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Potential for Attractive Semiochemical Lures in Rhagoletis cerasi (L.) Management: A Field Study
Laura Ioana MACAVEI¹* Ion OLTEAN¹ Iuliana VASIAN3 Teodora FLORIAN¹ Mircea VARGA¹ Raul BĂEŢAN¹ Viorel MITRE2 Lara MAISTRELLO4
1Faculty of Agriculture, University of Agricultural Science and Veterinary medicine Cluj-Napoca, Cluj-Napoca, Calea Mănăştur 1-3, ROMANIA 2Faculty of Horticulture, University of Agricultural Science and Veterinary medicine Cluj-Napoca, Cluj-Napoca, Calea Mănăştur 1-3, ROMANIA 3Babes-Bolyai” University, “Raluca Ripan” Institute for Research in Chemistry, Pheromones Production Center, Fantanele 30, Cluj-Napoca, ROMANIA 4Department of Life Sciences, University of Modena and Reggio Emilia, Pad. Besta, via G. Amendola 2, 42122 Reggio Emilia, ITALY *Corresponding author’s e-mail: [email protected]
ABSTRACT In the view of sustainable management of Rhagoletis cerasi (L.) (Diptera, Tephritidae), a key pest of cherry orchards in Europe, we tested the efficacy of five blends containing male produced volatiles that were used as lures on yellow sticky traps, during a two year field study. Results show a superior efficacy of one of the blends (RC1 = 2-hexanone: 3-heptanone: nonanal), which captured three times more individuals than control in both years. Good results were also obtained by RC2 (beta-phellandrene: geranyl acetate: (+)-limonene) with an average number of catches which was half that of RC1 in both years. Our findings showed that one of the tested blends, which possibly represents the male sexual pheromone, has a promising potential for practical applications of synthetic lures in monitoring, mass-trapping or attract and kill strategies. Key words: Attractant volatiles, European cherry fruit fly, integrated pest management, pheromones, Tephritidae.
INTRODUCTION Rhagoletis cerasi Loew (Diptera, Tephritidae) is a key pest of Romanian cherry orchards (Chireceanu, 2008) and also of other European countries (Daniel and Grunder, 2012). Depending on the cultivar, infestation level of fruits can vary from 60% (Bandzo et al., 2012) up to harvest jeopardizing (Fimiani and Cavalloro, 1983), especially in biological agrocenoses (Letcheva et al., 2001). The reliance on chemicals is often the most used management strategy. Given the side effects such as residual ecotoxicity to beneficial organisms and humans, cherry production is challenged by the withdrawal of insecticides in many European countries (Daniel, 2009). Therefore, Rhagoletis cerasi management is now focused on sustainable and effective strategies. 2 MACAVEI, L. I., OLTEAN, I., VASIAN, L., et al. Among the different alternatives being developed, the usage of semiochemicals is of particular interest, especially for their suitability in integrated pest management programs (Baker, 2009). Although their identification is challenging (Wehrenfennig et al., 2013), volatile compounds have been studied in more than 30 tephritid species of economic interest (Wicker-Thomas, 2007). Potential applicability of these semiochemicals in integrated management strategies has been reviewed (Benelli et al., 2014; Jeyasankar, 2009; Sivinski and Calkins, 1986). Among the methods involving semiochemicals in fruit flies control, a successful case was the combined use of sexual pheromone and food attractants in monitoring and mass-trapping of Bactrocera oleae (Bueno and Jones, 2002). Male lures (Tan et al., 2014) are also effectively used in mass trapping of Mediterranean fruit fly (Trimedlure) or in attract and kill strategies for Melon fly (“cue-lure”) and Oriental fruit fly (Methyl eugenol) (Witzgallet al., 2010). The use of attractive semiochemicals for fruit flies has also been explored in terms of biosecurity (Suckling, 2015), biological control mediated through bacteria semiochemicals (Leroy et al., 2011), or to switch on plant defense by attracting the natural antagonists (Pickett et al., 2012). In case of eradication programs (Suckling et al., 2014), the availability of specific lures will substantially increase the success (Tobin et al., 2014). The use of host marking pheromones allowed to achieve significant reductions in the pest incidence for Ceratitis capitata (Arredondo and Díaz-Fleischer, 2006) and Anestrepha obliqua (Aluja et al., 2009). Applicability of these semiochemicals in mass rearing process of the specific parasitoids has been suggested by Silvaet al. (2012). Regarding Rhagoletis genus, previous studies have shown that R. pomonella is efficiently attracted by parapheromones such as butyl hexanoate (Bostanian and Racette, 2001) and by food-attractants like ammonium carbonate (Yee et al., 2014). This type of volatiles can also be used in combined strategies for reduced-risk insecticide applications (Pelz-Stelinski et al., 2006) or in addition to monitoring traps (Pelz-Stelinski et al., 2005), where the use of ammonium acetate increased captures of R. cingulata. Currently monitoring for the European cherry fruit fly R. cerasi is performed by means of yellow sticky traps (“Rebell” type), and Katsoyannos et al. (2000) showed that adding the food attractant ammonium acetate increased trap efficiency. However, the use of other types of attractants has never been considered and relatively few studies are available, possibly due to difficulties in identification and formulation of the components, but also for the difficulties in rearing this species (Daniel and Grunder, 2012). Guerin et al. (1983) studied the response of several fruit flies to volatile substances that are known as “general green leaf volatile complex” substances, however, none of them was attractive to R. cerasi. Later, seventy-eight generally occurring plant volatiles and male cherry fruit volatiles were investigated by means of olfactory selectivity (Raptopoulus et al., 1994-1998). In terms of kairomones, methyl salicylate was shown to affect the fruit fly oviposition (Köppler et al., 2010). The oviposition host marking pheromone was successfully identified and obtained good results in the field (Aluja and Boller, 1992). Although the existence of an attractant sexual pheromone was mentioned (Katsoyannos, 1982), its exact composition has 3 Potential for Attractive Semiochemical Lures not been identified yet (Daniel and Grunder, 2012). Raptopoulos et al. (1995) later identified a high number of the volatiles emitted byR. cerasi males and after performing behavioral bioassays he obtained EAG responses on female antenna. The aim of this study was to determine the effectiveness of different semiochemical blends in field conditions for the European cherry fruit fly, using as a starting point the most attractive substances based on EAG responses, as identified by Raptopoulos et al. (1995), considered as attractant pheromones also by Wicker-Thomas (2007) and in the specific pheromone database (El-Sayed, 2014).
MATERIALS AND METHODS The experiment was carried out during two years in an organic cherry orchard (9 ha size), located in Cluj-Napoca city, Romania, with plants from mixed cherry cultivars (Ramon Oliva, Boambe de Cotnari, Germersdorf, Van, Stella and Rubin) randomly distributed all over the field. No chemical treatments were performed. The chosen volatile compounds, based on Raptopoulos et al. (1995) were: 2-hexanone, 3-heptanone, nonanal, beta-phellandrene, geranyl acetate and (+)-limonene (Fig. 1).
Fig. 1. The structure of the pheromonal components of Rhagoletis cerasi males, tested in the experiment. The five experimental lures consisted of blends of the six selected compounds considering the two groups carbonyl (ketones and aldehydes) and terpenes, and combinations of substances belonging to the two groups, using different proportions. Based on this, the following blends were tested: Lure RC1 = 2-hexanone: 3-heptanone: nonanal = 1:1:2 = 1mg/lure; Lure RC2 = beta-phellandrene: geranyl acetate: (+)-limonene = 1:1:1 = 1.5 mg/lure Lure RC3 = 2-hexanone: 3-heptanone: nonanal: beta-phellandrene: geranyl acetate = 1:1:1:1:1 = 1mg/lure; Lure RC4 = 2-hexanone: 3-heptanone: nonanal: beta-phellandrene: geranyl acetate: (+)-limonene = 1:1:1:1:1:1 = 1.2 mg/lure; Lure RC5= 2-hexanone: 3-heptanone: nonanal: beta-phellandrene: geranyl acetate = 1:1:1:1:1 = 2.5 mg/lure. 4 MACAVEI, L. I., OLTEAN, I., VASIAN, L., et al. Each lure was dissolved in a solution of (50 ml) n-hexane, incorporated in a rubber septa (15 mm diameter) (Romfarmachim, Romania) and then attached to the upper part of a yellow sticky trap. The red sleeve stopper was packed after the evaporation of n-hexan. The control consisted of a rectangular yellow sticky trap with double sided adhesive (210mm x 297mm) (Isabella yellow, Poliam Cluj-Napoca, Romania). The traps were placed at an approximate height of 1.7-1. 9 m, on the southern part of canopy, at a minimum distance of 20 m one from each other. Eight replicates for all five variants and eight replicates for control were set up. Traps reading was performed twice a week (flies were not sexed) from the beginning until the end ofR. cerasi flight, respectively between end of May to early July in 2013 and third week of May to beginning of July in 2014. During each experimental period, no changes of lures were performed, per manufacturer’s instructions. The substances 2-hexanone 98%, 3-heptanone 98% and nonanal 97% were purchased from Alfa Aesar (Romania); Beta-phellandrene and (+)- limonene was purchased from SC Terpena SRL (Romania). Geranyl acetate 98% was synthesized in the laboratory of “Raluca Ripan” Institute for Research in Chemistry by acetylation of geraniol 97% (Sigma Aldrich) with acetic anhydride in pyridine at reflux, purified by silica gel (n-Hexane:Diethylether = 10:1) and analyzed by GC-MS analysis. Due to heteroscedasticity, the differences in the numbers of insects captured using the different lure blends were compared, separately for each year, using non parametric Kruskal-Wallis analysis of variance, followed by post-hoc comparisons of mean ranks of all pairs of groups. Statistical tests were performed with STATISTICA 7.1 (StatSoft, 2005).
RESULTS The results show that in year 2013 highly significant differences were detected in the number of cherry fruit flies catches (H = 31.49, N = 48, P < 0.0001). Multiple comparisons showed that lure RC1 captured a significantly higher (P < 0.001) number of flies compared to Control (z = 3.51, p =0.006749), RC4 (z = 4.96, p = 0.000011) and RC5 (z = 4, p = 0.000987), whereas no differences were detected between RC1, RC2 and RC3 (Fig. 2). In addition, no significant differences were detected between RC4, RC5 and Control. During the year 2014, highly significant differences (H = 17.05, N = 48, P = 0.004) were observed, with multiple comparisons showing that RC1 captured a higher number of flies compared to Control (z = 3.018, p = 0.038185), RC3 (z = 3.11, p = 0.028336), RC4 (z = 3.08, p = 0.031013) and RC5 (z = 3.47, p = 0.007714) (Fig. 3). No differences were detected between RC1 and RC2. Control was not significantly different from RC3, RC4 and RC5.
DISCUSSION AND CONCLUSIONS Our study was aimed at comparing different semiochemical lures for attracting the European cherry fruit fly by means of a field trial performed over two years. We 5 Potential for Attractive Semiochemical Lures used male produced volatiles that were shown to be the most attractive components in laboratory bioassays (Raptopoulos et al., 1995). One of the lures, RC1, showed the best performance in both years with attraction to it three times greater than to the control. RC2 lure showed good potential also, with an average number of catches which was half that of RC1 in both years. In studies concerning the male volatiles of C. capitata, in laboratory experiments, blends with the five major components were attractive, though not as efficient as live males (Jang et al., 1994). In field tests the use of mixtures with the three male emitted major components proved to be attractive in Guatemala (Heath et al., 1991), whereas similar trials performed in Spain gave disappointing results (Howse and Knapp, 1996). On the other hand, the use of single components from male borne emissions showed unsatisfactory results for this fruit fly both in laboratory (Jang et al., 1994) and in field studies (Delrio and Ortu, 1988).
Fig. 2. Box and whisker plot representing the captures of Rhagoletis cerasi during 2013 in the traps baited with the different semiochemicals blends or in unbaited traps (control). Boxes indicated with the same letters are not significantly different after the Kruskal-Wallis analysis of variance, followed by post-hoc comparisons of mean ranks of all pairs of groups.
Fig. 3. Box and whisker plot representing the captures of Rhagoletis cerasi during 2014 in the traps baited with the different semiochemicals blends or in unbaited traps (control). Boxes indicated with the same letters are not significantly different after the Kruskal-Wallis analysis of variance, followed by post-hoc comparisons of mean ranks of all pairs of groups. RC1 consisted of a blend of 2-hexanone, 3-heptanone and nonanal and RC2 in beta-phellandrene: geranyl acetate: (+)-limonene. The RC1 and RC2 lures contain 6 MACAVEI, L. I., OLTEAN, I., VASIAN, L., et al. different groups of chemical compounds, with the first blend containing only carbonyl compounds and the second only terpenoid compounds. The attractiveness of these two groups used separately showed greater efficacy than the control whereas, when these groups were mixed in different proportions for the other three blends, the attractiveness was significantly diminished. Therefore, it appears that terpenoid and carbonyl compounds do not have a sinergistic action in attracting R. cerasi, suggesting that together their positive effects are cancelled out. The components of RC1 blend are utilized in chemical communication systems of a relatively small number of insects. Focusing on Diptera species, heptan-3-one and hexan-2-one are reported as pheromones only for R. cerasi (El-Sayed, 2014). Nonanal is reported as a kairomone for mosquito species, eg. Culex quinquefasciatus (Irish et al., 2014) and Culex tarsalis (El-Sayed, 2014), and for the fly Atherigona soccata (El-Sayed, 2014) and represents a pheromonal component for another fruit fly pest, Bactrocera oleae (El-Sayed, 2014). Field test with nonanal used as a single component resulted in failure of attraction for R. cerasi (Guerin et al., 1983). Regarding RC2 lure, its components are involved in chemical communication of a higher number of insects, among which Tephritidae family is represented by three more species beyond R. cerasi, Anastrepha fraterculus, A. ludens and C. capitata (El-Sayed, 2014). Therefore, the blend of lure RC1 presents a potential for fruit fly selectivity. In our study, the blends RC3, RC4 and RC5 that contained both heptan-3-one and geranyl acetate were not attractive, as compared with no odor in the controls. These substances, detected among the major R. cerasi male volatiles (Raptopoulos et al., 1995) have been identified also in its host plant (El-Sayed, 2014; Mattheiset al., 1992). Therefore, a possible explanation for the lack of attraction of these lures is the competition with the natural host odors. Similar hypothesis were made also by Howse and Knapp (1996) regarding failure of attraction of C. capitata male volatiles competing with citrus host in field trials. An alternative hypothesis is that these substances need to be part of a blend not yet identified, in particular ratios not yet tested. Our study tested only part of the major compounds identified from the male-produced odor range (Raptopoulos et al., 1995) and it is possible that the use of different blends with the identified components could achieve better results. Nevertheless, we demonstrated for the first time that a male derived semiochemical blend obtained very good results in attracting R. cerasi in the field. Due to the fact that in this fruit fly no male to male attraction or male to female attraction was observed (Katsoyannos, 1982), it is likely that a great number of the individuals captured with RC1 lure were females and therefore this blend could represent the male sexual pheromone. Having a minimal impact on the environment and on beneficial organisms (Wehrenfennig et al., 2013) the application of semiochemicals has been an integral part of sustainable pest management programs for more than 40 years, being used in several types of controlling actions (Baker, 2009). Regarding European cherry fruit fly management, our findings showed that one of the tested blends could represent a promising candidate for practical applications of synthetic pheromone lures. Further research is needed to investigate its role as a complementary tool to improve monitoring for R. cerasi. 7 Potential for Attractive Semiochemical Lures ACKNOWLEDGEMENTS This research was partially supported by Babes-Bolyai University, Pheromones Production Center, Cluj-Napoca, unique producer of insect pheromones in Romania. The authors thank Aurelia Pop for collaboration.
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Received: September 03, 2015 Accepted: December 25, 2017
J. Entomol. Res. Soc., 20(1): 11-19, 2018 ISSN:1302-0250
A Study of Trichoptera of the Blinajë Hunting Reserve Including the First Records of Ironoqua dubia (Stephens, 1837) (Limnephilidae) from the Hellenic Western Balkans
Halil IBRAHIMI1 Linda GRAPCI-KOTORI 2* Mladen KUČINIĆ3 Valentina Slavevska STAMENKOVIĆ4 Biljana RIMCHESKA5 Astrit BILALLI6
1, 2Department of Biology, Faculty of Mathematical and Natural Sciences, University of Prishtina “Hasan Prishtina”, “Mother Theresa” street, p.n. 10000 Prishtina, REPUBLIC OF KOSOVO 3Department of Biology (Laboratory of Entomology), Faculty of Science, University of Zagreb, Rooseveltov trg 6, 10000 Zagreb, CROATIA 4,5Institute of Biology, Faculty of Natural Science and Mathematics, Ss. Cyril and Methodius University, P.O. Box 162, 1000 Skopje, REPUBLIC OF MACEDONIA 6Faculty of Agribusiness, University of Peja “Haxhi Zeka”, “UÇK” street, 30000 Pejë, REPUBLIC OF KOSOVA e-mails: [email protected]; 2*[email protected]; [email protected]; [email protected]; [email protected]; [email protected]
ABSTRACT The results of investigation of Trichoptera of the Blinajë Hunting Reserve in Kosovo are presented. Two different sampling techniques for collecting adult caddisflies are compared. The most significant faunistic records are of Ironoquia dubia (Stephens, 1837) (Limnephilidae). This species has not been previously recorded from Ecoregion 6, the Hellenic Western Balkans. The Kosovo records are put in the context. Key words: Trichoptera, Balkan Peninsula, Ironoquia dubia, Ecoregion 6, Kosovo, sampling techniques.
INTRODUCTION The territory of the Blinajë hunting area designated as a special reserve zone is located in central part of Kosovo, 15 km on the western side of Lipjan town. The total surface of Blinajë Hunting Reserve is 5 500 ha and stretches into the territory of three municipalities: Lipjan, Shtime and Drenas. The altitude within this territory ranges from 670 to 860 m above sea level. There are 33 artificial lakes present inside Blinajë Hunting Reserve. This part of the Balkan Peninsula has been poorly investigated for caddisflies. It has been known for a long time (e.g. Crichton, 1965; Svensson, 1974; Usseglio- Polatera, 1986) that different sampling techniques capture a different range of species. This is especially important in biodiversity studies where the number of species, and especially including those with low densities, is increased by implying more sampling techniques. The life cycle of Ironoquia Banks, 1916 species that have been studied is most unusual. The fully grown larvae leave the water and burrow into the bank or piles of 12 Ibrahimi, H., Grapci-Kotori, L., Kučinić, M., et al. leaf litter by its side. They remain very moist but are effectively terrestrial. They stay as resting larvae until they pupate in the autumn. Larvae of I. dubia inhabit woodland streams, ditches and ponds in which the bottom is covered with dead leaves. They are found in a wide saprobic variety of freshwater habitats from totally unpolluted streams up to very organically polluted rivers and thus the species has no saprobic value (Graf et al., 2002; Ćuk, Vučković, 2010). I. dubia has no legal protection in annexes of EU directives but is listed as rare, threatened, presumably vulnerable or critically endangered in Denmark, Carinthia (Austria), some cantons of Germany and Hungary and it is also a priority species within the United Kingdom Biodiversity Action Plan (e.g. Nogradi, Uherkovich, 1999; Shirt, 1987). It is given the IUCN category of Critically Endangered in the United Kingdom in Wallace (2016). Wallace (2011) summarised information on the species. The goal of this paper is to give an overview of the composition of the caddisfly fauna of the Blinajë Hunting Reserve and also to compare species composition by using two different sampling techniques for adult caddisflies: ultra-violet light trap and hand searching and netting. The composition of the macrozoobethos during the spring and winter period has also been investigated. Another goal of this paper is to contribute to the knowledge on biogeographic distribution, ecological features and population characteristics of I. dubia in South-eastern Europe.
MATERIAL AND METHODS
Sample collection and processing Adult caddisfly specimens were collected with entomological net, sweeping net, handpicking and ultraviolet light trap. The sampling was carried out during the period May-December 2013. Collected samples were preserved in 80% ethanol. The specimens were identified under a stereomicroscope with determination keys from Malicky (2004) and Kumanski (1985; 1988). The collection is deposited at the Laboratory of Zoology of the Faculty of Natural and Mathematical Sciences, University of Prishtina, Kosovo. In order to verify the presence of larvae of I. dubia, macrozoobenthos specimens were collected with standard Surber net and D-net from the bottom of the stream during 2013 twice, during March and December, from various microhabitats in the investigated area. Macrozoobenthos specimens were not conserved but were released back to their habitat.
Study site The sampling site is located at the spring area of the only stream inside the Blinajë Hunting Reserve, adjacent to the biggest lake (Table 1). This first order stream is surrounded by a forested area, is in average about 1.2 m wide and 15 cm deep. A significant portion of the water from the spring goes directly through a pipe for use in the Administration Office of the Blinajë Hunting Reserve. The remaining water flows beside the lake and discharges near Lipjan town into Sitnicë River. The substrate is made by gravel, cobles and boulders surrounded by fine particles and is shaded 13 A Study of Trichoptera of the Blinajë Hunting Reserve throughout the year by nearby vegetation. The amount of the water during the summer significantly decreases and according to the information from the staff working in this hunting reserve, during some years the amount of flowing water is very low or absent at all giving the stream the characteristics of a temporary stream. Table 1. Locality and habitat assessment data after Plafkin et al., (1989) and Barbour et al., (1999) for the sampling station in Blinajë Hunting Reserve.
Parameters Sampling stacion characteristics
Latitude ˚N 42.5185˚N
Longitude ˚E 20.9788˚E
Altitude m 721
Distance from source (m) 5
Stream width (m) 1.2
Stream depth (cm) 15
Epifaunal substrate/ More than 50% of substrate favorable for epifaunal colonization and fish cover; mix of snags, submerged logs, Available cover undercut banks, cobble or other stable habitat and at stage to allow full colonization potential.
Embedeness Gravel, cobble and boulder particles are 20-50% surrounded by fine sediment.
Pool Substrate Mixture of soft sand, mud, or clay; mud may be dominant; some root mats and submerged vegetation present. Characterization Little or no enlargement of islands or point bars and less than 20% of the bottom affected by sediment Sediment deposition deposition.
Flow status Water fills 25-75% of the available channel, and/or riffle substrates are mostly exposed.
Bank stability Banks stable; evidence of erosion absent or minimal; <5% of bank affected.
More than 90% of the streambank surfaces and immediate riparian zones covered by native vegetation, Bank vegetation protection including trees, understory shrubs, or nonwoody macrophytes; vegetative disruption through grazing or mowing minimal or not evident; almost all plants allowed to grow naturally
Riparian vegetative zone Width of riparian zone >18 meters; human activities (i.e., parking lots, roadbeds, clear-cuts, lawns, or crops) width have not impacted zone.
RESULTS Two sampling methods for collecting adult caddisflies were applied in parallel: a) with entomological net, sweeping net and handpicking, and b) with UV light trap. Two hundred and thirty specimens (Table 2) belonging to thirteen caddisfly species were found with the first method. Fourteen caddisfly species with one hundred and eighty two specimens (Table 2) were sampled with the second method. Species collected only during the daylight with the first method are:Hydropsyche angustipennis (Curtis, 1834), Athripsodes billineatus (Linnaeus, 1758), Mystacides azureus (Linnaeus, 1761), Mystacides niger (Linnaeus, 1758) and Helicopsyche bacescui Orghidan, Botosaneanu, 1953 (Table 2). Seven species were found only with UV light trap: Rhyacophila fasciata Hagen, 1859, Grammotaulius nigropunctatus (Retzius, 1783), Halesus digitatus (von Paula Shrank, 1781), Limnephilus vittatus (Fabricius, 1798), Micropterna sequax McLachlan, 1875, I. dubia and Potamophylax pallidus (Klapalek, 1899) (Table 2). The last specimen of I. dubia was found on 25.11.2013. 14 Ibrahimi, H., Grapci-Kotori, L., Kučinić, M., et al.
Table 2. The list of species collected with entomological net, sweeping net and handpicking (D) and ultraviolet light trap (N) in Blinajë Hunting Reserve during the period May-December 2013.
Months May June July August September October November December
Species ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂
Rhyacophila fasciata Hagen, 1859 4 N 2 N 1 N 2 N 3 N 1 N
12 D 12 D 4 D 8 D Wormaldia occipitalis (Pictet, 1834) 5 D 4 D 13 N 6 N 6 N 3 N
Hydropsyche saxonica McLachlan, 1884 1N 3 N
Hydropsyche angustipenis (Curtis, 1834) 2 D 4 D
16 D Hydropsyche spp. 11 N 7 N 6 D 2 N 13 N
Cyrnus trimaculatus (Curtis, 1834) 4 D 5 D 14 D 7 D 5 D 3 D
Polycentropus flavomaculatus (Pictet, 1834) 1 D 2N
3 D Tinodes janssensi Jacquemart, 1957 2 D 5 D 2 N 2 N 5 D 2 D 2 D 6 D Chaetopteryx bosniaca Marinkovic-Gospodnetic, 1959 3 D 11 N 2 N 8 N 1 N
Grammotaulius nigropunctatus (Retzius, 1783) 3 N
Halesus digitatus (von Paula Shrank, 1781) 4 N 8 N 7 N 3 N
Ironoquia dubia (Stephen, 1738) 1 N 1 N
3 D Limnephilus vittatus (Fabricius, 1798) 1N
Micropterna nycterobia McLachlan, 1875 5N 7N 1 D 8N 7N 2N
Micropterna sequax McLachlan, 1875 5 N 2 N
Potamophylax pallidus (Klapalek, 1899) 2 N 11 N 5 N 7 N 1 N 1 N 2 N 5 N 1 N
Athripsodes bilineatus (Linnaeus, 1758) 3 D 11 D
Mystacides azureus (Linnaeus, 1761) 12 D 21 D 11 D 12 D 4 D 6 D
Mystacides niger (Linnaeus, 1758) 6 D 12 D
Helicopsyche bacescui Orghidan & Botosaneanu, 1953 1 D
In total, specimens of I. dubia represent only 0.48% of the total caddisfly specimens collected with both methods during the whole sampling period of 2013 year. Specimens of I.dubia represent 1.09% of the total caddisfly specimens collected with UV light trap during the sampling period. The macrozoobenthos is composed by the following groups: Trichoptera with six families, Plecoptera with three families, Ephemeroptera with three families, while Odonata, Diptera, Amphipoda and Gastropoda are represented each with one family only (Table 3). Only one larvae of I. dubia has been found during the sampling period of macrozoobenthos.
DISCUSSION Out of twenty taxa found during this investigation most are common and widespread species in the Balkan Peninsula and Europe. Most of the found species belong to the family Limnephilidae due to the characteristics of the stream: slow flow, low water level throughout the year and large quantities of food available for larvae of these species. It was noted the absence of species of the Rhyacophilidae family with the exception of R. fasciata which is a generalist occurring in different habitats. Most of the species of this family usually require fast flowing streams with high water level. Three species found during this investigation are notorious in terms of their scarce distribution in 15 A Study of Trichoptera of the Blinajë Hunting Reserve the Balkan Peninsula: Tinodes janssensi Jacquemart, 1957, Chaetopteryx bosniaca Marinkovic-Gospodnetic, 1959 and Ironoquia dubia. The endemic species of the Balkan Peninsula, T. janssensi beside Blinajë Hunting Reserve is only found in few localities in Albania, Greece and Kosovo (e.g. Ibrahimi et al., 2016a). The autumn limnephilid species C. bosniaca found during the autumn-winter period has been rarely sampled in Kosovo but also elsewhere in the Balkan Peninsula as well (e.g. Ibrahimi et al., 2015). However the most important faunistic finding during this investigation was the record of I. dubia. Table 3. The composition of the macrozoobenthos in the Blinajë Hunting Reserve during March and December 2013.
Taxa / Sampling month March December Taxa / Sampling month March December
Trichoptera Ephemeroptera
Rhyacophilidae 5 12 Baetidae 13 21
Philopotamidae 2 3 Ephemeridae 12 8
Hydropsychidae 19 8 Leptophlebidae 8 5
Psychomyiidae 8 Odonata
Leptoceridae 18 3 Gomphidae 5
Limnephilidae 31 19 Diptera
Ironoquia dubia 1 Tipulidae 2 1
Plecoptera Amphipoda
Perlidae 3 14 Gammaridae 11 13
Nemouridae 12 Gastropoda
Chloroperlidae 15 2 Lymnaeidae 2
The known distribution range of I. dubia in Europe (Fig. 1) extends over the United Kingdom, central and northern Europe up to Caucasus (Graf et al., 2015). It has been suggested that this species is absent from South-eastern Europe (e.g. Reding, 2006) but this seems to be incorrect proven by recent Croatian records (Čuk, Vučković, 2010) and current investigation. Our finding of this species is the first genus and species record for the Republic of Kosovo. It is reported for the first time from Ecoregion 6, Hellenic Western Balkans. I. dubia has been reported for the first time from several European countries and regions only during the last decade (e.g. Reding, 2006; Roos, Semmler-Elpers, 2008). Despite intensive caddisfly investigations in more than 100 sampling sites all over Kosovo during 2010 - 2016 including streams, brooks, rivers, standing waters, temporary waters and lakes I. dubia has not been found anywhere else up to now (e.g. Ibrahimi et al., 2007; 2013; 2014; 2015; 2016b; 2016c; Ibrahimi, Gashi, 2008). This suggests this species is extremely rare in Kosovo. In total, during the whole sampling period with entomological net, sweeping net, handpicking and UV light trap only two males have been found. However, this is usually a very secretive species and difficult to collect as an adult. At Millbarn Pond over several years only a single adult specimen was sampled among thousands of caddisflies (e.g. Crichton, 1960; 1965). Hiley (1970) reports larvae from the stream only a few metres from the 16 Ibrahimi, H., Grapci-Kotori, L., Kučinić, M., et al. light trap site, but running in a deep channel below it. Crichton, Baker (1959) cite communications with Swedish colleagues that suggest I. dubia adults never leave the stream bed during flight. Vick (1992) collected many adults in a Malaise Trap set close to the stream bed. However this situation is totally different in a locality in south east Norway, where this species was collected in large numbers as a dominant species (Andersen et al., 1990). Čuk, Vučković, (2010) report I. dubia larvae from 30% of the streams they investigated indicating thus that it is easier to collect it in larval stadium. However during our investigation even the standard methods in collecting macrozoobenthos did not produce a significant number of larvae of this species. Only one larvae of this species was found during March around the leaf package close to the stream shore. This indicates that either the species is relatively rare in this site or more efforts are needed in collecting larger number of specimens. It has been reported that I. dubia has a short flight period from the middle of September to the first week in October (Higler, 2008). The last specimen of Ironoquia dubia during our investigation was found during the third week of November. This implies that at least in Kosovo, I. dubia has longer flying period than previously thought. This may also depend on the weather conditions from year to year since it was observed in other species that during the years with higher temperatures during the late autumn months, the flying period of adult caddisflies is extended.
Fig. 1. Distribution of Ironoquia dubia in Europe (full circles-data from DAET 2014, Čuk, Vučković 2012, Urbanić, 2001; 2006), square - distribution in Kosovo (current investigation). 17 A Study of Trichoptera of the Blinajë Hunting Reserve By implying two different methods in collecting adult caddisflies the number of found species has been significantly increased. There is a significant difference in qualitative composition of caddisfly samples collected by applying two mentioned methods. The coefficient of similarity is only 40%. It is known that adult caddisflies of different species express their activity during the different parts of the day and thus many species often remain unexplored because only one particular method is used in sampling. Our investigation proves the importance of using different sampling techniques for adult caddisflies in alpha diversity studies. Finding of a rare species such as I. dubia during this investigation is a result of a combination of different sampling techniques. This was noted earlier as well, for example in Brezne Lake in Kosovo, where by implying different sampling techniques a rare species in the Balkan Peninsula, Triaenodes bicolor (Curtis, 1834) has been found (Ibrahimi et al., 2017). According to the predictions of Chao1 diversity index (Chao, 1984) when first samples contain several species with singletons, there are high chances that in these sites are hidden other species with low population densities. This was the case during this investigation and consequently, increased sampling efforts and especially different sampling techniques were proved to be a successful tool in sampling these species with small populations. This research shows that there are still poorly investigated areas in the Balkan Peninsula which contain rare or less known species of caddisflies. In addition to this, this investigation proves that application of different sampling techniques results in discovery of more species and especially those with small populations which are usually overlooked when only one particular method in collecting caddisflies is implied. This investigation highlights the Blinajë Hunting Reserve as an important area in regards to the caddisfly species. Some of them found during this investigation, or those reported earlier (Ibrahimi et al., 2016a or b) are rarely sampled in Kosovo or in the Balkan Peninsula in general.
ACKNOWLEDGEMENT We want to thank Professor Hans Malicky for verifying specimens of Ironoquia dubia. We also thank two anonymous reviewers whose comments and suggestions significantly improved this manuscript.
