Research Article |
Corresponding author: Vladimir E. Gokhman ( vegokhman@hotmail.com ) Academic editor: Maksim Proshchalykin
© 2021 Vladimir E. Gokhman, Matvey I. Nikelshparg.
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.
Citation:
Gokhman VE, Nikelshparg MI (2021) Eupelmus messene Walker, 1839 and E. microzonus Förster, 1860 as parasitoids of Aulacidea hieracii (Bouché, 1834) (Hymenoptera, Eupelmidae, Cynipidae). In: Proshchalykin MYu, Gokhman VE (Eds) Hymenoptera studies through space and time: A collection of papers dedicated to the 75th anniversary of Arkady S. Lelej. Journal of Hymenoptera Research 84: 87-102. https://doi.org/10.3897/jhr.84.68556
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In the southeast of European Russia, the gall wasp Aulacidea hieracii (Bouché, 1834) is attacked by ten parasitoid species, including Eupelmus (Eupelmus) microzonus Förster, 1860 and E. (Macroneura) messene Walker, 1839. Although both members of the genus Eupelmus Dalman, 1820 are idiobiont ectoparasitoids, they demonstrate different life-history strategies in respect to many bionomic features. Specifically, E. messene is represented by brachypterous thelytokous females which lay single eggs directly onto the host body. This species can parasitize both concealed and exposed larvae and pupae of A. hieracii, but fails to attack its primary parasitoids. On the contrary, arrhenotokous males and females of E. microzonus are fully winged. These parasitoids usually lay several eggs per host which are placed onto the wall of the host chamber and covered with a particular fibrous substance. E. microzonus never parasitizes pupae or exposed larvae, although it can readily attack concealed larvae of A. hieracii and its primary parasitoids. In addition, hibernating individuals of E. messene undergo obligatory larval diapause, but those of E. microzonus are able to develop without exposure to subzero temperatures. All these data collectively suggest that the former species is highly specialized to exploit A. hieracii as a host, whereas the latter one mostly exhibits the so-called morphotypical specialization. These different strategies allow E. messene and E. microzonus to coexist on the same host species, as a local specialist and a more or less evenly distributed generalist, respectively.
Arrhenotoky, brachyptery, diapause, host range, hyperparasitism, life-history strategy, niche partitioning, thelytoky
Aulacidea hieracii (Bouché, 1834) is a widely distributed Holarctic species of gall wasp attacking a number of perennial plants of the genus Hieracium Linnaeus (Asteraceae) (
The present paper is dedicated to the 75th anniversary of Prof. Arkady S. Lelej, a world-class expert on taxonomy, zoogeography and biology of the order Hymenoptera.
Galls of A. hieracii (Fig.
Emerged parasitic wasps were identified by VEG, identifications of Ichneumonidae, Pteromalidae and Eupelmidae were later checked by Andrey I. Khalaim, Ekaterina V. Tselikh (both from the Zoological Institute of the Russian Academy of Sciences) as well as by Lucian Fusu (Alexandru Ioan Cuza University) and Oksana V. Koscheleva (All-Russian Institute of Plant Protection) respectively. Voucher specimens of gall wasps (Fig.
Unless otherwise stated, all experiments were conducted at room temperature (23–25 °C) and 30–40% relative humidity. Ovipositing parasitoids were provided with water and diluted sugar syrup ad libitum. To study oviposition and feeding behavior of parasitic wasps as well as to identify their type of parthenogenesis (arrhenotoky vs. thelytoky), virgin females of both species were offered gall fragments containing larvae and pupae of A. hieracii (Fig.
During this study, ten parasitoid species were constantly reared from the galls of A. hieracii, including E. microzonus and E. messene (Table
Species | Males | Females |
---|---|---|
Aulacidea hieracii (Bouché, 1834) (Cynipidae) | 191 | 226 |
Exeristes roborator (Fabricius, 1793) (Ichneumonidae) | 5 | 0 |
Eurytoma cynipsea (Boheman, 1836) (Eurytomidae) | 80 | 98 |
E. hybrida Zerova, 1978 (Eurytomidae) | 0 | 2 |
Eurytoma sp. aff. strigifrons Thomson, 1876 (Eurytomidae) | 3 | 2 |
Sycophila submutica (Thomson, 1876) (Eurytomidae) | 24 | 34 |
Torymus chloromerus (Walker, 1833) (Torymidae) | 0 | 4 |
Ormyrus discolor Zerova, 2005 (Ormyridae) | 12 | 10 |
Pteromalus vibulenus (Walker, 1839) (Pteromalidae) | 22 | 45 |
Eupelmus (Macroneura) messene Walker, 1839 (Eupelmidae) | 0 | 6 |
E. (Eupelmus) microzonus Förster, 1860 (Eupelmidae) | 1 | 1 |
Females of E. messene are brachypterous (Fig.
