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Evaluation of Responses of Different Ant Species (Formicidae) to the Scavenger Deterrent Factor Associated with the Entomopathogenic Nematode-Bacterium Complex

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Evaluation of Responses of Different Ant Species (Formicidae) to the Scavenger Deterrent Factor Associated with the Entomopathogenic Nematode-Bacterium Complex EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 115: 312–317, 2018 http://www.eje.cz doi: 10.14411/eje.2018.030 ORIGINAL ARTICLE Evaluation of responses of different ant species (Formicidae) to the scavenger deterrent factor associated with the entomopathogenic nematode-bacterium complex BARIS GULCU 1, SELCUK HAZIR 2, EDWIN E. LEWIS 3 and HARRY K. KAYA4 1 Department of Biology, Faculty of Arts and Sciences, Duzce University, 81620, Duzce, Turkey; e-mail: [email protected] 2 Department of Biology, Faculty of Arts and Sciences, Adnan Menderes University, 09010, Aydin, Turkey; e-mail: [email protected] 3 Department of Entomology, Plant Pathology and Nematology, University of Idaho, 83843, Moscow, ID, USA; e-mail: [email protected] 4 Department of Entomology and Nematology, University of California, 95616, Davis, CA, USA; e-mail: [email protected] Key words. Ants, Formicidae, scavenger deterrent factor, pathogens, Heterorhabditis, Photorhabdus Abstract. According to previous observations, it was hypothesized that the feeding behavior of some ant species would be deterred by a scavenger deterrent factor (SDF), whereas for other species it would not. The effects of the SDF were studied on 11 ant species in three different subfamilies: Dolichoderinae Forel, 1878, Formicinae Latreille, 1809, and Myrmicinae Lepeletier de Saint-Fargeau, 1835. The experiments were conducted from 2014–2015 in Davis, California, United States, Aydin, Turkey, and Duzce, Turkey. Five-day-old Heterorhabditis bacteriophora (Poinar, 1976), (Hb)-killed and freeze-killed Galleria mellonella (Linnaeus, 1758) were exposed to ant colonies in the fi eld for 3 to 4 h. Seven ant species fed signifi cantly less on Hb-killed in- sects than freeze-killed insect. On the other hand, there was no signifi cant difference in cadaver consumption with fi ve species, but Liometopum occidentale Emery, 1895 did consume a higher rate of Hb-killed insects than freeze-killed insects and was not deterred by SDF. It was also observed that four ant species took Hb-killed insects into the nests, but two Myrmicinae species, Pogonomyrmex subdentatus Mayr, 1870 and Messor meridionalis (André, 1883) removed the cadavers after 30 min, whereas two Formicinae species, Cataglyphis nodus (Brullé, 1833) and Formica fusca Linnaeus, 1758, retained the cadavers in the nest. It was assumed that the latter two species consumed both Hb-killed and freeze-killed insects. Further studies are needed to explain why L. occidentale C. nodus and F. fusca are not deterred by SDF. INTRODUCTION “Ant Deterrent Factor” (ADF). Subsequently, Gulcu et al. The scavenger deterrent factor (SDF) is an unidenti- (2012) reported that ADF not only deters several ant spe- fi ed chemical compound(s) associated with insects killed cies but also repelled crickets, vespid wasps and callipho- by the entomopathogenic nematode-bacterium complex. rid fl ies from feeding on nematode-killed insects, and they This SDF affects scavengers and/or omnivores like ants renamed it SDF because it had a wider effect on different (Baur et al., 1998; Zhou et al., 2002) crickets, cockroach- species of scavenger insects. es, springtails, vespid wasps, and calliphorid fl ies (Gulcu EPNs are in the families Heterorhabditidae, Poinar, 1975 et al., 2012; Ulug et al., 2014), predatory insects (Foltan (Nematoda: Rhabditida) and Steinernematidae, Nguyen & & Puza, 2009; Jones et al., 2016), an insectivorous bird Smart, 1994 (Nematoda: Rhabditida) and as stated above, (Fenton et al., 2011), and more recently three cyprinid fi sh have a mutualistic relationship with bacteria in the genera species (Ramalingam et al., 2017) and results in complete Photorhabdus (Heterorhabditis) and Xenorhabdus (Stein- rejection or only partial consumption of nematode-killed ernema) (Kaya & Gaugler, 1993). In the EPN-bacterium insects. Zhou et al. (2002) demonstrated that the deter- life cycle, the 3rd stage infective juvenile (IJ) seeks an in- rent effect on scavenger ants was associated with the mu- sect host in the soil, enters via natural openings (mouth, tualistic bacterial genera, Photorhabdus (Boemare et al., anus or spiracle), penetrates into the host’s hemocoel and 1993) (Enterobacteriaceae) and Xenorhabdus Thomas & releases the bacterial cells that are sequestered in the IJ’s Poinar, 1979 (Enterobacteriaceae) of entomopathogenic intestine (Adams & Nguyen, 2002). The bacteria multi- nematodes (EPNs) and referred to the compound(s) as an ply and kill the host by septicemia in 24–48 h (Hazir et Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 312 Gulcu et al., Eur. J. Entomol. 