology, faintly imbricate and dark brown. Head
American Museum of Natural History. longer than wide (length 0.59 mm, width
Paratypes: Females (three specimens), 0.28 mm), breadth much greater than com¬
AMNH DR-11-3 (specimen with fig pollen pound eye length; gena narrower than com¬
grains), AMNH DR-14-92 (specimen with fig pound eye width (figs. 2b, 5b). Scape enlarged,
pollen grains and nematodes, and associated in rectangular in form, with small external,
the same resin flow with two thrips, two medial tubercle; third antennal article with
chalcidoid wasps, two nematocerans, an imma¬ prominent external projection bearing a stiff
ture insect, and vegetal remains), and AMNH apical seta; fifth to eleventh antennal articles
DR-14-710 (specimen with nematodes). bear one whorl of sensilla lineara, distalmost
Additional Material: Female, AMNH antennal article with sparse setae (figs. 3b, 5b);
DR-14-13 59. The specimen is poorly pre¬ flagellomeres cylindrical (fig. 3b). Mandible
served and the diagnostic characters of the apparently with a single, acutely pointed,
new species are not easily visible, hence our apical tooth (difficult to discern in holotype);
Fig. 1. Photomicrographs of Tetrapus delclosi Penalver and Engel, new species, a. Holotype in lateral
view (AMNH DR-14-576); note the trail of fig pollen grains at right (scale bar = 1 mm), b. Paratype
(AMNH DR-14-92) in dorsolateral view (scale bar = 1 mm) and detail of the female external genitalia (scale
bar = 0.1 mm).
6 AMERICAN MUSEUM NOVITATES NO. 3541
0.1 mm
mandibular
apical teeth
palp-likc
appendage
denticles
serrate
ridges
Ficus pollen
Fig. 2. Camera lucida drawings of the heads in ventral view of the two described species of Tetrapus, for
comparison, a. Head of Tetrapus delclosi Penalver and Engel, new species (holotype: AMNH DR-14-576);
note the mass of fig pollen grains under the mesosoma. b. Head of T. apopnus Penalver and Engel, new
species (holotype: AMNH DR-14-282). To the same scale.
2006 PENALYER ET AL.: DOMINICAN AMBER FIG WASPS 7
apical
process
third
antennal
article
b
0.1 mm
Fig. 3. Camera lucida drawings of the antennae of the two described species of Tetrapus, for
comparison, a. Antenna of Tetrapus delclosi Penalver and Engel, new species (holotype: AMNH DR-14-
576). b. Antenna of T. apopnus Penalver and Engel, new species (holotype: AMNH DR-14-282). To the
same scale.
AMERICAN MUSEUM NOVITATES NO. 3541
Fig. 4. Camera lucida drawings of the protibiae of the two described species of Tetrapus, for comparison,
a. External view of the left foreleg of Tetrapus delclosi Penalver and Engel, new species (paratype: AMNH
DR-11-3). b. Left pro tibia in external (upper) and internal views (below) of T. delclosi, new species (holotype:
AMNH DR-14-576), c. Right protibia of T. apopnus Penalver and Engel, new species (holotype: AMNH
DR-14-282), in internal view. Compare the internal protibial apex with spines of the two species (arrows).
All to the same scale.
mandibular appendage with at least 11 easily to as “inner row of teeth” by Wiebes, 1995)
visible outer (i.e., lateral) denticles, although (fig. 2b). Profemur distinctly swollen relative
there appear to be two more for a total of 13 to other femora; protibia with two elongate,
(referred to as “outer row of teeth” by Wiebes, medial setae (fig. 4c); protibial apical spines
1995), with 16 ventral serrate ridges (referred depicted in figure 4c, internally with a single,
2006 PENALYER ET AL.: DOMINICAN AMBER FIG WASPS 9
Fig. 5. Photomicrographs of the holotype of Tetrapus apopnus Penalver and Engel, new species (AMNH
DR-14-282). a. Ventral habitus (scale bar = 1 mm), b. Ventral view of the head (scale bar = 0.1 mm).
prominent, apical spine and two well-pro¬ Dominican Republic. The specimen is in
duced spines (slightly shorter than apicalmost a small piece of amber, with numerous
spine) that are largely fused along their length bubbles and microlayered flows, measuring
but with differentiated, blunt apices; ventral 13 mm in length X 9 mm in width X 7 mm in
surface of probasitarsus with conical spines depth (thickness). Syninclusions in the piece
(number not determinable); mesosoma slightly include the dehisced wings of a termite
longer than metasoma. Venation of forewing (Isoptera) and an entire nematoceran. The
reduced, with submarginal vein and incom¬ holotype, and only known specimen of the
plete parastigma that does not reach wing species, is in the Amber Fossil Collection,
anterior margin (fig. 6); marginal, postmargi¬ Division of Invertebrate Zoology, American
nal, and pterostigmal veins absent; various Museum of Natural History.
spectral lines in remigium of wing (fig. 6); hind Etymology: The specific epithet is the
wing with three hamuli. Protruding terminal Greek word apopnus, meaning “dead”.
pygostyles (cerci) absent; external portion of
ovipositor 1.07 mm in length, with two very
Genus P egos cap us Cameron
small apical spines; ovipositor valves slightly
longer than metasoma (1.00 mm length), Pegoscapus is the more diverse of the two
without apparent pilosity (fig. 6). Male. native genera of Neotropical fig wasps.
Unknown. Presently there are 47 recognized species of
Holotype: Female, AMNH DR-14-282, Pegoscapus, ranging throughout tropical
Early Miocene (Burdigalian) amber from the America from Florida and Mexico to
10 AMERICAN MUSEUM NOVITATES NO. 3541
Fig. 6. Camera lucida drawing of the ventral habitus of the holotype of Tetrapus apopnus Penalver and
Engel, new species (AMNH DR-14-282).
Argentina (Wiebes, 1995; Schiffler et al., some of these subgroups are now rightly
2002). Numerous subgenera were recognized recognized as separate genera (e.g., Jiang et
within Pegoscapus by Grandi (1919, 1963: as al., 2006). Once a cladistic analysis for
Blastophaga Gravenhorst in an older and Pegoscapus (in the modern, restricted sense)
much broader sense) but we agree with has been completed then the utility of a sub¬
Wiebes (1995) that a formal subgeneric generic arrangement can be re-evaluated,
classification is presently unwarranted and particularly if subgeneric clades could be