Wheat, Triticum aestivum L. (Poales: Poaceae), is the most important food crop in the world in terms of the total harvested weight and the amount used in both human and animal nutrition. Harmful insects are one of the factors affecting the quality and cost of wheat production.

Sunn pests, Eurygaster integriceps Puton, E. maura (L.), and E. austriaca Schrank (Heteroptera: Scutelleridae), are serious pests of wheat in Turkey and in neighboring countries in the Middle and Near East (Kınacı & Kınacı 2004). Among them, E. maura is distributed predominantly in western and northern Europe, whereas E. integriceps is distributed predominantly in southern and eastern Europe (Critchley 1998). Among the Eurygaster species, E. maura is the most common and important pest species of cereals. The proportion of E. maura in Central Anatolia, relative to other sunn pests, was 98.4% when studied by Koçak et al. (2014) and 99.3% when assessed by Memişoğlu (1985). Nymphs and adults of this species have been linked to plant damage, as they feed on leaves, stems, and grains of cereals (Critchley 1998). The sunn pests inject chemicals into the grain that can destroy the gluten and reduce the baking quality of flour (Hariri et al. 2000).

The European sunn pest, E. maura, is a major pest of grain crops and can cause crop losses up to 100% in the absence of control measures (Bandani et al. 2005; Kıvan & Kılıç 2006). In Central Anatolia, E. maura is clearly migratory and often reoccupies the same overwintering and invasion areas (Brown 1965). This univoltine species spends about 9 mo in an obligatory adult diapause under dry leaves, usually in Quercus (Fagales: Fagaceae) scrub or weed stubble on the mountains and hills near wheat fields. Soon after the wheat crop begins to grow in the spring, the European sunn pest enters crop fields and feeds and completes its development on wheat. Then, the adults of the new generation move to the mountains before the wheat and barley are harvested. During this period, climatic conditions, adult parasitoids, nematodes, and entomopathogenic fungi could play an important role in reducing this pest's populations.

Reports of mermithids attacking E. maura were made by Memişoğlu & Özer (1992; 1994) in Turkey; however, the mermithids were not identified to the species level. Many mermithids have been reported from species of closely related hemipterans. Examples include Mermis sp. (Nematoda: Mermithidae) and Hexamermis sp. (Nematoda: Mermithidae) parasitizing Aelia rostrata Boheman (Hemiptera: Pentatomidae) and E. integriceps in Turkey (Dikyar 1981; Memişoğlu & Özer 1994; Memişoğlu et al. 1994; Tarla et al. 2010; 2012a; 2012b) and Hexamermis sp. parasitizing Rhaphigaster nebulosa Poda (Heteroptera: Pentatomidae) in Italy (Manachini & Landi 2003). Pentatomimermis pentatomiae (Rubtzov) (Nematoda: Mermithidae) was reported from Elasmostethus interstinctus (L.) (Heteroptera: Acanthosomatidae) at Novosibirsk, Russia (Rubstov 1978). Also, nematodes of the genus Hexamermis were observed infesting Piezodorus guildinii (Westwood) and Acrosternum hilare (Say) (Heteroptera: Pentatomidae) in the United States (Kamminga et al. 2012). Recently, Hexamermis eurygasteri Tarla, Poinar & Tarla (Nematoda: Mermithidae) was first described from E. integriceps in Turkey (Tarla et al. 2011). In addition, mermithids were reported on some other insect species in Turkey (Demirbağ & Yaman 1999; Yaman et al. 2002, 2009; Mennan & Ertürk 2006).

The objective of this study was to determine the infection rates of E. maura with the recently recorded parasitic nematode Hexamermis sp. under natural conditions in the overwintering area and to assess the nematode's potential for natural suppression of the European sunn pest.

The parasitic nematode Hexamermis sp. was obtained from the body cavity of E. maura (Fig. 1A) for the first time at Ankara, Turkey, in 2013 (39°40′20″N, 32°55′15″W, 1,485 m). In the second year, before E. maura migrated to cereal fields, overwintering adults were collected by hand in dead leaves of Quercus from Beynam (39°40′18″N, 32°55′12″W, 1,483 m), an overwintering area in Ankara Province on 2 and 3 May 2014. The insects were brought to the laboratory in transparent plastic bags, where they were sexed (120 females and 114 males) in 2014. After being killed in ethyl alcohol (70%), the bugs were dissected in distilled water under a stereomicroscope (Leica Mz 75) to determine the presence or absence of mermithids. The rate of parasitism was calculated individually for female and male sunn pests. The adult parasitic nematodes were obtained according to the method described by Tarla et al. (2011). After emerging from infected insect (Fig. 1B), the postparasitic juvenile nematodes migrated into the moist soil, where they matured to the adult stage. The adult nematodes were removed carefully from the soil, killed in distillated hot water (65 °C), fixed in 5% formalin, and processed to glycerine. The study was carried out in a laboratory at Uşak University.

