ore

JHR 4 I: 1-29 (20 I 4) JOURNAL CF Apeerreviewed open-access journal
Siete. (4G) Hymenoptera

http://jhr.pensoft.net The insertional Society of ymenoptersts, RESEARCH

Revision of the neotropical genus Sendaphne Nixon
(Hymenoptera, Braconidae, Microgastrinae)

Jose L. Fernandez-Triana!?, James B. Whitfield’, M. Alex Smith‘,
Winnie Hallwachs®, Daniel H. Janzen?

| Canadian National Collection of Insects, 960 Carling Ave., Ottawa, ON KIA 0C6 Canada 2. Biodiversity
Institute of Ontario, University of Guelph, Guelph, ON NIG 2W1 Canada 3 Department of Entomology,
University of Illinois, Urbana, IL 61801 USA 4 Department of Integrative Biology, University of Guelph,
Guelph, ON NIG 2W1 Canada 5 Department of Biology, University of Pennsylvania, Philadelphia, PA
19104-6018 USA

Corresponding author: Jose L. Fernandez- Triana (jftriana@uoguelph.ca)

Academic editor: G. Broad| Received 15 September 2014 | Accepted 9 December 2014 | Published 22 December 2014
http://zoobank. ore/46F 876 D2-9F BD-4837-AB2C-A5FE64D8E468

Citation: Ferndndez-Triana JL, Whitfield JB, Smith MA, Hallwachs W, Janzen DH (2014) Revision of the neotropical
genus Sendaphne Nixon (Hymenoptera, Braconidae, Microgastrinae) . Journal of Hymenoptera Research 41: 1-29. doi:
10.3897/JHR.41.8586

Abstract

The Neotropical genus of parasitoid wasps Sendaphne (Hymenoptera, Braconidae, Microgastrinae) is re-
vised and the following six new species are described, all authored by Fernandez-Triana and Whitfield:
anitae, bennetti, broadi, dianariaspennae, penteadodiasae, and rogerblancoi. The greatest species richness is
found in northern South America, but the genus extends north to 23° N in Mexico. Most species have
been collected in rainforest below altitudes of 900 m, with only a few species found in cloud forests up to

1900 m. Nothing is known of the host caterpillars for these parasitoid wasps.

Keywords
Sendaphne, Microgastrinae, Neotropics, Area de Conservacién Guanacaste, taxonomic revision, parasitoid

wasps, DNA barcoding

Copyright Jose L Fernandez-Triana et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

2 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Introduction

The genus Sendaphne was described by Nixon (1965) to accommodate two Neo-
tropical species with a number of distinctive features: a very long and bilobate glossa,
slender body, extensive yellow coloration, mostly smooth mesosoma and metasoma,
enlarged hypopygium, and very long and curved ovipositor. Penteado-Dias (1995)
described two additional species, and Scatolini and Penteado-Dias (1999) added an-
other one. Four of the five species described so far are from Brazil, with the exception
being Sendaphne sulmo Nixon (1965), recorded from southeastern Mexico. No host is
known for Sendaphne, although the related genus Promicrogaster Brues & Richardson,
1913, has been reared from hosts living in bracket fungi (Mason 1981), among other
concealed hosts.

In spite of the rather unique morphological traits, the validity of Sendaphne as a
distinct genus has been questioned even by the same author who described it (Nixon
1965: 204), and it might eventually be determined to be a synonym of the more abun-
dant and diverse Promicrogaster. However, Mason (1981) considered the differences as
sufficient to maintain them as two genera. That decision has been followed by all sub-
sequent authors and, without a comprehensive phylogenetic study of Microgastrinae,
we agree that is better to keep it that way at present. The morphological and molecular
analysis of Whitfield et al. (2002), although not conclusive, also found those two gen-
era to be closely related. An anticipated revision of Promicrogaster may help to elucidate
the limits of these two genera in the future.

As part of comprehensive studies on the fauna of Microgastrinae from Area de
Conservacién Guanacaste (ACG), northwestern Costa Rica (e.g., Fernandez-Triana et
al. 2014 and references cited there) we found a new species from that area. The Cana-
dian National Collection of Insects (CNC) in Ottawa, Canada and the NSF-funded
“Insect Survey of a Hyperdiverse Country: Colombia” projects led by M. J. Sharkey,
B. V. Brown and the Humboldt Institute (Colombia) also contained additional unde-
scribed species from Central and South America. All these new species are described
below, altogether with a key to all known, previously described species of Sendaphne.

Methods

Among Microgastrinae, Sendaphne is one of the most rarely collected genera, and is
poorly represented in collections. This study is based on 73 specimens from four sources:
38 Neotropical specimens deposited in the CNC, 18 specimens from Colombia
(Humboldt Institute), 10 specimens from the ACG inventory, four specimens from
Unité d’Entomologie fonctionnelle et évolutive, Gembloux Agro-Bio Tech, Université
de Li¢ge (FUSAGx) and three specimens from the Natural History Museum, London,
England (BMNH).

All species previously described were deposited in the Universidade Federal de
Sao Carlos, S40 Carlos, S40 Paulo, Brazil (DCBU), Universidade Federal do Parana,

Revision of the neotropical genus Sendaphne Nixon... )

Curitiba, Parana, Brazil (UFPR), or in the BMNH. We did not examine the holotypes
of those species; however, their original descriptions and illustrations are sufficiently
detailed to allow us to describe the new species with confidence.

Morphological terms and measurements of structures are mostly as used by Mason
(1981), Huber and Sharkey (1993), Whitfield (1997), Karlsson and Ronquist (2012),
and Fernandez-Triana et al. (2014). Because the ovipositor in Sendaphne is strongly
curved, its length was difficult to measure accurately; the ovipositor length measure-
ments provided for each new species are only intended as an approximation. In any
case, the ovipositor and its sheaths are some of the longest observed in any Microgas-
trinae genera; they are usually two times longer than the metatibia length.

