Abstract
Insects rely mainly on their well-developed and highly sophisticated olfactory system to discriminate volatile cues released from host and nonhost substances, mates, oviposition substrates, and food sources. Onset of first mating, mating duration, and onset of first oviposition, oviposition period, fecundity (number of eggs laid by a female), and longevity of freshly emerged Musca domestica L. (Diptera: Muscidae) adults were observed in the presence of different animal manures: cow, horse, donkey, poultry, and an artificial diet. The M. domestica adults exposed to horse manure showed a delay in onset of first mating and first oviposition, prolonged mating duration, and reduced fecundity compared to the artificial diet (control). Likewise, the fecundity was reduced in the presence of donkey manure as compared to artificial diet. The onset of first mating was delayed and duration of first mating was shortened in the presence of cow manure as compared to artificial diet and no oviposition was observed throughout the duration of the experiment. However, the reproductive behaviors and all fitness measures in adults exposed to poultry manure were similar or even better, compared to the artificial diet. Surprisingly, in a free-choice attraction assay, the highest numbers of adult flies were attracted toward the cow manure as compared to all other manures as well as the artificial diet. However, the numbers of flies captured in all other types of manures were not different than the artificial diet (control). Furthermore, chemical analysis of headspace samples of manures revealed qualitative differences in odor (volatile) profiles of all manures and artificial diet, indicating that behavioral differences could be due to the differences in the volatile chemistry of the adult ovipositional substrates and larval growth mediums. This study may contribute toward both understanding the linkage between ecological adaptations and host selection mechanisms and the development of pest management strategies against this serious pest of medical and veterinary importance.
Similar content being viewed by others
References
Abbas N, Khan HAA, Shad SA (2014) Cross-resistance, genetics, and realized heritability of resistance to fipronil in the house fly, Musca domestica (Diptera: Muscidae): a potential vector for disease transmission. Parasitol Res 113:1343–1352
Abbas N, Shad SA, Ismail M (2015) Resistance to Conventional and New Insecticides in House Flies (Diptera: Muscidae) From Poultry Facilities in Punjab, Pakistan. J Econ Entomol 108:826–833
Anderson P, Alborn H (1999) Effects on oviposition behaviour and larval development of Spodoptera littoralis by herbivore-induced changes in cotton plants. Entomol Exp Appl 92:45–51
Anonymous (2005. Available:https://scholar.google.com.pk/scholar?hl=en&as_sdt=0,5&q=Statistica+for+Windows.+Analytical+Software,+Tallahassee,+Florida) Statistix for Windows. Analytical Software, Tallahassee, Florida.
Ascher KR (1958) The attraction of the Levant housefly Musca vicina Macq. to natural breeding media. Acta Trop 15:1–14
Azeem M, Rajarao GK, Nordenhem H, Nordlander G, Borg-Karlson AK (2013) Penicillium expansum volatiles reduce pine weevil attraction to host plants. J Chem Ecol 39:120–128
Azeem M et al (2015) A fungal metabolite masks the host plant odor for the pine weevil (Hylobius abietis). Fungal Ecol 13:103–111
Becher PG et al (2012) Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct Ecol 26:822–828
Bell HA, Robinson KA, Weaver RJ (2010) First report of cyromazine resistance in a population of UK house fly (Musca domestica) associated with intensive livestock production. Pest Manage Sci 66:693–695
Benton R (2006) On the origin of smell: odorant receptors in insects. Cell Mol Life Sci 63:1579–1585