REFERENCES
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Reding, J. P., 2006, Notes faunistiques sur Metreletus balcanicus (Insecta: Ephemeroptera) et Ironoquia dubia (Insecta: Trichoptera), Deux especes d’Insectes aquatiques du jura nouvelles pour la Suisse. Bulletin de la Societe Neuchateloise des Sciences Naturelles, 129: 73-86. Roos, P., Semmler-Elpers, R., 2008, Erster Nachweis von Ironoquia dubia (Stephens, 1837) (Trichoptera, Limnephilidae) fur Baden-Wurttemberg. Lauterbornia, 62: 129-130. Shirt, D. B., (Eds.) 1987, British Red Data Books 2. Insects. Peterborough, Nature Conservancy Council, 402. Svensson, B.W. 1974, Population movements of adult Trichoptera at a South Swedish stream. Oikos 25: 157-175. Urbanič, G., 2001, Contribution to the knowledge of caddisflies (Trichoptera) of the reservoir Ledavsko Jezeri, NE Slovenia. Acta Entomologica Slovenica, 9(2): 129-134. Urbanič, G., 2006, Distribution and structure of Trichoptera assemblages in the ecoregion “Hungarian Lowland” in Slovenia. Proceedings of the 36th International Conference of the International Association for Danube Research, 9-21. Usseglio-Polatera, P., 1986, The comparison of lght trap and sticky trap captures of adult Trichoptera in Proceedings of the 5th International Symposium on Trichoptera Series Entomologica, 39: 217-220. Vick, G. S., 1992, The caddisfly Ironoquia dubia (Stephens) in Britain (Trichoptera: Limnephilidae). Entomologist’s Gazette, 43: 297-302. Wallace, I. D., 2011, Species dossier: Ironoquia dubia. https://www.buglife.org.uk/sites/default/files/ Ironoquia%20dubia%20species%20dossier.pdf (03.12.2017) Wallace, I. D., 2016, A review of the status of the caddis flies (Trichoptera) of Great Britain (NECR191) http://publications.naturalengland.org.uk/publication/5436150266200064 (03.12.2017)
Received: July 28, 2016 Accepted: December 04, 2017
J. Entomol. Res. Soc., 20(1): 21-49, 2018 ISSN:1302-0250
Comparative Morphology and Morphometry of Badister (s. str) Species (Coleoptera: Carabidae), Occur in Baltic States, with Notes on Their Distribution in Local Fauna
Vytautas TAMUTIS1,2 Maksims BALALAIKINS3 Arvids BARŠEVSKIS3 Romas FERENCA1
1Kaunas Tadas Ivanauskas Zoological Museum, Laisvės al. 106, LT-44253 Kaunas, LITHUANIA. e-mail: [email protected] 2Aleksandras Stulginskis University, Studentu 11, LT-53361 Akademija, Kaunas distr., LITHUANIA. e-mail: [email protected] 3Daugavpils University, Institute of Life Sciences and Technology, Coleopterological Research Center, Vienības street 13, Daugavpils, LATVIA e-mails: [email protected]; [email protected]
ABSTRACT The results of studied problems of identification and distribution in the Baltic countries of four species of Badister (s. str.) subgenus: B. unipustulatus, B. meridionalis, B. bullatus, and B. lacertosus, are presented in the current paper. The relevance of a number of diagnostic body traits both in males and females is widely discussed and illustrated by original drawings. The morphological traits of some structures of the reproductive tract of females and their utility for identification of species have described for the first time. Based on analysis of published sources and on available material, the distribution of these species in Estonia, Latvia and Lithuania is specified and reviewed. Key words: Coleoptera, Carabidae, Badister, taxonomy, fainistical review, Baltic countries.
INTRODUCTION The genus Badister Clairville, 1806 is included to the tribe Licinini which comprises of 235 species worldwide that had been identified until 2005 (Lorenz, 2005). The ground beetles of this tribe are characterized by modified mouthparts (the mandibles are robust and shorter than in other ground beetles) and by more or less flattened head (Ball, 1959). Three subgenera which are characterised by the following details of mandibular structure and tarsal setation are classified within the genus: right mandible with dorsal surface notched and tarsomere 5 with row of setae on ventro-lateral margin (Badister (s. str.); right mandible with dorsal surface notched and tarsomere 5 with ventro-lateral margins asetose (Trimorphus Stephens, 1828); and left mandible notched and tarsomere 5 with ventro-lateral margins asetose (Baudia Ragusa, 1884) (Ball, 1959). By the number of species, it is a relatively small genus worldwide presently comprising 48 species placed in 3 subgenera: Badister (s. str.); 23, Trimorphus; 3, and Baudia; 22 (Anichtchenko et al., 2007-2017). Among 26 species distributed in 22 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F. the Palaearctic region, only 11 occur in Europe (Baehr, 2003). Nine species having wider distribution ranges are known in the Baltic countries as well (Silfverberg, 2010). Despite a small number of species and a relatively large body size, the taxonomy of this genus has quite a controversial history and is problematic till nowadays. Generally, the faithful identification of all EuropeanBadister species is based on the morphology of male genitalia (Makólski, 1952; Komarov, 1991; Hurka, 1996; Assman, 2004) while females remain poorly identifiable. Four species of subgenus Badister (s. str.) are reported in the Baltic countries (Silfverberg, 2010). Indeed, the extant distribution of these species is difficult because they are very similar morphologically and often are not identified safely. Although the morphology of the European species ofBadister (s. str.) is described and the keys of their identification are well presented in several most recent publications (Komarov, 1991; Hurka, 1996; Assman, 2004; Puchkov, 2013), however some morphological characters are specified differently or even controversially and make some confusion for users. Indeed, no particular attention to Badister species has been paid in the Baltic countries before, and available knowledge is far from the real situation of their prevalence in the territory of this region. Such circumstances were the main reason to compile a comprehensive review of ground beetles of Badister (s.str.) genus in the Baltic countries. Seeking trustworthy identification, we aimed to study the morphological structures of adults, both males and females, from different regions of Europe, to compare the variance of body and genitalic characters between and within species, and to find correct morphological characters which could be useful for an easier identification of “problematic” species.
MATERIAL AND METHODS
Specimens examined All available specimens deposited in collections of museums and scientific institutions and held by private collectors in Baltic countries were examined in this study: altogether 583 specimens. The material from the following institutional and private collections was examined: Kaunas Tadas Ivanauskas Zoological Museum, Lithuania (KZM), Latvian Museum of Natural History, Latvia (LMNH), Daugavpils University, Coleopterological Research Centre, Latvia (DUBC), Estonian Museum of Natural History, Estonia (EMNH), Private collection of Florian Savich (FS), University of Latvia, Faculty of Biology, Zoology and Animal Ecology Department (LUFB); Private collection of Alexander Napolov (AN), Private collection of Aleksandr Meržijevskij. Additionally, the specimens for comparative studies were loaned from the following collections: Berlin Nature Museum, Germany (BNM): 27 specimens of B. meridionalis, Bavarian State Collection of Zoology, Germany (BSCZ): 9 specimens of B. bullatus and 1 specimen of B. lacertosus), Museum and Institute of Zoology, Polish Academy of Science (MIZPAS): 5 paratypes of Badister kineli Makólski, 1952, Private collection of Dr. Oleg Aleksandrowich (Poland) (OA): 2 specimens of B. meridionalis, and Private collection of H. Ljungberg (Sweden) (HL): 1 specimen of B. meridionalis. The classifications of chorotypes were used following Gorodkov (1983). 23 Comparative Morphology and Morphometry Dissection and depiction methods Male and female genitalia were prepared for the study following the instruction described by Liebherr and Will (1998) and Will (1998). Male genitalia were removed after softening the specimens. For this reason dry specimens were placed in 70-80°C temperature water for 30-60 minutes, than using stereo-microscope and dissecting needles was made section throughout membrane between 5th and 6th abdomen tergites. Removed genitalia gently cleared in 50°C of 10% KOH for 10-15 minutes. Further dissections of genitalia were done in the drop of glycerine after neutralization of dissected material by 10% acetic acid and dehumidification. Females were softened like males, than using the same entomological equipment dissected abdomen throughout pleural membrane and removed dorsal part of abdomen with entrails. Removed material was cleared in 50°C of 10% KOH for 10-15 minutes.Further dissections of females genitalia were done in the drop of distilled water after neutralization of dissected material by 10% acetic acid. Dissected genitalia plus reproductive tract was placed in a saturated Clorazol Black® dye and distilled water solution. Than tracts were slide mounted in glycerine and examined using phase-contrast compound microscope. Examined genitalia and reproductive tracts both males and females were placed in genitalia micro vials in glycerine and pinned on the same pin as examined specimen. The terms for the parts of genitalia are either standard among carabidologists or taken from Ball and Shpeley (2009) and Erwin and Ball (2011). Drawings were made using an ocular grid. A stereomicroscope SMZ-168 Motic, digital camera Nicon D3100, and digital camera Canon EOS 400D DIGITAL with objective Canon EF 100 mm f/2.8 L IS USM were used for taking photographs. A confocal laser scanning microscope Zeiss LSM 5 Pascal and its software LSM 5 Pascal Release version 4.0 were used for the investigation of surface structures of elytra and acquisition of pictures. Distribution maps were prepared with the ArcGIS software.
Morphometric analyses All measurements were made using a stereoscopic microscope Motic and a calibrated ocular grid with magnification of 40 and 20 times. For each measured specimen, seven distance variables were measured, including: width of head (WH), measured between inner margins of eyes (shortest distance); length of head (LH), measured along the midline from the apical margin of the clypeus to the cervical suture; length of pronotum (LP), measured midline from the apical margin to the basal margin; width of pronotum (WP), measured latitudinal distance beside the insertion of midlateral setae (widest distance); width of elytra (WE), measured maximum width of both elytra combined; length of elytra (LE), measured from the humeral carina to the apical margin (tips) of elytra; longitudinal distance between the humeral carina of elytra and the anterior side of the lunular black spot of elytra (BS); and length of body (LB), measured from the apical margin of the clypeus to elytra tips, or LB = LH+LP+LE. The scheme of morphological measurements of the body and used special terms of genitalia of Badister (s. str.) species are given in figures (Figs. 1, 2). For statistic analysis, we used software Past version 3.11 (Hammer, 1999-2015). 24 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Fig.1. Habitus of B. meridionalis specimen collected in Sweden: KZM, IC-68557 and scheme of morphological measurements.
Fig. 2. Scheme of used special terms of genitalia of Badister (s. str.) species: b. ventral aspect of the reproductive tract of female of B. bullatus (KZM, IC-60106), b. ventral aspect of a complex of right gonocoxites and laterotergite of female of B. meridionalis (paratype of B. kineli) (MIZPAS, Pol-2); c. ventral aspect of the left paramere of B. unipustulatus (KZM, IC-60113); gc: gonocoxite, m: length f inner margin of gonocoxite 2, h: width of gonocoxite 2; scale 100μm. For graphically depicting groups of numerical data through their quartiles we used a boxplots. The length of the box is the interquartile range (IQR). A line inside the box is a median. The boundaries of the box are Tukey’s hinges. An asterisk (*) is an extreme outlier that is calculated as the value more than 3 IQR’s. A circle (○) is an outlier that is calculated as the value more than 1.5 IQR’s but less than 3 IQR’s. Usually, extreme outliers are taken away from analysis but not in this case due to limited data in the analysis.
RESULTS
Review of the material 25 Comparative Morphology and Morphometry Subgenus Badister sensu stricto Clairville, 1806
B. (s. str.) unipustulatus Bonelli, 1813
Examined material. Estonia: Tartu: Emajõgi, 23.04.1938 leg. H. Kuusik (1 ♂, EMNH); Ropka, 09.1831 leg. H. M. Asmuss (1 ♂, EMNH); Tartu, 05.1846 leg. H. M. Asmuss (1 ♀, EMNH); Valga: Helme, 2.07.1956 leg. R. Marivae (1 ♀, EMNH), 22.04.1958 leg. E. Marivae (1 ♀, EMNH), 12.06.1965 leg. O. Marivae (1 ♂, EMNH); Latvia: Aglona: Šķeltova, 26.08.1985, 5.04.1986 leg. A. Barševskis (1♂, 1 ♂, DUBC); Carnikava: Kalngale, Garciems, 3.05.1995 leg. R. Matrozis (2♀♀, FS); Daugavpils: Elerne, 30.09. 1993 leg. A. Barševskis (1 ♂, DUBC); Ilgas, 8.04.1994, 21-24.04.1995, 5.07.1995, 18.06. 1996 leg. A. Barševskis (2 ♂♂/1 ♀, 1 ♀, 1 ♂, 1♂, DUBC), 16.06.2008 leg. R. Cibulskis (2 ♀♀, DUBC), 8.04.1994 leg. F. Savich (1 ♂, FS); Slutišķi, 10.06.1996 N. Savenkovs (1 ♀, DUBC); Vabole, 20.07.1994, 14.10.1994 leg. R. Cibulskis (1 ♂, 1 ♂, DUBC); Gulbene: Stradi, Pededze Lower Reaches Nature Reserve, 06.2001 leg. A. Napolov (1 ex., AN); Ilūkste: “Straumēni”, 16.03.2008, 23-26.06.2010 leg. M. Janovska (1ex., 2 ♂♂, DUBC); Jēkabpils: Dunava, 10-13.08.1995, 24.08.1995 leg. A. Barševskis (1 ♂, 1 ♀, DUBC); Jelgava: Jelgava, 1.05.1997 leg. R. Matrozis (1 ♀, FS); Riebiņi: Stabulnieki, 20.04.1991 leg. A. Barševskis (1 ♂, DUBC); Rīga: Daugavgrīva isl., Garciems, Garupe, 29.05.1994, 3 05.1995, 16.05.1995 leg. R. Matrozis (2♀♀/1♂, 1 ♀, 1 ♀, FS); Gauja, Garupe, 25.05.1996 leg. F. Savich (5 ♀♀/1♂, FS); Talsi: Mazirbe, 06.2002, leg. A. Barševskis (1 ex., DUBC); Ventspils: Moricsala Nature Reserve, 05.2003 leg. U. Valainis (1 ex., DUBC); Lithuania: Akmenė: Kamanos Strict Nature Reserve, 15.05.1991, 18.07.1991, 18.10.1991 leg. Vidm. Monsevičius (1 ♂, 1 ♂, 1 ♀, KZM); Alytus: Punios šilas forest, 27. 06.2008 leg. V. Tamutis (1 ex., KZM); Jonava: Šėta, 08.1954 leg. S. Pileckis (1 ♀, KZM); Kazlų Rūda: Kazlų Rūda, 23.03.1966 leg. E. Gaidiene (1 ♂, KZM); Kaunas: Braziūkai, 15 08.2015 leg. V. Tamutis (5 ♂♂/3 ♀♀, KZM); Dubrava forest, 11.05.1999, leg. P. Zolubas (1 ♀, KZM); Margininkai, 2.07.1997 leg. V. Tamutis (1 ♂, KZM); Romainiai, 7.04.1966 leg. E. Gaidienė (3 ♂♂, KZM); Klaipėda: Giruliai, 20.04.1994, leg. S. Karalius (1 ♂, KZM); Neringa: Lapnugaris Landscape Reserve, 20.06.2007 leg. R. Ferenca (1 ♀, KZM); Pervalka, 2.06.1995 leg. B. Šablevičius (1 ♀, KZM); Palanga: Monciškė, 9.05.2001, 27.06. 2010 leg. R. Ferenca (1 ♀, 1 ♀, KZM); Plungė: Grigaičiai, 7.10.1998 leg. A. Gedminas (1 ♀, KZM); Tauragė: Buveiniai lake env., Viešvilė Strict Nature Rezerve, 27.07.2008 leg. V. Tamutis (1 ex., KZM); Utena: Antalgė, 26.04.1977, leg. A. Kaulinis (1 ♂, KZM). Additional material. Germany: Brandenburg Nauen, 29.03.1910 leg. M. Ude (2 ♀♀, BNM). Published records. Estonia: Harju, Pärnu, Tartu, Valga (Haberman, 1968); Hiiumaa (Miländer, 1993). Latvia: Livland, Curland (Seidlitz, 1872, 1887); Liepāja,Ventspils (Lackschewitz and Mikutowicz, 1939); Rīga (Stiprais, 1973); Garciems, Kalngale (Stiprais, 1975); Sigulda (Spuris, 1975); Melluži, Jurmala (Stiprais, 1984); Šķeltova (Barševskis, 1987); Šķeltiņi (Aglona), Stabulnieki (Riebiņi) (Barševskis, 1993), Līksna, Vabole, Daugavpils (Cibuļskis, 1994); Moricsala Nature Reserve (Barševskis et al., 2004); Gauja National Park (Kalniņš et al., 2007); Šedere (Barševskis et al., 2008); Mazirbe (Talsi), Ilgas (Daugavpils) (Barševskis et al., 2009); Butiški (Bukejs, 2011). Lithuania: Kaunas (Heyden, 1903); Žuvintas Nature Rezerve, Alytus, Meteliai (Sharova and Grüntal, 1973), Juodkrantė, Neringa (Žiogas, Zolubas, 2005), Description. The body pattern is typical of this group of species: black-colored head, metathorax, abdomen, and a single entire or divided transversely semi-lunular spot on each elytron and yellow-red pronotum, scutellum, mesothorax, and the remaining part of elytra, palpi and legs. Antennomeres are often red-brown or yellow-red, usually 2-6 antennomeres and the last palpomeres are darkened. The black pattern of elytra is usually composed of two spots on each elytron: a large irregular spot beside the middle and a narrow, falcate spot along the posterior margin of elytra (Fig. 3a, ♂). Occasionally, these spots join on 1-2 last marginal intervals in the anterior third of elytra by a slightly darkened interval (Fig. 3a, ♀). The larger spots on elytra vary in the shape of the front margin, which can be straight transversely, denticulate or convex, while their posterior margin usually has a constant distinct protrusion beside 5-7 rows of elytra. The row of distinct setae is visible on the apical margin of elytra (Fig. 4a). 26 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Fig. 3. Scheme of the pattern of elytra: a. ♂ - B. unipustulatus (KZM, IC-68686), a. ♀ B. unipustulatus (KZM, IC-1932), b. ♂ B. meridionalis (paratype of B. kineli) (MIZPAS, Pol-1), b. ♀ B. meridionalis (BNM, Ger-B-18), c. ♂ B. bullatus (KZM, IC-68680), c. ♀ - B. bullatus (KZM, IC-60109); d. ♂ B. lacertosus (KZM, IC-68680), d. ♀ B. lacertosus (KZM, IC-60118); scale 1mm.
Fig. 4. Fragment of the apex of elytra: a. B. unipustulatus (KZM, IC-11514), b. B. meridionalis (paratype of B. kineli) (MIZPAS, Pol-3). The microsculpture of elytra is very fine, composed by very fine transversal fissures, the contours of which are blind even magnified 150 times. Four to five fissures are distributed along the distance of 10 μm of the surface of elytra (Fig. 5a). The surface of elytra is strongly iridescent. The length of bodies is quite similar among genders: 6.1-7.3 mm of males and 6.4-7.4 mm of females. The sexual dimorphism is distinct. Despite the dilated first three tarsomeres of males, the bodies of both genders slightly differ in shapes of their parts. The WH and LH in males average 1.132 and 1.102, respectively, and are significantly lower compared to those in females (U = 56.5; p < 0.01; U = 15.5; p < 0.001). The pronotum slightly differs in the straightness of lateral margins and roundness of posterior angles (Fig. 6a), but its width and length values in males (1.96 and 1.288 mm, respectively) are not significantly differing from those in females (Table 1). However, the ratio of LH/LP in males is 0.86, and it is significantly lower than in females (U = 30; p < 0.001). The ratio of LP/WP in males is about 0.657, which is significantly higher than in females (U = 51.5; p < 0.001). The females have significantly wider elytra (U = 81.5; p < 0.0259). The distance between the anterior 27 Comparative Morphology and Morphometry margin of the base of elytra and the anterior side of the lunular black spot of elytra (BS) in males is about 1.517 mm, which is significantly shorter than in females (U = 73.5; p < 0.0107). The median lobe of the aedeagus is distinctly asymmetric in ventral view (Fig. 7a), apically inclined ventrally with an inflated protuberance (Fig. 9a). The left paramer is wide, its proximal margin is broadly rounded, and apical margin is slightly convex, with distinct indentation in the basal part of the proximal margin (Fig. 8. a). The right paramer is triangular, its proximal margin is slightly rounded (Fig. 10. a). The genital ring is wide and oval, rather asymmetric, with a fairly short apex which is curved right (Fig. 11a). Gonocoxite 1 is triangular, funnelform, the inner margin is gradually convex, without distinct punctation. Gonocoxite 2 is elongated, rather curved, blade sharp in the apex; a dorso-median ensiform, slightly curved seta is situated slightly above the middle of the gonocoxite. All setae located on the apical margin of the ventral surface of laterotergites are directed forward, more or less perpendicular to the margin.
Fig. 5. Fragments of the first half of the base of surface of elytra (intervals are numbered): a. B. unipustulatus (KZM, male, IC-68687), b. B. meridionalis (KZM, male, IC-68335), c. B. lacertosus (KZM, male, IC-68205; d. B. bullatus (KZM, male, IC-68219)
Fig. 6. Pronotum: a. B. unipustulatus (♂ KZM, IC-68920; ♀ KZM IC-20346); b. B. meridionalis (♂ paratype of B. kineli, MIZPAS, Pol-3; ♀ paratype of B. kineli, MIZPAS, Pol -2); c, d B. bullatus (c, ♂ KZM IC- 68223, d, ♂ KZM, IC-60108, c, ♀ KZM, IC-68226; d, ♀ KZM, IC-60103); e. B. lacertosus (♂ KZM, IC-60123, ♀ KZM, IC-60116); scale 500μm. 28 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Table 1. Sex differences in body traits (means and Standard Error of means) in four ofspecies Badister (s.str.). The Mann-Whitney test results are shown; with significance levels estimated using the permutation procedure (PMonteCarlo). Statistically significant results are in bold, M - males, F - females, N - number of specimens, LB - length of body, WH - width of head, LH - length of head, WP - width of pronotum, LP - length of pronotum, WE - width of elytra, LE - length of elytra, BS - distance between the base and the apical margin of the lunular black spot of elytra).
Species Traits Male Female Mann-Whitney test
MeanN SEM MeanN SEM U PMonteCarlo Z LB 6.79 17 0.063 6.87 17 0.060 103 0.2378 -1.174
WH 1.132 17 0.017 1.232 17 0.020 56.5 0.0016 3.060 LH 1.102 17 0.014 1.222 17 0.010 15.5 <0.001 -4.485 WP 1.96 17 0.024 2.019 17 0.021 94.5 0.0832 -1.721
LP 1.288 17 0.018 1.257 17 0.017 107.5 0.1926 -1.289
B. unipustulatus WE 2.761 17 0.036 2.894 17 0.044 81.5 0.0259 -2.218 LE 4.355 17 0.056 4.385 17 0.038 129.5 0.6193 -0.504
BS 1.517 17 0.014 1.594 17 0.026 73.5 0.0107 -2.491 Ratio LH/LP 0.860 17 0.020 0.973 17 0.011 30 <0.001 -3.934 Ratio LP/WP 0.657 17 0.008 0.622 17 0.005 51.5 <0.001 -3.190 3.385 Ratio LE/LP 17 0.036 3.494 17 0.036 89 0.051 -1.897
Ratio LE/BS 2.870 17 0.026 2.760 17 0.041 82.5 0.033 2.122 LB 6.19 22 0.078 6.18 19 0.047 169 0.9838 0.015
WH 0.93 22 0.016 0.99 19 0.012 77 0.0038 -2.85 LH 0.93 22 0.016 0.98 19 0.014 86 0.0078 -2.596 WP 1.75 22 0.025 1.78 19 0.022 159 0.7437 -0.322
LP 1.24 22 0.019 1.23 19 0.011 147 0.4866 0.700 WE 2.47 22 0.038 2.55 19 0.021 130 0.2176 -1.215 B. meridionalis LE 4.00 22 0.047 3.97 19 0.029 154.5 0.6509 0.463 BS 1.38 22 0.034 1.39 19 0.038 151.5 0.5754 -0.575
Ratio LH/LP 0.760 22 0.011 0.804 19 0.010 113.5 <0.011 -2.488 Ratio LP/WP 0.71 22 0.005 0.697 19 0.005 139 <0.068 -1.819 Ratio LE/LP 3.220 22 0.029 3.225 19 0.019 177.5 0.414 -0.811 Ratio LE/BS 2.910 22 0.053 2.872 19 0.070 169 0.293 1.033 LB 5.359 72 0.033 5.414 72 0.044 2118 0.0552 -1.90
WH 0.785 72 0.006 0.864 72 0.008 906.5 0.0001 -6.809 LH 0.824 72 0.007 0.882 72 0.009 1423 0.0001 -4.179 WP 1.59 72 0.010 1.629 72 0.015 2039 0.0264 -2.216
LP 1.165 72 0.008 1.171 72 0.010 2545 0.8502 -0.189
WE 2.139 72 0.022 2.186 72 0.019 2071 0.0360 -2.093 B. bullatus LE 3.361 72 0.023 3.368 72 0.027 2448 0.5604 -0.577 BS 0.965 72 0.010 0.960 72 0.012 2483 0.6572 -0.442
Ratio LH/LP 0.704 72 0.005 0.750 72 0.006 1328 <0.001 -5.142 Ratio LP/WP 0.738 72 0.002 0.720 72 0.002 1502 <0.001 -4.452 Ratio LE/LP 2.852 72 0.010 2.880 72 0.011 2398 0.363 -0.907 Ratio LE/BS 3.493 72 0.046 3.540 72 0.050 2475 0.5416 -0.605 29 Comparative Morphology and Morphometry
Table 1. Continued.
Species Traits Male Female Mann-Whitney test
MeanN SEM MeanN SEM U PMonteCarlo Z LB 6.217 21 0.050 6.295 21 0.079 173.5 0.2410 -1.171
WH 0.886 21 0.009 0.941 21 0.009 83 <0.001 -3.516 LH 0.883 21 0.009 0.939 21 0.014 110.5 0.0052 -2.828 WP 1.763 21 0.014 1.810 21 0.019 128 0.0206 -2.234
LP 2.279 21 0.010 2.271 21 0.015 207.5 0.7493 0.3218 WE 2.455 21 0.025 2.488 21 0.037 162.5 0.1473 -1.461 B. lacertosus LE 3.705 21 0.034 3.728 21 0.047 194 0.5167 -0.658 BS 1.152 21 0.020 1.133 21 0.022 197 0.5565 -0.585
Ratio LH/LP 0.691 21 0.006 0.732 21 0.009 95.5 0.0017 -2.979 Ratio LP/WP 0.726 21 0.005 0.702 21 0.005 119.5 0.01 -2.531 Ratio LE/LP 2.899 21 0.023 2.935 21 0.029 187 0.4063 -0.830 Ratio LE/BS 3.231 21 0.050 3.306 21 0.053 182.5 0.3367 -0.944
The posterior part of laterotergites is slightly prolonged, bell-shaped (Fig. 12a), well sclerotized. The reproductive tract is proximally with a short, broad, cap-shaped bursa copulatrix and a long C-shaped spermatheca with a coiled distal portion (Fig. 13a). Variations. A few variations of the pattern of elytra were previously noted for this species (Puel, 1925; Jeannel, 1942). But most of our examined specimens have the black lunular spot on elytra divided transversely by a narrower or wider space into a broad semi-rounded spot in the middle of elytra and a narrow, falciform spot in the apex. The shape and size of these spots slightly differ between individuals. The pronotum slightly varies by the shape of the lateral margin and basal angle both in males and females. The lateral margin can be almost straight or slightly convex on the posterior half of the pronotum. Posterior angles of the pronotum can be distinct or slightly rounded. No distinct variations in the structures of genitalia were detected.
Fig. 7. Aedeagus, ventral side: a. B. unipustulatus (KZM, IC-60113), b. B. meridionalis (BNM, Ger-B-16); c. B. bullatus (KZM, IC-60103), d. B. bullatus (KZM, IC-68227), e. B. lecertosus (KZM, IC-68685), scale 200μm. 30 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Fig. 8. Left paramere, ventral side: a. B. unipustulatus (KZM, IC-60113), b. B. meridionalis (BNM, Ger-B-16); c. B. bullatus (KZM, IC-60103), d. B. bullatus (KZM, IC-68227), e. B. lecertosus (KZM, IC-68685), scale 200μm.
Fig. 9. Aedeagus, lateral side: a. B. unipustulatus (KZM, IC-60113), b. B. meridionalis (BNM, Ger-B-16); c. B. bullatus (KZM, IC-60103), d. B. bullatus (KZM, IC-68227), e. B. lecertosus (KZM, IC-68685), scale 200μm.
Fig. 10. Right paramere, ventral side: a. B. unipustulatus (KZM, IC-60113), b. B. meridionalis (BNM, Ger-B-16); c. B. bullatus (KZM, IC-60103), d. B. bullatus (KZM, IC-68227), e. B. lecertosus (KZM, IC-68685), scale 200μm. Differential diagnosis. Badister unipustulatus is a well distinguished species among other Central European Badister (s. str.) species by parameters of a number of its body traits: largest head, widest pronotum, longest elytra, etc. However, sometimes small specimens of B. unipustulatus can be confused with B. meridionalis, or conversely 31 Comparative Morphology and Morphometry large B. meridionalis can be confused with B. unipustulatus. Especially it could happen in case of females. The most characteristic body traits of this species are a row of well visible setae on the apical margin of elytra (Fig. 4a) and longer blades of gonocoxite 2. Contrary to B. unipustulatus, the black lunule spot on elytra of B. meridionalis is generally complete, not divided transversely (Fig. 3b). General distribution. Euro-Sibero-Central Asiatic species widely distributed in Europe, from the coasts of the Mediterranean Sea in the south to southern Finland in the north (Lindroth, 1992; Hristovski and Guéorguiev, 2015); from British Islands in the west to Western Siberia in the east (Krizhanovskyj et al., 1995; Dudko, Lyubechanskii, 2002; Baehr, 2003), also known in Kazakhstan, Uzbekistan and Turkey (Baehr, 2003).
Fig. 11. Genital ring, ventral side: a. B. unipustulatus (KZM, IC-60113), b. B. meridionalis (BNM, Ger-B-16); c. B. bullatus (KZM, IC-60103), d. B. bullatus (KZM, IC-68227), e. B. lecertosus (KZM, IC-68685), scale 200μm.
Fig. 12. Right complex of gonocoxites and laterotergite of females: a. B. unipustulatus (KZM, IC-60112), b. B. meridionalis (paratype of B. kineli, MIZPAS, Pol-2); c. B. bullatus (KZM, IC-68226); d. B. bullatus (KZM, IC-60106); e. B. bullatus (KZM, IC-20345); f. B. lacertosus (KZM, IC-68338); g. B. lacertosus (KZM, IC-68332) 32 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Fig. 13. Reproductive tract of females: a. B. unipustulatus (KZM, IC-60112); b. B. meridionalis (BNM, Ger-B-15); c. B. bullatus (KZM, IC-60103); d. B. bullatus (KZM, IC-60106), e. B. bullatus (KZM, IC- 20314); f. B. lacertosus (KZM, IC-68338) , scale 75μm. Remarks. Contrary to the description of the elytral pattern of B. unipustulatus presented in previous well known identification keys of Central European Badister species (Makólski, 1952; Freude, 1976; Hurka, 1996; Assman, 2004; Arndt et al., 2011), almost all examined specimens have the semi-lunular spot on elytra divided into two parts transverselly. Similar observations on the pattern of elytra are described by Lindroth (1986) and Komarov (1991). Such aberration of B. unipustulatus was described and named ab. quadripustulatus by Letzner (1851). A second controversial point we found was on parameters of the head and the pronotum and their ratios described by Hurka (1996). This incongruence is perhaps related to different means of morphometrical measurements used in the studies.
