AN UNIDENTIFIED FILARIAL SPECIES AND ITS IMPACT ON FITNESS IN WILD POPULATIONS OF THE BLACK-FOOTED FERRET (MUSTELA NIGRIPES)

Disease can threaten the restoration of endangered species directly by substantially decreasing host survival or indirectly via incremental decreases in survival and reproduction. During a biomedical survey of reintroduced populations of the highly endangered black-footed ferret from 2002 to 2005, microfilariae discovered in the blood were putatively identified as Dirofilaria immitis, and widespread screening was initiated using a commercially available antigen-based ELISA test. A subset of animals (n=16) was screened for D. immitis using a highly sensitive PCR-based assay. Microfilariae were also molecularly and morphologically characterized. Of 198 animals at six reintroduction sites, 12% had positive results using the ELISA test. No antigen-positive animals which were screened via PCR (n=11) had positive PCR results, and all antigen-positive animals (n=24) were asymptomatic. No significant differences were found in body mass of antigen-positive (male: 1223±82 g [mean±SD], female: 726±75 g) vs. antigen-negative (male: 1,198±119 g, female: 710±53 g) individuals (P=0.4). Antigen prevalence was lower in juveniles (3%) than adults (12%; P=0.03), and higher in in situ, captive-reared individuals (33%) than wild-born individuals (10%; P=0.005). Morphologic analysis of microfilariae revealed they were neither D. immitis nor any other previously characterized North American species. PCR amplification of the 5S spacer region of rDNA revealed that the filarial sequence shared only 76% identity with D. immitis. This previously unidentified filarial sequence was present in all antigen positive animals (11 of 11 tested). It appears that black-footed ferrets were infected with a previously undescribed species of filaria whose antigen cross-reacted with the ELISA assay, although further analysis is needed to make a conclusive statement. Nonetheless, this previously undescribed filaria does not appear to threaten recovery for this highly endangered mammal.

[1]  Charles F. Code,et al.  Handbook of Physiology; a Critical, Comprehensive Presentation of Physiological Knowledge and Concepts , 2011 .

[2]  Victoria J. Bakker,et al.  SEROLOGIC SURVEY OF THE ISLAND SPOTTED SKUNK ON SANTA CRUZ ISLAND , 2006 .

[3]  J. Guerrero,et al.  Epidemiology of heartworm: what is happening in South America and Mexico? , 2005, Veterinary parasitology.

[4]  H. Weimerskirch.  Diseases threaten Southern Ocean albatrosses , 2004, Polar Biology.

[5]  M. Tewes,et al.  Helminths of the Ocelot from Southern Texas , 2003, Journal of wildlife diseases.

[6]  B. Sacks,et al.  RECONSTRUCTING THE SPREAD OF DIROFILARIA IMMITIS IN CALIFORNIA COYOTES , 2003, The Journal of parasitology.

[7]  W. Karesh,et al.  Putting Theory into Practice: Wildlife Health in Conservation , 2001 .

[8]  G. Roemer,et al.  SPATIAL AND TEMPORAL VARIATION IN THE SEROPREVALENCE OF CANINE HEARTWORM ANTIGEN IN THE ISLAND FOX , 2000, Journal of wildlife diseases.

[9]  E. Kanda,et al.  Prevalence of dirofilarial infection in raccoon dogs in Japan. , 2000, Parasitology international.

[10]  B. Sacks,et al.  Effects of canine heartworm (Dirofilaria immitis) on body condition and activity of free-ranging coyotes (Canis latrans) , 2000 .

[11]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[12]  C. Marks,et al.  Canine heartworm (Dirofilaria immitis) detected in red foxes (Vulpes vulpes) in urban Melbourne. , 1998, Veterinary parasitology.

[13]  J. Mccall.  Dirofilariasis in the domestic ferret. , 1998, Clinical techniques in small animal practice.

[14]  G. Plumb,et al.  Ketamine-medetomidine or isoflurane immobilization of black-footed ferrets , 1998 .

