Sulfur Dust Bag: A Novel Technique for Ectoparasite Control in Poultry Systems

Journal of Economic Entomology, 109(5), 2016, 2229–2233 doi: 10.1093/jee/tow146 Advance Access Publication Date: 18 July 2016 Veterinary Entomology Research article Sulfur Dust Bag: A Novel Technique for Ectoparasite Control in Poultry Systems Amy C. Murillo1 and Bradley A. Mullens Department of Entomology, University of California, Riverside, CA 92521 ([email protected]; [email protected]), and 1 Corresponding author, e-mail: [email protected] Downloaded from https://academic.oup.com/jee/article/109/5/2229/2200584 by guest on 07 August 2022 Received 12 April 2016; Accepted 1 June 2016 Abstract Animal welfare-driven legislation and consumer demand are changing how laying chickens are housed, thus creating challenges for ectoparasite control. Hens housed in suspended wire cages (battery cages) are usually treated with high-pressure pesticides. This application type is difficult in enriched-cage or cage-free production. Alternatives to pesticide sprays are needed in enriched-cage or cage-free systems. In this study, we tested the efficacy of sulfur dust deployed in “dust bags” for control against the northern fowl mite (Ornithonyssus sylvia- rum), which causes host stress, decreased egg production, and reduced feed conversion efficiency. Dust bags were hung from the tops of cages or were clipped to the inside front of cages. We also tested permethrin- impregnated plastic strips, marketed for ectoparasite control in caged or cage-free commercial and backyard flocks. Previous work has shown sulfur to be very active against poultry ectoparasites; however, we found that the placement of bags was important for mite control. Sulfur in hanging bags reduced mites on treatment birds by 95 or 97% (depending on trial) within one week of being deployed, and mite counts on these birds were zero after 2 wk. Clipped sulfur bags acted more slowly and did not significantly reduce mites in one trial, but reduced mite counts to zero after 4 wk in trial 2. Permethrin strips had no effect on mite populations. This may have been due to mite resistance, even though this mite population had not been exposed to pyrethroids for several years. Sulfur bags should be effective in caged or cage-free systems. Key words: Ornithonyssus sylviarum, northern fowl mite, Gallus gallus domesticus, control, sulfur Animal welfare concerns are driving poultry production away from inflammation, immune system activation, irritation, anemia, and traditional battery cages to larger enriched-cage or cage-free produc- even rarely death as a result of exsanguination (DeVaney and Ziprin tion systems. Enriched cages allow for more space per bird and in- 1980, Burg et al. 1988, Minnifield et al. 1993, Mullens et al. 2009, clude upgrades such as perches, nest boxes, and scratch pads. Owen et al. 2009). This mite is a permanent ectoparasite (all life “Cage-free” birds may include several types of production systems stages live on-host) that is found on chickens regardless of housing (e.g., aviary, free-range, pasture), but all provide birds with some type (Lay et al. 2011). Mites can be introduced to flocks by wild type of nest boxes and perches. Ectoparasite control in wire battery birds or rodents, or contaminated equipment or people, and are very cages is achieved by high-pressure insecticidal sprays (Mullens et al. difficult to eradicate once introduced to a poultry facility (Kells and 2009). These products must penetrate the feather layer from under Surgeoner 1996, Axtell 1999). the birds to treat mites, which are found primarily in the vent region One option for enriched-cage or cage-free production is self- of the bird. It is difficult or impossible to spray birds in this way in treatment of animals. Self-application of insecticidal dust by rubbing enriched-cage or cage-free systems because of the complex environ- or bumping against large dust bags has been used for the control of ments or solid floors. In addition, pyrethroid and organophosphate pests on cattle for several decades (Turner 1965). For poultry, sulfur resistance is a growing concern (Mullens et al. 2004). As poultry has proven to be a highly effective acaricide at low doses in dust- production moves away from battery cages due to legislation (e.g., boxes in cage-free settings, eliminating ectoparasites even on birds California’s Proposition 2 “Standards for Confining Farm that did not dustbathe in the material (Martin and Mullens 2012). Animals”; Sumner et al. 2008) or increased consumer demand, new Sulfur