Binyameen M, Hussain A, Yousefi F, Birgersson G, Schlyter F (2013) Modulation of reproductive behaviors by non-host volatiles in the polyphagous Egyptian cotton leafworm, Spodoptera littoralis. J Chem Ecol 39:1273–1283
Cickova H, Pastor B, Kozanek M, Martínez-Sanchez A, Rojo S, Takac P (2012) Biodegradation of pig manure by the housefly, Musca domestica: a viable ecological strategy for pig manure management. PLoS ONE 7:e32798
Clavel A et al (2002) House fly (Musca domestica) as a transport vector of Cryptosporidium parvum. Folia Parasitol 49:163–164
Cook SM, Khan ZR, Pickett JA (2006) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375
Cosse AA, Baker TC (1996) House flies and pig manure volatiles: wind tunnel behavioral studies and electrophysiological evaluations. J Agric Entomol 13:301–317
De Bruyne M, Baker T (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897
Fasanella A, Scasciamacchia S, Garofolo G, Giangaspero A, Tarsitano E, Adone R (2010) Evaluation of the house fly Musca domestica as a mechanical vector for an anthrax. Plos One 5:e12219
Fatchurochim S, Geden C, Axtell R (1989) Filth fly(Diptera) oviposition and larval development in poultry manure of various moisture levels. J Entomol Sci 24:224–231
Ferrar P (1987) A guide to the breeding habits and immature stages of Diptera Cyclorrhapha. Entomonograph 8:907
Forster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K (2007) Pilot study on synanthropic flies (eg Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res 101:243–246
Foster S, Harris M (1997) Behavioral manipulation methods for insect pest-management. Annu Rev Entomol 42:123–146
Gerry A, Mellano V, Kuney D (2005) Outdoor composting of poultry manure reduces nuisance fly production. University of California Riverside, College of Natural and Agricultural Sciences, Department of Entomology, white paper, June 21. Available: http://www.sandiegocounty.gov/reusable_components/images/dpw/recyclingpdfs/Manure.pdf
Hajek AE (2004) Natural enemies: an introduction to biological control. Cambridge University Press
Hazell P, Wood S (2008) Drivers of change in global agriculture. Philos T Roy Soc B 363:495–515
Hedges LV, Olkin I (2014) Statistical method for meta-analysis. Available: http://files.eric.ed.gov/fulltext/ED227133.pdf. Academic press.
Hogsette JA (1996) Development of house flies (Diptera: Muscidae) in sand containing varying amounts of manure solids and moisture. J Econ Entomol 89:940–945
Huang J, He J, Zhang J, Yu Z (2007) Identification of volatile organic compounds in the manures of cow, hog and chicken by solid phase microextraction coupled with gas chromatography/mass spectrometry. Se pu = Chinese J chromatography/Zhongguo hua xue hui 25:425–429
Hussain A, Tian M-Y, He Y-R, Bland JM, Gu W-X (2010) Behavioral and electrophysiological responses of Coptotermes formosanus Shiraki towards entomopathogenic fungal volatiles. Biol Control 55:166–173
Jactel H, Birgersson G, Andersson S, Schlyter F (2011) Non-host volatiles mediate associational resistance to the pine processionary moth. Oecologia 166:703–711
Jactel H, Van Halder I, Menassieu P, Zhang Q, Schlyter F (2001) Non-host volatiles disrupt the response of the stenographer bark beetle, Ips sexdentatus (Coleoptera: Scolytidae), to pheromone-baited traps and maritime pine logs. Integr Pest Manage Rev 6:197–207
Jeanbourquin P, Guerin PM (2007) Chemostimuli implicated in selection of oviposition substrates by the stable fly Stomoxys calcitrans. Med Vet Entomol 21:209–216
Jonfia-Essien W, Alderson P, Tucker G, Linforth R, West G (2007a) Behavioural Responses of Tribolium castaneum (Herbst) to Volatiles Identified from Dry Cocoa Beans. Pak J Biol Sci 10:3549–3556