Badister (s. str.) meridionalis Puel, 1925 Examined material. Livonia (a historical region on the eastern shores of the Baltic Sea): leg. Bolz (3 ♂♂/1♀, EMNH); Lithuania: Kaunas: Kamša forest, 3.05.1938 leg. A. Palionis (1 ♀, KZM), Nevėžis Lanscape Rezerve, 4.07.2007, leg. R. Ferenca (1 ♂ KZM). Additional material. Belarus: Žitkavičy: Hlupin, 20.07.2014 leg. A.V. Kulak (2 ♂♂, OA); Czech: Bohemia: Čelakovice, 1924 leg. Z. Tesar (1 ♂, KZM); Croatia: Gunja, 1929, 1930 leg. Bischoff (1 ♂, 1 ♂, BNM), Račinovci, 1930 leg. Bischoff (1 ♀, BNM); Germany: Brandenburg, Neuendorf, 12.05.1991 leg. W. Renner (1 ♀, BNM); Zarrentin am Schaalsee, 1.05.2005 leg. Materlik (1 ♂, BNM); Hungary: Kiskunsag, National Park Bugac, 06.1979, 12-13.06.1979 leg. Uhlig (8 ♂♂/7♀♀, 5 ♀♀, BNM); Poland: Warszawa: Goclawek, 23-25.03.1947 leg. J. Makolski (2 ♂♂/2♀♀, paratypes of B. kineli, MIZPAS); Sweden: Öland: Vickleby, 08.05.2000 leg. H. Ljungberg (1 ♂, HL); Ukraine: Kherson: Novochornomoria (label data: Falzfeinowo am Dniepr), 12.05.1914, 7.06.1914 leg. W. Ramme (1♂/1♀, BNM), Dnepropetrovsk: Pavlograd, Levadki evnironments, 10-20.06.1994, leg. V. Brygadyrenko (1♂/1♀, KZM). 33 Comparative Morphology and Morphometry
Published records: Estonia: Harju, Järva, Tartu, Valga (Haberman, 1968), these records were based on misidentified material which specimens belong to B. bullatus; Latvia: Ilgas (Daugavpils), Šķeltiņi, “Barševski” (Aglona), Jersika (Līvāni) (Barševskis, 1993), Līksna (Cibulskis, 1994), Gauja National park (Kalniņš et al., 2007), Skrīveri (Aizkraukle) (Bukejs et al., 2009), Sakas Island, Salas parish (Jēkabpils) (Bukejs, 2009), but these records were not confirmed in our study, because the material was not available. We related these records to B. bullatus as most presumable for this species. In Rubeņi (Leskina, 2000), Jersika (Barševskis et al., 2009), and these records were based on misidentified material, it was related to B. bullatus; Lithuania: Zarasai (Barševskis, 2001) not confirmed in our study, because the material is not available. We related this record to B. bullatus too. Description. The body pattern: black-colored head, metathorax, abdomen, and semi-lunular spot on each elytron and yellow-red pronotum, palpi, legs and the remaining part of elytra; however, scutellum and mesothorax can be red-yellow or entirely black. Antennomeres are often red-brown or yellow-red, usually the upper sides of antenomere 1, antenomeres 2-6 are completely and the last palpomeres partly darkened. The black pattern of elytra is composed of one semi-lunular spot on each elytron (Figs. 1, 3b); occasionally this spot is divided into two parts transversely. The interior margins of semi-lunules are curved and forming a yellow-red spot on both sides of the suture, which can vary in shape from round to trapeziform or rectangular (Figs. 1, 3b). The black semi-lunule is confined in the front usually by a broadly curved line running from the first row to the exterior side of the elytron (Figs. 1, 3b); occasionally this line is denticulate or bracket formed. The row of very short, indistinct setae is situated on the apical margin of elytra (Fig. 4b). The microsculpture of elytra is very fine, composed of very fine transversal fissures, the contours of which are blind even magnified 150 times. Five to six fissures are arranged along the distance of 10 μm of the surface of elytra (Fig. 5b). The surface of elytra is strongly iridescent. The sexual dimorphism is less distinct than that of B. unipustulatus. The length of bodies is quite similar among genders: 5.6-6.8 mm in males and 5.8-6.5 mm in females. However, WH and LH in males average 0.93 and are significantly lower compared to those of females (U = 77; p < 0.01; U = 86; p < 0.01). The pronotum slightly varies in straightness of lateral margins and roundness of posterior angles, but differences are weak among genders (Fig. 6b), the ratio of LP/WP is 0.697 of females and 0.71 of males (Table 1). However, the ratio of LH/LP in males is 0.76, and it is significantly lower that of females (U = 113.5; p = 0.011). The distance between the anterior margin of the base of elytra and the anterior side of the lunular black spot of elytra (BS) differs insignificantly between genders and the mean varies from 1.38 to 1.39 mm. The median lobe of the aedeagus is smooth and has a small kink directed toward the ventral side on the apex (Fig. 8b). The median lobe is slightly asymmetric and distinctly incurved on the apex in ventral view (Fig. 7b). The left paramer is wide, the proximal margin is rounded; the apical margin is gradually convex (Fig. 9b). The right paramer is trowel-form, rounded, rarely obtuse in the apex (Fig. 10b). The genital ring is wide and slightly oval, rather asymmetric, with a fairly short apex which is curved right (Fig. 11b). Gonocoxite 1 is triangular, funnelform, the inner margin is gradually convex, without distinct punctation. Gonocoxite 2 is like that of B. unipustulatus, but shorter; rather less curved. All setae deposited on the apical margin of the ventral surface of laterotergites are directed forward, more or less perpendicular to the margin. 34 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F. The posterior part of laterotergites is less prolonged, bell-shaped, well sclerotized (Fig. 12b). The reproductive tract is proximally with a short, broad, cap-shaped bursa copulatrix and a long C-shaped spermatheca with a coiled distal portion (Fig. 13b). Variations. The pattern of elytra is quite uniform, but anterior and interior margins of black semi-lunules vary in shape. Its anterior margin is often confined by a broadly or sharply curved line (Fig. 3b ♀), but it also could be denticulate or angulate (Fig. 3b ♂). Also, a different shape of the interior margin can make various forms of the bright spot between semilunules: circular, drop-like, rectangular, trapeziform or cordiform. No substantial variations of the shape of the pronotum and of structures of genitalia were detected. Differential diagnosis. Badister meridionalis seems quite a problematic species regarding its faithful identification. Due to the variety of some traits of the body, such as: its length, shape of pronotum, pattern of elytra, color of mesothorax, and this species is often confused with other species of the group. The most characteristic body traits we found are fine microsculpture, strong iridescence, and the distance from the base to the anterior side of the lunular black spot of elytra, which generally is at least 1.4 times longer than that of B. bullatus and at least 1.2 times longer than that of B. lacertosus. The median lobe of the aedeagus is smooth in the dorsal side of B. meridionalis unlike in B. bullatus (Figs. 8c, d), and contrary to B. lacertosus (Fig. 7e) it has a distinct sag in the apex. A narrower and more convex upper side of the body, lack of a row of long, well visible setae on the apical margin of elytra, and a specific curvature of the median lobe of the aedeagus can be good differential characters for the separation of this species from B. unipustulatus. The blade of gonocoxite 2 and the posterior part of laterotergites are less prolonged (Figs. 2b, 12b) compared with those of B. unipustulatus (Fig. 12 a); spermathecal walls are finer, distinctly wrinkled transversely (Fig. 13 b).B. meridionalis has more convexed dorsally and longer elytra than B. lacertosus and B. bullatus have. The ratio of length of elytra and length of pronotum of B. meridionalis is average 3.22, while those are 2.86 of. B. bullatus and 2.91 of B. lacertosus. General distribution. Western-Palearctic species widely distributed in Central and Southern Europe, also known in Northern Africa, Kazakhstan (Baehr, 2003), West Siberia (Novosibirsk region, Russia) (Dudko, Lyubechanskii, 2002). The northern border of the distribution range of this species reaches Denmark, southern Sweden, Lithuania, Belarus, central part of the Russian Plain (Lindroth, 1992; Krizhanovskyj et al., 1995). Remarks. B. meridionalis was briefly described as an aberration of B.bipustulatus =bullatus by Puel in 1925. Subsequently Jeannel (1942) after revision of Puel’s material concluded that B. meridionalis should be considered a Mediterranean region race of B. bipustulatus, because male genitalia are similar to those of B. bipustulatus. The status of valid species of this form was established only in 1952 by Makólski and it was named Badister kineli. Later this name was placed to the status of junior synonym of B. meridionalis by Lohse (1954). It is interesting to note that it was made without any comments on similarity of these taxa. Makólski’s description is the most comprehensive and assuredly proving the status of valid species of this taxon. The 35 Comparative Morphology and Morphometry microsculpture of elytra and the shape of the aedeagus were taken as the main assent of characters of B. kineli distinguishing it from B. bipustulatus. Indeed, we did not find any substantial differences between specimens determined as B. meridionalis from Croatia (specimens from the locality closest to the locality of Puel’s material) and Hungary and paratypes of B. kineli. The means of the length and width of the pronotum of our examined paratypes of B. kineli slightly differed from the means of the holotype described by Makólski (1952) and did not exceed 1.225 and 1.75 mm, respectively, while the means for the holotype indicated by Makólski (1952) were 1.4 and 2.2, respectively. In case of coloration of scutellum and mesothorax, our observations completely fit descriptions of Komarov (1991) and Arndt et al. (2011), but partly disagree with Hurka (1996). The coloration of these parts of body of our examined specimens varies from black to red-brown or orange, or some specimens’ mesothorax is bicolored: black with a reddish anterior part.
Badister (s. str.) bullatus Schrank, 1798 Examined material. Estonia: Harju: Keila, 06.1938 leg. Anonymous (1♀, EMNH); Nissi, 8.06.1936 leg. A. Juris (1♂, EMNH); Paaskula, 4.05.1983 leg. G. Milländer (1 ex., EMNH); Padise, 24.06.1929 leg. H. Haberman (1♂, EMNH); Tallin, 23.04.1935 leg. B. Gebauer (1 ♂, EMNH), 30.09.1956 leg. G. Milländer (1♂, EMNH); Marivalja, 25.04.1953 leg. G. Milländer (1♀, EMNH); Lääne Viru: Tapa, Läste, 18.04.1935 leg. Anonymous (1♀, EMNH); Põlva: Põlva, 05.1897 leg. Anonymous (1♀, EMNH); Rapla: Kehtna, Saarepõllu, 15.06.1956 leg. H. Haberman (1♀, EMNH); Lipstu, 1.06.1957 leg. H. Haberman (1♂, EMNH); Raikküla, 14.09.1956 leg. H. Haberman (1♂, EMNH); Vigala, 28 07.1952 leg. H. Haberman (1♂, EMNH); Saare: Kiirassaare, 10.06.1911 leg. K. Krausp (1♀, EMNH); Tartu: Rõngu, Valguta, 1846 leg. L. Schrenk (1♂, EMNH); Ropka, 06.1827 leg. H. M. Asmuss (1♂, EMNH); Tähtvere, 1834 leg. A. Lejmann (1♂, EMNH); Tartu, 1829 leg. H. Haberman (1♂, EMNH), 10.03.1846 leg. Chleboforf (1♀, EMNH), 04.1861 leg. L. Schrenk (1♂, EMNH), 04.1880 leg. Anonymous (3♂♂/2♀♀, EMNH), - 04.1881 leg. Anonymous (1♂/1♀, EMNH), 14.05.1938 H. Kuusik (1♀, EMNH); Karlova park, 04.1831 leg. H. M. Asmuss (1♀, EMNH), Toomemägi, 17.05.1930 leg. H. Haberman (1♀, EMNH); Võnnu, 1.06.1986, leg. J. Vilbaste (1♂, EMNH); Valga: Helme, Kirikuküla, 27.03.1958 leg. E. Marivee (1♂, EMNH); Helme, 13.04.1963 leg. R. E. Marivee (1♀, EMNH), 7.09.1963 leg. R. E. Marivee (1♂, EMNH); Viljandi: Võhma, 14.05.1939 leg. Anonymous (1♀, EMNH); Livonia (a historical region on the eastern shores of the Baltic Sea): 1858 leg. Anonymous (1♀, EMNH); Latvia: Aglona: Kastuļina, Stivriņi, 28.08. 1989 leg. A. Barševskis (1♂, DUBC); Šķeltova, Suveizdi, 8.04.1995, 29.04.1995 leg. A. Barševskis (1♀, 1♂, DUBC); Šķeltova, 5.04.1986, 29.03.1987, 18-19.03.1989, 8.04.1991, 17.10.1992, 4.04.1993, 25.02.1995, 17.03.1995, - 07.2002, 10.04.2009 leg. A. Barševskis (1♂, 1♀, 3♀♀, 2♀♀, 1♂/1♀, 3♂♂/1♀, 1♂/2♀♀, 1♂/♀, 1♂, 1 ex., DUBC); Aknīste: Aknīste, - 05.1993 leg. A. Barševskis (1♀, DUBC); Daugavpils: Ambeļi, - 04.1988 leg. A. Barševskis (1♂, DUBC); Elerne, 24.05.2007 leg. A. Pankjans (1♀, DUBC); Ilgas, 10.10. 1992, 14.05.1993, 18.06.1993, 29.06.1995, 1-30.06.2002, 22.04.2009 leg. A. Barševskis (3♂♂, 1♂/1♀, 1♀, 1♂, 1♂/1♀, 1♂, DUBC), 5-10.06.2006 leg. M. Verdenfelde (1♂, DUBC); Stropi, 11.06.2009 leg. A. Barševskis (1♂, DUBC); Višķi, 30.03.1986, 12-27.04. 1991, 14.12.1991 leg. A. Barševskis (2♂♂, 1♂/1♀, 1♂, DUBC); Engure: Abragciems, 18.07.2001 leg. A. Napolov (1 ex., AN); Ilūkste: Bebrene, 18.09.2006, 28.10.2006, leg. E. Rudans (1♀, 2♂♂/1♀, DUBC); Dviete, - 07.2006 leg. Anonymous (1♀, DUBC); Ilūkste, 17.04.1993 leg. A. Barševskis (1♂, DUBC); Šarlote, 14.09.1991 leg. A. Barševskis (1♂/1♀, DUBC), 4.05.2009 leg. K. Aksjuta (1♂, DUBC); Šedere, 12.06.2007 leg. M. Murd (1 ex., DUBC); Jēkabpils: Dunava, 11.04.1993, 1.01.1995, 15.04.1995, 6.04.1996, 22.09.1996, 10-30.06.2007, 12-18.07.2009 leg. A. Barševskis (2♂♂, 1♂, 2♂♂, 1♀, 1♀, 1♂/1♀, 1♀, DUBC); Rubeņi, 1.06.1997, 28.03.1999 (published as B. meridionalis (Leskina 2000), 4.04.1999 leg. I. Leiskina (1♂, 1♀, 1♂, DUBC); Jelgava: Jelgava, 1.05.1997 leg. R. Matrozis (2♂♂/1♀, FS); Jūrmala: Kauguri, 1.05.1992 leg. A. Barševskis (1♂, DUBC); Krāslava: Ūdrīši, “Zapoļņiki”, 8-10.05.2009 leg. M. Janovska (1 ex., DUBC); Kaplava, Varnaviči, 27.05.1990 leg. A. Barševskis (1♀, DUBC); Madona: Bērzaune, Gaiziņkalns, 5 11.2005, leg. A. Barševskis (2♀♀, DUBC); Arona, Lautere, 1-3.06.2006 leg. A. Ilzēna-Rozentāle (1♀, DUBC); Preiļi: Jersika, 21.05.2005, 7.09.2008, 1-10.05.2009, 36 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
28.06.2009, leg. A. Barševskis (1♂, 1♂ 1♀, DUBC), 7.09.2008 leg. A. Barševskis and K. Barševska, published as B. meridionalis (Barševskis et al. 2009) (1♀, DUBC); Rēzekne: Rēzekne, 8. 11.2008, leg. J. Kupce (1♂/1♀, DUBC); Rīga: Rīga, 8.05.1994, 29.04.1997 leg. R. Matrozis (1♀, 1♀, FS), 5.06.1994 leg. F. Savich (1♂, FS); Garciems, Garupe, 3.05.1995 leg. F. Savich (1♀, FS); Garupe, 14.05.1994 leg. F. Savich (1♀, FS); Rumbula, 12.04 1994 leg. F. Savich (1♂, FS); Rucava: Pape, 24.06.1998 leg. F. Savich (1♀, FS); Saldus: Šķēde, 7.10.1995 leg. F. Savich (1♂, FS); Sigulda: Allaži, Kangarnieki, 29.04.2006 leg. M. Kalniņš (1♂, DUBC); Talsi: Slīteres Nacionālais parks, 13.06.2007 leg. K. Aksjuta (1♂, DUBC); Vārkava: Vārkava, 25.06.1992 leg. G. Spuriņš (1♀, DUBC); Ventspils: Moricsala Nature Reserve, - 10.2010 leg. U. Valainis (1 ex., DUBC); Usma, 19.07.2007, 5-6.10.2011 leg. A. Barševskis (1♀, 1♂, DUBC); Zilupe: Pasiene, 19.07.1989, leg. A. Barševskis (1♂, DUBC); Lithuania: Akmenė: Gimbetiškė, 9.05.1995 leg. Vidm. Monsevičius (1♀, KZM); Kamanos Strict Nature Reserve, 4.05.1992 leg. R. Ferenca (1♂, KZM), 2.05.1984, 11.06. 1984, 19.08.1984, 19.10.1997, 31.05.2002 leg. Vidm. Monsevičius (1♂, 1♀, 1♀, 1♂, 1♀, KZM); Alytus: Žuvintas Strict Nature Reserve, 15.04.1979, leg. Vidm. Monsevičius (1♂, KZM); Anykščiai: Deveniai, 19.06.1989 leg. B. Šablevičius (1♂, KZM); Katlėriai, 19.08. 1988 leg. S. Karalius (1♀, KZM); Kurklė, 14.05.2016, 26.05.2016, 9.06.2016, leg. Ž. Obelevičius (2♀♀, 1♀, 1♂, KZM), Maciūnai, 14.05.2016, 26.05.2016, 19.06.2016 leg. Ž. Obelevičius (3♀♀, 1♀ 1♀, KZM) Surdaugiai, 26.05.2016, 9.06.2016, 19.06.2016, 13.07. 2016, 28.07.2016, 14.08.2016, 26.08.2016 leg. Ž. Obelevičius (1♀/1♂, 1♀, 1♀/1♂, 1♂, 1♀/1♂, 1♂, 2♀♀/1♂, KZM); Kaišiadorys: Kruonis, 20.04.2002 leg. A. Meržijevskij (1♂, AM); Vaiguva forest, 27.05.2003 leg. R. Ferenca (1♂/1♀, KZM); Kalvarija: Juodeliai, 27.06.1995 leg. H. Ostrauskas (3♂♂, KZM), Norvydai, 19.08.1981 leg. R. Ferenca (1♀, KZM); Kaunas: Akademija, 3.05.2004 leg. V. Tamutis (1♀, KZM); Aleksotas, 19.03.2002 leg. V. Tamutis (1♂, KZM); Braziūkai, 15 .07.2004, 26.06.2006, 10.09.2016 leg. V. Tamutis (1♀, 1♂, 1♀, KZM); Dubrava forest, 29.07.1984, leg. R. Ferenca (1♂, KZM), - - 1987 leg. A. Ragelis (1 ex., KZM); 2.05.1999 leg. P. Zolubas (1 ex., KZM); Ežerėlis, 25.06. 2008 leg. A. Meržijevskij (1 ex., AM); Jiesia Landscape Reserve, 25.05.1984, 9.04.1989, 18.09.1992, 31.05.2001, 10.05.2008, leg. R. Ferenca (1, 1, 1, 2, 1 ex., KZM), 30.05.2010 leg. A. Meržijevskij (1♂, AM); Kamša forest, 6.05.1992, 20.05.1992 leg. V. Tamutis (1♂/1♀, 1♂/1♀, KZM); Kaunas, 15.09.1989 leg. R. Ferenca (1♀, KZM); Margininkai, 31 08.1997, 9.05.1999, 20.06.1999 leg. V. Tamutis (1♀, 1♂, 1♂, KZM); Noreikiškės, 23.05. 1995, 22.09.1995, 15.11.2008, leg. V. Tamutis (2♂♂, 2♂♂, 1♀, KZM); Pajiesiai, 7.05.1938 leg. A. Palionis (1♀, KZM); Papiškės, 31.03.2007 leg. V. Tamutis (1♂, KZM); Papiškinė forest, pheromone trap for Ips typographus, 10.05.2016 leg. V. Tamutis (1♀, KZM), Ringaudai, 22.10.2003 leg. V. Tamutis (2♂♂, KZM); Klaipėda: Klaipėda, 27.04.1990, 12.05.1990, leg. S. Karalius (1♂, 1♂, KZM); Smiltynė, 22.07.1988, 17.07.1991 leg. S. Karalius (1♂, 1♀, KZM), 11.04.2004, leg. R. Ferenca (1♂, KZM); Palanga: Manciškė, 9.05.2001 leg. R. Ferenca (3♀♀, KZM); Palanga aeroport env., 8.05.2001 leg. R. Ferenca (1♂, KZM); Šakiai: Tervydoniai, 8.05.1988, 27.09.2014, 27.06.2015, 27.03.2016 leg. R. Ferenca (1♀, 1♂, 1♀, 1♂, KZM); Šiauliai: Dzidai, 4.08.2002 leg. V. Tamutis (2♀♀, KZM); Šilalė: Juodžiai, 4.04.2010, leg. R. Ferenca (3♂♂, KZM); Medvėgalis, 7.07.2005 leg. P. Ivinskis (1 ex., KZM); Švenčionys: Jakeliai, 1.05.2015 leg. R. Patapavičius (1♂, KZM); Trakai: Bitiškiai Lake env., 12.08.1927 leg. B. Ogijewicz (1 ex., KZM); Galvė Lake env., 13.08.1927, 10.07.1929, 28.07.1929, 9.08.1929 (leg. B. Ogijewicz (1♀, 1♂, 1♂, 1♂/1♀, KZM); Skaistis Lake env., 1.09.1928, 23.06.1929, 6.10.1929 leg. B. Ogijewicz (1 ex., 1♀, 1♀, KZM); Trakai, 6.08.1896, leg. Markiewicz (1♂, KZM), 2.01.1937, leg. Anonymous (1♀, KZM); Varnikai, 30.06.1994 leg. H. Ostrauskas (1ex., KZM); Ukmergė: Zujai -Vidiškiai, 30.10.1983, leg. L. Tiškevičius (1♀, KZM), 17-25.04.1984, 5-24.05.1984 3-24.07.1984 leg. R. Dvilevičius (1♂/3♀♀, 2♂♂/5♀♀, 2♂♂, KZM), 8.11.1983 leg. A. Čepelė (1♀, KZM), 21.04.1984 leg. G. Švitra (1♀, KZM); Utena: Utena, 7.06.1964 leg. E. Gaidienė (1 ex., KZM); Varėna: Jablanavas, 13.06.1998 leg. A. Gedminas (1 ex., KZM); Vilnius: Dūkštų ąžuolynas forest, 1.06.2003 leg. S. Morkūnas (2♀♀, KZM); Veliučionys, 13.05.1971 leg. A. Manikas (1♂,); Vilnius, 12.08.1927 21.05.1930, 27.07.1930, leg. B. Ogijewicz (1♀, 1♀, 1♀, KZM); Zarasai: Salakas, 24.06.1996 leg. H. Ostrauskas (2♀♀, KZM). Additional material: Germany: Bavaria: München: Schleisheim, 19.06.2005 leg. H. Kulzer (1♂, BSCZ), Wessling, 11.05.1994 leg. O. Bühlmann (1♀, BZCZ), Überlingen - 03. 1994, leg. A. Horion (1♀, BSCZ), Aschau, 4.04.1946 leg. H. Freude (1♂, BSCZ), Garhing, - 04.1950, - 05.1955, leg. K. E. Hüdephl (1♀, 1♀, BSCZ), Sammlung, 9.06.1948, 7.08. 1948 leg. O. Bühlmann (1♀, 1♂, BSCZ); Berlin: Müllkippe Marienfelde, 16.07.1971, leg. H. Korge (1♂, BNM), Berlin-Biesdorf, Süd Garten, 4.06.2005 leg. H. Wendt (1♂/1♀, BNM); Mecklenburg: Vorpommern, LSG Schlosspark, 12-21.05.2007, leg. M. Grünwald (1♂, BNM); Dorf Wehlen; Turkey: Kastamonu, 25 km SE Tosya, 1600 altitude, pine forest, 6.04.2009 leg. V. Assing and P. Wunderle (1♂, 1♀, BNM), 37 Comparative Morphology and Morphometry
Published records: Estonia: Harju, Lääne, Lääne Viru, Põlva, Rapla, Saaremaa, Tartu (Haberman, 1968); Hiiumaa (Miländer, 1993). Latvia: Kurzeme (Kawall, 1866); Koknese (as synonym of B. bipustulatus) (Seidlitz, 1872, 1887); Melluži (Jūrmala) (Stiprais, 1984); Arteņi, Daugavpils, Ilgas, Svente, Krauja, Medumi, Naujene, Nīcgale, Vasarģelišķi, Višķi (Daugavpils), Šarlote, Eglaine, Pilskalne (Ilūkste) Šķeltiņi, Šķeltova (Aglona), Izvalta, Krāslava, Kombuļi, Piedruja (Krāslava), Kuprava (Viļaka), Stabulnieki (Riebiņi), Koknese, Viskāļi (Koknese), Teiču Nature Reserve, Krustkalni Nature Reserve (Barševskis, 1987, 1993); Līksna, Vabole (Daugavpils) (Cibulskis, 1994); Silene (Daugavpils) (Barševskis et al., 2002); Moricsala Nature Reserve (Barševskis et al., 2004); Gauja National Park (Kalniņš et al., 2007); Bebrene, Šedere (Ilūkste), Ūdrīši (Krāslava), Dunava (as B. lacertosus) (Jēkabpils), Jersika (as B. lacertosus) (Preili), Slitere National Park (Talsi) (Barševskis et al., 2009), Skrīveri (Aizkraukle) (Bukejs et al., 2009), Poki (Jelgava) (Gailis and Turka, 2014). Lithuania: Kaunas (Heyden, 1903, Ferenca, 2006); Trakai, Vilnius (Roubal, 1910, Ogijewicz, 1933); Panevėžys (Ferenca, 2006); Žuvintas Nature Rezerve, Lazdijai, Alytus (Sharova and Grüntal, 1973); Ukmergė (Dvilevičius et al., 1988). Description. The body pattern is almost similar to that of B. meridionalis; however, scutellum and mesothorax are constantly black to black-brown, the first antennomere is entirely yellow or red-yellow, 2-6 antennomeres are darkened. The black pattern of elytra is generally composed of one semi-lunular spot on each elytron (Fig. 3c); occasionally this spot is divided into two parts transversely. The interior margins of semi-lunules are curved variously and forming various shape yellow-red spots on both sides of the suture. The black semi-lunule is confined mostly by a more or less convex line, occasionally by a wiggle in the front. Short setae are absent from the apical margin of elytra. The microsculpture of elytra is fine, composed of transversal fissures, the contours of which can be well visible magnified 80 times. Two or three fissures are arranged along the distance of 10 μm of the surface of elytra (Fig. 5d). The surface of elytra is distantly iridescent. The sexual dimorphism is distinct by the width diameters of the head, pronotum and elytra (Table 1). The means of WH and LH in males average 0.785 and 0.824 mm, respectively, and are significantly lower compared to females (U = 906.5; p < 0.01; U = 1423; p < 0.01). The pronotum slightly varies in the straightness of lateral margins and roundness of posterior angles by both genders (Figs. 6c, d), but it is significantly wider in females (1.629 mm) than in males (1.59 mm) (U = 2039; p < 0.0264) (Table 1). Also, the mean of the width of elytra, LH/WH and LP/WP are significantly higher in females (P < 0.05) (Table 1). The distance from the base of elytra to the anterior side of the lunular black spot of elytra (BS) differs insignificantly between genders and varies from 0.7 to 1.2 mm. The aedeagus has a relatively short ending part of the median lobe (Figs. 7c, d). A small kink directed toward the ventral side on the apex and a small tooth or knoll (sometimes indistinct) directed upward and situated in the apex of the median lobe are visible in lateral view (Figs. 9c, d). The median lobe is distinctly asymmetric and distinctly incurved on the apex (Figs. 7. c, d). The left paramer is wide, the proximal margin is broadly rounded, the basal margin varies from almost straight to convex, without distinct indentation or slightly indented in the proximal margin (Figs. 8c, d); the apical margin ungradually rounded; the basal process is curved variously. The right paramer is trowel-form, confined by a blunt to slightly rounded margin in the apex (Figs. 10c, d). The genital ring is elongated, with straight or slightly convexed margins, rather asymmetric, with a fairly short apex which is curved right (Figs. 11. c, d). Gonocoxite 1 is triangular or funnelform, the inner margin is convex, without 38 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F. distinct punctation. Gonocoxite 2 is curved, disorderly punctate; the blade is blunt and short (Fig. 12d) to sharp, rather elongated finger-form and curved (Figs. 12c, e). The median and lateral ensiform setae are sharp (Figs. 12c, e) to short and blunt (Fig. 12 d). All setae on the apical margin of laterotergites are directed outward, more or less by a sharp angle to the margin (Figs. 12c, d, e). The posterior part of laterotergites varies from more or less prolonged (Figs. 12 d, e) to short, bell-shaped (Fig. 12 c). The reproductive tract is with a short, broad, cap-shaped bursa copulatrix and a diverse by thickness C-shaped spermatheca and a coiled distal portion (Figs. 13c-e). Variations. It is a very polymorphic species. Some of aberrations and variations of this species based on different shape of semi-lunular black spots of elytra have been mentioned by Puel (1925) and Jeannel (1942). Two of them, B. meridionalis and B. lacertosus, presently have the status of valid species (Baehr, 2003). Actually, this species varies not only by the pattern of elytra, but also by the shape of the pronotum, color of the scutellum, depth of elytral striae, and shapes of structures of genitalia. Interior margins of black semi-lunules on elytra are curved variously and forming various shape yellow-red spots on both sides of the suture: round, trapeziform, rectangular, semi-lunular, cordiform or wedgeform; also, its front line is confined variously: sharply or broadly curved, denticulate or bracketformed. In combination of these characters, almost each specimen of this species is different. One more strongly varying character is the shape of the pronotum. Despite differences of pronotum width among genders, the lateral margins and roundness of posterior angles vary within genders as well (Figs. 6. c, d). The small tooth directed upward of the apex of the median lobe of the aedeagus is mentioned as a certain character for distinguishing this species, but it can be reduced to an indistinct knoll in some males. Also, very interesting is variability of shape of left parameres from almost oval to rather rectangular (Figs. 8c, d). Basal processes both of left and right parameres vary by their falling to the basal margin of the paramer from angles of 45º up to 80º. The gonocoxites 2 of females vary by their length and apex of blades from rather long, sharp, fingerform, with normal ensiform, slightly curved setae (Figs. 12c, e) to short and blunt, with short and blunt setae (Fig. 12d). The shape of spermatheca and its coiled distal portion varies as well (Figs. 13c-e). Differential diagnosis. Due to the variety of some of above-mentioned traits of body, this species is often confused with B. meridionalis and B. lacertosus. It seems quite explainable that these currently valid species were previously regarded as variations of B. bullatus (Puel, 1925; Jeannel, 1942). We found that the most characteristic body traits could be the thinner fissures of elytral microsculpture and distant iridescence compared with the same traits of B. meridionalis and B. lacertosus. Of course, B. bullatus seems to be the smallest species and it significantly differs from other species of this subgenus by its body length, width and length of the head, pronotum and elytra, distance from the base of elytra to the anterior side of the lunular black spot (Table 2), but sometimes these parameters overlap (Figs. 14a-h.). The median lobe of the aedeagus is quite characteristic by its small tooth directed upward on the apex (Fig. 9c), but it could be reduced to weak and indistinct (Fig. 9d). In that case the ventral view could be helpful, where the apex of the median lobe is rather broader than that 39 Comparative Morphology and Morphometry of B. meridionalis and B. lacertosus and there is distinct sag on the apex, which is absolutely missing in B. lacertosus. The shape of gonocoxite 2 and setation of the apical margin of laterotergites could be helpful for identification of females. Differently from B. meridionalis and B. lacertosus, the blade of gonocoxites 2 is usually prolonged (has some distance with parallel margins in the basal half), the inner margin is less convexed than in B. meridionalis (Fig. 12b), but distinctly shorter than in B. lacertosus (ratio h/m = 1.4-1.9) (Figs. 12f, g). The setae on the apical margin of laterotergites are directed by a more or less sharp angle to the margin (Figs. 12c-e), differently fromB. meridionalis (Figs. 2b; 12b). General distribution. Euro-Sibero-Central Asiatic species widely distributed in Europe, known in Caucasus, Turkey, Iraq, Iran, Uzbekistan, Kazakhstan, Siberia (Baehr, 2003). The northern border of its distribution range reaches 62º latitude in Europe and 60º latitude in Siberia, and the eastern border goes as far as the Amur River lowland (Lindroth, 1992; Krizhanovskyj et al., 1995). This species is still unknown in Portugal, Spain, southern Italy, Macedonia, Tadzhikistan, China.
Table 2. Inter-specific differences in body morphological traits (pair groups with significant differences of mean values p≤0.05 are showed) in four species of Badister (s.str.). The Kruskal-Wallis test results estimated with the permutation procedure (PMonteCarlo) are reported (M - males, F - females, a, b, c, d, e, f, g, h - codes of groups, LB - length of body, WH - width of head, LH - length of head, WP - width of pronotum, LP - length of pronotum, WE - width of elytra, LE - length of elytra, BS - distance between the base of elytra and the black spot)
Species B. unipustulatus B. meridionalis B. bulatus B. lacertosus Chi square Traits M F M F M F M F M F a b c d e f g h LB c, e, g d, f, h a, e b, f a, c, g b, d, h a, e b, f 95.3 90.41 WH c, e, g d, f, h a, e b, f, h a, c, g b, d, h a, c, e b, d, f 89.47 78.97 LH c, e, g d, f, h a, e b, f a, c, g b, d, h a, e b, d, f 68.26 64.91 WP c, e, g d, f, h a, e b, f a, c, g b, d, h c, e b, f 78.53 72.12 LP e f e - a, c, g b, d, h a, e b, f 36.44 31.16 WE c, e, g d, f, h a, e b, f, h a, c, g b, d, h a, c, e b, f 87.75 85.74 LE c, e, g d, f, h a, e, g b, f, h a, c, g b, d, h a, c, e b, d, f 92.79 88.97 BS c, e, g d, f, h a, e, g b, f, h a, c, g b, d, h a, c b, d, f 95.38 87.9 Ratio LH/LP c, e, g d, f, h a, e, g b, f, h a, c b, d, h a, e b, d 56.8 60.21 Ratio LP/WP c, e, g d, f, h a, e b, f, h a, c b, d a b, d 46.36 56.98 Ratio LE/LP c, e, g d, f, h a, e, g b, f, h a, c b, d, h a, c b, d 82.74 79.51 Ratio LE/BS e, g f, h e, g f, h a, c, g b, d a, c, e b, d, f 57.73 62.22 40 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Fig. 14. Measured traits: A. body length; B. width of head (WH), C. length of head (LH), D. width of pronotum (WP), E. length of pronotum (LP), F. width of elytra (WE), G. length of elytra, H. distance between base and apical margin of lunular black spot of elytra; Bm. Badister meridionalis, Bu. Badister unipustulatus, Bl. Badister lacertosus, Bb. Badister bullatus. 41 Comparative Morphology and Morphometry Remarks. The pattern of elytra is regarded as a valuable character for distinguishing this species (Makólski, 1952; Komarov, 1991; Arndt et al., 2011; Puchkov 2013). But we found that this character is very variable and has a low value for identification of the Badister bullatus species group. The shape of the median lobe of the aedeagus seems to be the most faithful character, but its variations (mentioned above) should be considered.
