Next Article in Journal
Factors Influencing the Distribution of Endemic Damselflies in Vanuatu
Next Article in Special Issue
Growth Performance, Waste Reduction Efficiency and Nutritional Composition of Black Soldier Fly (Hermetia illucens) Larvae and Prepupae Reared on Coconut Endosperm and Soybean Curd Residue with or without Supplementation
Previous Article in Journal
Two Complete Mitochondrial Genomes of Mileewinae (Hemiptera: Cicadellidae) and a Phylogenetic Analysis
Previous Article in Special Issue
The Influence of Food Waste Rearing Substrates on Black Soldier Fly Larvae Protein Composition: A Systematic Review
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effect of Prey Species and Prey Densities on the Performance of Adult Coenosia attenuata

1
Biological Control of Insects Research Laboratory, Institute of Plant Protection, Tianjin Academy of Agricultural Sciences, Tianjin 300384, China
2
Biological Control of Insects Research Laboratory, USDA–Agricultural Research Service, Columbia, MO 65203, USA
3
Key Laboratory of Integrated Pest Management in Crops, Ministry of Agriculture, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
4
College of Horticulture and Landscape, Tianjin Agricultural University, Tianjin 300392, China
*
Author to whom correspondence should be addressed.
Insects 2021, 12(8), 669; https://doi.org/10.3390/insects12080669
Submission received: 31 May 2021 / Revised: 10 July 2021 / Accepted: 21 July 2021 / Published: 23 July 2021

Abstract

:

Simple Summary

The predaceous fly Coenosia attenuata Stein has received attention because of its ability to effectively suppress a wide range of agricultural pests, such as fungus gnats, whiteflies and leaf miners. An effective level of control requires large numbers of C. attenuata to be available at low cost for release. Adult fungus gnats and drosophilids are now the main prey used to rear C. attenuata adults. However, previous studies showed C. attenuata fertility is lower when fed drosophilids compared to fungus gnats. The current study investigated the performance of C. attenuata adults when reared on different densities of adult Drosophila melanogaster Meigen or Bradysia impatiens (Johannsem). Results showed that the optimal prey density in the mass rearing of adult C. attenuata was 12–24 adult B. impatiens daily per predator. Additionally, C. attenuata adults suffered more wing damage, at some of the prey densities, when reared on D. melanogaster compared to B. impatiens. This information will be used to optimize rearing methods and decrease the cost of mass rearing in C. attenuata.

Abstract

Mass production of Coenosia attenuata Stein at low cost is very important for their use as a biological control agent. The present study reports the performance of C. attenuata adults when reared on Drosophila melanogaster Meigen or Bradysia impatiens (Johannsem). Different densities (6, 9, 15, 24 and 36 adults per predator) of D. melanogaster or (6, 12, 24, 36 and 48 adults per predator) of B. impatiens were used at 26 ± 1 °C, 14:10 (L:D) and 70 ± 5% RH. The results concluded that C. attenuata adults had higher fecundity, longer longevity and less wing damage when reared on B. impatiens adults compared to D. melanogaster adults. Additionally, C. attenuata adults demonstrated greater difficulty catching and carrying heavier D. melanogaster adults than lighter B. impatiens adults. In this case, 12 to 24 adults of B. impatiens daily per predator were considered optimal prey density in the mass rearing of adult C. attenuata.

1. Introduction

The predaceous fly Coenosia attenuata Stein (Diptera: Muscidae), also known as “tiger fly”, “killer fly” or “hunter fly” [1,2,3,4], is native to Southern Europe [4,5] and has been reported to have spontaneously colonized a number of crops outdoors and in greenhouses in many countries worldwide [5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21]. It has received attention because of its ability to effectively suppress a wide range of agricultural pests, such as fungus gnats (Diptera: Sciaridae), whiteflies (Hemiptera: Aleyrodidae), leaf miners (Diptera: Agromyzidae), winged aphids (Hemiptera: Aphididae), leafhoppers of the genera Eupteryx (Hemiptera: Cicadellidae) and Empoasca (Hemiptera: Cicadellidae), midges (Diptera: Chironomidae), moth flies (Diptera: Psychodidae), shore flies (Diptera: Ephydridae) and fruit flies (Diptera: Drosophilidae) [7,8,13,22,23,24,25,26,27,28,29,30,31,32,33,34,35]. The wide range of prey used as food make the tiger-fly an attractive alternative to conventional control methods.
Intact wings play an important role in the life of C. attenuata adults. Adults of C. attenuata catch their prey while in flight and pursue targets at the range of 23–212 mm. Hence, they employ an interception strategy that is more energy efficient to intercept targets, which allows C. attenuata to cope with the extremely high line-of-sight rotation rates and thus prevents overcompensation of steering [36]. Adults of C. attenuata use mean flight speeds of 0.69 ms1, mean wingbeat frequency of 306, 19 Hz and acceleration of mean peak 9.3 ms2 to intercept prey [36]. The flight of C. attenuata individuals is affected by environmental factors, adjusting in response to changes in temperature, the number of prey flights and conspecific density [37]. Therefore, wing damage will cause negative effects on the life of C. attenuata adults.
Mass rearing of C. attenuata is important given the environmental, health and resistance issues associated with the use of chemical insecticides. To achieve an effective level of control, however, requires the production of a large number of C. attenuata at low cost. Adults of fungus gnat and drosophilid are now the main prey used to rear C. attenuata adults [17,23,38,39]. Rearing drosophilids is quick, easy and not particularly expensive. However, they were used primarily as a complement to the fungus gnat diet because C. attenuata fertility is lower when fed drosophilids compared to fungus gnats [23]. The reason why the performance of C. attenuata reared on drosophilids is lower than those reared on fungus gnats have not been assessed. The present study reports our finding that C. attenuata adults had less wing damage, higher fecundity and longer longevity when reared on Bradysia impatiens (Johannsem) (Diptera: Sciaridae) compared to Drosophila melanogaster Meigen (Diptera: Drosophilidae).

2. Materials and Methods

2.1. Vinegar Flies

The vinegar fly, D. melanogaster were reared on bananas in open plastic canisters (about 1200 cm3) in tissue bags (40 × 30 cm2, 0.4-mm mesh openings) closed with binder clips. Adults were introduced into the tissue bags and the adults of the following generation started to emerge after ca. 11 days. The colony was maintained in a laboratory incubator and held at 26 ± 1 °C, 14:10 (L:D) and 70 ± 5% RH.