Jonfia-Essien W, Alderson P, Tucker G, Linforth R, West G (2007b) The growth of Tribolium castaneum (Herbst) and Lasioderma serricorne (Fabricius) on feed media dosed with flavour volatiles found in dry cocoa beans. Pak J Biol Sci 10:1301–1304
Khan HAA, Akram W, Shad SA (2013a) Resistance to conventional insecticides in Pakistani populations of Musca domestica L. (Diptera: Muscidae): a potential ectoparasite of dairy animals. Ecotoxicol 22:522–527
Khan HAA, Shad SA, Akram W (2012) Effect of livestock manures on the fitness of house fly, Musca domestica L. (Diptera: Muscidae). Parasitol Res 111:1165–1171
Khan HAA, Shad SA, Akram W (2013b) Combination of phagostimulant and visual lure as an effective tool in designing house fly toxic baits: a laboratory evaluation. PLoS One 8:e77225
Khan M (2009) Economic evaluation of health cost of pesticide use: willingness to pay method. Pak Dev Rev 48:459–470
Kristensen M, Jespersen JB (2003) Larvicide resistance in Musca domestica (Diptera: Muscidae) populations in Denmark and establishment of resistant laboratory strains. J Econ Entomol 96:1300–1306
Lam K (2010 Available http://summit.sfu.ca/item/10043) Oviposition ecology of house flies, Musca domestica (Diptera: Muscidae): competition, chemical cues, and bacterial symbionts. PhD thesis, Biological Sciences Department-Simon Fraser University
Lam K, Geisreiter C, Gries G (2009) Ovipositing female house flies provision offspring larvae with bacterial food. Entomol Exp Appl 133:292–295
Larrain P, Salas C (2008) House fly (Musca domestica L.)(Diptera: Muscidae) development in different types of manure. Chil J Agr Res 68:192–197
Larsen JR, Pfdat RE, Peterson LG (1966) Olfactory and oviposition responses of the house fly to domestic manures, with notes on an autogenous strain. J Econ Entomol 59:610–615
Malik A, Singh N, Satya S (2007) House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health, Part B 42:453–469
Mann RS, Kaufman PE, Butler JF (2010) Evaluation of semiochemical toxicity to houseflies and stable flies (Diptera: Muscidae). Pest Manage Sci 66:816–824
McLeod G et al (2005) The pathogen causing Dutch elm disease makes host trees attract insect vectors. Proc R Soc Lond [Biol] 272:2499–2503
Moon R, Hinton J, O’Rourke S, Schmidt D (2001a) Nutritional value of fresh and composted poultry manure for house fly (Diptera: Muscidae) larvae. J Econ Entomol 94:1308–1317
Moon R, Hinton J, O’Rourke S, Schmidt D (2001b) Nutritional value of fresh and composted poultry manure for house fly (Diptera: Muscidae) larvae. J Econ Entomol 94:1308–1317
Myers HM, Tomberlin JK, Lambert BD, Kattes D (2008) Development of black soldier fly (Diptera: Stratiomyidae) larvae fed dairy manure. Environ Entomol 37:11–15
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605
Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17:857–872
Ortiz D et al (2002) Overview of human health and chemical mixtures: problems facing developing countries. Environ Health Persp 110:901
Papadopoulos N, Kouloussis N, Katsoyannos B (2006) Effect of plant chemicals on the behavior of the Mediterranean fruit fly. Proceedings of International Fruit fly Meeting Brazil Salvador, Brasil:pp. 97–106
Pfeil R, Mumma R (1993) Bioassay for evaluating attraction of the phorid fly, Megaselia halterata to compost colonized by the commercial mushroom, Agaricus bisporus and to 1-octen-3-ol and 3-octanone. Entomol Exp Appl 69:137–144
Pimentel D (2005) Environmental and economic costs of the application of pesticides primarily in the United States. Environ Dev Sustainability 7:229–252
Quinn BP, Bernier UR, Geden CJ, Hogsette JA, Carlson DA (2007) Analysis of extracted and volatile components in blackstrap molasses feed as candidate house fly attractants. J Chromatogr 1139:279–284
