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2014 Air Sac Nematode Monopetalonema alcedinis in a Belted Kingfisher (Megaceryle alcyon) in Maryland, USA Ellen Bronson Maryland Zoo in Baltimore, [email protected]

Kathleen Kelly Johns Hopkins University

Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected]

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

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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. Hoberg31Maryland Zoo in Baltimore, 1876 Mansion House Drive, Baltimore, Maryland 21217, USA; 2Department of Molecular and Comparative Pathobiology, Johns Hopkins 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 of Biomedical Sciences, Cornell University, College of Veterinary Medicine, Ithaca, New York 14853, USA; 5Corresponding author (email: [email protected])

ABSTRACT: Sporadic and geographically wide- and crickets), amphibians, and small birds spread reports of parasites affecting the Belted also are consumed (Cornell Laboratory of Kingfisher (Megaceryle alcyon) have been Ornithology 2009). Over the past century, published but few have described details of the pathology. A female, adult kingfisher was information about the diversity and distri- found dead in a heavily wooded area of a zoo in bution of the helminth fauna of kingfishers Maryland, USA. At necropsy, numerous sexu- across North America has increased (Muz- ally dimorphic, 4.4–40.5-cm adult Monopetalo- zall et al. 2011), although implications of nema alcedinis nematodes were found tightly parasitism on the health status of this wound within the coelomic cavity between organs and completely filling the caudal tho- common avian species were not examined. racic and abdominal air sacs. Abundant, 30–60- We describe dramatic lesions and mortal- mm diameter, larvated, thick-walled ova were ity in a Belted Kingfisher from Maryland, found in the bronchi and parabronchi, within USA infected with M. alcedinis. the mesentery, and in the serosa of multiple A female, adult, free-ranging kingfisher coelomic organs. Monopetalonema alcedinis is a characteristic member of the superfamily was found dead in an exhibit pool in a Diplotriaenoidea, a group of nematodes occur- heavily wooded area at the Maryland Zoo ring in birds and reptiles. Infective larvae in Baltimore, Maryland, USA in January within an invertebrate intermediate host are 2009. On gross examination, the bird was ingested and penetrate the intestine, traveling in good body condition. Upon opening the to the lungs and then into the air sacs, where the adult females release eggs. The ova are coelomic cavity, multiple 1–2-mm diame- coughed up by the avian host and passed in ter, 4.4–40.5-cm long, white nematodes feces. Specimens of M. alcedinis have been were found tightly wound within the found in the Belted Kingfisher, although coelomic cavity between organs including typically intensity of infection is low and around the mesentery, liver, and especially infections remain asymptomatic. In contrast, we report the second documented case of high concentrated around the ventriculus. The numbers of M. alcedinis resulting in pathologic parasites appeared to fill the caudal changes in which parasitism contributed to host thoracic and abdominal air sacs complete- mortality. ly (Fig. 1). The air sacs appeared cloudy, Key words: Air sac nematode, Belted thickened, and tan. The serosal surface of Kingfisher, diplotriaenid parasite, Diplotriae- noidea, Megaceryle alcyon, Monopetalonema the ventriculus was thickened, irregular, alcedinis, nematode. and adhered to the mesentery and intes- tines. The adult worms were removed The Belted Kingfisher (Megaceryle al- from the coelomic cavity intact and placed cyon), a member of the Coraciiformes, is in isopropyl alcohol. The specimens were found commonly throughout North Amer- examined, identified, and accessioned into ica along rivers, streams, ponds, and lakes the US National Parasite Collection with clear water and high banks for (USNPC) in Beltsville, Maryland, USA nesting. The diet consists primarily of (USNPC 102692). The nematodes were fishes, but aquatic and terrestrial inverte- identified as adult Monopetalonema alce- brates (crayfish, mollusks, aquatic insects, dinis (Rudolphi 1819) based on the