is also effective for mites in a water slurry sprayed onto a pesticide delivery systems for use in nonbattery cage production sys- bird’s body (Mullens et al. 2012). Self-treatment reduces labor costs tems will need to be developed. and treatment-associated stress to the birds (Jones and Kissam The most damaging ectoparasite of US laying hens is the north- 1983). Previous work suggests that mite populations below a score ern fowl mite, Ornithonyssus sylviarum (Canestrini & Fanzango) of 3 (ca. 100 mites per bird) are not as economically damaging to (Axtell and Arends 1990). These blood-feeding mites induce skin producers as higher mite numbers (Mullens et al. 2009). C The Authors 2016. Published by Oxford University Press on behalf of Entomological Society of America. V All rights reserved. For Permissions, please email: [email protected] 2229 2230 Journal of Economic Entomology, 2016, Vol. 109, No. 5 In this study, we tested sulfur dust bags for mite control in caged treatment). Cage groupings were separated into different cage rows or birds. Dust bags were either clipped onto the front of the cage or by at least three to six empty cages to prevent cross-contamination hung from the top of the cage. We also tested permethrin- and minimize mite movement among treatment groups. When per- impregnated plastic strips, which are available for commercial and forming daily hen care duties or scoring birds, nitrile gloves were home use on northern fowl mites (Hall et al. 1983). changed between each treatment group. Mite levels were monitored weekly for four additional weeks (posttreatment) and the study was concluded at week 9. Two complete trials were conducted Materials and Methods (November–December 2014 and December 2015–February 2016). Birds Ectoparasite-free white leghorn (Highline strain CV20) chickens (17– Statistical Analyses 19 wk old) were acquired from local commercial producers. All birds Statistical analyses were performed using SAS software (SAS were beak trimmed before they arrived, which is routine for commer- Institute Inc., Cary, NC, 2010, v. 9.3). Proc means were used to gen- cial chickens to reduce feather pecking, cannibalism, and feed waste erate averages and standard errors of mite scores. Mixed model (Mertens et al. 2009). Birds were housed individually at the repeated-measures analysis was used to examine the effect of treat- Downloaded from https://academic.oup.com/jee/article/109/5/2229/2200584 by guest on 07 August 2022 University of California Riverside Agricultural Operations (AgOps) in ments (hanging bag, clipped bag, permethrin strip, control) on mite plain wire cages measuring 31 by 31 cm with a photoperiod of 16:8 score. Bird was the fixed effect and week was the repeated measure. (L:D) h. Animal care was approved under University of California Trials were combined for this part of the analysis. Analyses were Riverside Institutional Animal Care and Use Protocol A-20150009. separated into pre- and posttreatment time frames (weeks 1–5 and 6–9, respectively). Tukey’s test was used to separate treatment Mites means (by trial) for each week posttreatment. Northern fowl mites were maintained on white leghorn chickens at AgOps. For inoculation, mites were aspirated with pipettes from those source birds. Mites then were applied to the vent region of Results each experimental bird (Martin and Mullens 2012). Once a week Mean mite scores for trials 1 and 2 are shown in Fig. 2. No signifi- for the duration of the study all treatment and control birds were cant differences were found between trials (F ¼ 0.01; df ¼ 1, 40; visually scored (by ACM) for level of mite infestation. The scoring P ¼ 0.92) or treatment groups (F ¼ 0.04; df ¼ 3, 40; P ¼ 0.99) during system used is as follows: 1 ¼ 1–10, 2 ¼ 11–50, 3 ¼ 51–100, the pretreatment period (weeks 1–5). During the posttreatment 4 ¼ 101–500, 5 ¼ 501–1,000, 6 ¼ 1,001–10,000 and 7 ¼ >10,000 period (weeks 6–9) significant differences among treatments were (Arthur and Axtell 1983). observed (F ¼ 45.96; df ¼ 3, 40; P < 0.0001; Fig. 2). Control birds in both trials had mite populations that grew steadily. At week 5 Dust Bags (pretreatment) control bird mite scores were 5.33 6 0.42 and Cloth bags measured ca. 7.5 by 12.7 cm and were constructed from a 5.67 6 0.33 (mean 6 SE; trials 1 and 2, respectively). In both trials single layer of 100% cotton gauze (ca. 20 mm openings; Hobby Lobby, chickens treated with sulfur hanging bags had significantly lower Inc, Oklahoma City, OK). Dust bags were filled with 30 g (6 1) of mite populations after just 