Badister (s. str.) lacertosus Sturm, 1815
Examined material. Estonia: Harju: Kaila, Laulasmaa, - 06.1938 leg. Anonymous (2 ex., EMNH); Keila, 07.1939 leg. Anonymous (1 ex., EMNH); Lääne: Növa, 28.05.1956 leg. J. Vilbaste (1 ex., EMNH); Tartu: Tartu, 1827 leg. Anonymous (1 ex., EMNH); Valga: Helme, Kirikuküla, 24.09.1956 leg. E. Marivee (1 ex., EMNH); Latvia: Aglona: Kastuļina, Stivriņi, 06.10.1986 leg. A. Barševskis (1♀, DUBC); Šķeltova, 27.10.1991 leg. A. Barševskis (1♀, DUBC); Auce: 6 km E. Auce, 12.06.2015 leg. M. Balalaikins (2♂♂/4♀♀, KZM); Daugavpils: Elerne, 04.2002 leg. A. Barševskis (1♀, DUBC); Ilgas, 19.06.1994 leg. A. Barševskis (2♂♂/2♀♀, DUBC); Naujene, 16.04.1987 leg. A. Barševskis (1♂, DUBC); Ilūkste: Pilskalne, 16.03.1989, 29.04.1994 leg. A. Barševskis (1♀, 2♂♂, DUBC), Straumēni, 27.05.2007 leg. M. Janovska (1♂, DUBC); Jēkabpils: Dunava, 12.07.1994 leg. A. Barševskis (1♀, DUBC), 1-8.06.2009 leg. K. Barševska (1♂, DUBC); Krāslava: Izvalta, 13.09.1986 leg. A. Barševskis (1♀, DUBC); Limbaži: Vitrupe forest, 21.05.-19.06.2011 leg. V. Spungis (2 ex., LUFB); Madona: Krustkalni Nature Reserve, 17.07.2007 leg. A. Barševskis (1♀, DUBC), 4 km E Madona, 3.06.2015 leg. M. Balalaikins (3♂♂, 1♀, KZM); Rīga: Rīga, 31.05.1974 leg. L. Danka (1 ex., LMNH), Riga Mežaparks, 8.06.2005 leg. A. Napolov (1, ex., AN); Rucava: Rucava, 26.04.-29.05.1997, 23.04.-20.05.1998 leg. V. Spungis (1, 1 ex., LUBF); Vārkava: Vārkava, 09.05.1992 leg. G. Spuriņš (1♀, DUBC); Ventspils: Moricsala Nature Reserve, Viskūžu Island, 27.09.2003 leg. V. Tamutis (1♂, KZM), Moricsala Nature Reserve, 29.06.2006, 14.07.2009, 16.08. 2010 leg. A. Barševskis (1♂, 1♀, 1♀, DUBC); Vecumnieki: 6 km NW Bārbele, 16.06.2015 leg. M. Balalaikins (1♂, KZM); Lithuania: Akmenė: Gimbetiškė, 17.05.1991 leg. Vidm. Monsevičius (1♀, KZM); Kamanos Strict Nature Reserve, 7.07.1984, 15.09.1984, 30.06. 1997, 30.06.2002 leg. Vidm. Monsevičius (1♂, 2♂♂, 1♂, 1♂, KZM), Užpelkiai, 05.05.1999 leg. Vidm. Monsevičius (1♀, KZM); Anykščiai: Kurklė, 14.05.2016, 9.06.2016 leg. Ž. Obelevičius (2♂♂/1♀, 2♀♀, KZM), Maciūnai, 13.07.2016 leg. Ž. Obelevičius (1♂); Biržai: Miegonys, 25.06.1973 leg. A. Manikas (1♂,KZM); Neringa: Juodkrantė, 14-15.06.2012 leg. R. Ferenca (1♂, KZM); Kaišiadorys: Kaukinė Botanical-Zoological Rezerve, 24.09. 1994 leg. B. Šablevičius (1♂, KZM), Pravieniškės, 09.05.1986 leg. R. Ferenca (1♀, KZM); Kalvarija: Trakėnai, 05.09.1999 leg. V. Monsevičius (1♀, KZM); Kaunas: Braziūkai, Anthriscus sylvestris owergrowth, 10.07.2007 leg. V. Tamutis (2♂♂, KZM), Dubrava forest, pheromone trap for Ips typographus, 02.05.1999, leg. P. Zolubas (1♂, KZM); Kamša Botanical-Zoological Rezerve, 02.04.1992, 15.04.1992, 08.04.1997 leg. V. Tamutis (1♀, 1♀, 2♂♂, KZM), Noreikiškės, 20.05.1994 leg. V. Tamutis (1♀, KZM); Šakiai: Juškinė Forest, 30.04.2000 leg. R. Ferenca (1♂, KZM), Tervydoniai, 27.09.2014, 27.03.2016 leg. R. Ferenca (1♂, 1♂, KZM); Šilalė: Juodžiai, 05.04.2010 leg. R. Ferenca (1♀, KZM); Trakai: Trakai, 23.06.1929 leg. B. Ogijewicz (1♀, KZM); Ukmergė: Dukstyna Entomological Reserve, 04.05.1984 leg. R. Dvilevičius (3♂♂, KZM), Kalnai forest, 5.04. 2017 leg. V. Tamutis (1♂, KZM), Ratkalnis forest, 5.04.2017 leg. V. Tamutis (1♂, KZM), Vytinėlė forest, 20.04.2004, 10.06.2004, 21.06.2004, 30.06.2004, 19.07.2004, 29.07.2004, 18.08.2004, 28.08.2004 leg. N. Noreika (2♂♂, 4♀♀, 2♂♂/1♀, 1♂, 2♂♂, 1♀, 2♀♀, 1♀, 1♀, 1♂, KZM); Utena: Antalgė, 03.04.1977 leg. A. Kaulinis (1♀, KZM); Varėna: Pogarenda, 19.09.1981 leg. V. Monsevičius (1♂, KZM); Vilnius: Baltupiai, 14.04.1931 leg. B. Ogijewicz (1♀, KZM). Additional material. Germany: Berlin: Tegel, Flughafensee Wald, 10.07.2004 leg. Diehr (1♂, BNM); Frankfurt (Oder), 6.05.1997 leg. A. Barševskis (1♂, DUBC); Görlitz: Weinhübel, 30.07.1962 leg. Anonymous (1♀, BNM); München: Ampermoching, 22.09.1955 leg. Dr. Engelhardt (1♀, BSCZ); Weimar: Bad Berka, - 06.1983, leg. Materlik (1♂, BNM); Russia: Kaliningrad oblast: Svetlogorsk, 26.04.1998 leg. V. I. Alekseev (1♂, DUBC); Irkutsk oblast: 17 km SW Irkutsk, 18.05.1990 leg. A. Anichtchenko (1♀, DUBC). Published records. Estonia: Harju, Lääne, Rapla, Tartu (Haberman, 1968); Hiiumaa (Miländer, 1993). Latvia: Kurzeme (Fleischer, 1829; Kawall, 1866); Rīga (Stiprais, 1973); Ilūkste, Daugavpils, Aglona, Krāslava (Barševskis, 1993), Gauja National park (Kalniņš et al., 2007); Elerne (Daugavpils), 42 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
Bebrene (Ilūkste), Šķeltova (Aglona), Slītere National Park (Talsi), Moricsala Nature rezerve (Ventspils) (Barševskis et al., 2009); Lithuania: Kaunas (Tamutis and Dapkus 2008), Vilnius (Ogijewicz, 1933); Ukmergė (Dvilevičius et al., 1988) and Varėna (Miländer et al., 1988). Description. The body pattern: black-colored head, mesothorax, metathorax, abdomen, and a semi-lunular spot (it can be divided into two spots transversely) on each elytron; yellow-red pronotum, scutellum, the remaining part of elytra, palpi and legs. The first antennomere is yellow or red-yellow, slightly darkened anterior, 2-6 antennomeres are darkened, the remaining are brown. The interior margins of semi-lunules, if entire, are curved variously and forming various shape yellow-red spots on both sides of the suture; its front margin is usually straight (roughly 50% of all our examined specimens) (Fig. 3d, ♂), but also can be slightly rounded (about 25 %) (Fig. 3d, ♀) or wiggled (about 25%). Short setae are absent from the apical margin of elytra. The microsculpture of elytra is fine, composed of thin transversal fissures, the contours of which are well visible magnified 150 times, but become blend magnified less than 90 times. Three or four fissures are arranged along the distance of 10 μm of the surface of elytra (Fig5 c). The iridescence of the surface of elytra is distinct. The length of bodies is quite similar among genders: 5.7-6.7 mm in males and 5.5-6.9 mm in females. However, the head and pronotum are significantly wider in females compared to males (Table 1). The WH and LH are 0.886 and 0.883 mm, respectively, in males, and that is significantly lower than in females (U = 83; p < 0.01; U = 110.5; p < 0.05). The pronotum slightly varies in sinuation of lateral margins to posterior by both genders (Fig. 6e), and it is significantly wider in females (1.81 mm) than in males (1.763 mm) (U = 207.5; p < 0.0206) (Table 1). Also, the LH/LP is significantly higher in females (p < 0.01); however, the ratio of length and width of pronotum is significantly higher in males (p = 0.01) (Table 1). The aedeagus has a relatively long ending part of the median lobe (Figs. 7e, 8e). A small tooth directed toward the ventral side on the apex is well visible in lateral view (Fig. 9 e). The median lobe is slightly asymmetric without any incurvation on the apex in dorsal view (Fig. 7e). The left paramer is wide, proximal margin is broadly rounded, basal margin is almost straight, without indentation in the proximal part (Fig. 8e); the apical margin is slightly, gradually rounded; the basal process is rather curved. The right paramer is trowelform, roundly confined in the apex (Fig. 10e). The genital ring is wide and elongate, its lateral margins are weakly convex (Fig. 11. d). Gonocoxite 1 is triangular, funelform or buttleform, the inner margin is gradually convexed (Fig. 12f), or forming an obtuse angle (Fig. 12g). Gonocoxite 2 is disorderly punctate, inner margin is almost straight; its blade is blunt to sharp, rather elongated and slightly curved. The ensiform setae are fingerform, relatively long, sharped or blunted in the apex. Most of the setae (some of them are directed differently) of the apical margin of laterotergites are directed more or less by a sharp angle to the margin. The posterior part of laterotergites is short, bell-shaped, well sclerotized (Figs. 12f, g). The reproductive tract is with a short, broad, cap-shaped bursa copulatrix and a long C-shaped, relatively fine spermatheca with a coiled distal portion directed to the left (Fig. 13f). Variations. This species was considered a morphological variation of B. bullatus (bipustulatus) (Puel, 1925; Jeannel, 1942) till Lindberg (1948) gave a detail description 43 Comparative Morphology and Morphometry and incontrovertible evidence of the valid species status of this form. Also, Lindberg (1948) described some of possible intraspecific variations ofB. lacertosus in the shape of the median lobe of the aedeagus. However, this species varies by the pattern of elytra, shapes of the pronotum and gonocoxites like B. bullatus (Figs. 3.d; 6e; 12f, g). The interior margins of black semi-lunular spots are curved variously and forming various shape yellow-red spots on both sides of the suture (Fig. 3d). The front margin of black semi-lunules is confined mostly by a straight line, but we found that it can be slightly convex or wiggled as well. Despite differences of pronotum width among genders, the sinuation of lateral margins slightly varies within genders as well. The lateral margins of the pronotum could vary from gradually convex to almost straightly sinuate posteriorly. The shape of the median lobe of the aedeagus both in ventral and lateral view slightly varies, but unfortunately, we did not find it to be distinct. However, gonocoxites 2 vary strongly by their length and apex of blades: they vary from rather long, sharpened to short and blunt. The same variation can be detected in the shape of medial and lateral ensiform setae of gonocoxite 2 (Figs. 12f, g). Differential diagnosis. Due to the variety of some of body traits, this species is often confused with B. meridionalis and B. bullatus. The most characteristic body trait we have found is the microsculpture rougher than in B. meridionalis, but finer than in B. bullatus (Fig. 5b-d). The iridescence of elytra is distinct, but weaker than in B. meridionalis. Length of body, width of head, width of pronotum, width of elytra are often similar to these body traits in B. meridionalis, but length of head, length of elytra, and distance from the base of elytra to the anterior side of the lunule black spot (BS) are significantly lower. Compared withB. bullatus, almost all values of parameters of body traits are higher; however, their ratios are quite similar, except for the ratio of length of elytra and BS (Table 2), but sometimes these parameters overlap (Figs 14 a-h). The median lobe of the aedeagus is quite characteristic by its length, more or less gradually sinuated lateral margins and lack of distinct incurvation on the apex. The apex of the median lobe is rather slender compared with those of B. meridionalis and B. bullatus. The shape of gonocoxite 2 and setation of the apical margin of the ventral surface of laterotergites are quite similar to those of B. bullatus. However, the blade is generally shorter, its inner margin is longer (ratio h/m = 0.9-1.1). Remarks. The pattern of elytra is regarded as a valuable character for distinguishing this species (Makólski, 1952; Komarov, 1991; Arndt et al., 2011; Puchkov, 2013). But we found that this character varies and is not so good for identification. It is worthy to note that the microsculpture of elytra of B. lacertosus is distinctly coarser than that of B. meridionalis, contrary to the result given by Makólski (1952) and Assman (2004). Komarov (1991) detected the microsculpture of elytra to be almost similar for all three species: B. meridionalis, B. bullatus, and B. lacertosus. General distribution. Trans-Eurasian - temperate-Southern Siberian species widely distributed in Europe, known in Kazakhstan, Kyrgyzstan (Krizhanovskyj et al., 1995; Baehr, 2003). The northern border of its distribution range reaches 63º latitude in 44 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F. Europe and 60º latitude in Siberia, eastern border reaches as far as South Sakhalin (Krizhanovskij et al., 1995) and South Primorye (Sundukov, 2009).
DISCUSSION Analysis of morphological characters High variability of morphological characters within species of Badister (s. str.) has been recognized previously and well presented, in particular for North American species (Ball, 1959), while for European species this trait is still studied incompletely. The greatest attention was paid to varieties of coloration of elytra by Puel (1925). Even five variations and aberrations for B. unipustulatus and eight for Badister bipustulatus (Fabricius, 1792) (= Badister bullatus (Schrank, 1798)) were presented in his comprehensive key of European Badister species. However, new descriptions or redescriptions of some variations or aberrations remain brief in later papers (Jeannel, 1942; Makólski, 1952). Later, two of them: B. lacertosus and B. meridionalis, were started to be ranked as valid species (Lindberg, 1948; Lohse, 1954). Additionally, some variations of the shape of the pronotum of Badister bullatus were presented by Komarov (1991). Despite a comparatively small dispersion of our examined material (only a small number of specimens from other regions have been additionally included in our study), we found variations of morphological characters of all species. Especially high variability was detected among specimens of B. bullatus. We found high variability not only in the shape of the pronotum, coloration of the scutellum and elytra, but also in the structure of genitalia both of males and females (it is described above in detail). We carefully examined each specimen of this species for variability and tried to find a complex of good indications as a background for description of new species, but our findings were not substantial. In our opinion, a deeper study including material from different parts of the distribution range and using molecular research methods could explain this phenomenon. Differences between genders and sexual dimorphism are distinct in Badister species, and they are mostly distinguished by dilated three first tarsomeres of the fore tarsus and two setiferous punctures on sixth abdominal sternites of males and not dilated tarsomeres of the fore tarsus and four setiferous punctures on sixth abdominal sternites of females (Ball, 1959; Lindroth, 1986; Komarov, 1991). Additionally, we found that females of all four species have a surely larger head than males; also, the pronotum is wider of females of B. bullatus and B. lacertosus (Table 1). The ratios of parameters of these parts of the body are also differentiated. The utility of the female reproductive tract for taxonomy and inferring phylogenetic relationships in Carabidae have been well demonstrated by Liebherr and Will (1998), although this system is explored particularly only for Naerctic and Neotropical species of the tribe Licinini (Will, 1998; Erwin, Ball 2011). We found that the reproductive tract of females of our studied four species of Badister (s. str) subgenus is markedly similar to each other and is quite analogous to homologous structures of species from the western hemisphere (Will, 1998; Erwin, Ball 2011). Differently from them, our examined species have a more intensive, generally C-shaped, basal uncoiled portion of the spermatheca. Spermathecal distal coiled portions are quite long, compact, have at least six coils; 45 Comparative Morphology and Morphometry gonocoxite 1 is asetose; gonocoxite 2 is falcate, having two dorsal ensiform and one ventral ensiform setae like Badister amazonus Erwin and Ball, 2011 (Figs. 12, 13). The most useful character for the recognition of species we found to be the setation of the apical part of laterotergites and the shape of gonocoxites 2. Assuming the stability of our examined morphological characters of Badister (s. str.) species, we propose the following key for identification of the species: 1. The mean of ratio of elytra length and distance from base of elytra to apical margin of lunular spot <3; apical margin of elytra with a row of setae (Fig. 4); microsculpture of elytra consisting of very tightly deposited transversal fissures, at least five fissures arranged along the distance of 10 μm of surface of elytra (Figs 5a, b) …...... 2 - The mean of ratio of elytra length and distance from base of elytra to apical margin of lunular spot >3; row of setae completely absents on apical margin of elytra; microsculpture of elytra consisting of tightly deposited transversal fissures, at maximum four cells arranged along the distance of 10 μm of surface of elytra (Figs. 5c, d) ….3 2. The setae on apical margin of elytra as long as half of second interval, well visible (Fig. 4a); mesepisternum and scutellum entirely pale; black semi-lunular spot on elytra usually divided transversely or joined narrowly beside outer margin of elytra (Fig. 3a); median lobe apically inclined ventrally with inflated protuberance (Fig. 8a); inner margin of gonocoxite 2 slightly convex, almost straight, punctation on apical margin of laterotergites dispersed along outer margin (Fig. 12a); body length 6.1-7.4 mm...... B. unipustulatus - The setae on apical margin of elytra as long as ¼ of second interval, indistinct (Fig. 4b); mesepisternum and scutellum dark, black semi-lunular spot on each elytron regularly continuous, rarely divided into two parts transversely; median lobe with smooth and small kink directed toward ventral side on apex (Fig. 9b), markedly sinuated laterally, with distinct incurvation in the top (Fig. 7b); inner margin of gonocoxite 2 distinctly convex, punctuation on apical margin of laterotergites more concentrated on apex, setae directed forward, more or less perpendicular to margin (Fig. 12b); body length 5.6-6.8 mm...... B. meridionalis 3. The contours of fissures of microsculpture invisible and blended under magnification of 90 times; black semi-lunular spot on each elytron regularly confined by more or less straight or widely convex line (Fig. 3d); distal part of median lobe relatively long, with smooth and small tooth directed toward ventral side on the apex (Fig. 9e), gradually sinuated laterally, without any incurvation in the apex (Fig. 7e); inner margin of gonocoxite 2 straight almost as long as width of gonocoxite 2 measured beside first ventro-lateral ensiform seta (Figs. 12f, g)...... B. lacertosus - The contours of fissures of microsculpture visible under magnification of80 times; iridescence of elytra absent; black semi-lunular spot on each elytron regularly confined by more or less curved line (Fig. 3c); ending part of median lobe relatively short, with small tooth directed toward ventral side on the apex and small tooth or knoll (sometimes indistinct) directed upward at its apex (Figs. 9c, d), ungradually sinuated 46 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F. laterally, with distinct incurvation in the apex (Figs. 7c, d); inner margin of gonocoxite 2 almost straight or slightly convex, but rather shorter than width of gonocoxite 2 measured beside first ventro-lateral ensiform seta (Figs. 12c, d, e)...... B. bullatus
Ecological traits Ecologically, most of Badister (sensu lato) species prefer moist or semi-moist habitats and are regarded as hygrophilous species (Lindroth, 1986, 1992), and only some of them could tolerate mesophilic stations. Particular representatives of such tolerants are B. bullatus and B. lacertosus. B. bullatus is regarded as the most eurytopic species occurring both in dry and moist, open and partly shaded habitats (Lindroth, 1986), but it avoids swamps or rather dark forests (Makólski, 1952). The indifference of this species to habitat conditions is well confirmed by studies of Brygadyrenko (2015) where it is presented as the most drought-resistant species of the genus in the Ukraine’s steppe zone. Moreover, the findings of this species in agricultural or urban landscapes (Andersen, 2000; Elek, Lövei, 2005; Veselý, Šarapatka, 2008; Bukejs et al., 2009; Galis, Turka, 2014) demonstrate its ability to survive under some anthropogenic pressure. Most of our collected specimens were found in mesophilic, open or partly shaded grasslands in the period from April to June. B. lacertosus is widely regarded as a mesophilic, forest species (Makólski, 1952; Komarov, 1991; Barševskis, 2003; Puchkov, 2013; Aleksandrowicz, 2014), but some authors classified it as a species that prefers wet habitats like B. unipustulatus (Lindroth, 1986; Hurka, 1996; Assman, 2004; Brygadyrenko, 2015). All our findings ofB. lacertosus were done in forests (mostly in deciduous) or forest edges, in moderately moist habitats in the period from March to October. This species quite often was found together with B. bullatus in grasslands of forest edges or bushy areas. We found more stable positions regarding the ecology of B. meridionalis and B. unipustulatus. Makólski (1952) describing a new species B. kineli pointed a clear preference of the species to waters. “It lives near water in open areas with preference for wet meadows flooded in springtime” (Makólski, 1952). This position was confirmed later by other authors as well (Lindroth, 1986; Komarov, 1991; Hurka, 1996; Barševskis, 2003; Puchkov, 2013; Aleksandrowicz, 2014). Contrary to B. meridionalis2B. unipustulatus prefers more shadowed habitats (Makólski, 1952; Lindroth, 1986), though its indifference to shadow was noted by Komarov (1991), Kirichenko (2000), Puchkov (2013), Brygadyrenko (2015). We can confirm the positive reaction to ultraviolet light in the night time for both these species as it was noted previously by Komarov (1991), because part of our studied specimens, according to label data, have been caught using light traps. It is interesting to note that our detected similarity of morphology of these species, particularly the row of setae on the apex of elytra, could be associated both of them to wet, often flooded habitats.
Distribution in Baltic countries Although first data on the distribution of carabid species in the Baltic countries go back to the 19th century (Fleischer, 1829; Seidlitz, 1872; 1875), the first noticeable faunistic review on Estonian carabids was published more than 100 years later by 47 Comparative Morphology and Morphometry Haberman (1968). Brief descriptions of morphology, biology and distribution of Badister species were published in his monograph. Later, almost similar overviews of the genus were presented in Lithuania and Latvia (Pileckis and Monsevičius, 1995; Barševskis, 2003). The data on distribution of four species, including B. unipustulatus, B. bullatus (=bipustulatus), B. lacertosus and B. meridionalis, in Estonia and Latvia was presented; however, the last-mentioned species was absent from Lithuanian fauna. The first record of B. meridionalis in Lithuania was noted by Barševskis (2001). Assuming the results of our study, we largely confirm the distribution ofB. unipustulatus, B. bullatus and B. lacertosus in the Baltic countries; however, we suggest corrections of the data on B. meridionalis. We found that some previously published data on distribution of this species (Haberman, 1968; Leskina, 2000; Barševskis, 2003; Barševskis et al., 2009) were based on misidentifications. Unfortunately, the material of some Latvian records of this species (Barševskis, 1993; Cibulskis, 1994; Kalniņš et al., 2007; Bukejs et al., 2009; Bukejs 2009) and one Lithuanian record (Barševskis, 2001) were not available for reexamination. Nevertheless, we assuredly doubt the records of B. meridionalis in winter rape and potato crops (Bukejs, 2009; Bukejs et al., 2009) and wish to attribute them to B. bullatus. Four specimens of B. meridionalis we examined from the Estonian Museum of Natural History contained label information on two pieces of papers: “Livonia” and “Bolz”. Unfortunately, these data are not enough for trustworthy confirmation of collecting these specimens in Estonia or Latvia. Two specimens of B. meridionalis were examined from the Kaunas Tadas Ivanauskas Zoological Museum (Lithuania) collected in central part of Lithuania in Kaunas environs. So, currently we can confirm the distribution of all four our studied species only for Lithuania, while in Estonia and Latvia only three species: B. unipustulatus, B. bullatus, and B. lacertosus, are really detected (Fig. 15). It is believable that the northern border of the distribution range of B. meridionalis can extend further north and the occurrence of this species in Latvia and Estonia is quite realistic.
ACKNOWLEDGMENT We are grateful to Berndt Jeager (Berlin Nature Museum, Germany), Katja Neven (Bavarian State Collection of Zoology, Germany), Tomasz Huflejt (Museum and Institute of Zoology, Polish Academy of Science), Märt Kruuz (Estonian Museum of Natural History, Estonia), Viktor Brygadyrenko (Dniepropetrovsk National University, Ukraine), Håkan Ljungberg (Sweden), Oleg Aleksandrowich (Poland), Dmitry Telnov, Florian Savich, Alexander Napolov, Voldemars Spungis, Janis Gailis, Nikolajs Savenkovs (Latvia), Aleksandr Meržijevskij (Lithuania) for loaning material for the study. Also, we award many thanks to Borislav Gueorguiev (Bulgaria), Alexander Anichtchenko (Latvia) and Pietro Brandmayr (Italy) for valuable advice and Gintautas Steiblys, Kazymieras Martinaitis, (Lithuania) and Raimonds Cibulskis (Latvia) for making some photographs. 48 Tamutis, V., Balalaikins, M., Barševskis A., Ferenca, F.
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Received: August 19, 2016 Accepted: November 13, 2017
J. Entomol. Res. Soc., 20(1): 53-58, 2018 ISSN:1302-0250
Notes on Some Species of Gnophini (Ennominae, Geometridae, Lepidoptera) from Turkey, with New Records
Erdem SEVEN
Department of Gatronomy and Culinary Arts, School of Tourism and Hotel Management, Batman University, 72060 Batman, TURKEY, e-mail: [email protected]
ABSTRACT In this paper, three species of the tribe Gnophini are recorded for the first time from Turkey:Charissa adjectaria Staudinger, 1898; C. annubilata (Christoph, 1885) and Gnophos sacraria Staudinger, 1895. Furthermore, two little-known Gnophos Treitschke, 1825 species are presented: G. mardinaria Staudinger, 1901 and G. libanotica (Wehrli, 1931). Male genitalia and adult images of Charissa annubilata, Gnophos sacraria and G. mardinaria with female genitalia and adult images of G. libanotica are illustrated here as new. Key words: Ennominae, Geometridae, Lepidoptera, new records, Siirt, Batman, Turkey.
INTRODUCTION The subfamily Ennominae, in terms of described species largest and morphologically most diversified moths in the family Geometridae, with over 10.700 described species so far (Scoble, 1999; Scoble and Hausmann, 2007). Majority, of species are well defined by a morphological character, the weakening or absence of the vein M2 in the hind wings. On the other hand, the tribal composition and phylogeny of the subfamily are still far from being resolved (Beljaev, 2006; Sihvonen et al., 2011). In fact, some classification difficulties are ongoing in this group (Gnophini), even at the genus level. In this regard, detailed morphological and molecular studies are required to solve problems. To determine the distrubition areas and for identification of the species in this paper references of Prout, 1912-1916; Seven, 1991; Doğanlar and Kornoşor, 2003; Özdemir, 2007; Okyar and Mironov, 2008; Koçak and Kemal, 2009; Skou and Sihvonen, 2015 were used. Studies on the family Geometridae are still inadequate, especially for the south east of Turkey. With this study, the author provides important new faunistic information, which is relevant not only for Turkey, but also for the adjacent areas. In addition, the illustration of species (adults and genitalia) as photographs are very valuable because in many instances these have not been published before. 54 SEVEN, E. MATERIALS AND METHODS The materials were caught between in the years 2014 and 2015, on the territory of Batman and Siirt Provinces from SE Turkey. In addition, some specimens, which were collected in the 2013 and couldn’t have been exactly identified, were also utilized. Moths were caught in an entomological light trap, killed by ethyl acetate, and pinned or packed in transport envelopes. Specimens were prepared, labeled, and deposited according to standard entomological methods. For the exact identification, the author prepared the genitalia of the species. The materials are deposited in the laboratory of Batman University, Faculty of Arts and Sciences, Department of Biology. In this species-rich group, where relatively little has been published recently, for many taxa identifications appear impossible without genitalia dissections. External and internal morphological characters of the species in this study were compared with in the Museum für Naturkunde (Germany), for warranting the correct identification.
RESULTS
Charissa adjectaria Staudinger, 1897 (Fig. 1)
Material examined: 7♂♂, Batman, Batıraman, 570 m, 15.10.2015 (Genital dissection: Gp2015-57♂; Gp2015-58♂). Diagnosis: Wing span 19-20mm in male. Antenna bipectinate, pale brownish-greyish. The discal spot and postmedian line of fore wing not very clearly marked. Hind wing dirty white-grey, discal spot darker colored. Underside dirty white-grey, quite weakly marked. Male genitalia: Uncus well developed, broad. Juxta long and has two-pronged arms almost half length of valva. Costa has a spine, slightly curved apically. Aedeagus long, with a cornutus covering almost half of its length.
Fig. 1. Adult and male genitalia of Charissa adjectaria Staudinger, 1897 (Gp2015-57). Remarks: The species ‘‘adjectaria’’ was described and illustrated by Staudinger (1897) from Jordan Valley. After that, Prout (1912-1916) presented on its distribution as “Palestine” without exact locality. This species is distributed in Central Asia (Turkmenistan), with a subspecies C. adjectaria daritshevae Viidalepp, 1991 (Vasilenko, 2016). C. adjectaria is recorded for the first time from Turkey. It was collected in October, at the rocky mountainous steppe area from Batman Province, 55 Notes on Some Species of Gnophini from Turkey south-eastern Turkey. For identification, studies of Staudinger (1897), Prout (1912- 1914) and Hausmann (1991) were used.
Charissa annubilata (Christoph, 1885) (Fig. 2)
Material examined: 6♂♂, 2♀♀ Siirt, Şirvan: 1♂ Nergizli, 650 m, 04.10.2013 (Genital dissection: Gp308♂♂); 3♂♂ Karaca crossroad, 1300 m, 13.10.2013 (Genital dissection: Gp310♂♂); 2♂♂ 1♀ Maden crossroad, 965 m, 17.10.2014; 1♀ Nergizli (rocky area), 650 m, 08.10.2014. Diagnosis: Wing span: 16-17 mm in male, 20-21 mm in female. Antenna filiform. Fore wing yellowish-grey, towards the distal margin especially dark, discal spots weak, barely visible. Antemedial line broad, arcuated outwards, postmedial line angled obtusely near the costal margin and a little oblique, slightly dentate outwards. Male genitalia: Uncus narrow, well developed. Harpe elongated, tapering spine-shaped. Aedeagus small and weak sclerotized. Male genitalia of this species are characteristic and different from all others in the genus.
Fig. 2. Adult and male genitalia of Charissa annubilata (Christoph, 1885) (Gp310). Remarks: The species was described and illustrated by Christoph (1885) from Khotchaldagh near Lagodekhi in Azerbaidjan. Prout (1912-1916) mentions it from “Transcaucasia”. The present knowledge on distribution of the species is from Georgia (Didmanidze, 2002), Azerbaidjan, Iran (Koçak and Kemal, 2014), to Turkmenistan (Vasilenko, 2016). It is reported as new for the fauna of Turkey. For identification, the original description of Christoph (1885) was used.
Gnophos libanotica (Wehrli, 1931) (Fig. 3)
Material examined: 2♀♀ Siirt, Şirvan, Nallıkaya (Dikilitaş), 1870 m, 12.06.2015 (Genital dissection: Gp2015-15♀). Diagnosis: Wing span 29 mm in female. Antenna of female filiform. Medial line of fore wing broader and dentate, yellowish-brown colored, postmedial line not very definite. Pattern of hind wing similar to that of forewing but discal spot less definite. Underside pale-white and without spots. Female genitalia: Ductus bursae long, sclerotized and straight with many spines fused to inside and attached to the slender corpus bursae. Papillae anales large and sclerotized. Appendix bursae large and slipper shaped. Remarks: The valid name ‘‘libanotica’’ was described in 1931 by Wehrli from Lebanon. In Turkey, this species is, hitherto known from Antalya (Koçak, 1966-2016) 56 SEVEN, E. and Niğde (Aladağları) Provinces (Riemis, 1998). It is new for the Lepidoptera fauna of Siirt Province and Şirvan discrict (Seven, 2014). The species inhabits humid area with intense Quercus and Astragalus plant species. For identification, the studies of Wehrli (1931) and Prout (1912-1914) were used.
Fig. 3. Adult and female genitalia of Gnophos libanotica (Wehrli, 1931) (Gp2015-15).
Gnophos mardinaria Staudinger, 1901 (Fig. 4)
Material examined: 21♂♂ 10♀♀ Siirt, Şirvan: 5♂♂ 1♀ İncekaya, 1200 m, 16.07.2013; 1♂ Maden gate, 1400 m, 01.07.2013; 1♂ 1♀ Centre of Şirvan, 1000 m, 13.04.2013, 30.06.2013; 1♂ Boylu, 1000 m, 11.07.2013; 8♂♂ Yağcılar, 1150 m, 12.07.2013 (Genital dissection: Gp272♂, Gp291♂, Gp456♂); 2♀ Yayladağ, 1500 m, 16.07.2013; 2♂♂ Maden crossroad; 965 m, 27.06. 2014; 3♀♀ Suluyazı 1320 m, 28.04.2014; 2♂ Hürmüz crossroad, 1150 m, 12.05.2014; 1♂ Maden road, 1100 m, 05.07.2014; 3♀♀ Tomdere (bridge), 600 m, 27.05.2015. Diagnosis: Wing span 29-31 mm in male, 31-32 mm in female. Antenna thick and filiform. Terminal line on the fore wing, indistinct, dark brown. Medial line unclear, discal spot big and definite. The distal margin of the hind wing is deeply arched. Underside yellowish and characterized by having a broad blackish distal border to both wings. Male genitalia: Uncus broad and well developed. Sacculus sclerotized, at tip projecting outwards. Ventral (posterior) arms of juxta broad, at tip truncate and pronged. Lateral arms of juxta short and digitiform. Aedeagus large, robust, with a thin stick-shaped cornutus.
