Us Como Predador De Musca

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A^/^ The Coleopterists Bulletin, 42(3):211-216. 1988.

ROLE OF THE LESSER MEALWORM, ALPHITOBIUS DIAPERINUS (PANZER) (COLEOPTERA: TENEBRIONIDAE), AS A PREDATOR OF THE HOUSE FLY, MUSCA DOMESTICA L. (DIPTERA: MUSCIDAE), IN POULTRY HOUSES’ JOSEPH L. DESPINS,2 JEFFERSON A. VAUGHAN,3

AND

E. CRAIG TURNER, JR.

Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. U.S.A.

ABSTRACT The role of the lesser mealworm, Alphitobius diaperinus (Panzer), as a predator of house fly Musca domeslica L., maggots and puparia in poultry houses is discussed. Late instar larval and adult A. diaperinus fed on house fly maggots when isolated together in glass vials. Lesser mealworm adults and middle instar larvae significantly reduced house fly emergence from apparatus which simulated the manure pit environment of high rise caged layer egg house.

The lesser mealworm, Alphitobius diaperinus (Panzer), is the most common coleopteran inhabiting high rise, caged layer houses during some times of the year (Pfeiffer and Axtell 1980), where it may be found in the upper 15 cm of the collected droppings in the manure pits of these houses (Green 1982). The insect is an omnivorous scavenger, feeding on material which falls into the manure pit, such as manure, spilled chicken feed, cracked eggs, and chicken carcasses. The lesser mealworm is of economic importance by virtue of its destructive behavior; late instar larvae and adults leave the manure habitat and burrow into the house insulation (Dale et al. 1976; Ichinose et al. 1980; Le Torc’h 1979; Chaix 1980; Wildey 1983; Vaughan et al. 1984). Extensive tunneling results in gradual disintegration ofthe insulation, with a concomitant reduction in its insulating capability (Dale et al. 1976; Vaughan et al. 1984; Despins et al. 1987). Alphitobius diaperinus is quite voracious, and has been reported feeding on the flesh of pigeon squabs (Lewis 1958; Keifer 1935 as cited in Crook et al. 1980) and actually killed and completely consumed the soft tissues of a teninch rat snake (Elaphe sp.), a DeKay’s snake {Storeria dekayi) and a salamander (Harris 1966). The insect will also feed on the flesh and internal organs ofdead and moribund chicks (Harding and Bissell 1958) and on the breasts of incapacitated broiler chickens (W. D. Weaver, pers. comm., Poultry Science Department, VPI & SU). Harris (1966) found as many as 5,762 beetles occurring on and inside a broiler carcass.

supported by Grant Number 82-1332-05 from the Virginia Agricultural Council, Present address: Tick and Scabies Research Unit, USDA, ARS, P.O. Box 3008-KjngshilI, Saint Croix, U.S. Virgin Islands 00850. Present address; DepartmenI of Microbiology & Immunology, University of Maryland School of This research

Medicine, Baltimore, MD 22201.

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THE COLEOPTERISTS BULLETIN 42(3), 1988

Despite its voracity, little work has been published on the predatory potential of the lesser mealworm. Koszlov (1970) found the lesser mealworm to be an effective predator of the chicken mite, Dermanyssvs galUnae Redi. Toyama and Ikeda (1976) reported predation of only first instar house fly, Musca domestica L., larvae. Armitage (1986) showed an inverse relationship between lesser mealworm and house fly populations in three high rise houses in Great Britain, and alluded to the predatory potential of the lesser mealworm. Lesser mealworms are also thought to have an indirect impact on house fly populations by physically altering the habitat of the maggots by tunneling through the manure. Habitat tunneling by the lesser mealworm is a behavior which occurs in the second instar and continues through the remainder of the larval stage (Wilson and Miner 1969). Tunneling promotes aeration and drying of the manure pad, producing a suboptimum environment for noxious fly development (Axtell 1986). This study provides information on this heretofore neglected aspect oflesser mealworm biology. The objective was to examine the potential of the lesser mealworm as a predator of the house fly under the simulated conditions of a high rise caged layer house.

