If you don’t look, you’ll never find anything: Nematode biodiversity where you least expect it


Gary Phillips and Ernest C. Bernard

University of Tennessee at Knoxville

Entomology, Nematology and Plant Pathology


  Narceus gordanus  (yellow millipedes) – the host for  Heth pivari  and  Coronostoma claireae.  As many as 1,700 nematodes have been found in just one millipede!

Narceus gordanus (yellow millipedes) – the host for Heth pivari and Coronostoma claireae. As many as 1,700 nematodes have been found in just one millipede!

  Heth pivari  (male and female) –  Heth  females are easily identified by their cuticular ornamentation and unique head morphology.

Heth pivari (male and female) – Heth females are easily identified by their cuticular ornamentation and unique head morphology.

  Coronostoma claireae  (a predatory nematode) – DIC image on left and SEM on right. Note the lack of a grinding valve, the muscular esophagus, very large first annule and the projecting, conical amphids.

Coronostoma claireae (a predatory nematode) – DIC image on left and SEM on right. Note the lack of a grinding valve, the muscular esophagus, very large first annule and the projecting, conical amphids.

The discovery of life that is new to science is a feeling that few will ever experience. However, if you take the time to look, new life abounds around all of us, especially in places that you would never think to look. In the late 1840s, Dr. Joseph Leidy, “the last man to know everything,” and the father of American parasitology, was the first to describe several new species of nematodes living in the hindgut of a millipede he identified as Julus marginatus (=Narceus americanus). Dr. Leidy identified a small group of nematodes that belong to the infraorders Rhigonematomorpha and Oxyuridomorpha, such as Ascaris infecta (=Rhigonema infecta), Streptostomum agile (=Aorurus agile), and Thelastomum attenuatum (=Thelsatoma attenuatum). These nematodes appear to be harmless to their millipede hosts and the diversity of life within their intestinal tracts is quite surprising.

During the past 170 years, only a few dozen researchers worldwide have conducted research on this understudied group of nematodes. Our lab is attempting to pick up where Leidy left off. Beginning in 2013, we set off to conduct a comprehensive analysis of nematodes living commensally inside the intestines of millipedes and to identify and describe the many species we expected to discover.

Our first discoveries came in 2014 when we went on a collecting trip to the Ocala National Forest in central Florida. In the early morning hours, we collected several specimens of millipedes called Narceus gordanus, one of the largest diplopods in North America. Upon dissection, we observed a nematode that neither of us recognized. After several weeks of research, we finally identified the genus of this mystery nematode as Coronostoma sp. Coronostoma spp. are unique because they are nematophagous (predators on other nematodes), not bacterivores, as are all the other nematodes living inside the guts of millipedes. Coronostoma spp. lacks a grinding valve, has a very muscular esophagus and conical, projecting amphids. Of the nearly 79,000 nematodes that we have collected during the past five years, we’ve only found 198 specimens of Coronostoma, and of the 198, only 17 were males. After two years of careful study, we named this nematode Coronostoma claireae, after Gary’s daughter, who actually found the millipede host (Phillips et al., 2016).

Coronostoma was not thought to inhabit North America, as the six known species (described between 1958 and 2014) were known only from the tropics. Since the beginning of our research, we have identified at least six undescribed species, three indigenous to temperate interior North America and three in an African diplopod.

In addition to discovering C. claireae, we found specimens of Heth, also a large genus of 49 species, all of which were described from millipedes in tropical areas.  Dr. Ramon Carreno and colleagues (2013) discovered Heth mauriesi in an introduced millipede, Anadenobolus monilicornis from Key Largo, Florida, the first report of Heth north of Mexico. This nematode was first described from Martinique in A. politus.  Recently we collected a distinct species (Heth pivari), again from the indigenous Florida millipede, Narceus gordanus. Heth spp. are unique in their head morphology and cuticular ornamentation and are easily recognized by their rapidly swiveling head movements.

Since our research began, we have dissected 1,175 millipedes spanning six orders, 18 families and 61 species from 21 states. We have extracted nearly 79,000 nematodes belonging to nine families and have discovered about 25 new species of nematodes. Among the more unique nematodes we’ve found is a species of the genus Golovatchinema, originally found only in a spirobolid millipede, Rhinocricus sp., from Cuba (Spirinidov, 1984). In 2017, we examined the intestinal nematofauna of an African millipede and discovered several new species of nematodes, including a second species of Golovatchinema. This nematode is unlike any other that we have seen living commensally in millipedes. The head of the third-stage juvenile resembles the parasite that popped out of the chest of the character Kane (John Hurt) in the 1979 movie Alien. The J3 head is apparently unique in the nematode world and this stage bears no resemblance to the adult.

Golovatchinema, Coronostoma, and Heth are just a few examples of the many nematodes that we have discovered in a common backyard organism. Millipedes are good host organisms for nematodes and for those that are budding nematode taxonomists, they offer numerous species to be discovered and studied. One only needs to look beyond classical nematology and examine understudied host organisms to find life where you least expect it.

  Rhigonema  sp. – a common nematode found in numerous species of millipedes. Photo courtesy of Dr. Jon Eisenback

Rhigonema sp. – a common nematode found in numerous species of millipedes. Photo courtesy of Dr. Jon Eisenback

 
  Golovatchinema  sp. – SEM of the 3rd stage juvenile. This juvenile stage bears no resemblance to the adults.

Golovatchinema sp. – SEM of the 3rd stage juvenile. This juvenile stage bears no resemblance to the adults.

Carreno R.A., Ordosch, D., Koltek, J.K., Hamill, D.R., Tuhela, L. 2013. First United States records of the rhigonematid genera Heth and Ruizia (Nematoda: Rhigonematida) from the introduced millipede, Anadenobolus monilicornis (Diplopoda: Rhinocricidae) in Key Largo, Florida, U.S.A. Comparative Parasitology 80(2):225–232. 

Phillips, G., Bernard, E. C., Pivar, R. J., Moulton, J. K., and Shelley, R. M. 2016. Coronostoma claireae n. sp. (Nematoda: Rhabditida: Oxyuridomorpha: Coronostomatidae) from the Indigenous Milliped Narceus gordanus

(Chamberlain, 1943) (Diplopoda: Spirobolida) in Ocala National Forest, Florida. Journal of Nematology 48(3): 159-169.

Spiridonov, S. E. 1984. New species of oxyurids from intestine of Diplopoda, Rhinocricus sp. Trudy Zoologicheskogo Instituta 126: 33-49.

 
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