ore

JHR 49: 65-79 (20 I 6) JOURNAL OF A peer-reviewed open-access journal
doi: 10.3897/JHR.49.7862 (f-) Hymenoptera

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

First record of egg sac predation on a wall crab spider
Selenopidae (Araneae) by the wasp Camera lunavenatrix
sp. n. (Ichneumonidae, Cryptinae)

German Antonio Villanueva-Bonilla', Helena Carolina Onody’,
Bernardo FE Santos’, Jodo Vasconcellos-Neto*

| Programa de Pés-Graduacao em Biologia Animal, Departamento de Biologia Animal, Instituto de Biologia,
Caixa Postal: 6109. Universidade Estadual de Campinas - UNICAMP. 13083-970, Campinas, SP Brazil
2 Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de Sao Carlos, Rodovia Washington
Luiz, km 325, 13 565-905 - Séo Carlos, SP Brazil 3 Richard Gilder Graduate School, American Museum
of Natural History, Central Park West at 79th street, New York, NY, USA - 10024-5192 4 Departamento de
Biologia Animal, Instituto de Biologia, Caixa Postal: 6109. Universidade Estadual de Campinas - UNICAMP
13083-970, Campinas, SP Brazil

Corresponding author: German A.V. Bonilla (germanvillanueva9@gmail.com)

Academic editor: M/. Shaw | Received 21 January 2016 | Accepted 24 March 2016 | Published 28 April 2016
http.//zoobank.org/D4 1 127B1-BA23-482A-BCCD-ABOD2DAIF 147

Citation: Villanueva-Bonilla GA, Onody HC, Santos BF, Vasconcellos-Neto J (2016) First record of egg sac predation on
a wall crab spider Selenopidae (Araneae) by the wasp Camera lunavenatrix sp. n. (Ichneumonidae, Cryptinae). Journal of
Hymenoptera Research 49: 65-79. doi: 10.3897/JHR.49.7862

Abstract

We report the first record of egg sac predation on the wall crab spider Selenops cocheleti by wasps of the
genus Camera (Ichneumonidae: Cryptinae) with the description of a new species, as well as biological
information on the wasp and the spider host. The rearing record and information presented herein are the

first biological data for the genus.

Keywords

Egg sac structure, egg predation, Hymenoptera, neotropical

Copyright German A.V. Bonilla 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.

66 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

Introduction

Interactions between adult spiders and predatory or parasitoid wasps are a well-known
phenomenon. Wasps from the families Crabronidae, Sphecidae and Pompilidae para-
lyze adult or sub-adult spiders, which are taken as food for the larvae (Hanson and
Gauld 2006). The transport of prey items to pre-made nests was hypothesized to be a
pre-adaptation for the evolution of social behavior (Evans 1957, Evans and Shimizu
1996); as a consequence, such interactions have sparked much attention. Ichneumonid
wasps from the Polysphincta group (Wahl and Gauld 1998) are koinobiont ectopara-
sitoids of various groups of spiders (Sobczak et al. 2012a, 2014, Gonzaga et al. 2015).
Likewise, this has drawn much interest due to the phenomenon of host behavioral
manipulation (Gonzaga and Sobczak 2011, Takasuka et al. 2015).

On the other hand, predators of spider eggs have received much less attention,
particularly in regard to their host-seeking behavior and their influence on the fitness
of spiders.

Some groups of wasps are egg parasitoids, including members of the families
Encyrtidae, Eulophidae (Hieber 1984, Austin 1985, Schoeninger et al. 2015) and
Platygastridae (Fitton et al. 1987, Godfray 1994, Stevens and Austin 2007, Bowden
and Buddle 2012). In this case, each of these wasp larvae consumes only one egg
of the spider host (LaSalle 1990). Other wasp lineages, including members of Eu-
pelmidae, Eulophidae, Eurytomidae, Pteromalidae and Ichneumonidae (e.g. Gelis
festinans), are known to act as predators in attacking and consuming successive eggs
in the sacs (Fitton et al. 1987, Baarlen et al. 1994, 1996, Quicke 2015). In the tem-
perate zone, several genera of Cryptinae (Ichneumonidae) are recorded preying on
ege sacs of various groups of spiders, including Agasthenes, Gelis, Hidryta, Idiolispa,
Thaumatogelis and Trychosis (Townes 1970, Schwarz and Shaw 1998, 1999, 2000).
In the Neotropics, however, relatively few studies are aimed at spider egg predators
(e.g. Sobczak et al. 2012b).

