JHR 93: 139-149 (2022) or JOURNAL OF > 4?eerteewed open-access Jourel

doi: 10.3897/jhr.93.93865 RESEARCH ARTICLE () Hymenopter a
.

https://jhr.pensoft.net The Inarasional Sociry of Hymenopeeriss, RESEARCH

Description of the nest of the pollen wasp
Celonites jousseaumei Du Buysson, 1906
(Hymenoptera, Vespidae, Masarinae) with a new
host association of the cuckoo wasp Spintharina innesi
(Du Buysson, 1894) (Hymenoptera, Chrysididae)

Volker Mauss', Christophe Praz*, Andreas Miiller?, Rainer Prosi*, Paolo Rosa°

I Staatliches Museum fur Naturkunde, Abt. Entomologie, Rosenstein 1, D-70191 Stuttgart, Germany
2 University of Neuchatel, Institute of Biology, Emile-Argand 11, 2000 Neuchatel, Switzerland 3 ETH Ziirich,

Institute of Agricultural Sciences, Biocommunication and Entomology, Schmelzberestrafse 9/LFO, CH-8092
Ziirich, Switzerland 4 Lerchenstraffe 81, D-74564 Crailsheim, Germany 5 Laboratory of Zoology, Institute of
Biosciences, University of Mons, Place du Parc, 20, 7000 Mons, Belgium

Corresponding author: Volker Mauss (volker.mauss@gmx.de)

Academic editor: Michael Ohl | Received 23 August 2022 | Accepted 19 October 2022 | Published 31 October 2022
Attps://zoobank. org/DC5B62DF-3F6C-4D86-9E9F-018369FD6E7F

Citation: Mauss V, Praz C, Miiller A, Prosi R, Rosa P (2022) Description of the nest of the pollen wasp Celonites
jousseaumei Du Buysson, 1906 (Hymenoptera, Vespidae, Masarinae) with a new host association of the cuckoo wasp
Spintharina innesi (Du Buysson, 1894) (Hymenoptera, Chrysididae). Journal of Hymenoptera Research 93: 139-149.
https://doi.org/10.3897/jhr.93.93865

Abstract

Two nests of Celonites jousseaumei are described in detail from the Antiatlas in Morocco. The nests con-
sisted of two or three linearly arranged earthen brood cells that were attached to the almost vertical
surface of medium sized stones. The brood cell provisions consisted exclusively of Heliotropium pollen
(Boraginaceae). Species affiliation of developmental stages by DNA barcoding revealed that one of the

brood cells contained a pupa of Spintharina innesi in a cocoon.

Keywords

brood parasitism, COI-5P, nest construction, Palaearctic

Copyright Volker Mauss 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.

140 Volker Mauss et al. / Journal of Hymenoptera Research 93: 139-149 (2022)

Introduction

The knowledge about nest architecture of the more than 40 Palaearctic species of the
pollen wasp genus Celonites is fragmentary. Detailed nest descriptions are only available
for Celonites abbreviatus (Villers, 1789) (Ferton 1901, 1910; Bellmann 1984, 1995),
Celonites tauricus Kostylev, 1935 (Mauss et al. 2016) and Celonites fischeri Spinola,
1838 (Mauss and Miller 2014), which are all members of the C. abbreviatus-group
of the subgenus Ce/onites s.str. In contrast, information about nesting in the subgenus
Eucelonites Richards, 1962 is not available despite a short note by Richards (1962: 224)
concerning two specimens of Celonites (Eucelonites) jousseaumei senegalensis Richards,
1962 from Bambey, Senegal that “had pinned with them some mud cells which from
their shape must have been attached end to end, longitudinally, on a plant-stem. The
cells were approximately 9.0 mm long and 3.5 mm in diameter”. During a field trip to
Morocco in 2019 two nests of Celonites (Eucelonites) jousseaumei were discovered that
are described in the present paper.

