TY - JOUR
AU - Büyükgüzel,, Ender
AB - Abstract Understanding the effects of diet on metabolic events is crucial for biological control programs of parasitoid insects. As bioindicators of long-term physiological stress: survivorship of fifth instar larvae, pupation, adult survival, and developmental time for stages of endoparasitoid Pimpla turionellae L. (Hymenoptera: Ichneumonidae) were investigated by rearing the parasitoid on the host, Galleria mellonella L. (Lepidoptera: Pyralidae) pupae were treated with neomycin. First instar larvae of G. mellonella were reared on artificial diets containing 0.005, 0.01, or 0.5 g neomycin (g/100 g of diet) until seventh instar larvae; the pupae from these larvae were used as a host for rearing P. turionellae. In the control group, the pupae from larvae reared on artificial diets without neomycin were used as a host. Survivorship of fifth instar, pupal, and adult stages of P. turionellae L. reared on G. mellonella pupae as a host fed with different concentrations of neomycin were significantly decreased in comparison to the control group. Approximately eighty percent of P. turionellae L. pupae were produced from control host pupae, while other neomycin concentrations significantly decreased the pupation of the parasitoid. Pimpla turionellae L. larvae reared on control host pupae reached fifth instar in about 9.6 ± 0.61 d, while the larvae reared from a host pupae exposed to the highest antibiotic concentration completed their development to the fifth instar in about 7.4 d. These results showed that neomycin, and possibly its metabolites, contaminated P. turionellae L. larvae from a host and affected larval stages of the parasitoid. neomycin, survivorship, development, Galleria mellonella, Pimpla turionellae The irregular and random use of agrochemicals in pest control has resulted in public health issues, environmental problems, soil and water pollution, as well as significant adverse effects on nontargeted useful organisms and other living species (Guo et al. 2018, Togola et al. 2018). This fact has accelerated the search for alternative methods of agricultural pest control, and studies have started to focus on the method globally including cultural, biological, and structural strategies, to control a multitude of pest problems known as Integrated Pest Management (IPM) (Çelik et al. 2002). The parasitoids, Pimpla turionellae L. is a parasitoid species in the Hymenoptera order, and a common insect used in biological control; it completely inhibits the development of the pest by parasitizing the pupa stage of Lepidoptera order insects (Schmidt et al. 2001, Güçlü and Özbek 2011, Sarwar 2014). To complete its development within the host, the adult female parasitoid secretes multiple factors that inhibit the immune system and cause physiological changes in the host species; these factors include calyx fluid, teratocytes, venom secretion, and polydnaviruses via ovipositor either before or while laying eggs (Richards and Edwards 2000, Nakamatsu and Tanaka 2003, Jervis et al. 2008). Determining the nutritional requirements of these organisms and the effects of their diet on metabolic events are crucial for biological control programs (Chang 2004). Therefore, biochemical and physiological properties of these groups of insects are important to determine in the laboratory environment. Against various chemical substances, Hymenopter parasitoids are more sensitive than their Lepidopteran hosts (Büyükgüzel 2006, Uçkan et al. 2007). The amount and quality of the essential diets that parasitoid insects acquire from the host are significant for pre- and postmature development (Magro and Parra 2004, Nakamatsu and Tanaka 2004, Ueno and Ueno 2007). Since the nutritional requirements of holometabol host insects in premature stages vary, the type of ingested diet also affects physiological activities in the adult organism (Hajek 2004). Consequently, they are highly likely to be affected by the insecticides used in pest control. Traditional insecticides used in pest control could have an adverse effect on the developmental stages of the parasitoid insect (Sak et al. 2006). However, there are limited studies on the effects of less toxic compounds like neomycin in the application of parasitoids on hosts in which the parasitoid insects have completed their development and this eco-friendly compounds transfer from the host to the parasitoid. Neomycin, an aminoglycoside antibiotic, is naturally produced by the Streptomyces fradiae bacterium. Due to binding of the bacterial ribosomes to the 30S subunit, and, in some cases, to the 50S subunit, the bacterium was shown to act by inhibiting the protein synthesis during the initiation and prolongation phases (Kaul and Pilch 2002, Kaul et al. 2003). The antibiotic kills bacteria by preventing the production of necessary vital proteins. It was determined that neomycin and other aminoglycoside antibiotics bind to phosphoinositide-type lipids (phosphatidylinositol 4,5 bisphosphate) in eukaryotes, thereby preventing hydrolysis of these lipids, and thus, inhibiting the functions mediated by phosphoinositide (Arbid et al. 2013). Concerns over the adverse effects of the continued use of conventional pesticides on human health and the environment, together with continuing problems of pest resistance, have