2.2. Fungus Gnats

A colony of fungus gnats was initiated with about 400 B. impatiens adults captured from a greenhouse at Wuqing Experiment Station (Tianjin, China). Fungus gnats were reared using the method very similar to that reported by Zou et al. (2021) [39]. Modifications were made to simplify and improve the processes of rearing and collecting fungus gnats for use in bioassays. Briefly, 300 mL of black peat (Lvdimeijing Science and Technology Co., Ltd., Beijing, China) and 55 to 60 g of dry kidney bean powder were placed in an open plastic box (25.5 × 19 × 7.8 cm3). The mix was then moistened with 250 mL of tap water and 0.2-cm thick layer of moist coir (Shanghai Galuku Agricultural Science and Technology Co., Ltd. Shanghai, China; desalted, EC = 0.5, family pack, common grade) was placed on the top of the mix. Then the open plastic box was placed in a tissue bag (50 × 35 cm2, 0.4-mm mesh openings). In this case, 400 to 500 newly emerged adult fungus gnats were placed in the tissue bag and closed with a binder clip. Fresh rearing medium was prepared daily and new cultures were set up daily.
The new fungus gnat adults deposited eggs on the media consisted of black peat, tap water and kidney bean powder. Newly hatched larvae fed on the media and adults emerged after 18–22 d. The colony was maintained in a laboratory incubator and held at 26 ± 1 °C, 14:10 (L:D) and 70 ± 5% RH.

2.3. Tiger-Fly

The C. attenuata used to establish a laboratory colony in this study were collected at Leizhuangzi flower farm of Tianjin, China. Adults were provided an oviposition tissue cage (60 × 55 × 50 cm3), in which an open plastic box (29 × 20 × 7 cm3) containing black peat, tap water, kidney bean powder and eggs of B. impatiens. A 0.5-cm thick layer of moist coir was placed on the top of the rearing media and used for oviposition. B. impatiens and D. melanogaster adults were supplied as prey daily. Five to 6 days later, the plastic boxes containing eggs of C. attenuata and rearing media were removed to another cage and second and third instar larvae of B. impatiens were added to the box to feed larvae of C. attenuata. Distilled water was added to the box when the media became dry. About 20 to 21 days later, adults of C. attenuata emerged. The colony was maintained in an artificial climate chamber and held at 26 ± 1 °C, 14:10 (L:D) and 70 ± 5% RH.

2.4. Performance of Tiger-Fly Adults Reared on Different Prey Species at Different Prey Densities

Five female/male pairs of newly emerged adults of C. attenuata (<24-h-old), in the first generation that originated from field-caught adults, were transferred into tissue cages (60 × 55 × 50 cm3) containing an open 90-mm-diameter Petri dish containing of 0.7-cm thick layer of moist coir for oviposition. The moist coir was replenished after collecting egg daily. Two 110 cm strings were hung inside each cage and served as a perch for adult predators. In this case, 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens (<24-h-old) were provided daily per predator adult. Prey were used only once and fresh prey were added daily. Five female/male pairs of C. attenuata adults (in one cage) were tested until death in each treatment and replicated 9 times. In total, 45 pairs of C. attenuata adults were tested in each treatment within a phytotron held at 26 ± 1 °C, 14:10 (L:D) and 70 ± 5% RH. Wing damage in C. attenuata adults was measured daily using a Mitutoyo 500-196-30 digital caliper (Mitutoyo, Kawasaki, Japan). Wing damage occurred along the long axis of wing. The extent of damage was calculated as a percentage using the length of damaged wing/the total length of wing × 100%. Both wings were assessed and the average was taken. The numbers of surviving and killed prey were recorded daily. Eggs deposited in the moist coir were collected and counted from each cage daily using a 00-sized paintbrush. They were then placed in 60-mm-diameter Petri dishes containing a single 55-mm-diameter filter paper, moistened with distilled water, sealed with Parafilm and inverted to keep the eggs moist. Hatch occurred ca. 6 days after oviposition and egg viability was calculated. Distilled water was sprayed to each tissue cage two times in the morning and afternoon per day. Tiger-flies were maintained in this manner until death.

2.5. Comparation of Body Weight and Body Length in C. attenuata, D. Melanogaster and B. Impatiens

The adults of C. attenuata caught prey in flight. So carrying prey with different body weights may cause different levels of wing damage for adults of C. attenuata. Adults of C. attenuata (<24-h-old) and D. melanogaster (<24-h-old) were placed in tissue bags (40 × 30 cm2) and held in a Siemens BCD-501W fridge (Siemens, Nanjing, China) at −20 °C for 2 min before taking body length and weight measurements. Adults of B. impatiens (<24-h-old) were handled in the same way with C. attenuata and D. melanogaster and held at −20 °C for 3 min before using. Adult body length was measured (in resting position) from the apex of the head to the wing tip for C. attenuata and D. melanogaster. For B. impatiens, body length was measured (in resting position) from the apex of the head to the abdomen tip. Body length measurements were made using a Mitutoyo 500-196-30 digital caliper (Mitutoyo, Kawasaki, Japan). Weight measurements were made using a Sartorius BP 211D (Sartorius AG, Göttingen, Germany) balance. In this case, 30 females and 30 males were measured for each species.

2.6. Statistical Analyses

One-way ANOVA with subsequent Tukey’s HSD test at α = 0.05 was used to compare the proportion of damaged wing, number of prey killed, preovipositional period, total fecundity between different prey densities, body weight and body length between insect species. To avoid possible mistakes due to multiple testing of the same data base, the p-values were Bonferroni corrected. Two sample t-tests for means were used to compare proportion of damaged wing, preovipositional period and total fecundity between prey species. These comparisons were carried out on day 4 and the last day. The proportion of eggs successfully hatched was compared between treatments by the Chi-square test at α = 0.01. All the statistical tests were carried out using SAS version 9.4.

