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Biology of the predatory fly Coenosia tigrina (Fab.) (Diptera: Anthomyiidae): reproduction, development, and larval feeding on earthworms in the laboratory
Abstract and Figures
Adults of the anthomyiid Coenosia tigrina (Fab.), which are predators of flying insects including pest Diptera such as the onion maggot fly, feed on earthworms in the larval stage. The bionomics of C. tigrina females were studied in the laboratory at 15, 20, and 25°C, under different mating regimes. Adult female longevity slightly exceeded 1 month at 25°C and was close to 2 months at 15°C. Oviposition started 1–3 weeks after emergence, the delay tending to decrease with increased male presence. Females laid eggs at intervals of 1 to several days, in batches averaging 10–30 eggs depending on temperature. Fecundity reached an average of 230 eggs at 25°C with the sustained presence of males. Egg hatch decreased with the mother’s age, except when males were present for most of the female’s lifetime. Females exhibited maximal daily rate of predation at 25°C, but maximal lifetime predation was observed at 20°C. Male predation was less than females’, and female predation decreased with age. The time to eclosion decreased from 11 to 5 days as the temperature of egg incubation increased from 15 to 25°C. Larval weight at eclosion decreased with mother’s age. Postembryonic development and larval growth were studied at 15, 20, and 25°C, larvae being fed on four lumbricids. Development times decreased with increasing temperature between 15 and 25°C: from 35 to 15 days for larval development, and 28 to 12 days for pupal development. Males developed at a slower rate than females, but females weighed more at emergence. Larval survival was 30–60% on worm sections, and dropped to 17% on live mature Eisenia foetida (Sav.); but survival reached 90% on live, immature E. foetida 1–2 cm long. The larvae of C. tigrina penetrate the epidermis of earthworms, and feed internally with a preference for circulatory and chlorogogonous tissues.
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... The treatment with one pair per cage gave poor results, with only 32.5% of the cages producing adults. With just one male in a cage, there may be a high risk of failure in the mating or fertilization processes, as Morris & Cloutier (1987) report that Coenosia tigrina (Fabricius, 1775) females occasionally refuse males that attempt to mate with them. In addition, 100% of the cages with 5 and 10 pairs produced Fig. 1. ...
... 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. Our predators lived longer, possibly because they had a better food supply and the temperature was lower, since Morris & Cloutier (1987) report that C. tigrina longevity is significantly reduced by an increase in temperature, even from 20 to 25°C. ...
... Future studies should determine the optimum ratio of males to females instead of using pairs. According to Morris & Cloutier (1987), multiple copulations are recorded for both sexes of C. tigrina and a male is able to successfully fertilize six females. Another point that needs further study is the relative merits of using an M substrate obtained by mixing soil and coconut fibre after fungus gnats have been separately added to the soil and coconut fibre versus one in which the soil and coconut fibre are mixed together before the fungus gnats are added, which avoids any potential injury to the fungus gnat larvae during the mixing process. ...
The tiger-fly Coenosia attenuata Stein (Diptera: Muscidae) is a predator that is currently thought to be a useful biological control agent in greenhouses, especially in the Mediterranean region. Here, we present a method for rearing this predator in the laboratory by feeding it on fungus gnats (fed on Pleurotus ostreatus fungus) and drosophilids (Diptera). Over the past two years, this method has been continuously used to successfully produce predators for bioecological studies in the laboratory. Rearing cages with one, five or 10 male-female pairs, either of laboratory or field origin, were compared using females that were either unmated and recently emerged, or mated and about 20 days old (post-emergence). We evaluated the following parameters: number of rearing cages in which adults emerged, number and sex ratio of emerged adults, period from the introduction of parental pairs into cages and the emergence of the first offspring adults, and the period over which emergence occurred in the cages. Based on our results and in order to minimize the space needed for the colony, cages should be stocked with ca. 10 parental pairs, either of field or laboratory origin, with at least some mated females about 20 days post emergence. We also found that the predator's rearing substrate in the cages is improved if coconut fibre is mixed with the soil. These findings will improve the efficiency of C. attenuata rearing, an important step if it is to be used as a biological control agent.
... This species is adapted to high temperatures (Gilioli et al., 2005) , which is important for surviving inside Mediterranean greenhouses. It also kills more prey than it consumes, making it an effi cient biological control agent (Morris & Cloutier, 1987;Martinez & Cocquempot, 2000). Laboratory studies indicate that it prefers whitefl ies and leafminers to other species usually present in protected crops (Martins et al., 2012) . ...