115: 312–317, 2018 doi: 10.14411/eje.2018.030 al., 2003; Boemare & Akhurst, 2006). After infection, the MATERIAL AND METHODS nematodes develop to adults and it takes a week or more Nematodes and infection of larvae before the newly produced IJs emerge to seek out new The EPN, Heterorhabditis bacteriophora (Hb) (Bakersfi eld hosts. strain) (Poinar, 1976) (Nematoda: Rhabditida) was used in the During bacterial multiplication in the insect host, a vari- experiments in USA and in Turkey. This nematode strain was ety of small molecules are produced that protect the cadav- maintained in Dr. Edwin E. Lewis’ laboratory in the Department er from bacterial and fungal contamination (Boemare & of Entomology & Nematology, Davis, California. The nematode Akhurst, 2006; Hinchliffe et al., 2010; Tobias et al., 2017) was cultured using last instar Galleria mellonella (Linnaeus, as well as invertebrates and some vertebrates (Baur et al., 1758) (Lepidoptera: Pyralidae) larvae at 23–24°C according to 1998; Foltan & Puza, 2009; Fenton et al., 2011; Gulcu et Kaya & Stock (1997). The Hb-killed larvae were transferred to al., 2012; Jones et al., 2016; Ramalingam et al., 2017). Pos- a White trap, and emerging IJs were harvested from the water (White, 1927) and stored at 15°C for no more than 3 weeks when sibly, SDF is a small molecule (s) within the anthraqui- they were used to infect the test insects. nones (AQs) which are ecologically important metabolites To obtain the nematode-killed larvae for fi eld studies, 10 G. for Photorhabdus and appear to protect nematode-killed mellonella were exposed to 100 IJs/larva in a plastic petri dish insects more than metabolites from Xenorhabdus that does (100 × 15 mm) lined with a fi lter paper. Petri dishes were placed not have AQs (Pankewitz & Hilker, 2008; Bode, 2009; in plastic bags to maintain moisture and kept at 25°C for 5 days. Gulcu et al., 2012; Ulug et al., 2014). Ant colonies Ants (Hymenoptera: Formicidae) are one of the most Twelve ant colonies representing 11 species in three subfami- successful groups of eusocial insects in the world (Fittkau lies were observed for their response to nematode-killed insects & Klinge, 1973). They are important as scavengers, herbi- (Table 1). Ant species from the USA and Turkey were identifi ed vores, or predators and show highly specialized behaviors by Dr. Phillip S. Ward, University of California-Davis, Depart- like farming fungi, harvesting seeds, herding and milking ment of Entomology and Nematology, and Dr. Kadri Kiran, of other insects (e.g., aphids), communal nest weaving, Trakya University, Department of Biology, respectively. Six of cooperative hunting in packs, social parasitism and slave- the colonies were from Davis, California, USA and the other six making (Hölldobler & Wilson, 1990). Other species are of were from Duzce, and Aydin, Turkey. omnivores feeding on a variety of food sources. Studies Of the 12 colonies, two were colonies of Tetramorium cf. caes- conducted by Baur et al. (1998), Zhou et al. (2002), Gulcu pitum (Linnaeus, 1758) (Hymenoptera: Formicidae); one collect- ed in California and the other from Turkey (Table 1). et al. (2012), and Ulug et al. (2014) showed that several ant species do not feed on Steinernema- or Heterorhab- Experimental design ditis-killed insects that were more than 2-days old and Four G. mellonella cadavers were pinned on a piece of card- heterorhabditids produce a stronger deterrent factor than board (10 cm × 12 cm) and placed nearby ant nests or trails. (See steinernematids. Some scavenger species, such as ants and Fig. 1 for arrangement of cadavers on cardboard.) The color of crickets, partly consume 2-day-old Steinernema-killed in- cardboards was brownish which is similar to the color of the soil. sects but not Heterorhabditis (Gulcu et al., 2012; Ulug et Two cadavers were fi ve-day-old Hb-killed and two were freeze- killed larvae. Five-day-old EPN-killed cadavers were used be- al., 2014). Recently, it was observed that two ant species, cause in the previous studies, the highest SDF activity was re- Cataglyphis nodus (Brullé, 1833) (Hymenoptera: Formi- ported after four days (Gulcu et al., 2012). The experiments were cidae) and Liometopum occidentale Emery, 1895 (Hyme- repeated three times for each ant species. The cadavers were noptera: Formicidae), did consume Heterorhabditis-killed placed out in the fi eld for 3 to 4 h between 0600 and 1100 h, or in insects. Accordingly, it was hypothesized that the response the late afternoon between 1500 and 2000 h in a shaded location of ants to SDF varied by species and we report herein a in summer of 2014 and 2015. Ant activity was observed hourly quantitative study to determine differential responses of over the 3 h period,
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