Fig. 4. Adult and male genitalia of Gnophos mardinaria Staudinger, 1901 (Gp456). Remarks: Gnophos mardinaria was described by Staudinger in 1901 from Mardin Province (Turkey). Prout (1912-1916) has indicated its distribution as “Mesopatamia’’. Later, the species was reported by Koçak and Kemal (2014) from Turkey, Iran and Iraq. The reliable record was given in Turkey from Mardin Province by Staudinger (1901) and Kayseri Province (Koçak and Kemal, 2009; Koçak, 1966-2016). The 57 Notes on Some Species of Gnophini from Turkey present record is new for the fauna of Siirt Province! For identification, the studies of Staudinger (1901) and Prout (1912-1916) were used.
Gnophos sacraria Staudinger, 1894 (Fig. 5)
Material examined: 8♂♂, 3♀♀ Siirt, Şirvan: 6♂♂ Kasımlı, 650 m, 06.10.2013 (Genital dissection: Gp283♂, Gp284♂); 2♀♀ Nergizli, 650 m, 07.10.2014; 2♂♂ 1♀ Maden crossroad, 965 m, 11.10.2014. Diagnosis: Wing span 23-25 mm in male, 25-26 in female. Antenna bipectinate. Palpus extremely small. Fore wing brown-greyish, finely and densely spotted with dark scales, and with indefinite traces of antemedial line, small but definite discal spot, postmedian line consisting of dots. Hind wing with the discal spot unclear, postmedial line same on forewing. Male genitalia: Costa of valva sclerotized, with a short and thick horn. Uncus well developed. Ventral arms of juxta long and two-pronged shaped. Dorsal arms of juxta short, enlarged and sclerotized. Aedeagus long and thickened near apex.
Fig. 5. Adult and male genitalia of Gnophos sacraria Staudinger, 1894 (Gp284) Remarks: The species was described by Staudinger (1894) from Israel (Jerusalem). After that, Rebel (1912) has recorded it from Egypt and Prout (1912-1916) has specified its distribution as “Palestine”. In the current study the author suggests that this species shows a wider distribution in the northern countries of the Middle East. In Turkey, it was found only from Siirt Province, southeast of Turkey, with this study. It was captured in October near by river side. For identification, studies of Staudinger (1894) and Prout (1912-1916) were used.
ACKNOWLEDGEMENTS I would like to thank Dr. Sven Erlacher (Museum für Naturkunde, Chemnitz, Germany) and Dr. Ahmet Ö. Koçak, Dr. Muhabbet Kemal Koçak (Yüzüncü Yıl University, Van, Turkey) for their considerable help in determining of the species and for useful suggestions.
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Received: September 11, 2016 Accepted: November 15, 2017 J. Entomol. Res. Soc., 20(1): 59-72, 2018 ISSN:1302-0250
New Contributions to the Ichneumoninae (Hymenoptera, Ichneumonidae) from Turkey
Matthias RIEDEL1 Erich DILLER1 Saliha ÇORUH2*
1Zoologische Staatssammlung München, Münchhausenstr. 21, D-81247 Munich, GERMANY. 2Atatürk University, Faculty of Agriculture, Department of Plant Protection, 25240 Erzurum, TURKEY. *e-mail: [email protected]
ABSTRACT In this study new distributional records of 63 species of the subfamily Ichneumoninae (Hymenoptera, Ichneumonidae) are given from Turkey, 22 of them (Aethecerus exilis Wesmael, Baeosemus mitigosus (Gravenhorst), Diadromus pulchellus Wesmael, Dicaelotus erythrostoma Wesmael, Dicaelotus rufiventris (Berthoumieu), Heterischnus bicolorator (Aubert), Heterischnus coxator (Thomson), Heterischnus filiformis (Gravenhorst), Heterischnus nigricollis (Wesmael), Heterischnus pictipes (Kriechbaumer), Heterischnus pulex (Müller), Tycherus fuscicornis fuscicornis (Wesmael) Tycherus ophtalmicus ophtalmicus (Wesmael), Coelichneumon moestus (Gravenhorst), Barichneumon vicarius (Wesmael), Barichneumon peregrinator (Linnaeus), Cratichneumon rufifrons (Gravenhorst), Ctenichneumon devylderi (Holmgren), Ctenichneumon tauricus (Kriechbaumer), Limerodes arctiventris (Schiödte), Rictichneumon pachymerus (Hartig), Triptognathus rubrocinctus (Lucas), are new for the Turkish fauna. The number of known Turkish Ichneumoninae has increased to 237 species. Key words: Ichneumoninae, Ichneumonidae, new record, Turkey.
INTRODUCTION The ichneumonids are one of the most important parasitic insects and also one of the largest in the Insecta (Gauld, 2002). Ichneumonidae present a number of biological and behavioral features resulting from the forms life of special interest. Because of the abundance of species, their wide distribution, and their importance in natural control of many leading crop pests, they have been extensively studied and a vast literature is available (Yu et al., 2012). But despite their abundance and important role in ecosystems and as biological pest control, the taxonomy, ecology, and distribution of many groups of Ichneumonidae still remain incompletely known (Quicke, 2015). The Ichneumoninae is the second largest subfamily of Ichneumonidae with about 424 genera and 4300 species (Yu et al., 2012) Up to 1995 (Kolarov, 1995), only 65 ichneumonine species belonging to 27 genera have been documented. Although the Ichneumoninae fauna of Turkey has been studied extensively in the last years, the biodiversity of Turkey is still incompletely known. After 1995, with the below mentioned contributions (Özdemir, 1996; Kolarov et al., 1997; Yurtcan et al., 1999; Çoruh et al., 60 RIEDEL, M., DILLER, E., ÇORUH S. 2002; Kolarov et al., 2002; Özbek et al., 2003; Çoruh et al., 2005; Kolarov, 2007; Çoruh and Özbek, 2008; Çoruh and Kesdek, 2008; Riedel, 2008; Gürbüz et al., 2008; Yurtcan and Okyar, 2008; Riedel et al., 2010; Çoruh et al., 2011; Eroğlu et al., 2011; Riedel et al., 2011; Çoruh et al., 2011; Çoruh and Özbek, 2013; Çoruh et al., 2014; Kolarov et al. 2014a,b, Özdan, 2014; Çoruh, 2017) the numbers of Ichneumoninae fauna of Turkey reached to 215 species and 61 genera. The aim of this study is to present the complete records of preserved material in order to improve knowledge about diversity of this important group in Turkey.
MATERIAL AND METHODS The material of Ichneumoninae was collected in different localities (Erzurum, Erzincan, Ardahan, Isparta, Kars, Rize, Iğdır, Artvin, Bayburt, Bolu, Diyarbakır, Ankara, Giresun, Trabzon, Hakkari, Kayseri, Sivas, Antalya, Antakya, Ağrı, Konya, Bolu) in Turkey (Fig. 1). The materials were collected from different flowering plants by using a standart sweeping net. Besides, malasia traps were set in some localities (Kars, Sarıkamış, Karakurt) and caught in this way. General distributions of the species were taken from Yu et al. (2012). In this study, all identifications of Phaeogenini were done by E. Diller, the other groups were determined by M. Riedel. All specimens were deposited at the following museums:
Abbreviation of institutions EDI-National Museums of Scotland, Edinburgh/Scotland, EMET-University of Atatürk, Erzurum/Turkey, NHM-Natural History Museum, London/England, ZSM-Zoologische Staatssammlung München/Germany
RESULTS
Tribe: Phaeogenini Förster, 1869
Genus: Aethecerus Wesmael, 1845
Aethecerus exilis Wesmael, 1848
Material examined: Erzurum, Hınıs, 1750 m, 19.07.2011, 1♂, leg. S. Çoruh (EMET). Distribution: Europe, new for Turkey.
Genus: Baeosemus Forster, 1869
Baeosemus mitigosus (Gravenhorst, 1829)
Material examined: Erzurum, Güngörmez, Dumlubaba, 2500 m, 01.07.2010, 1♂, leg. E. Yıldırım (EMET). Distribution: Palearctic region, new for Turkey. 61 New Contributions to the Ichneumoninae from Turkey
Fig. 1. Study map.
Genus: Colpognathus Wesmael, 1844
Colpognathus divisus Thomson, 1891
Material examined: Erzurum, Ispir, Fısırık 2300 m, 12.07.2011, 1♂, leg. S. Çoruh (EMET). Distribution: Palearctic region, known from Turkey (Diller and Schönitzer, 2003; Kolarov et al., 2014a).
Genus: Diadromus Wesmael, 1844
Diadromus collaris (Gravenhorst, 1829)
Material examined: Erzurum, Hınıs, 1750 m, 19.07.2001, 1♂, leg. S. Çoruh (EMET), Oltu, Başaklı, 1850 m, 22.08.2001, 1♂, leg. S. Çoruh (EMET), Tutmaç-Oltu, 1700-2100 m, 31.07.2001, 1♀, 1♂, leg. Ö. Çalmaşur (EMET), Tortum, Bağbaşı, 1600 m, 11.09.2001, 1♀, leg. S. Çoruh (EMET). Distribution: Almost worldwide, known from Turkey (Avcı and Özbek, 1990; Özdemir, 1996; Çoruh et al., 2002; Özbek et al., 2003; Çoruh et al., 2013; Çoruh et al., 2014).
Diadromus pulchellus Wesmael, 1845
Material examined: Erzurum,Tortum, Katıklı, 1850 m, 1♀, 12.07.2001, leg. E. Yıldırım (EMET). Erzincan, Çağlayan road side, 1100 m, 1♀, 1♂, 06.07.2001, leg. H. Özbek (EMET). Distribution: Europe, new for Turkey. 62 RIEDEL, M., DILLER, E., ÇORUH S. Diadromus subtilicornis (Gravenhorst, 1829)
Material examined: Ardahan, 2015 m, 17.07.2004, 1♀, leg. S. Çoruh (EMET). Distribution: Holarctic region, known from Turkey (Özdemir, 1996; Özbek et al., 2003; Çoruh et al., 2014).
Genus: Dicaelotus Wesmael, 1844
Dicaelotus erythrostoma Wesmael, 1845
Material examined: Erzurum, Konaklı, 2000-2400 m, 22.07.2000, 1♂, leg. S. Pekel (Çoruh) (EMET), Güngörmez, Dumlubaba, 2500 m, 1.07.2010, 1♂, leg. E. Yıldırım (EMET), Abdurrahman Gazi Türbesi, 2400 m, 8.07.2004, 1♂, leg. O. Kaya (EMET). Distribution: Europe, new for Turkey.
Dicaelotus morosator Aubert, 1969
Material examined: Erzincan, Gülkaymak, 1200 m, 25.05.2001, 2♂♂, leg. R. Hayat (EMET). Erzurum, Umudum Yaylası, 2100 m, 26.06.2003, 1♂, leg. E. Yıldırım (EMET). Kars, Sarıkamış, Karakurt, 10-19. VI.2003, 1♂, leg. H. Özbek (EMET). Distribution: Western Palearctic region, known from Turkey (Kolarov, 1995).
Dicaelotus rufiventris (Berthoumieu, 1899)
Material examined: Erzincan, Bahçeli, 1350 m, 28.05.2001, 2♂♂, leg. Ö. Çalmaşur (EMET), Gülkaymak, 1200 m, 25.05.2001, 1♂, leg. R. Hayat, 29.05.2001, 1♂, leg. C. Güçlü (EMET). Erzurum, Aşkale, Aşağı Kop Mountain 1900 m, 29.05.2001, 1♂, leg. C. Güçlü (EMET), Şenkaya, Gaziler, 1100 m, 17.05.2005, 1♂, leg. C. Güçlü (EMET), Soğanlı Mountain, 2450 m, 04.08.2005, 1♂, leg. S. Çoruh and C. Güçlü (EMET). Kars, Aras Valley, TCK Fountain, 1500-1800 m, 23.05.2001, 1♂, leg. S. Çoruh (EMET). Distribution: Europe, new for Turkey.
Genus: Dirophanes Foerster, 1869
Dirophanes benjamini Hower, 2006
Material examined: Isparta, Dere Mahallesi, 7.07.2004, 1♀, leg. S. Çoruh (EMET). Distribution: Only known from Turkey (Schönitzer et al., 2006).
Dirophanes regenerator (Fabricius, 1804)
Material examined: Erzurum, Oltu, Subatık, 09.08.2000, 1♂, leg. H. Özbek (EMET). Kars, Sarıkamış, Karakurt, TCK Fountain, 1500 m, 19.08.2003, 1♀, leg. S. Çoruh (EMET). Distribution: Palearctic region, known from Turkey (Schönitzer et al., 2006).
Genus Heterischnus Wesmael, 1859
Heterischnus bicolorator (Aubert, 1965)
Material examined: Erzurum, Konaklı, 2000-2400 m, 22.07.2000, 1♂, leg. Ö. Çalmaşur (EMET). 63 New Contributions to the Ichneumoninae from Turkey Distribution: Europe, new for Turkey.
Heterischnus coxator (Thomson, 1891)
Material examined: Rize, Ovit, Ikizdere, 2300 m, 29.07.2000, 1♀, leg. H. Özbek (EMET). Distribution: Western Palearctic region, new for Turkey.
Heterischnus filiformis (Gravenhorst, 1829)
Material examined: Kars, Aras Valley, TCK Fountain, 1500-1600 m, 23.05.2001, 1♀, leg. Ö. Çalmaşur (EMET). Distribution: Western Palearctic region, new for Turkey.
Heterischnus nigricollis (Wesmael, 1845)
Material examined: Erzurum, Senkaya, Turnalı, 1750 m, 22.08.1999, 1♂, leg. E. Yıldırım (EMET). Distribution: Palearctic region, new for Turkey.
Heterischnus pictipes (Kriechbaumer, 1894)
Material examined: Iğdır, Çalpala, 950 m, 16.06.2001, 1♀, leg. C. Güçlü (EMET). Distribution: Europe, new for Turkey.
Heterischnus pulex (Müller, 1776)
Material examined: Erzurum, Uzundere, Balıklı, 1000 m, 29.06.2003, 1♂, leg. S. Çoruh (EMET). Distribution: Western Palearctic region, new for Turkey.
Heterischnus ridibundus (Costa, 1885)
Material examined: Artvin, 300 m, 16.05.2005, 1♀, leg. C. Güçlü (EMET). Distribution: Western Palearctic region, known from Turkey (Yurtcan et al., 1999).
Genus Tycherus Forster, 1869
Tycherus fuscicornis fuscicornis (Wesmael, 1845)
Material examined: Erzincan, Bahçeli, 1350 m, 26.05.2001, 1♀, leg. Ö. Çalmaşur (EMET). Erzurum, Ilıca, Atlıkonak, 2100 m, 21.06. 2004, 1♀, leg. C. Güçlü (EMET), Şenkaya, Çakırbaba Pass, 2450 m, 09.08.2003, 1♂, leg. S. Çoruh (EMET). Distribution: Europe, new for Turkey.
Tycherus ophtalmicus ophtalmicus (Wesmael, 1845)
Material examined: Ardahan, Göle, Ormanlık Alan, 2160 m, 25.07.2005, 1♀, leg. C. Güçlü (EMET). Distribution: Holarctic region, new for Turkey. 64 RIEDEL, M., DILLER, E., ÇORUH S. Tribe Platylabini Berthoumieu,1904 Genus: Apaeleticus Wesmael, 1845 Apaeleticus bellicosus Wesmael, 1845
Material examined: Erzurum, Ilıca, Atlıkonak 2000-2400 m, 29.06.2001, 1♀, leg. Ö. Çalmaşur (EMET). Kars, Sarıkamış, Karakurt 1501 m, 10-19.06.2003, 1♀, leg. S. Çoruh (EMET). Distribution: Western Palaearctic region, known from Turkey (Riedel et al., 2010; Çoruh et al., 2014). Apaeleticus inimicus (Gravenhorst, 1820)
Material examined: Erzurum, Güngörmez, Dumlubaba 2500 m, 1.07.2010, 1♂, leg. E. Yıldırım, (EMET), Hınıs, 1750 m, 19.07.2001, 1♀, leg. S. Çoruh (EMET). Distribution: Western Palaearctic region, known from Turkey (Coruh et al., 2011; Çoruh et al., 2014). Genus: Linycus Cameron, 1903 Linycus exhortator (Fabricius, 1787)
Material examined: Rize, Camlıhemşin, 500-1200m, 30.07.2000, 1♂, leg. E. Yıldırım (EMET). Distribution: Holarctic regions, known from Turkey (Fahringer, 1922; Kolarov, 1995; Özbek et al., 2003; Çoruh et al., 2014). Genus: Platylabus Wesmael, 1844 Platylabus iridipennis (Gravenhorst, 1829)
Material examined: Kars, Sarıkamış, Karakurt, 1425 m, 09.05.2002, 1♂, leg. G. Tozlu (EMET). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010; Çoruh et al., 2014). Platylabus tricingulatus (Gravenhorst, 1820)
Material examined: Artvin, Coruh valley near Oltu-Yusufeli Road, 16.06.2001, 2 ♀♀, leg. Ö. Çalmaşur (EMET). Distribution: Palaearctic region, known from Turkey (Özdemir, 1996; Riedel et al., 2010; Çoruh et al., 2014).
Tribe: Listrodromini Förster,1869
Genus: Anisobas Wesmael, 1844
Anisobas brombacheri Heinrich, 1933
Material examined: Erzincan, Mercan Yollarüstü, 1360 m, 4.08.2003, 1♀, leg. S. Çoruh (EMET). Erzurum, Konaklı, 2000-2400 m, 22.07.2000, 1♀, leg. H. Özbek (EMET). 65 New Contributions to the Ichneumoninae from Turkey Distribution: Palaearctic region, known from Turkey (Özbek et al., 2003; Çoruh et al., 2014).
Anisobas cingulatellus Horstmann, 1997 (syn. cingulatorius Gravenhorst)
Material examined: Artvin, Yusufeli, Sebzeciler, 560 m, 16.06.2010, 1♀, leg. E. Yıldırım, (EMET). Erzurum, Tortum, Yukarısivri, 21.07.2010, 1♂, leg. H. Özbek (EMET). Distribution: Palaearctic region, known from Turkey (Kohl, 1905, Yurtcan et al., 1999, Coruh et al., 2005; Riedel et al., 2010; Çoruh et al., 2011; Çoruh et al., 2013; Kolarov et al., 2014a, Kolarov et al., 2014b; Özdan, 2014).
Genus Neotypus Förster,1869
Neotypus coreensis Uchida, 1930 (syn. lapidator Fabricius)
Material examined: Bayburt, Çalıdere 1700 m, 17.06.2010, 1♀, leg. S. Çoruh (EMET). Erzurum, Tortum, Yukarısivri, 21.07.2010, 1♀, leg. H. Özbek (EMET). Distribution: Holarctic regions, known from Turkey (Riedel et al., 2010).
Tribe: Heresiarchini Ashmead, 1900
Genus: Coelichneumon Thomson, 1893
Coelichneumon moestus (Gravenhorst, 1829)
Material examined: Erzurum, Oltu, Kaleboğazı, 1450 m, 18.09.2001, 1♀, leg. S. Çoruh (EMET). Distribution: Western Palaearctic region, new for Turkey.
Coelichneumon pararudis Riedel, 2008
Material examined: Erzurum, Atatürk University Campus, 1850 m, 14.07.2003, 1♀, leg. H. Özbek (EMET). Distribution: Known from Kyrgyzstan and Turkey (Riedel, 2008).
Tribe: Ichneumonini Latreille,1802
Genus: Baranisobas Heinrich, 1972
Baranisobas ridibundus (Gravenhorst, 1829)
Material examined: Isparta, Dere Mahallesi, 07.07.2004, 1♀, leg. S. Çoruh (EMET). Distribution: Western Palaearctic region, known from Turkey (Riedel et al., 2010).
Genus: Barichneumon Thomson, 1893
Barichneumon albicaudatus (Fonscolombe, 1847)
Material examined: Erzurum: Oltu, Başaklı, 1850 m, 22.08.2001, 1♀, leg. S. Çoruh (EMET). 66 RIEDEL, M., DILLER, E., ÇORUH S. Distribution: Palaearctic region, known from Turkey (Özdemir, 1996; Riedel et al., 2010).
Barichneumon bilunulatus (Gravenhorst, 1829)
Material examined: Erzurum, Kargapazarı Mountain, 2700 m, 25.07.2001, 1♂, leg. C. Güçlü (EMET). Distribution: Palaearctic region, known from Turkey (Aubert, 1993; Riedel et al., 2010).
Barichneumon vicarius (Wesmael, 1845) syn. sedulus auct.
Material examined: Bolu, Abant Izzet Baysal University Campus, 11-14.06.1999, 1♂, leg. Shaw (EDI). Distribution: Palaearctic region, new for Turkey.
Barichneumon peregrinator (Linnaeus, 1758)
Material examined: Diyarbakır, Dicle University Campus, 700 m, 01.06.2002, ♂, leg. H. Özbek (EMET). Distribution: Palaearctic region, new for Turkey.
Genus: Cratichneumon Thomson, 1893
Cratichneumon rufifrons(Gravenhorst, 1829)
Material examined: Ankara, Şereflikoçhisar, 11.07.1998, 1♂, leg. C. Güçlü (EMET). Distribution: Palaearctic region, new for Turkey.
Genus: Ctenichneumon Thomson, 1894
Ctenichneumon castigator (Fabricius, 1793)
Material examined: Artvin, Above Artvin 1800 m, 06.06.1962, 1♂ (NHM). Erzurum, 20 km S Ispir-Ikizdere Road, 1700 m, 01.06.1962, 1♀, 02.06.1962, 1♂ (NHM). Giresun, Yavuzkemal, 1600 m, 16.05.1962, 1♂ (NHM). Rize, Sivrikaya, 1700 m, 03.06.1962, 2♀♀ (NHM). Trabzon, Hamsiköy, 1245 m, 23.05.1962, 1♀ (NHM), Zigana Mountain, 4200 ft, 14.07.1960, 1♀ (NHM). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010; Riedel et al., 2011).
Ctenichneumon devylderi (Holmgren, 1871)
Material examined: Erzurum, Pasinler, Pelitli, 2200 m, 14.07.1996, 1♂, leg. E. Yıldırım (EMET). Distribution: Palaearctic region, new for Turkey.
Ctenichneumon inspector (Wesmael, 1845)
Material examined: Artvin, Çoruh Valley, 16.06.2001, 1♂, leg. S. Çoruh (EMET). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010).
Ctenichneumon nitens (Christ, 1791)
Material examined: Erzurum, Oltu, Camlıbel, 1500 m, 02.07.1997, 1♂, leg. E. Yıldırım, (EMET), Palandöken, 2400 m, 9.07.1996, 1♂, leg. E. Yıldırım (EMET). 67 New Contributions to the Ichneumoninae from Turkey Distribution: Palearctic region, known from Turkey (Riedel et al., 2011).
Ctenichneumon repentinus (Gravenhorst, 1820)
Material examined: Erzurum, Palandöken Mountain, 2400 m, 01.07.1996, 1♂, leg. E. Yıldırım (EMET), 1♂, 23.07.1996, leg. S. Pekel (Çoruh) (EMET). Hakkari, 16 km SE Yüksekova, 1700 m, 26.06.1985, 1♀, leg. M. Schwarz (ZSM). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010).
Ctenichneumon tauricus (Kriechbaumer, 1888)
Material examined: Ankara, Idris Mountain, 1300 m, 30.06.1962, 1♂ (NHM). Erzurum, 20 km S Ispir-Ikizdere Road, 1700 m, 02.06.1962, 1♂ (NHM). Trabzon, Hamsiköy, 1245 m, 23.05.1962, 2♂♂ (NHM). Distribution: Southern Europe, new for Turkey.
Genus: Diphyus Kriechbaumer, 1890
Diphyus longimanus (Wesmael, 1857)
Material examined: Erzurum, Palandöken Mountain, 2400 m, 23.07.1997, 1♂, leg. S. Pekel (Çoruh) (EMET). Distribution: Western Palaearctic region, known from Turkey (Çoruh et al., 2011).
Diphyus pseudomercator s.str. Heinrich, 1978
Material examined: Erzurum, Konaklı, 2000-2400 m, 22.07.2000, 1♂, leg. Ö. Çalmaşur (EMET). Distribution: Known from Turkey (Heinrich, 1978; Özbek et al., 2003).
Diphyus quadripunctorius (Müller, 1776)
Material examined: Ankara, Beynam, 15.06.1999, 1♀, leg. M. R. Shaw (EDI). Distribution: Palaearctic region, known from Turkey (Fahringer, 1922; Kolarov, 1989; Kolarov, 1995; Riedel et al., 2010).
Diphyus raptorius (Linnaeus, 1758)
Material examined: Ankara: Beynam, 15.06.1999, 1♀, leg. M. R. Shaw (EDI). Distribution: Palaearctic region, known from Turkey (Yurtcan et al., 1999).
Genus: Eutanyacra Cameron, 1903
Eutanyacra picta (Schrank, 1776)
Material examined: Erzurum, Palandöken DSI Göleti, 2000 m, 12.10.2002, 1♂, leg. M. Kesdek (EMET). Distribution: Palaearctic and Oriental regions, known from Turkey (Riedel et al., 2010). 68 RIEDEL, M., DILLER, E., ÇORUH S. Genus: Fileanta Cameron, 1901
Fileanta flaveolaeta(Berthoumieu, 1892)
Material examined: Hakkari, 30 km W Yüksekova, 1850 m, 19.07.1986, 1♂, leg. A.W. Ebmer (ZSM). Distribution: Known from Irnas and Turkey (Heinrich, 1978; Kolarov, 1995).
Fileanta radoszkowskii (Berthoumieu, 1892)
Material examined: Kayseri, Göreme, 1000 m, 09.07.1988, 1♂, leg. Schmid-Egger (ZSM). Konya, 25 km N Konya, 11.06.1966, 1♀, leg. H.H.F. Hamann (ZSM), Sille, 08.06.1978, 1♂, leg. M. Schwarz (ZSM). Distribution: Near East, Central Asia, known from Turkey (Kolarov, 1995).
Genus: Hepiopelmus Wesmael, 1845
Hepiopelmus melanogaster (Gmelin, 1790)
Material examined: Erzurum, Şenkaya, Soğanlı Mountain, 2450 m, 13.08.1998, 1♀, leg. H. Özbek (EMET). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010).
Genus: Ichneumon Linnaeus, 1758
Ichneumon balteatus Wesmael, 1845
Material examined: Erzurum, Oltu, Sarısaz, 1450 m, 21.06.2000, 1♂, leg. Ö. Çalmaşur (EMET). Distribution: Palaearctic region, known from Turkey (Özdemir, 1996; Riedel et al., 2010).
Ichneumon proletarius Wesmael, 1855
Material examined: Erzurum, Küçükgeçit, 1685 m, 20.06.1996, 1♀, leg. I. Aslan (EMET). Distribution: Palaearctic region, known from Turkey (Hilpert, 1992; Kolarov, 1995; Riedel et al., 2010; Çoruh et al., 2011; Kolarov et al., 2014a).
Ichneumon tuberculipes Wesmael, 1848
Material examined: Bayburt, Kop Pass, 31.08.2002, 1♂, leg. M. Kesdek (EMET). Erzurum, Altınçanak, 1150 m, 08.09.2005, 1♀, leg. H. Özbek, Palandöken, 2200 m, 06.08.1996, 1♀, leg. E Yıldırım, Atatürk University Campus, 15.08.1996, 1♂, leg. E. Yıldırım (EMET). Distribution: Palaearctic region, known from Turkey (Riedel et al., 2010).
Genus: Limerodes Wesmael, 1845
Limerodes arctiventris (Schiödte, 1838)
Material examined: Sivas, Cumhuriyet University Campus, 7-9.06.1999, 1♂, leg. M. R. Shaw (EDI). Distribution: Palaearctic region, new for Turkey. 69 New Contributions to the Ichneumoninae from Turkey Genus: Obtusodonta Heinrich, 1962
Obtusodonta equitatoria (Panzer, 1786)
Material examined: Kayseri, Develi, Erciyes Mountain, 1800 m, 05.07.1984, 1♀, leg. A. W. Ebmer (ZSM), Karakurt, Arastal, 1400 m, 09.06.1976, 1♀, leg. Ressl (ZSM). Distribution: Palearctic region, known from Turkey (Kolarov, 1989; Özdemir, 1996; Yurtcan, et al., 1999; Riedel et al., 2010; Çoruh et al., 2011; Çoruh and Özbek, 2013).
Genus: Pseudoamblyteles Heinrich, 1926
Pseudoamblyteles homocerus (Wesmael, 1854)
Material examined: Antalya, Finike, 50-100 m, 07.04.1962, 5♂♂ (NHM). Distribution: Holarctic regions, known from Turkey (Avcı and Özbek, 1990; Özdemir, 1996; Özbek et al., 2003; Riedel et al., 2010; Çoruh et al., 2011).
Genus Rictichneumon Heinrich, 1961
Rictichneumon lombardi (Berthoumieu, 1897)
Material examined: Antakya, 03.06.1952, 1♀, leg. M. Schwarz (ZSM). Erzurum, Konaklı, 2000-2400 m, 22.07.2000, 1♀, leg. Ö. Çalmaşur (EMET), 20 km SW Oltu, 2000 m, 07-08.07.1985, 1♀, leg. M. Schwarz (ZSM), Palandöken Mountain, 2200-2400 m, 28.07.1986, 1♀, leg. A.W. Ebmer (ZSM). Distribution: Western Palaearctic region, known from Turkey (Özbek et al., 2003; Riedel et al., 2010; Çoruh et al., 2011; Kolarov et al., 2014a).
Rictichneumon pachymerus (Hartig, 1838)
Material examined: Bolu, Abant Izzet Baysal University Campus, 11-14.06.1999, 1♀, leg. Shaw (EDI). Distribution: Holarctic regions, new for Turkey.
Genus Spilichneumon Thomson, 1894
Spilichneumon occisorius (Fabricius, 1793)
Material examined: Kars, 20 km W Sarıkamış, 2150 m, 04-06.07.1985, 1♀, leg. M. Schwarz (ZSM). Kayseri, Karakurt, Arastal,1400 m, 09.06.1976, 1♀, leg. Ressl (ZSM). Distribution: Palearctic region, known from Turkey (Özdemir, 1996; Özbek et al., 2003; Riedel et al. 2010; Özdan, 2014).
Genus: Thyrateles Perkins, 1953
Thyrateles camelinus (Wesmael, 1845)
Material examined: Erzurum, Serinkaya, 1850 m, 25.07.1996, 1♂, leg. E. Yıldırım (EMET). Distribution: Palearctic region, known from Turkey (Riedel et al., 2010). 70 RIEDEL, M., DILLER, E., ÇORUH S. Genus: Triptognathus Berthoumieu, 1904
Triptognathus atripes (Gravenhorst, 1820)
Material examined: Bayburt, Maden, 1650 m, 16.06.2000, 1♀, leg. Ö. Çalmaşur (EMET). Erzincan, Tercan, 17.07.1997, 1♂, leg. S. Pekel (Çoruh) (EMET). Erzurum, Olur, Süngübayır, 1850 m, 30.07.1999, 1♂, leg. I. Aslan (EMET). Distribution: Palearctic region, known from Turkey (Kolarov, 1995; Riedel et al., 2011).
Triptognathus rubrocinctus (Lucas, 1849)
Material examined: Ağrı, 50 km E Ağrı, 1800 m, 02.07.1985, 1♂, leg. M. Schwarz (ZSM). Hakkari, 10 km NE Oramar, 1700 m, 29.06.1985, 1♂, leg. M. Schwarz (ZSM). Distribution: Palearctic region, new for Turkey.
Triptognathus uniguttatus (Gravenhorst, 1829)
Material examined: Konya, Beyşehir, 16-19.06.1966, 1♀, leg. H. Hamann (ZSM). Distribution: Palearctic region, known from Turkey (Kohl, 1905).
DISCUSSION The numbers of Ichneumoninae fauna of Turkey is 215 species and 61 genera (Çoruh, 2017). With our new findings, the number has increased to 237 Turkish Ichneumoninae. In addition Dirophanes benjamini Hower is endemic to Turkey. However, comparing to better studied Mediterranean countries such as Spain with 406 species or Italy with 374 reported taxa (Yu et al., 2012), we suspect that there are many more taxa in Turkey.
ACKNOWLEDGEMENT We would like to thank G. Broad (London/England) and M.R. Shaw (Edinburgh/ Scotland) for their generous loan of Ichneumoninae species for identification. We are grateful to following persons who kindly help in the collection of the material: Dr. Hikmet Ozbek (retired), Erol Yıldırım, İrfan Aslan, Önder Çalmaşur, Göksel Tozlu (University of Atatürk, Erzurum), Coşkun Güçlü (Eskişehir University, Eskişehir), Memiş Kesdek (Sıtkı Koçman University, Muğla) and Orhan Kaya (Erzurum). We are also kindly thankful to Metin Demir (Atatürk University, Erzurum) for their contributions in the study map.