During the laboratory experiments conducted from 2018 to 2021, five and twelve ovipositing females of E. microzonus and E. messene produced 22 males and 20 females, respectively. We therefore were able to breed the latter species under laboratory conditions for at least four generations. As for E. microzonus, its reproduction in the lab terminated every time when all reared virgin females of this species produced exclusively male progeny.
For newly hatched females of E. microzonus and E. messene, it takes about 20–25 and 25–30 days, respectively, to start ovipositing. Although the latter species, apart from E. microzonus, can successfully utilize exposed hosts in the lab (see below), the basic scheme of attacking concealed hosts appears to be virtually the same in females of both members of the genus Eupelmus. Nevertheless, this scheme can be substantially modified depending on the parasitoid species. The following observations are based on the experiments with eight and twelve females of E. microzonus and E. messene respectively.
The described scheme is subject to modification, since parasitoids can either repeat certain acts or terminate the whole sequence at almost every stage. The female usually abandons the host after the initial examination, unsuccessful drilling attempts, host immobilization or probing. Anyway, our preliminary study did not reveal any significant difference regarding duration of main behavioral acts between the two species. In addition, E. messene can successfully attack both exposed and concealed hosts, whereas E. microzonus never lays eggs on the former ones. Moreover, E. messene acts as a strictly primary parasitoid of A. hieracii and can develop on both its larvae and pupae. On the other hand, E. microzonus often attacks larvae of Eurytoma spp. and Sycophila submutica, thus displaying facultative hyperparasitism, but this parasitoid does not find host pupae suitable for oviposition. Specifically, females of E. messene laid eggs on twenty-nine exposed immature individuals of A. hieracii in our experiments (including eleven pupae), but failed to oviposit onto five larvae of Eurytoma as well as onto two larvae and ten pupae of Sycophila. On the other hand, females of E. microzonus rejected seven and three exposed larvae and pupae of A. hieracii, respectively, as well as seven concealed pupae of the same host species that were offered to ovipositing parasitoids. Individuals of E. microzonus could also develop on at least two concealed larvae of Eurytoma spp., in addition to three larvae of S. submutica.
A. hieracii, the principal host of E. microzonus and E. messene in the studied habitat, is a univoltine species, with adults emerging in May and mature larvae overwintering in galls (
In E. microzonus, the egg is longish-oval (about 0.05 × 0.2 mm) and semi-transparent, with a very short anterior process and a longer posterior one (Fig.
The life cycle of E. messene generally resembles that of the previous species. In addition, immature stages of E. messene are also similar in size and morphology to those of E. microzonus (Fig.
Duration of developmental stages of two Eupelmus species (mean ± standard deviation, days).
Stage | E. messene | E. microzonus |
---|---|---|
Egg | 4 ± 1 (9 females) | 3 ± 1 (8 males) |
Larva | 14 ± 0 (9 females) | 12 ± 1 (3 males) |
Pupa | 10 ± 2 (9 females) | 12 ± 0 (9 males) |
Adult | 55 ± 5 (9 females) | 18 ± 4 (8 males), 53 ± 9 (4 females) |
Among the parasitic wasps reared during the present study, certain genera and species were already associated with A. hieracii (
There was a number of historical reports on the ecology and behavior of Eupelmidae and of the genus Eupelmus in particular (
Previous observations on the biology of E. microzonus and E. messene are scarce. Specifically, E. microzonus mostly attacks Cynipidae and Eurytomidae on herbaceous plants and certain shrubs (
Both male and female E. microzonus have fully developed wings, whereas these organs are obviously reduced and non-functional in E. messene. Since many members of the genus Hieracium, including H. robustum, usually form more or less dense patches (see e.g.