... Based on previous observations this predator is very voracious and able to capture large numbers of prey. In some situations, only some of them are actually consumed (Morris & Cloutier, 1987;Moreschi & Süss, 1998) (Figueiredo et al., 2016). The higher the number of prey consumed the expectation is that the detectability times for particular prey species is increased, which means that the detection times obtained in this study are likely underestimated comparing to what happens in fi eld settings. ...
The tiger-fly Coenosia attenuata Stein (Diptera: Muscidae: Coenosiini) is a generalist predator that preys on several pests of greenhouse crops and is considered a biological control agent in the Mediterranean region. Previous behavioural observations identified its preferred prey, but a more in-depth evaluation will benefit from using Polymerase Chain Reaction amplification of prey DNA remains in the gut of this predator. To evaluate the rate of decay and suitability of this method for use in the field assessments, we carried out a laboratory feeding calibration experiment on 355 females of C. attenuata, which were killed at different intervals of time after ingestion (10 time points from 0 to 48 h). The prey species tested were: Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae: Trialeurodini), Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae), Diglyphus isaea (Walker) (Hymenoptera: Eulophidae: Cirrospilini), Bradysia impatiens (Johannsen) (Diptera: Sciaridae) and Drosophila mercatorum Patterson & Wheeler (Diptera: Drosophilidae: Drosophilini). Based on a probit model, amplification success of prey DNA declined exponentially with increasing time after ingestion. The half-time molecular detection differed between species, ranging from an average of 5 h for T. vaporariorum and D. isaea, 6 h for B. impatiens, 15 h for L. huidobrensis to more than 40 h for D. mercatorum. This study confirmed the feasibility of using DNA based detection to identify prey species in the gut contents of C. attenuata and provided calibration curves for a better understanding of predation activity in this agroecosystem.
... According to Fabian et al. (2018), adult C. attenuata employ an interception strategy and uses a navigational constant of N ≈ 1.5 with a time delay of ≈ 18 ms to intercept targets, which is a complicated strategy, but also more energy efficient allowing C. attenuata to cope with the extremely high line-of-sight rotation rates and thus prevents overcompensation of steering. Additionally, it has been reported to kill more prey than it can consume (Martinez and Cocquempot 2000) as a result of a so called "predation instinct" (Morris and Cloutier 1987;Moreschi and Süss 1998). Furthermore, C. attenuata has been reported as having little impact on natural enemies (Téllez and Tapia 2006;Garcia 2011;Martins et al. 2012;Ndiaye et al. 2015). ...
... Santos et al. (2013) reported that the tiger-fly larvae fed on the bisected earthworm portions but seem to have difficulty to penetrate in the cuticle of the alive and moving Lumbricus terrestris Linnaeus, 1758 (Opisthopora: Lumbricidae). Work by Yahnke and George (1972) and Morris and Cloutier (1987) with Coenosia tigrina (Fabricius, 1775) (Diptera: Muscidae) suggests that live, immature E. fetida may be a better food source. Rearing on prekilled European corn borer, Ostrinia nubilalis (Hübner, 1796) (Lepidoptera: Crambidae), was only slightly more successful, yielding a 94.5% mortality rate and a larval developmental period averaging 20 d (Moreschi and Süss 1998). ...
The performance of the tiger-fly Coenosia attenuata Stein was examined when fed on larvae of the buzzer midge, Chironomus plumosus (Linnaeus), and combination of buzzer midge and fungus gnat, Bradysia impatiens (Johannsen). Significant differences were observed in the developmental time of larvae, body length, and body weight of pupae and adults of C. attenuata in response to species and preservation status of prey but not in response to instar and prey number of C. plumosus. Most biological characteristics except for developmental time of pupae, length of female pupae, survival rate from the 5th day to pupation, and adult emergence improved for tiger-fly larvae fed on live B. impatiens larvae in the first four days and live C. plumosus larvae from the fifth day to pupation compared to those fed on live C. plumosus larvae in all larval stages. When live alternative prey were replaced with the frozen prey, the developmental time of larvae was prolonged, and adult male body length, survival rate from the fifth day to pupation, and the percentages of pupation and adult emergence decreased. The survival rate of larvae in the first 4 days and percentage of pupation improved with decreased alternative prey instar and increased alternative prey number. These results indicate live C. plumosus larvae can serve as an alternative food source for mass rearing of C. attenuata. As an alternative food source, C. plumosus larvae provide significant advancements for the application of tiger-fly in banker media system and/or open rearing.
