Polysphinctine wasps of the genus Hymenoepimecis act as koinobiont ectoparasitoids of orb-weaver spiders. Hymenoepimecis japi is already known to parasitize the tetragnathid spider Leucauge roseosignata. Here, we record the dome-weaver spider Mecynogea biggiba as a second host for H. japi, as well as the behavioral manipulations induced by the parasitoid. We found that H. japi alters the web construction behavior of M. biggiba, resulting in a complex three-dimensional cocoon web. This modified web differs from that of L. roseosignata, which is a simpler structure composed of a few support threads. Our finds add to the literature the first case of a Hymenoepimecis species parasitizing spiders of two distinct families.

Cocoon web, parasitoid wasp, Polysphincta genus-group, polysphinctine, Serra do Japi

Spider-wasp interactions are considered a hot topic in the understanding of behavioral manipulation, since some parasitoid wasps can improve their own survival by inducing the host spiders to construct a modified web or “cocoon web” (Eberhard 2000a, b). Several studies have described behavioral manipulations of spiders by the clade of koinobiont ectoparasitoid wasps of the Polysphincta genus-group (hereafter polysphinctine wasps) (Ichneumonidae: Pimplinae) (Gonzaga and Sobczak 2007, 2011, Matsumoto 2009, Korenko and Pekár 2011, Eberhard 2013, Sobczak et al. 2014, Kloss et al. 2016). Eberhard (2010) proposed that psychotropic substances released by wasp larva are the driving force behind behavioral manipulations of host spiders, but no additional studies have confirmed this hypothesis. Thus, every new record focused on spider-polysphinctine interactions is of value to comprehend the mechanism of behavioral manipulation induced by wasps.

Within polysphinctine wasps, the Neotropical genus Hymenoepimecis Viereck, 1912 is probably the most studied with respect to interactions with host spiders (Pádua et al. 2016). These parasitoid wasps are known to attack spiders of five genera, namely: Nephila (Araneidae; Finke et al. 1990, Gauld 1991, 2000, Gonzaga et al. 2010), Leucauge (Tetragnathidae; Gauld 1991, Eberhard 2000a, 2001, Sobczak et al. 2009, Eberhard 2013, Pádua et al. 2016), Cyrtophora (Araneidae; Gauld 2000), Araneus (Araneidae; Gonzaga and Sobczak 2007, Sobczak et al. 2011, Sobczak et al. 2012, 2014) and Manogea (Araneidae; Sobczak et al. 2009). Until now, 12 of the 20 valid-species of Hymenoepimecis are confirmed to be capable of parasitizing subadult and adult orb-weaving spiders (summarized in Pádua et al. 2016) and inducing their hosts to construct a variety of cocoon web designs, from simple two-dimensional to complex three-dimensional tangles of non-sticky threads.

On current understanding, Hymenoepimecis-spider interactions are frequently species-specific, with an exception in H. veranii Loffredo & Penteado-Dias, 2009 that parasitizes two congeneric and sympatric araneid spiders Araneus omnicolor (Keyserling, 1893) and A. orgaos Levi, 1991 (Gonzaga and Sobczak 2007, Sobczak et al. 2014). Our study species, Hymenoepimecis japi Loffredo & Penteado-Dias, 2009 (male described by Sobczak 2012), is known to parasitize the orb-weaver spider Leucauge roseosignata Mello-Leitão, 1943 (Tetragnathidae) (Sobczak et al. 2009). Through this parasitism, the spiders experience behavioral manipulation that results in the host constructing a cocoon web with a simple structure composed of a few strong radial lines and the absence of the sticky spirals that are characteristic of orb-weavers. Here we report a novel spider family parasitized by H. japi and describe the behavioral manipulations on Mecynogea biggiba Simon, 1903 (Araneidae) by the parasitoid wasp.

In total, we found four parasitized spiders, one adult male (body length = 5.2 mm) and two adult females (5 and 5.3 mm) in February plus one adult female (5.4 mm) in December 2010 (Fig. 2A–B). Hymenoepimecis japi completed its immature growth through three larval stages (Fig. 2A–C). The larvae remained attached dorsolaterally or anterodorsally on the host’s abdomen, feeding on the spider’s hemolymph through a small hole in its cuticle. The third (final) instar larvae presented eight dorsal tubercles with minute hooks, which will serve to hold the larva on the cocoon web (Fig. 2C–E).

Figure 2. 

Mecynogea biggiba parasitized by Hymenoepimecis japi. A Adult female spider and first instar larvae B Adult female spider with second instar larvae on its abdomen C Third instar larvae of H. japi after killing its host spider D Third instar larvae consuming the hemolymph of M. biggiba E Detail of dorsal tubercles bearing several hooks F Cocoon of H. japi G Dense weave of cocoon threads in detail.