3. Results

3.1. Comparison of Wing Damage of C. attenuata When Reared on Different Prey at Different Prey Densities

The mean proportion of damaged wings of C. attenuata females fed on D. melanogaster and males fed on B. impatiens or D. melanogaster did not differ significantly between prey densities at early ages (day 4) (F4, 220 = 1.27, p = 0.2826; F4, 220 = 1.55, p = 0.1886; F4, 220 = 2.4, p = 0.0513, respectively) (Figure 1B–D). However, C. attenuata females fed 48 adults of B. impatiens daily lost more wings compared with those fed 12 adults of B. impatiens daily on day 4 (F1, 88 = 9.39, p = 0.0029, Bonferroni-corrected p = 0.005) (Figure 1A). The wing damage increased with age in every case, but at different rates depending on prey species and density. When fed with B. impatiens, C. attenuata females showed significant differences at late age (31 days) between prey densities of 12 and 24 (F1, 88 = 13.15, p = 0.0004, Bonferroni-corrected p = 0.005), or between prey densities of 36 and 48 (F1, 88 = 10.16, p = 0.002, Bonferroni-corrected p = 0.005) (Figure 1A). For C. attenuata males, there were no significant differences between prey densities at late age (19 days) (F4, 220 = 0.63, p = 0.6425) (Figure 1B). When fed with D. melanogaster, both females and males of C. coenosia did not show significantly different wing damage between prey densities at later age (8 days) (F4, 220 = 2.08, p = 0.0848; F4, 220 = 2.07, p = 0.0856, respectively) (Figure 1C,D).
Females and males of C. attenuata had much shorter longevity when fed D. melanogaster adults compared to those fed B. impatiens adults (maximum age of 12 for D. melanogaster and of 46 for B. impatiens in females; maximum age of 10 for D. melanogaster and of 35 for B. impatiens in males). Mean proportion of wing damage in flies fed with B. impatiens at age 8 ranged from 3.25 to 22.42% in females and from 4.68 to 9.58% in males, while in flies fed with D. melanogaster it ranged from 12.28 to 21.56% in females and from 9.16 to 19.77% in males (Figure 1).
C. attenuata females fed 6 adults of D. melanogaster daily lost significantly more wings than those fed 6 adults of B. impatiens daily on day 4 (t = −2.935, df = 88, p = 0.0043) (Figure 1A,C). However, there was no significant difference in wing damage for C. attenuata females fed 24 adults of D. melanogaster compared with those fed 24 adults of B. impatiens daily, or for C. attenuata females fed 36 adults of D. melanogaster compared with those fed 36 adults of B. impatiens daily on day 4 (t = −1.934, df = 88, p = 0.0564; t = −0.447, df = 88, p = 0.6561, respectively) (Figure 1A,C). C. attenuata females lost significantly more wings when fed adults of D. melanogaster daily compared to B. impatiens at the prey density of 6 and 36 on day 8 (t = −4.556, df = 88, p < 0.0001; t = 2.803, df = 88, p = 0.0062, respectively). However, there was no significant difference in wing damage for C. attenuata females when fed 24 adults of D. melanogaster compared with those fed 24 adults of B. impatiens on day 8 (t = −0.874, df = 88, p = 0.3847) (Figure 1A,C).
There was no significant difference in wing damage for C. attenuata males fed 6 adults of D. melanogaster compared with those fed 6 adults of B. impatiens, or for C. attenuata males fed 36 adults of D. melanogaster compared with those fed 36 adults of B. impatiens on day 4 (t = −1.35, df = 88, p = 0.1805; t = −1.1, df = 88, p = 0.2743, respectively) (Figure 1B,D). C. attenuata males lost significantly more wings when fed adults of D. melanogaster daily compared to B. impatiens at the prey density of 24 on day 4 (t = −2.302, df = 88, p = 0.0237) and the prey density of 6 on day 8 (t = −2.631, df = 88, p = 0.01). However, there was no significant difference in wing damage for C. attenuata males when fed adults of D. melanogaster daily compared to B. impatiens at the prey density of 24 or 36 on day 8 (t = −0.362, df = 88, p = 0.7181; t = −0.482, df = 88, p = 0.6311, respectively) (Figure 1B,D).

3.2. Number of Prey killed by C. attenuata Reared on Different Prey at Different Prey Densities

C. attenuata adults killed all B. impatiens adults when fed 6 prey daily per predator adult except for the last 3 days, which suggests 6 adults of B. impatiens are not enough for C. attenuata adults (Figure 2). Most of B. impatiens adults were killed by C. attenuata adults when fed 12 prey daily per predator adult. The number of prey killed by C. attenuata adults fluctuated when fed 24, 36 and 48 prey daily per predator adult. The numbers of prey killed per predator daily were 15.33 to 23.77, 25.99 to 35.70 and 33.00 to 47.45 for C. attenuata adults fed 24, 36 and 48 prey daily per predator adult, respectively. The number of prey killed daily per predator decreased in the last few days with the increase of age and the mean proportion of damaged wings for C. attenuata adults fed 12, 24, 36 and 48 prey daily per predator adult (Figure 2). The number of B. impatiens adults killed daily per predator adult differed significantly between prey densities at early ages (day 4) (p < 0.0001 for 9 comparisons), except for densities of 24 vs. 36 (F1, 16 = 5.61, p = 0.0308, Bonferroni-corrected p = 0.005) (Figure 2). At later age (day 31), the number of B. impatiens adults killed daily per predator adult differed significantly between prey densities (p < 0.0001 for 9 comparisons), except for densities of 36 vs. 48 (F1, 4 = 0.26, p = 0.6392, Bonferroni-corrected p = 0.005) (Figure 2).
C. attenuata adults killed 3.17 to 4.52 D. melanogaster adults when fed 6 prey adults daily per predator adult (Figure 3). The number of prey killed by C. attenuata adults fluctuated when fed 9, 15, 24 and 36 prey daily per predator adult. The numbers of prey killed daily per predator were 4.27 to 6.54, 4.37 to 7.29, 7.57 to 11.98 and 9.58 to 15.55 for C. attenuata adults fed 9, 15, 24 and 36 prey daily per predator adult, respectively. The number of prey killed per predator daily decreased in the last few days with the increase of age and the proportion of broken wings for C. attenuata adults in all treatments. The number of D. melanogaster adults killed daily per predator adult differed significantly with prey densities of 6 vs. 9 (F1, 16 = 10.64, p = 0.0049, Bonferroni-corrected p = 0.005), 9 vs. 36 (F1, 16 = 17.21, p = 0.0008, Bonferroni-corrected p = 0.005) and with the prey densities of 6 vs. 15, 6 vs. 24, 6 vs. 36 and 15 vs. 36 (all p < 0.0001) at early ages (day 4). No significant differences were found in the other 4 comparisons at early ages (day 4) (Figure 3). Additionally, no significant differences were found in all 10 comparisons at later age (day 8) (Figure 3).

3.3. Preovipositional Period of C. attenuata Female Reared on Different Prey at Different Prey Densities

There were no significant differences in preovipositional period in any of the treatments of C. attenuata females when fed 6, 9, 15, 24 or 36 adults of D. melanogaster prey (F4, 40 = 2.43, p = 0.064) (Figure 4). The preovipositional period of C. attenuata female was from 4.22 to 5.22 days when fed D. melanogaster prey. Similar, there were no significant differences in preovipositional period in any of the treatments of C. attenuata females when fed 6, 12, 24, 36 or 48 adults of B. impatiens (F4, 40 = 1.73, p = 0.162). The preovipositional period of C. attenuata female was from 3.89 to 4.67 days when fed B. impatiens prey. There were no significant differences in the preovipositional period for C. attenuata females when fed 6 adults of D. melanogaster prey or 6 adults of B. impatiens prey, or for C. attenuata females when fed 36 adults of D. melanogaster prey or 36 adults of B. impatiens prey (t = −0.686, df = 16, p = 0.5025; t = −1.715, df = 16, p = 0.1056, respectively) (Figure 4). The preovipositional periods were significantly longer for C. attenuata females fed 24 adults of D. melanogaster prey than of C. attenuata females fed 24 adults of B. impatiens prey. These differences, although statistically significant, were small (t = −2.132, df = 16, p = 0.0489) (Figure 4).

