Boletín de la Sociedad Zoológica del Uruguay, 2022
Vol. 31 (2): e31.2.2
ISSN 2393-6940
https://journal.szu.org.uy
DOI: https://doi.org/10.26462/31.2.2
ABSTRACT
The flat wasps Bethylidae are the largest family of
Chrysidoidea. Because of their undeniable ecological
contribution, these insects are also important due to their
potential use as biological controllers of Coleoptera and
Lepidoptera that act as agricultural pests. This is the first
study focused on the diversity of Bethylidae in Uruguay
and the attempt to get to know the Bethylidae fauna of this
country. They were collected from three environments,
natural field area (NFA), pasture system area (PSA),
integrated livestock production system with winter and
summer agriculture (IAAa and IAAb) near Castillos,
Rocha Department, Uruguay, between December 2014
and December 2016. A total of 682 bethylids were
collected, representing four subfamilies and 13 genera, of
which one subfamily (Scleroderminae) and eight genera
(Nothepyris, Plastanoxus, Cephalonomia, Allobethylus,
Aspidepyris, Chlorepyris, Laelius and Dracunesia) were
first registered for Uruguay.
Key words: flat wasps, Neotropical, parasitoid wasps,
South America
RESUMEN
Composición genérica de Bethylidae (Hymenoptera,
Chrysidoidea) del Este del Uruguay. Las avispas
planas Bethylidae son la familia más grande de
Chrysidoidea. Por su innegable contribución ecológica,
estos insectos también son importantes por su potencial
uso como controladores biológicos de Coleoptera y
Lepidoptera que actúan como plagas agrícolas. Este es el
primer estudio centrado en la diversidad de Bethylidae en
Uruguay. En este estudio, en un intento de conocer la
fauna de Bethylidae de este país, se colectaron de tres
ambientes, área de campo natural (NFA), área del
sistema de pastos (PSA), sistema integrado de
producción ganadera con agricultura de invierno y verano
(IAAa e IAAb), cercanos a Castillos, Departamento de
Rocha, Uruguay, entre diciembre de 2014 y diciembre de
2016. Se recolectaron 682 betilidos, que representan
cuatro subfamilias y 13 géneros, de los cuales una
subfamilia (Scleroderminae) y ocho géneros (Nothepyris,
Plastanoxus, Cephalonomia, Allobethylus, Aspidepyris,
Chlorepyris, Laelius y Dracunesia) fueron registraron por
primera vez para Uruguay.
Palabras clave: avispas plana, avispas parasitoide,
Neotropical, Sudamerica.
INTRODUCTION
Bethylidae (Hymenoptera, Chrysidoidea) are a
cosmopolitan and very diverse family of parasitoid
wasps, especially in tropical areas (Azevedo et al.,
2018). The family has about 3,000 species, belonging
to 100 genera in nine subfamilies (Azevedo et al., 2018;
Colombo et al., 2020). These wasps exhibit a
fascinating diversity in their parasitoid behavior, with a
great uniformity for their hosts: beetle larvae
Bol. Soc. Zool. Uruguay (2ª época). 2022. ISSN 2393-6940Vol. 31 (2): e31.2.2
GENERA COMPOSITION OF BETHYLIDAE (HYMENOPTERA, CHRYSIDOIDEA) FROM EASTERN
URUGUAY
1* 1 2* 1
Wilson J. Marques Jr. , Gustavo K. Campos , Wesley D. Colombo , Isabel D. C. C. Alencar ,
3 3 4 2
Nelson W. Perioto , Rogéria I. R. Lara , Enrique Castiglioni & Celso O. Azevedo
1Instituto Federal de Educação, Ciência e Tecnologia do Espírito Santo. Av. Vitória, 1729, 29040-780, Vitória,
ES, Brazil.
2Universidade Federal do Espírito Santo, Departamento de Ciências Biológicas. Av. Fernando Ferrari, 514,
29075-910, Vitória, ES, Brazil.
3 Instituto Biológico, Laboratório de Sistemática e Bioecologia de Predadores e Parasitoides. Av. Bandeirantes,
2419, 14030-670, Ribeirão Preto, SP, Brazil.
4 Universidad de la República, Centro Universitario Regional del Este. Ruta Nacional nº 9 intersección con
Ruta Nacional nº 15, Rocha, Uruguay.
*Corresponding authors: wilsonjmarquesj@gmail.com; wesleycolombo@gmail.com
Fecha de recepción: 21 de enero de 2022
Fecha de aceptación: 26 de setiembre de 2022
2
MARQUES, W. Jr. et al.
(Coleoptera) are the hosts in Pristocerinae,
Scleroderminae, Mesitiinae and most Epyrinae, and
small moths (Lepidoptera) in Bethylinae and the
remaining Epyrinae (Evans, 1964; Gauld and Bolton,
1988; Gordh and Móczár, 1990; Azevedo et al., 2018).