Materials and methods

The nests were found and dissected on the 19" of April 2019. Outer cell dimensions
were measured using a calliper rule (accuracy 0.1 mm), inner cell dimensions were
reconstructed from macro photos. All brood cells were dissected with fine tweezers
(Dumont INOX No. 5 Biologie, No. 7 and spring steel tweezers) using a combination
of two reading glasses that provided a sufficient magnification. Photos were taken with
a Canon EOS 70D or 80D camera with a 50 mm or 100 mm macro lens (scale up
to 1:1, resolution 20 or 24 mega pixel) and macro flash-lights. Dry specimens of all
Celonites species were labelled with an individual, serial database number (dbM = data-
base Mauss) printed on the determination label and placed in the collection of Volker
Mauss (C. jousseaumei 14 dbM 5402 19 dbM 5386; C. pictus 52 dbM 5385, 5398—
5401). Specimens of all plant species that were visited by pollen wasps were collected
and preserved dried. The material was placed in the herbarium of the State Museum of
Natural History in Stuttgart (Herbarium STU).

Pollen samples from brood cell provisions were prepared using the method out-
lined by Westrich and Schmidt (1986). The content of each provision was distributed
over two or three slide preparations. ‘The different pollen types were ascertained under
a light microscope at magnifications of 400x and determined to generic level with the
aid of a reference collection. For each slide all pollen grains were determined along
three randomly chosen lines transversal to the cover glass.

12 Celonites jousseaumei (dbM 5421 [BOLD process ID: CECYP002-20]) and
12 Celonites pictus (dbM 5422 [CECYP004-20]) from the nest locality, as well as
the pupa from cell B2 [CECYP001-20] and the larva from cell N1 [CECYP003-20]
from the brood cells were preserved in 96% pure ethanol for DNA barcoding. For

Description of the nest of Celonites jousseaumei 141

further reference, the barcoding fragment of the mitochondrial gene was sequenced
from 14 (dbM 4320 [AIMEJ011-20]), 42 (dbM 4319 [AIMEJ010-20], dbM 5590
[CECYP035-22], dbM 5592 [CECYP036-22], dbM 5594 [CECYP037-22]) of
C. jousseaumei, and 14 (dbM 5117 [AIMEJ013-20]), 19 (dbM 4322 [AIMEJ012-20])
of Celonites afer from different localities in Morocco. To facilitate identification of
possible cuckoo wasp nest parasites, we barcoded dry specimens of six chrysidid wasps
morphologically close to Spintharina that had been collected at four localities in
Morocco between 2011 and 2019 identified as Spintharina procuprata (Linsenmaier,
1959) [CECYP022-22], Spintharina innesi (du Buysson, 1894) [CECYP023-22,
CECYP024-22, CECYP025-22, CECYP026-22] and Chrysis patruela Linsenmaier,
1999 [CECYP027-22]. Species identification was based on morphological characters
of the imagines. DNA barcoding followed standard methods of DNA extraction
from a single leg of dry specimens or specimens collected and stored in 96% pure
ethanol. The barcoding fragment of the gene Cytochrome Oxidase subunit 1 (COI-
5P) was amplified in PCR using the universal primers LepF and LepR (Hebert et
al. 2004). Sequencing was performed bi-directionally using the same primers and
the resulting chromatograms were edited in Geneious 6.0.6 (Kearse et al. 2012).
DNA barcoding of the additional reference specimens that had not been collected
at the nest site was accomplished by AIM Advanced Identification Methods GmbH
Leipzig. All nucleotide sequences were uploaded and analysed using the BOLD
database (https://www.boldsystems.org). Another four public COI-5P sequences
of two taxa of Spintharina were added from the BOLD database. Genetic distances
were computed using Kimura 2-parameter (K2P) distance model in a test version of
Paup 4.0 (Swofford 2002) kindly provided by D. Swofford. Finally, a species ID tree
was computed using the following parameters: distance model Kimura 2 Parameter;
pairwise deletion of positions containing gaps and missing data; minimum complete
overlap 0 bp; alignment with BOLD Aligner (Amino Acid based HMM); individual
nucleotide sequence length varied from 252 to 675 bp.

Results and discussion

Locality

Two nests of Celonites jousseaumei were found at Ait Daoud (WGS 84: 29°36.977'N,
08°59.009'W), 15 km south of Tafraout in the Antiatlas in Morocco, situated at a
height of 1140 m a.s.l. The climate of the area is arid with a mean annual precipita-
tion of 235 mm and a mean annual temperature of 16.6 °C (data from Tafraout, AM
ONLINE Project). The habitat consisted of a richly flowering roadside (Fig. 1b) with
adjacent former terraces of almond orchards that were left fallow since approximately
ten years because of increasing aridity (Fig. 1a). The stony area was heavily grazed and
somewhat polluted with rubbish, i.e. along little dry drainage channels.

