Parasitism in Theridion sp.

(Araneae: Theridiidae) by
Zatypota riverai Gauld, 1991 (Hymenoptera:
Ichneumonidae: Pimplinae)

Authors: Sobczak, Jober Fernando, Paiva Arruda, Italo Diego, de

Pádua, Diego Galvão, and Villanueva-Bonilla, German Antonio
Source: The Journal of Arachnology, 47(2) : 266-270
Published By: American Arachnological Society
URL: https://doi.org/10.1636/JoA-S-18-103

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 2019. Journal of Arachnology 47:266–270

SHORT COMMUNICATION

Parasitism in Theridion sp. (Araneae: Theridiidae) by Zatypota riverai Gauld, 1991

(Hymenoptera: Ichneumonidae: Pimplinae)

Jober Fernando Sobczak1, Italo Diego Paiva Arruda2, Diego Galvão de Pádua3 and German Antonio Villanueva-Bonilla4:
1
Instituto de Ciências Exatas e da Natureza, Universidade da Integração Internacional da Lusofonia Afro-Brasileira,
Rod. CE 060, Redenção, Ceará, Brazil. 2Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento
de Biologia, Universidade Federal do Ceará, 60440-900, Fortaleza, Ceará, Brazil. 3Programa de Pós-Graduação em
Entomologia, Instituto Nacional de Pesquisas da Amazônia - INPA, Manaus, Amazonas, Brazil. 4Universidade
Estadual de Campinas, Instituto de Biologia, Departamento de Biologia Animal, Rua Monteiro Lobato, 255,
Campinas, São Paulo, Brazil; E-mail: germanvillanueva9@gmail.com

Abstract. The hymenopteran genus Zatypota Förster, 1869 (Ichneumonidae: Pimplinae, Ephialtini) comprises highly
specialized koinobiont ectoparasitoids of spiders and is the largest genus of the Polysphincta group of genera in the world,
with more than 50 described species. The vast majority of species of Zatypota are parasitoids of the spider family
Theridiidae. In this study, we present information about a new interaction between the parasitoid spider wasp Zatypota
riverai Gauld, 1991 and the host spider Theridion sp. Walckenaer, 1805 (Theridiidae) with information about host weight
selection. We collected 102 non-parasitized adult and subadult females of Theridion sp. and six spiders with larvae of Z.
riverai attached to host’s abdomen. The pupal development takes about 8–11 days, though the development time of the
pupa varies with the sex of the wasp. All larvae collected in the field completed their life cycle on the host spiders, even
though all of the hosts were small, indicating that the host biomass was sufficient for larval development and no larger-
sized spiders are needed. Moreover, larger Theridion probably pose a greater risk because they are more likely to be
successful at wasp predation, even if they offer a greater resource to the larva.
Keywords: Biodiversity, Ephialtini, parasitoid wasps, Polysphincta group.