3.4. Total Fecundity of C. attenuata Female Reared on Different Prey at Different Prey Densities

The total fecundity per female of C. attenuata fed D. melanogaster prey differed significantly with prey densities of 6 vs. 36 (F1, 16 = 17.38, p = 0.0007, Bonferroni-corrected p = 0.005), 9 vs. 36 (F1, 16 = 19.82, p = 0.0004, Bonferroni-corrected p = 0.005), 24 vs. 36 (F1, 16 = 18.90, p = 0.0005, Bonferroni-corrected p = 0.005) and the other 4 comparisons (6 vs. 9, 6 vs. 15, 6 vs. 24 and 15 vs. 36, all p < 0.0001). No significant differences were found in other 3 comparisons (Figure 5). The total fecundity per female of C. attenuata fed B. impatiens prey did not differ significantly with prey densities of 6 vs. 48 and 12 vs. 36 (F1, 16 = 0.17, p = 0.6829; F1, 16 = 9.54, p = 0.007, respectively, Bonferroni-corrected p = 0.005). However, the total fecundity per female of C. attenuata fed B. impatiens prey differed significantly between prey densities for the other 8 comparisons (all p < 0.0001) (Figure 5). Additionally, the total fecundity was much higher for females of C. attenuata fed B. impatiens adults than for those fed D. melanogaster prey at the same prey densities of 6, 24 and 36 (t = 31.971, df = 16, p < 0.0001; t = 36.609, df = 16, p < 0.0001; t = 32.954, df = 16, p < 0.0001, respectively).

3.5. Proportion of Eggs Successfully Hatched in C. attenuata Reared on Different Prey at Different Prey Densities

There was a significantly higher proportion of eggs that successfully hatched for C. attenuata fed 9 adults of D. melanogaster than for those fed 24 and 36 adults of D. melanogaster daily per predator adult (χ2 = 8.37, p = 0.004; χ2 = 20.56, p < 0.0001, respectively) (Figure 6). However, there were no significant differences in the proportion of eggs that successfully hatched between C. attenuata fed 9 adults of D. melanogaster and those fed 6 or 15 adults of D. melanogaster2 = 6.36, p = 0.012; χ2 = 0.81, p = 0.368, respectively). There were no significant differences in proportion of eggs successfully hatched between C. attenuata fed 24 adults of B. impatiens and those fed 6, 12 or 36 adults of B. impatiens2 = 5.97, p = 0.015; χ2 = 1.28, p = 0.257; χ2 = 2.92, p = 0.087, respectively). The proportion of eggs that successfully hatched was significantly higher for C. attenuata fed 24 adults of B. impatiens than for those fed 48 adults of B. impatiens daily per predator adult (χ2 = 6.87, p = 0.009). Additionally, the proportion of eggs that successfully hatched was much higher for C. attenuata adults fed B. impatiens adults than for those fed D. melanogaster adults at the same prey densities of 6, 24 and 36 (χ2 = 15.14, p < 0.0001; χ2 = 43.35, p < 0.0001; χ2 = 43.26, p < 0.0001, respectively).

3.6. Comparation of Body Weight and Body Length in C. attenuata, D. melanogaster and B. impatiens

Adult females of C. attenuata were significantly longer than those of D. melanogaster and B. impatiens (F2, 87 = 1335.80, p < 0.0001) (Table 1). Adult females of D. melanogaster were significantly longer than those of B. impatiens (F2, 87 = 1335.80, p < 0.0001). Similar, adult males of C. attenuata were significantly longer than those of D. melanogaster and B. impatiens (F2, 87 = 2101.27, p < 0.0001) and the body length was significantly longer for adult males of D. melanogaster than for adult males of B. impatiens (F2, 87 = 2101.27, p < 0.0001).
Adult females of C. attenuata were significantly heavier than those of D. melanogaster and B. impatiens and there was a significant difference in the body weight of adult females between D. melanogaster and B. impatiens (F2, 87 = 2188.57, p < 0.0001). Similar, adult males of C. attenuata were significantly heavier than those of D. melanogaster and B. impatiens and there was a significant difference in the body weight of adult males between D. melanogaster and B. impatiens (F2, 87 = 1164.34, p < 0.0001) (Table 1).