... Although predatory flights only accounted for around 6% of the total flights in C. attenuata, >60% of such flights resulted in successful prey capture. Coenosia tigrina (Fabricius) females displayed a higher frequency of predatory flights (Morris & Cloutier, 1987). Territorial defense flights, detected in C. attenuata for the first time, occurred at a low frequency but were more common than predatory flights, highlighting the high energetic investment in this activity. ...
... Additional research in a greenhouse environment is needed to further our understanding of the interactions between predator larvae and their prey in soil (Ugine et al., 2010). The length of the life cycle and the emergence rate of C. attenuata are related to biotic and abiotic factors such as prey availability, temperature, and soil moisture (Moreschi & S€ uss, 1998;Moreschi & Colombo, 1999;T ellez et al., 2009), and an adequate prey supply is essential for ensuring a regular mating system, fertile eggs, and larval development, as reported by Morris & Cloutier (1987) for C. tigrina. Increasing predator-species richness in the greenhouse environment may help in achieving more effective pest control, although the effects of species richness are density dependent (Griffiths et al., 2008). ...
Adults of the predatory fly Coenosia attenuata Stein (Diptera: Muscidae) catch their prey while in flight. I investigated this activity over two seasons in a tomato greenhouse naturally infested with Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae). The flight of C. attenuata individuals was affected by environmental factors and was increased in response to increases in temperature, the number of prey flights, and conspecific density. Predator and prey flights were distributed throughout the day, but there was a regular daily trend, each with two partially overlapping activity peaks. The possibility of predation was limited by differences in daily flight-activity times. Predatory flights comprised a small percentage (ca. 6%) of the total flights, with a predation success rate of 61%. Overall, the predatory activity of C. attenuata depended on the selection of hunting sites with good visibility to ensure a clear view before take-off and allow the capture of prey in flight. Similar numbers of overall flights were made by both sexes, but C. attenuata females performed more predation flights and territorial defense activities than males. The ecological role of C. attenuata and its limited adaptability to greenhouses is discussed in light of its possible use in biological control of whiteflies.
... The pupal stage lasted 16-45 days. Besides, in Canada, Morris & Cloutier (1987) bred larvae from earthworms of the species A. chlorotica, A. rosea, Aporrecteda sp. and E. fetida in the laboratory. The larvae were observed to penetrate the epidermis and feed inside the worm. ...
A comprehensive review of all earthworm-parasitizing genera within the Oestroidea superfamily (namely Bellardia Robineau-Desvoidy, Calliphora Robineau-Desvoidy, Onesia Robineau-Desvoidy, Pollenia Robineau-Desvoidy and Sarcophaga Meigen) was conducted, including a list of rearing records found in the SMNS (Staatliches Museum für Naturkunde Stuttgart, Germany) and NHMUK (Natural History Museum, London, UK) collections. Sarcophaga flies and earthworms were collected in the field at eight localities around Stuttgart (Germany). Besides, a morphological and molecular analysis (using COI DNA-barcoding) of Sarcophaga (Sarcophaga) carnaria (Linnaeus), S. (S.) variegata (Scopoli) and S. (S.) subvicina Rohdendorf was performed to revise existing identification keys. In total, 126 males and 54 females were used for the morphological analysis, and 51 females were identified using DNA-barcoding. The review showed that some species of Bellardia, Onesia, Pollenia and Sarcophaga (s. str.) can be considered as earthworm endoparasitoids. Due to the lack of recorded observations, species of Calliphora could not be confirmed as earthworm parasitoids. In total, 172 Sarcophaga specimens belonging to twelve species were collected in the field, and one living earthworm was found infected with three larvae of S. variegata. Dissected females of S. subvicina can be split from S. carnaria and S. variegata by exhibiting a length/width ratio of sternite 7 greater than 0.9 (smaller than 0.9 in S. carnaria and S. variegata). Females of S. carnaria could not be reliably differentiated morphologically from those of S. variegata. The distributions of dusting and setation on syntergosternite 7+8 could not be confirmed as sufficiently reliable characters to differentiate male S. subvicina from S. carnaria and S. variegata, as used in a previously published key.