encouraged the search for safer and more environmentally-sustainable alternatives for pest management. A number of publications detail the development of new eco-friendly chemical materials for pest management. For this purpose, some articles have shown that many antibiotics can be used as an alternative to traditional chemicals used on Galleria mellonella (Büyükgüzel and Kalender 2008, 2009; Hız et al. 2016; Çalık et al. 2016). Galleria mellonella L. larvae, a P. turionellae host, causes significant economic damage in beehives. Galleria mellonella L. (beeswax moth) is a species in the Lepidoptera family, which includes about 160,000 other species. As bioindicators of long-term physiological stress responses, the survivorship of fifth instar larvae, pupation, adult survival, and developmental time for these stages of endoparasitoid P. turionellae were investigated by rearing the parasitoid on a host, G. mellonella, treated with neomycin as an alternative to insecticides which are conventionally used in agriculture. Previous studies have been conducted on the effects of different some aminoglycoside antibiotics on the survival and development of parasitoid insects, P. turionellae, by using synthetic diets (Singh and House 1970a,b; Büyükgüzel and İçen 2004). However, the effects of these antibiotics on parasitoid insects that are cultured on their natural hosts are unknown. Material and Methods Host Insect Culture Honeycombs, naturally infected with greater wax moth, were collected from apicultural area of Zonguldak, Turkey. We separated larvae and pupae of G. mellonella on the honeycombs and obtained newly-emerged adults were used to start a colony. Galleria mellonella culture was maintained in constant darkness at 28 ± 2°C and 65 ± 5% relative humidity in an ES500 incubator (Nüve, Ankara, Turkey). The artificial diet contained bran (420 g), filtered honey (150 ml), glycerol (150 ml), ground dark honeycomb (20 g), and distilled water (30 ml) per 1,000 g of diet (Bronskill 1961). Newly-emerged females were placed in jars and provided a piece of dark honeycomb on the diet for egg deposition and feeding of newly-hatched larvae (Ortel 1995). After a period of 25–30 d, seventh instar larvae were transferred to another jar lined with filter paper. The filter paper was used to provide a dry surface for pupation. Parasitoid Insect Culture Pimpla turionellae individuals were cultured using natural host large beeswax moth G. mellonella pupae under laboratory conditions at a temperature of 28 ± 1°C and relative humidity of 75 ± 5% with 16 h of daylight. Adults were fed daily with a 50% honey solution at the same time and for a certain period, and G. mellonella pupae were provided so that they could feed on the pupal hemolymph. Experimental Design Neomycin was added directly to the diet during the preparation. For G. mellonella, three different neomycin concentrations of 0.005, 0.01, and 0.5%, and a control diet (without neomycin) were tested in four independent replicates. One-day G. mellonella pupae were obtained from the larvae fed with the treated diets. For each concentration, 15 G. mellonella pupae were used for laying eggs from P. turionellae female adults. The neomycin concentrations that were used in the present study were based on previous studies, in which the effect of antibiotics on G. mellonella and certain parasitoid insect species, i.e., P. turionellae was investigated (Büyükgüzel and Yazgan 1996, Büyükgüzel 2001). The concentration ranges in which the host insects could complete development up to the adult stage were determined. The concentrations of neomycin on P. turionellae were determined and their effects on the survival and developmental time of parasitoid insects and male and female longevity were examined. Determination of Survival, Developmental Time, and Adult Longevity The antibiotic amounts determined in preliminary tests were added to the synthetic diets. The prepared synthetic diet was divided into food containers (jars, 60 × 120 mm). Then, the control diet and other diets that contained neomycin were placed in food containers in equal amounts. Galleria mellonella female and male were left on these foods for laying eggs and for producing larvae. The tests were repeated independently four times. In each independent repetition, seventh stage G. mellonella larvae that had completed their development were placed in containers (jars, 30 × 60 mm) to develop into the pupal stage. Folded thin tissue paper was left in these containers to help pupal transformation. Seven to eight days after pupal stage was reached, 15 G. mellonella pupae from each concentration were placed in P. turionellae cages for parasitizing by adult P. turionellae. To prevent the P. turionellae adults from feeding on the hemolymph of the G. mellonella pupae, they were placed in the cages using special small apparatus surrounded by wires. These wires had openings where only the P. turionellae could lay eggs and also, it is connected with corrugated cardboard plates in which the G. mellonella pupae can be place. After the pupae were placed in the cages, they were placed in a dark room for 30 min and the parasitizing process was completed. Each parasitized pupae was placed in 30-ml plastic sample containers (Orlab L190030, Ankara, Turkey) with one pupa in each well. This