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Received: October 28, 2016 Accepted: January 22, 2018 J. Entomol. Res. Soc., 20(1): 73-85, 2018 ISSN:1302-0250
Annotated Checklist of Indian Elasmus (Hymenoptera: Chalcidoidea : Eulophidae) with a New Synonymy
Sarfrazul Islam KAZMI* Saroj SHEELA
Zoological Survey of India, M-Block, New Alipore, Kolkata 700 053, INDIA e-mails: *[email protected], [email protected]
ABSTRACT Here we present an annotated checklist of Elasmus from Indian region. The list is based on published literature and survey collection under state fauna series of zoological survey of India. It comprises total of 58 species of Elasmus Westwood, 1833 is given together with the Indian records in different states and Union territory of India. Besides the original combination, citation of the original description and type locality of each species is presented. Elasmus nigricoxa Prakash and Verma is probably a junior synonym of Elasmus punensis Mani and Saraswat. Key words: Elasmus, Elasmini, Chalcidoidea, India, biogeography.
INTRODUCTION The tribe Elasmini contains only genus Elasmus (Eulophidae, Eulophinae), based on molecular studies and DNA analyses of Eulophidae and Elasmidae, genus Elasmus has been reduced to a tribe of the subfamily Eulophinae, formerly classified as a separate family, Elasmidae (Gauthier et al. 2000). The genus contains over 258 species worldwide (Noyes, 2016). The Indian species of the genus Elasmus were reviewed by Verma et al., 2002 and Narendran et al., 2008. This genus is mostly primary parasitoids of the larvae of Lepidoptera or hyperparasitoids on them through various Hymenoptera, in particular the Ichneumonidae and Braconidae. Some species develop regularly both as primary and hyperparasitoids and are usually gregarious. The present paper contains a checklist of 58 species of Elasmus distributed in different states and Union territory of India. Original combination, type locality and synonymy of each taxon are given. Elasmus nigricoxa Prakash and Verma is probably a junior synonym of Elasmus punensis Mani and Saraswat.
MATERIAL AND METHODS The species are arranged in alphabetical order. The present checklist is reasonably completed to end of September 2016. The references given here are mainly to indicate the published literature consulted in extracting information on species described or recorded from the localities. The following abbreviations used in the text: BMNH - The Natural 74 KAZMI, S. I., SHEELA, S. History Museum, London, DZAMU - Department of Zoology, Aligarh Muslim University, Aligarh, India, DZUC - Department of Zoology, University of Calicut, Kerala, India, QMB - Queensland Museum, Brisbane, USNM - The U. S. National Museum, Washington, D.C., ZSIC, Zoological Survey of India Calicut, ZSI, Zoological Survey of India, Kolkata.
RESULTS
Genus Elasmus Westwood, 1833 Elasmus Westwood, 1833: 343 [Type species Elasmus flabellatus Fonscolombe, by monotypy]. Aneure Nees, 1834: 194 [Type species Aneure nuda Nees, designated by Gahan and Fagan, 1923: 12. Synonymy by Westwood, 1839: 74]. Heptocondyla Rondani, 1877: 182 [Type species Heptocondyla unicolor Rondani, by monotypy. Synonymy by Bouček, 1974: 252, 279]. Cyclopleura Cameron, 1913: 96 [Type species Cyclopleura fumipennis Cameron (Elasmus cameroni Verma and Hayat as replacement name), designated by Gahan and Fagan, 1923: 41. Synonymy by Waterston, in Mahdihasan, 1925]. Austelasmus Riek, 1967: 148 [Type species Elasmus trifasciativentris Girault, by original designation. Synonymy by Burks, in Krombein et al., 1979: 1020].
Elasmus alami Verma and Hayat, 2002 Elasmus alami Verma and Hayat, 2002: 271-272, ♀. Holotype ♀: India, Uttar Pradesh, Aligarh (BMNH). Distribution: Kerala, Bihar, Uttar Pradesh, Odisha, West Bengal. Host: Philodonta modesta Weise.
Elasmus alaris Narendran, 2008 Elasmus alaris Narendran, 2008 : 8-9, ♀. Holotype ♀: India, Kerala, Palghat (ZSIC). Distribution: Kerala. Host: Unknown.
Elasmus albopictus Crawford, 1910 Elasmus albopictus Crawford, 1910: 132, ♀♀. Type ♀: Philippine Islands, Manila (USNM). Distribution: Uttar Pradesh, West Bengal. Host: Tryporyza incertulus on Paddy, Eucosma critica Meyrick, Cnaphalocrosis medinalis Guenee.
Elasmus anamalaianus Mani and Saraswat, 1972 Elasmus anamalaianus Mani and Saraswat, 1972: 461-462, ♀. Holotyope ♀: India, Annamalai Hills (USNM). 75 Annotated Checklist of Indian Elasmus Distribution: Karnataka, Tamil Nadu. Host: Unknown.
Elasmus anticles Walker, 1846 Elasmus anticles Walker, 1846: 181, ♀. Type ♀: India, Mumbai (=Bombay) (BMNH). Elasmus albomaculatus Gahan, 1920: 347, ♀. Holotype ♀: Philippines, Manila, Luzon (USNM). Synonymy by Kerrich, 1970: 89-91. Elasmus ricinus Husain and Kudeshia, 1984: 363-365, ♀: India, Aligarh (Type lost?). Synonymy by Narendran et al., 2008: 15. Distribution: Kerala, Karnataka, Tamil Nadu, Uttarakhand, Uttar Pradesh, Gujarat, Jharkhand, Madhya Pradesh, Maharashtra, Odisha. Host: Apanteles malevolus Rolston through Hyblaea puera Cramer, Bracon sp. and Cheionus sp. through Epicephala pulcherrima (Linn.) in Philippines. Inglisia bivalvata Green (Coccidae) on Sandalwood.
Elasmus bathyskius Narendran, 2008 Elasmus bathyskius Narendran, 2008: 8, ♂, ♀. Holotype ♀: India, Kerala, Kottayam (ZSIC). Distribution: Kerala, Odisha. Host: Unknown.
Elasmus binocellatus Mani and Saraswat, 1972 Elasmus binocellatus Mani and Saraswat, 1972: 462-463, ♀. Holotype ♀: India, Nilgiri Hills (USNM). Distribution: Kerala, Tamil Nadu, Uttar Pradesh, Rajasthan, Delhi. Host: Unknown.
Elasmus brevicornis Gahan, 1922 Elasmus brevicornis Gahan, 1922: 50, ♂, ♀. Type ♀: Indonesia, Java, Buitenzora (USNM). Distribution: Kerala, Tamil Nadu, Andhra Pradesh, Goa, Maharashtra, Delhi, Madhya Pradesh, Odisha, Punjab, Uttarakhand, Uttar Pradesh, Rajasthan, West Bengal, Chhattisgarh, Assam, Haryana, Gujarat. Host: Biloba subsecivela; Cnaphalocrocis medinalis; Diaphania indica; Hapalia machaeralis on Tectona grandis; Lamprosema indicate; Lygropia quarternalis defoliating Helictares isora; Marasma suspicalis; Nausinoe geometralis. Braconid, Apanteles machaeralis.
Elasmus caligneus Narendran, 2008 Elasmus caligneus Narendran, 2008: 10, ♀. Holotype ♀: India, Kerala, Malappuram, Chandakunnu (ZSIC). 76 KAZMI, S. I., SHEELA, S. Distribution: Kerala, West Bengal. Host: Unknown.
Elasmus cameroni Verma and Hayat, 2002 Cyclopleura fumipennis Cameron, 1913: 97, ♀. Lectotype ♀: Borneo, Kuching (BMNH). Preoccupied in Elasmus by fumipennis Thomson, 1878. Elasmus fumipennis (Cameron): Ferriere, 1929: 416. Elasmus cameronii Verma and Hayat , 1986: 174. Replacement name for fumipennis Cameron not Thomson. Distribution: Kerala, Karnataka. Host: parasite of Lac and Sal.
Elasmus cavicolous Verma and Hayat, 2002 Elasmus cavicolous Verma and Hayat, 2002: 285-286, ♀. Holotype ♀: India, Maharashtra (BMNH). Distribution: Maharashtra, Madhya Pradesh, Uttarakhand. Host: Unknown.
Elasmus ceylonicus Ferriere, 1929 Elasmus ceylonicus Ferriere, 1929: 418, ♀. Lectotype ♀: Sri Lanka, Pelmadulla (BMNH). Distribution: Kerala, Karnataka, Tamil Nadu. Host: Psyche albipes Moore.
Elasmus claripennis (Cameron), 1913 Cyclopleura claripennis Cameron, 1913: 92, ♀. Type ♀: India, Dehradun (BMNH). Elasmus colemani Madhihassan, 1923: 69, ♀. Type ♀: India, Bangalore (?). Synonymy by Ferriere, 1928: 171. Elasmus claripennis (Cameron): Ferriere, 1928: 171-172. Distribution: Andhra Pradesh, Jharkhand, Karnataka, Odisha, Uttarakhand, Uttar Pradesh. Host: Cnaphalocrosis medinalis Guenee; Eublemma amabilis Moore parasitic on Kerria lacca Kerr.; Eublemma scitula ; Holocera pulveria Meyr. On lac; bred from lac Pelopidas mathias Fab.
Elasmus cyanomontanus Mani and Saraswat, 1972 Elasmus cyanomontanus Mani and Saraswat, 1972: 464, ♂. Holotype ♂: India, Nilgiri Hills (USNM). Distribution: Tamil Nadu. Host: Unknown. 77 Annotated Checklist of Indian Elasmus Elasmus dalhousieanus Mani and Saraswat, 1972 Elasmus dalhousieanus Mani and Saraswat, 1972: 465-467, ♂. Holotype ♂: India, Dalhousie (USNM). Distribution: Himachal Pradesh. Host: Unknown.
Elasmus deccanus Mani and Saraswat, 1972 Elasmus deccanus Mani and Saraswat, 1972: 467-468, ♂. Holotype ♂: India, Pune (USNM). Distribution: Maharashtra. Host: Unknown.
Elasmus dexotus Narendran, 2008 Elasmus dexotus Narendran, 2008: 6-7, ♀. Holotype ♀: India, Kerala, Wayanad, Kalpetta (ZSIC). Distribution: Kerala. Host: Unknown.
Elasmus dubiatus Narendran, 2008 Elasmus dubiatus Narendran, 2008: 6, ♀. Holotype ♀: India, Kerala, Calicut Univ. campus (ZSIC). Distribution: Kerala. Host: Unknown.
Elasmus flavescens Verma and Hayat, 2002 Elasmus flavescens Verma and Hayat, 2002: 284-285, ♀. Holotype ♀: India, Karnataka (BMNH). Distribution: Kerala, Karnataka, Maharashtra. Host: Unknown.
Elasmus flavocorpusHusain and Kudeshia, 1984 Elasmus flavocorpusHusain and Kudeshia, 1984: 28, ♀. Holotype ♀: India, Aligarh (Not found in ZDAMU). Distribution: Kerala, Delhi, Uttar Pradesh, Himachal Pradesh. Host: Cocoons of Apanteles sp. on Ricinus communis L.
Elasmus fulvicornis Verma and Hayat, 2002 Elasmus fulvicornis Verma and Hayat, 2002: 286-287, ♀. Holotype ♀: India, Uttar Pradesh, Aligarh (BMNH). Distribution: Uttar Pradesh, West Bengal. Host: Unknown. 78 KAZMI, S. I., SHEELA, S. Elasmus grimmi Girault, 1920 Elasmus grimmi Girault, 1920: 186, ♀. Holotype ♀: Australia, Locality not given (QMB). Austelasmus grimmi (Girault): Riek, 1967:148. Distribution: Tamil Nadu, Karnataka, Kerala, Uttar Pradesh, Rajasthan. Host: Unknown.
Elasmus homonae Ferriere, 1929 Elasmus homonae Ferriere, 1929: 415-416, ♀, ♂. Lectotype ♀: Sri Lanka (BMNH). Distribution: Kerala, Tamil Nadu, Uttar Pradesh. Host: Cydia leucostoma Meyrick; C. tricentra Meyrick; Homona coffearia Nietn.
Elasmus hustoni Ferriere, 1929 Elasmus hustoni Ferriere, 1929: 412, ♀. Lectotype ♀: Sri lanka, Pelmadulla (BMNH). Austelasmus hustoni (Ferriere): Reick, 1967: 148. Distribution: Kerala, Karnataka. Host: Bagworm (Psyche albipes Moore).
Elasmus hyblaeae Ferriere, 1929 Elasmus hyblaeae Ferriere, 1929: 414, ♀. Type ♀, India, Arvallica, Nilambur (BMNH). Elasmus nigricus Hussain and Kudeshia, 1984: 365, ♀. Holotype ♀: India, Aligarh (Type lost). Synonymy by Narendran et. al., 2008: 13. Distribution: Kerala, Tamil Nadu, West Bengal, Madhya Pradesh, Meghalaya, Assam, Odisha, Uttar Pradesh, Andhra Pradesh, Uttarakhand. Host: Hyblaea puera; Noorda moringa.
Elasmus indicoides Mani and Saraswat, 1972 Elasmus indicoides Mani and Saraswat, 1972: 460, ♀. Holotype ♀: India, Annamalai Hills (USNM). Elasmus nigricorpus Hussain and Kudeshia, 1984: 27-28, ♀. Holotype ♀: India, Aligarh (Type lost). Synonymy by Narendran et. al., 2008: 15. Distribution: Kerala, Tamil Nadu. Host: Apanteles sp. on Ricinus communis L.
Elasmus indicus Rhower, 1921 Elasmus indicus Rohwer, 1921: 123-124, ♀. ♂. Holotype ♀: India, Coimbatore (USNM). Distribution: Karnataka, Maharashtra, Tamil Nadu, Uttarakhand, Gujarat. 79 Annotated Checklist of Indian Elasmus Host: Anomalococcus sp.; A. indicus; coccids on Acacia sp. Diaphania (Margaronia) indica; Lamprosema indicate; Eublemma sp. predaceous on A. indicus; probably parasitic on larvae of Eublemma sp.; Sylepta derogate.
Elasmus johnstoni Ferriere,1929 Elasmus johnstoni Ferriere, 1929: 258, ♀, ♂. Type ♀: Sudan, Wad Medani (BMNH). Elasmus valparaicus Mani and Saraswat, 1972: 481, ♀. Holotype ♀: India, Valparai (USNM). Synonymy by Narendran et al., 2008: 12. Distribution: Madhya Pradesh, Maharashtra, Haryana, Jharkhand, Rajasthan, Tamil Nadu, Uttarakhand, Uttar Pradesh, Chhattisgarh, Punjab, West Bengal. Host: Earias insulana; E. cupreoviridis; E. fabia; Hapalia machaeralis; Hyblaea puera; Nephanteryx rhodobasalis; Pectinophora gossypiella; Sylepta derogate. Braconidae: Apanteles impartunus; A. machaeralis; A. malevolus.
Elasmus khandalus Mani and Saraswat, 1972 Elasmus khandalus Mani and Saraswat, 1972: 471-472, ♀. Holotype ♀: India, Khandala (USNM). Distribution: Kerala, Maharashtra, West Bengal, Rajasthan. Host: Unknown.
Elasmus kodaianus Mani and Saraswat, 1972 Elasmus kodaianus Mani and Saraswat, 1972: 472, ♂. Holotype ♂: India, Kodaikanal (USNM). Distribution: Tamil Nadu. Host: Unknown.
Elasmus kollimalaianus Mani and Saraswat, 1972 Elasmus kollimalaianus Mani and Saraswat, 1972: 473-474, ♀. Holotype ♀: India, Kollimalai Hills (USNM). Distribution: Kerala, Tamil Nadu, West Bengal. Host: Unknown.
Elasmus krishnagiriensis Mani and Saraswat, 1972 Elasmus kollimalaianus Mani and Saraswat, 1972: 474-475, ♀. Holotype ♀: India, Mumbai (=Bombay) Krishnagiri (USNM). Distribution: Kerala, Meghalaya. Host: Unknown.
Elasmus longicornis Verma and Hayat, 2002 Elasmus longicornis Verma and Hayat, 2002: 276-277, ♀. Holotype ♀: India, Kerala, Periyar Animal Sanctuary (BMNH). 80 KAZMI, S. I., SHEELA, S. Distribution: Kerala. Host: Unknown.
Elasmus longiventris Verma and Hayat, 2002 Elasmus longiventris Verma and Hayat, 2002: 277-278, ♀. Holotype ♀: India, Kerala, Periyar Animal Sanctuary (BMNH). Distribution: Kerala, West Bengal, Uttar Pradesh. Host: Unknown.
Elasmus lutens Crawford, 1914 Elasmus lutens Crawford, 1914: 461-462, ♀. Holotype ♀: Philippines, Luzon, Manila (USNM). Distribution: Madhya Pradesh. Host: Unknown.
Elasmus mahabalii Mani and Saraswat, 1972 Elasmus mahabalii Mani and Saraswat, 1972: 477, ♀. Holotype ♀: India, Mahabalipuram (USNM). Distribution: Kerala, Karnataka, Maharashtra, Tamil Nadu. Host: Unknown.
Elasmus munnarus Mani and Saraswat, 1972 Elasmus munnarus Mani and Saraswat, 1972: 478-479, ♀. Holotype ♀: India, Munnar (USNM). Distribution: Kerala, Tamil Nadu. Host: Unknown.
Elasmus neoflavescens Narendran, 2008 Elasmus neoflavescens Narendran, 2008: 7-8, ♀. Holotype ♀: India, Kerala, Thiruvananthapuram (ZSIC). Distribution: Kerala. Host: Unknown.
Elasmus neoflavocorpusNarendran and Hema, 2008 Elasmus neoflavocorpus Narendran, 2008: 9, ♀. Holotype ♀: India, Kerala, Alappuzha, (ZSIC). Distribution: Kerala, Chhattisgarh, Odisha, Uttar Pradesh. Host: Unknown. Elasmus neopunctulatus Narendran, 2008 Elasmus neopunctulatus Narendran, 2008: 11, ♀. Holotype ♀: India, Kerala, Palghat (ZSIC). 81 Annotated Checklist of Indian Elasmus Distribution: Kerala. Host: Unknown. Elasmus nephantidis Rohwer, 1921 Elasmus nephantidis Rohwer, 1921: 123, ♀. Holotype ♀: India, Coimbatore (USNM). Distribution: Kerala, Tamil Nadu. Host: Opisina arenosella Walker. Elasmus nigritus Verma and Hayat, 2002 Elasmus nigritus Verma and Hayat, 2002: 252-253, ♀. Holotype ♀: India, Tamil Nadu, Coimbatore (BMNH). Distribution: Kerala , Tamil Nadu. Host: Unknown. Elasmus noyesi Verma and Hayat, 2002 Elasmus noyesi Verma and Hayat, 2002: 258-259, ♀. Holotype ♀: India, Karnataka, Mudigere (BMNH). Distribution: Kerala, Karnataka, Uttar Pradesh. Host: Unknown. Elasmus nuperus Narendran, 2008 Elasmus nuperus Narendran, 2008: 5-6, ♀. Holotype ♀: India, Kerala, Calicut (ZSIC). Distribution: Kerala. Host: Unknown. Elasmus philippinensis Ashmead, 1904 Elasmus philippinensis Ashmead, 1904: 138, ♀. ♂. Holotype ♀: Philippine, Manila (USNM). Distribution: Madhya Pradesh. Host: Sylepta derogata Fab.
Elasmus pletyedrae Ferriere, 1935 Elasmus pletyedrae Ferriere, 1935: 368-370, ♂. ♀. Type ♀: Egypt, Giza (BMNH). Elasmus elongates Ferriere, 1947: 579- 580, M. ♂. Type ♀: France (BMNH). Synonymy by Graham, 1995: 14. Distribution: Maharashtra. Host: Pectinophora gossypiella 82 KAZMI, S. I., SHEELA, S. Elasmus polistis Burk, 1971 Elasmus polistis Burk, 1971: 195-196, ♀. ♂. Holotype ♀: Georgia, Madison Co. (USNM). Distribution: Punjab. Host: Polistes annularis (L.) Elasmus pulchellus Verma and Hayat, 2002 Elasmus pulchellus Verma and Hayat, 2002: 274-275, ♀. Holotype ♀: India, Uttar Pradesh, Aligarh (BMNH). Distribution: Kerala, Karnataka, Uttar Pradesh. Host: Unknown. Elasmus punctulatus Verma and Hayat, 2002 Elasmus punctulatus Verma and Hayat, 2002: 267-268, ♀. Holotype ♀: India, Tamil Nadu, Muthumalai (BMNH). Distribution: Kerala, Karnataka, Maharashtra, Tamil Nadu. Host: Unknown. Elasmus punensis Mani and Saraswat, 1972 Elasmus punensis Mani and Saraswat, 1972: 479, ♀. Holotype ♀: India, Pune, Khandakwasla Sinhagarh Fort (USNM). Elasmus nigricoxa Prakash and Verma, 2012: 12-14, ♀. Holotype ♀: India, Uttar Pradesh, Bareilly (Type deposition ?) Syn. Nov. Distribution: Kerala, Maharashtra, Tamil Nadu, Karnataka, Andhra Pradesh, Uttar Pradesh, Himachal Pradesh, Odisha, Uttarakhand, West Bengal. Host: Unknown. Remarks: The first author several time requested for type material to Ved Prakash but he did not reply. Based on the original description and line diagrams of E. nigricoxa by Prakash and Verma probably a junior synonym of E. punensis Mani and Saraswat. Elasmus queenslandicus Girault, 1913 Elasmus queenslandicus Girault, 1913: 82, ♀. Holotype ♀: Australia, Queensland, Kuranda (QMB) . Synonyms given in Riek 1967: 159. Distribution: Kerala, Karnataka, Tamil Nadu, Odisha, Uttar Pradesh, Uttarakhand, West Bengal, Jharkhand, Delhi, Chhattisgarh, Himachal Pradesh, Maharashtra. Host: Unknown. Elasmus rajasthanicus Verma and Hayat, 2002 Elasmus rajasthanicus Verma and Hayat, 2002: 262-263, ♀. Type ♀: India: Rajasthan, Arnajee (ZSI). Distribution: Kerala, Rajasthan, West Bengal. Host: Unknown. 83 Annotated Checklist of Indian Elasmus Elasmus scutellofurvus Narendran, 2008 Elasmus scutellofurvus Narendran, 2008: 11-12, ♀. Holotype ♀: India, Kerala, Wayanad, Thariyodu (ZSIC). Distribution: Kerala, Assam. Host: Unknown.
Elasmus sigillatus Narendran, 2008 Elasmus sigillatus Narendran, 2008: 10-11, ♀. Holotype ♀: India, Kerala, Malappuram, Calicut Univ. campus (ZSIC). Distribution: Kerala. Host: Unknown.
Elasmus syleptae Ferriere, 1929 Elasmus syleptae Ferriere, 1929: 420, ♀. Holotype ♀: Africa, Nyasiland, Namiwara (BMNH). Distribution: Kerala. Host: Sylepta derogata Fab.
Elasmus viridiscutellatus Verma and Hayat, 2002 Elasmus viridiscutellatus Verma and Hayat, 2002: 270-271, ♀. Holotype ♀: India, Maharashtra, Elephanta, Caves of Mumbai (BMNH). Distribution: Andhra Pradesh, Bihar, Maharashtra, Tamil Nadu, West Bengal, Punjab, Assam, Odisha, Uttar Pradesh, Rajasthan. Host: Cnaphalocrosis medinalis, larvae.
Elasmus zehntneri Ferriere, 1929 Elasmus sp. Zehntner, 1900: 1 (by Ferriere, 1929). Elasmus zehntneri Ferriere, 1929: 417, ♀, ♂. Type ♀: Indonesia, West Java (BMNH). Elasmus mahabaleswarensis Mani and Saraswat, 1972: 475-476, ♀. Holotype ♀: India, Mahabaleswar (USNM). Synonymy by Narendran et al., 2008: 13. Distribution: Kerala, Andhra Pradesh, Bihar, Delhi, Punjab, West Bengal, Karnataka, Tamil Nadu, Maharashtra. Host: Bissetia steniella; Chilo infuscatellus; Pectinophora gossypiella; Scirpophaga sp. S. auriflue; Tryporyza monostigma; T. novella; T. rhodoproctalis.
Elasmus zotonus Narendran and Sheeba, 2008 Elasmus zotonusNarendran and Sheeba, 2008: 5, ♀. Holotype ♀: India, Kerala, Kasaragod, CPCRI (ZSIC) Distribution: Kerala. Host: Unknown. 84 KAZMI, S. I., SHEELA, S. DISCUSSION Out of 58 described Indian species of genus Elasmus Westwood three species namely E. cyanomontanus Mani and Saraswat, E. dalhousieanus Mani and Saraswat and E. deccanus Mani and Saraswat are based on males while another three species E. philippinensis Ashmead, E. pletyedrae Ferriere and E. polistis Burk are placed under ‘species Insertae Sedis’ because of lacking real identity (Mani and Saraswat,1972; Narendran et al, 2008). Based on the original description and line diagrams Elasmus nigricoxa Prakash and Verma is probably a junior synonym of Elasmus punensis Mani and Saraswat.
ACKNOWLEDGEMENTS We are grateful to Dr. Kailash Chandra, Director, Zoological Survey of India, Kolkata, for providing facilities. We are also grateful to Dr. K.C. Gopi, Additional Director and Officer-in-Charge of Entomology Division (A), Zoological Survey of India, Kolkata for his useful suggestions. We wish to acknowledge the constructive comments of two anonymous reviewers which helped to improve our manuscript.
REFERENCES
Ferriere, C., 1929, The Asiatic and African species of Elasmus Westwood (Hymenoptera: Chalcidoidea). Bulletin of Entomological Research, 20: 411-423. Gauthier, N., La Salle, J., Quicke, D. L. J., Godfray, H. C. J., 2000, Phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with a reclassification of Eulophinae and the recognition that Elasmidae are derived eulophids. Systematic Entomology, 25: 521-539. Girish Kumar, P., Kazmi, S. I., 2012, Eulophidae and Eupelmidae (Insecta: Hymenoptera: Chalcidoidea) of Indian Thar Desert. In: J. C. Grunwaldt et. al. (Eds.), Deserts Fauna, Flora an Environment. Nova Science Publishers, Inc. New York, U.S.A. 155-164. Graham, M. W. R. de V., 1995, European Elasmus (Hymenoptera: Chalcidoidea, Elasmidae) with a key and descriptions of five new species. Entomologist’s Monthly Magazine, 131: 1-23. Kazmi, S. I., Girish Kumar, P., 2013, The species of Elasmus Westwood (Hymenoptera: Eulophidae: Eulophinae) from West Bengal, India. Prommalia, 1: 79-92. Kazmi, S. I., Girish Kumar, P., 2015, Elasmus Westwood (Hymenoptera: Chalcidoidea: Eulophidae: Eulophinae: Elasmini) of Maharashtra, India. Munis Entomology and Zoology, 10(2): 460-467. Kazmi, S. I., Sheela, S., 2017, Record of Elasmus Westwood (Hymenoptera: Chalcidoidea: Eulophidae: Eulophinae: Elasmini) of Punjab, India. Munis Entomology and Zoology, 12(1): 280-284. Kazmi, S. I., Sheela, S., Girish Kumar, P., 2008, The Species of Elasmus Westwood (Hymenoptera: Eulophidae: Eulophinae) from Uttar Pradesh, India. Columban Journal of Life Science, 9 (1, 2): 124-129. Khan, F. R., Hayat, M., 2011, Record of some species of Elasmus from India (Hymenoptera: Chalcidoidea: Eulophidae). Bionotes, 13(1): 7-10. Mani, M. S., 1989, Elasmidae. In: Director, Zoological Survey of India (Eds.). Fauna of India. Chalcidoidea Part II: Zoological Survey of India, Government of India: 1158-1205. Mani, M. S., Saraswat, G. G., 1972, On some Elasmus (Hymenoptera: Chalcidoidea) from India. Oriental Insects, 6: 459-506. 85 Annotated Checklist of Indian Elasmus
Narendran, T. C., Sheeba, M., Kulkarni, H., 2008, A review on the taxonomy of the Indian species of Elasmus Westwood (Hymenoptera: Chalcidoidea: Eulophidae: Eulophinae: Elasmini). Biospectra, 3(1): 1-25. Noyes, J. S., 2016, Universal chalcidoidea database. http://www.nhm.ac.uk/research-curation/projects/ chalcidoids/Accessed: 14.09.2016. Prakash, V., Verma, M., 2012, Description on a new species of Elasmus Westwood (Hymenoptera: Chalcidoidea) with notes on host-parasitic relationship of some Indian species. International Multidisciplinary Research Journal, 2(11): 12-14. Riek, E. F., 1967, Australian Hymenoptera Chalcidoidea, family Eulophidae, subfamily Elasminae. Australian Journal of Zoology, 15: 146-199. Verma, M. Hayat, M., 1985, Family Elasmidae, In: B. R. Subba Rao and M. Hayat (Eds),The Chalcidoidea (Insecta: Hymenoptera) of India and the adjacent countries. Part I. Oriental Insects, 19: 233-234. Verma, M., Hayat, M., 1986, Family Elasmidae. In: B. R. Subba Rao and M. Hayat (Eds),The Chalcidoidea (Insecta: Hymenoptera) of India and the adjacent countries. Part 2. Oriental Insects, 20: 173-178. Verma, M., Hayat, M., Kazmi, S. I., 2002, The species of Elasmus from India (Hymenoptera: Chalcidoidea: Eulophidae). Oriental Insects, 36: 245-306.
Received: November 01, 2016 Accepted: November 13, 2017
J. Entomol. Res. Soc., 20(1): 87-93, 2018 ISSN:1302-0250
Species-Specific Effect of Parasitization of Ectoparasitoid, Bracon hebetor (Hymenoptera: Braconidae) on the Larval Haemocyte Counts of Corcyra cephalonica and Ephestia kuehniella (Lepidoptera: Pyralidae)
Muhammad S. KHALIL1,2 Abu Bakar M. RAZA1 Muhammad Z. MAJEED1,* Muhammad AFZAL1 Muhammad A. AQUEEL1 Inès PONS-GUILLOUARD2 Huma KHALIL1,2 Thierry HANCE2
1Department of Entomology, College of Agriculture, University of Sargodha, Sargodha, PAKISTAN 2Earth and Life Institute, Biodiversity Research Centre UCL, Louvain-la-Neuve, BELGIUM e-mails: [email protected], [email protected], [email protected]*, [email protected], [email protected], [email protected], hmkhalil25@ gmail.com, [email protected]
ABSTRACT Many studies have described post-parasitization physiological changes in insect hosts for koinobiont endoparasitoids. However, not much is known regarding idiobiont ectoparasitoids that how these parasitoids affect their target hosts’ physiology. The present study aimed to determine the effectof parasitization by Bracon hebetor (Hymenoptera: Braconidae), an efficient idiobiont ectoparasitoid of many lepidopterous larvae, on the total haemocyte counts (THCs) of 5th instar larvae of Corcyra cephalonica and Ephestia kuehniella, two important stored product pyralid pests. Results showed that B. hebetor parasitization differentially affected THCs in parasitized E. kuehniella and C. cephalonica larvae. In E. kuehniella larvae, THCs steadily increased till 12th hour observation after a sharp decline in the very first hour of parasitization and then started decreasing from 24th hour post-parasitization. Highest THCs value (2800 ± 300 cells mL-1) was observed at 6th day of parasitization. While on the contrary, C. cephalonica THCs exhibited a boost in first 6 hours of post-parasitization with maximum THCs value (3413 ± 139 cells mL-1) at 6th hour, but then gradually decreased till the end of experiment on 9th day. Average THCs in fresh unparasitized larvae of E. kuehniella and C. cephalonica were 2078 ± 137 and 1474 ± 47 cells mL-1, respectively. These findings indicate that parasitization by idiobiont parasitoids may alter the haemocyte profiles of their hosts and these responses are species-specific. However, future studies on the interaction of post-parasitization changes in haemocyte profiles and immunity mechanisms of host larvae would help in better comprehension of the effects of ectoparasitoids parasitization on their host physiology. Key words: Bracon hebetor, Corcyra cephalonica, ectoparasitoids, Ephestia kuehniella, parasitization, total haemocyte counts.
INTRODUCTION Pyralid moths (Lepidoptera; Pyralidae) are destructive insect pests of stored food products worldwide (Madrid and Sinha, 1982; Cox and Bell, 1991; Ghimire and Phillips, 2014). Their larvae cause substantial losses through feeding and by favoring 88 KHALIL, M. S., RAZA, A. B. M., MAJEED, M. Z. et. al. mold and other pathogenic development on grains. Among these moths, Ephestia kuehniella (Mediterranean flour moth) and Corcyra cephalonica (rice moth) are the most damaging pests of stored products especially in the milled products (Ghimire and Phillips, 2014). Nevertheless, these pyralid moths are being used as well in different biological control and research programs focusing on various insect predator and parasitoid studies (Vieira et al., 1992; Rahman et al., 2004). Bracon hebetor (Hymenoptera; Braconidae) is an important idiobiont ectoparasitoid that has the ability to parasitize many lepidopterous larvae particularly of above mention pyralid moths (Brower et al., 1996; Yu et al., 2003). This species has been widely used in various host-parasitoid interaction studies because of wide range of host species they attack, their short generation time and high reproductive potential (Gündüz and Gulel, 2005). Female B. hebetor firstly stings and paralyzes its host larvae, usually within 15 minutes of venom injection and then lays eggs singly or in clusters on or near the body surface of paralyzed host. The paralysis is eventually lethal, however, paralyzed larvae without parasitization may live up to a month and consumed by wasp larvae (Altuntaş et al., 2010). The venom blocks neuromuscular transmission at a presynaptic site and apparently has no effect on haemolymph circulation or midgut functioning (Eliopoulos and Stathas, 2008; Altuntaş et al., 2010). Species-specific interactions that occur in the host-parasitoid systems result in diverse effects of parasitization on the total haemocyte counts (THCs) of hosts. Haemocytes play an important role in insect immunity and defense mechanisms (Strand, 2008; Kacsoh and Schlenke, 2012). Parasitoid associated factors and parasitization usually induce changes in haemocytes morphology and physiology and variations in total and differential haemocyte counts (Stettler et al., 1998; Er et al., 2011). Many studies have described post-parasitization physiological changes in insect hosts for koinobiont endoparasitoids (Pennacchio and Strand, 2006; Yu et al., 2007; Nishikawa et al., 2013; Teng et al., 2016). However, there is a lack of knowledge regarding the effect of idiobiont ectoparasitoids that how these parasitoids alter their target hosts’ physiology, particularly haemolymph dynamics. In this study, therefore, we compared the effect of B. hebetor parasitization on the haemocyte profiles (total haemocyte counts) in the haemolymph of parasitized and unparasitized larvae of C. cephalonica and E. kuehniella. We hypothesized a suppression of haemocytes in both larval hosts by idiobiont ectoparasitoid B. hebetor parasitization as observed in case of koinobiont endoparasitoids (Yu et al., 2007). The results provide better understanding of the interactions between parasitism and bio-resources potentially available for the nutrition and larval development of idiobiont parasitic wasps within their parasitized hosts.