... 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. ...
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.
... Like C. attenuata, the adults of C. tigrina significantly reduce the population of greenhouse pests (Perron et al. 1956, Hobby 1931 and also attack the larvae of the onion maggot fly, Delia antiqua (Meigen, 1826) (LeRoux & Perron 1960, Perron & LaFrance 1952. Larvae of C. tigrina have been observed to feed on the lumbricid earthworm Eisenia rosea (Savigny, 1826) by penetrating the epidermis of their hosts (Morris & Pivnick 1991, Morris & Cloutier 1987, Yahnke & George 1972). ...
An identification key to the seven known Iranian species of the genus Coenosia Meigen, 1826 is given, including Coenosia
persica Pont & Parchami-Araghi, sp. nov. as well as the newly recorded C. humilis Meigen, 1826, C. nigridigita Rondani,
1866 and C. testacea (Robineau-Desvoidy, 1830). Photographs of the habitus and male genitalia of the studied material
in addition to illustrations of the male genitalia of the new species are provided.
... For example, C. attenuata is active over a wide range of temperatures (from ≈ 12 to 42°C) (Gilioli et al. 2005). Additionally, it has been reported to kill more prey than it can consume (Martinez and Cocquempot 2000) as a result of a so called Bpredation instinct ( Morris and Cloutier 1987;Moreschi and Süss 1998). ...
The development of immature tiger-fly Coenosia attenuata (Stein) was examined when reared in coir substrate and fed third-instar larvae of the fungus gnat Bradysia impatiens (Johannsen). Single larvae of C. attenuata were fed 3, 5, 7 and 9 prey per day and two larvae were fed 6, 10, 14 and 18 prey per day. Optimal prey density was determined for larval developmental rate, time to adult eclosion, larval survival, and percentage of pupation. Other biological characteristics, such as pupal weight, pupal length, and adult body length, continued to increase with an increase in prey density. The use of coir for a rearing substrate resulted in a more efficient use of prey, less cannibalism, and improved developmental time, and survival than previously reported when agarose gel or a mixture of soil and coir were used for rearing substrates. These improvements in rearing methods are significant advancements for the use of C. attenuata as a biological control agent against whiteflies, leaf miners, fungus gnats and winged-aphids. Additionally, coir substrate serves as a mulch layer when fungus gnats are controlled with C. attenuata, such as Bradysia odoriphaga (Yang et Zhang) in Chinese chive, and B. impatiens in potted ornamental plants.
... Como larva predam artrópodos presentes no solo. O adulto nutre-se de insectos voadores, tais como aleirodídeos, esciarídeos e agromizídeos, atacando apenas presas em movimento (Morris & Cloutier, 1987). Por apresentar tais hábitos predatórios, o género Coenosia assume um papel de particular importância como auxiliar no combate a diversos fitófagos de culturas protegidas (Moreschi, 1999). ...
In theoretical and experimental approaches to the study of sperm competition, it is often assumed that ejaculates always contain enough sperm of good quality and that they are successfully transferred and used for fertilization. However, this view neglects the potential effects of infertility and sperm limitation. Permanent or temporal male infertility due to male sterility, insemination failures, or failures to fertilize the ova implies that some males do not achieve sperm representation in the female reproductive tract after mating. A review of the literature suggests that rates of nonsperm representation may be high; values for the proportion of infertile matings across 30 insect species vary between 0% and 63%, with the median being 22%. I simulated P2 (the proportion of offspring fathered by the second male to copulate with a female in a double‐mating trial) distributions under a mechanism of random sperm mixing when sample sizes and rates of male infertility varied. The results show that nonsperm representation can be responsible for high intraspecific variance in sperm precedence patterns and that it can generate misleading interpretations about the mechanism of sperm competition. Nonsperm representation might be a common obstacle in the studies of sperm competition and postcopulatory female choice.