Spiders of the species Selenops cocheleti Simon 1880 (Araneae: Selenopidae) are sit-
and-wait predators occurring on tree trunks, under bark or in crevices of rocks (Cor-
ronca 1998, Alayén-Garcia 2005, Valdez-Mondragén 2007). They are skilled hunters
with nocturnal habits and fast movements to capture prey and escape from predators.
When disturbed, individuals promptly hide in inaccessible places (Crews et al. 2008,
Alayén-Garcia 2005), making observational studies rather difficult. As a result, knowl-
edge of the ecological interactions involving these spiders is still sparse. In fact, there
are no records of egg predation by wasps upon spiders of the family Selenopidae.

In this study we present information on the egg sac structure of Selenops cocheleti,
as well as the first record of egg predation by wasps of the genus Camera (Ichneu-
monidae: Cryptinae), with the description of a new species. We also present biological
information on the wasp and the spider host.

First record of egg sac predation on a wall crab spider Selenopidae (Araneae)... 67

Methods

Study site

The Serra do Japi highlands area is a small mountainous region in southeastern Brazil, locat-
ed in the west of the Atlantic Plateau in the state of Séo Paulo. This area has an altitudinal
variation between 700 m and 1300 m above sea level. Average annual temperatures oscil-
late between 15.7 °C and 19.2 °C in the higher and lower parts of the highlands. A meso-
phyll seasonal forest covers most of the forest area of Serra do Japi (Morellato 1992). ‘The
material was collected in a farm near to the Base Ecoldgica at Serra do Japi (23°13'53.60"S,
46°52'47.01"W) in two sites denominated “Chacara do Lima” (23°13'53.60"S,
46°55'47.01"W) and “Monte Horebe” (23°14'01.17"S, 46°55'47.01"W).

Collection of Selenops cocheleti egg sacs

On September 28" and October 3“ of 2014, we searched at night (18:00 to 21:00) for
ege sacs and for gravid adult females of Selenops cocheleti in trunks of Plinia cauliflora
(Myrtaceae; commonly known as jaboticaba) and Pinus elliottii (Pinaceae) where these
spiders are frequently seen.

The egg sacs and gravid adult females obtained in the field were photographed and
taken to the laboratory where they were kept in plastic pots to inspect for potential
larvae or pupae of parasitoids or predators. The attacked egg sacs were isolated and the
emerging adult wasps collected. All egg sacs (attacked or not) were opened for struc-
tural analysis and description. Gravid adult females of S. cocheleti collected in the field
were also taken and maintained under laboratory conditions. Then we collected the
ege sacs laid by the females to estimate the number of eggs per sac and the develop-
ment time of the early instars of this species of spider.

Taxonomic treatment

All methods and conventions, including morphological terminology and biometrics,
follow Santos and Aguiar (2013), except that the cell 1+2Rs is called “areolet” for
simplicity.

The studied specimens are deposited at DCBU (Departamento de Ecologia e Bio-
logia Evolutiva da Universidade Federal de Sao Carlos, Sao Carlos, SP, Brazil) and
MZUSP (Museu de Zoologia da Universidade de Sao Paulo, Sao Paulo, Sao Paulo,
Brazil). The numbers that follow the depository acronyms refer to the registration of
each specimen in the institutions.

68 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

Results

Egg sac structure and number of eggs of Selenops cocheleti

Selenops cocheleti builds an egg sac consisting of three steps, with layers of web giving
protection to the eggs: (1) The female at first produces a concave dish that is adhered
to the bark of the tree where the eggs are laid; (2) later it builds a layer that will
close the egg sac; and (3) when the egg sac is complete, a dense layer of silk threads
is added. The egg sac can be found attached on the inner surface of loose bark on
Plinia and Pinus tree trunks (Figure 1A). The two inner layers serve as a wrap for the
eggs and the outermost layer is thicker and more resistant (Figure 1B). Adult females
rest on the egg sac during the day, and leave their shelter at night to feed. The egg sac
can contain up to 287 eggs (Figure 1C) when it is not attacked (average = 181.75;
SD = 82.13; n = 4). The eggs hatched within 16 + 2 days (n = 2) inside the egg sac
(Figure 1D). During this period (approximately two weeks) adult females take care
of the egg sac standing over it. About three days later, the spiderlings moulted for
the first time (into their second instar) whilst still within the egg sac; they remain
within the egg sac for on average 18 days, after which they perform a second moult
and become more active. Two days after the second molt, spiderlings left the egg sac
and scattered. Thus, development time from egg laying to the spiderlings leaving the
ege sac was about 40 days. In the egg sacs (n=2) laid by females maintained in the
laboratory and in two of the egg sacs collected in the field that were not attacked
by Camera lunavenatrix sp. n. about 10% of the eggs remained without embryonic
development, even after 18 days.