Descriptions of the new species are based on the study of all available female speci-
mens, so as to reflect intraspecific variation, but always include data from the holotype.
As an exception, two new species only known from males are described below because
they were sufficiently distinct to be distinguished from all others; the males of those
two species may be identified by the key, but males of most other species may not be
readily identified unless associated with females via rearing or molecular data.

The descriptions include 17 characters that are commonly used in describing Mi-
crogastrinae (e.g., body measurements such as length of body and fore wing, ovipositor
sheath; and also color of particular body areas). Those descriptions are complemented
with extensive color photos of every species. Geographic distribution is also provided
in the key as supplementary information to aid the morphological identification of
species, though we recognize that with time the current known geographic distribution
may eventually become obsolete.

Photos were taken with a Keyence VHX-1000 Digital Microscope, using a lens
with a range of 13—-130x. Multiple images through the focal plane were taken of a
structure and these were combined to produce a single in-focus image, using the soft-
ware associated with the Keyence System.

Together with morphological studies, we also analyzed DNA barcodes (the
5’ region of the cytochrome c oxidase I (CO1) gene, Hebert et al. 2003) whenever
available. DNA barcodes for all ACG inventory Sendaphne specimens were obtained
using DNA extracts prepared from single legs using a glass fibre protocol (Ivanova
et al. 2006). Briefly, total genomic DNA was re-suspended in 30 ul of dH2O, and
a 658-bp region near the 5’ terminus of the CO1 gene was amplified using standard
primers (LepF1l—LepR1) following established protocols (Smith et al. 2006, 2007,
2008). If the initial 658 bp amplification was unsuccessful, smaller sequences were
generated using internal primers. If each amplification worked a composite sequence
was generated, however in cases where only one read amplified, this shorter sequence
was used. All information for the sequences associated with each individual specimen
can be retrieved from the Barcode of Life Data System (BOLD) (Ratnasingham
and Hebert 2007) using the following public DOI: http://dx.doi.org/10.5883/DS-
SENDAPH. A Neighbor-Joining tree based on Kimura 2-parameter distances of
all described species of Sendaphne with DNA barcodes available in BOLD was also
generated (Suppl. material 2).

4 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Results

Six new species of Sendaphne are described below, increasing the total known species
from five to 11. We are aware of potential additional new species in the CNC collec-
tion, from Costa Rica (but not ACG), Ecuador, and Brazil. However, they are not
described here because each is only represented by a single specimen and they are not
sufficiently distinct to warrant description without further specimens and evidence.
Sendaphne is a Neotropical genus. To date it is most abundant and diverse in
South America (eight species), while Central America has three species. It extends from
23° N in central Mexico (Durango) to 27° S in Paraguay (Pirapo) and southern Brazil
(Santa Catarina). Most of the species have been collected in rain forests, at altitudes be-
tween 100 m and 900 m. However, a few species have been found only in cloud forests
between 1,450 m and 1,900 m. The specimens collected at higher altitudes have darker
coloration (especially on mesosoma and metasoma) than those found in the lowlands.
An interesting result of our morphological study was the relation between body
and fore wing lengths. Body proportions in Microgastrinae have not been explored in
detail, but in most genera and species with available data the fore wing length tends
to be slightly longer than the body length (usually by 0.1—-0.2 mm). In the specimens
of Sendaphne described here, the body length was longer than the fore wing length
(usually by 0.2-0.4 mm). The main reason is the long and slender body form (rather
than exceptionally short wings), and an unusually enlarged and extended hypopygium.

Observations of COI barcodes for Sendaphne

Of 46 specimens sampled (Suppl. material 1), we recovered sequences for only 24
specimens. Only three sequences were over 600 base pairs, while the rest were mostly
minibarcodes of 102-390 base pairs each. However, six out of the 11 known spe-
cies now have some molecular data associated (Suppl. material 2). Many of the initial
amplifications from ACG were characterised by unintended amplification of the en-
dosymbiont bacteria Wolbachia that were amplified in the first round LepF1/LepR1.
These sequences were not mistaken for the wasp DNA (Smith et al. 2012) and are
retained on BOLD in the trace files. The standard strategy of amplifying two smaller
and overlapping regions secondarily was then followed (as the first round was consid-
ered a ‘failure’). In this case the 5’ amplification (LepF1/C_ANTMRID) worked and
the 3’ amplification (RonMWASPdeg_tl - LepR1) failed. Thus many of the ACG
Sendaphne are ~260—280bp in length. Finally, regarding the CNC specimens, these
were, on average, 35 years old. In those cases, greater success with smaller amplifica-
tions compared to larger amplifications is to be expected (Hajibabaei et al 2006). In
2010 and 2011 when these specimens were submitted to the Biodiversity Institute of
Ontario (Guelph) for DNA barcoding, they only had the primers generating mini-
barcode (smaller amplicons) used for PCR. The longer amplicon generating primer
pairs were not attempted on these specimens.

Revision of the neotropical genus Sendaphne Nixon... 5

Genus Sendaphne

Sendaphne Nixon, 1965: 203.

Diagnosis. Glossa elongate and bilobate (Figs 2, 9, 34, 48, 58, 70). Lateral face of
scutellum with polished area (=lunules) occupying most of the lateral face (Figs 5, 12,
19, 28, 44, 49, 56). Propodeum usually smooth and without carina (exceptionally
having sparse punctures and few rugae on the nucha) (Figs 7, 13, 19, 28, 33, 44, 49,
60, 74). Metacoxa very long, about the same length as metafemur length and metatibia
length (Figs 8, 13, 15, 29, 50, 54, 61, 68, 74). Mediotergite 1 strongly narrowing
towards posterior margin (Figs 4, 14, 19, 50, 51). Mediotergite 2 subtriangular, much
longer medially than its width at its anterior margin (and usually also longer medially
than its width at posterior margin). Ovipositor very long for a microgastrine wasp
(two times longer than metatibia length) and strongly curved (Figs 1, 20, 35, 53,
54, 57, 64, 68); apex of ovipositor usually not sinuate (exceptionally with very slight
sinuation). Fore wing with very wide first discal cell, and with small areolet (Figs 3,
17, 17, 24, 39, 55, 62, 69) (areolet sometimes not well-defined because veins 3RSa
and r-m are spectral, as in Figs 10, 31, 47). Body color often mostly yellow to orange
(with a few exceptions from species collected at higher altitudes, which have head,
mesosoma and parts of metasoma dark brown to black). Body length longer than the
fore wing length, usually by 0.2—0.4 mm. Within Microgastrinae, Sendaphne can only
be confused with Promicrogaster, but the later has a more transverse mediotergite 2,
apex of ovipositor clearly sinuate, and propodeum usually with more sculpture and
carination present.