1 wk of treatment. Birds with sulfur- 90% wettable sulfur (Yellow Jacket; Georgia Gulf Sulfur Corp., clipped bags had more variable results. Mean mite scores on the per- Valdosta, GA) then stapled shut. Bags were either hung from the top methrin strip-treated birds never differed significantly from the con- of the cage with a paper clip which was inserted straight through the trol group. gauze material (“hanging bag”) or were folded over the front inside of In trials 1 and 2, mean mite scores on hanging bag-treated birds the cage at the bottom of the cage door and affixed with a large binder fell from a score of around 6.00 to 2.17 6 0.48 and 1.67 6 0.42, re- clip (“clipped bag”; Fig. 1). Each clipped bag also was filled with 30 g spectively, 1 wk posttreatment. There was a 95% or 97% reduction (6 1) of 90% wettable sulfur. In trial 2 the dust bags were weighed in mite scores (versus pretreatment) just 2 wk after treatment in tri- weekly (6 0.1 g) to determine weight of sulfur lost. als 1 and 2, respectively, while control mite scores remained high (above a score of 5). In both trials mean mite scores were Permethrin Strips 0.00 6 0.00 by week 8, 3 wk posttreatment. Plastic permethrin-impregnated strips measured 22 by 1.5 by 1.5 cm The sulfur-clipped bags had more variable results; trial 1 birds (Die No Mite Strips; Car Mac Products, Houston, TX). Each strip had decreased mite levels after treatment, though those did not differ weighed 6.5 g and contained 10% permethrin (active ingredient; AI) significantly from control birds (5.67 6 0.33 at wk 5 [pretreatment] and 6% piperonyl butoxide (synergist). The labeled rate was 1 strip compared to 5.00 6 0.82 at wk 6 [1 wk posttreatment]). Average per 5 birds; we provided each bird with 1 strip which was hung mite scores for trial 1 clipped bags were lowest at wk 9 from the inside top of the cage (Fig. 1). The strips must make contact (3.67 6 1.05). In trial 2 birds treated with sulfur-clipped bags had with the birds for the active ingredient to be effective. Because of the significantly fewer mites compared to controls 2 wk after treatment. small cage size, contact with the strip was frequent. Two weeks posttreatment mean mite scores were 1.83 6 0.95 for birds with clipped bags compared to 6.00 6 0.26 at week 5 Dust Bag Studies (pretreatment). Average mite scores for trial 2 clipped bags were At week 1, twenty-four birds in each of two trials were experimentally lowest at week 9 (0.00 6 0.00). infested with 20–30 adult mites each (described above). Mite popula- The amount of sulfur dispensed per bag per week varied greatly tions were allowed to develop for 4 wk, with weekly visual mite among birds, and over weeks 5–9 release levels were 0.2–18.9 g for scores recorded for each animal. This was the pretreatment period hanging bags and 0.3–14.9 g for clipped bags (trial 2). One week (weeks 1–5). At week 5, birds were divided into four groups of six ad- posttreatment, trial 2 hanging bags had lost on average 7.4 g of sulfur jacent cages. Then one of four treatments was assigned to each bird’s (range: 1.6–16.5 g) while clipped bags lost on average 3.4 g of sulfur cage: hanging bag, clipped bag, permethrin strip, or control (no (range: 0.3–8.5 g). Some sulfur remained in nearly all bags at week 9. Journal of Economic Entomology, 2016, Vol. 109, No. 5 2231 Downloaded from https://academic.oup.com/jee/article/109/5/2229/2200584 by guest on 07 August 2022 Fig. 1. Cotton gauze bags filled with sulfur were deployed by either clipping bags to the bottom of the inside of the cage door (top left) or by hanging from the top of the cage (top right). Permethrin-impregnated strips were hung with metal rings from the top of the cage (bottom). Despite high variation in rates of sulfur release, mites were dramatic- were on average below 3 and were at 0 3 wk posttreatment. ally reduced in all hanging bag cages 1 wk after bags were added. This Previous work suggests that visual mites scores of 3 (100 mites included the cage with the lowest sulfur release, where the hen’s mite per bird) are not as economically damaging to laying hens on a com- score dropped from a 6 to a 2 after a release of only 1.6 g of sulfur. mercial scale as are higher mite numbers (Mullens et al. 2009). In trial 1, clipped bags did not reduce mite populations significantly from control (untreated) birds. However in trial 2 we did observe Discussion significantly reduced mite populations 2 wk posttreatment using the Treatment with hanging sulfur dust bags decreased mite populations clipped bags. The hanging