MATERIALS AND METHODS

Lesser mealworms typically inhabit manure with

a 30 to

40% moisture

content (pers. obser.), whereas house fly maggots inhabit much wetter manure (60 to 75% moisture) (Miller et al. 1974). As third instar maggots prepare for metamorphosis, they disperse to drier areas in the manure to pupariate, thus

providing a greater probability for interspecific interaction. For this reason, third instar house fly maggots and puparia were the only prey stages used in these experiments. Initial observations of house fly predation were accomplished by isolating a single maggot with either a larval or adult lesser mealworm in the bottom of a four dram (14 cc) patent lip glass vial. Vials were held at room temperature (21Q. Counts of predation were made eight hours later. Four additional experiments were conducted (designated hereafter as "Fly Tests*’). Fly Tests One and Two involved an examination of predation of puparial and eclosing house flies. Fly Tests Three and Four simulated natural habitats in the manure pit of a high rise caged layer house. FLY TEST ONE. Nine, open-lid, 236.6 ml Mason(R) jars each containing 50 house fly puparia were placed into cylindrical 1.9 liter ice cream cartons. Five adult beetles were placed into each of three ofthe jars, five middle instar larvae were set into each of three other jars, and the other three jars received no beetles. The top of each ice cream carton was fitted with a chamber into which successfully emerged house flies could crawl. Units were kept at 21C and the number of flies which had emerged was counted at the end of 14 days. FLY TEST Two. Observations were conducted using third instar house fly maggots. A similar apparatus to Fly Test One was used, except glass Mason(R) jars were not used, and the maggots were placed directly on the ice cream carton floor. The same number of insects (i.e., identical ratio of prey to predator) was used as in Fly Test One, and they were placed into each of four cartons; four cartons received no beetles. Cartons were kept at 27C, and were examined for emerged flies over a 14 day period. Emerged flies were removed by aspiration and preserved in 70% ethanol. FLY TEST THREE. Fifty g of air dried, semipulverized chicken manure were placed into a plastic container measuring 11 cm top diameter x 9 cm bottom

THE COLEOPTERISTS BULLETIN 42(3), 1988

213

Table 1. Fly Test One. Effect of adult and middle instar lesser mealworms on house fly emergence under laboratory conditions; house fly puparia used as prey.

No. house flies’ Treatment2 Adult lesser mealworms Larval lesser mealworms Fly puparia only

Emerged

Not emerged

94 109

56 41

141

9

Observed frequencies of emergence significantly different from the expected (x3 2, P 0.001). 1:10. to fly Ratio of lesser mealworm stage prey

42.6749, df

diameter x 7.5 cm height. Based on the manure dry weighi, enough distilled water was added to create a 50% manure moisture habitat. Fifty house fly puparia were placed on the manure surface, after which 20 adult lesser mealworms were added to each manure container- Each container was placed into an ice cream carton apparatus as described earlier in Fly Test One, and kept at 21C. Four treatment chambers and four control chambers (i.e., no beetles) were prepared. Emerged flies were removed by aspiration daily over the 14 day test period and preserved in 70% ethanol. FLY TEST FOUR. This investigation involved creating a separate beetle and house fly habitat within the ice cream carton apparatus. Chicken manure was collected from beneath caged layers housed at a research facility at VPI & SU, and frozen for three days to kill any insect life. Manure was thawed, warmed in a water bath, and placed up to the lip of seven plastic-lined 473.2 ml cups, each of which was placed in a 1.9 liter ice cream container. The space between the manure cup and the ice cream carton wall was filled with coarse sand to within 2.5 cm of the manure cup lip; the remaining 2.5 cm above the sand was filled with a mixture of sterilized 16% protein standard layer diet and split fresh green corn kernels (for moisture). The environment surrounding the manure cup represented a drier habitat and provided a site for fly pupariation. Each manure cup was seeded with 100 first instar house fly maggots. Twenty-five adult lesser mealworms were placed into four of the prepared chambers, on the chicken diet/corn habitat, and three remaining chambers served as control treatments. Chambers were placed into a constant temperature cabinet and held at 27C and 24 hours darkness. Manure cups were lightly misted with distilled water every other day to prevent desiccation and to ensure that maggots, prior to pupariating, would disperse into the beetle habitat. The experiment was ended after 10 days, and the emerged flies were collected and counted from the emergence chamber and from the habitat chamber.

RESULTS Both adults and late instar lesser mealworm larvae fed on the house fly maggots when isolated together in the patent lip glass vials. Late instar larvae consumed a significantly greater proportion of the prey (31 of 43 maggots) than was observed in the adult stage (S of 42 maggots) (Fisher’s exact test, P < 0.0001). The larva was able to subdue the violently wrigglmg maggot by partially wrapping its body around the maggot and chewing through the integument of the prey. Adults apparently could not consume the maggot in this manner because of their more rigid body structure.