Key to Sendaphne species

[This key is intended for female specimens, although two species are only known from
males, and in those cases the key accommodates them. Generally, males tend to have
darker coloration than the females, especially on the metasoma].

1 Head and mesosoma entirely dark brown to black (Figs 23, 24, 27, 28, 37—
44, 68-75), metasoma entirely dark brown (Figs 69, 74, 75) or at most with
mediotergites 1—2 orange-yellow (as in Figs 24, 25, 28, 39, 44) [all specimens
collected above 1,460 m, in cloud forests] ............cceeeeeeccccccecesssseeeccceeeeeaeeeees 2

— Color variable but much lighter than previous couplet, #fhead entirely dark
brown to black, then mesosoma entirely or mostly yellow, orange or reddish-
yellow, and metasoma at most with brown bands on posterior margins of
mediotergites 3+ [all specimens collected below 900 m, in rainforests] ....... 4

2(1) Tegula, metacoxa, and mediotergites 1-2 dark brown to black (Figs 69, 73-
75); body very slender, metasoma longer than combined length of head and
mesoseriartPigs.68): || Gosta ical arise hcads 5s sassncatees tauivagenconnehseoeaban oma ssaidts se
rao Sendaphne rogerblancoi Fernandez-Triana & Whitfield, sp. n.

3(2)

9(7)

Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Tegula, metacoxa and mediotergites 1-2 yellow to reddish-yellow (Figs
23-28, 37-40, 42-44); body less slender, metasoma shorter than combined
length of head and mesosoma (Figs 23, 37) [Ecuador, Mexico] ...........eee 3
Mediotergite 1 length 6.0 x its width at posterior margin, mediotergite 2
length 1.5 x its width at posterior margin (Figs 24, 25, 28); first discal cell
210 eas wide-as hich (Pie. 24s) euad or |.08v..c0d0Re rs oeaecoene eee suettace Dente
Fee aus nates ae Sendaphne broadi Fernandez-Triana & Whitfield, sp. n.
Mediotergite 1 length 4.0 x its width at posterior margin, mediotergite 2
length 1.0 x its width at posterior margin (Figs 39, 42, 44); first discal cell
123 x as wide-asshigh (Pig 39). [MrexiGO] sss ses Ssssinesdssnncagaacovkchanasdebsdentvatsoucuaur.
LPR era Sendaphne bennetti Fernandez-Triana & Whitfield, sp. n.
Plcad pe Ow tO! LeUCs MVC] LOW.» <diin.maceaterautdanearcuenniosreie Dantea amen teeaeenars 5
Fieadidarkibrownstotblack: "somos ee ee SO ee eee 7
Mesosoma with dark brown areas on anteromesoscutum and mesopleuron
(Figs 54, 56, 58); dark brown coloration on posterior margin of mediotergite
3 and most of mediotergites 4—6 (Figs 54, 55, 57, 59) [Brazil, Paraguay] .....
pag eohet guithat ne Hbesn Sendaphne paranaensis Scatolini & Penteado-Dias, 1999
Mesosoma uniformly orange-yellow to reddish-yellow; metasoma either entirely
yellow or with brown bands on posterior margin of mediotergites 4-6 ........... 6
Metasoma with brown bands on posterior margin of mediotergites 4—6 (Figs
50-53) [Brazil, French Guiana, Peru)....... Sendaphne olearus Nixon, 1965
Metasoma entirely yellow (Figs 31, 32, 35, 36) [Brazil, Ecuador, French Gui-
ATRL A ban eee tidal cad the Mentone tae Sendaphne jatai Penteado-Dias, 1995
Female metasoma either with extensive dark brown coloration on tergites 3+
or with some narrow brown bands on posterior margin of mediotergites 5—7
CPigstO3 GA) spe ach ote, 20 Ben akcas nS wale Be eras duper Maude Reese Aa 8
Female metasoma entirely yellow (Figs 3, 4, 7, 18, 19, 22) veces 9
Metasoma with dark brown bands on posterior margin of mediotergites 3-6
and mediotergite 7 entirely dark brown to black; fore wing vein 1Cu-a much
shorter than vein 1Cu-b; T1 10.0 x as long as width at posterior margin; T1
Urcaslong as ID interacoxa ll xas longi as metaleMmU tin ccicnncvdscnnawmronnrnens
TF Ra AAD AA A ahaha eat Ae Sendaphne brasilianus Penteado-Dias, 1995
Metasoma with some narrow brown bands on posterior margin of medi-
otergites 5—7 (Figs 63, 64); fore wing veins 1Cu-a and 1Cu-b subequal; T1
6.0 x as long as width at posterior margin; T1 1.4 x as long as T2; metacoxa
f) OS iO axtAs- LOM Opa SEC LAL CIINUN shun fiwuh leoulashinclmbane es caunbougslt rit phees auiauan hide!
Peace Sendaphne penteadodiasae Fernandez-Triana & Whitfield, sp. n.
Fore wing r and 2RS not clearly distinct from each other (Fig. 3); medioter-
gite 2 length 1.0 x its width at posterior margin (Figs 3, 4, 7); face centrally
orange (Fig. 2); ovipositor 1.8—1.9 x as long as metatibia [Ecuador].............
Psu cesboisuersesoneseness Sendaphne anitae Fernandez-Triana & Whitfield, sp. n.
Fore wing with veins r and 2RS clearly distinct from each other, and meeting
at a sharp angle (not clearly visible in Fig. 17); mediotergite 2 length 1.8—2.0

