Survivorship, developmental period, and adult longevity of the fruit fly, Drosophila melanogaster Meigen (Diptera: Drosophilidae), exposed to penicillin G, a beta-lactam antibiotic, was determined in laboratory testing. In the study, neonate larvae were placed and reared on dietary antibiotics at concentrations of 100, 200, 400, or 800 mg/L. All penicillin concentrations significantly decreased survivorship in an inverse relationship with third instars, pupae, and adults. Larvae fed on control diets of 0 mg/L of penicillin had a survival level of 91.00 ± 3.27% to third instar and pupation, and 89.00 ± 4.09% to adult emergence. Feeding on a diet containing the highest concentration of penicillin (800 mg/L) significantly decreased survivorship to third instar to 11.00 ± 2.59% (χ2 = 128.051; df = 1; P = 0.0001) and to pupation (χ2 = 131.233; df = 1; P = 0.0001) and adult emergence to approximately 10.00 ± 1.00% (χ2 = 124.832; df = 1; P = 0.0001). The highest concentration of dietary penicillin (800 mg/L) also significantly prolonged developmental time from neonate to third instars by 1.5 d (F = 17.229; df = 4; P = 0.0001) and from neonate to adult emergence by 3 d (F = 2.004; df = 4; P = 0.032). Compared to the control group, adult longevity was significantly reduced by the antibiotic in a dose-related manner. The use of this antibiotic in insect artificial rearing enables an extensive search of possible insecticidal action of penicillin with high dietary levels for agricultural purposes.

Antibiotics have been widely used in the treatment of human and animal diseases and as feeding stimulatants for increasing animal performance and yield (Gaskins et al. 2002). Penicillin group antibiotics do not easily persist in the environment (Blackwell et al. 2005). These antibiotics with the beta-lactam structure prevent synthesis of peptidoglycan, which plays an important role in the formation of bacterial cell wall structure (Kümmerer 2009).

Insects may be exposed to antibiotic chemicals, particularly the penicillins, that are released into the environment by microorganisms that produce them naturally (Grenni et al. 2018). The actual mechanism of action of this antibiotic on insects is unknown. However, it is known that penicillin and other antibiotics added to diets used in mass production of insects have negative effects on survival, development (Büyükgüzel and Kalender 2007, 2008), and adult fitness by weakening the enzymatic antioxidant defense system, especially against oxidative stress, following exposure to high dietary concentrations (Büyükgüzel and Büyükgüzel 2019).

Recently, antibiotics have been added to artificial diets used in the cultivation of insects under laboratory conditions to prevent bacterial contamination, to produce reproductively sterile insects, or to determine concentrations that have negative effects on insects. However, there is insufficient research on their effects on insects. And, before intensive physiological and biochemical studies are performed, the effects of antibiotics on biological parameters on insects should be known.

The fruit fly, Drosophila melanogaster Meigen (Diptera: Drosophilidae), has short life cycle and longevity, and is easily produced in large numbers of individuals in a short period of time, with embryo formation within 24 h following fertilization. It is widely used as a model organism as an alternative to mammalian hosts in biological and biomedical studies due to its similarity in genetic composition with mammals (approximately 60%), its similarity in metabolic and signal transduction pathways with mammals, and its ease and relatively inexpensive rearing in laboratory conditions (Staats et al. 2018). Drosophila melanogaster is also widely used as an alternative model organism for mammalian hosts to determine pathogenicity of microorganisms in humans and other mammals (Chamilos et al. 2011), to investigate the efficacy of developed pharmaceuticals (Avanesian et al. 2009), and to detect industrial pollution for toxicological studies (Posgai et al. 2011).

In chemical control of agricultural and industrial pest insects, it is extremely important to use chemicals that are effective in low doses but harmless to nontarget organisms, especially humans. The effects of antibacterials, anthelmintics, and antiviral drugs for various purposes are studied extensively on D. melanogaster as a model organism. A study has shown that these drugs adversely affect the survival and development of the insect by increasing the oxidative stress in different tissues at various stages of the insect's development and weakening the antioxidative defense system (Aslan et al. 2019). Thus, new information is obtained about the mechanism of the effects of antimicrobial drugs on the survival and development of some other insects (Çelik et al. 2019, Harmancı et al. 2019). Studies on the direct effect of antimicrobial drugs on the survival and development of D. melanogaster are limited. We undertook this study to define the effect of penicillin, a bacterial antibiotic, on insects and for its potential as an insecticide against pest insects. Penicillin is an antibiotic that has demonstrated effects on prokaryotic microorganisms. Its impact on eukaryotic organisms such as insects may differ, with a different mode of action. Therefore, in this study larvae of D. melanogaster, which is a model organism, were fed on penicillin-containing diets and changes in insect survivorship and development until adult stage, along with adult longevity, were determined.