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THE COLEOPTERISTS BULLETIN 42(3), 1988

Table 2. By Test Two. Effect ofadult and middle instar lesser mealworms on house fly emergence under laboratory conditions; house fly maggots used as prey.

No. house Hies’ Treatment2 Adult lesser mealworms Larval lesser mealworms Fly puparia only

Emerged

Not emerged

28 38 51

42

52

29

Observed frequencies of" emergence significantly different from the expected (x2 P 0.005). Ratio of lesser mealworm stage to fly prey 1:10.

13.3083.df

2,

Both lesser mealworm adults or middle instar larvae, when isolated in a chamber of exposed house fly puparia, significantly reduced house fly emergence (Fly Test One, Table 1). Although fewer house flies emerged from the adult treatment than from the larval treatment, emergence data from the adults and larval treatments were not statistically different (x2 2.9861, df= 1, P > 0.05). Likewise, presence ofA diaperinus in the interaction chamber containing house fly maggots also significantly reduced fly emergence when compared to fly emergence from chambers containing maggots only (Fly Test Two, Table 2). Fly emergence from the adult and larval treatments did not differ statistically from one another (x2 2.0889, df 1, P > 0.05). Both simulated poultry house environment studies showed that adults caused significant reductions in house fly emergence, producing as much as a 42% population reduction in comparison with the control treatment (Fly Tests Three and Four, Tables 3

and 4, respectively).

DISCUSSION Alphitobius diaperinus had a significant impact on house fly emergence in our laboratory systems. Late instar larval lesser mealworms were effective predators of house fly maggots. However, while these results corroborate the report of research recently conducted in Great Britain (Armitage 1986), the potential of the lesser mealworm as a biological control agent against house flies will probably remain overshadowed by its destructive tendencies in poultry houses, unless chemical or physical barriers can be developed that will effectively prevent lesser mealworm tunneling into insulating materials. The significance of lesser mealworm predatory behavior may not lie in

Table 3. Fly Test Three. Effect of adult lesser mealworms on house fly emergence under 50% manure moisture environment.

No. house flies’ Treatment2

Adult lesser mealworms Fly puparia only

Emerged

Not emerged

113 194

87 6

Observed frequencies of emergence significantly different from the expected (x2 0.001). 1, P Ratio of adult lesser mealworms to fly puparia 2:5.

89.6641, df

THE COLEOPTERISTS BULLETIN 42(3), 1988

215

Table 4. Fly Test Four. Effect of adult lesser mealworms on house fly emergence under simulated poultry house conditions (greater than 60% manure moisture).

No. house flies’ Treatment2

Adult lesser mealworms Fly maggots only

Emerged

Not emerged

194

206 97

203

significantly different from the expected (x2 Observed frequencies of emergence 1,^< 0.001). 1:4. Ratio of adult lesser mealworms to fly prey

24.8783, df

control of house fly populations, but in the effects which might occur during releases of other house fly biological control agents. Recent work conducted in Florida (Hogsette 1979), South Carolina (Nolan and Kissam 1985), and Virginia (E. C. Turner, unpubl. data, Dept. of Entomology, VPI & SU) confirm the value of black garbage fly maggots, Ophyra aenescens (Weidemann) (Diptera: Muscidae), as predators of immature house flies in high rise caged layer houses. Release of the black garbage flies in high rise houses consists ofdumping a number of trays of laboratory-reared maggots onto the manure surface near larval house fly habitats- We found that the highly proteinaceous 0. aenescens rearing medium was very attractive to lesser mealworms, and observed a great number of beetles surrounding the garbage fly release sites. The beetles which were feeding on the rearing medium probably consumed black garbage fly maggots and puparia as well. Future studies should be conducted to evaluate the effect of lesser mealworm predation in the dynamics of the Ophyra aenescensiMusca domestica predator-prey system.

ACKNOWLEDGMENTS We thank Cecil Kessinger for his expertise in rearing house flies. We gratefully acknowledge the efforts of Felicia Johnson, who translated the French journal articles, and Koichi Ono, who translated the Japanese journal article. LITERATURE CITED ARMITAGE, D. M. 1986. Population changes of four species of insects (Col. &. Dipt.) in three deep pit poultry houses, Entomol. Mon. Mag. 122:75-77. AXTELL, R. C. 1986. Fly management in poultry production: cultural, biological and chemical. PSA symposium on arthropods of economic importance to the poultry industry. Poult. Sci. 65:657-667.