Egg predation

We collected five egg sacs in the field, of which three had Camera lunavenatrix sp. n.
larva feeding on the eggs, in each case gregariously (Table 1). The wasps pupated inside

Table 1. Number of pupae of Camera lunavenatrix sp. n. (Ichneumonidae: Cryptinae) per egg sac of S.
cocheleti recorded in the trees trunks of jaboticaba (Plinia cauliflora, Myrtaceae) and pine (Pinus elliottii,
Pinaceae) during September (Sep.) and October (Oct.) of 2014 in the Ecological Station Serra do Japi,
SP-Brazil.

Females Survival rate of spiders
Egg sac 1 - 0%
Egg sac 2 2 0%
Egg sac 3 , 0 0 88%
Egg sac 4 0 2 0%
Egg sac 5 0 0 91%
Total 3 4

First record of egg sac predation on a wall crab spider Selenopidae (Araneae)... 69

Figure |. Egg sac of Selenops cocheleti. A In a tree trunk B Egg sac structure in layers C Eggs D Newly
emerged spiderlings from the egg inside the egg sac (1* instar) and detail of one of the embryos E Second
instar spiders F Spiderling (3" instar) on tree trunk G Adult female on Plinia cauliflora (Myrtaceae) tree
trunk in Serra do Japi, SP, Brazil.

the egg sac (Figure 2A). The adult wasps emerged 5—7 days after collection of the egg
sacs. In one of the collected egg sacs, two wasp pupae did not emerge as adults.

After the emergence of the adult wasps, we dissected all attacked egg sacs and did
not find spiderlings or exuviae inside, indicating that all of the eggs had been con-
sumed. The wasp pupae were arranged next to each other in all the egg sacs attacked
(Figure 2C). To leave the egg sac, the adult wasps cut a hole in the walls with their
mandibles (Figure 2D).

Wasp behavior

Adult females of the wasp Camera lunavenatrix were observed in the field from
19:50 PM to 20:25 PM inspecting cracks in the trunk as well as spaces under bark
on Plinia trees trunks, possibly looking for egg sacs of Selenops cocheleti. On the
trunks, the female wasps performed a “hammering” movement with the antennae
on the trunk surface for about 15 minutes before flying to another trunk to continue
searching.

70 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

Figure 2. Pupae of Camera lunavenatrix sp. n. in egg sac of Selenops cocheleti (Selenopidae). A, B Egg
sac collected under bark of jaboticaba (Plinia cauliflora, Myrtaceae) with wasp larvae developing; the
white fragments correspond to consumed eggs C Egg sac collected under bark of pine (Pinus elliottii)

D, E Adult female of Camera lunavenatrix emerging from the egg sac of Selenops cocheleti.

Taxonomy

Camera Townes 1962

Camera: Townes 1962: 432. Type species: Mesostenus euryapsis (Cameron, 1885), by
original designation.

Diagnosis. Clypeus distinctly convex, subpyramidal in profile; malar space 0.80—1.00
as long as basal width of mandible. Mesoscutum only slightly convex; hind margin

First record of egg sac predation on a wall crab spider Selenopidae (Araneae)... 71

of metanotum with distinct tooth-like projection. Propodeum short, about as long
as maximum length of mesopleuron; anterior and posterior transverse carinae usually
complete, posterior carina sometimes medially indistinct. Areolet moderately small,
longer than wide, crossveins 2r-m and 31r-m subparallel or weakly convergent. First
metasomal tergite with anterolateral tooth, its spiracle placed at posterior 0.4—0.3;
ovipositor sheath 0.25—0.42 as long as hind tibia.