Revision of the neotropical genus Sendaphne Nixon... 7

x its width at posterior margin (Figs 18, 19); face entirely dark brown to
black (Fig. 16); ovipositor 2.0—2.2 x as long as metatibia [Brazil, Colombia,
Cold WORE) |ocaic ca save er ancwanescarum cacaesutccs ae canada cavaciu cave ourmse nescaJautccseateaneivons 10
10(9) Distance between anatomical line tangent to posterior margin of anterior
ocellus and anterior margin of posterior ocelli 0.5 x diameter of anterior
ocelli (Fig. 77); ocular—ocellar line 2.5 x as long as posterior ocellus diameter;
interocellar distance 1.6 x as long as posterior ocellus diameter; T1 relatively
narrower medially, T1 width at half length of tergite clearly less than width
at anterior margin, and 1.5 x as wide as width at posterior margin (Fig. 78);
T2 1.8 x as long as wide [Mexico] .............. Sendaphne sulmo Nixon, 1965
— Distance between anatomical line tangent to posterior margin of anterior ocel-
lus and anterior margin of posterior ocelli 0.2—-0.3 x diameter of anterior ocelli
(partially visible in Fig. 16); ocular—ocellar line 2.1—2.4 x as long as posterior
ocellus diameter; interocellar distance 1.2—1.4 x as long as posterior ocellus
diameter; T1 relatively wider medially, T1 width at half length of tergite about
same as width at anterior margin, and at least 2.0 x as wide as width at poste-
rior margin (Figs 18, 19); T'2 2.0 x as long as wide [Brazil, Colombia]...........
pateead Sendaphne dianariaspennae Fernandez-Triana & Whitfield, sp. n.

Taxonomic treatment of species, in alphabetical order

Sendaphne anitae Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/5A29AD35-D955-44B 1-B1C3-64182FDO0E55B
Figs 1—7

Holotype. Female, CNC. ECUADOR, Napo, Reventador; 11.iii.1983; coll. L. Hug-
gert. DNA Voucher code: CNCHYM 07027.

Paratypes. 4 9 (CNC), same locality and collecting date than holotype. Two of
the specimens also have DNA Voucher codes: CNCHYM 07026, CNCHYM 07028.

Diagnosis. This species is morphological similar to Sendaphne dianariaspennae
and S. su/mo but differs from those species in the shape and angle of junction of veins
r and 2RS, shape of mediotergite 2, ovipositor length, and head coloration (orange-
yellow on clypeus and face centrally in anitae, head entirely dark brown to black in
dianariaspennae and sulmo).

Description. Head color: dark brown to black, except for orange-yellow on cl-
ypeus and face centrally. Mesosoma color: orange-yellow. Tegula color: orange-yellow.
Metasoma color (dorsally): yellow. Metacoxa color: yellow. Anatomical line tangent to
posterior margin of anterior ocellus crossing very slightly (less than 0.01 mm) above
anterior margin of posterior ocelli. Ocular—ocellar line: 0.20 mm. Interocellar dis-
tance: 0.09 mm. Posterior ocellus diameter: 0.09 mm. Body length: 4.0-4.5 mm.
Fore wing length: 3.6—-4.1 mm. Ovipositor length: 2.4—2.6 mm. Metacoxa length: 1.3
mm. Metafemur length: 1.2 mm. Metatibia length: 1.3-1.4 mm. T1 length/width at

8 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 1-7. Sendaphne anitae, female holotype. | Habitus, lateral view 2 Head, frontal view 3 Fore
wing 4 Metasoma, dorsal view 5 Head and mesosoma (partially) lateral view 6 Metasoma, ventro-lateral

view 7 Mesosoma and metasoma (partially) dorsal view.

Revision of the neotropical genus Sendaphne Nixon... 9

posterior margin: 0.6 mm/0.15 mm. T2 length/width at posterior margin: 0.26—0.30
mm/0.3 mm.
Distribution. Only known from the type locality in Ecuador.
Molecular data. No DNA was recovered from the three specimens sampled.
Etymology. Named after Ana Maria (Anita) Fernandez Galliano, daughter of the

senior author, for being such a joyful and wonderful person.

Sendaphne bennetti Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/FB93B9D4-E93C-4939-9740-9C6901154A60
Figs 37-44

Holotype. Male, CNC. MEXICO, Durango, 39km W of La Ciudad, 2120m;
2.vii. 1964; coll. WRM Mason. DNA Voucher code: CNCHYM 07032.

Diagnosis. This species is morphologically similar to Sendaphne broadi from Ec-
uador, but S. bennetti has a wider mediotergite 1 (length 4.0 x its width at posterior
margin vs 6.0 x in broadi), a less transverse first discal cell in the fore wing (1.3 x as
wide as high vs 2.0 x), and a geographical distribution far apart.

Description. Head color: black. Mesosoma color: black. Tegula color: yellow.
Metasoma color (dorsally): mediotergites 1, 2 and anterior half of 3 yellowish-red,
rest dark brown to black. Metacoxa color: yellow. Anatomical line tangent to pos-
terior margin of anterior ocellus crossing beneath anterior margin of posterior ocel-
li. Ocular—ocellar line: 0.21 mm. Interocellar distance: 0.14 mm. Posterior ocellus
diameter: 0.09 mm. Body length: 4.1 mm. Fore wing length: 4.0 mm. Metacoxa
length: 1.1 mm. Metafemur length: 1.2 mm. Metatibia length: 1.4 mm. T1 length/
width at posterior margin: 0.60 mm/0.12 mm. T2 length/width at posterior margin:
0.35 mm/0.35 mm.

Distribution. Only known from the type locality in Mexico.

Molecular data. No DNA could be recovered from the specimen sampled.

Comments. Even though only one male specimen is known, it is sufficiently dis-
tinctive to warrant description. This species is the northernmost known distribution
of the genus Sendaphne.

Etymology. Named after Dr. Andrew Bennett of the Canadian National Collec-
tion, Ottawa, and Canadian expert on Ichneumonidae, in appreciation for his support
and encouragement to study braconid wasps.