[15]  C. Packer,et al.  A canine distemper virus epidemic in Serengeti lions (Panthera leo) , 1996, Nature.

[16]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[17]  Steven A. Williams,et al.  Molecular phylogenetic studies on filarial parasites based on 5S ribosomal spacer sequences. , 1994, Parasite.

[18]  Weissman Bw.  Raccoon heartworm causing a facial mass. , 1992 .

[19]  M. Scott.  The Impact of Infection and Disease on Animal Populations: Implications for Conservation Biology , 1988 .

[20]  E. Williams,et al.  Disease and Endangered Species: The Black‐footed Ferret as a Recent Example , 1988, Conservation Biology.

[21]  M. L. Eberhard.  Brugia lepori sp. n. (Filarioidea: Onchocercidae) from rabbits (Sylvilagus aquaticus, S. floridanus) in Louisiana. , 1984, The Journal of parasitology.

[22]  C. Bartlett.  Zoogeography and taxonomy of Dirofilaria scapiceps (Leidy, 1886) and D. uniformis Price, 1957 (Nematoda: Filarioidea) of lagomorphs in North America , 1983 .

[23]  J. Smith.  Redescription of Dipetalonema (Acanthocheilonema) procyonis Price 1955 (Nematoda: Filarioidea from the raccoon. , 1980, The Journal of parasitology.

[24]  R. May,et al.  Regulation and Stability of Host-Parasite Population Interactions: I. Regulatory Processes , 1978 .

[25]  W. R. Davidson.  Dirofilariaformia pulmoni sp. n. (Nematoda: Onchocercidae) from the eastern gray squirrel (Sciurus carolinensis Gmelin). , 1975, The Journal of parasitology.

[26]  R. Sheets.  A Trap for Capturing Black-Footed Ferrets , 1972 .

[27]  R. Warner.  THE ROLE OF INTRODUCED DISEASES IN THE EXTINCTION OF THE ENDEMIC HAWAIIAN AVIFAUNA , 1968 .

[28]  P. Beaver,et al.  Morphology and relationship of Dirofilaria tenuis and Dirofilaria conjunctivae. , 1965, The American journal of tropical medicine and hygiene.

[29]  W. A. Webster,et al.  DIPETALONEMA MEPHITIS N. COMB. (=MICROFILARIA MEPHITIS: WEBSTER AND BEAUREGARD, 1964) FROM THE SKUNK, MEPHITIS MEPHITIS. , 1965, Canadian journal of zoology.

[30]  L. Ash,et al.  BRUGIA BEAVERI SP. N. (NEMATODA: FILARIOIDEA) FROM THE RACCOON (PROCYON LOTOR) IN LOUISIANA. , 1964, The Journal of parasitology.

[31]  W. H. Wright,et al.  The occurrence of a dog filariid other than Dirofilaria immitis in the United States. , 1956, The Journal of parasitology.

[32]  R. C. Anderson,et al.  Dipetalonema sprenti n.sp. from Castor canadensis Kuhl , 1953, Parasitology.

[33]  P. R. Highby.  Dipetalonema arbuta n.sp. (Nematoda) from the porcupine, Erethizon dorsatum (L.). , 1943 .

[34]  B. Weissman.  Raccoon heartworm causing a facial mass. , 1992, Southern medical journal.

[35]  T. C. Orihel,et al.  Loaina gen. n. (Filarioidea: onchocercidae) for the Filariae parasitic in rabbits in North America , 1984 .

[36]  L. Ash,et al.  OCCURRENCE OF DIROFILARIA STRIATA IN THE BOBCAT (LYNX RUFUS) IN LOUISIANA WITH OBSERVATIONS ON ITS LARVAL DEVELOPMENT. , 1964, The Journal of parasitology.

[37]  D. L. Price.  Description of Dipetalonema interstitium n.sp. from the grey squirrel and Dipetalonema llewellyni n.sp. from the raccoon. , 1962 .