procedure was repeated for each G. mellonella pupae in each concentration. Eight to ten days after this procedure, fifth stage P. turionellae larvae in the pupae were placed in No. ‘0’ (zero) transparent drug capsules that contained blotting paper and 5 μl water, then replaced in the same state size of containers, and their development until the adult stage was monitored. Pimpla turionellae individuals that were regularly controlled every day and reached the adult stage were removed from the No. 0 transparent capsules and placed in 30-ml plastic containers. The nutritional needs of adult individuals were satisfied by small stubs of cotton that contained a mixture of 50 % water and 50 % honey. Following the emergence of parasitoid adults, the sex of each enclosed adult was recorded. Newly-emerged adults were transferred into 30-ml plastic cups covered with screened lids. The parasitoids were provided with 1:1 honey water solution. The number of dead adults in each of the treatment groups was counted and recorded daily until all adults had died, to determine average adult longevity. Statistical Analysis Data on developmental time and adult longevity were evaluated by conducting an analysis of the variance (ANOVA). To determine significant differences between means least significant difference (LSD) test (SPSS 1997) was used. Data on survivorship were compared by a χ2 test (Snedecor and Cochran 1989). When the F and χ2 estimates exceeded the probability of 0.05, the differences were considered significant. Results Pimpla turionellae, grown in pupae of G. mellonella, fed on the different concentrations of neomycin, significantly shortened the survival of fifth larvae, pupae, and adults (Figs. 1, 2, and 3). In the control group, the survival of larvae was 86.6 ± 3.33%, whereas the survival after feeding on diets containing 0.005 and 0.01% neomycin, respectively, decreased to 31.6 ± 3.63 and 28.2 ± 7.59%. The survival of larvae increased significantly with the highest concentration of neomycin, as compared to the lowest concentration (Fig. 1). On the other hand, the pupae and adult survival was significantly reduced in all neomycin concentration, as compared to the control group (Figs. 2 and 3). Fig. 1. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae fifth larvae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). Fig. 1. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae fifth larvae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). Fig. 2. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae pupae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). Fig. 2. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae pupae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). Fig. 3. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae adult. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). Fig. 3. Open in new tabDownload slide Effects of neomycin on survival of parasitoid insect P. turionellae adult. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (χ2 test). Control diet (without Neomycin). While P. turionellae larvae grown in host pupae, reared without a neomycin diet, reached 79.9 ± 2.35% pupae stage, the other neomycin concentrations reduced the pupae survival of parasitoid by approximately 50%. In comparison to the control, 0.01% neomycin concentration significantly decreased P. turionellae pupal survivorship (Fig. 2). Pimpla turionellae larvae grown in G. mellonella pupae, reared with a control diet, 78.3 ± 1.44% reached the adult stages; in comparison, P. turionellae larvae growing with other concentrations were reduced by approximately 1/3. In 0.01% neomycin concentration, 19.9 ± 2.35% of adult parasitoids were obtained from host pupae reared with this concentration (Fig. 3). The highest concentration of neomycin shortened the developmental time of reaching the fifth larval stage of P. turionellae by an average of 2 d. P. turionellae larvae, reared on the control group host pupae, reached the fifth stage in an average of 9.6 ± 0.61 d. At the highest concentration of neomycin treatment, parasitoid larvae reached the last larval stage in an average 7.4 ± 0.02 d (Fig. 4). None of the neomycin concentrations had a significant effect on the developmental time of the parasitoids’ pupal stage and adult stage (Figs. 5 and 6). Fig. 4. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae fifth larvae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Fig. 4. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae fifth larvae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Fig. 5. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae pupae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Fig. 5. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae pupae. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Fig. 6. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae adult. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Fig. 6. Open in new tabDownload slide Effects of neomycin on developmental time of parasitoid insect P. turionellae adult. Four replicates per treatment with neomycin 15 parasite G. mellonella pupae per replicate. Values labeled with the same letter are not significantly different from each other within each concentration of neomycin, P > 0.05 (LSD test). Control diet (without Neomycin). Galleria mellonella pupae, reared with different neomycin concentrations, were used to obtain parasitoid adults to investigate the longevity of male and female adult parasitoids. This test group showed that a 0.01% concentration of neomycin shortened the adult female longevity by approximately 32 d, as compared to the control diet (Table 1). Table 1. Male and female adult longevity (day) of Pimpla turionellae reared on a Galleria mellonella pupae treated with neomycin Neomycin (%) Adult longevity (day) Male (mean* ± SE)† Female (mean* ± SE)† 0.000‡ 44.6 ± 7.12a 71.01 ± 3.31a 0.005 56.5 ± 2.72ab 66.62 ± 4.21a 0.01 55.4 ± 7.27ab 38.54 ± 11.47b 0.5 29.0 ± 9.63a 63.65 ± 3.21a Neomycin (%) Adult longevity (day) Male (mean* ± SE)† Female (mean* ± SE)† 0.000‡ 44.6 ± 7.12a 71.01 ± 3.31a 0.005 56.5 ± 2.72ab 66.62 ± 4.21a 0.01 55.4 ± 7.27ab 38.54 ± 11.47b 0.5 29.0 ± 9.63a 63.65 ± 3.21a *There were four replicates per treatment with neomycin. Fifteen G. mellonella pupae were parasitized per replicate. †Mean values within a column followed by the same lowercase letter are not significantly different. P > 0.05 (LSD test). ‡Control diet (without neomycin). Open in new tab Table 1. Male and female adult longevity (day) of Pimpla turionellae reared on a Galleria mellonella pupae treated with neomycin Neomycin (%) Adult longevity (day) Male (mean* ± SE)† Female (mean* ± SE)† 0.000‡ 44.6 ± 7.12a 71.01 ± 3.31a 0.005 56.5 ± 2.72ab 66.62 ± 4.21a 0.01 55.4 ± 7.27ab 38.54 ± 11.47b 0.5 29.0 ± 9.63a 63.65 ± 3.21a Neomycin (%) Adult longevity (day) Male (mean* ± SE)† Female (mean* ± SE)† 0.000‡ 44.6 ± 7.12a 71.01 ± 3.31a 0.005 56.5 ± 2.72ab 66.62 ± 4.21a 0.01 55.4 ± 7.27ab 38.54 ± 11.47b 0.5 29.0 ± 9.63a 63.65 ± 3.21a *There were four replicates per treatment with neomycin. Fifteen G. mellonella pupae were parasitized per replicate. †Mean values within a column followed by the same lowercase letter are not significantly different. P > 0.05 (LSD test). ‡Control diet (without neomycin). Open in new tab Discussion The effects of the natural host G. mellonella fed with different neomycin concentrations on the survival parameters of P. turionellae were determined in a laboratory environment. The study findings demonstrated that neomycin significantly affected on the survival of P. turionellae larvae, pupa, and adults; developmental time of fifth larvae of P. turionellae; and adult longevity of the females and males. It was found that all neomycin concentrations had an adverse effect on P. turionellae larval, pupal, and adult survival, as compared to the control diet, and there was a statistically significant difference between the control and other concentrations. Although we used an antibiotic neomycin for endoparasitoid P. turionellae, similar techniques were applied and conducted on the different developmental stages of an ectoparasitoid Bracon hebetor in a study by Ebeid et al. (2017). It was demonstrated that three insecticides (Profenofos, Cyfluthrin, and IGR [Runner]) caused an indirect effect on egg hatchability, pupation, and adult emergence of B. hebetor. Their data showed that egg hatchability of B. hebetor parasitized on G. mellonella decreased in a concentration-dependent manner, compared to the control group. In a similar study, the plant growth hormone Gibberellic acid (GA3) was administered to G. mellonella, a host species, in different doses and demonstrated no statistically significant differences in the parasitoid adult developmental time, despite the reduction in the host’s developmental time. It was suggested that GA3 could have affected host growth by affecting diet quality, and could have been detoxified in the host’s metabolism by the host’s defense system, or could have failed to affect the parasitoid developmental time due to the reduction of the effect (Öztürk 2010). In the present study, all neomycin concentrations demonstrated a significant decrease in the likelihood of reaching adulthood. This could either be the result of the parasite defense failing to reduce the action of the utilized chemical substance, or the insufficiency of the insect’s detoxification system (Usmani and Knowles 2001). The highest-tested neomycin concentration significantly shortened the time required for fifth larvae of P. turionellae, however, there was no statistically significant difference in the pupal and adult developmental times at the same concentration. We infer from these results that this positive effect on the developmental time of the fifth larvae of P. turionellae may have occurred in the physiological compensatory process for the indirect effect of neomycin. A similar result (Büyükgüzel 1999) demonstrated that P. turionellae cultured in 30 mg and higher concentrations of erythromycin significantly shortened the period required to reach the fifth and pupal stages for P. turionellae; however, it was also demonstrated that this positive effect was not significantly reflected in the time required to reach the last larval stage, unlike our present findings. In the same study, it was determined that the tested concentrations of streptomycin, one of the antimicrobial aminoglycoside antibiotics and a member of the same group as neomycin, were effective during the time required for the insect to reach the fifth instar larva and adult stages (Büyükgüzel 1999). Similar to our study, Büyükgüzel