The earthworm Lumbricus terrestris is widespread and abundant. Its biomass may reach 1000 kg ha −1, and > 20 worms m −2 may surface simultaneously at night. Earthworms are thus potentially available to subterranean predators, to those that dig them up and those which catch them on the surface. Earthworm tissue has a high protein content and is rich in essential amino acids (Sabine, Chapter 24). It contains a considerable amount of fat variously estimated it 1.5%(Lawrence and Millar, 1945),4.6%(French et al., 1957) and 17.3 /~ (Durchon and Lafon, 1951) and this is reflected in a high energy content of about 22.24 kJg−1 dry wt, (Bolton and Phillipson, 1976). This abundant food resource is utilized by diverse predators and for some of them is seasonally the principal food. Earthworms feature in the diets of hundreds of species of terrestrial vertebrates but the adaptations of these predators to securing earthworms as prey have been studied in very few of them. This chapter reviews (a) a selection of studies of the importance of earthworms in the diets of sympatric species, (b) the few studies that have investigated predation on Lumbricus, and (c) the relationships between the ecology of the earthworm and the behaviour and social organization of these predators.
In laboratory tests, Ravinia lherminieri (Robineau-Desvoidy) larvae significantly reduced the numbers of face fly, Musca autumnalis De Geer, eggs or larvae (98% mortality), in 100 ml of bovine feces at R. lherminieri to face fly ratios down to 10:200. Face fly immature mortality due to R. lherminieri decreased from 98% to 0% as the volume of feces per larva increased from 10 ml to 80 ml. Although R. lherminieri larvae survived on feces alone, their survival increased 26% (63% vs. 89%) when face fly immatures were added to the feces.
Parasitism by Pollenia rudis (Fabr.) larvae on earthworms in the field was found only in Allolobophora chlorotica (Sav.) and Eisenia rosea (Sav.). Other species of worms were infected in the laboratory. Slime and coelomic fluid, from all species of worms tested, induced penetration behaviour. Penetration occurs mainly on the dorsal surface of the worm, and less frequently towards either end. Larvae repenetrated after leaving the original penetration site. Autonomy by the host of the parasitized segments was observed in E. rosea. Possible reasons for the restricted natural host range are discussed.
The percentage of first-instar cluster-fly larvae successfully penetrating their earthworm hosts, Eisenia rosea (Sav.), remained quite constant at 13 °C when ratios of larvae to worms were from 7.5:1 to 0.5:1. Larvae descended into undisturbed soil only by following naturally occurring pore spaces (inter-ped spaces or those caused by vegetation or earthworms). In disturbed soil lacking natural pores, few earthworms were penetrated by the larvae, partly due to earthworm behaviour of blocking their burrows with casts. The significance of soil conditions and other factors as it affects this parasitic relationship is discussed.
Coenosia tigrina (F.), an important anthomyiid predator of the onion maggot, Hylemya antiqua (Meig.), in Quebec, was found in all stages of development in field populations of the latter. The species was named by Fabricius (1775). A description of the adult was given by Perron et al. , 1956, but no description of the immature stages is available. This is a report on the external morphology of the immature stages of this species, the determination of the overwintering sites of the larvae, and the effect of predation by adults on adult H. antiqua in field cages.
In investigations on the life-history of the onion maggot at St. Jean, Que., in 1951, a few specimens of a dipterous predator were found in the rearing cages in the laboratory. They were feeding voraciously on the adults, destroying a colony of nearly 300 flies within two weeks.
Specimens were identified by Mr. A. R. Brooks, Systematic Entomology, Division of Entomology, Saskatoon, Sask., as
Coenosia tigrina
(F.). Mr. G. E. Shewell, Systematic Entomology, Division of Entomology, Ottawa, has stated that nothing is known in Canada about the life-history of this species, but that it is apparently well known as a predator in Europe and that B. M. Hobby has published a long list of species on which it preys, including many anthomyiids.
Coenosia tigrina (F.) was first observed in Canada in 1943 at Ottawa by Mr. A. R. Brooks of the Entomology Division (Mr. G. E. Shewell, Entomology Division, Ottawa, personal communication). By 1917 the insect had been collected as far west as Guelph, Ontario. It was first recorded from the province of Quebec in 1951 by Perron and Lafrance (1952), who observed it preying on adults of Hylemya antiqua (Mg.) in rearing cages at St. Jean. Later observations and surveys by these workers indicated the predator to be very abundant in southwestern Quebec. More recently Mr. F. M. Cannon (personal communication), Field Crop Insect Section, Science Service Laboratory, Charlottetown, Prince Edward Island, and Mr. L. A. Miller (personal communication), Entomology Laboratory, Chatham, Ont., reported C. tigrina to be present as far east as Charlottetown and as far west as Chatham.