938 SHORT COMMUNICATIONS 939

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

FIGURE 1. Coelomic cavity of a Belted Kingfish- The bronchi and parabronchi were lined er (Megaceryle alcyon) from Maryland, USA, with with hyperplastic and hypertrophic respi- several individuals of Monopetalonema alcedinis ratory epithelium, and the mucosa occa- between and encompassing the coelomic organs sionally was disorganized with increased and filling the majority of air sac space. numbers of mucous cells. The air sac epithelium was thickened and lined by prominent cuboidal cells occasionally ar- redescription of this species from Ontario, ranged in short papillary projections. Canada (Anderson 1959) and on compar- Similarly, the coelomic serosa was lined ison to voucher specimens in the USNPC. by plump serosal hyperplastic epithelium Nineteen adults were found: Six males and variably thickened by lymphohistiocy- with a mean length of 6.4 cm (4.4–7.3 cm) tic inflammation, most prominently sur- and 13 females with a mean length of rounding the blood vessels. The air sacs 26.2 cm (11.0–40.5 cm). On histologic and mesentery contained a few mineral- examination, numerous 30–60-mm diame- ized larvae. Diffuse, moderate to severe, ter larvated nematode ova with a 1–2-mm pulmonary and meningeal hemorrhage thick, double-contour, refractile wall were was present. In addition, a cross-section found in the bronchi and parabronchi, of a nematode consistent with Capillaria mesentery, air sacs, the serosa of the sp. was present within the mucosa of the pancreas, proventriculus, ventriculus, ventriculus. The proximal cause of death small intestine, ovary, and within the was attributed to acute, severe trauma capsules of the spleen and liver (Fig. 2). with pulmonary and meningeal hemor- In the lung, abundant basophilic mucus rhage. The extensive parasitism and along with eosinophilic cellular debris and marked coelomic tissue reaction were variable lymphocytes, plasma cells, foamy considered contributory. Based on the macrophages, multinucleated cells, and lack of other parasites besides the one lesser numbers of heterophils surrounded Capillaria nematode not associated with basophilic ova containing coiled larvae. inflammation, the pathologic changes 940 JOURNAL OF WILDLIFE DISEASES, VOL. 50, NO. 4, OCTOBER 2014 throughout the coelom not attributed to and mild lymphocytic pneumonia. Hetero- acute trauma appeared to be caused solely granulomatous inflammation surrounded by M. alcedinis. ova and larvae of M. alcedinis in the lungs Monopetalonema alcedinis is in the and other organs with increased mucus in nematode superfamily Diplotriaenoidea, the airways. Adults are reported to punc- a group of parasites distinct from but ture the air sacs and advance into the often misclassified as Filarioidea (Ander- coelomic cavity, causing inflammation and son 2000; Sterner and Cole 2008) due to extensive adhesions between the coelomic similar morphology of the long, thin adults organs, as was demonstrated in this case, and sexual dimorphism. In contrast to most notably around the ventriculus. filarioids, diplotriaenoids do not have a Monopetalonema alcedinis appears to microfilarid stage, and lack hematopha- be a relatively common nematode that is gous insects such as black flies or mosqui- not well documented in the literature in toes as vectors, but instead have fully Belted Kingfishers across North America differentiated first-stage larvae (L1) that (Muzzall et al. 2011). Parasite voucher develop within an insect intermediate host. specimens in the USNPC collected over All diplotriaenids parasitize birds and the past century document the occurrence reptiles and are characterized by thick- of these nematodes in Belted Kingfishers shelled, larvated eggs passed through the from North Carolina (USNPC 17418), intestinal system. Some members of the Texas (43886), Maine (45407), Indiana superfamily are more commonly encoun- (56031), and Arizona (84373). Most pub- tered in air sacs, including Diplotriaena lished reports emanated from eastern and Serratospiculum, and all possess an regions of the continent, and often provide arthropod intermediate host and involve incidental observations based on few hosts, transmission via foraging of the definitive or were summarized in studies of other avian host. Thus, the suggestion by Boyd helminth parasites in Belted Kingfishers and Fry (1971) that simulids or other (Muzzall et al. 2011). These diplotriaenids biting flies are involved in the transmission have a broad