Insect culture. Insects used in this study were collected from a colony of the Oregon R strain of D. melanogaster (Diptera: Drosophilidae). Insects were reared aseptically by standard methods in 250-ml glass bottles containing diet. Insects in the bottles were reared in an ES 500 incubator (Nüve, Ankara, Turkey) at 25 ± 2°C and 60–70% relative humidity (RH) on a 12:12-h light:dark photoperiod. Neonate larvae were removed from these colonies for use in the experiments described herein.

The artificial diet used for rearing of the colony and for preparation of treatments was described by Roberts (1986: p. 19). Briefly, it contained (per 1,000 ml total volume) 8 g agar (Merck & Co., New York), 20 g sucrose (Carlo Erba Reagents S.A.S, Sabadell, Barcelona, Spain), 11.78 g dry yeast (Dr. Oetker Food Industry and Trade, Inc., Torbalı-İzmir, Turkey), 36 g of potato puree (Knorr, Unilever Co., Ümraniye, İstanbul, Turkey), 0.8 g l-ascorbic acid (Carlo Erba Reagents S.A.S), 7.72 ml of nipagin (p-hydroxybenzoic acid methyl ester, crystal; Sigma-Aldrich Co., St. Louis, MO) prepared in 3.5% ethanol and 1,000 ml of water. The methods used to prepare and transfer diets into containers, and the methods used to obtain eggs and larvae and their placement onto diets were described previously by Aslan et al. (2019).

Penicillin G (benzylpenicillin sodium salt, 96–102.0%, water soluble, Sigma-Aldrich Co.) was added to diets to establish concentrations of 100, 200, 400, and 800 mg/L. This antibiotic is water soluble and was added directly to the diet preparation in a weight per volume basis. The control was the diet without penicillin added. These penicillin concentrations were determined according to previous studies on the effect of other antibiotics on D. melanogaster (Aslan et al. 2019, Graf and Benz 1970).

Survivorship and development duration. Twenty-five neonates from the stock colonies were transferred into 5 ml of diet, which was then poured into small 15-ml glass bottles. By using a soft-tipped brush, 25 larvae were placed on control and treatment diets. Bottles were covered with hydrophilic cotton. These were held in incubators maintained at 25 ± 2°C and 60–70% RH on a 12:12-h light:dark photoperiod. We noted that third-instar larvae migrated from the diet to the inside surface of the glass container where they pupated. Newly formed pupae were marked on the external surface of the glass and recorded. Survivorship to the third instar, pupal stage, and adult stage was calculated as a percentage of the total number of neonates initially introduced into each rearing bottle. The duration of the developmental period was determined and is expressed by the time in days to reach the third instar, the pupal stage, and the adult stage. The five treatments were replicated four times with 25 larvae per replication (bottle).

Adult longevity. In a separate test, newly emerged adults were placed individually into bottles containing 5 ml of the respective diets with 0, 100, 200, 400, and 800 mg/L of penicillin. Treatments were replicated four times with 25 adults per replicate. These were maintained as previously described. Diets were changed daily. When adults died, the date of death was noted and survival time was noted and reported as adult longevity. Observations were made and mortality recorded in each container until all adults had expired.

Statistical analysis. The developmental duration and adult longevity data were subjected to a one-way analysis of variance (SPSS 1997). Where appropriate, treatment means were separated using the least significance difference. The χ2 test (Snedecor and Cochran 1989) was used to assess significant differences among the survivorship treatments.

All penicillin concentrations added to the artificial diet significantly reduced the survival rate to the third larval instar, the pupal stage, and the adult stage (Table 1). For example, survivorship to the third instar was 91.00 ± 3.27% for the control diet, 75.00 ± 0.86% for the 100 mg/L diet (χ2 = 9.072; df = 1; P = 0.0026), 55.00 ± 4.55% for the 200 mg/L of diet (χ2 = 32.877; df = 1; P= 0.0001), 34.00 ± 1.00% for the 400 mg/L of diet (χ2 = 69.312; df = 1; P = 0.0001), and 11.00 ± 2.59% for the 800 mg/L of diet (χ2 = 128.051; df = 1; P = 0.0001). Survivorship to the pupal and adult stages was very similar for each diet treatment (Table 1).

Table 1

Mean ± SE survivorship and developmental time of Drosophila melanogaster in response to increasing concentrations of penicillin G in larval diet.*

Mean ± SE survivorship and developmental time of Drosophila melanogaster in response to increasing concentrations of penicillin G in larval diet.*
Mean ± SE survivorship and developmental time of Drosophila melanogaster in response to increasing concentrations of penicillin G in larval diet.*

Developmental duration also was impacted by penicillin-treated diet. On the control diet lacking penicillin, the developmental period from neonate to third instar was 3.01 ± 0.01 d, from neonate to pupae was 4.03 ± 0.08 d, and from neonate to adult emergence was 8.12 ± 0.08 d (Table 1). Feeding on the diet containing 400 mg/L of diet significantly extended the developmental duration from neonate to third instar to 3.45 ± 0.08 d (F= 17.229; df = 4; P= 0.014), while there was no significant impact on duration to pupation (F= 2.636; df = 4; P= 0.094) or adult emergence (F = 2.004; df = 4; P = 0.480). When fed the diet containing the highest concentration of penicillin (800 mg/L), development to third instar was extended to 4.35 ± 0.18 d (F = 17.229; df = 4; P = 0.0001), development to pupation was 4.95 ± 0.27 d (F = 2.636; df = 4; P= 0.017), and development to adult emergence was 11.12 ± 1.28 d (F = 2.004; df = 4; P = 0.032) (Table 1). Adult longevity was decreased with exposure to diet containing penicillin with the following results, ranging from greatest to lowest: 0 mg/L > 100 mg/L > 200 mg/L > 400 mg/L > 800 mg/L (F = 960.047; df = 4; P = 0.0001) (Fig. 1).

Fig. 1

Effects of penicillin on the adult longevity of Drosophila melanogaster. Each column represents the mean of four treatment groups; 25 adults were used for each group. The different lowercase letters above each bar indicates that the treatment means were significantly different from each other, P < 0.05 (least significant difference).

Fig. 1

Effects of penicillin on the adult longevity of Drosophila melanogaster. Each column represents the mean of four treatment groups; 25 adults were used for each group. The different lowercase letters above each bar indicates that the treatment means were significantly different from each other, P < 0.05 (least significant difference).

Close modal

Recently, research on the effects of clinically important antibacterial, antifungal, antiviral, and anthelmintic agents used in the treatment of infectious and parasitic diseases of humans and animals has intensified. This study showed that an antibacterial antibiotic, penicillin, has a negative effect on the biological parameters of D. melanogaster at high dietary concentrations. Penicillin added to the diet is not known to be effective on insects with its own mode of action; therefore, the antibiotic is presumed to have a different mode of action on these insects. Biochemical studies should be conducted in conjunction with studies of changes in biological parameters to fully elucidate the mode of action.

The effect of penicillin on survivorship and development of D. melanogaster up to adult stage varies according to the larval, pupal, and adult stages of the insect and dietary concentrations of the antibiotic. The high concentrations of penicillin (400 and 800 mg/L) added to the diet reduced the survivorship rate at different stages of D. melanogaster and significantly increased the developmental time. The severe negative effect was recorded for the highest antibiotic concentration. Aslan et al. (2019) demonstrated that different antibiotic substances had a negative impact on D. melanogaster, similar to the effect of penicillin we observed in our study. Similar to the results of previous studies, high dietary concentrations of penicillin reduced the survivorship in larval, pupal, and adult stages and delayed development of D. melanogaster. As suggested in an earlier study (Büyükgüzel and Yazgan 1996), penicillin can be expected to interfere with the nutritional components of the diet and alter the quality of the artificial diet. As this situation may change the diet consumption rate of larvae, the survival rate of the insect towards the adult stage may be decreased and its development may be delayed. The deterioration in the balance of the components of the diet taken in the larval stage as a result of decreased nutritional quality impairs biological properties of adults reared on this diet (Slansky and Scriber 1985) and antioxidant enzymatic defense is adversely affected (Nielsen and Toft 2002). The results obtained in these studies support our postulation.