Sendaphne brasilianus Penteado-Dias, 1995: 251.

Holotype. Female, DCBU. BRAZIL. Distrito Federal, Brasilia, xii-1981, Malaise trap

(not examined).

10 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 8-14. Sendaphne sulmo, male specimen from Mexico. 8 Habitus, lateral view 9 Head, frontal

view 10 Fore wing I | Meso- and metasoma (partially), lateral view, and hind legs 12 Head and meso-

soma, dorsal view 13 Meso- and metasoma (partially), dorsal view 14 Metasoma, dorsal view.

Revision of the neotropical genus Sendaphne Nixon... re

Diagnosis. This species is morphologically similar to Sendaphne penteadodiasae
but it has a slightly different color pattern, fore wing vein 1Cu-a much shorter than
vein 1Cu-b (subequal in penteadodiasae), much longer and narrow T1, and slightly
longer metacoxa.

Distribution. Only known from the type locality in Brazil.

Molecular data. No specimen is known to have been sampled for DNA.

Comments. We could not study a specimen of this species, but the original de-
scription is sufficiently detailed for recognition, including several line drawings of the
metasoma, fore wing, tip of antenna and hind leg (Penteado-Dias 1995).

Sendaphne broadi Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/BOC5F4FA-617 1-4DFC-93B3-293898C2E94B
Figs 23-28

Holotype. Male, CNC. ECUADOR, Napo, 5km S of Baeza, 1,700 m; 13.ii.1983;
coll. Masner & Sharkey. DNA Voucher code: CNCH3323.

Paratypes. 2 3 (CNC). One specimen with same locality and collecting date
than holotype, the other collected at 1900 m on 9.ii.1983. DNA Voucher codes:
CNCH3322 and CNCH3324.

Diagnosis. This species is morphologically similar to Sendaphne bennetti from
Mexico, but S. broadi has a narrower mediotergite 1 (length 6.0 x its width at poster-
ior margin vs 4.0 x in bennetti), a more transverse first discal cell in the fore wing (2.0
x as wide as high vs 1.3 x), and a geographical distribution far apart.

Description. Head color: dark brown. Mesosoma color: dark brown. Tegula col-
or: yellow. Metasoma color (dorsally): mediotergites 1-2 yellowish-brown, rest brown
to dark brown. Metacoxa color: yellow. Anatomical line tangent to posterior margin
of anterior ocellus crossing very slightly (less than 0.01 mm) above anterior margin of
posterior ocelli. Ocular—ocellar line: 0.17 mm. Interocellar distance: 0.09 mm. Poster-
ior ocellus diameter: 0.07 mm. Body length: 3.5-3.7 mm. Fore wing length: 3.3—3.5
mm. Metacoxa length: 1.1 mm. Metafemur length: 1.2 mm. Metatibia length: 1.4
mm. T1 length/width at posterior margin: 0.45 mm/0.06—0.07 mm. T2 length/width
at posterior margin: 0.25 mm/0.20 mm.

Distribution. Ecuador.

Molecular data. No DNA could be recovered from the three specimens sampled.

Comments. Even though only male specimens of this species are known, they are
sufficiently distinctive to warrant description.

Etymology. Named after Dr. Gavin Broad, of the Natural History Museum, Lon-
don, England, and British expert on Ichneumonidae, in appreciation for his support
over the years, including sharing pictures of and facilitating access to type material
deposited in London.

12 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 15-22. Sendaphne dianariaspennae, female holotype. 15 Habitus, lateral view 16 Head,
frontal view (some inclination downwards) 17 Fore wing 18 Propodeum and metasoma, dorsal view
19 Meso- and metasoma (partially), dorsal view. 20-22: Details of the ovipositor, ovipositor sheaths,

and hypopygium.

Revision of the neotropical genus Sendaphne Nixon... 13

Sendaphne dianariaspennae Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/423 FCOAA-4087-414C-B242-856191CFF5AD
Figs 15-22

Holotype. Female, CNC. BRAZIL, Rio de Janeiro, Mangaratiba; i.1976; coll. M.
Alvarenga. DNA Voucher code: CNCHYM 07025.

Paratypes. 3 9, 1 4 (CNO), Brazil, same locality and date than holotype. 1 9
(CNC), Brazil, Nova Teutonia, 27°11'S, 52°23'W, 300-500m, 21.iii.1961, coll.
F. Plaumann. 2 3 (CNO), Brazil, Guanabara and Represa Rio Grande, i.1969 and
i.1972. 1 6 (CNC), Brazil, Caruaru, Pernambuco, v.1972. 8 2, 10 3 (Humboldt In-
stitute), Colombia, Magdalena, PNN Tayrona Zaino, 50m, 11°20'N, 74°2'W, speci-
mens collected between 13.v.2000 and 30.viii.2000, coll. R. Henriquez.

Diagnosis. This species is morphological similar to Sendaphne sulmo but differs
in the smaller, less separated ocelli (which form a lower triangle, compared to higher
triangle in su/mo), T1 relatively wider medially, and T2 relatively slender than su/mo.
The geographical distribution of the two species is more than 2,000 km apart.

Description. Head color: dark brown to black. Mesosoma color: orange-yellow.
Tegula color: orange-yellow. Metasoma color (dorsally): yellow. Metacoxa color: yel-
low. Anatomical line tangent to posterior margin of anterior ocellus crossing slightly
(0.01—-0.02 mm) above anterior margin of posterior ocelli. Ocular—ocellar line: 0.17
mm. Interocellar distance: 0.10 mm. Posterior ocellus diameter: 0.07—0.08 mm. Body
length: 3.2-3.5 mm. Fore wing length: 3.0—3.2 mm. Ovipositor length: 2.3-3.0 mm.
Metacoxa length: 0.90-0.95 mm. Metafemur length: 0.90 mm. Metatibia length:
1.12-1.35 mm. T1 length/width at posterior margin: 0.45—0.50 mm/0.05—0.06 mm.
T2 length/width at posterior margin: 0.35 mm/0.18—0.20 mm.