MATERIALS AND METHODS
Insect collection and rearing Larvae of host pyralids, Corcyra cephalonica and Ephestia kuehniella (Lepidoptera: Pyralidae) were procured from the laboratory of Earth and Life Institute, Biodiversity 89 Species-Specific Effect of Parasitization of Ectoparasitoid, Bracon hebetor Research Center, Université Catholique de Louvain, Louvain-la-Neuve, Belgium. These host larvae were reared on rice and wheat flour diets separately in plastic boxes under controlled laboratory conditions (26 ± 1ºC, 25-35% relative humidity, 16:8 hours light and dark photoperiod). Adults of idiobiont ectoparasitoid Bracon hebetor (Hymenoptera: Braconidae) were collected from the field and were reared under similar controlled laboratory conditions as mentioned above on the larvae of both lepidopterous hosts separately in plastic vials (7 cm H and 3.5 cm Ø) provided with 50% sugar solution diets as well. In order to get synchronized progeny of parasitoids, five full grown larvae of each lepidopterous host species were exposed to 24 hours old mated female wasps for parasitism on daily basis. After parasitization, the parasitized larvae were removed and confined in a petri dish for adult parasitoids emergence. Similarly, both pyralid moths were reared for many generations in order to obtain synchronized progeny to be used in experimentation. All the equipment, materials and solutions used during the study were sterilized.
Parasitization and total haemocyte counts Experimental protocol regarding the parasitization of host larvae by parasitoid wasps and post-parasitization haemocyte counts of host larvae involved the exposure of a set of five th5 instar larvae of each host species (C. cephalonica and E. kuehniella) to 24 hours old mated female of B. hebetor confined within sterilized plastic vials, separately. After parasitization, parasitized host larvae were removed and placed in separate petri dishes (five larvae per petri dish). Three independent petri dish sets were maintained for each lepidopterous host species and for each of different post-parasitization sampling periods viz; 1 hour, 6 hours, 12 hours, 24 hours, 3 days, 6 days and 9 days. Prior to the collection of haemolymph, parasitized larva was surface sterilized with 75% ethanol (v/v) and air-dried on paraffin film. The haemolymph was squeezed out from each of the five larvae of each treatment by cutting larval proleg with sterilized fine-tipped forceps and was pooled in a 200 µL sterilized Eppendorf tube and this pooled sample was considered as one replicate for each treatment. Unparasitized larvae were inactivated by putting on ice for few seconds and were then subjected to haemolymph collection in the same way as explained above for parasitized larvae. Total haemocyte counts (THCs) were determined by transferring 5 µL of pooled haemolymph samples in 5 µL phosphate buffered saline solution (PBS) and then this 10 µL of diluted haemolymph sample was transferred to Neubauer hemocytometer (VWR Scientifics, West Chester, PA) and counting was made under the phase contrast stereomicroscope (LEICA DMC-4500; Leica Microsystems, Bannockburn, IL). Under the microscope, a total of 10 cells of Neubauer hemocytometer were observed on random basis for the counting of haemocytes. Measurements were made for three independent replicates for each sampling period.
Statistical analysis The effect of ectoparasitoidB. hebetor parasitization on the haemocyte counts of their host C. cephalonica and E. kuehniella larvae was compared using total haemocyte counts (THCs) values as dependent variable. For both host species, the difference 90 KHALIL, M. S., RAZA, A. B. M., MAJEED, M. Z. et. al. between THCs of unparasitized (control) and parasitized individuals at 1 hour to 9 days post-parasitization were analyzed using repeated measures general linear ANOVA models (GLM) with LSD post-hoc test at significance level of 0.05 after validation of the normal distribution. Statistical analyses were performed using software R v.3.0.2 (R development Core Team 2014).
RESULTS B. hebetor parasitism played a significant role in increasing or decreasing total haemocyte counts (THCs) in parasitized E. kuehniella and C. cephalonica larvae throughout the time period of experiment. Initially, there was a steep decline in the THCs in E. kuehniella larvae observed at 1st hour post-parasitization (1113 ± 112cells/ mL) as compared to the control (unparasitized) larval THCs (2100 ± 114cells/mL) (Fig. 1). Later on, THCs increased steadily up to 12 hours post-parasitization (1113 ± 112 to 2040 ± 271 cells/mL), and then started decreasing at 24th hours post-parasitization (1513 ± 138 cells/mL). Highest THCs was observed at 6th day of parasitism with 2800 ± 300 cells/mL. THCs in unparasitized control larvae ranged from 1981 to 2175 cells mL-1 for E. kuehniella.
Ephestia kuehniella 4000
/ml) ** 3000 cells
Control 2000 * * ** *** 1000 Total hemocyte hemocyte countTotal ( 0 1h 6h 12h 24h Day3 Day6 Day9 Time post-parasitism
Fig. 1. Effect of parasitization by Bracon hebetor on total haemocyte counts (THCs) of 5th instar larvae of Ephestia kuehniella. Bars represent mean values of THCs ± standard errors (n = 15). Dotted red lines show THCs variation in control (unparasitized) larvae. Asterisk symbols ‘***’, ‘**’ and ‘*’ show signifi- cance between parasitized and unparasitized larvae at P < 0.001, P < 0.01 and P < 0.05, respectively. Similarly, B. hebetor parasitization induced significant variations in the THCs ofC. cephalonica (Fig. 2). As a result of B. hebetor venom injection, there was a significant increase in the THCs of parasitized larvae of C. cephalonica after 1st hour of larval parasitization (2220 ± 42 cells/mL) in comparison with the freshly extracted haemolymph of control larvae (1440 ± 99 cells/mL). These haemocyte numbers gradually increased up to 6th hour observation with highest and significant THCs values observed at 6th hour (3413 ± 139 cells/mL). THCs then gradually decreased along with the time reaching its significant lowest THCs values at day 9 (860± 111 cells/mL). The average THCs value in unparasitized control larvae of C. cephalonica was 1473 ± 47 cells mL-1 (Fig. 2). 91 Species-Specific Effect of Parasitization of Ectoparasitoid, Bracon hebetor
Corcyra cephalonica
4000 *** /ml) cells 3000 ** count ( 2000 Control
hemocyte * *** 1000 Total Total 0 1h 6h 12h 24h Day3 Day6 Day9 Time post-parasitism
Fig. 2. Effect of parasitization by Bracon hebetor on total haemocyte counts (THCs) of 5th instar larvae of Corcyra cephalonica. Bars represent mean values of THCs ± standard errors (n = 15). Dotted red lines show THCs variation in control (unparasitized) larvae. Asterisk symbols ‘***’, ‘**’ and ‘*’ show significance between parasitized and unparasitized larvae at P < 0.001, P < 0.01 and P < 0.05, re- spectively.
DISCUSSION Results of the study showed that B. hebetor parasitization had a differential effect on the larval THCs of both host species. In the first few hours post-parasitization, a sudden suppression and then gradual increase in haemocyte counts were observed in E. kuehniella; while on the contrary, parasitization in C. cephalonica larvae exhibited a stimulation in THCs in the initial hours of observations indicating a boost in the production of haemocytes within C. cephalonica larvae in response to parasitization by B. hebetor. Parasitization may induce species-specific effects on the host physiology including haemolymph kinetics as demonstrated by Stettler et al. (1998). In our study, the haemocyte profiles varied significantly throughout the time period of experiment in larvae of both lepidopterous species (C. cephalonica and E. kuehniella) in response to parasitization by an ectoparasitoid B. hebetor. In E. kuehniella, higher haemocyte counts were observed in the late stages of parasitization as compared to earlier ones. Similar post-parasitization haemocyte profile patterns have been observed in case of endoparasitoid Cotesia chilonis by Teng et al. (2016) where haemocyte counts in Chilo suppressalis showed a boost from 72 hours post-parasitization till 9th day of experiment. Some other studies also observed a post-parasitization increase in total haemocyte counts in various insect pest species parasitized by endoparasitoid wasps such as in Malacosoma disstria parasitization by Hyposoter fugitivus (Stoltz and Guzo, 1986) and in Pseudoplusia includens parasitization by Microplitis demolitor (Strand and Noda, 1991). Although parasitization by ectoparasitoids have been shown causing perturbations and suppression of many physiological and developmental aspects of host lepidopterous larvae including haemolymph enzymatic activities (Weaver et al., 1997; Mosson et al., 2000; Richards and Edwards, 2000), but there is a paucity of knowledge regarding their effect on host haemolymph profiles. Nonetheless, one study 92 KHALIL, M. S., RAZA, A. B. M., MAJEED, M. Z. et. al. by Richards and Edwards (2000) has demonstrated both quantitative and qualitative changes in haemolymph proteins and haemocytes by ectoparasitoid parasitization and these findings are in line with our findings. However, sometimes host parasitization by parasitoids results in considerable THCs suppression. In our study, for instance, the parasitism by same parasitoid species resulted into a gradual decrease in THCs in parasitized C. cephalonica larvae. These results are in agreement with those of many previous works done on endoparasitoids (Doucet and Cusson, 1996; Yu et al., 2007; Nishikawa et al., 2013) and ectoparasitoids (Richards and Edwards, 2000; Yu et al., 2003). This THCs reduction would most probably be due to the stimulation of immune-suppression mechanisms (Stettler et al., 1998) or hematopoietic organ histolysis and circulating haemocytes cell death (Teramoto and Tanaka, 2004; Altuntaş et al., 2010). In brief, present study demonstrated a differential effect of parasitization by an idiobiont ectoparasitoid B. hebetor on the total haemocyte counts of 5th instar larvae of C. cephalonica and E. kuehniella. THCs in C. cephalonica stimulated upon parasitization and then gradually decreased till 9th day of observation, while this pattern was inverse in case of E. kuehniella. However, future focus on the regulation of immunity mechanisms of these lepidopterous larvae by B. hebetor ectoparasitoids would help in better understanding of the post-parasitization changes in haemocyte profiles.
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Received: November 07, 2016 Accepted: January 30, 2018
J. Entomol. Res. Soc., 20(1): 95-112, 2018 ISSN:1302-0250
Ethology of Holopogon snowi Back, 1909 (Diptera: Asilidae) in Northeastern Florida, U.S.A.
D. Steve DENNIS
1105 Myrtle Wood Drive, St. Augustine, Florida 32086-4838, U.S.A. e-mail:[email protected]
ABSTRACT Holopogon snowi Back, 1909 foraged from plant twig tips, capturing prey in flight, and immobilizing them in flight or at the feeding site. Identified prey came from eight orders: Araneae (0.5%), Blattodea (family Termitidae; 9.9%), Coleoptera (0.5%), Diptera (8.8%), Hemiptera (26.4%), Hymenoptera (11.0%), Psocoptera (11.0%), and Thysanoptera (27.5%). Male courtship preceded mating in the tail-to-tail position. Females dropped eggs on the twigs of scrub oak or directly onto the ground. This species demonstrated a distinct daily rhythm of activity for feeding, mating, and ovipositing. Grooming behavior did not occur often but resembled that of other species of Asilidae. Habitat, resting behavior, and predators also are discussed. This is the first record ofH. snowi occurring in Florida. Key words: Asilidae, behavior, robber flies, prey, new Florida record.
INTRODUCTION Twenty-one species of robber flies in the genus Holopogon occur in the United States of America (U.S.A.) (Geller-Grimm, 2016). Despite their wide distribution, different aspects of the ethology of only seven species has been described: H. albipilosus Curran, 1923 (Dennis and Lavigne, 1975) and H. seniculus Loew, 1866 (Lavigne et al., 1993) in Wyoming; H. caesariatus Martin, 1959 in Idaho and Oregon (Martin, 1959); H. currani Martin, 1959 in Arizona (Martin, 1959); H. phaeonotus Loew, 1874 in Florida (Dennis, 2014); H. stellatus Martin, 1959 in California (Martin, 1959); and H. wilcoxi Martin, 1959 in Arizona (Hespenheide and Rubke, 1977). This paper provides detailed information on the ethology of H. snowi Back, 1909 in the Moses Creek Conservation Area (MCCA), near the southern boundary of St. Augustine in northeastern Florida.
MATERIALS AND METHODS The author studied a population of H. snowi from 24 March through 5 May 2016 on both sides of a sand road that follows an electrical transmission line corridor. During this period, two to 59 (mean of 16) asilids were observed during a day, each for up to 90 minutes. Total number of hours of observation was approximately 103. The 96 DENNIS, D. S identification ofH. snowi was confirmed using the key in Martin (1959) and description in Back (1909). Male and female specimens will be deposited in the Smithsonian Institution, National Museum of Natural History, Washington, D.C. Observations began with the author standing, kneeling, or sitting on the ground and observing one or more flies until they were lost from sight in order to collect information on their various behaviors and diurnal activities. When sufficient data were gathered on an individual’s behaviors, the author walked along the edges of the road to observe the activities of many flies. These actions also allowed for the collection of prey and the observation of mating pairs and ovipositing females. Some behaviors, such as prey manipulation and oviposition, were confirmed by observing them with Pentax Papilio 8.5x21 binoculars. Collected prey was placed in glass vials with the following information: sex of predator (if observed), date, time, and location. The author then identified the prey in the office using primarily prey that had been previously identified for H. phaeonotus (Dennis, 2014) by Research Entomologists at the U.S. Department of Agriculture, Agricultural Research Service, Systematic Entomology Laboratory, Beltsville, Maryland U.S.A. Some H. phaeonotus and H. snowi prey, was not identifiable to family, genus, or species because of the unavailability of specialists, inadequate keys, or poor condition of the specimens. In the office, prey length was determined by measuring each prey to the nearest 0.5 mm with a clear, plastic ruler. Temperature and wind are important environmental variables that determine the activities in which adult robber flies engage. A hand held Taylor thermometer and a Cooper-Atkins DPP400W Digital Thermometer were used to take air temperatures and a Dwyer Hand-Held Wind Meter was used to measure wind speed.
RESULTS AND DISCUSSION
Morphology and distribution Like other Holopogon, H. snowi is a small (approximately 6-8.5 mm in length, excluding antennae) blackish species with white setae on the body. Back (1909) described the tibiae and tarsi as dark reddish. In the population studied in the MCCA, the fore- and mid-tibiae are light reddish brown to dark reddish, and at least the proximal 1/4-1/2 of the hind tibiae has similar coloration. The fore- and mid-tarsi are also light reddish brown as are at least the ventral part of the hind tibiae. The dorsal part of the hind tibiae may be black. Depending on the light conditions in the field and the angle of view, H. snowi tibiae and tarsi may look reddish black to black, and the setae may look yellowish to black. Holopogon snowi has historically been reported to occur in Kansas, Oklahoma, and Texas (Back, 1909; Martin, 1959). More recently Williams (1999) observed it in Wisconsin. The observation of this species in Florida is a new record for the state and the first time that it has been reported in eastern U.S.A. 97 Ethology of Holopogon snowi Back, 1909 Habitat The 8.6-14.2 m (mean 11.3 m) wide, 1,129 m long section of the electrical transmission line corridor and associated sparsely vegetated road, passes through a scrub vegetation community where H. snowi occurs (Fig. 1). This community grades into mesic flatwoods and upland mixed forest vegetation communities, and so there is some overlap in the vegetation. An area west of the road was sprayed with herbicide late Summer to Fall 2015 for up to 3.7 m (mean 1.5 m) and is dominated by dead scrub oak (Quercus spp.) with heights up to 2.7 m. The area east of the road was not sprayed and is dominated for a distance up to 3 m with live scrub oak that is up to 3.7 m tall. On either side of these areas taller vegetation grows, in particular sand pine [Pinus clausa (Chapm. ex Engelm.) Vasey ex Sarg.]. The vegetation in the H. snowi habitat is shown in Table 1. Table 1. Vegetation in habitat in which Holopogon snowi was studied in the Moses Creek Conservation Area.
Family/Genus/Species/Common Name Family/Genus/Species/Common Name Annonaceae Fabaceae Asimina sp./Pawpaw Erythrina herbaceae L./Coralbean Aquifoliaceae Galactia sp./Milkpea Ilex opaca Alton/American holly Fagaceae Arecaceae Quercus geminata Small/Sand live oak Serenoa repens (W. Bartram) Small/Saw Quercus spp. /Scrub oaks palmetto Asteraceae Magnoliaceae Balduina angustifolia (Pursh) B. L. Rob./ Magnolia grandflora L./Southern magnolia Coastalplain honeycombhead Eupatorium sp. /Fennel Pinaceae Carphephorus corymbosus (Nutt.) Torr. Pinus clausa (Chapm. ex Engelm.) Vasey ex Sarg./ and A. Gray/Coastalplain chaffhead Sand pine (Florida paintbrush) Liatris tenuifolia Nutt. var. quadriflora Poaceae Chapm./Shortleaf gayfeather Pityopsis graminifolia (Michx.) Nutt./ Andropogon sp./Bluestem Narrowleaf silkgrass Solidago sp./Goldenrod Other grasses Cactaceae Smilaceae Opuntia humifusa (Raf.) Raf./Prickly pear Smilax bona-nox L./Saw greenbrier vine cactus Ericaceae Smilax glauca Walter/Cat greenbrier vine Lyonia ferruginea (Walter) Nutt./Rusty Vitaceae lyonia Lyonia lucida (Lam.) K. Koch/Fetterbush Vitis rotundifolia Michx./Muscadine vine Vaccinium myrsinitas Lam./Shiny blueberry Zamiaceae Euphorbiaceae Zamia integrifolia L./Florida arrowroot (Coontie) Cnidoscolus stimulosus (Michx.) Engelm. & A. Gray/Tread-softly Holopogon snowi occur primarily on the tips of 1-4 mm diameter scrub oak twigs (a small branch without leaves) and up to 7 mm diameter buds. In areas where there are a large number of scrub oak plants close together (within 15-30 cm of each other), flies rest on and forage from the outside of the plants facing open areas of habitat or on top of the plants. 98 DENNIS, D. S
Fig. 1. Holopogon snowi habitat along electrical transmission line corridor. Some individuals also were observed on leaves of scrub oak, twigs of rusty lyonia (Lyonia ferruginea (Walter) Nutt.), 1/2 mm diameter tendrils of saw greenbrier vines (Smilax bona-nox L.), dead sand pine and sand live oak (Quercus geminata Small) branches, and the tips of dead bluestem (Andropogon sp.) grass stems, and shortleaf gayfeather (Liatris tenuifolia Nutt. var. quadriflora Chapm.) stems. Williams (1999) found H. snowi on marbleseed (Onosmodium molle Michx.) plant and commented that some predator arthropod fauna hunted over an entire plant and others (presumably including H. snowi) “…hunted at the shoot tips and about the flowers, where insect activity was usually greatest.” Other species ofHolopogon in the U.S.A. also are known to forage from the tips of twigs and from low weeds or bushes: H. albipilosus (Dennis and Lavigne, 1975); H. caesariatus and H. currani (Martin, 1959); H. guttulus (Wiedeman, 1821) (Back, 1909; Bromley, 1931, 1946, 1950; Goslin, 1950; McAtee and Banks, 1920, all as H. guttula); H. phaeonotus (Dennis, 2014); H. seniculus (Lavigne et al., 1993); H. stellatus (Martin, 1959); and H. wilcoxi (Hespenheide and Rubke, 1977). Several species of Holopogon in the former Union of Soviet Socialist Republics (U.S.S.R.), occur on the tips of high grasses and twig tips of shrubs (Lehr, 1964, 1972). In France, Musso (1972) found H. venustus (Rossi, 1790) on the extreme tips of 2-3 mm diameter twigs.
Resting behavior Holopogon snowi rests on and forages from twig tips (Fig. 2) 15 cm to 2.7 m above the ground, but are most frequently seen at an elevation of at least 30.5 cm. Other species of Holopogon are generally observed at heights from 10 cm to 3 m above the substrate (Dennis, 2014; Dennis and Lavigne, 1975; Hespenheide and Rubke, 1977; Lavigne et al., 1993; Lehr, 1972; Martin, 1959; Musso, 1972). Individuals rest in a horizontal position on the twig tip or below (up to 1.9 cm) the tip with their bodies parallel to the bare branch. When on the branch they would often face away from the tip. Similar resting behavior was observed for H. phaeonotus (Dennis, 2014). The twigs would often vibrate or wave in the wind when the wind gusted in excess of 14.5 km/hr. In these circumstances the flies move to lower elevations on the 99 Ethology of Holopogon snowi Back, 1909 vegetation (e.g., from 1.2 m to 0.3-0.6 m) where the wind blew less (6.4- 9.7 km/hr). Also, they would more often face away from the twig tips, hold themselves closer to the twigs, or move to the sides of the twigs with their heads turned down towards the twigs. When individuals remained on top of the twigs, one or both wings would often blow open when the wind gusted as low as 6.4-9.7 km/hr, in particular when the asilids faced away from the direction of the wind. Holopogon phaeonotus also made postural adjustments on twigs when the wind gusted 11-16 km/hr (Dennis, 2014).
Fig. 2. Holopogon snowi resting and grooming while on scrub oak twig tip. While resting, H. snowi remains motionless for variable periods of time ranging from 1-5 seconds to 5 minutes. During this time they only move the head and body slightly as they watch other insects flying by or the author moving around. One individual rested for 45 minutes, with intermittent periods of motionless and slight movements, before resuming foraging and other activities. Holopogon phaeonotus would rest for up to 7 minutes before resuming other activities, in particular foraging (Dennis, 2014). Lehr (1972) commented on H. claripennis avor Lehr, 1972 turning its head and following a person and “not losing him from sight.” Holopogon snowi, like H. phaeonotus (Dennis, 2014), usually did not turn so that one of its sides faced and was elevated to the sun or flatten themselves against the twig they were on, such as when the sun was obscured by clouds and air temperatures ranged from 24.0-35ºC. (n=21, mean 29.3ºC). Many other species of robber flies including H. priscus (Meigen, 1821) (Lehr, 1972), attempt to maintain their body temperature by changing their position in relation to the sun, flattening themselves against the substrate that they are on, and/or resting on the shady side of vegetation (Dennis, 2016; Dennis and Lavigne, 1975; Lavigne and Holland, 1969). According to Morgan et al. (1985), and Morgan and Shelly (1988), foraging neotropical and desert robber flies regulate their body temperatures by microhabitat selection and postural adjustments. Lehr (1972) commented that each species of Holopogon occupy a habitat with specific microclimate components. Thus, both H. snowi and H. phaeonotus (Dennis, 2014) may primarily use microhabitat selection to regulate their body temperature. 100 DENNIS, D. S When resting and feeding, a few individuals expelled a drop of creamy-white to brownish liquid from their anus. Similar behavior was observed for H. phaeonotus (Dennis, 2014), and Lehr (1958c) commented that the expulsion of liquid from the anal opening is quite common in robber flies.
Foraging and feeding behavior Holopogon snowi forages primarily from scrub oak twig tips. A few individuals infrequently foraged from scrub oak leaves, twigs of rusty lyonia, saw greenbrier vine tendrils, dead sand pine branches on the ground and on a fallen tree, dead sand live oak branches on the ground, tips of dead bluestem grass stems, and shortleaf gayfeather stems. Individuals are active in both sun and shade. Other species of Holopogon have been reported to forage primarily from twig tips (Dennis, 2014; Dennis and Lavigne, 1975; Lehr, 1972; Martin, 1959). Foraging height depends on vegetation height and the location of sunlight on the twigs. Holopogon snowi generally forages higher in the vegetation in the morning. As these areas become shaded, the asilids move to lower areas in sunlight. This is similar behavior to that described for H. phaeonotus (Dennis, 2014). Hespenheide and Rubke (1977) speculated that H. wilcoxi spent the night in areas where they would be in sunlight earliest in the morning and then moved to areas better suited for foraging. Holopogon snowi foraging individuals usually held their bodies at a 30 to 45 degree angle with their heads facing up or down. Foraging H. priscus hold their heads downward and their bodies at an angle to the side of the grass stem that they are on (Lehr, 1972). A few H. snowi foraged from a horizontal position on the twig tip. In these postures and positions they would pivot and make quick movements (generally every 2-3 seconds) of their heads and bodies, often turning 180° to face another direction. Holopogon albipilosus also rapidly faces different directions while remaining on the same twig when foraging (Dennis and Lavigne, 1975), but H. phaeonotus does not (Dennis, 2014). In the morning, once the sun was shining and until about 2:00-3:00 PM, H. snowi in the area on the western side of the road would face primarily south, southeast, and east. Then in the afternoon, because of increased shade on the western side, most flies moved across the road to the area on the eastern side where they would face west towards the sun. During cloudy weather, H. snowi more frequently face other directions in both areas on the western and eastern sides of the road. The directions that H. snowi faces and their foraging postures or attitudes, presumably allows the flies to use backlighting to better see their prey because of their position relative to the prey and the sun. Also the body held at a 45-degree angle allows H. snowi to see potential prey more clearly because the incoming light is at right angles to the surface of the forward, flattened ommatidia. Similar observations have been made for H. phaeonotus and other species of robber flies (Dennis, 2014). According to Nation (2008), robber flies have higher visual acuity near the forward part of their eyes and this probably enhances their ability to see and capture prey. 101 Ethology of Holopogon snowi Back, 1909 A few foraging H. snowi made investigatory flights without making contact with potential prey. Flies made these flights when potential prey were 12.7-17.8 cm below or directly in front of its position, and they also often chased them for up to 30.5 cm. Investigatory flights are common forH. phaeonotus and many species of robber flies (Dennis, 2014). A few H. phaeonotus captured insects and released them while still in flight (Dennis, 2014). Except in one case, H. snowi did not capture insects and release them in flight. Like H. phaeonotus, a number of H. snowi released captured insects after returning to their foraging twig tip and while manipulating the prey with their tarsi prior to insertion of their proboscis. One individual discarded the prey after insertion of its proboscis in flight, landing at its feeding site, and prior to manipulating the prey with its tarsi. This may indicate that H. snowi uses visual and other stimuli to select prey as mentioned by Dennis and Lavigne (1975). Lehr (1958) commented that robber flies often cannot determine whether a flying insect is acceptable prey. Short flights about a foraging position without being directed towards any potential prey are called orientation flights (Dennis and Lavigne, 1975).Holopogon snowi made orientation flights within 5-91 cm of its foraging position, most often in a circle in front of its foraging twig tip. Holopogon snowi would forage from the same twig tip for 30 seconds to 79 minutes with an mean of 28 minutes. During this period of time, an individual could feed on a number of prey and make numerous investigatory and orientation flights. When an individual moved to a new foraging position, it was within 15 cm to 1.2 m of its previous position. Based on 44 prey capture records, H. snowi captured 31 of its prey in the air 2.5-75 cm (mean 21 cm) in front of its foraging position (Table 2). These prey were 2.5-30 cm above (n=16; mean 8.3 cm), at the same level (n=13; mean 24.8 cm), or 2.5-5 cm below (n=2; mean 3.8 cm) the level of the foraging position. Thus, H. snowi captured the largest number of prey in front of and above their foraging position, similar to Holopogon albipilosus that captured most prey 7.5-30 cm in front of and above their foraging position (Dennis and Lavigne, 1975). Holopogon phaeonotus captured its prey in the air within 7.5-45 cm in front of or 5-15 cm to the side or slightly behind their foraging position (Dennis, 2014). Holopogon snowi would forage until wind gusts reached 11.5 km/hr and as long as the twig they perched on was not waving excessively in the wind. Once the gusts reached 14.5-17.7 km/hr and the twig vibrated or waved in the wind, the robber flies stopped foraging, held their bodies closer and parallel to the twig, and often faced the interior of the plant. Also, similar to when they were resting, some flies moved lower down in the vegetation to forage where the wind gusts were not as high. For example, at 1:44 PM on 08.04.2016, at an elevation of 1.2 m above the ground the wind gusted to 16.1 km/hr and the flies moved to an elevation of 0.6 m (61 cm) where the wind was 6.4 km/hr. One asilid was blown off a waving twig during a sudden gust of 19.3-22.5 km/hr. 102 DENNIS, D. S
Table 2. Location, number, and distance of prey captured in relation to foraging level of Holopogon snowi.
Horizontal Vertical Distance Number Prey Location Distance (cm) Above/Below (cm) of Prey (Average cm) (Average cm) In Front of H. snowi 2.5–75 At Same Foraging Level 13 N/A1 (24.8) 2.5–45 2.5–30 Above Foraging Level 16 (19.2) (8.3) 2.5–15 2.5–5 Below Foraging Level 2 (8.8) (3.8) To Left of H. snowi 5–25 At Same Foraging Level 4 N/A (15.6) 17.5–20 5 Above Foraging Level 2 (18.8) (5) To Right of H. snowi 30–45 At Same Foraging Level 2 N/A (37.5) 12.5–20 5 Above Foraging Level 3 (15.8) (5) Behind H. snowi 20 At Same Foraging Level 1 N/A (N/A) Straight Above H. snowi 10 Above Foraging Level 1 N/A (N/A)
1 N/A = not applicable. When it captured prey, H. snowi would most often return to its foraging twig tip and hold onto the twig tip with one of its mid-tarsi. However, one individual held onto the twig tip with its right fore tarsi during prey manipulation and a few individuals that had inserted their proboscis in flight, landed on the twig tip in normal resting posture without holding on with one of their mid-tarsi. If the robber fly had not inserted its proboscis in the prey before landing, it would insert it while holding the prey with the tarsi not used to hold onto the twig tip. Also, some individuals still held onto prey with the tarsi when the proboscis had been inserted in flight, possibly to prevent the prey’s movement from dislodging from the fly’s proboscis. Holopogon phaeonotus either inserted its proboscis in flight or at the feeding site while holding onto prey with tarsi not used to hold onto a twig (Dennis, 2014). Most prey of H. albipilosus were immobilized at the feeding site while the asilid held onto a twig with one of its mid-tarsi and held the prey with the rest of its tarsi; only a few flies immobilized prey in the air prior to landing to feed (Dennis and Lavigne, 1975). Holopogon snowi would manipulate prey one to nine (n=42; mean four) times during feeding. When it manipulated prey, an asilid would hold onto the side of a twig tip with one of its mid-tarsi (Fig. 3) and manipulate the prey with the other tarsi. Then it would re-insert its proboscis and stand up on the twig tip to resume feeding. During prey manipulation, both H. phaeonotus (Dennis, 2014) and H. albipilosus (Dennis and Lavigne, 1975) held onto the twig tips with either their fore- or mid-tarsi. 103 Ethology of Holopogon snowi Back, 1909 In general, the number of times the flies manipulated prey depended upon the length (not including folded wings) and shape of the prey and the amount of time spent feeding. H. snowi fed on small prey (0.5 mm) such as thrips (Thysanoptera), for 1-5 minutes and did not manipulate them. They fed on larger prey (3-3.5 mm; Hemiptera: Cixiidae, Cixius sp.), for 9 1/2-13 1/2 minutes and either did not manipulate or manipulated them 1-2 times. Holopogon snowi fed on slightly larger prey with a narrower shape [3.5-4 mm; alate Blattodea (formerly Isoptera): Kalotermitidae, Calcaritermes nearcticus Snyder, 1933 and Rhinotermitidae, Reticulitermes virginicus (Banks, 1907)] for 8 1/2-20 minutes and manipulated them 2-9 times.