Ramachandran R, Norris DM, Phillips JK, Phillips TW (1991) Volatiles mediating plant-herbivore-natural enemy interactions: soybean looper frass volatiles, 3-octanone and guaiacol, as kairomones for the parasitoid Microplitis demolitor. J Agric Food Chem 39:2310–2317
Sadek MM, Anderson P (2007) Modulation of reproductive behaviour of Spodoptera littoralis by host and non-host plant leaves. Basic Appl Ecol 8:444–452
Scott JG, Alefantis TG, Kaufman PE, Rutz DA (2000) Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manage Sci 56:147–153
Shah RM, Abbas N, Shad SA, Sial AA (2015) Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitol Res 114:487–494
Shelly TE, Villalobos EM (2004) Host plant influence on the mating success of male Mediterranean fruit flies: variable effects within and between individual plants. Anim Behav 68:417–426
Siriwattanarungsee S, Sukontason KL, Olson JK, Chailapakul O, Sukontason K (2008) Efficacy of neem extract against the blowfly and housefly. Parasitol Res 103:535–544
Sutherland O (1977) Plant chemicals influencing insect behaviour. N Z Entomol 6:222–228
Tang JD, Caprio MA, Sheppard DC, Gaydon DM (2002) Genetics and fitness costs of cyromazine resistance in the house fly (Diptera: Muscidae). J Econ Entomol 95:1251–1260
Tawatsin A et al (2006) Repellency of essential oils extracted from plants in Thailand against four mosquito vectors (Diptera: Culicidae) and oviposition deterrent effects against Aedes aegypti (Diptera: Culicidae). Southeast Asian J Trop Med Public Health 37:915
Taylor DB, Moon RD, Mark DR (2012) Economic impact of stable flies (Diptera: Muscidae) on dairy and beef cattle production. J Med Entomol 49:198–209
Taylor GK, Krapp HG (2007) Sensory systems and flight stability: what do insects measure and why? Adv Insect Physiol 34:231–316
Vazirianzadeh B, Shams Solary S, Rahdar M, Hajhossien R, Mehdinejad M (2011) Identification of bacteria which possible transmitted by Musca domestica (Diptera: Muscidae) in the region of Ahvaz, SW Iran. Jundishapur J Microbiol 1:28–31
Whalon ME, Mota-Sanchez D, Hollingworth RM (2008) Global pesticide resistance in arthropods, vol pp,170. Cabi, International, Wallingford
Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100
Zakir A, Sadek MM, Bengtsson M, Hansson BS, Witzgall P, Anderson P (2013) Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore. J Ecol 101:410–417
Zhang P-J, Liu S-S, Wang H, Zalucki MP (2007) The influence of early adult experience and larval food restriction on responses toward nonhost plants in moths. J Chem Ecol 33:1528–1541
Zhang Q-H, Schlyter F (2004) Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer inhabiting bark beetles. Agric For Entomol 6:1–20
Acknowledgments
We are highly thankful to Mr. M. Imran, Dr. N. Abass, Prof. F. Schlyter, and Dr. A. Waheed for their valuable inputs and help in analyzing the results. We are also wholeheartedly thankful to Dr. S. Saeed for the provision of cages to perform the attraction assays. We are very thankful to Prof. Anna Karin Borg-Karlson for the nice gift of SPME fibers and holder. Efforts of Mr. Q. Ali are highly acknowledged for collection of manure samples.
Author’s contribution
RMS, MB, and SAS designed the experiments. RMS, FA, and MA performed the experiments. RMS, MB, and MA analyzed the data and wrote the manuscript. MB and SAS supervised the experiments. WBW provided the technical help for the preparation of final manuscript including English language and scientific-content editing.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Shah, R.M., Azhar, F., Shad, S.A. et al. Effects of different animal manures on attraction and reproductive behaviors of common house fly, Musca domestica L. Parasitol Res 115, 3585–3598 (2016). https://doi.org/10.1007/s00436-016-5124-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5124-0