Distribution. Brazil and Colombia.

Molecular data. Four of the paratypes from Brazil (DNA Voucher codes:
CNCHYM 07023, CNCHYM 07024 and CNCHYM 07040) as well as the holotype
were sampled for DNA. Only one of the paratypes (CNCHYM 07040) rendered a
minibarcode of 103 base pairs.

Comments. The Brazilian specimens of S. dianariaspennae were collected between
January and March, while the Colombian specimens were collected between May and
August.

Etymology. Named after Diana Carolina Arias-Penna (Colombia), in recogni-
tion of her blossoming career studying neotropical Braconidae, especially species from
South America.

Sendaphne jatai Penteado-Dias, 1995: 252.
Figs 29-36

Holotype. Female, DCBU. BRAZIL. Sao Paulo, Reserva Ecoldégica do Jatat, gallery
forest of Mogi River; 24.v.1991; sweeping (not examined).

14 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 23-28. Sendaphne broadi, male holotype. 23 Habitus, lateral view 24 Fore wing 25 Metasoma,

dorsal view 26 Metasoma, lateral view 27 Head and mesosoma (partially), dorsal view 28 Mesosoma and
T1-T2, dorsal view.

Revision of the neotropical genus Sendaphne Nixon... 1)

Figures 29-36. Sendaphne jatai, female specimen from Brazil. 29 Habitus, lateral view 30 Head and

mesosoma (partially), dorso-lateral view 31 Fore wing 32 Metasoma, dorsal view 33 Scutellar disc,

propodeum and T1 (partially), dorsal view 34 Head, frontal view 35 Metasoma, lateral view 36 Meso-
soma and metasoma (partially), dorsal view.

16 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 37-44. Sendaphne bennetti, male holotype. 37 Habitus, lateral view 38 Habitus, dorsal view
39 Fore wing 40 Head and mesosoma (partially), dorsal view 41 Head, fronto-lateral view 42 Metasoma,
dorsal view 43 Metasoma, lateral view 44 Scutellar disc, propodeum and T1-T2 (partially), dorsal view.

Revision of the neotropical genus Sendaphne Nixon... 17

Specimens examined. 1 9 (CNC), Brazil, Mato Grosso, Sinop, x.1974, coll. M.
Alvarenga, DNA Voucher code: CNCH3320. 1 9, 1 3 (CNC), Ecuador, Pichincha,
47 km S of Santo Domingo, Rio Palenque, 200m, 18—30.v.1975 and 22-31 .vii.1976,
coll. S. & J. Peck, DNA Voucher codes: CNCHYM 07034 and CNCHYM 07035.
1 Q (FUSAGx), French Guiana, Saul, Crique popote, Mont Belvédere, 3°36'N,
53°10'W, ii.2001, coll. J. Tarin.

Diagnosis. ‘This is the only species where female specimens have the body entirely yellow.

Distribution. Brazil, Ecuador, French Guiana.

Molecular data. The two specimens from Ecuador rendered minibarcodes of 102
base pairs (CNCHYM 07034) and 164 base pairs (CNCHYM 07035).

Comments. The male specimen from Ecuador has some dark bands on medioter-
gites 5—7, but otherwise is similar to the original description.

Sendaphne olearus Nixon, 1965: 204.
Figs 45-53, 79-80

Holotype. Female, BMNH. BRAZIL, Nova Teutonia, 2.iii.1937 (not examined).

Specimens examined. 1 2 (CNC), Brazil, Nova Teutonia, 27°11'S, 52°23'W,
300-500m, 2.iv.1966, DNA Voucher code: CNCHYM 07019. 3 @ (FUSAGx),
French Guiana, Kaw Mountain, Patawa, 4°32'42.20"N, 52°09'09.19"W, v.1999
and viii.1999, Malaise trap. 1 2 (BMNH) Peru, Loreto, Estacion Jenaro Herrera,
4°53'55.0"S, 73°39'00.4"W, 121m, 13—23.i.2011, D. Karlsson & N. Dale-Skey,
BMNH(E) 2011-72, BMNH(E)#1249978.

Diagnosis. This species is similar to Sendaphne jatai, both having the lightest (i.e.,
more yellowish) coloration among all known species within the genus. S. olearus has
brown bands on posterior margin of mediotergites 4—6, and its body coloration is
generally more yellow-reddish (jatai body color is entirely yellow).

Distribution. Brazil, French Guiana, Peru.

Molecular data. The CNC specimen from the type locality in Brazil (CNCHYM
07019) rendered a minibarcode of 164 base pairs.

Comments. We could not see the holotype of this species, but the original descrip-
tion is adequately detailed for discrimination. We examined one female from the type
locality (collected 30 years after the holotype female), the only known male specimens
(from French Guiana), which were discussed in Braet (2006), and the first known
specimen from Peru.

Sendaphne paranaensis Scatolini & Penteado-Dias, 1999: 53.
Figs 54—60

Holotype. Female, UFPR. BRAZIL, Reserva Biologica Samuel Klabin, Malaise trap

(not examined).

18 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

52 53

Figures 45-53. Sendaphne olearus, female specimen from Brazil. 45 Habitus, lateral view 46 Head

and mesosoma, lateral view 47 Fore wing 48 Head, frontal view 49 Mesosoma and T1, dorsal view
50 Mesosoma and metasoma (partially), dorsal view 51 Metasoma, dorsal view 52 Metasoma, lateral view

53 Details of the ovipositor and ovipositor sheaths.

Revision of the neotropical genus Sendaphne Nixon... 19)

Figures 54-60. Sendaphne paranaensis, female specimen from Brazil. 54 Habitus, lateral view 55 Fore
wing 56 Head and mesosoma (partially), dorsal view 57 Metasoma and legs, lateral view 58 Head, frontal
view 59 Metasoma (partially), dorsal view 60 Scutellar disc, propodeum and T1-T2 (partially), dorsal

view.