4. Discussion

The flight of C. attenuata individuals was affected by environmental factors and was increased in response to increases in the number of prey flights [37]. Bonsignore (2016) found that predatory flights of adult C. attenuata comprised a small percentage (ca. 6%) of the total flights, with a predation success rate of 61% [37]. In our study, the mean proportion of damaged wings of C. attenuata females when fed 6, 12, 24 and 36 adults of B. impatiens daily per predator adult was increased in response to increases in the number of prey densities. However, the mean proportion of wing damage in C. attenuata females was lower for prey densities of 48 adults of B. impatiens than for prey densities of 36. The high density of 48 adults of B. impatiens probably increased the predation success rate and thereby decreased the mean proportion of damaged wings of C. attenuata female although the tiger-fly is regarded to have predation instinct [40,41]. Damaged wings of C. attenuata males fed on B. impatiens continued to increase with an increase in age of C. attenuata. However, the mean proportions of damaged wings in C. attenuata males were not consistent with those of females. Prey density did not cause significant effect on wing damage for C. attenuata males, which suggests prey density was not the only factor affecting wing damage in C. attenuata males. Being attacked by female C. attenuata and attempting to mate with female C. attenuata could also influence wing damage. Additionally, male adults required less prey compared to female adults, which means low prey densities could increase the predation success rate and thereby decreased the proportion of damaged wings of C. attenuata males. According to the damaged wings and longevity of C. attenuata adults, prey densities of 12 to 24 should be optimal density for mass rearing of adult C. attenuata.
Prey density of vinegar fly did not cause a significant effect on the mean proportion of damaged wings in both female and male adults of C. attenuata. It seems reasonable to conclude that the short lifespan of the tiger-fly was too short to manifest an effect of D. melanogaster prey density on wing damage of C. attenuata adults. C. attenuata adults fed D. melanogaster prey daily lost more wings compared to those fed B. impatiens prey at the same age for some prey density. This may be related to the increased difficulty in carrying heavier D. melanogaster adults than B. impatiens adults.
Bonsignore (2016) sorted adult C. attenuata flights into three groups, movement flights, territory defense flights and predatory flights in greenhouse [37]. However, we observed that there should be another type of flight, escape flights in cage. We hypothesize that adult C. attenuata want to escape from the cage when encountering high density of prey, resulting in less wing damage. Escaping from the environment with high prey density may be a self-protection response for adult C. attenuata.
We found that females lived longer than males, as reported by Kühne et al. (1997) [23]. However, these authors record 38 days and 33 days as the maximum female and male longevity, respectively, under laboratory conditions (25 °C and 50–60% RH) and an estimated longevity of eight weeks under greenhouse conditions. Predators fed B. impatiens adults in our study lived 46 days and 35 days as the maximum female and male longevity, respectively, possibly because they had a better food supply. However, in our study, predators fed adult D. melanogaster flies lived only 12 days and 10 days as the maximum female and male longevity, respectively. We speculate that C. attenuata adults were able to more easily capture lighter B. impatiens adults than heavier adult D. melanogaster. Additionally, adult C. attenuata were able to attack adult B. impatiens on the bottom of cage when they could only jump or crawl because of damaged wings. However, it is difficult for C. attenuata with damaged wings to capture adult D. melanogaster.
Female adult C. attenuata were found to exhibit a type I functional response to adult sciarid flies, which was conducted in glass vials 8 cm long and 8 cm in diameter at 25 °C at 60–80% RH, with a 16L:8D photoperiod. Sciarids were consumed in significantly different numbers at densities from 5 to 20 individuals (the number of killed flies changed from 2.90 to 8.4, respectively). However, increasing prey availability beyond 20 individuals resulted in no substantial increase in predation [30]. However, female adult C. attenuata were found to exhibit a type II functional response to adult D. melanogaster flies, which was conducted in Plexiglas cages with a dimension of 25 by 25 by 25 cm at 30 °C at 65 ± 5% RH, with a 12L:12D photoperiod. D. melanogaster flies were consumed in significantly different numbers at densities from 5 to 55 individuals (the number of attacked flies changed from 3.50 to 5.67, respectively) [42]. Kühne (2000) states that each adult C. attenuata needs either 1.5 adults of D. melanogaster or 6.9 adults of B. impatiens per day [25]. We did not analyze the functional response to adult B. impatiens or D. melanogaster flies because more than one factor affected functional response, such as intraspecific competition and predation. The number of killed prey in our study was more than those mentioned above, which was probably caused by intraspecific competition and predation instinct resulting from cage and space differences. The flight ability of adult B. impatiens is weak and often some of them stayed on the bottom of cage which made it more convenient for adult C. attenuata without flight ability, because of damaged wings, to catch the adult B. impatiens. In contrast, the flight ability of adult D. melanogaster is strong and it is more difficult for adult C. attenuata with weakened flight ability to catch adult D. melanogaster, although adult C. attenuata has been proved to be more efficient in information sampling and processing than adult D. melanogaster [43,44].
The preoviposition period of C. attenuata is approximately 4 days [23]. Our reports showed similar preoviposition periods when fed adults of B. impatiens with 3.89–4.67 days and adults of D. melanogaster with 4.22–5.22 days. Prey density, prey species and damaged wings did not cause negative effects on the preoviposition period of C. attenuata. Sanderson et al. (2009) found the tiger-flies laid more eggs with fungus gnat prey than shore fly prey [27]. We found that the tiger-flies laid much more eggs with fungus gnat prey than vinegar fly prey. However, the total fecundity per female of C. attenuata did not continue to increase with an increase in prey density. Shorter life span probably cause the lower fecundity for C. attenuata female when fed adult D. melanogaster compared to adult B. impatiens. Martins et al. (2015) presented an optimized method for mass rearing C. attenuata with fungus gnats and Drosophilids as prey, where the number of adults that emerged per parental pair ranged from 1.8 to 9.0 (= per pair progeny production, or the number of adult offspring that emerged in each cage divided by the number of parental pairs) [38]. In our study, the number of adult offspring that emerged ranged from 4.96 to 7.64 and 21.16 to 39.27 at least for per parental pair when fed adult D. melanogaster and B. impatiens, respectively according to survival rates of larvae, percentages of pupation and adult emergence in our previous reports [17,39]. The proportion of eggs that successfully hatched was much higher for C. attenuata adults fed B. impatiens adults than for those fed D. melanogaster adults at the same prey densities. Longer longevity in male C. attenuata and lighter body weight in B. impatiens prey correlated to increased proportion of eggs that successfully hatched in C. attenuata.
Predation by adult C. attenuata is rapid, and adults take off as soon as they observe their prey in flight, although they do not know the absolute size of the potential prey prior to the flight [45]. One important physical factor affecting predator responses is prey size [46]. Body length and body weight of adult C. attenuata, D. melanogaster and B. impatiens were analyzed in our study to better understand the complexity of predation. We report body length and body weight of adult C. attenuata from Tianjin to be similar to those reported by us previously [17,39] and to those reported in Uruguay where the C. attenuata flies measured approximately 2.5–5.00 mm in length [47]. Body weight of adult D. melanogaster measured in this study is similar to those reported by Chen et al. (2019) [48]. Body length of adult B. impatiens analyzed in this study is similar to those reported by Wilkinson and Daugherty (1970) [49]. Obviously, it is more difficult for adult C. attenuata to catch and carry heavier adult D. melanogaster than lighter adult B. impatiens. Most importantly, it is more difficult for male adult C. attenuata to catch and carry female adult D. melanogaster, that are 74.15% weight of male adult of C. attenuata than to catch adult female B. impatiens that only weigh 28.57% of their weight.
In our study, we demonstrated that adult B. impatiens was an optimal prey in the mass rearing of adult C. attenuata although rearing drosophilids is quick, easy and not particularly expensive. In addition, we provide evidence that damage to wings of adult C. attenuata when fed adult D. melanogaster vs. B. impatiens is an important consideration for prey selection. We conclude a prey density of 12–24 adult fungus gnats daily per adult predator as optimal for mass rearing of adult C. attenuata. Rearing cost, nutritional difference, digestion efficiency, chemical, morphological and behavioral defense mechanisms of a prey will be explored in future studies.

5. Conclusions

We present the first report of wing damage for C. attenuata adults when reared on different prey. The results indicate that C. attenuata adults had higher fecundity, longer longevity and generally less wing damage when reared on B. impatiens compared to D. melanogaster. Lighter body weight and weaker flight ability in adult B. impatiens prey likely contributed to prolonged longevity and increased fecundity in adult C. attenuata. In this case, 12 to 24 adults of B. impatiens daily per predator were considered optimal prey density in the mass rearing of adult C. attenuata adult.