Spiders are among the most common and abundant predators of 1979) (Dictynidae) in the Holarctic. Recently, Sobczak et al.
terrestrial ecosystems (Turnbull 1973; Coddington & Levi 1991). In (2017a) described for the first time the male of Z. riverai Gauld,
this way, spiders constitute an important resource in the diet of many 1991, in addition to providing new information about this wasp
predators, parasites and also parasitoids (Gonzaga & Sobczak 2007). parasitizing the spider Anelosimus baeza Agnarsson, 2006 (Theri-
Ichneumonid wasps of the Polysphincta genus group (sensu Gauld & diidae) in Brazil.
Dubois 2006) (hereafter polysphinctine wasps) are well known to act The genus Theridion Walckenaer, 1805 (Theridiidae) is a cosmo-
exclusively as koinobiont ectoparasitoids of spiders (Gauld & Dubois politan group of spiders that currently consists of 586 described
2006). This monophyletic group is currently formed by 24 genera species (World Spider Catalog 2018). Theridion sp. is a small-sized
(Gauld & Dubois 2006; Palacio et al. 2007; Matsumoto 2016) with spider, with an orange brown cephalothorax, dark brown bands on
more than 200 species described (Yu et al. 2012). The host range of the legs and a lighter brown abdomen. Theridion sp. individuals do
these wasps is remarkably narrow and often species-specific; some not construct webs, but build a shelter made with a leaf and silk. The
polysphinctine genera (e.g., Hymenoepimecis, Acrotaphus) usually leaf is wrapped by silk threads and remains suspended, close to the
attack orb-weaver spiders (Sobczak et al. 2014; Pádua et al. 2016), ground, by silk threads in the vegetation. Inside this refuge, the spider
whereas others are specialized on spiders that construct three- deposits up to four egg sacs and provides maternal care. Currently
dimensional webs (e.g., Zatypota) (e.g., Korenko & Pekár 2011; there are some records of species of Theridion being parasitized by
Fritzén 2014). Zatypota wasps in the temperate (Fitton et al. 1987; Gauld & Dubois
The genus Zatypota Förster, 1869 comprises highly specialized 2006) and Neotropical region (Weng & Barrantes 2007; Barrantes et
koinobiont ectoparasitoids of spiders and is the largest genus of the al. 2008). In this study, we present new information about the biology
polysphinctine wasps in the world, with more than 50 described of a new interaction between the parasitoid spider wasp Zatypota
species (Yu et al. 2012; Korenko 2017). The vast majority of species riverai and the host spider Theridion sp. (Theridiidae) with
of Zatypota are parasitoids of spiders in the family Theridiidae information about host weight selection.
(Korenko & Pekár 2011; Korenko et al. 2011). There are only three This study was conducted in Mulungu, Ceará State, Brazil
Zatypota species that attack spiders of other families: (1) Zatypota (4818 0 40 00 S, 38858 0 05 00 W, altitude of 840 m) (Fig. 1A), a municipally
sulcata Matsumoto, 2010 associated with the sheet-web spider in the APA (Área de Proteção Ambiental) of the Maciço de Baturité.
Turinyphia yunohamensis (Bösenberg & Strand, 1906) (Linyphiidae) This area, considered a biodiversity hotspot, is peculiar because it
in Japan (Matsumoto & Takasuka 2010); (2) Zatypota picticollis forms an island of mountainous, semideciduous tropical forest
(Thomson, 1888) associated with the orb-web spiders Mangora surrounded by a semi-arid region of Caatinga Biome. The mean
acalypha (Walckenaer, 1802), Cyclosa conica (Pallas, 1772), and annual temperature is 20.88 C, the mean annual rainfall is 1221 mm
Zilla diodia (Walckenaer, 1802) (Araneidae) in Europe (Korenko et (Araújo et al. 2007) and the humidity is 50%, showing diel variation
al. 2015); and (3) Zatypota anomala (Holmgren, 1860) associated (Sobczak et al. in prep.). This area is an important locale for studies
with cribellate tangle-web spiders of the genus Dictyna Sundevall, involving the interaction between polysphinctine wasp groups of the
1833 (Korenko 2017) and Mallos pallidus (Banks, 1904) (Vincent Brazilian Northeast.
266