geographic distribution, with of M. alcedinis is incorrect (Anderson several species of Monopetalonema occur- 2000). Larvated diplotriaenids eggs are ring as typical parasites in various species of released into the environment via the kingfisher from North America, South feces of the avian host, and L1s are America, Africa, and probably Eurasia subsequently ingested by an invertebrate (Anderson 1959); only M. alcedinis is host. In the insect, the larvae develop into documented in North America. second- and then third-stage larvae (L3) Monopetalonema alcedinis was first before being consumed by birds which documented as causing severe disease in feed on infected intermediate hosts. The a Belted Kingfisher with numerous adult L3 penetrate the intestine of the bird and parasites involving multiple organs and migrate along the hepatic portal system to filling the coelomic cavity of the host the vena cava, the heart, and finally via the (Swanson 1933). In contrast, low intensity pulmonary arteries to the lungs and then was otherwise reported for this diplotriae- air sacs. Here the adults develop and can nid, and infections were subclinical and survive for several years. Ova are depos- asymptomatic. A survey of the arthropod ited into the air sacs, then move into the and helminth parasites of 50 Belted lungs via movement of air and mucus, and Kingfishers from Ontario, Canada and finally are coughed up and swallowed Massachusetts, USA revealed M. alcedinis (Sterner and Cole 2008). in 18% of birds (Boyd and Fry 1971). In this case numerous, large, adult There were 1–8 adult nematodes found in nematodes were associated with chronic each host with an average of three per inflammation and fibrosis of the air sacs bird. The longest nematode was 38 cm SHORT COMMUNICATIONS 941 long. Another survey of the helminths in collection records and identification of birds from Florida, USA revealed M. specimens. alcedinis in four of seven Belted Kingfish- ers, with 2–6 adults per host (Forrester LITERATURE CITED and Spalding 2003). Despite the fact that Anderson RC. 1959. The morphology of Monopeta- this parasite is generally considered to not lonema alcedinis (Rudolphi, 1819) (Nematoda: impact the host, larger numbers of adults Filaroidea) including its first-stage larva. Can J within the air sacs and coelomic cavity can Zool 37:609–614. Anderson RC. 2000. The Superfamily Diplotriaenoi- displace organs, cause inflammation, dis- dea. In: Nematode parasites of vertebrates: Their rupt effective breathing, and cause mor- development and transmission. 2nd Ed. CABI bidity and mortality in rare cases. We Publishing, Wallingford, UK, pp. 535–539. suggest in the present case that parasitism Boyd EM, Fry AE. 1971. Metazoan parasites of the contributed to the cause of death, result- Eastern Belted Kingfisher (Megaceryle alcyon alcyon). J Parasit 57:150–156. ing in weakness and debilitation prior to Cornell Laboratory of Ornithology. 2009. Belted the trauma (i.e., striking a window or Kingfisher (Megaceryle alcyon); The birds of exhibit wall), which caused fatal hemor- North America online. http://bna.birds.cornell. rhage. The bird was found in a pool but edu/bna/species/084. Accessed January 2014. lacked evidence of drowning, suggesting Forrester DJ, Spalding JG. 2003. Miscellaneous that the bird likely died before falling into birds. In: Parasites and diseases of wild birds in Florida. University Press of Florida, Gaines- the water. ville, Florida, pp. 979–1000. We report the first detailed histopath- Muzzall PM, Cook V, Sweet DJ. 2011. Helminths of ologic observations associated with this Belted Kingfishers, Megaceryle alcyon Linnaeus, parasite, which typically is associated with 1758, from a fish hatchery in Ohio, U.S.A. Comp low worm intensity and subclinical dis- Parasitol 78:367–372. ease. Further studies are needed to Sterner MC III, Cole RA. 2008. Diplotriaena, Serratospiculum, and Serratospiculoides. In: identify the intermediate host(s) and Parasitic diseases of wild birds, Atkinson CT, document patterns of transmission in Thomas NJ, Hunter DB, editors. John Wiley and North America. Sons, Inc., Ames, Iowa, pp. 434–438. We thank Nadia Bischof for assistance Swanson G. 1933. A heavy case of internal parasitism with the gross necropsy examination and of the Belted Kingfisher. Wilson Bull 40:80–82. Richard Montali for in-depth discussions and assistance with histology and identifi- Submitted for publication 29 March 2014. cation. Patricia Pilitt assisted with parasite Accepted 28 May 2014.