Under laboratory conditions, insect rearing studies have focused mainly on lepidopterans, likely because of the damage that these insects cause to plants of economic importance. A variety of artificial diets have been developed and used for the purpose of rearing these insects in the laboratory without using natural hosts. Because microbial contamination is frequently encountered in the artificial diets, antimicrobial agents have been routinely used largely for management or prevention of bacterial contaminants (Çelik et al. 2019, Clark et al. 1985, Costa et al. 1997, Kılıç et al. 2015). However, especially when they were used for this purpose, their high dietary concentrations had negative effects on insects. Similar results obtained in our study were recorded on different insects reared with various antibiotics. A dipteran, Agria affinis (Fallén) (Diptera: Sarcophagidae), is grown with diets containing different antibacterial and antifungal antibiotics including penicillin G (Singh and House 1970). Grenier (1977) showed that the survival rate of the larvae was significantly reduced when a parasitic species, Phryxe caudata (Rondani) (Diptera: Tachinidae), is reared on the diet with methyl p-hydroxybenzoate (nipagin M, 0.01, 0.04, and 0.1%). Some traditional antibacterial antibiotics, such as penicillin, streptomycin, and rifampicin at high concentrations, have adversely affected the survivorship and development of Pimpla turionellae L., an endoparasitoid hymenopteran (Büyükgüzel and Yazgan 1996). Many antimicrobial agents, including penicillin G, streptomycin sulfate, and some antifungals, prolonged the developmental time of the lepidopteran Galleria mellonella L. and decreased the survival rate in postlarval stages (Büyükgüzel and Kalender 2007, 2008). Some of our studies indicate reduced survivorship and prolonged development when P. turionellae was reared with novobiocin, an antibacterial antibiotic that inhibits DNA synthesis (Büyükgüzel 2001). Some conventional antifungals, such as nistatin, cycloheximide, and sodium benzoate, increased mortality in pupal and adult stages of the egg parasitoid Trichogramma dendrolimi Matsumura, while another antifungal agent, methyl p-hydroxybenzoate, had no significant effect (Grenier and Liu 1990, 1991; Xie et al. 1986). Similar to the results of these studies, penicillin showed such an effect in D. melanogaster in our study. These similar reactions and results suggest that different antibiotics are effective in insects with a similar mechanism.

In the present study, coincident with these negative effects on survival rate, adult longevity was reduced in a dose-related manner. The adverse effect on the life parameters of D. melanogaster may be attributed to a reduction of diet quality due to penicillin. The nutritional quality of diets that is consumed in the larval stage impacts postlarval developmental stages of many insects, especially the adult stage (May et al. 2015). Many studies have shown that toxic or nutritionally unsuitable diets led to decreases in various life-table parameters of the insect (Aslan et al. 2019, Güneş and Büyükgüzel 2017, Üstündağ et al. 2019). Üstündağ et al. (2019) indicated that a significant decrease was observed in D. melanogaster adult longevity with the increasing dietary niclosamide concentration. Aslan et al. (2019) also found that lower concentrations of gemifloxacin prolonged D. melanogaster male and female longevity, whereas the highest concentration of this antibiotic reduced longevity. It also has been shown that gemifloxacin decreased survivorship and has a retarding effect on the developmental period of this fruit fly as the concentrations in the diets increased. Güneş and Büyükgüzel (2017) showed that boric acid feeding at high concentrations in all developmental stages of D. melanogaster is more effective on oxidative stress indicators and detoxification enzymes. They suggested that low concentrations of boric acid may be added to the adult nutrient as an ingredient to improve the capacity of D. melanogaster adults; however, potential cell damages due to oxidative stress should be considered. Severe effects of penicillin at high concentration on survivorship, development, and adult longevity in our study may be attributed to impairment of nutritional quality of diets by penicillin. We need further experiments to prove this suggestion and other biochemical analyses to determine other modes of action of penicillin on deteriorated life cycle parameters of the insect.

This study may also be evaluated in terms of insect nutrition, as in some other studies on insects belonging to different groups (Heys et al. 2018, Thakur et al. 2016). It will also lead to the identification of low dietary concentrations that have minimum negative effects on insects and their gut microbiota, but that prevent microbial contaminations in artificial diet. In this study, some biochemical, toxicological, and physiological studies should be performed in order to fully elucidate the mechanism of penicillin at both ineffective low concentrations and at high concentrations that cause negative effects on the insect. As stated by Thakur et al. (2016), although the biological properties of the insect are not adversely affected by the antibiotic, there may be changes in the activities of antioxidant defense enzymes and detoxification enzymes for adaptation to the tested concentrations of the antibiotic. As suggested in previous studies with antibiotics and anthelmintics (Aslan et al. 2019, Büyükgüzel and Büyükgüzel 2019, Çalık et al. 2016, Çelik et al. 2019, Harmancı et al. 2019, Hız et al. 2016, Kılıç et al. 2015), further investigations are needed to determine the mechanism by which penicillin exerts a negative effect on insects. As Büyükgüzel and Büyükgüzel (2016a, 2016b) also emphasized for the antiviral agent acyclovir, regardless of the mechanism of action of the antibiotic, the concentration of antibacterial, antifungal, antiviral, and anthelmintic drug active ingredients, which are clinically important additions to larval diets for preventing contamination, should be carefully determined by considering their effects on other parameters such as adult fitness as well as preadult survival and developmental parameters.

This study was supported by Zonguldak Bülent Ecevit University, Research Fund (Project Number: 2019-84906727-03).

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