142 Volker Mauss et al. / Journal of Hymenoptera Research 93: 139-149 (2022)

Figure |. a, b habitat of Celonites jousseaumei at Ait Daoud, 15 km south of Tafraout, Morocco a nest

site b foraging area C exterior view of nest B d, e stones used as base for nests of C. jousseaumei d nest N
e nest B.

Description of the nest of Celonites jousseaumei 143

In the area Celonites jousseaumei and C. pictus were recorded. Imagines of both spe-
cies were exclusively observed to visit flowers of Heliotropium crispum Desf. (number of
sightings at H. crispum flowers: C. jousseaumei 1¢ 39, C. pictus 662), although other
plants were flowering at the site, for example Cladanthus arabicus (L.) Cass., Centaurea
calcitrapa L., Pallenis spinosa (L.) Cass., Senecio glaucus subsp. coronopifolius (Maire) C.
Alexander (all Asteraceae), Echium horridum Batt. (Boraginaceae), Lotus sp. (Fabaceae)
and Convolvulus trabutianus Schweinf. & Muschl. (Convolvulaceae).

Nest site

Both nests were situated at the steep edge of a 0.5 m high terrace with an exposure of 70°
to the north (ENE) (Fig. 1a). The site was approximately 10 m away from large patches of
Heliotropium crispum flowering on the embankment of the road (Fig. 1b). Both nests were
attached to almost vertical surfaces of medium sized stones (Table 1, Fig. 1d, e), 6 cm and
29 cm respectively above the foot of the terrace. The distance between the nests was 75 cm.

Nest structure

The nests were made of fine clayey soil with a small proportion of tiny stones and consisted
of 2 or 3 cells (Table 1). The cells were arranged in a longitudinal row in which each
subsequent cell abutted with its basal end onto the apical end of the completed preceding
cell. The resulting almost vertical or diagonal linear construction was 15.5 mm or 20.9 mm
long, with the apical ends of the cells oriented downward (Figs 1c, 2a). An additional
nest covering was not present. This exclusively linear arrangement of the brood cells is
in congruence with the fragmentary nest description of Celonites jousseaumei senegalensis
by Richards (1962). Linearly arranged brood cells were also observed in a few nests of
C. abbreviatus (Lichtenstein 1869) and C. fischeri (Mauss & Miiller, 2014), but in these
nests at least a single cell was also attached longitudinally to the others in addition. Moreover,
in most nests of C. abbreviatus (Bellmann 1984) and C. fischeri (Mauss & Miiller, 2014)
the cells are only attached longitudinally to each other, which is also the case in all of the
few known nests of other members of the C. abbreviatus-group, in particular C. tauricus
(Mauss et al. 2016) and C. mayeti Richards, 1962 (Lichtenstein 1875). Therefore, the

observed exclusively linear arrangement of the brood cells of C. jousseaumei is of note.

Table |. Parameters of two nests of Celonites jousseaumei recorded at Ait Daoud, Morocco.

Nest Condition Height above Orientation to Nest substrate Xcells Contact between Nest
ground (cm)' __ the North (°) adjacent cells covering
B sealed, 29 70 stone (base 18x23 cm, 2 linear absent
current season height 10 cm)
N sealed, 6 0 stone (base 17x7 cm, 3 linear absent
current season height 10 cm)

‘measured from the lowest part of the nest to the foot of the terrace.

144 Volker Mauss et al. / Journal of Hymenoptera Research 93: 139-149 (2022)

The brood cells were cylindrical with almost parallel sides, rounded at the basal
and truncate at the apical end (Fig. 2b, c). The median dimensions of the cells were:
outer length 7.3 mm (n = 5), outer diameter 3.6 mm (n = 5), inner length 6.3 mm
(n = 4), inner diameter at the cell opening 3.4 mm (n = 4) (Table 2). The outer cell
surface showed a distinct “fish scale” pattern (Figs 1c, 2a) while the inner surface was
smooth (Fig. 2c). Towards the stone it was attached to, the cell wall was not completely
constructed resulting in a few spots in the median axis where the surface of the stone
formed the boundary of the cell (Fig. 2c). The outer cell wall continued between ad-
jacent cells laterally covering the small hollow space between them that resulted from
the existence of two separate cell walls that is the transversal apical wall of the basal
cell and the rounded basal wall of the apical cell (Fig. 2b, c). At the apical end of the
nest the outer wall of the last cell was produced into a small rim protruding the api-
cal transversal cell wall by 2.1 mm (Fig. 2b). The wall of the rim had one or two deep
notches and was slightly bent outwards (Fig. 1c). Within this short tube-like entrance,
the nest was sealed by a circular, curved, circa 0.2-0.3 mm thick mud plug (Fig. 2b).
This nest seal was positioned about 0.2 mm above the apical wall of the last cell and 1
mm inwards from the edge of the nest opening resembling the bottom of a new cell in
form, position and structure.

