Defining parasite biodiversity at high latitudes of North America: new host and geographic records for Onchocerca cervipedis (Nematoda: Onchocercidae) in moose and caribou

Abstract

BackgroundOnchocerca cervipedis is a filarioid nematode of cervids reported from Central America to boreal regions of North America. It is found primarily in subcutaneous tissues of the legs, and is more commonly known as ‘legworm’. Blackflies are intermediate hosts and transmit larvae to ungulates when they blood-feed. In this article we report the first records of O. cervipedis from high latitudes of North America and its occurrence in previously unrecognized host subspecies including the Yukon-Alaska moose (Alces americanus gigas) and the Grant’s caribou (Rangifer tarandus granti).MethodsWe examined the subcutaneous connective tissues of the metacarpi and/or metatarsi of 34 moose and one caribou for parasitic lesions. Samples were collected from animals killed by subsistence hunters or animals found dead in the Northwest Territories (NT), Canada and Alaska (AK), USA from 2005 to 2012. Genomic DNA lysate was prepared from nematode fragments collected from two moose. The nd5 region of the mitochondrial DNA was amplified by PCR and sequenced.ResultsSubcutaneous nodules were found in 12 moose from the NT and AK, and one caribou from AK. Nematodes dissected from the lesions were identified as Onchocerca cervipedis based on morphology of female and male specimens. Histopathological findings in moose included cavitating lesions with multifocal granulomatous cellulitis containing intralesional microfilariae and adults, often necrotic and partially mineralized. Lesions in the caribou included periosteitis with chronic cellulitis, eosinophilic and lymphoplasmacytic infiltrate, and abundant granulation associated with intralesional adult nematodes and larvae. Sequences of the nd5 region (471bp), the first generated for this species, were deposited with Genbank (JN580791 and JN580792). Representative voucher specimens were deposited in the archives of the United States National Parasite Collection.ConclusionsThe geographic range of O. cervipedis is broader than previously thought, and extends into subarctic regions of western North America, at least to latitude 66°N. The host range is now recognized to include two additional subspecies: the Yukon-Alaska moose and Grant’s caribou. Accelerated climate change at high latitudes may affect vector dynamics, and consequently the abundance and distribution of O. cervipedis in moose and caribou. Disease outbreaks and mortality events associated with climatic perturbations have been reported for other filarioids, such as Setaria tundra in Fennoscandia, and may become an emerging issue for O. cervipedis in subarctic North America.

A cryptic species of Onchocerca (Nematoda: Onchocercidae) in blackflies (Simulium spp.) from southern California, USA

“…There is a need to reassess the type-material of O. cervipedis , and to further characterize specimens collected from the two hosts, and ideally from the original localities using integrated classical and molecular tools. At this stage, it cannot be determined if either O. cervipedis sensu Verocai et al, 2012 [ 11 ] or the cryptic species isolated in the present study and in the skin of WTD in New York belong to O. cervipedis as originally described. The potential for zoonotic infections among species of Onchocerca establishes the need to characterize the recently recognized cryptic species, to explore for broader currently hidden diversity and to define the host and geographical limits within this assemblage.…”

“…To date in North America only one species, O. cervipedis , has been formally described and has been reported to infect five species of cervids and the pronghorn [ 8 , 11 , 12 ]. Our work provides further evidence for the existence of a cryptic, undescribed species of Onchocerca associated with wild ungulates in North America [ 7 ].…”

“…is atypical among species of Onchocerca , with only a few species known to infect multiple hosts [ 1 ]. The O. cervipedis species complex encompasses an extensive geographical distribution, ranging from tropical forests in Costa Rica, Central America [ 10 ] to subarctic environs of northern North America [ 11 ]. The original description of O. cervipedis by Wehr & Dikmans [ 8 ] was based on specimens collected from the subcutaneous tissues of the hindquarters, ankles and foot of two hosts and localities: white-tailed deer from Montana, USA, and Columbia black-tailed deer ( O. h. columbianus ) from British Columbia, Canada.…”

“…In addition to these observations from Asia, there is molecular evidence for a cryptic species infecting the white-tailed deer Odocoileus virginianus (Zimmermann) from North America [ 7 ]. Until recently, Onchocerca cervipedis Wehr & Dikmans, 1935 was the only recognized species infecting wild ungulates across North and Central America, and it remains the only formally described species [ 8 – 11 ]. Its reported host range includes five cervids: the white-tailed deer; the mule deer Odocoileus hemionus (Rafinesque); moose Alces americanus (Clinton); elk or wapiti Cervus canadensis Erxleben; and caribou Rangifer tarandus (L.); and also, the antilocaprid pronghorn Antilocapra americana Ord [ 8 , 10 – 19 ].…”

Isolation ofOnchocerca lupiin Dogs and Black Flies, California, USA

“…flies are known to be vectors for several Onchocerca species for which sequence data are not available ( 33 , 34 ). However, previous studies have suggested that sequence variation in the mitochondrial genome varies from 7% to 15% among Onchocerca species ( 9 , 35 ), and intraspecies variation within the mitochondrial genome is limited in the genus Onchocerca ( 9 , 35 ). Therefore, the sequences detected in the flies are unlikely to have derived from a species other than O. lupi .…”