Eurygaster maura and E. integriceps are very difficult to separate taxonomically without dissection or examination of genitalia (Gaffour-Bensebbane 1991; Critchley 1998). Therefore, taxonomic distinction of E. maura species was completed according to characteristics of the male aedeagus, which has 2 internal spines (Fig. 2).

The E. maura adults collected from the overwintering area were found to be parasitized by mermithid nematodes in 2013. In the second year of this study, infection rates in the bodies of dissected E. maura were calculated separately for females and males. In 2014, the parasitism rate for females (n = 120) was 20.0% and that for males (n = 114) was 31.6%.

Fig. 1.

Post-parasitic juvenile Hexamermis sp. in the body cavity (A) and emerging from the cervix of Eurygaster maura (B) (scale bar: 2.1 mm).

Fig. 2.

Internal spines of Eurygaster maura male's aedeagus.

The mean body lengths of adults (n = 5) and post-parasitic (n = 5) stages of the nematodes were measured as 76.8 ± 12.91 (63.9-93.7) mm and 103.3 ± 11.17 (89.7-120.2) mm, respectively. Description: Bodies are medium-large, slender, color white, and cuticle containing prominent crisscross fibers visible with the light microscope. Mouth terminal and head containing 6 cephalic papillae, no lip papillae, amphids reduced, and 6 hypodermal cords at mid-body. Post-parasitic juvenile tail tip has a finger-like appendage (Fig. 3A). But, after molting (Fig. 3C), posterior end of female has bluntly rounded tail (Fig. 4A). Head of female is pointed (Fig. 4B). Vulva has short lips and distinctive cuticular cone (Fig. 4C). Juvenile has cephalic papillae and amphids reduced in size (Fig. 3B). Male is unknown. Due to presence of those characters described above, the nematode species was placed in the genus Hexamermis Steiner, 1924. The taxonomic distinction of the genus of this nematode was completed according to published literature (Nickle 1972; Rubstov 1978; Artyukhovsky 1990; Kaiser 1991). The post-parasitic juveniles of Hexamermis differ from Agamermis Cobb, Steiner & Christie, 1923 by the tail tip appendage always being preserved after the final molt (Hernández-Crespo & Santiago-Alvarez 1997; Achinelly & Camino 2008).

The mermithid nematode parasite of the genus Hexamermis discovered in Turkey was found to parasitize more than 25% of the total E. maura population in the overwintering area in 2014. Naturally occurring entomophagous nematodes are important regulatory factors for some insect populations (Smart 1995; Rahaman et al. 2000). In some cases, mermithids are the major determinant of grasshopper abundance (Baker & Capinera 1997); thus, they may similarly be key factors governing population dynamics of European sunn pest.

Our morphological observations on juveniles and adult females of the Hexamermis sp. obtained from E. maura revealed that it may not be H. eurygasteri. For this reason, our future studies will include efforts to obtain the males of this species and will involve determining DNA sequences of the parasite. Although Hexamermis species have not previously been reported from E. maura, there are earlier reports of unidentified mermithids attacking E. maura (Memişoğlu & Özer 1992, 1994) in Turkey. Memişoğlu & Özer (1992, 1994) reported that the mortality caused by parasitic nematodes was 15.5 and 7.2% in 1983 and 1984, respectively. Later, Tarla et al. (2011) described H. eurygasteri parasitizing E. integriceps, a major pest of wheat in Turkey, and this was the first description of a mermithid parasitizing a species of Eurygaster (Tarla et al. 2011). Also, Tarla et al. (2012a) reported parasitism rates of 13.8 and 16.0% for females, and 7.5 and 7.1% for males, in 2008 and 2009, respectively. Thus, this report of parasitism of Eurygaster by Hexamermis sp. is consistent with previous research.

In conclusion, natural parasitism of E. maura by Hexamermis sp. is reported for the first time. The findings suggest that this nematode species may be an important natural mortality factor for regulation of populations of E. maura under field conditions because it showed high rates of parasitism. Thus, additional research should be conducted to further assess the potential of Hexamermis sp. for suppression of E. maura.

This research was funded by the Uşak University Scientific Research Coordination Agency (BAP) (project number: 2013/MF005).

Fig. 3.

Tail appendage (A), anterior portion of female (B), and posterior end of molting female of post-parasitic juvenile Hexamermis sp. (C) (scale bar: A, 42 μm; B, 43 μm; C, 58 μm).

Fig. 4.

Tail of female (A), anterior portion of female (B), and vulva of Hexamermis sp. (C) (scale bar: A, 78 μm; B, 32 μm; C, 89 μm).