Brood cell content

The content of the brood cells is summarized in Table 2. The provision consisted of a
yellowish-white, viscous pollen mass with shining surface forming a pollen loaf. The
surface of the loaf was characteristically papillated (Fig. 2b) so that it barely touched
the cell walls. Between the apical end of the pollen loaf and the apical wall of the cell
remained a hollow space measuring approximately 0.8—0.9 mm (Fig. 2b). Inwards the
pollen mass became more sticky and rather liquid, so that it could not be removed as a
whole with a pair of tweezers. The provision in the cells of both nests consisted exclu-
sively of Heliotropium pollen indicating narrow oligolecty (sensu Miiller and Kuhlmann
2008) of C. jousseaumei at this locality. Both eggs of Celonites jousseaumei were whitish
and curved. Each egg was situated on top of the provision close to the basal end of the
cell indicating that it was laid by the female prior to brood cell provisioning (Fig. 2b).
Small remnants of membranous material attached to one pole of each egg suggested
that the eggs had initially been attached to the wall. The small larva from cell N1 was
also situated basally on top of the pollen mass, where it fed on the provision (Fig. 2b).

Species identification

The COI-5P gene sequence of the larva from brood cell N 1 was 100% identical (distance of
0) to the sequence of a Celonites jousseaumei female [CECYP037-22] collected northeast
of Sidi Ifni at a distance of approximately 100 km from the nest site. Four additional
specimens of C. jousseaumei from Morocco were sequenced; the average within-species
genetic distance among these specimens was 0.51% (minimum 0, maximum 1.19). The

Description of the nest of Celonites jousseaumei 145

Figure 2. Structure of Celonites jousseaumei nest N on 19" of April: a exterior view b brood cells opened

in longitudinal direction ¢€ cell content removed. (N1—N3 = brood cell numbers; aw = apical cell wall;
bw = basal cell wall; e = egg; hs = hollow space below pollen loaf; | = larva; nr = nest rim; ns = nest seal;
p = pollen loaf; pa = papilla on surface of pollen loaf; s = bare stone surface; measurements and cell content
summarized in Table 2).

sequence of the larva from brood cell N1 to C. pictus [CECYP004-20] was 24.25%.
In the distance-based tree (Fig. 3), the larva N1 clusters together with the imagines
of C. jousseaumei. Therefore, it can be concluded that the recorded nests belong to
C. jousseaumei. This is in congruence with the cell dimensions that are too small for
C. pictus but match the size of C. jousseaumei (median total length of females 7.46 mm
(n = 8) in C. pictus versus 5.75 mm (n = 7) in C. jousseaumei).

146 Volker Mauss et al. / Journal of Hymenoptera Research 93: 139-149 (2022)

Table 2. Measurements and condition of brood cells from two nests of Celonites jousseaumei recorded at

Ait Daoud, Morocco.

Nest Cell Condition Outer cell Outer Inner cell Inner cell Content Species Pollen type
No. length cell width length width affiliation composition
(mm) (mm) (mm) (mm) of provision

B Bl sealed Cie) 3.5 5.8 2.8 yellowish-white pollen loaf, exclusively
dead dry larva Heliotropium!

B2 sealed 8.2 3.6 pupa in light yellowish cocoon Spintharina
innest
N N1 sealed Girl 3.6 6.4 3.3 yellowish-white pollen loaf, Celonites exclusively

small larva feeding on basalend jousseaumei Heliotropium!
of provision

N2 sealed 7.0 4.0 6.2 3.4 yellowish-white pollen loaf, exclusively
curved egg basally on top Heliotropium!
of provision
N3 sealed 7.9 37 Fd 3.4 yellowish-white pollen loaf, exclusively
curved egg basally on top Heliotropium!

of provision

‘at most very rarely with single pollen grains of other plant taxa.