and Kalender 2008 showed that sublethal doses of penicillin and streptomycin significantly shortened developmental time of G. mellonella. In another publication, it was determined that P. turionellae larvae had a high tolerance for different antibiotic concentrations and types. Among the tested antibiotics, it was demonstrated that only the highest nutritional concentration of streptomycin, an aminoglycoside antibiotic, had an adverse effect on the time required to reach the adult stage (Büyükgüzel and Yazgan 2002). Several studies have confirmed that various insecticides have a toxic effect on the host–parasite relationship, and that chemical stress on the host negatively affects the developmental period of parasitoid insects (Ortel et al. 1993, Stapel et al. 2000, Kramarz and Stark 2003, Penagos et al. 2005, Fernandes et al. 2010, Turchen et al. 2016; D’Ávila et al. 2018). In our case, when the 0.01 neomycin concentration was compared to the control group, it was found that it significantly decreased the P. turionellae female adult longevity. Our results are confirmed by Alix et al. (2001); they inferred that the longevity of parasitoids surviving a sublethal dose was reduced. In our present study, neomycin caused a significant reduction in adult male longevity in the 0.5% concentration group, as compared to the control group. In yet another study, Robert and Olson (1989) were observed that adult insect’s longevity, egg yield, and egg hatching decreased when sublethal methoprene and malathion doses were administered to fourth stage female Culex quinquefasciatus (Diptera: Culicidae) larvae. Previous studies have shown that exposed doses of insecticides are highly correlated with adult longevity (Fernandes et al. 2010). Since the P. turionellae larvae have a closed intestine, they can empty the intestinal contents only in the pupal stage. Another remarkable effect of antimicrobial agents on the survival and development of P. turionellae was the irregularity observed in the effects of certain agents. For example, the effects of linkomycin hydrochloride and the cefradin monohydrate on the survival rate in postlarval stages of the insects were similar. The highest-tested doses of these antibiotics (60 mg/100 ml diet) significantly increased the survival rate that the previously tested amount (45 mg/100 ml diet) had actually decreased. Such irregularities might result from the antimicrobial agents being ingested with the diets, altering the intestinal osmotic pressure of the insects, and leading to different amounts of absorption, as well as affecting the intestinal and digestive tract pH, causing a change in their activity. Furthermore, it was noted that the intestinal absorption of beta-lactam antibiotics (Catnach et al. 1994), cephalosporin (Snyder et al.1997), and ofloxacin (Rabbaa et al.1997) found in the fluoroquinolone in several organisms occurred due to the carriers in the proton-dependent peptide structure, and that pH plays an important role in this absorption. The application of toxic substances, such as insecticide, can block some physiological or biochemical processes of target and nontarget species. These processes may impact the survival, growth, development, reproduction, and behavior of the organism (Delpuech and Meyet 2003, Tomizawa and Casida 2003, Fernandes et al. 2010). In this study, the negative effects on the survival and development parameters of P. turionellae obtained from neomycin-treated Galleria pupae may have blocked the physiological and biochemical processes of the parasitoid insect with an indirect effect on neomycin. In the developmental stages of P. turionellae (which can be used as a biological control agent) and similar species, intended to be mass-produced for biological control, various factors, such as environmental conditions, the host’s properties, the host’s exposure to toxic substances, and diet contamination, are important factors that affect the development of parasitoid insects. Endoparasitoid P. turionellae was fed with various synthetic diets (with known chemical structures) that contain insecticides, and its effects were investigated. There are only a limited number of studies conducted with natural hosts because it is difficult to culture both the host and the parasitoid insect concurrently. Thus, the effects of neomycin-treated host insect G. mellonella pupae on the growth, development, and adult longevity of P. turionellae, a long-term physiological stress bio-indicator and endoparasitoid insect species, in larval, pupal, and adult stages were investigated in the present study. The present study is considered significant, as it can provide a basis for future research. Acknowledgments This study was supported by Zonguldak Bülent Ecevit University, Research Fund (Project No: 2014-50737594-02). References Cited Alix A., A. M. Cortesero J. P. Nénon , and J. P. Anger . 2001 . 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TI - The Effect of Neomycin on Survival and Development of Pimpla turionellae L. (Hymenoptera: Ichneumonidae) Reared on a Natural Host
JF - Journal of Economic Entomology
DO - 10.1093/jee/toy419
DA - 2019-05-22
UR - https://www.deepdyve.com/lp/oxford-university-press/the-effect-of-neomycin-on-survival-and-development-of-pimpla-5NPjOGUWz4
SP - 1081
VL - 112
IS - 3
DP - DeepDyve
ER -