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 SOBCZAK ET AL.—THERIDION–ZATYPOTA INTERACTION 267

then classified into three types based on the recorded weight (small,
medium, large). To evaluate if host weight selection exists, we
performed a Chi-square test to compare the total availability of
spiders in each weight class with the total parasitized spiders. For
this test, the P-value was calculated using the Monte Carlo
simulation (Hope 1968) with 5000 replicates. Later, to evaluate if
differences exist in the development time between females and males
of the parasitoid wasp, we used a T test. We used the free software R
(R Core Team 2016) with the package ‘‘rmngb’’ and an alpha value
of 0.05 for the analyses.
Digital images of adult wasp and cocoon were taken using a
DMC4500 digital camera attached to a Leica M205A stereomicro-
scope and combined by using the software Leica Application Suite
V4.10.0. In the field, the digital images were taken using a Canon EOS
6D digital camera with a 105 mm macro lens.
The parasitoid specimens that emerged from the cocoons were
fixed in alcohol 70% and refrigerated. Voucher specimens of the
parasitoid were deposited in the Invertebrate Collection of Instituto
Nacional de Pesquisas da Amazônia (INPA, curator M. L. Oliveira).
The spider was identified by Dr. Antonio Brescovit, and it was
deposited in Laboratório Especial de Coleções Zoológicas in Instituto
Butantan, São Paulo (IBSP, A.D. Brescovit, curator).
We collected 102 unparasitized adult and subadult Theridion sp.
and six parasitized adult females of Theridion sp. with first instar (Fig.
1B) or second instar (Fig. 1C) larvae of Z. riverai attached to the
lateral portion of their abdomens.
No parasitized spider had more than a single larva of Z. riverai
(Fig. 1D). Larvae were located from the posterior to the anterolateral
dorsal section of the abdomen. The last larval instar (Fig. 1E) has
eight dorsal retractile tubercles, each with several hooks on its surface.
The larva is capable of retracting each tubercle inside its body
independently. When it reaches this last instar, the larva continues
consuming the hemolymph of the host and increases near three times
its size. Host death occurs within the leaf that was previously used as
a shelter.
After killing the host, the larva discarded the spider carcass and
started to construct the cocoon using the tubercle hooks to affix its
body to the silk wall, attached to the inner surface of the sheet that
the spider used as shelter. The larva performed repetitive back and
forth movements with the head adding silk strands between the leaf
walls and the center of the leaf. The total time of cocoon
construction lasted about 12 hours. The cocoon remained upright
and attached to the shelter leaf. Soon after the construction, the
cocoon acquired a light-yellow color (Fig. 1F), turning dark orange
Figure 1.—Studied area and adult female of Theridion sp. after two days.
(Theridiidae) parasitized by Zatypota riverai Gauld, 1991 (Ichneu-
The pupal stage lasted 8–11 days. However, we observed that the
monidae: Pimplinae). (A) Semideciduous tropical forest in Mulungu,
development time of the pupa varies with the sex of the wasp. Most of
Ceará State, Brazil; (B) Larval instar I of the wasp adhering to the
the females (n ¼ 3) emerged after 11 days, while males (n ¼ 2) emerged
abdomen of a spider accompanying an egg sac; (C) Larval instar II;
in eight days (T¼ 6.862, df ¼ 2.8698, P ¼ 0.007295). Adult wasps
(D) Larval instar III; (E) Larval instar IV; (F) Adult attacking the
emerged (Fig. 1G) by cutting the silk threads of the apical portion of
host; (G) Adult of Z. riverai; (H) Empty cocoon.
the cocoon (Fig. 1H). The adult hymenopteran stayed in the cocoon
web for approximately one hour (n ¼ 2), stretching its wings before
flying. All the wasps emerged from the cocoon under temperatures
Adult females of Theridion sp. with larvae of Z. riverai attached to higher than 258 C.
the abdomen, as well as unparasitized adults and subadults, were The weights of the 108 spiders recorded were from 0.0007 to 0.0351
located on trails inside the forest in October of 2017 in ‘‘sı́tio grams. Based on the frequency of distribution of these weights (Fig.
Gameleiras’’ in the municipality of Mulungu. The parasitized 2A), spiders between 0.0007 and 0.0133 grams would correspond to
spiders collected were kept in plastic containers (8 3 10 3 10 cm) small spiders; spiders between 0.014 and 0.0266 grams are medium;
that were sealed with a thin screen. The spiders were fed daily with and spiders weighing more than 0.0267 grams would be large spiders.
Drosophila sp. flies and a nutrient solution (Zanata & Vasconcellos- The six parasitized spiders had weights between 0.0055 and 0.0122
Neto, unpublished data). In the laboratory, all parasitized and non- grams, placing them in the ‘‘small’’ class. There were no significant
parasitized spiders were weighed on an analytical balance before differences between the observed and expected value of parasitized
they were fed (Gonzaga & Sobczak 2011). To determine the weight spiders in the three weight classes (X2: 0.582; P ¼ 0.7473; in 5000
of the parasitized spiders, the weight of a first or second instar Z. simulations; Fig. 2B).
riverai larva (previously determined; unpublished data) was sub- Unfortunately, in the Theridion – Z. riverai interaction, we did not
tracted from the weight of the parasitized spiderþlarva. Spiders were observe differences between modified webs and normal webs in the

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 268 JOURNAL OF ARACHNOLOGY

Figure 2.—Individuals of Theridion sp. (Theridiidae) collected in field. (A) Frequency and weight range of Theridion sp. individuals; (B)
Observed and expected frequencies of Theridion sp. parasitized by Zatypota riverai Gauld (Ichneumonidae: Pimplinae).

field. In fact, in the interaction Anelosimus baeza–Z. riverai, the Pimplinae) parasitizing Achaearanea tingo Levi, 1963 (Theridiidae)
general structure of the modified web was apparently similar to the (Sobczak et al. 2017b). As mentioned by other authors, the
normal web, but with greater amount of silk strands in the central significance of the larva’s placement on the host spider is still unclear,
part of the modified web (Sobczak et al. 2017a). but it may be useful in identifying the parasitoid taxon (Sobczak et al.
The placement of the larva of Z. riverai is quite similar to that of 2017a).
larvae of other Zatypota species, such as Z. petronae Gauld, 1991 on Biological aspects of parasitic wasp larvae such as larval
Theridion evexum Keyserling, 1884 and Z. riverai on A. baeza (Weng development time or the time required to construct the pupae,
& Barrantes 2007; Sobczak et al. 2017a). The head of the larva points unfortunately, are not always recorded due to larval or spider
toward the posterior part of the spider’s abdomen in all of these mortality. In our study, we were able to record the pupal development
species, as well as Flacopimpla varelae Gauld, 1991 (Ichneumonidae: time (8–11 days) which was not different from that recorded for Z.

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 SOBCZAK ET AL.—THERIDION–ZATYPOTA INTERACTION 269

anomala (nine days on average) (Korenko 2017) and for Z. the orb-weaver spider Argiope argentata (Araneae: Araneidae) by
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