Veterinary Parasitology 246 (2017) 30–37

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Veterinary Parasitology

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Review article A review of the biology, ecology, and control of the northern fowl mite, MARK Ornithonyssus sylviarum (Acari: Macronyssidae) ⁎ Amy C. Murillo , Bradley A. Mullens

Department of Entomology, University of California, Riverside, CA 92521, United States

ARTICLE INFO ABSTRACT

Keywords: The northern fowl mite, Ornithonyssus sylviarum (Canestrini & Fanzago, 1877), is found on several continents and Mesostigmata has been a major pest of poultry in the United States for nearly a century. Lack of earlier USA reports in the Macronyssidae United States suggests an introduction or change to pest status in domestic poultry systems occurred in the early Ornithonyssus sylviarum 1900s. Though predominantly a nest-parasite of wild birds, this obligate hematophagous mite is a permanent Mite ectoparasite on domestic birds, especially egg-laying chickens. Economic damage is incurred by direct blood Poultry feeding and activation of the of host’s immune responses. This in turn causes decreased egg production and feed Chicken conversion efficiency, and severe infestations can cause anemia or death to birds. Here we review the biology, ecology, and recent control measures for the northern fowl mite. Photomicrographs are included of adult males and females, protonymphs, and larvae with key characters indicated. Special emphasis is placed on current knowledge gaps of basic and applied science importance.

1. Introduction Bishopp and Wood (1917), in reviewing USA poultry pests, ad- dressed many arthropods, prominently including the red mite Derma- The northern fowl mite (NFM), Ornithonyssus sylviarum nyssus gallinae (DeGeer), but notably did not mention O. sylviarum. The (Canestrini & Fanzago, 1877) is the most common and damaging ecto- northern fowl mite was first recorded in the USA in Maryland in 1917 parasite of poultry in the United States (Axtell and Arends, 1990; Hinkle as “a slight variety of Liponyssus bursa Berlese [tropical fowl mite, Or- and Hickle, 1999; Mullens et al., 2009). It is an obligate hematophagous nithonyssus bursa]” and was first recognized as a potentially serious mite that causes direct damage to poultry and decreased economic poultry pest by Wood (1920). Wood (1920) referred to NFM as the output. Severe infestations and economic damage occur primarily in “feather mite” because it was seen occupying the vent feathers of egg-laying chickens (hens) or breeders (chickens or turkeys), which are chickens. Given the known association of NFM with the highly an- raised for longer periods of time than other poultry types (such as meat thropophilic house sparrow in Europe, it is tempting to speculate that birds). This allows high mite populations to develop and be maintained. sparrows, nesting peridomestically and very near chicken coops over an The reader is referred to the comprehensive, annotated review of extended period of time, may have been the origin of the eventual NFM Hogsette et al. (1991) for older literature. This review will focus on establishment in USA poultry. Early records on poultry premises found research carried out since that review, with select older papers high- NFM in sparrow nests, and it was recommended that these nests be lighted and an emphasis on NFM in domestic poultry species. “destroyed by fire” to protect poultry (Wood, 1920). By the early 1930s O. sylviarum merited prominent mention in an updated poultry pest 2. History and distribution of NFM as a poultry pest review, having become a poultry pest “during the last few years” (Bishopp and Wood, 1931). While wild birds harbor and can introduce Many North American records indicate that over 70 species of wild northern fowl mites to domestic poultry, once introduced to a property birds can serve as hosts for NFM (Knee and Proctor, 2007). The North mite populations probably persist on premises between flocks by hiding American NFM host records include two exotic abundant bird species in cracks and crevices or wild bird nests. In addition to introduction intentionally introduced into the USA from Europe in the mid-late from wild bird populations, NFM can also be readily moved around via 1800s (Tenner, 1996): the common starling, Sturnus vulgaris L. and the people, equipment, or rodents (Kells and Surgeoner, 1997; Axtell, house sparrow, Passer domesticus (L.) The house sparrow, in particular, 1999). is known to harbor NFM in Europe (Szabo et al., 2002). Though widespread, NFM is not a major problem in commercial

⁎ Corresponding author. E-mail address: [email protected] (A.C. Murillo). http://dx.doi.org/10.1016/j.vetpar.2017.09.002 Received 18 July 2017; Received in revised form 31 August 2017; Accepted 1 September 2017 0304-4017/ © 2017 Elsevier B.V. All rights reserved. A.C. Murillo, B.A. Mullens Veterinary Parasitology 246 (2017) 30–37 poultry uniformly across the globe. It is considered a key pest of laying undeveloped mouthparts. The mouthparts of the very active proto- hens in North America (see above), Brazil (Soares et al., 2008; Rezende nymphs are well set up for blood-feeding, while the sternal and ventral et al., 2013), China (Pan et al., 2009; Wang et al., 2010), and Australia plates of the transitional deutonymphs (non-blood-feeding) are fused (Levot, 1992). While the NFM is known from poultry in western Europe (Fig. 4). (e.g., Bruneau et al., 2002; Jansson et al., 2014) it is not comparable to Northern fowl mites are haplodiploid with female-biased (ca. 4–1) Europe’s problems with the red mite D. gallinae (Sparagano et al., sex ratios (Oliver, 1965; Mašán and Országhová, 1995). McCulloch and 2014). The reasons for this disparity are unclear and are discussed by Owen (2012) showed that unmated females can lay unfertilized eggs Roy et al. (2010). which produce male offspring (arrhenotoky); females then mate with their sons to produce fertilized eggs and female offspring (oedipal mating). Thus, introduction of a single unmated female, even if im- 3. Identification and life history mature, may be all that is required to infest a new host. When infesting chickens, NFM eggs are laid primarily onto feathers Ornithonyssus sylviarum is the type species in the genus (Radovsky, of the vent region. This region, just anterior to the cloaca, offers the 2007). Ornithonyssus sylviarum closely resembles the tropical fowl mite optimum feather structure and microclimate that is favored by mites, O. bursa (Berlese) in life history and appearance. However, O. bursa is though mites will occasionally occupy the area posterior to the cloaca, found mainly in subtropical and tropical regions. Though O. bursa is a as the skin temperature in the vent region is lower than under the wings pestiferous poultry mite, even in Brazil O. sylviarum is the more severe and the humidity is higher (DeVaney and Beerwinkle, 1980; Hogsette commercial poultry pest (Rezende et al., 2013). In a comprehensive 3- et al., 1991; Halbritter and Mullens, 2011; Murillo et al., 2016). Dense year survey of NFM on 26 southern California caged layer poultry farms clusters of mites, cast exuviae, copious mite feces and matted feathers from 1999 to 2001, only one farm had some (not all) mites that were (Fig. 5) create somewhat porous microhabitats that may be several cm morphologically identified as O. bursa or possibly O. sylviarum-O. bursa thick, especially if multiple feathers are essentially “glued” together by hybrids (Mullens et al., 2004). A useful key character for separating mite debris. The humidity in such microhabitats has not been mea- slide-mounted Ornithonyssus is that adult females of O. bursa or O. bacoti sured, but likely approaches 100%. Wood (1920) described NFM living (Hirst) (tropical rat mite) have the last pair of setae on the dorsal shield, on the fluffy down feathers lining house sparrow nests; the vent feathers while they are off the posterior edge of the shield in O. sylviarum. While of adult chickens have a large down section and often a secondary this character is fluid (there may be 1 seta off and 1 seta on O. syl- feather at the base and vent feather structure may be an important viarum) it is easier to observe than dorsal setal pattern or relative dorsal characteristic for permanent NFM on-host survival. This down layer shield shape. essentially provides a “nestlike” environment directly on the body of Superficially O. sylviarum resembles another common and eco- the chicken, and enables NFM to complete the entire life cycle on nomically important poultry ectoparasitic mite, the chicken red mite D. chicken hosts. The entire feather layer is about 3–6 cm deep and mite gallinae. However, the two species are readily distinguished morpho- position on individual feathers is influenced by ambient temperatures, logically (Weisbroth, 1960; Di Palma et al., 2012). The anal shields of suggesting that mites thermoregulate over distances of several cm adult females are distinctly different, with O. sylviarum having a tear- within this region, settling in zones of 28–30 °C if available (Halbritter drop-shaped anal plate compared to D. gallinae’s square or keystone- and Mullens, 2011; De La Riva et al., 2015). shaped anal plate (Fig. 1). Adult O. sylviarum are generally smaller (ca. The northern fowl mite life cycle was studied by a few early re- 0.6 mm) than D. gallinae adults (ca. 1.5 mm). They differ prominently searchers such as Cameron (1938), but was first described in substantial by the claw-like chelicerae of O. sylviarum compared to whip-like che- detail and under controlled conditions by Sikes and Chamberlain licerae of D. gallinae (Fig. 2). (1954). Eggs hatch into hexapod larvae, a rather sessile, non-feeding Within O. sylviarum, females have a distinct sternal plate (Fig. 1) stage that lasts about a day. This is followed by an active and blood- whereas males have a fused genito-ventral plate (Fig. 3). Male O. syl- feeding protonymph stage and a non-feeding deutonymph stage, before viarum have visible spermatodactyls, specialized organs for sperm molting into active, blood-feeding adults. The entire life cycle requires transfer, between the fixed and movable digits of the chelicerae (Fig. 3). ca. 5–12 days to complete (Fig. 6). Large numbers of mites are highly While the mate-finding and copulatory behaviors of northern fowl visible on infested birds; feathers look “dirty” because of the collection mites have not been described, based on other Dermanyssina it is pre- of mites, cast skins, eggs, and mite feces. Mites are able to survive off- sumed that sperm from the primary genital opening (Fig. 3) is collected host for periods of at least 1–3 weeks; protonymphs survive much better by the spermatodactyl before transfer to the female genital opening than adults and survival of both stages is worse at higher temperatures (Walter and Proctor, 1999). NFM larvae are hexapod and have

Fig. 1. Ornithonyssus sylviarum (left) and Dermanyssus gallinae (right) adult females cleared and slide-mounted in Hoyer’s medium (100×). The anal plates (a) are distinct, with O. sylviarum being teardrop- shaped and D. gallinae being keystone- shaped. Additionally O. sylviarum has a dis- tinct sternal shield (ss) and D. gallinae’s re- tracted whip-like chelicerae are visible (mp). Dermanyssus gallinae are larger than O. sylviarum.

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