The pupa from brood cell B2 turned out to belong to a species of Chrysididae, as
the obtained COI-5P gene sequence of the pupa closely matched the public sequences
of Spintharina versicolor Spinola, 1808 within BOLD database. However, the identity of
the sequences was only 92%, indicating that the pupa belongs to a different but related
species. After additional sequencing of the reference chrysidid specimens from Morocco,
a match was found between the pupa and a specimen of Spintharina innesi collected in
Tizourgane [CECYP026-22] (Fig. 3). Three additional specimens of Spintharina innesi
were sequenced; the average within-species genetic distance was 0.71% (minimum
0.33, maximum 1.31). The genetic distances between the pupa from brood cell B2
and Spintharina procuprata or Chrysis patruela were 17.20% and 12.13%, respectively.
Therefore, it can be concluded that Celonites jousseaumei is a host of Spintharina innesi.
Host-parasite associations of Spintharina with Celonites seem to be common. In Europe
Spintharina versicolor has been recorded as a brood parasite of Celonites abbreviatus
(Bliithgen 1961; Erlandsson 1972), while in the Afrotropical Region Spintharina arnoldi
(Brauns, 1928) and Spintharina bispinosa (Mocsary, 1902) were reared from brood cells
of two different Ce/onites species (Brauns 1913; Gess 1996). Moreover, Pauli et al. (2019)
found a close phylogenetic relationship between Spintharina and the Nearctic Chrysurissa,
which also appear to parasitize exclusively pollen wasps. This phylogenetic placement
indicates that both genera are descendants of a last common ancestor which may already
have exploited pollen wasps as hosts, suggesting an old and exclusive association with
pollen wasps in this clade. However, the host specificity of numerous Spintharina species
is poorly known and it remains to be shown whether Spintharina innesi is restricted
to C. jousseaumei or if it may also parasitize brood cells of other species of Celonites or
even of other pollen wasp genera. Conversely, there are at least three other species of
Spintharina recorded from Morocco that are all suitable in size to fit the brood cells of
C. jousseaumei (cf. Linsenmaier 1999, classified as species of the Chrysis versicolor-group),
so that this pollen wasp may be parasitized by more than one Spintharina species.

Description of the nest of Celonites jousseaumei

147
Celonites jousseaumei CECYP036-22; 315bp
Celonites jousseaumei AIMEJO10-20; 623bp

Celonites jousseaumei AIMEJ011-20; 607bp

Celonites jousseaumei CECYP035-22; 316bp

Larva cell N1 CECYP003-20: 624bp

Celonites jousseaumei CECYP037-22; 316bp

elonites jousseaumei CECYP002-20; 624bp

Celonites afer AIMEJ012-20; 578bp
Celonites afer AIMEJ013-20; 623bp
Celonites pictus CECYP004-20; 624bp
Spintharina vagans GBMNB61592-20; 675bp
Pupa cell B2 CECYP001-20; 636bp
Spintharina innesi CECYP023-22; 320bp
Spintharina innesi CECYP026-22; 317bp
Spintharina innesi CECYP024-22; 267bp
Spintharina innesi CECYP025-22; 319bp
Spintharina versicolor SICOD049-19,; 658bp
pintharina versicolor GBMNB61735-20; 675bp
Spintharina versicolor GBAH0554-06; 615bp
Chrysis patruela CECYP027-22; 252bp
x8 Spintharina procuprata CECYP022-22; 257bp

Figure 3. Neighbour joining tree of COI-5P sequences of 9 imagines of Ce/onites (Masarinae) from

Morocco, 10 imagines of Spintharina (Chrysididae) and 2 immature stages collected from brood cells of
two Celonites nests from Morocco (see text for details).

148 Volker Mauss et al. / Journal of Hymenoptera Research 93: 139-149 (2022)

Acknowledgements

Annette Rosenbauer kindly identified the collected plants. Comments by Alexander
Fateryga and James Carpenter improved the manuscript.

References

AM ONLINE Project (2017) Climate-Data https://climate-data.org [retrieved 2 October 2017]

Bellmann H (1984) Beobachtungen zum Brutverhalten von Celonites abbreviatus Villers
(Hymenoptera, Masaridae). Zoologischer Anzeiger 212: 321-328.

Bellmann H (1995) Bienen, Wespen, Ameisen — Hautfliigler Mitteleuropas. Kosmos
Naturftihrer, Franckh-Kosmos Verlags-GmbH, Stuttgart, 336 pp.