Author Contributions

Conceptualization, D.Z. and H.W.; methodology, D.Z., L.Z. and H.W.; software, W.X. and J.X.; validation, D.Z., T.A.C., L.Z., W.X., J.X. and H.W.; formal analysis, D.Z. and L.Z.; investigation, D.Z., M.W. and X.X.; resources, W.X. and H.W.; data curation, D.Z., M.W., X.X. and H.W.; writing—original draft preparation, D.Z.; writing—review and editing, T.A.C., L.Z., W.X., J.X. and H.W.; visualization, D.Z., T.A.C., L.Z., W.X., J.X. and H.W.; supervision, H.W.; project administration, D.Z., J.X. and X.X.; funding acquisition, D.Z., T.A.C., L.Z., W.X. and H.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Science and Technology Innovation Foundation for Young Scientists of Tianjin Academy of Agricultural Sciences (No. 201911), National Key Research and Development Program of China (No. 2017YFD0201000, 2017YFD0201707) and the USDA Agricultural Research Service project Insect Biotechnology Products for Pest Control and Emerging Needs in Agriculture (No. 5070-22000-037-00-D).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank Wan-Qi Xue (Shenyang Normal University, China) for helping in species identification.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript or in the decision to publish the results. USDA is an equal opportunity provider and employer. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