Virgin females of E. microzonus and E. messene produced only male and female progeny, respectively, thus confirming arrhenotoky in the former species and thelytoky in the latter (
Both studied Eupelmus species normally attacked immature stages of A. hieracii inside the galls. However, E. messene could also oviposit onto the exposed larvae and pupae of this gall wasp, but E. microzonus completely failed to attack them in our experiments. On the other hand, the latter species readily oviposited not only on A. hieracii, but also on Eurytoma spp. and S. submutica, i.e., it displayed facultative hyperparasitism. In contrast to E. microzonus, E. messene was a strictly primary parasitoid and never demonstrated hyperparasitic behavior. Finally, E. messene could attack and successfully develop either on larvae or pupae of A. hieracii, whereas E. microzonus always rejected pupae of this gall wasp and of its parasitoids.
Before the female of E. microzonus begins to oviposit, it has to feed on the host’s hemolymph. To get access to it, the parasitoid first pierces the host’s skin with its ovipositor, and then constructs a feeding tube (see above). As for E. messene, it can feed on host’s hemolymph in a direct contact with the hosts, but construction of the feeding tube was never reported for this species (
E. microzonus usually deposits several eggs into the host chamber, thus exhibiting superparasitism (
Both studied Eupelmus species were strictly univoltine in our experiments, like most other members of the family (
Taken together, our observations and experimental data clearly demonstrate that E. microzonus and E. messene exhibit different life-history strategies as parasitoids of A. hieracii within the same habitat (Table
Main differences between life-history strategies of two Eupelmus species attacking A. hieracii.
Character | E. messene | E. microzonus |
---|---|---|
Motility | Fully winged | Brachypterous |
Type of parthenogenesis | Thelytoky | Arrhenotoky |
Ability to oviposit onto exposed hosts | Present | Absent |
Facultative hyperparasitism | Absent | Present |
Ability to oviposit onto host pupae | Present | Absent |
Number of eggs laid by single female onto host | Single | Usually several |
Placement of eggs | Directly onto host | Into host chamber |
Fibrous attachment of eggs | Absent | Usually present |
Construction of feeding tube | Not observed | Present |
Obligatory winter diapause | Present | Absent |
We also noted that biological characters of E. messene (often referred to as “thelytokous E. vesicularis” in the previous literature) studied in the present work often substantially differ from those described by preceding authors. Although some of these discrepancies (e.g., the obligatory winter diapause) can be more or less reliably attributed to intraspecific variation (
Apart from E. messene, E. microzonus is adapted to exploit larvae of various host species inside the galls of A. hieracii. In other words, this parasitoid exhibits the so-called morphotypical specialization (
All observations and experimental data described and summarized in the present study therefore collectively suggest that different life-history strategies exhibited by the two Eupelmus species allow them to coexist on A. hieracii. Although both members of the genus Eupelmus utilize this species as an important host, their ecological strategies significantly differ due to apparent niche partitioning (
1. In the southeast of European Russia, A. hieracii is attacked by ten parasitoid species, including two members of the genus Eupelmus, E. microzonus and E. messene.
2. Although both Eupelmus species are idiobiont ectoparasitoids, they demonstrate different life-history strategies in respect to their flight ability, type of parthenogenesis, potential hyperparasitism, range of suitable host stages, mode of hibernation, and other traits.
3. E. messene is highly specialized to exploit A. hieracii as a host, whereas E. microzonus mostly exhibits morphotypical specialization.
4. These different strategies allow E. messene and E. microzonus to coexist on the same host species, as a local specialist and a more or less evenly distributed generalist, respectively.
The authors are grateful to Lucian Fusu (Alexandru Ioan Cuza University, Iasi, Romania), Andrey I. Khalaim and Ekaterina V. Tselikh (Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia) as well as to Oksana V. Koscheleva (All-Russian Institute of Plant Protection, St. Petersburg, Russia) for identifying parasitoids, to Richard R. Askew (Le Bourg, St Marcel du Périgord, Ste Alvère, France) for providing certain references, to Alexander S. Prosvirov (Moscow State University, Moscow, Russia) for helping with macrophotography as well as to Vasilyi V. Anikin (Saratov State University, Saratov, Russia) for useful advice and discussion. We greatly appreciate a thorough revision of the text performed by Maxim Yu. Proshchalykin (Federal Scientific Center of the East Asia Terrestrial Biodiversity, Vladivostok, Russia), George Melika (National Food Chain Safety Office, Budapest, Hungary) and especially by Lucian Fusu, which substantially improved the manuscript. The present study was conducted within the framework of the State Order no. 121031600193-7 of the Government of the Russian Federation to Moscow State University.