Bliithgen P (1961) Die Faltenwespen Mitteleuropas (Hymenoptera, Diploptera). Abhandlungen
der Deutschen Akademie der Wissenschaften zu Berlin Klasse ftir Chemie, Geologie und
Biologie 2: 1-249. https://doi.org/10.1515/9783112537084

Brauns H (1913) Dritter Beitrag zur Kenntnis der Masariden (Hym.) von Siidafrika.
Entomologische Mitteilungen 2: 193-209. https://doi.org/10.5962/bhl.part. 14992

Erlandsson S (1972) Hymenoptera Aculeata from the European parts of the Mediterranean
Countries. Eos 48: 11-93.

Ferton C (1901) Notes détachées sur l’instinct des Hyménopteéres melliféres et ravisseurs avec
la description de quelques espéces. Annales de la Société Entomologique de France 70:
83-148.

Ferton C (1910) Notes détachées sur Pinstinct des Hyménoptéres melliféres et ravisseurs. 6e
Série. Annales de la Société Entomologique de France 79: 145-178.

Gess SK (1996) ‘The pollen wasps — Ecology and natural history of the Masarinae. Harvard
University Press, Cambridge, Massachusetts, 340 pp. https://doi.org/10.4159/
harvard.9780674281684

Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one:
DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes
fulgerator. Proceedings of the National Academy of Sciences 101: 14812-14817.
https://doi.org/10.1073/pnas.0406166101

Kearse M, Moir R, Wilson A, Stones-Havas S$, Cheung M, Sturrock S, Buxton S, Cooper A,
Markowitz S, Duran C, Thierer T, Ashton B, Meintjes PR. Drummond A (2012) Geneious
Basic: an integrated and extendable desktop software platform for the organization and
analysis of sequence data. Bioinformatics 28: 1647-1649. https://doi.org/10.1093/
bioinformatics/bts199

Lichtenstein J (1869) No title. Annales de la Société Entomologique de France (4) 9 Bulletin
entomologique: XXIX.

Lichtenstein J (1875) No title. Annales de la Société Entomologique de France (5) 5 Bulletin
entomologique: CCX, CCXI.

Linsenmaier W (1999) Die Goldwespen Nordafrikas (Hymenoptera, Chrysididae).
Entomofauna, Zeitschrift fir Entomologie Supplement 10: 1-281.

Description of the nest of Celonites jousseaumei 149

Mauss V, Fateryga AV, Prosi R (2016) Taxonomy, distribution and bionomics of Celonites tauricus
Kostylev, 1935, stat. n. (Hymenoptera, Vespidae, Masarinae). Journal of Hymenoptera
Research 48: 33-66. https://doi.org/10.3897/JHR.48.6884

Mauss V, Miiller A (2014) First contribution to the bionomics of the pollen wasp Celonites fischeri
Spinola, 1838 (Hymenoptera, Vespidae, Masarinae) in Cyprus. Journal of Hymenoptera
Research 39: 119-153. https://doi.org/10.3897/JHR.39.7841

Miller A, Kuhlmann M (2008) Pollen hosts of western palaearctic bees of the genus Colletes
(Hymenoptera: Colletidae): the Asteraceae paradox. Biological Journal of the Linnean
Society 95(4): 719-733. https://doi.org/10.1111/j.1095-8312.2008.01113.x

Pauli T, Castillo-Caja RE Rosa P, Kukowka S, Berg A, van den Berghe E, Fornoff F,
Hopfenmiiller S, Niehuis M, Peters R, Staab M, Strumio EF, Tischendorf S, Schmitt T,
Niehuis O (2019) Phylogenetic analysis of cuckoo wasps (Hymenoptera: Chrysididae)
reveals a partially artificial classification at the genus level and a species-rich clade of bee
parasitoids. Systematic Entomology 44: 322-335. https://doi.org/10.1111/syen.12323

Richards OW (1962) A revisional study of the masarid wasps (Hymenoptera, Vespoidea).
British Museum (Natural History), London, 294 pp.

Swofford DL (2002) PAUP 4.0 Phylogenetic Analysis using Parsimony (and other Methods).
Version 4. Sinauer Associates, Sunderland.

Westrich P, Schmidt K (1986) Methoden und Anwendungsgebiete der Pollenanalyse bei
Wildbienen (Hymenoptera, Apoidea). Linzer biologische Beitrage 18: 341-360.
https://doi.org/10.1051/apido: 19870209