References

  1. Cock, M.J.W. Bemisia Tabaci, an Update 1986–1992 on the Cotton Whitefly with an Annotated Bibliography; CAB International Institute of Biological Control: Ascot, UK, 1993; p. 78. [Google Scholar]
  2. Gerling, D.; Alomar, O.; Arn, J. Biological control of Bemisia tabaci using predators and parasitoids. Protection 2001, 20, 779–799. [Google Scholar] [CrossRef]
  3. Parrela, M.P. Biological control in protected culture: Will it continue to expand? Phytoparasitica 2008, 3, 3–6. [Google Scholar] [CrossRef]
  4. Seabra, S.G.; Brás, P.G.; Martins, J.; Martins, R.; Wyatt, N.; Shirazi, J.; Rebelo, M.T.; Franco, J.C.; Mateus, C.; Figueiredo, E.; et al. Phylogeographical patterns in Coenosia attenuata (Diptera: Muscidae): A widespread predator of insect species associated with greenhouse crops. Biol. J. Linnean Soc. 2015, 114, 308–326. [Google Scholar] [CrossRef] [Green Version]
  5. Hennig, W. Muscidae. In Die Fliegen der Palaearktischen Region; Lindner, E., Ed.; Schweizerbart’sche Verlagsbuchhandlung: Stuttgart, Germany, 1964; Volume 7. [Google Scholar]
  6. Colombo, M.; Eördegh, F.R. Discovery of Coenosia attenuata, an active predator on aleyrodids, in protected crops in Liguria and Lombardia. L’Informatore Agrar. 1990, 47, 187–189. [Google Scholar]
  7. Kühne, S. Open rearing of generalist predators: A strategy for improvement of biological pest control in greenhouses. Phytoparasitica 1998, 26, 277–281. [Google Scholar] [CrossRef]
  8. Martinez, M.; Cocquempot, C. La mouche Coenosia attenuata nouvel auxiliaire prometteur en culture protégée. PHM-Rev. Hortic. 2000, 414, 50–52. [Google Scholar]
  9. Rodríguez-Rodríguez, M.D.; Aguilera, A. Coenosia attenuata, una nueva mosca a considerar en el control biológico de las plagas horticólas. Phytoma España 2002, 141, 27–34. [Google Scholar]
  10. Hoebeke, E.R.; Sensenbach, E.J.; Sanderson, J.P. First report of Coenosia attenuata Stein (Diptera: Muscidae), an old world ‘hunter fly’ in North America. Proc. Entomol. Soc. Wash. 2003, 105, 769–775. [Google Scholar]
  11. Pohl, D.; Uygur, F.N.; Sauerborn, J. Fluctuations in population of the first recorded predatory fly Coenosia attenuata in cotton fields in Turkey. Phytoparasitica 2003, 31, 446–449. [Google Scholar] [CrossRef]
  12. Xue, W.Q.; Tong, Y.F. A taxonomic study on Coenoia tigrina species-group (Diptera: Muscidae) in China. Entomol. Sin. 2003, 10, 281–290. [Google Scholar]
  13. Pohl, D.; Kühne, S.; Karaca, İ.; Moll, E. Review of Coenosia attenuata Stein and its first record as a predator of important greenhouse pests in Turkey. Phytoparasitica 2012, 40, 63–68. [Google Scholar] [CrossRef]
  14. Ndiaye, O.; Ndiaye, S.; Djiba, S.; Ba, C.T.; Vaughan, L.; Rey, J.-Y.; Vayssières, J.-F. Preliminary surveys after release of the fruit fly parasitoid Fopius arisanus Sonan (Hymenoptera Braconidae) in mango production systems in Casamance (Senegal). Fruit 2015, 70, 91–99. [Google Scholar] [CrossRef]
  15. Téllez, M.M.; Tapia, G. Acción depredadora de Coenosia attenuata Stein (Díptera: Muscidae) sobre otros enemigos naturales en condiciones de laboratorio. Bol. San. Veg. Plagas 2006, 32, 491–498. [Google Scholar]
  16. Zou, D.Y. Current research status of key natural enemies in Tianjin. Chin. Rur. Sci. Technol. 2015, 10, 38–39. [Google Scholar]
  17. Zou, D.Y.; Coudron, T.A.; Xu, W.H.; Gu, X.S.; Wu, H.H. Development of immature tiger-fly Coenosia attenuata (Stein) reared on larvae of the fungus gnat Bradysia impatiens (Johannsen) in coir substrate. Phytoparasitica 2017, 45, 75–84. [Google Scholar] [CrossRef]
  18. Zou, D.Y.; Xu, W.H.; Liu, X.L.; Bai, Y.C.; Liu, B.M.; Xu, J.Y.; Hu, X.; Gu, X.S.; Wu, H.H. Coenosia attenuata Stein (Diptera: Muscidae): Research progress and prospects in biological control. J. Environ. Entomol. 2017, 39, 444–452. [Google Scholar]
  19. Bautista-Martínez, N.; Illescas-Riquelme, C.P.; García-Ávila, C.J. First report of “hunter-fly” Coenosia attenuata (Diptera: Muscidae) in Mexico. Fla. Entomol. 2017, 100, 174–175. [Google Scholar] [CrossRef]
  20. Solano-Rojas, Y.; Pont, A.; De Freitas, J.; Moros, G.; Goyo, Y. First record of Coenosia attenuata Stein, 1903 (Diptera: Muscidae) in Venezuela. An. Biol. 2017, 39, 223–226. [Google Scholar] [CrossRef]
  21. Couri, M.S.; Sousa, V.R.; Lima, R.M.; Dias-Pini, N.S. The predator Coenosia attenuata Stein (Diptera, Muscidae) on cultivated plants from Brazil. An. Acad. Bras. Ciênc. 2018, 90, 179–183. [Google Scholar] [CrossRef] [Green Version]
  22. Kühne, S.; Schrameyer, K.; Müller, R.; Menzel, F. Räuberische fliegen: Ein bisher wenig beachteter nützlingskomplex in Gewächshäusern. Mitt. Biol. Bundesanst. 1994, 302, 1–75. [Google Scholar]
  23. Kühne, S.; Schiller, K.; Dahl, U. Beitrag zur lebensweise, morphologie und entwicklungsdauer der räuberischen fliege Coenosia attenuata Stein (Diptera: Muscidae). Gesunde Pflanz. 1997, 49, 100–106. [Google Scholar]
  24. Moreschi, I.; Colombo, M. Una metódica per l’allevamento dei Ditteri predatori Coenosia attenuata e C. strigipes. Inf. Fitopatol. 1999, 49, 61–64. [Google Scholar]
  25. Kühne, S. Räuberische Fliegen der Gattung Coenosia Meigen, 1826 (Diptera: Muscidae) und die Möglichkeit ihres Einsatzes bei der biologischen Schädlingsbekämpfung. Stud. Dipterol. 2000, 9, 78. [Google Scholar]
  26. Prieto, R.; Figueiredo, E.; Mexia, A. Coenosia attenuata Stein (Diptera: Muscidae): Prospeccao e actividade em culturas protegidas em Portugal. Bol. San. Veg. Plagas 2005, 31, 39–45. [Google Scholar]
  27. Sanderson, J.; Ugine, T.; Wraight, S.; Sensenbach, E. Something for nothing: The beneficial hunter fly may be helping you manage pests. Growertalkers 2009, 73, 74–76. [Google Scholar]
  28. Sensenbach, E.J.; Wraight, S.P.; Sanderson, J.P. Biology and predatory feeding behavior of larvae of the hunter fly Coenosia attenuata. IOBC/WPRS B. 2005, 28, 229–232. [Google Scholar]
  29. Pinho, V.; Mateus, C.; Rebelo, M.T.; Kühne, S. Distribuição espacial de Coenosia attenuata Stein (Diptera: Muscidae) e das suas presas em estufas de hortícolas na região Oeste, Portugal. Bol. San. Veg. Plagas 2009, 35, 231–238. [Google Scholar]
  30. Téllez, M.D.M.; Tapia, G.; Gámez, M.; Cabello, T.; van Emden, H.F. Predation of Bradysia sp. (Diptera: Sciaridae), Liriomyza trifolii (Diptera: Agromyzidae) and Bemisia tabaci (Hemiptera: Aleyrodidae) by Coenosia attenuata (Diptera: Muscidae) in greenhouse crops. Eur. J. Entomol. 2009, 106, 199–204. [Google Scholar] [CrossRef]
  31. Kühne, S.; Heller, K. Sciarid fly larvae in growing media—Biology, occurrence, substrate and environmental effects and biological control measures. In Peat in Horticulture—Life in Growing Media; Schmilewski, G., Ed.; International Peat Society: Amsterdam, The Netherlands, 2010; pp. 95–102. [Google Scholar]
  32. Ugine, T.A.; Sensenbach, E.J.; Sanderson, J.P.; Wraight, S.P. Biology and feeding requirements of larval hunter flies Coenosia attenuata (Diptera: Muscidae) reared on larvae of the fungus gnat Bradysia impatiens (Diptera: Sciaridae). J. Econ. Entomol. 2010, 103, 1149–1158. [Google Scholar] [CrossRef]
  33. Martins, J.; Domingos, C.; Nunes, R.; Garcia, A.; Ramos, C.; Mateus, C.; Figueiredo, E. Coenosia attenuata (Diptera: Muscidae), um predador em estudo para utilização em culturas protegidas. Rev. Ciênc. Agrár. 2012, 35, 229–235. [Google Scholar]
  34. Mateus, C. Bioecology and behaviour of Coenosia attenuata in greenhouse vegetable crops in the Oeste region, Portugal. Bull. Insectol. 2012, 65, 257–263. [Google Scholar]
  35. Zou, D.Y.; Zhang, L.S.; Wu, H.H.; Gu, X.S.; Xu, W.H.; Liu, X.L. Population dynamics of Coenosia attenuata and prey in Tianjin. In Green Plant Protection and Rural Revitalization; Chen, W.Q., Zheng, C.L., Wen, L.P., Ni, H.X., Feng, L.Y., Eds.; China Agricultural Science and Technology Press: Beijing, China, 2018; pp. 171–172. [Google Scholar]
  36. Fabian, S.T.; Sumner, M.E.; Wardill, T.J.; Rossoni, S.; Gonzalez-Bellido, P.T. Interception by two predatory fly species is explained by a proportional navigation feedback controller. J. R. Soc. Interface 2018, 15, 20180466. [Google Scholar] [CrossRef] [Green Version]