Comments. The new species C. /unavenatrix is the fifth species for the genus.
There are three other Neotropical species, from Brazil, Mexico and Cuba, in addition
to the type species, Camera euryapsis, which occurs from Texas to Mexico and also in
Cuba. Species of Camera seem to be rarely collected by Malaise and yellow pan traps
(e.g., none collected by the extensive sampling of Aguiar and Santos 2010), and exa-
mination of tens of thousands of specimens Neotropical Cryptini does not indicate a
large number of undescribed species (unpublished data). Camera shares a number of
features with Holarctic genera of Cryptini that attack spider eggs — such as Trychosis,
Idiolispa and Hidryta — including a short ovipositor, relatively flat mesoscutum, strong-
ly convex clypeus and a simple, unmodified tip of the apical flagellomere. The rearing
record and information presented herein are the first biological data for the genus.

Camera lunavenatrix Santos & Onody, s
http://zoobank.org/4394F 1 C7-E421-437D- SFEG. C75DE28527F5

Type material. Holotype 2 (DCBU# 91323): BRAZIL, Sao Paulo, Jundiai, Serra do
Japi, 23°11'S, 46°52'W. Emerged on 24.x.2014 from egg sac of Selenops cocheleti (Ara-
neae: Selenopidae) collected on 17.x.2014. G. Villanueva. Paratypes: 1 9 (MZUSP#
54697), same data as holotype; 2 9, 3 d (DCBU# 91324-91326; MZUSP# 54698,
54699), same data as holotype, except egg sacs collected on 18.ix.2014 and emergences
on 23—25.ix.2014.

Diagnosis. Head, mesosoma and metasoma almost entirely black except legs fer-
ruginous; occipital carina incomplete ventrally; tergite 1 relatively short, almost as
long as tergite 2; body covered with moderately dense white pilosity; ovipositor short,
0.25x as long as hind tibia; clypeus convex, in lateral view almost pyramidal; posterior
transverse carina of propodeum medially arched forwards, raised laterally; crossveins
2r-m and 3r-m of areolet subparallel; vein 2m-cu almost straight, reclivous; forewing
vein lcu-a arising distinctly basad of 1M+Rs.

Female. Forewing 9.0 mm. Head. Densely pilose; mandible stout, apex 0.6x as
wide as base; malar space 0.8x as long as basal width of mandible. Clypeus densely
punctate, 2.0x as wide as high, in front view more or less trapezoidal, width at apex
1.4x of basal width, distinctly convex, apically abruptly truncate, in lateral view almost
pyramidal; apical margin medially straight, laterally not projecting. Antenna with 33
flagellomeres; first flagellomere 6.5x as long as wide; apex of apical flagellomere uni-
formly tapered; area between antennae with small rounded tubercle. Supra-clypeal

F2 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

Figures 3-4. Camera lunavenatrix sp. n. 3 Holotype habitus 4 Male paratype habitus. Scale bar: 0.5 mm.

First record of egg sac predation on a wall crab spider Selenopidae (Araneae)... 73

area convex, distinctly rugose-punctate. Supra-antennal area distinctly rugose-punc-
tate, medially with a distinct longitudinal depression. Vertex finely punctate. Occipital
carina sharp, laterally sinuous, incomplete ventrally, not meeting hypostomal carina
or base of mandible.

Thorax. Mostly mat, uniformly and densely pilose. Pronotum densely punctate,
ventrally striate; epomia distinct, diverging from pronotal collar, dorsally straight, al-
most reaching dorsal margin of pronotum. Mesoscutum almost flattened, subcircular,
1.1x as long as wide, shiny, densely punctate; notaulus distinct over more than 0.5
of mesoscutum length, with transverse striae, strongly impressed anteriorly, weaker
posteriorly; scutellum shiny, punctate; scuto-scutellar groove deep, anteriorly mostly
smooth, posteriorly with longitudinal striae. Mesopleuron ranging from densely punc-
tate to rugose-punctate; subalar ridge distinctly projecting, narrow; epicnemial carina
reaching about 0.7 of distance to subalar ridge; sternaulus incomplete and weak, reach-
ing 0.6 of distance to mid coxa. Transverse sulcus at base of propodeum deep, about
0.4x as long as anterior area of propodeum, medially smooth; metapleuron densely
punctate, juxtacoxal carina absent. Fourth tarsomere not bilobed.

Propodeum.1.1x as long as wide; anterior margin medially concave, with distinct
anterolateral projections; anterior area moderately punctate, shiny and smooth between
punctures and slightly rugose on first lateral area, medially with distinct longitudinal
carina; spiracle elliptic, spiracle 2.0x as wide as long; anterior transverse carina medially
slightly arched forwards. Posterior area of propodeum rugulose; posterior transverse
carina complete, medially distinctly arched forwards, raised laterally; median longitu-
dinal carina of propodeum present between anterior and posterior transverse carinae.

Wings. Forewing vein 1-Rs+M and crossvein 1m-cu both almost straight; bulla of
1-Rs+M placed almost on its midlength; forewing crossvein lcu-a arising distinctly
basad of 1M+Rs; vein 2Cua 1.1x as long as crossvein 2cu-a; crossvein 2m-cu almost
straight, reclivous, bulla placed on midlength; areolet of moderate size, 1.30 as long as
pterostigma, pentagonal, 1.1x as long as wide; crossveins 2r-m and 3r-m subparallel,
about same length; vein 3-M distinctly shorter than 2-M. Hind wing vein 1-M forming
right angle with vein Cua; vein Cub weakly convex, forming right angle with vein Cua.

Metasoma. First tergite moderately short, almost as long as tergite 2, about 2.0x
as long as maximum width; in cross section approximately depressed, mostly striate,
sparsely pilose; apex 2.5x as wide as base; spiracle at posterior 0.4 of its length, dis-
tinctly prominent; ventrolateral and median dorsal carinae absent; dorsolateral carinae
present, reaching 0.5 of tergite 1 length. Tergite 2 short, 1.1x as long as maximum
width, in dorsal view trapezoidal, posterior width 1.7x anterior width, mostly strongly
punctate, apically finely punctate; thyridium slightly longer than wide; tergites 3-8
finely pilose and punctate. Ovipositor very short, 0.25x as long as hind tibia, slender,
straight, distinctly compressed, nodus slight but distinct; lower valve without con-
spicuous teeth.

Color. Black with ferruginous legs. Head: black; palpi ferruginous; antenna black,
flagellomeres 6 apically and 7—13 entirely white. Mesosoma: black; legs mostly fer-
ruginous; fore and mid legs basally slightly dark ferruginous, generally lighter towards

74 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

Figures 5-10. Camera lunavenatrix sp. n. (2 holotype). 5 Head in lateral view 6 Mesoscutum in dor-

sal view 7 Mesopleuron and metapleuron in lateral view 8 Propodeum in dorsal view 9 Fore and hind
wings 10 Ovipositor in lateral view. Scale bars: 0.25 mm (5); 0.2 mm (6); 0.5 mm (7); 0.25 mm (8);
0.5 mm (9); 0.1 mm (10).

apex except tarsomere 5 of foreleg and tarsomeres 3—5 of mid leg dark brown; hind
leg with coxa, trochanters and femur dark ferruginous; hind tibia ferruginous on basal
0.65, apical 0.35 blackish; hind tarsomeres 1 basally, 3 apically and 4-5 dark brown
to blackish, tarsomeres 1 apically and 2 entirely white. Metasoma: black, except very
base of tergite 1 marked with ferruginous; ovipositor ferruginous and ovipositor sheath
black; wings hyaline, apically infumate.

Male. Forewing 6.0-8.0 mm long. Generally similar to female except: vertex more
sparsely punctate; first flagellomere shorter, about 3.5x as long as wide; tergite 1 apically

First record of egg sac predation on a wall crab spider Selenopidae (Araneae)... 75

narrower, its maximum width about 1.3—-1.5x minimum width; hind leg with tibia
more extensively blackish and basal 0.25 of tarsomere 1 and tarsomere 5 entirely black.

Variation. Forewing 9-9.5 mm long. Two females have metasoma with tergites
2-8 having some dark ferrugineous areas.