sulfur bags reduced mite levels more in both trials (Fig. 2). Within one week of treatment, mite scores quickly and consistently between the two trials compared to the 2232 Journal of Economic Entomology, 2016, Vol. 109, No. 5 7 Mean mite scores on permethrin strip-treated birds did not differ A A significantly from control birds at any time posttreatment in either 6 A trial (Fig. 2). Each bird was treated with 1 strip (greater than label A A A A rate of 1 strip/5 birds) and made frequent contact with the strip be- 5 Mean Mite Score A A cause of the limited space per cage. Thus, the failure of this product 4 A to control northern fowl mites is likely due to resistance. The mite A A population used in this study (maintained on amplifier hens at 3 AgOps) is derived from mites collected from a commercial poultry B 2 facility over a decade ago, and has not been exposed to permethrin or other pesticides since being established in laboratory colony. 1 B Mullens et al. (2004) found 50% of northern fowl mite field popula- B B 0 tions in southern California to be very resistant (>1,000) to com- 1 2 3 4 5 6 7 8 9 mercial formulations of permethrin. The mechanism conferring Week permethrin resistance in our northern fowl mite population likely Downloaded from https://academic.oup.com/jee/article/109/5/2229/2200584 by guest on 07 August 2022 7 has low fitness costs to maintain. Alternatively the resistance may be A A A A fixed in the population. It appears to have persisted over time even 6 A A in the absence of selection pressure. Recent, independent laboratory A A 5 Mean Mite Score bioassays with technical permethrin confirmed our mite population 4 is resistant to this chemical class, so it probably was not a failure of the permethrin strip treatment to release acaricide (B. A. M., unpub- 3 lished data). Currently there is very limited availability of registered 2 products for northern fowl mite control in California, with most B B products containing the active ingredient permethrin. This highlights 1 the need for alternative control options for northern fowl mite in B B 0 B commercial poultry. B 1 2 3 4 5 6 7 8 9 Sulfur deployed via dust bags could be a great alternative to trad- Week itional pesticide applications. Sulfur is a natural material that is ac- tive against mites in very small doses (Mullens et al. 2012). Dust Control Permethrin Clipped Hanging bags allow the birds to effectively self-treat, eliminating the need for large-scale deployment of dust, which can be an inhalation or com- Fig. 2. Weekly mean (6 SE) mite scores for trial 1 (top) and 2: control, per- bustion risk (Mullens et al. 2012). Sulfur treatments also effectively methrin strip, clipped bag, hanging bag. Treatments were deployed after mite counts at week 5 (arrow). Weekly means after treatment date with the same control poultry lice (Creighton et al. 1943, Martin and Mullens letter are not significantly different (P ¼ 0.05). 2012) and possibly other poultry ectoparasites, such as Dermanyssus gallinae or Echidnophaga gallinacea, that are reemerg- clipped bags. The frequency of bag contact by individual hens may ing (Murillo and Mullens 2016). In this study each bird was held in have contributed to this variation for clipped bags. Birds had to an individual cage with a single dust bag, but on a commercial scale come into contact with the hanging sulfur bags in order to reach the one bag per cage holding multiple birds would probably be suffi- feeder. When birds came in contact with these bags, much of the sul- cient. In Martin and Mullens (2012) sulfur deployed in dustboxes in fur that came out would fall directly onto the bird. The clipped bags cage-free houses achieved mite control even on birds that did not were in the front of the cage near the feed trough, and when sulfur dustbathe, further highlighting the effectiveness of sulfur. released from the clipped bags much of it would fall down and Overall, hanging sulfur dust bags worked very well to control through the wire floor of the cage. northern fowl mites below economically damaging levels in just 1 We were unable to measure how much sulfur actually got onto wk. This technique could be successful in either cages or conven- the birds. We did measure the amount of sulfur lost in each bag tional cage-free facilities. The sulfur used in this study is currently (clipped and hanging) each week in trial 2. Weekly sulfur loss varied labeled for use in poultry at a rate of 200–250 lbs per 20,000 ft2 from 0.2–18.9 g per bag. Loss was difficult to correlate directly with applied as a dust