Before reaching the third instar, the penultimate instar larva modified the host’s behavior, inducing the spider to construct a modified web composed of several threads interconnected with the vegetation and converging radially to the center of the web (Fig. 3). All cocoon webs were built in the same site of the normal webs as a modification of the previous one. The dome-shaped part was absent, except for its hub, and we noted a dense tangle of threads surrounding the central portion. The larva constructs its cocoon attached to the lower surface of the hub, and the cocoon remains suspended between the hub and a dense tangle of barrier threads. Following web construction by the spider, the parasitoid larva performed its last ecdysis, killed the host and sucked its hemolymph, and then discarded the host’s drained carcass. To build its cocoon, the parasitoid larva moved towards the hub of the modified web, turned downwards, and wove several threads repeatedly on the lower surface of the center of the web. The larvae (N = 4) built their cocoons over approximately 9 h. The cocoon is initially white, acquiring an orange coloration in approximately three days (Fig. 2F), and it was not possible to observe the larva through the dense cocoon threads (Fig. 2G). The larva released the meconium three days after cocoon construction and, in one case, a female adult wasp emerged after ten days. The wasp remained on the external surface of the cocoon for approximately 10 minutes before flying away.

Figure 3. 

Web modification in Mecynogea biggiba induced by the parasitoid wasp Hymenoepimecis japi. A Normal web of M. biggiba B–C Cocoon webs in lateral view, and D close of the center of the cocoon web. Arrows indicate the dome-shaped part of the web (white), hub of the dome (red) and support threads (green).

During the second expedition, we found a low frequency of parasitism (N = 1 female; 0.014%). We analyzed 71 adult individuals of M. biggiba, of which 32 were males and 39 females. The tertiary sex ratio of the species was not biased, presenting similar number of male and female individuals (1 male:1.2 females). The average body length of female (3.78 mm ± 0.79) and male (3.78 mm ± 0.68) spiders did not differ (t = 0.04, df = 69, p = 0.4841).

The cocoon web constructed by M. biggiba resembles those induced by other Hymenoepimecis (Gonzaga et al. 2010) and Acrotaphus wasp parasitism (Gonzaga and Sobczak 2011) by the presence of a dense and irregular tangle of non-sticky threads with several points of contact with the surrounding vegetation. The absence of the normal dome shaped portion and the high number of condensed support threads consists of a physical barrier that probably protects the cocoon and enhances the stability of the web. Unlike the cocoon web of M. biggiba, the modified web of L. roseosignata (another host of H. japi) consists of three axes made of several radial threads and a closed hub, where the parasitoid constructs its cocoon (see Sobczak et al. 2009). Thus, we believe that the modified web’s architecture is defined not only by the wasp, but by both the host spider and the wasp.

We observed a low rate of parasitism by H. japi on M. biggiba. In fact, many spider–polysphinctine interactions typically occur at low relative frequency, with little impact on their host spider’s populations. In contrast, Gonzaga and Sobczak (2007) reported a high mortality rate (~40%) of Araneus omnicolor (Keyserling, 1893) (Araneidae) caused by the polysphinctine wasp H. veranii Loffredo & Penteado-Dias, 2009. Although we have found few spiders parasitized, they were all large adult individuals. Previously, Gonzaga and Sobczak (2011) have argued that some wasp species attack intermediate-sized spiders more frequently as this size class provides sufficient biomass for parasitoid larval development while minimizing the risk to the wasp during its attack on the spider (Gonzaga and Sobczak 2011). For the interaction we studied, we believe that even the larger adult spiders of M. biggiba (~ 5 mm) are significantly smaller than adult H. japi (~ 9 mm; Sobczak et al. 2009), and are easily managed by the wasps during the attack. Thus, we encourage future studies that investigate host selection by the wasps for specific host sizes.

Although most interactions between spiders and polysphinctine wasps are species-specific, in some cases the wasps may have a broader host range. To the best of our knowledge, our finds add to the literature the first Hymenoepimecis species that parasite spiders belonging to different families. Even though building quite different webs, both L. roseosignata (orb-weaver) and M. biggiba (dome-weaver) present similarities in their natural histories and foraging strategies. These species are visually similar (at least under the human visual system), inhabiting shrub vegetation at forest edges, and construct horizontal webs, positioning themselves facing the ground. Therefore, it is possible that H. japi selects its hosts according to these traits and it would be interesting to know whether the use of host from more than one spider family is seen in populations from different environments, but additional studies are necessary to test these hypotheses.

We thank Drs William G. Eberhard, Rikio Matsumoto, Mark R. Shaw and an anonymous reviewer by the critical reading and comments that certainly increased the consistency and readability of this work. We also thank Luciana Fernandes for the MEV images and Prefeitura Municipal de Jundiaí for allowing access to the study area. We were financially supported by Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides da Região Sudeste Brasileira (HYMPAR/Sudeste – CNPq/FAPESP/CAPES), CNPq (grant number 446473/2014-6 to JFS), FUNCAP (BP2-0107-00127.01.00/15 to JFS) and CAPES (1378147 to YFM).