CHAIX, M. 0. 1980. La desinsectisation des locaux d’elevage. Phytoma 314:18-20. CROOK, P. G., J. A. NOVAK, AND T. J. SPILMAN. 1980. The lesser mealworm, Alphiiobius diaperinus. in the scrotum of Ratlus norvegicus, with notes on other vertebrate associations (Coleoptera: Tenebrionidae; Rodentia: Muridae). Coleopts Bull. 34: 393-396. DALE, P. S., J. C. HAYES, AND J. JOHANNESSON. 1976. New records of plant pests in New Zealand. N. Z. J. Agric. Res. 19:265-269. DESPINS, J. L-, E. C. TURNER, JR-, AND P. L. RUSZLER. 1987. Construction profiles of high rise caged layer houses in association with insulation damage caused by the lesser mealworm, Alphiiobius diaperinus (Panzer), in Virginia. Poult. Sci. 66:243250. GREEN, D. B. 1982. The fauna and environment of two Lancashire deep-pit poultry

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houses. Minisl. of Agriculture, Fisheries and Food Poultry, Sect. A Quarterly Journal, March (140):15-32. HARMNG, W. C., AND T- L. BISSELL. 1958. Lesser mealworms in a brooder house. J. Econ. Entomol. 51:112. HARRIS, F. 1966. Observations on the lesser mealworm, Alphitobius diaperinus (Panz.). J. Ga. Entomol. Soe. 1:17-18. HOGSETTE, J. A., JR. 1979. The evaluation of poultry pest management techniques in Florida poultry houses. Ph.D dissertation, University of Florida, Gainesville. 307 pp. ICHINOSE, T., S. SHIBAZAKI, AND M. OHTA. 1980. Studies on the biology and mode of infestation of the tenebrionid beetle, Alphitobius diaperinus Panzer, harmful to broiler-chicken houses. Jap. J. Appl. Entomol. Zool. 24:167-174 (in Japanese with English abstract). KEEPER, H. H. 1935. The black fungus beetle and the lesser mealworm. Calif. Agric. Mon.BuII. 24:316. K.OSZLOV, V. I. 1970. The tenebrionid Alphitobius diaperinus Panz., a predator of Dermanyssus gallinae Redi. Parazitologiya 4:363-364 (in Russian with English abstract). LE TORC’H, J. M. 1979. Un nouveau ravageur des batiments d’elevage. Phytoma 308: 31-33. LEWIS, D. J. 1958. Coleoptera of medical interest in the Sudan Republic. Proc. Royal Entomol. Soc. London, Ser. A 33:37-42. MILLER, B. F., J. S. TEOTIA, AND T. 0. THATCHER. 1974. Digestion of poultry manure by Musca domestica. Br. Poult. Sci. 15:231-234. NOLAN, M. P., Ill, AND J. B. KISSAM. 1985. Ophyro. aenescens: a potential bio-control alternative for bouse fly control in poultry houses. J. Agric. Entomol. 2:192-195. PFEIFFER, D. G., AND R. C. AXTELL. 1980. Coleoptera of poultry manure in cagedlayer houses in North Carolina. Environ. Entomol. 9:21-28. TOYAMA,G.M.,ANDJ.K.IKEDA. 1976. An evaluation of fly predators at animal farms on leeward and central Oahu. Proc. Hawaii. Entomol. Soc. 22:369-379. VAUGHAN, J. A., E. C. TURNER, JR., AND P. L. RUSZLER. 1984. Infestation and damage of poultry house insulation by the lesser mealworm, Alphitobius diaperinus (Panzer). Poult. Sci. 63:1094-1100. WILDEY, K. B. 1983. Insect pests in animal houses-current control developments [pp. 1-11]. In: Bateman, P. L. G. (editor). Proceedings, Sixth British Pest Control Conference, paper no. 20, Robinson College, Cambridge, September 7th-10th 1983, British Pest Control Association. London. WILSON, T. H., AND F. D. MINER. 1969. Influence of temperature on development of the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). 3. Kans. Entomo], Soc. 42:294-303.

(Received 19 May 1986; revised 26 October 1986; accepted 8 January 1987)