Bethylidae could be of agricultural importance as
biocontrols and have already been used successfully in
limited cases – for example Goniozus legneri Gordh
(Legner and Silveira-Guido, 1983) and Prorops nasuta
Waterston (Infante et al., 2005) for control of navel
orangeworm and coffee borer beetle, respectively.
Even though it is one of the most diverse lineages of
Chrysidoidea, few studies report the abundance and
richness of Bethylidae (Mugrabi et al., 2008). Studies
within the Neotropical Region are mostly from Brazil:
Azevedo (1991) for São Paulo; Azevedo (1996) for
Mato Grosso; Azevedo and Helmer (1999) for Brasília;
Azevedo et al. (2002) for Acre; Azevedo et al. (2006) for
several sites in Paraná, and Mugrabi et al. (2008) for
Espírito Santo. So, there exists an evident gap about
the bethylids in many regions of the Neotropics.
In Uruguay, the invertebrate diversity is much less
studied and known than the vertebrate fauna (Ghione
et al., 2008). However, some studies were performed
with Hymenoptera and a great diversity for these
groups was recorded (see Zolessi et al., 1989;
Castiglioni et al., 2017; Fernandes et al., 2019). The
country is subject to extreme loss of habitat. In just a
few decades, several regions of Uruguay have lost
their natural ecosystems to agriculture (Ghione et al.,
2008), and for this reason, studies focused on the local
fauna are important and necessary.
For Bethylidae, a total of three subfamilies, five
genera, and only seven species have been recorded
for Uruguay hitherto: Goniozus legneri (Gordh, 1982)
and Goniozus negrifemur (Ashmead, 1894)
(Bethylinae), Anisepyris proteus (Evans, 1966a),
Anisepyris durini (Barbosa and Azevedo, 2018) and
lautus (Evans, 1977) (Epyrinae),
Pseudisobrachium uruguayense (Oglobin, 1938) and
Dissomphalus connubialis (Evans, 1966b)
(Pristocerinae).
In this study, we evaluated the diversity and generic
composition of Bethylidae in three environments, NFA,
PSA, IAAa and IAAb. This is the first study focused on
the diversity of Bethylidae in Uruguay.
MATERIALS AND METHODS
The specimens studied were collected in four
localities, near Castillos, Department of Rocha,
Uruguay, between December 2014 and December
2016, using Malaise traps. The studied environments
Rysepyris
Fig. 1. Collection points in the municipality of Castillos, Rocha Department, Uruguay. A. natural field area (NFA) (blue); B. pasture
system area (PSA) (purple); C. integrated livestock production system with winter and summer agriculture (IAAa) (green); integrated
livestock production system with winter and summer agriculture (IAAb) (red).
Bol. Soc. Zool. Uruguay (2ª época). 2022. ISSN 2393-6940Vol. 31 (2): e31.2.2
3Bethylidae from Uruguay
Fig. 2. Abundance of Bethylidae genera collected by subfamily: A. Pristocerinae; B. Scleroderminae; C. Epyrinae; D. Bethylinae. The sites are represented by colors: natural field area
(NFA) in blue; pasture system area (PSA) in purple; C. integrated livestock production system with winter and summer agriculture (IAAa) in green); integrated livestock production system
with winter and summer agriculture (IAAb) in red. Important to note each graphic is limited by the maximum number of specimens collected.
Bol. Soc. Zool. Uruguay (2ª época). 2022. ISSN 2393-6940Vol. 31 (2): e31.2.2
MARQUES, W. Jr. et al.
were: a) natural field area (NFA), 34°05'01.07''S,
53°45'43.08''W, altitude 57m; b) pasture system area
(PSA), 34°05'26.08''S, 53°52'14.04''W, altitude 89m,
and c) integrated agriculture area (IAA),
34°02'33.07''S, 53°50'02.07''W, altitude 26m (between
December 2014 and December 2015 (IAAa) and
34°24'42.02''S, 54°08'10.05''W, altitude 18m (between
January and December 2016 (IAAb)) (Fig. 1) (for more
details see Fernandes et al., 2019).
The bethylids were identified to genus level under a
stereomicroscope using the taxonomic keys proposed
by Azevedo et al. (2018).
The genera composition of Bethylidae in each
environment was performed using rarefaction curves
using RStudio® (R Core Team, 2015) by the script
described by Rossi (2011) and the abundance analysis
was performed using Excel® (Microsoft, 2022). To
verify the quality of the sampling in IAA, the data were
analyzed using the number of individuals for each
sampled location. The map was prepared using the
free website SimpleMappr® (Shorthouse, David P.)
and the graphics of abundance and diversity were
edited using image edition software.