Fig. 3. Holopogon snowi manipulating prey holding onto scrub oak twig tip. While H. snowi fed, prey hung free on their proboscises without support by the tarsi. Similar behavior was observed for H. phaeonotus (Dennis, 2014). Female H. snowi fed on prey that averaged slightly longer than those fed upon by males. The mean prey length for females was 2.3 mm (n = 67) with a range from 0.5-5.0 mm; whereas, for males it was 1.9 mm (n = 32) with a range from 0.5 -4.0 mm. Overall mean prey length was 2.1 mm. Both female and male Holopogon phaeonotus fed on longer prey than H. snowi with a range from 1.0-7.0 mm (Dennis, 2014). Female and male H. albipilosus and H. seniculus fed on slightly smaller prey with prey length ranging from 1.6-1.9 mm (Dennis and Lavigne, 1975; Lavigne et al., 1993). Mean predator to prey ratios show the relationship between predator to prey lengths, with a smaller ratio indicating larger prey. Based on the mean prey length and the mean length of 10 male and female H. snowi each, the mean predator to prey ratio is 3.3:1.0. This indicates that H. snowi is over three times the length of its prey. Mean predator to prey ratios for H. albipilosus (Dennis and Lavigne, 1975), H. phaeonotus (Dennis, 2014), and H. seniculus (Lavigne et al., 1993) are 3.5:1.0, 2.6:1.0, and 3.1:1.0, respectively. For H. wilcoxi, the overall range of prey sizes varied from 1/10 to 1/2 the length of the fly (Hespenheide and Rubke, 1977). At the completion of feeding, H. snowi individuals discarded most prey (46 out of 79 observations) by pushing them off the proboscis with the fore tarsi while still at the feeding site. The second most common method of prey disposal was dropping prey in flight as the asilid left the feeding site (n=16), followed by allowing prey to drop off the 104 DENNIS, D. S proboscis at the feeding site (n=9), and dropping during feeding while manipulating prey (n=8). The most common methods for H. phaeonotus (Dennis, 2014) and H. seniculus (Lavigne et al., 1993) to discard prey was to push it off their proboscis while still at the feeding site and to drop prey during feeding while manipulating them. Holopogon albipilosus pushed prey off its proboscis with the fore tarsi while still at the feeding site (Dennis and Lavigne, 1975). The length of time H. snowi spent feeding on individual prey varied from 1-20 minutes (n=35), with an mean of 4.7 minutes. Time between feedings (interfeeding time) varied between 0-55 minutes (n=16), with an mean of 8.8 minutes. There were two - zero minute interfeeding times where individuals dropped prey at the feeding site or in flight after leaving the feeding site and immediately captured another prey. The theoretical number of prey an individual H. snowi could feed on in one day can be calculated if it is assumed that, (1) it continually forages and feeds between 11:00 AM and 6:00 PM (the observed major period of foraging and feeding activity for 97.6% of the feedings), and (2) it captures and feeds on prey every 13.5 minutes (based on the mean feeding and interfeeding times). Thus, over a seven-hour period an individual could feed on approximately 31 prey. It was calculated that H. phaeonotus (Dennis, 2014) and H. albipilosus (Dennis and Lavigne, 1975) could feed on approximately 33 and 15 prey per day during 6 and 5.5-hour periods of foraging activity with mean 11 and 21 minute feeding and interfeeding times, respectively. This is in comparison to H. claripennis avor that Lehr (1964) calculated could feed on approximately 14 prey per day. Other investigators have estimated that asilids feed on 1 to 35 prey per day, as reported by Dennis (2014) and Lehr (1964).
Prey Holopogon snowi individuals preyed primarily on Thysanoptera (27.5%) and Hemiptera (26.4%), followed by Hymenoptera (11.0%) and Psocoptera (11.0%), Blattodea (Isoptera alates, 9.9%), Diptera (8.8%), Araneae (0.5%), and Coleoptera (0.5%) (Table 3). In the U.S.A. other species of Holopogon have been reported to prey on insects representing similar orders including: Coleoptera, Diptera, Hemiptera (as Hemiptera and Homoptera), Hymenoptera, Lepidoptera, Plecoptera, Psocoptera, and Thysanoptera (Dennis, 2014; Dennis and Lavigne, 1975, 2007; Dennis et al., 2010; Hespenheide and Rubke, 1977; Lavigne et al., 1993). According to Musso (1970, 1972), Holopogon venustus fed on Hemiptera (Aphididae) in France. The Asilidae Predator-Prey Database has eight records of Holopogon feeding on spiders (Dennis et al., 2012). Lehr (1964, 1972) commented on Holopogon spp. in the U.S.S.R. feeding on Araneae, and the insect orders Coleoptera, Diptera, Hemiptera (as Hemiptera and Homoptera), and Hymenoptera. Male and female H. snowi generally preyed on the same insect orders. Although males preyed more on Hemiptera and females preyed more on Thysanoptera. One female over a 23.5-minute period preyed on five Thysanoptera and one Hemiptera (Cixiidae, Cixius sp.). Approximately 2 1/2 times as many females as males were captured with prey. Other investigators have reported collecting more female than 105 Ethology of Holopogon snowi Back, 1909 male asilids with prey (Dennis, 2014; 2015a and 2015b). Table 3. Number and percent composition of orders of prey taken by Holopogon snowi.
Male Female Unknown sex Total Order Number Percent Number Percent Number Percent Number Percent Araneae 1 2.0 0 0 0 0 1 0.5 Blattodea 4 7.8 14 10.9 0 0 18 9.9 (Isoptera) Coleoptera 0 0 0 0 1 50.0 1 0.5 Diptera 4 7.8 12 9.3 0 0 16 8.8 Hemiptera 19 37.3 29 22.5 0 0 48 26.4 Hymenoptera 8 15.7 12 9.3 0 0 20 11.0 Psocoptera 4 7.8 16 12.4 0 0 20 11.0 Thysanoptera 10 19.6 40 31.0 0 0 50 27.5 Unidentified 1 2.0 6 4.6 1 50.0 8 4.4 Totals 51 100.0 129 100.0 2 100.0 182 100.0
The following is a list of prey taken by H. snowi. All prey was collected between 30 March and 5 May 2016. The number and sex (if known) of the predator follows the prey record.
ARANEAE, Unidentified, 11.04.2016 (1♂). BLATTODEA (ISOPTERA, alates), Kalotermitidae: Calcaritermes nearcticus (Snyder, 1933), 31.03.2016 (1♀), 19.04.2016 (1♀), 22.04.2016 (1♂), 25.04.2016 (1♂, 2♀♀), 27.04.2016 (1♀); Rhinotermitidae: Reticulitermes virginicus (Banks, 1907), 7.04.2016 (2♂♂, 2♀♀), 14.04.2016 (1♀), 23.04.2016 (4♀♀), 2.05.2016 (1♀), 5.05.2016 (1♀). COLEOPTERA, Curculionidae: Dendroctonus sp., 30.03.2016 (1 unknown sex). DIPTERA, Cecidomyiidae: unidentified, 18.04.2016 (1♂, 1♀), 19.04.2016 (1♂). Chironomidae: unidentified, 31.03.2016 (1♀), 3.04.2016 (2♀♀). Dolichopodidae: Condylostylus sp., 5.04.2016 (1♀). Sciaridae: unidentified, 19.04.2016 (1♀), 21.04.2016 (2♀♀). Unidentified, 4.04.2016 (1♀), 11.04.2016 (1♂), 19.04.2016 (1♂), 26.04.2016 (1♀), 27.04.2016 (1♀), 2.05.2016 (1♀). HEMIPTERA, Auchenorrhyncha, Cicadellidae: Empoasca sp., 31.03.2016 (1♂), 5.04.2016 (2♀♀), 7.04.2016 (1♂, 1♀), 8.04.2016 (1♂), 9.04.2016 (1♂, 1♀), 11.04.2016 (1♂), 18.04.2016 (1♀), 21.04.2016 (2♂), 22.04.2016 (1♀), 23.04.2016 (1♀), 26.04.2016 (1♀); unidentified, 30.03.2016 (2♂♂, 1♀), 3.04.2016 (3♀♀), 6.04.2016 (1♂), 18.04.2016 (1♂). Cixiidae: Cixius sp., 31.03.2016 (1♂), 1.04.2016 (♀), 6.04.2016 (2♀), 7.04.2016 (1♀), 8.04.2016 (1♂), 11.04.2016 (1♀), 12.04.2016 (1♀), 18.04.2016 (1♂), 19.04.2016 (1♂, 3♀♀), 21.04.2016 (3♀♀), 23.04.2016 (1♂), 26.04.2016 (2♀♀), 29.04.2016 (1♂); unidentified, 1.04.2016 (1♂), 21.04.2016 (2♀♀), 27.04.2016 (1♀). Sternorrhyncha, Aphididae: unidentified, 18.04.2016 (1♂). HYMENOPTERA, Chalcidoidea: 30.03.2016 (1♀), 05.04.2016 (2♂♂), 11.04.2016 (1♂), 13.04.2016 (1♂), 18.04.2016 (1♂). Cynipidae: Andricus sp., 6.04.2016 (1♀); Callirhytis sp., 4.04.2016 (1♀), 8.04.2016 (1♂); Synergus sp., 31.03.2016 (1♂), 3.04.2016 (1♀), 5.04.2016 (1♀), 7.04.2016 (1♀). Formicidae (alates): Linepithema sp., 31.03.2016 (1♀); unidentified, 31.03.2016 (1♀), 4.04.2016 (1♂), 15.04.2016 (1♀), 22.04.2016 (1♀); Sphecidae: unidentified, 8.04.2016 (1♀). Unidentified: 22.04.2016 (1♀). PSOCOPTERA, Unidentified, 31.03.2016 (5♀♀), 3.04.2016 (2♀♀), 4.04.2016 (2♀♀), 5.04.2016 (1♂, 1♀), 6.04.2016 (2♀), 7.04.2016 (1♂, 2♀), 9.04.2016 (1♂), 11.04.2016 (1♀), 25.04.2016 (1♀), 26.04.2016 (2♂♂). THYSANOPTERA, Unidentified, 3.04.2016 (1♀), 6.04.2016 (5♀♀), 7.04.16 (1♂), 8.04.2016 (1♂, 1♀), 9.04.2016 (1♂, 2♀♀), 11.04.2016 (2♀♀), 12.04.2016 (1♂, 1♀), 13.04.2016 (3♀♀), 14.04.2016 (1♂), 18.04.2016 (3♂♂, 3♀♀), 19.04.2016 (1♂, 7♀♀), 21.04.2016 (3♀♀), 25.04.2016 (2♀♀), 26.04.2016 (4♀♀), 27.04.2016 (3♀♀), 29.04.2016 (1♂, 1♀), 5.05.2016 (2♀♀). UNIDENTIFIED: 30.03.2016 (1♀, 1 unknown sex), 31.03.2016 (1♀), 11.04.2016 (2♀♀), 19.04.2016 (2♀♀), 26.04.2016 (1♂).
Courtship and mating behavior Male courtship prior to mating has been described for five species ofHolopogon : H. albipilosus (Dennis and Lavigne, 1975), H. claripennis avor and H. priscus (Lehr, 1972), H. phaeonotus (Dennis, 2014), and H. seniculus (Lavigne et al., 1993). Lavigne 106 DENNIS, D. S (2003) suggested that male courtship is probably widespread in the genus. Holopogon snowi males will court both females and other males with or without prey. Holopogon phaeonotus males also court both females and males (Dennis, 2014) and male courtship of prey-feeding females has been reported for H. priscus (Lehr, 1972) and H. seniculus (Lavigne et al., 1993). The author observed 57 courtships, 12 mating pairs, and three complete matings. During courtship, most H. snowi males hovered 1.9-12.7 cm (mean 2.0 cm) in front of (n=17 out of 35) and slightly above (n=11) the level of the courted asilid. A few males also hovered to the side (n=3), behind (n=3), or directly above (n=1) the female. Only one of the three complete matings observed began with courtship; the other two were initially observed as the male landed on the female’s dorsum to begin mating. The male of the complete mating that was observed from courtship, hovered in a stationary position 12.5 cm immediately in front of and 5.0-7.5 cm above the female for 5 seconds. While hovering male abdomens were straight and the fore- and mid-legs were held against the thorax with the tibiae and tarsi pointed forwards. The hind legs were angled posteriorly at about a 30-45˚ angle to the thorax and the hind tibiae and tarsi hung straight down or bent slightly forward. Each courtship hover lasted 3-26 seconds with an mean of 10 seconds. During courtship the male remained stationary, had a slight forward or backwards motion, or moved sideways in an arc up to 7.5 cm. When a male or non-receptive female was courted, they frequently flew off with the courting male in pursuit. A non-receptive female often assumed an agonistic posture by spreading her wings, usually at a 45° angle (range from 30-90˚) to her body and/ or by crawling to the side of the twig. A female would often spread her wings up to three to four times. Following courtship, a male would land on or next to a female and attempt to clasp her genitalia. When unsuccessful, the male would either fly off or repeat the courtship sequence before flying away. One male intermittently courted a non-receptive female for 26 minutes with variable periods of rest, with the longest rest for 5 minutes. The complete matings began when the male flew and landed on the female’s dorsum, clasped her genitalia, and straightened out in the tail-to-tail position (Fig. 4). Most mating pairs (n=10) stayed in a straight tail-to-tail position or were at about 120° to each other, sometimes with their abdomens bent up to form an inverted “V”. Two pairs mated in an inverted “V” position with their abdomens curved around the tip of a twig. Other species of Holopogon also mate in the tail-to-tail position (Dennis, 2014). The complete matings lasted for 54-59 minutes (mean 57 minutes). Most matings ended when a male unclasped the female and immediately flew off. Two matings ended when the asilids flew up and separated in flight within 7.5-12.5 cm above the twig on which they mated. One mating ended when the male unclasped the female, then walked forward on the twig and flew away. During mating, H. snowi remained relatively inactive and moved very little, with only slight adjustments on the twig they stood on. While a female is mating, other males may court the female, land on her dorsum and attempt to mate with her. One 107 Ethology of Holopogon snowi Back, 1909 male courted a mating female and landed on her dorsum four times before flying off.
Fig. 4. Mating pair of Holopogon snowi in the tail-to-tail position. Matings took place in both the sun and shade, and when the sky was overcast. Air temperature at the height of the matings on the twigs ranged from 27.0-34.5ºC with a mean of 29.3°C. Holopogon phaeonotus also mated within a similar temperature range from 27.5-34.0ºC (Dennis, 2014).
Oviposition Female robber flies with acanthophorite-bearing spines at the tips of their ovipositors generally oviposit in soil, as was observed for H. phaeonotus (Dennis, 2014). Although H. snowi females have acanthophorites with spines, they dropped eggs on the scrub oak twigs where they stood or onto the ground below the twigs. Five complete ovipositions were observed during which one to three eggs were quickly oviposited. Females began to exhibit oviposition behavior when they curved their abdomen down and touched the twig with their ovipositor, turned perpendicular to the twig as they extended the abdomen, or they extended their abdomen over a twig tip (Fig. 5). During this process, some females also stroked their abdomens from anterior to posterior, with both hind tibiae and/or tarsi, presumably to help push the eggs out. One female also extended her abdomen prior to dropping a brown liquid and another female had an extended abdomen during mating.
Fig. 5. Female Holopogon snowi ovipositing with extended abdomen and wings blown open by wind. 108 DENNIS, D. S No eggs were recovered from the ovipositions. They were lost in the wind as they were dropped on the ground or twigs, or the wind blew them off the twigs and they could not be found on the ground. The eggs were shiny or glistening white and oblong or elongate, similar to the eggs of H. phaeonotus (Dennis, 2014). Temperatures at the height of the H. snowi ovipositions ranged from 28.5-35.0ºC with an mean of 31.7 ºC. Air temperature above two H. phaeonotus ovipositions in soil were 32ºC and 33ºC.
Grooming Holopogon snowi, like H. phaeonotus (Dennis, 2014), did not frequently groom themselves. This may be because the asilids occupy various heights on vegetation and do not land on the ground. When H. snowi did groom it was in much the same way as reported for H. phaeonotus and other species of robber flies (Dennis, 2014). Holopogon snowi always used the fore legs to groom their heads, and the hind legs to groom their wings (Fig. 2.) and abdomen. Generally grooming of the head followed feeding and grooming of the abdomen followed mating. Grooming of the head was usually preceded and followed by the rubbing together of the fore tarsi. When grooming the head H. snowi used the distal part of the fore femora, the entire tibiae, and the proximal part of the tarsi, often as the asilid quickly turned its head. Holopogon snowi sometimes rubbed its hind tarsi together, leaned forward and down, and then curved the abdomen down before grooming the abdomen and wings. Grooming of the wings and abdomen always proceeded from anterior to posterior with the hind tibiae and tarsi. When the wings were closed, only the top surface was groomed; when the wings were spread at a 45˚ angle to the body, both the tops and bottoms of the wings were groomed outward for about 3/4 of their length. During separate matings, a male and female groomed the tops of their closed wings with their hind tarsi. Also, during feeding one female groomed the tops and bottoms of her spread wings and then the posterior 1/2 of the dorsal part of her abdomen with her hind tibiae.
Daily rhythm of activity Each day, H. snowi began foraging high up (approximately 1.8-2.1 m) on the twigs of vegetation in the areas on the western side of the road where the sun was shining and the areas on the eastern side were still in shade. As the day progressed, the asilids on the western side moved down to lower twigs of vegetation as these areas became exposed to the sun. When the western areas of vegetation became shaded and sunlight was shining on some eastern areas of vegetation (1:00-2:00 PM), the flies began to move across the road to forage from these sunny areas. Between 4:30-6:30 PM, most of the western side of the road was in shade and the majority of asilids had moved to the sunlit areas on the eastern side of the road. Holopogon snowi feeding began between 10:00-11:00 AM with the peak period (65.4% of feeding) from 12:00 noon to 3:00 PM, with a steady tapering off until between 6:00-7:00 PM (Fig. 6). The largest number of mating pairs (66.7%) occurred during 109 Ethology of Holopogon snowi Back, 1909 two peaks, the first peak between 2:00-3:00 PM and the second between 4:00-5:00 PM with seven of eight mating pairs on the eastern side of the road during these time periods. Peak period for ovipositing (three of five ovipositions) occurred between 1:00-2:00 PM with a smaller peak between 11:00 AM-12:00 noon; oviposition behavior (i.e., females extending their abdomens) was observed between 11:20 AM to 2:44 PM.
Mating Ovipositing Feeding
70
60
50
40
30
Specific Behaviors Specific 20
10 Percent of Individuals Engaged of in Percent
0 9-10 10-11 11-12 12-1 1-2 2-3 3-4 4-5 5-6 6-7 7-8 A.M. Time of Day P.M.
Fig. 6. Daily rhythm of activity of Holopogon snowi based on 12, 5, and 182 observations for mating, ovipositing, and feeding, respectively. The peak period of feeding for H. phaeonotus occurred between 10:00 AM and 1:00 PM, and between 1:00-2:00 PM for mating and oviposition (Dennis, 2014). Based on the percent of flies with prey, H. wilcoxi had two peak periods of feeding from about 8:00-10:00 AM and 2:00-4:00 PM (Hespenheide and Rubke, 1977). Holopogon albipilosus also had two peak periods of feeding from 11:00 AM-12:00 noon and from 4:00-5:00 PM, with the peak period for mating from 2:00-3:00 PM (Dennis and Lavigne, 1975). Holopogon claripennis avor foraged primarily from 8:00-9:00 AM, 10:00-11:00 AM and 5:00-6:00 PM (Lehr, 1972). In deserts, where there can be acute changes in weather over 24 hours, Holopogon forage early in the morning and evening and mate and oviposit during the daylight hours (Lehr, 1972).
Predators The same species of robber flies often prey upon each other or exhibit cannibalism (Lavigne et al., 2000). However, H. snowi did not prey upon each other. Cannibalism also has not been observed for other species of Holopogon (Dennis, 2014; Dennis and Lavigne, 1975; Hespenheide and Rubke, 1977; Lavigne et al., 1993; Lehr, 1964, 1972). Proctacanthus brevipennis (Wiedemann, 1828) and Laphria saffrana Fabricius, 1805 occurred in the same habitat as H. snowi, but did not prey on them. In Texas, Bromley (1934) reported Atomosia puella (Wiedemann, 1828) preying on H. snowi. One female H. snowi was caught in a basilica orbweaver [Mecynogea lemniscata (Walckenaer, 1841)] spider web between scrub oak twig tips approximately 60 cm above the ground. Holopogon phaeonotus (Dennis, 2014) and H. seniculus (Lavigne et al., 1993) also has been reported as prey of spiders. 110 DENNIS, D. S The sphecid wasp Steniolia elegans Parker, 1929, preyed on H. atripennis Back, 1909 (Evans, 1973).
CONCLUSIONS Various details have been reported on the ethology of only four of twenty-one species of Holopogon (H. albipilosus, H. phaeonotus, H. seniculus, and H. wilcoxi) in the United States. This paper provides information on a fifth species, H. snowi. This species rested on and foraged from plant twig tips, primarily scrub oak. Holopogon snowi did not attempt to maintain its body temperature by changing its position on the twig tips such as by turning one side towards the sun or by moving into shade of surrounding vegetation. However, each day individuals began foraging higher up in sun-exposed vegetation in areas on the western side of a road and as these areas became shaded, they moved to lower areas of vegetation and to sunlit vegetation on the eastern side of the road. All prey was captured in flight and consisted of Araneae, Blattodea (Isoptera, alates), Coleoptera, Diptera, Hemiptera, Hymenoptera, Psocoptera, and Thysanoptera. During feeding, H. snowi most frequently manipulated prey by holding onto the side of a twig tip with one of its mid-tarsi and manipulating prey with the other tarsi. Males courted females prior to mating, which occurred in the tail-to-tail position. Females extended their abdomens and oviposited on the twigs where they stood or dropped eggs directly onto the ground. Peak period for feeding occurred from 12:00 noon to 3:00 PM. Mating had two peaks from 2:00 to 3:00 PM and 4:00 to 5:00 PM, and the oviposition peak was from 1:00 to 2:00 PM. Holopogon snowi did not frequently groom themselves, possibly because they stayed on vegetation and were never observed on the ground. Holopogon snowi were not cannibalistic, but one female was caught in a spider’s web.
ACKNOWLEDGMENTS The author thanks the staff of the St. Johns River Water Management District for the issuance of the Special Use Authorization that allows the study of robber flies in the Moses Creek Conservation Area. He also acknowledges the anonymous reviewers for their constructive comments on the manuscript.
REFERENCES
Back, E. A., 1909, The robber-flies of America, north of Mexico, belonging to the subfamilies Leptogastrinae and Dasypogoninae. Transactions of the American Entomological Society, 35: 137-400, 12 plates. Bromley, S. W., 1931, A preliminary annotated list of the robber flies of Ohio.Ohio State, Museum Science Bulletin, 1: 1-18. Bromley, S. W., 1934, The robber flies of Texas (Diptera, Asilidae). Annals of the Entomological Society of America, 27: 74-113. Bromley, S. W., 1946, Guide to the insects of Connecticut. Part VI. The Diptera or true flies of Connecticut. Third Fascicle. Asilidae. Connecticut State Geological and Natural History Survey Bulletin, 69, 1-48. 111 Ethology of Holopogon snowi Back, 1909
Bromley, S. W., 1950, Florida Asilidae (Diptera) with description of one new species. Annals of the Entomological Society of America, 43: 227-239. Dennis, D. S., 2014, Ethology of Holopogon phaeonotus Loew, 1874 (Diptera: Asilidae) in Northeastern Florida, U.S.A. Journal of the Entomological Research Society, 16: 141-158. Dennis, D. S., 2015a, Ethology of Diogmites crudelis Bromley, 1936 (Diptera: Asilidae) in Northeastern Florida, U.S.A. Journal of the Entomological Research Society, 17: 23-44. Dennis, D. S., 2015b, Ethology of Proctacanthus fulviventris Macquart, 1850 (Diptera: Asilidae) in Northeastern Florida, U.S.A. Journal of the Entomological Research Society, 17: 1-21. Dennis, D. S., 2016, Ethology of Promachus bastardii (Macquart, 1838) (Diptera: Asilidae) in Northeastern Florida, U.S.A. Journal of the Entomological Research Society, 18: 69-92. Dennis, D. S., Lavigne, R. J., 1975, Comparative behavior of Wyoming robber flies II (Diptera: Asilidae). Agricultural Experiment Station University of Wyoming-Laramie. Science Monograph 30: 68 pp. Dennis, D. S., Lavigne, R. J., 2007, Hymenoptera as prey of robber flies (Diptera: Asilidae) with new prey records. Journal of the Entomological Research Society, 9: 23-42. Dennis, D. S., Lavigne, R. J., Dennis, J. G., 2010, Hemiptera (Heteroptera/Homoptera) as prey of robber flies (Diptera: Asilidae) with unpublished records. Journal of the Entomological Research Society, 12: 27-47. Dennis, D. S., Lavigne, R. J., Dennis, J. G., 2012, Spiders (Araneae) as prey of robber flies (Diptera: Asilidae). Journal of the Entomological Research Society, 14: 65-76. Evans, H. E., 1973, Notes on the nesting behavior of Steniolia elegans (Hymenoptera: Sphecidae). Great Basin Naturalist, 33: 29-30. Geller-Grimm, F., 2016, Robber flies (Asilidae), database, catalog of species. Available from http://www. geller-grimm.de/catalog/species.htm (28.11.2016). Goslin, R. M., 1950, Some robber flies from Campbell County Tennessee. Journal of the Tennessee Academy of Science, 25: 303-306. Hespenheide, H. A., Rubke, M. A., 1977, Prey, predatory behavior, and the daily cycle of Holopogon wilcoxi Martin (Diptera: Asilidae). The Pan-Pacific Entomologist, 53: 277-285. Lavigne, R. J., 2003, Evolution of courtship behavior among the Asilidae (Diptera), with a review of courtship and mating. Studia dipterologica, 9(2002): 703-742. Lavigne, R. J., Bullington, S. W., Stephens, G., 1993, Ethology of Holopogon seniculus (Diptera: Asilidae). Annals of the Entomological Society of America, 86: 91-95. Lavigne, R. J., Dennis, D. S., Gowen, J. A., 2000, Asilid literature update 1956-1976 including a brief review of robber fly biology (Diptera: Asilidae).Agricultural Experiment Station University of Wyoming Science Monograph, 36: 134 pp. Lavigne, R. J., Holland, F. R., 1969, Comparative behavior of eleven species of Wyoming robber flies (Diptera: Asilidae). Agricultural Experiment Station University of Wyoming Laramie. Science Monograph, 18: 61 pp. Lehr, P. A., 1958, On the biology and behavior of robber flies (Asilidae-Diptera). Trudy Instituta Zoologii, Akademiya Nauk Kazakhstan, SSR, 8: 173-196. (In Russian) Lehr, P. A., 1964, On the nutrition and significance of Asilidae. Trudy nauchno-issledovaniya Instituta Zaschti Rasteniy, KazASKhN (Proceedings of the Scientific Research Institute for Protection of Plants, Kazakhstan), Alma-Ata, 8: 213-244. (In Russian) Lehr, P. A., 1972, The robber flies of the genera Holopogon Loew and Jothopogon Becker (Diptera, Asilidae) in the fauna of the USSR. Entomological Review, 51: 99-109. Martin, C. H., 1959, The Holopogon complex of North America, excluding Mexico, with the descriptions of a new genus and a new subgenus (Diptera, Asilidae). American Museum Novitates, 180: 40 pp. McAtee, W. L., Banks, N., 1920, District of Columbia Diptera: Asilidae. Proceedings of the Entomological Society of Washington, 22: 13-33. 112 DENNIS, D. S Morgan, K. R., Shelly, T. E., 1988, Body temperature regulation in desert robber flies (Diptera: Asilidae). Ecological Entomology, 13: 419-428. Morgan, K. R., Shelly, T. E., Kimsey, S., 1985, Body temperature regulation, energy metabolism, and foraging in light-seeking and shade-seeking robber lies. Journal of Comparative Physiology, 155: 561-570. Musso, J. J., 1970, Contribution à l’étude des Asilides de la Basse Provence (Dip. Asilidae) listes de proies. Annales de la Faculté des Sciences de Marseille, 44: 143-153. Musso, J. J., 1972, Observations sur les moeurs prédatrices de quelques Asilides [Dipt. Brachycera] de la Basse Provence. Annales de la Societe Entomologique de France (N.S.), 8: 409-421. Nation, J. L., 2008, Eyes and vision. In: J. L. Capinera (Ed). Encyclopedia of Entomology (2nd edition). Springer, New York, New York, 1386. Williams, A. H., 1999, Arthropod fauna using marbleseed in Wisconsin. Proceedings of the Sixteenth North American Prairie Conference, 16: 165-171.
Received: January 06, 2017 Accepted: January 02, 2018 AUTHOR GUIDELINES Journal of the Entomological Research Society (J. Entomol. Res. Soc.) accepts and publishes original research articles in the all field of entomology. The journal publishes regular research papers, review articles. Short, timely reports may be submitted as short communications. The Editors first evaluate all manuscripts. At this stage insufficiently original, have serious scientific flaws, have poor grammar or English language, or are outside the aims and scope of the journal papers will be rejected. Those that meet the minimum criteria are passed on to at least 2 experts for review. Authors of manuscripts rejected at this stage will usually be informed at most 1 months of receipt. Authors should suggest ([email protected]) four reviewer name, address and e-mail address about manuscript subject to examine the manuscript. At most two of them will be in your country and others will be different countries. Two reviewers are selected from these or editor assign another reviewers. A final decision to accept or reject the manuscript will be sent to the author along with any recommendations made by reviewers. Editor’s Decision is final Reviewers advise the editors, who are responsible for the final decision to accept or reject the article. Manuscript must be written in Arial with 12 type size with double spacing in Word for Windows. Please do not make paragraph in the text. Manuscripts generally should not exceed 30 pages.
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Text: The standard order of sections for original papers is as follows: Introduction, Material and Methods, Results, Conclusions and Discussion, Acknowledgements, References. The scientific names (e.g. genus- and species-group names) are to be italicized. For faunistic research follow this order, Distribution:.., Material examined:…, Host plant:…. Example: Sphex oxianus Gussakovskij, 1928 Distribution: Central and South West Asia, Afghanistan, Iran, Israel, Turkey (Bohart and Menke, 1976; Menke and Pulawski, 2000; Kazenas, 2001), Turkey: Artvin (De Beaumont, 1967). Material examined: Ankara, Altındağ, Çubuk Dam Lake, 900 m, 29. 07. 1998, 1 ♂; Kalecik, 600 m, 24. 06. 2001, 2 ♀♀. Host plant: Echinophora sp. Please use ♀, ♂ symbols. Please write upper genus categories with capital letters.
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References: In the text, reference to the literature should conform to the “name- and- date” system, e.g. (Lyneborg, 1983); Beirne and Young (1953); Edwards (1894-1896); Gayuboet al. (2003). Titles of papers published in languages other than the major ones (English, German, French, Spanish, Portuguese, Turkish) should be an English translation (in parentheses) with an explanatory note at end, e.g. (in Russian). The list references will be given at the end of the article and listed alphabetically, according to the following examples, all periodicals must be unabbreviated and italicized.
Journal Article Beirne, B. P., Young, D. A., 1953, The North American species of Cicadula (Homoptera, Cicadellidae). Canadian Entomologist, 85: 215-226.
Book Chapter Kirejtshuk, A. G., 1992, Evolution of mode of life as the basis for division of the beetles into groups of high taxonomic rank. In: Zunino, M., Bellés, X., Blas, M. (Eds.). Advances in Coleopterology. European Association of Coleopterology, Barcelona, 249-261.
Book Steinmann, H., Zombori, L., 1985, An Atlas of Insect Morphology. 2nd edn. Akadèmiai Kiadò, Budapest, Hungary, 253.
URLs Geller-Grimm, F., 2007, Database Asilidae: Catalog of Species. http://www.geller-grimm.de/ catalog/species.htm (10.03.2010). Nomenclature must be in absolute agreement with current ICZN rules. The only acceptable type concepts are: holotype, paratype etc. The following abbreviations should be adopted: gen. n., sp. n., stat. n. and comb. n. 10 free reprints are supplied per contribution: An additional number may be ordered at the prices quoted on the order form sent to the corresponding author. Journal of the Entomological Research Society uses the Open Journal Systems (OJS) platform, which will enable the journal to accept submissions online. For submitting a manuscript please go to web page http://www.entomol.org and register as author and submit your manuscript online. Manuscripts send by e-mail will be not accepted. URL: http://www.entomol.org e-mails: [email protected] Address: Journal of the Entomological Research Society, P.box.110 Bahcelievler P.Isl.Mud. 06502, Ankara/TURKEY CONTENTS
MACAVEI, L. I., OLTEAN, I., VASIAN, I., FLORIAN T., VARGA, M., BĂEŢAN R., MITRE V., MAISTRELLO L., Potential for Attractive Semiochemical Lures in Rhagoletis cerasi (L.) Management: A Field Study...... 1
IBRAHIMI, H., GRAPCI-KOTORI L., KUČINIĆ M., STAMENKOVIĆ V. S., RIMCHESKA B., BILALLI A., A Study of Trichoptera of the Blinajë Hunting Reserve Including the First Records of Ironoqua dubia (Stephens, 1837) (Limnephilidae) from the Hellenic Western Balkans...... 11
TAMUTIS V., BALALAIKINS M.,BARŠEVSKIS A., FERENCA, R., Comparative Morphology and Morphome- try of Badister (s. str) Species (Coleoptera: Carabidae), Occur in Baltic States, with Notes on Their Distribution in Local Fauna...... 21
SEVEN E., Notes on Some Species of Gnophini (Ennominae, Geometridae, Lepidoptera) from Turkey, with New Records...... 53
RIEDEL M., DILLER E., ÇORUH S., New Contributions to the Ichneumoninae (Hymenoptera, Ichneumon- idae) from Turkey ...... 59
KAZMI S. I., SHEELA S., Annotated Checklist of Indian Elasmus (Hymenoptera: Chalcidoidea : Eulophidae) with a New Synonymy ...... 73
KHALIL M. S., RAZA A. B. M., MAJEED M. Z., AFZAL M., AQUEEL M. A., PONS-GUILLOUARD I., KHALIL H., HANCE T., Species-Specific Effect of Parasitization of Ectoparasitoid, Bracon hebetor (Hyme- noptera: Braconidae) on the Larval Haemocyte Counts of Corcyra cephalonica and Ephestia kuehniella (Lepidoptera: Pyralidae) ...... 87
DENNIS D. S., Ethology of Holopogon snowi Back, 1909 (Diptera: Asilidae) in Northeastern Florida, U.S.A...... 95