Why Parasites?

Brief intro from Dr. Rollins

Ten years ago we sat in a motel room in Sweetwater with a team of 10 scientists from Texas A&M, Texas A&M – Kingsville, Texas Tech University, and the University of North Texas.  We had been given a charge from Rick Snipes, President of the Rolling Plains Quail Research Foundation.  Our charge was to design and conduct a comprehensive scientific investigation into disease (in the broadest context) as a possible explanation for the decline of bobwhites in the Rolling Plains.  Over the next 24 hours, we pondered pathogens and parasites, and the procedures and collaborations that would be necessary to pull it off.

Read more about this project

RPQRF’s Position Statement on Eyeworms & Cecal Worms

(revised 2-21)

Introduction

  • Researchers at RPQRR have investigated infections of helminths (parasitic worms) in bobwhites since 2009. Results from our “Operation Idiopathic Decline” initiative subsequently prompted much interest, effort, and dollars in subsequent studies.
  • Research on eyeworms and cecal worms, and their potential impacts on quail populations, can be contentious. The following position statement has been approved by RPQRF’s Board of Directors.
  • Historical background- Operation Idiopathic Decline canvassed 35 counties across west Texas and western Oklahoma, see Figure 1. Bobwhite and scaled quail were trapped in Aug and Oct 2011-13 and birds sampled for various pathogens. The prevalence of eyeworms and cecal worms, see Figure 2, across these sites prompted subsequent research to determine possible impacts on quail populations.
  • Key terms used in this discussion
    • Prevalence – proportion of individuals in a population that are infected by a species of parasite; expressed as percent.
    • Intensity – the number of parasites of a given species (e.g., eyeworms) for only the infected subset of individuals in a population.
    • Example: If ten bobwhites are examined for eyeworms and half are infected (n =5), then prevalence is 50% (5/10). If each infected bobwhite has 7 worms, the average intensity is 7 worms per bird.

What We Know: Eyeworms

  • Eyeworms were first documented infecting bobwhites in 1959 in Cottle County (Matador wildlife Management Area).
  • Infection rates reported were similar (e.g., prevalence, intensity) as seen in contemporary studies. (source: reports from TPWD from the Matador WMA));
  • Subsequent research on helminths (parasitic worms) in quails mostly failed to investigate the importance of eyeworms as researchers tended to examine only the intestines and ignore the eyes (especially the tissues behind the eyeballs). Hence, these early reports were conservative estimates of prevalence and intensity.
  • See Appendix Table 1 for a comparison of infection levels across various areas and time periods.
  • Bobwhites in the Rolling Plains ecoregion of Texas have the highest documented prevalence and intensity of eyeworms in the country to date. See Figure 3.
  • Eyeworms are 8X more prevalent in bobwhite from Rolling Plains vs South Texas Plains;
  • Prevalence of eyeworms in the Rolling Plains varies year-to-year and ranch-to-ranch. Among years and across ranches, prevalence of eyeworms across the Rolling Plains averaged 59.7%.
  • Since 2017 the RPQRR has monitored eyeworm dynamics in bobwhites across multiple counties in Texas, see Figure 4. The average intensity observed across all counties in 2017 was 19.2 worms per bird. Several counties reported average intensities of >30 worms per bird.
  • Intensity also varies from year to year and site to site. Average intensity on various ranches sampled in the Rolling Plains during 2014–2016 was 16.2 worms per bird. See Figure 5.
  • Bobwhite accumulate eyeworms over time. Thus, prevalence and intensity are higher in adults than juveniles. “Poor” quail seasons (e.g., 2019) will yield higher eyeworm prevalence and intensities because few juvenile quail are present in the population.
  • Eyeworms feed on interstitial fluids, blood, and tissues behind the eyes of their hosts.
  • Eyeworm presence may cause keratitis (scarring of the cornea) and other symptoms indicative of inflammation.
  • As many as 24 potential intermediate hosts have been identified including cockroaches, field crickets, and several species of grasshoppers which are all key food components for quail.
  • Techniques for assessing prevalence in the field have been tested by RPQRR; these examinations are 70-80% accurate for gauging prevalenc, see Figure 8.
  • New molecular techniques are available to allow for on-site, non-lethal sampling of quail to detect eyeworm infection.
  • Infections in scaled quail are typically about 25% of those observed in bobwhites.