Comments. Camera lunavenatrix sp. n. is similar in general morphology to the
North American species C. euryapsis Cameron and C. californica Kasparyan and Ruiz-
Cancino. The three species have the body approximately cylindrical, with the propode-
um about as tall dorso-ventrally as the anterior part of the thorax, and a relatively short
tergite 1. However, C. /unavenatrix can be readily distinguished from the other two
species by the body almost entirely black (versus with extensive yellow marks); clypeus
almost pyramidal in lateral view (versus only moderately convex, with rounded pro-
file); posterior transverse carina of propodeum medially distinctly arched, bell-shaped
(versus slightly and uniformly arched); and ovipositor quite short, only 0.25x as long
as hind tibia (versus 0.42).

The Brazilian species C. thoracica Szépligeti is quite different from the other species
of the genus in having the anterior part of the thorax rather stout, with the propodeum
distinctly shorter in lateral view; furthermore, tergitel is distinctly longer than tergite
2, very different from the short tergite1 of the other species. Additionally, C. lunavena-
trix can be separated from C. thoracica by the black metasoma (versus bright orange);
and forewing vein lcu-a arising based to crossvein 1M+Rs (versus opposite).

Etymology. From the Latin /una (“moon”) and venatrix (““huntress”). The name
of the spider genus Se/enops derives from Selene, the moon goddess, and the sufhx -ops,
Greek for “eye”. Therefore the new species is deemed a “moon huntress” as it para-
sitizes egg sacs of Selenops.

Discussion

It is known that the egg sac works as a physical barrier isolating the eggs from the
outside environment. In addition, maternal care provides additional protection by
guarding of the eggs (Austin 1985). These protections do not provide absolute defense
against predators such as C. /unavenatrix but can provide protection against a broad
spectrum of opportunistic predators, e.g. ants and other spiders (Austin and Anderson
1978, Austin 1982, 1985).

The observation of adult females of C. /unavenatrix inspecting tree trunks between
19:50 PM and 20:25 PM seems to suggest some degree of nocturnal activity for the
species. This is somewhat inconsistent with the general tendency of nocturnal ichneu-
monids to have pale body color and enlarged ocelli (Gauld 2006). It is unclear whether
C. lunavenatrix may be also (or mostly) active during the day. Diurnal activity has been
observed in other cryptine egg predators such as some European species of the genus
Trychosis, Hidryta and Gnypetomorpha (M. Schwarz pers. comm.).

Females of C. /unavenatrix may search for egg sacs of S. cocheleti during the night
because during this period the adult spider female leaves its shelter to feed, leaving the

76 German A. Villanueva-Bonilla et al. / Journal of Hymenoptera Research 49: 65-79 (2016)

ege sac vulnerable. On the other hand, while the (rather rapid) development of the
wasp takes place, the female spider continues to guard the egg sac. This suggests that
the spider may be unable to perceive any wasp activity or change inside the egg sac.
The larvae of C. lunavenatrix observed in this study consumed 100% of spider
eggs. This is not unusual, as recorded for Tromatobia sp. (Ichneumonidae: Pimplinae)
and Aprostocetus sp. (Ichneumonidae: Eulophidae) attacking Araneus omnicolor (Ara-
neidae) (Sobczak et al. 2012b, 2015). However, other records show that egg consump-
tion is not always complete; if the number of parasitoids in the egg sac is low (Cobb
and Cobb 2004) some spiderlings may emerge (Fitton et al. 1988, Schwarz and Shaw
1999). Similar results were recorded for Nephila edulis (Nephilidae) when attacked by
larvae of the moth Anatrachyntis terminella (Lepidoptera: Cosmopterigidae); in that
case, even with low infestation (six larvae per egg sac), only up to 20% of the eggs

hatched (Austin 1977).

Acknowledgements

This research was supported by Fundacao de Amparo a Pesquisa do Estado de Sao
Paulo (Processes: 2013/16469-8; 2012/15875-0) and the Instituto Nacional de Cién-
cia e Tecnologia dos Hymenoptera Parasitoides da Regiao Sudeste (INCT-HYMPAR/
SUDESTE) (CNPq, FAPESP, CAPES).The third author was supported by a fellow-
ship from the Richard Gilder Graduate School; a “mini-ARTS” award by the Society
of Systematic Biologists; a Doctoral Dissertation Improvement Grant by the National
Science Foundation (Award # 1501802) and an Annette Kade Graduate Student Ex-
change Fellowship Program by the American Museum of Natural History. We are
grateful to the editor and the two reviewers for their appropriate and constructive sug-
gestions to improve the paper.

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