20 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Specimens examined. 1 2 (CNC), Brazil, Rio de Janeiro, Guanabara, Silva
Jardim, iii.1974, DNA Voucher code: CNCHYM 07022. 1 4 (CNC), Brazil, Espi-
rito Santo, Castello, xi.1976, DNA Voucher code: CNCHYM 07039. 2 3 (CNC),
Paraguay, Pirapo, 1—3.i.1972, DNA Voucher codes: CNCHYM 07037, and CN-
CHYM 07038.

Other material mentioned in the original description. Almost 70 specimens
(females and males) from Brazil, Parana, Telémaco Borba, collecting dates between
viii. 1986 and iii.1987.

Diagnosis. S. paranaensis is one of only three Sendaphne species with head en-
tirely yellow (or yellow-orange). It differs from the other two species (S. jatai and S.
olearus) in having dark brown areas on the anteromesoscutum and mesopleuron, and
mediotergites 4+ entirely black.

Distribution. Brazil, Paraguay.

Molecular data. Of the four specimens in the CNC sampled for DNA, only one
(CNCHYM 07037) rendered a minibarcode of 164 base pairs.

Comments. The male specimens from Paraguay are much darker in coloration,
but similar variation is mentioned in the original description for the male paratypes

from Brazil (Scatolini and Penteado-Dias 1999: 53).

Sendaphne penteadodiasae Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/7FDD9815-D39B-49EE-9645-749C02277F24
Figs 61-67

Holotype. Female, CNC. BRAZIL, Campina Grande, near Curitiba, 15.ii.1966, coll.
H. & M. Townes. DNA Voucher code: CNCHYM 07020.

Paratype. 1 @, same locality as holotype, 10.ii.1966. DNA Voucher code:
CNCHYM 07021.

Diagnosis. ‘This species is morphologically similar to Sendaphne brasilianus but
it has a slightly different color pattern, fore wing vein 1Cu-a subequal to vein 1Cu-b
(much shorter in brasilianus), shorter and wider T1, and slightly shorter metacoxa.

Description. Head color: dark brown to black. Mesosoma color: orange-yellow.
Tegula color: orange-yellow. Metasoma color (dorsally): mostly orange-yellow, with
some narrow brown bands on posterior margin of mediotergites 5—7. Metacoxa color:
yellow. Anatomical line tangent to posterior margin of anterior ocellus crossing very
slightly (less than 0.01 mm) above anterior margin of posterior ocelli. Ocular—ocel-
lar line: 0.12 mm. Interocellar distance: 0.10 mm. Posterior ocellus diameter: 0.08
mm. Body length: 4.2 mm. Fore wing length: 3.9 mm. Ovipositor length: 2.5 mm.
Metacoxa length: 1.20 mm. Metafemur length: 1.25 mm. Metatibia length: 1.11 mm.
T1 length/width at posterior margin: 0.35 mm/0.06 mm. T2 length/width at posterior
margin: 0.25 mm/0.12 mm.

Distribution. Only known from the type locality in Brazil.

Molecular data. No DNA could be recovered from the two specimens sampled.

Revision of the neotropical genus Sendaphne Nixon... 21

Comments. The specimens of this species (housed in the CNC) were previous-
ly identified by W.R.M. Mason as “Sendaphne sulmo”. However, the morphological
differences from the original description of Sendaphne sulmo (see key and diagnosis
above), and the disparate geographical distribution allows us to consider the Brazilian
and Mexican specimens as separate species.

Etymology. Named after Dr. Angélica Maria Penteado Martins-Dias (Brazil), in
recognition of her career studying Braconidae, and also for her work describing most
of the previously known species of Sendaphne.

Sendaphne rogerblancoi Fernandez-Triana & Whitfield, sp. n.
http://zoobank.org/O9ABEGF 1 -4EFC-43B5-BE10-5631E671B76E
Figs 68—75

Holotype. Female, CNC. COSTA RICA, Guanacaste, Area de Conservacién Guan-
acaste, Sector Cacao, Sendero Cima, 1,460 m, 10.93328, -85.45729; 18.xii.2008; coll.
D.H. Janzen & W. Hallwachs. DNA Voucher code: DHJPAR0031465.

Paratypes. 4 9,592 (BMNH, CNC, INBio, NMNH), same locality as holotype.
Collecting dates are mostly on December 2008, with one record each in November
2008, March 2009, and April 2009. All specimens are from one Malaise trap at the
very peak of Volcan Cacao.

Diagnosis. This is the most distinctive species of Sendaphne based on coloration
(head, mesosoma, metasoma, and metacoxa black), shape of first discal cell, and nar-
row mediotergite 1.

Description. Head color: black. Mesosoma color: black. Tegula color: dark
brown. Metasoma color (dorsally): black. Metacoxa color: dark brown to black.
Anatomical line tangent to posterior margin of anterior ocellus crossing very slightly
(less than 0.01 mm) above anterior margin of posterior ocelli. Ocular—ocellar line:
0.17-0.18 mm. Interocellar distance: 0.09 mm. Posterior ocellus diameter: 0.08 mm.
Body length: 4.3-4.6 mm. Fore wing length: 4.2-4.3 mm. Ovipositor length: 3.8—4.2
mm. Metacoxa length: 1.10—-1.11 mm. Metafemur length: 0.85—0.90 mm. Metatibia
length: 1.5-1.6 mm. T1 length/width at posterior margin: 0.80—0.85 mm/0.15—0.16
mm. T2 length/width at posterior margin: 0.45 mm/0.25 mm.

Distribution. Only the summit cloud forest at 1,450 m on Volcan Cacao, north-
western Costa Rica.

Molecular data. In BOLD there are data for 16 specimens of this species (the
holotype, the paratypes and other specimens that we could not examine) which ren-
dered partial barcodes, most of them from 260 to 390 base pairs. Only the holotype
(DNA Voucher code: DHJPAR0031465) had a longer barcode (633 base pairs).

Etymology. This unique species, the only Sendaphne known from Costa Rica so far, is
named after Sr. Roger Blanco Segura, of Area de Conservacién Guanacaste (ACG), north-
western Costa Rica, in recognition of his 3+ decades of intense care and management of
ACG in an enormous variety of circumstances and for a very large array of purposes.

2? Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Figures 61-67. Sendaphne penteadodiasae, female holotype. 61 Habitus, lateral view 62 Fore wing
63 Metasoma, dorsal view 64 Ovipositor and hypopygium, lateral view 65 Head, frontal view 66 Head

and mesosoma (partially), dorsal view 67 Propodeum, T1-T2 (partially), dorsal view.

Revision of the neotropical genus Sendaphne Nixon... 25

Figures 68-75. Sendaphne rogerblancoi, female holotype. 68 Habitus, lateral view 69 Fore wing
70 Head, frontal view 71 Hypopygium and hind legs (partially), lateral view 72 Ovipositor, ovipositor

sheaths, and hypopygium, lateral view 73 Head and mesosoma (partially), lateral view 74 Propodeum
and T1, dorsal view 75 Propodeum and mesosoma, dorsal view.

Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

78

Figures 76-78. Sendaphne sulmo, female holotype. 76 Habitus, lateral view 77 Head and mesosoma

(partially), dorsal view 78 Propodeum and metasoma, dorsal view.

Revision of the neotropical genus Sendaphne Nixon...

80

Figures 79-80. Sendaphne olearus, female specimen from Peru. 79 Habitus, lateral view 80 Detail of

the fore wing.

26 Jose L. Fernandez-Triana et al. / Journal of Hymenoptera Research 41: 1-29 (2014)

Sendaphne sulmo Nixon, 1965: 204.
Figs 8-14, 76-78

Holotype. Female, BMNH. MEXICO, Tabasco, Teapa (not examined).

Specimens examined. 3 3 (CNC). Mexico, Chiapas, 16°58'N, 91°47'W, 560 m;
(collecting dates: 6.ix.1978, 28.x.1978, 8—11.xi.1978); coll. J. Rawlins. DNA Voucher
codes: CNCHYM 07030 CNCHYM 07031 and CNCHYM 07033.

Diagnosis. ‘This is the only known species of Sendaphne with a higher ocellar tri-
angle (i.e., anatomical line tangent to posterior margin of anterior ocellus crosses far
above anterior margin of posterior ocelli). The distance between anatomical line tan-
gent to posterior margin of anterior ocellus and anterior margin of posterior ocelli is
0.5 x the diameter of anterior ocelli (Fig. 77), while for all other known species of
Sendaphne it is usually 0.10.3 x.

Distribution. Only known from lowlands (100-560 m) of Mexico.

Comments. We could only study some photos of the holotype (Figs 76-78) and
the original description which included a line drawing of the metasoma (Nixon 1965:
207, Figure 255). The drawing shows a T1 slightly narrower medially than the photos
of the actual holotype reveal, but the rest of the original description is in agreement
with the photos we examined. The males mentioned above are, however, different
from the female holotype in having a darker anteromesoscutum, scutellar disc, and
metasoma (Figs 8—14), and also the ocellar triangle is not as elevated. Lacking more
specimens to examine (especially females), we have refrained from considering those
male specimens as a different species because the two localities are not too far apart and
males are known to be darker in other species of Sendaphne. If more material becomes
available for study in the future, the status of those specimens may be clarified.

Molecular data. The three male specimens sampled for DNA rendered minibar-
codes of 103 base pairs each.

Acknowledgements

We emphatically and gratefully acknowledge the support of the ACG parataxonomist
team in finding and rearing these caterpillars, their parasitoids and their hyperparasi-
toids, and Area de Conservacion Guanacaste (ACG) for preserving the forests in which
they live, and the Guanacaste Dry Forest Conservation Fund, the Wege Foundation,
the International Conservation Fund of Canada, the JRS Biodiversity Foundation,
Jessie Hill, Steve Stroud, Permian Global, and the University of Pennsylvania for fund-
ing portions of the research. Several Colombian specimens were collected during a
project supported by NSF grant DEB 0205982 awarded to M. J. Sharkey and B. V
Brown. This study was also supported by NSF DEB 0515699 to DHJ and by a Natu-
ral Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant
to MAS. Laboratory analyses of these sequences were funded by the Government of
Canada through Genome Canada and the Ontario Genomics Institute (2008-0GI-

Revision of the neotropical genus Sendaphne Nixon... 27

ICI-03), and by BOLD/iBOL of the Biodiversity Institute of Ontario and Univer-
sity of Guelph. JFT thanks Yves Braet (Belgium) for making specimens from French
Guiana available for this study and Gavin Broad (BMNH) for sending pictures of the
specimens housed in London. ‘The suggestions from two anonymous reviewers and the
editor considerably improved the final version of this paper.

References

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Société Royale Belge d’Entomologie 142(7-12):155-172.

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letin of the British Museum (Natural History), Entomology series, Supplement 2: 1-284.

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inglife.org). Molecular Ecology Notes 7: 355-364. doi: 10.1111/j.1471-8286.2007.01678.x

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Revision of the neotropical genus Sendaphne Nixon... 29

Supplementary material |

Details of Sendaphne specimens with sequences in BOLD.

Authors: Jose L. Fernandez-Triana, James B. Whitfield, M. Alex Smith, Win-

nie Hallwachs, Daniel H. Janzen

Data type: species data

Explanation note: The Excel file contains details on locality, sampling date, collectors,
museum codes, sequence length, and other data related to Sendaphne specimens.

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.

Supplementary material 2

Data for phylogenetic analysis.

Authors: Jose L. Fernandez-Triana, James B. Whitfield, M. Alex Smith, Win-

nie Hallwachs, Daniel H. Janzen

Data type: sequence data

Explanation note: Neighbor-Joining tree based on Kimura 2-parameter distances of
all described species of Sendaphne with DNA barcodes available. Sequence data
from the Barcode of Life Data Systems (http://www.boldsystems.org/). For every
sequence the species name, specimen code, length of sequence (in base pairs), and
country/province or country/state is shown.

Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License
(ODDbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.