What We Know: Cecal Worms

  • Across their range, bobwhites are parasitized by numerous species of cecal nematodes, or roundworms, in the middle part of the quail’s gut (ceca). The most frequently occurring cecal worm in the Rolling Plains and South Texas is A. pennula.
  • Prevalence and intensity vary by year and site. On average, prevalence of A. pennula is approximately 85% for bobwhite in the Rolling Plains, typically less in south Texas.
  • A. pennula is an “imbibing” (i.e., free-floating) nematode that has not been documented to cause necrosis or penetration of the cecal wall or direct immune response in bobwhite. However, distension and hemorrhaging of the terminal pouches of the ceca have been noted when infection levels are extreme (>300 worms per bird).
  • Average intensity is 117 and 82 worms per bird for bobwhite in the Rolling Plains and South Texas, respectively. In the 2017-18 hunting season RPQRR birds (denoted by red arrow) averaged 410 worms, see Figure 6. Average intensity across all sites in 2017-18 averaged 227 worms.
  • Over 1,700 worms have been found in a single bird.
  • Thirteen different species of grasshoppers have been identified as potential intermediate hosts.
  • New molecular techniques are available to allow for on-site, non-lethal sampling of quail to detect cecal worm infections.
  • See: https://www.quailresearch.org/resources/#faqq for more on “what are cecal worms?”

What We Don’t Know (at this point)

  • While bobwhite and scaled quail in the Rolling Plains are infected at a seemingly high prevalence and intensity, it has not been documented at this time whether parasites are a limiting factor for quail populations.
  • There is currently much speculation as to the effect of helminths (parasitic worms) on bobwhite and scaled quail populations. At this time, these should be considered hypotheses neither supported nor refuted by independent, replicated scientific studies.
  • We do not know the threshold at which infections begin to manifest negative consequences (if any) on survival and reproduction, by whatever ecological mechanism.
  • A “yardstick” of different levels of infection for eyeworms and cecal worms has been proposed, see Figure 7.
  • Due to the microhabitats where adult eyeworms occur (in tissues behind the eye, nasal sinuses), infections have the potential to impair respiratory function, cause visual obstruction, increase energy expenditure, and reduce flight and forage ability.
  • Additional research is needed to understand the impact, if any, that these worms have at the population level in order to assess the impact(s) of these nematodes as potential factors in quail decline.

Where We’re Headed

  • RPQRF anticipates the approval of “QuailGuard®,” a medicated feed to be used for treatment of wild quails. When the medicated feed QuailGuard is approved by the FDA (hopefully in 2022), additional research will be required to understand if and how (e.g., feeding rates, distribution) the application of a medicated feed works to benefit quail demographics (e.g., survival, reproduction).
  • We will continue to conduct research with other scientists to determine the effectiveness of QuailGuard for impacting survival and reproduction of bobwhite and scaled quail.
  • We will determine costs of implementing a medicated feed program at the ranch-level.