RESULTS
A total of 682 specimens of Bethylidae were
collected representing 13 genera (~13% of the genera
diversity of Bethylidae) and four subfamilies. Five
genera of Epyrinae were obtained: Anisepyris Kieffer,
1905 (135 specimens/~20% of total of Bethylidae
collected), Aspidepyris Evans (13/~2%), Chlorepyris
Kieffer (5/~0.7%), Laelius Ashmead (7/~1%) and
Kieffer (1/~0.1%); three of Pristocerinae:
Pseudisobrachium Kieffer (264/~39%), Dissomphalus
Ashmead (187/~ 27%) and Dracunesia Alencar &
Azevedo (11/~1%); four of Scleroderminae:
Cephalonomia Evans (15/~2%, Allobethylus, Kieffer
(1/~0.1%), Nothepyris Evans (1/~0.1%) and
Plastanoxus Kieffer (1/~0.1%) and one of Bethylinae:
Goniozus Förster (41/~6%). Pseudisobrachium and
Dissomphalus were the most abundant genera,
representing ~66% of the sampled Bethylidae (Fig. 2).
Pseudisobrachium was the most abundant genus
in two of the three studied locations: ~43% (184
specimens) in NFA and ~40% (50 specimens) in PSA.
However, Dissomphalus was the most abundant in
IAAb with ~7% (50 specimens) and Goniozus was the
most abundant in IAAa, with ~3% (22 specimens) (Fig.
2). For the genera rarefaction curve, in IAA and PSA
the curve did not reach an asymptote and presented a
similar diversity. For NFA, there was also a tendency to
reach an asymptote (Fig. 3).
DISCUSSION
Dissomphalus and Pseudisobrachium were the
most abundant pristocerine genera and Anisepyris was
the most abundant Epyrinae genus, as was reported by
Mugrabi et al. (2008) in Atlantic Forest areas in Brazil.
Martins et al. (2020) studied the Chrysidoidea in
Rysepyris
4
Fig. 3. Diversity of Bethylidae genera by specimens.
Bol. Soc. Zool. Uruguay (2ª época). 2022. ISSN 2393-6940Vol. 31 (2): e31.2.2
5Bethylidae from Uruguay
conventional coffee crops and agroforestry systems in
Southeastern Brazil and reported Epyris as the most
abundant bethylid genus. However, this data is not
recovered here and a reason could be the taxonomic
key used by Martins et al. (2020), proposed by Vargas
and Terayama (2006) for genera of Bethylidae. The key
in Vargas and Terayama is outdated and not suitable for
identifying bethylids as the subfamily Epyrinae
included Scleroderminae genera when the key was
published.
The reported differences between the
environments reflect the differences in the level of
preservation of natural vegetation. The NFA is the most
preserved area, showing the biggest abundance and
diversity of the genera. The bethylids collected in the
other environments (IAA and PSA) can be associated
with agricultural pests. Goniozus was the genus most
abundant in IAAa and Dissomphalus was the most
abundant in IAAb, both areas with integrated
agriculture. Previous studies (Colombo and Azevedo,
2016; Martins et al., 2020) have recorded the
occurrence of these genera in areas with agriculture
and less preserved vegetation. The composition of
parasitoid wasps is affected by reducing the degree of
preservation of habitats and, consequently, availability
of hosts. Similar results have already been identified for
other Hymenoptera, for example, Ichneumonoidea
collected in the same areas of the present study
(Fernandes et al., 2019).
Malaise traps were the only method for sampling
and even with studies evaluating its efficiency in
sampling for Hymenoptera (see Noyes, 1989), the
result can be biased towards flying wasps. All females
of Pristocerinae, and some Scleroderminae, are
apterous and probably for this reason, no apterous
specimens have been collected. In this sense, the
generic diversity may have been affected by the
adopted sampling method.
More rigorous studies are needed regarding the
bethylid fauna in Uruguay. The present study resulted
in the first occurrence records for eight genera of
Bethylidae for that country: Nothepyris, Plastanoxus,
Cephalonomia, Allobethylus, Aspidepyris, Chlorepyris,
Laelius and Dracunesia. Greater sampling efforts and
deeper taxonomic studies will certainly cause
Uruguay's Bethylidae diversity to increase
considerably, which may be able to corroborate our
estimates.
ACKNOWLEDGEMENTS
The authors are grateful to anonymous reviewers
and the Subject Editor for providing valuable
suggestions and corrections on the final version of the
manuscript. We thank Karina S. Furieri for discussion
about statistical analysis and Carly M. Tribull for the
English review. This contribution was supported by the
Instituto Nacional de Investigación Agropecuaria of the
República Oriental del Uruguay (INIA) (Proyecto FTPA
312, Convocatoria 2012), INCT-Hymenoptera
Parasitoides CNPq grant #3037482018-4, FAPES
PRONEM #80600417/17 FAPES #157/2020 and
FAPES PRONEX #980/2022. WJMJ and GKC thanks
to Instituto Federal do Espírito Santo – Campus Vitória
for providing PIBIC-Jr bursary. COA is grateful for
research bursary to CNPq grant #3037482018-4. WDC
is grateful to FAPES/CNPq PROTAX grant #224/2021
for providing post-doctoral fellow bursary. The authors
declare no conflict of interest.
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