  37. Bonsignore, C.P. Environmental factors affecting the behavior of Coenosia attenuata, a predator of Trialeurodes vaporariorum in tomato greenhouses. Entomol. Exp. Appl. 2016, 158, 87–96. [Google Scholar] [CrossRef]
  38. Martins, J.; Mateus, C.; Ramos, A.; Figueiredo, E. An optimized method for mass rearing the tiger-fly, Coenosia attenuata (Diptera: Muscidae). Eur. J. Entomol. 2015, 112, 470–476. [Google Scholar] [CrossRef] [Green Version]
  39. Zou, D.Y.; Coudron, T.A.; Xu, W.H.; Xu, J.Y.; Wu, H.H. Performance of the tiger-fly Coenosia attenuata Stein reared on the alternative prey, Chironomus plumosus (L.) larvae in coir substrate. Phytoparasitica 2021, 49, 83–92. [Google Scholar] [CrossRef]
  40. Morris, D.E.; Cloutier, C. Biology of the predatory fly Coenosia tigrina (Fab.) (Diptera: Anthomyiidae): Reproduction, development, and larval feeding on earthworms in the laboratory. Can. Entomol. 1987, 119, 381–393. [Google Scholar] [CrossRef]
  41. Moreschi, I.; Süss, L. Osservazioni biologiche ed etologiche su Coenosia attenuata Stein e Coenosia strigipes Stein (Diptera Muscidae). Boll. Zool. Agrar. Bachicol. 1998, 30, 185–197. [Google Scholar]
  42. Gilioli, G.; Baumgärtner, J.; Vacante, V. Temperature influences on functional response of Coenosia attenuata (Diptera: Muscidae) individuals. J. Econ. Entoml. 2005, 98, 1524–1530. [Google Scholar] [CrossRef]
  43. Gonzalez-Bellido, P.T.; Wardill, T.J.; Juusola, M. Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands. PNAS 2011, 108, 4224–4229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Song, Z.; Juusola, M. Refractory sampling links efficiency and cost of sensory encoding to stimulus statistics. J. Neurosci. 2014, 34, 7216–7237. [Google Scholar] [CrossRef] [Green Version]
  45. Wardill, T.J.; Gonzalez-Bellido, P.T.; Tapia, G.; Peng, H.; Olberg, R.M. The miniature dipteran killer fly Coenosia attenuata exhibits adaptable aerial prey capture strategies. In Proceedings of the International Conference on Invertebrate Vision, Fjälkinge, Sweden, 1–8 August 2013. [Google Scholar] [CrossRef]
  46. Sabeli, M.W. Predatory arthropods. In Natural Enemies; Crawley, M.J., Ed.; Blackwell Scientific: Oxford, UK, 1992; pp. 225–264. [Google Scholar]
  47. Giambiasi, M.; Rodríguez, A.; Arruabarrena, A.; Buenahora, J. First report of Coenosia attenuata (Stein, 1903) (Diptera, Muscidae) in Uruguay, confirmed by DNA barcode sequences. Check List 2020, 16, 749–752. [Google Scholar] [CrossRef]
  48. Chen, M.Y.; Liu, H.P.; Cheng, J.; Chiang, S.Y.; Liao, W.P.; Lin, W.Y. Transgenerational impact of DEHP on body weight of Drosophila. Chemosphere 2019, 221, 493–499. [Google Scholar] [CrossRef] [PubMed]
  49. Wilkinson, J.D.; Daugherty, D.M. The biology and immature stages of Bradysia impatiens (Diptera: Sciaridae). Ann. Entomol. Soc. Am. 1970, 63, 656–660. [Google Scholar] [CrossRef]
Figure 1. Mean proportion of damaged wings of all Coenosia attenuata when fed different prey at different densities daily per predator adult (mean values with 95% confidence intervals; error bars: 95% CI): (A) females fed 6, 12, 24, 36 and 48 adults of Bradysia impatiens; (B) males fed 6, 12, 24, 36 and 48 adults of Bradysia impatiens; (C) females fed 6, 9, 15, 24 and 36 adults of Drosophila melanogaster; (D) males fed 6, 9, 15, 24 and 36 adults of Drosophila melanogaster.
Figure 1. Mean proportion of damaged wings of all Coenosia attenuata when fed different prey at different densities daily per predator adult (mean values with 95% confidence intervals; error bars: 95% CI): (A) females fed 6, 12, 24, 36 and 48 adults of Bradysia impatiens; (B) males fed 6, 12, 24, 36 and 48 adults of Bradysia impatiens; (C) females fed 6, 9, 15, 24 and 36 adults of Drosophila melanogaster; (D) males fed 6, 9, 15, 24 and 36 adults of Drosophila melanogaster.
Insects 12 00669 g001
Figure 2. Mean number of prey killed per C. attenuata adult when fed 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult (values are mean ± SE, single values were present when only one adult C. attenuata was left in the end).
Figure 2. Mean number of prey killed per C. attenuata adult when fed 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult (values are mean ± SE, single values were present when only one adult C. attenuata was left in the end).
Insects 12 00669 g002
Figure 3. Mean number of prey killed per C. attenuata adult when fed 6, 9, 15, 24 and 36 adults of D. melanogaster daily per predator adult (values are mean ± SE, single values were present when only one adult C. attenuata was left in the end).
Figure 3. Mean number of prey killed per C. attenuata adult when fed 6, 9, 15, 24 and 36 adults of D. melanogaster daily per predator adult (values are mean ± SE, single values were present when only one adult C. attenuata was left in the end).
Insects 12 00669 g003
Figure 4. Preovipositional periods of C. attenuata female adult when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities using one-way ANOVA, Tukey’s HSD test (p = 0.05 and n = 9).
Figure 4. Preovipositional periods of C. attenuata female adult when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities using one-way ANOVA, Tukey’s HSD test (p = 0.05 and n = 9).
Insects 12 00669 g004
Figure 5. Total fecundity per female of C. attenuata when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities (corrected p value for multiple testing by Bonferroni correction is 0.005 and n = 9).
Figure 5. Total fecundity per female of C. attenuata when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities (corrected p value for multiple testing by Bonferroni correction is 0.005 and n = 9).
Insects 12 00669 g005
Figure 6. Proportion of eggs successfully hatched for C. attenuata when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities at a 0.01 level of significance using Chi-square test (n = 450, first 50 eggs were collected from each cage, 9 repetitions in each treatment).
Figure 6. Proportion of eggs successfully hatched for C. attenuata when fed 6, 9, 15, 24 and 36 adults of D. melanogaster and 6, 12, 24, 36 and 48 adults of B. impatiens daily per predator adult. Different letters above each bar indicate significant differences between prey densities at a 0.01 level of significance using Chi-square test (n = 450, first 50 eggs were collected from each cage, 9 repetitions in each treatment).
Insects 12 00669 g006
Table 1. Body length (mm) and body weight (mg) of adult Coenosia attenuata, Drosophila melanogaster and Bradysia impatiens (n = 30).
Table 1. Body length (mm) and body weight (mg) of adult Coenosia attenuata, Drosophila melanogaster and Bradysia impatiens (n = 30).
InsectsBody Length of Adult Female a (mm)Body Length of Adult Male a (mm)Body Weight of Adult Female b (mg)Body Weight of Adult Male b (mg)
Coenosia attenuata4.49 ± 0.04 a3.68 ± 0.02 a 2.52 ± 0.04 a 1.47 ± 0.03 a
Drosophila melanogaster3.12 ± 0.02 b2.78 ± 0.02 b1.09 ± 0.01 b0.72 ± 0.01 b
Bradysia impatiens2.22 ± 0.02 c1.70 ± 0.02 c0.42 ± 0.01 c0.23 ± 0.01 c
Values are mean ± SE. Means in columns with the same letter are not significantly different at a 0.05 level of significant. a Adult body length measured < 24 h after adult emergence. b Adult body weight measured < 24 h after adult emergence.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Zou, D.; Coudron, T.A.; Zhang, L.; Xu, W.; Xu, J.; Wang, M.; Xiao, X.; Wu, H. Effect of Prey Species and Prey Densities on the Performance of Adult Coenosia attenuata. Insects 2021, 12, 669. https://doi.org/10.3390/insects12080669

AMA Style

Zou D, Coudron TA, Zhang L, Xu W, Xu J, Wang M, Xiao X, Wu H. Effect of Prey Species and Prey Densities on the Performance of Adult Coenosia attenuata. Insects. 2021; 12(8):669. https://doi.org/10.3390/insects12080669

Chicago/Turabian Style

Zou, Deyu, Thomas A. Coudron, Lisheng Zhang, Weihong Xu, Jingyang Xu, Mengqing Wang, Xuezhuang Xiao, and Huihui Wu. 2021. "Effect of Prey Species and Prey Densities on the Performance of Adult Coenosia attenuata" Insects 12, no. 8: 669. https://doi.org/10.3390/insects12080669

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop