University of Nebraska - LincolnDigitalCommons@University of Nebraska - LincolnFaculty Publications from the Harold W. ManterLaboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

2014

Air Sac Nematode Monopetalonema alcedinis in aBelted Kingfisher (Megaceryle alcyon) in Maryland,USAEllen BronsonMaryland Zoo in Baltimore, ellen.bronson@marylandzoo.org

Kathleen KellyJohns Hopkins University

Eric P. HobergUnited States Department of Agriculture, Agricultural Research Service, geocolonizer@gmail.com

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Bronson, Ellen; Kelly, Kathleen; and Hoberg, Eric P., "Air Sac Nematode Monopetalonema alcedinis in a Belted Kingfisher (Megacerylealcyon) in Maryland, USA" (2014). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 799.http://digitalcommons.unl.edu/parasitologyfacpubs/799

DOI: 10.7589/2014-03-080 Journal of Wildlife Diseases, 50(4), 2014, pp. 938–941# Wildlife Disease Association 2014

Air Sac Nematode Monopetalonema alcedinis in a Belted Kingfisher

(Megaceryle alcyon) in Maryland, USA

Ellen Bronson,1,5 Kathleen Kelly,2,4 and Eric P. Hoberg3 1Maryland Zoo in Baltimore, 1876 Mansion HouseDrive, Baltimore, Maryland 21217, USA; 2Department of Molecular and Comparative Pathobiology, JohnsHopkins Medicine, 600 N Wolfe Street, Baltimore, Maryland 21287, USA; 3US National Parasite Collection,Agricultural Research Service, US Department of Agriculture, Animal Parasitic Diseases Laboratory, BARC-East,Building 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20705, USA; 4Current address: Department ofBiomedical Sciences, Cornell University, College of Veterinary Medicine, Ithaca, New York 14853, USA;5Corresponding author (email: ellen.bronson@marylandzoo.org)

ABSTRACT: Sporadic and geographically wide-spread reports of parasites affecting the BeltedKingfisher (Megaceryle alcyon) have beenpublished but few have described details ofthe pathology. A female, adult kingfisher wasfound dead in a heavily wooded area of a zoo inMaryland, USA. At necropsy, numerous sexu-ally dimorphic, 4.4–40.5-cm adult Monopetalo-nema alcedinis nematodes were found tightlywound within the coelomic cavity betweenorgans and completely filling the caudal tho-racic and abdominal air sacs. Abundant, 30–60-mm diameter, larvated, thick-walled ova werefound in the bronchi and parabronchi, withinthe mesentery, and in the serosa of multiplecoelomic organs. Monopetalonema alcedinis isa characteristic member of the superfamilyDiplotriaenoidea, a group of nematodes occur-ring in birds and reptiles. Infective larvaewithin an invertebrate intermediate host areingested and penetrate the intestine, travelingto the lungs and then into the air sacs, wherethe adult females release eggs. The ova arecoughed up by the avian host and passed infeces. Specimens of M. alcedinis have beenfound in the Belted Kingfisher, althoughtypically intensity of infection is low andinfections remain asymptomatic. In contrast,we report the second documented case of highnumbers of M. alcedinis resulting in pathologicchanges in which parasitism contributed to hostmortality.

Key words: Air sac nematode, BeltedKingfisher, diplotriaenid parasite, Diplotriae-noidea, Megaceryle alcyon, Monopetalonemaalcedinis, nematode.

The Belted Kingfisher (Megaceryle al-cyon), a member of the Coraciiformes, isfound commonly throughout North Amer-ica along rivers, streams, ponds, and lakeswith clear water and high banks fornesting. The diet consists primarily offishes, but aquatic and terrestrial inverte-brates (crayfish, mollusks, aquatic insects,

and crickets), amphibians, and small birdsalso are consumed (Cornell Laboratory ofOrnithology 2009). Over the past century,information about the diversity and distri-bution of the helminth fauna of kingfishersacross North America has increased (Muz-zall et al. 2011), although implications ofparasitism on the health status of thiscommon avian species were not examined.We describe dramatic lesions and mortal-ity in a Belted Kingfisher from Maryland,USA infected with M. alcedinis.

A female, adult, free-ranging kingfisherwas found dead in an exhibit pool in aheavily wooded area at the Maryland Zooin Baltimore, Maryland, USA in January2009. On gross examination, the bird wasin good body condition. Upon opening thecoelomic cavity, multiple 1–2-mm diame-ter, 4.4–40.5-cm long, white nematodeswere found tightly wound within thecoelomic cavity between organs includingaround the mesentery, liver, and especiallyconcentrated around the ventriculus. Theparasites appeared to fill the caudalthoracic and abdominal air sacs complete-ly (Fig. 1). The air sacs appeared cloudy,thickened, and tan. The serosal surface ofthe ventriculus was thickened, irregular,and adhered to the mesentery and intes-tines. The adult worms were removedfrom the coelomic cavity intact and placedin isopropyl alcohol. The specimens wereexamined, identified, and accessioned intothe US National Parasite Collection(USNPC) in Beltsville, Maryland, USA(USNPC 102692). The nematodes wereidentified as adult Monopetalonema alce-dinis (Rudolphi 1819) based on the

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redescription of this species from Ontario,Canada (Anderson 1959) and on compar-ison to voucher specimens in the USNPC.

Nineteen adults were found: Six maleswith a mean length of 6.4 cm (4.4–7.3 cm)and 13 females with a mean length of26.2 cm (11.0–40.5 cm). On histologicexamination, numerous 30–60-mm diame-ter larvated nematode ova with a 1–2-mmthick, double-contour, refractile wall werefound in the bronchi and parabronchi,mesentery, air sacs, the serosa of thepancreas, proventriculus, ventriculus,small intestine, ovary, and within thecapsules of the spleen and liver (Fig. 2).In the lung, abundant basophilic mucusalong with eosinophilic cellular debris andvariable lymphocytes, plasma cells, foamymacrophages, multinucleated cells, andlesser numbers of heterophils surroundedbasophilic ova containing coiled larvae.

The bronchi and parabronchi were linedwith hyperplastic and hypertrophic respi-ratory epithelium, and the mucosa occa-sionally was disorganized with increasednumbers of mucous cells. The air sacepithelium was thickened and lined byprominent cuboidal cells occasionally ar-ranged in short papillary projections.Similarly, the coelomic serosa was linedby plump serosal hyperplastic epitheliumand variably thickened by lymphohistiocy-tic inflammation, most prominently sur-rounding the blood vessels. The air sacsand mesentery contained a few mineral-ized larvae. Diffuse, moderate to severe,pulmonary and meningeal hemorrhagewas present. In addition, a cross-sectionof a nematode consistent with Capillariasp. was present within the mucosa of theventriculus. The proximal cause of deathwas attributed to acute, severe traumawith pulmonary and meningeal hemor-rhage. The extensive parasitism andmarked coelomic tissue reaction wereconsidered contributory. Based on thelack of other parasites besides the oneCapillaria nematode not associated withinflammation, the pathologic changes

FIGURE 1. Coelomic cavity of a Belted Kingfish-er (Megaceryle alcyon) from Maryland, USA, withseveral individuals of Monopetalonema alcedinisbetween and encompassing the coelomic organsand filling the majority of air sac space.

FIGURE 2. Parasitism of a Belted Kingfisher(Megaceryle alcyon) from Maryland, USA. Numer-ous larvated, thick-walled eggs of Monopetalonemaalcedinis surrounded by mucus and predominantlylymphohistiocytic inflammation with fewer multinu-cleated cells and heterophils. The bronchus is linedwith hypertrophic and hyperplastic respiratory epi-thelium with lymphohistiocytic inflammation. H&Estain; 2003 magnification.

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throughout the coelom not attributed toacute trauma appeared to be caused solelyby M. alcedinis.

Monopetalonema alcedinis is in thenematode superfamily Diplotriaenoidea,a group of parasites distinct from butoften misclassified as Filarioidea (Ander-son 2000; Sterner and Cole 2008) due tosimilar morphology of the long, thin adultsand sexual dimorphism. In contrast tofilarioids, diplotriaenoids do not have amicrofilarid stage, and lack hematopha-gous insects such as black flies or mosqui-toes as vectors, but instead have fullydifferentiated first-stage larvae (L1) thatdevelop within an insect intermediate host.All diplotriaenids parasitize birds andreptiles and are characterized by thick-shelled, larvated eggs passed through theintestinal system. Some members of thesuperfamily are more commonly encoun-tered in air sacs, including Diplotriaenaand Serratospiculum, and all possess anarthropod intermediate host and involvetransmission via foraging of the definitiveavian host. Thus, the suggestion by Boydand Fry (1971) that simulids or otherbiting flies are involved in the transmissionof M. alcedinis is incorrect (Anderson2000). Larvated diplotriaenids eggs arereleased into the environment via thefeces of the avian host, and L1s aresubsequently ingested by an invertebratehost. In the insect, the larvae develop intosecond- and then third-stage larvae (L3)before being consumed by birds whichfeed on infected intermediate hosts. TheL3 penetrate the intestine of the bird andmigrate along the hepatic portal system tothe vena cava, the heart, and finally via thepulmonary arteries to the lungs and thenair sacs. Here the adults develop and cansurvive for several years. Ova are depos-ited into the air sacs, then move into thelungs via movement of air and mucus, andfinally are coughed up and swallowed(Sterner and Cole 2008).

In this case numerous, large, adultnematodes were associated with chronicinflammation and fibrosis of the air sacs

and mild lymphocytic pneumonia. Hetero-granulomatous inflammation surroundedova and larvae of M. alcedinis in the lungsand other organs with increased mucus inthe airways. Adults are reported to punc-ture the air sacs and advance into thecoelomic cavity, causing inflammation andextensive adhesions between the coelomicorgans, as was demonstrated in this case,most notably around the ventriculus.

Monopetalonema alcedinis appears tobe a relatively common nematode that isnot well documented in the literature inBelted Kingfishers across North America(Muzzall et al. 2011). Parasite voucherspecimens in the USNPC collected overthe past century document the occurrenceof these nematodes in Belted Kingfishersfrom North Carolina (USNPC 17418),Texas (43886), Maine (45407), Indiana(56031), and Arizona (84373). Most pub-lished reports emanated from easternregions of the continent, and often provideincidental observations based on few hosts,or were summarized in studies of otherhelminth parasites in Belted Kingfishers(Muzzall et al. 2011). These diplotriaenidshave a broad geographic distribution, withseveral species of Monopetalonema occur-ring as typical parasites in various species ofkingfisher from North America, SouthAmerica, Africa, and probably Eurasia(Anderson 1959); only M. alcedinis isdocumented in North America.

Monopetalonema alcedinis was firstdocumented as causing severe disease ina Belted Kingfisher with numerous adultparasites involving multiple organs andfilling the coelomic cavity of the host(Swanson 1933). In contrast, low intensitywas otherwise reported for this diplotriae-nid, and infections were subclinical andasymptomatic. A survey of the arthropodand helminth parasites of 50 BeltedKingfishers from Ontario, Canada andMassachusetts, USA revealed M. alcedinisin 18% of birds (Boyd and Fry 1971).There were 1–8 adult nematodes found ineach host with an average of three perbird. The longest nematode was 38 cm

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long. Another survey of the helminths inbirds from Florida, USA revealed M.alcedinis in four of seven Belted Kingfish-ers, with 2–6 adults per host (Forresterand Spalding 2003). Despite the fact thatthis parasite is generally considered to notimpact the host, larger numbers of adultswithin the air sacs and coelomic cavity candisplace organs, cause inflammation, dis-rupt effective breathing, and cause mor-bidity and mortality in rare cases. Wesuggest in the present case that parasitismcontributed to the cause of death, result-ing in weakness and debilitation prior tothe trauma (i.e., striking a window orexhibit wall), which caused fatal hemor-rhage. The bird was found in a pool butlacked evidence of drowning, suggestingthat the bird likely died before falling intothe water.

We report the first detailed histopath-ologic observations associated with thisparasite, which typically is associated withlow worm intensity and subclinical dis-ease. Further studies are needed toidentify the intermediate host(s) anddocument patterns of transmission inNorth America.

We thank Nadia Bischof for assistancewith the gross necropsy examination andRichard Montali for in-depth discussionsand assistance with histology and identifi-cation. Patricia Pilitt assisted with parasite

collection records and identification ofspecimens.

LITERATURE CITED

Anderson RC. 1959. The morphology of Monopeta-lonema alcedinis (Rudolphi, 1819) (Nematoda:Filaroidea) including its first-stage larva. Can JZool 37:609–614.

Anderson RC. 2000. The Superfamily Diplotriaenoi-dea. In: Nematode parasites of vertebrates: Theirdevelopment and transmission. 2nd Ed. CABIPublishing, Wallingford, UK, pp. 535–539.

Boyd EM, Fry AE. 1971. Metazoan parasites of theEastern Belted Kingfisher (Megaceryle alcyonalcyon). J Parasit 57:150–156.

Cornell Laboratory of Ornithology. 2009. BeltedKingfisher (Megaceryle alcyon); The birds ofNorth America online. http://bna.birds.cornell.edu/bna/species/084. Accessed January 2014.

Forrester DJ, Spalding JG. 2003. Miscellaneousbirds. In: Parasites and diseases of wild birdsin Florida. University Press of Florida, Gaines-ville, Florida, pp. 979–1000.

Muzzall PM, Cook V, Sweet DJ. 2011. Helminths ofBelted Kingfishers, Megaceryle alcyon Linnaeus,1758, from a fish hatchery in Ohio, U.S.A. CompParasitol 78:367–372.

Sterner MC III, Cole RA. 2008. Diplotriaena,Serratospiculum, and Serratospiculoides. In:Parasitic diseases of wild birds, Atkinson CT,Thomas NJ, Hunter DB, editors. John Wiley andSons, Inc., Ames, Iowa, pp. 434–438.

Swanson G. 1933. A heavy case of internal parasitismof the Belted Kingfisher. Wilson Bull 40:80–82.

Submitted for publication 29 March 2014.Accepted 28 May 2014.

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