or 25–50 lbs per 100 gallons of water applied as a mite reduction, since bag weight measurements were taken weekly spray. Sulfur only carries the signal word “caution,” though there but the hanging sulfur bag worked more quickly than that. may be an ignition risk when it is suspended densely in air. Applying Preliminary data (unpublished) showed large reductions in mite sulfur via dust bags is a more targeted approached and eliminates numbers in as little as 5 d posttreatment. Daily mite and sulfur the need to apply to large areas, which could be hazardous to work- measurements would yield a better idea of how much sulfur is ers and may miss birds. In caged or cage-free poultry, dust bags required to decrease mite populations. Mullens et al. (2012) applied could be hung near shared resources such as in nest boxes, near a sulfur and water slurry directly to the vent region to treat northern feeders, or in doorways to coops to achieve ectoparasite control. fowl mite-infested birds. Just 0.2 g of sulfur eliminated mites for 4–5 Future work on commercial properties would be useful in refining wk, demonstrating that very small amounts of sulfur are effective how best to use sulfur dust bags, including how frequently they against mites (Mullens et al. 2012). The mode of action of sulfur should be deployed, replaced, or recharged. Using dust bags at the against mites is currently unknown. It probably acts as a fumigant in beginning of a flock cycle, when mite naı̈ve birds are most suscep- the feather layer of hens by reducing to hydrogen sulfide at tible to economic damage by mites (Mullens et al. 2009), would temperatures >21 C (Ware 1993, Mullens et al. 2012). Hen feather likely be the most economical and efficient method of mite control. temperatures in the mite habitation zone are usually well above that, It may even be possible to eliminate mite populations on a poultry and temperatures at the feather base generally are above 30 C (De operation in this manner, which is difficult to achieve with most in- La Riva et al. 2015). secticidal sprays. The dust bag material should be investigated Journal of Economic Entomology, 2016, Vol. 109, No. 5 2233 further to optimize durability and release of sulfur dust over time. Hall, R. D., J. M. Vandepopuliere, F. J. Fischer, J. J. Lyons, and K. E. Doisy. The cotton gauze material worked well enough in this study, but 1983. Comparative efficacy of plastic strips impregnated with permethrin would not likely hold up in a commercial flock. and permethrin dust for northern fowl mite control on caged laying hens. Poult. Sci. 62: 612–615. Sulfur dust is one of the oldest pesticides and has been used for Jones, E. M., and J. B. Kissam. 1983. The effectiveness of polyvinyl chloride northern fowl mite control since the mite was first described on do- plastic bands impregnated with permethrin as a control for the northern mestic poultry (Cleveland 1923). Bishop and Wood (1931) recom- fowl mite, Ornithonyssus sylviarum (Canestrini and Fanzago), infesting mended “flowers of sulphur” in either a liquid dip form or as a dust caged laying chickens. Poult. Sci. 62: 1113–1116. and claimed it would eradicate “feather mites” (northern fowl Kells, S. A., and G. A. Surgeoner. 1996. Dispersion of northern fowl mites, mites), which then were rather new North American poultry pests. Ornithonyssus sylviarum, between poultry facilities via infested eggs from However, the use of a slow release self-treatment dust bag for de- layer and breeder flocks. J. Agric. Entomol. 13: 265–274. ployment in poultry systems is, to our knowledge, a novel technique Lay, D. C., M. Fulton, P. Y. Hester, D. M. Karcher, J. Kjaer, J. A. Mench, B. A. Mullens, R. C. Newberry, C. J. Nicol, N. P. O’Sullivan, et al. 2011. Hen for controlling ectoparasites on poultry. Sulfur dust bags 1) increase welfare in different housing systems. Poult. Sci. 90: 278–294. worker safety relative to broadcast sprays, 2) decrease the environ- Martin, C. D., and B. A. Mullens. 2012. Housing and dustbathing effects on mental impact of pesticides by using small amounts of targeted sul- Downloaded from https://academic.oup.com/jee/article/109/5/2229/2200584 by guest on 07 August 2022 northern fowl mites (Ornithonyssus sylviarum) and chicken body lice fur, and 3) have the potential to be used in caged and cage-free (Menacanthus stramineus) on hens. Med. Vet. Entomol. 26: 323–333. poultry production. Mertens, K., J. Löffel, K. De Baere, J. Zoons, J. De Baerdemaeker, E. Decuypere, and B. 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