Related Webisodes

Publications of the Wildlife Toxicology Laboratory Texas Tech University

  1. Dunham, N.R., Soliz, L.A., Fedynich, A.M., Rollins, D., Kendall, R.J. 2014. Evidence of an Oxyspirura petrowi epizootic in Northern bobwhites (Colinus virginianus). Journal of Wildlife Diseases. 50:552-558.
  2. Dunham, N.R. and Kendall, R.J. 2014. Evidence of Oxyspirura petrowi in migratory songbirds found in the Rolling Plains of West Texas. Journal of Wildlife Diseases. 50:711-712.
  3. Dunham, N.R., Peper, S.T., Baxter, C.E., Huddleston, J.E., Kendall, R.J. 2014. The parasitic eyeworm Oxyspirura petrowi as a possible cause of decline in the threatened Lesser Prairie-Chickens (Tympanuchus pallidicinctus) found in Kansas. Plos One. 9:9.
  4. Kistler, W.M., Parlos, J.A., Peper, S.T., Dunham, N.R., Kendall, R.J. 2016. A quantitative PCR protocol for detection of Oxyspirura petrowi in Northern bobwhites (Colinus virginianus). PLoS One. 11(11):e0166309.
  5. Dunham, N.R., Reed, S., Rollins, D., Kendall, R.J. 2016. Oxyspirura petrowi infection leads to pathological consequences in Northern bobwhite (Colinus virginianus). International Journal for Parasitology: Parasites and Wildlife. 5:273-276.
  6. Dunham, N.R., Peper, S.T., Downing, C., Brake, E., Rollins, D., Kendall, R.J. 2016. Infection levels of the eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula in the Northern bobwhite and scaled quail from the Rolling Plains of Texas. Journal of Helminthology. 91(5):569-577.
  7. Dunham, N.R. and Kendall, R.J. 2016. Eyeworm infections of Oxyspirura petrowi, Skrjabin, 1929 (Spirurida: Thelaziidae), in species of quail from Texas, New Mexico and Arizona, USA. Journal of Helminthology. 91(4):491-496.
  8. Kistler, W.M., Hock, S., Hernout, B., Brake, E., Williams, N., Downing, C., Dunham, N.R., Kumar, N., Turaga, U., Kendall, R.J. 2016. Plains lubber grasshopper (Brachystola magna) as a potential intermediate host for Oxyspirura petrowi in Northern bobwhites (Colinus virginianus). Parasitology Open. 2(e7):1-8.
  9. Dunham, N.R., Bruno, A., Almas, S., Rollins, D., Fedynich, A.M., Presley, S.M., Kendall, R.J. 2016. Eyeworms (Oxyspirura petrowi) in Northern bobwhites (Colinus virginianus) from the Rolling Plains Ecoregion of Texas and Oklahoma, 2011-2013. Journal of Wildlife Diseases. 52(3):562-567.
  10. Henry, C., Brym, M.Z., Kendall, R.J. 2017. Oxyspirura petrowi and Aulonocephalus pennula infection in wild Northern bobwhite quail in the Rolling Plains ecoregion, Texas: Evidence of a possible die-off. Archives of Parasitology. 1:109.
  11. Henry, C., Brym, M.Z., Blanchard, K.R., Kendall, R.J. 2017. Helminth infection and Northern bobwhite (Colinus virginianus). Archives of Parasitology. 1(2):e102.
  12. Kalyanasundaram, A., Blanchard, K.B., Kendall, R.J. 2017. Molecular identification and characterization of partial COX1 gene from caecal worm (Aulonocephalus pennula) in Northern bobwhite (Colinus virginianus) from the Rolling Plains ecoregion of Texas. International Journal for Parasitology: Parasites and Wildlife. 6:195-201.
  13. Dunham, N.R., Henry, C., Brym, M., Rollins, D., Helman, R.G., Kendall, R.J. 2017. Caecal worm, Aulonocephalus pennula, infection in the Northern bobwhite quail, Colinus virginianus. International Journal for Parasitology: Parasites and Wildlife. 6:35-38.
  14. Brym, M.Z., Henry, C., Kendall, R.J. 2018. Potential parasite induced host mortality in Northern bobwhite (Colinus virginianus) from the Rolling Plains ecoregion of West Texas. Archives of Parasitology. 2:1.
  15. Kalyanasundaram, A., Blanchard, K., Henry, C., Brym, M.Z., Kendall, R.J. 2018. Development of a multiplex quantitative PCR assay for eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) detection in Northern bobwhite quail (Colinus virginianus) of the Rolling Plains ecoregion, Texas. Veterinary Parasitology. 253:65-70.
  16. Henry, C., Brym, M.Z., Kalyanasundaram, A., Kendall, R.J. 2018. Molecular identification of potential intermediate hosts of Aulonocephalus pennula from the Order Orthoptera. Journal of Helminthology. 13:1-6.
  17. Blanchard, K., Henry, C., Brym, M.Z., Kalyanasundaram, A., Kendall, R.J. 2018. Regional surveillance of parasitic infections in wild Northern bobwhite quail (Colinus virginianus) utilizing a mobile laboratory platform. Parasitology Open. 4:e14.
  18. Brym, M.Z., Henry, C., Kendall, R.J. 2018. Elevated parasite burdens as a potential mechanism affecting Northern bobwhite (Colinus virginianus) population dynamics in the Rolling Plains of West Texas. Parasitology Research. 117:1683-1688.
  19. Kalyanasundaram, A., Henry, C., Brym, M.Z., Kendall, R.J. 2018. Molecular identification of Physaloptera sp. from wild northern bobwhite (Colinus virginianus) in the Rolling Plains ecoregion of Texas. Parasitology Research. Published online July 7.

Publications by Other Authors Supported by RPQRF:

Bedford, K. 2015. Parasitological survey of scaled quail from west Texas. Thesis. Texas A&M University, Kingsville.

Bruno, A., A. M. Fedynich, A. Smith-Herron, and D. Rollins. 2015. Pathological response of northern bobwhites to Oxyspirura petrowi infections. Journal of Parasitology 101:364–368.

Bruno, A., A.M. Fedynich, D. Rollins, and D.B. Wester. 2018. Helminth community and host dynamics in northern bobwhites from the Rolling Plains Ecoregion, U.S.A. Journal of Helminthology 1–7. https://doi.org/10.1017/S0022149X18000494

Ferro, P.J., O. Khan , C. Vuong , S. M. Reddy , L. LaCoste , D. Rollins , and B. Lupiani. 2012. Avian Influenza Virus Investigation in Wild Bobwhite Quail from Texas. Avian Diseases, 56:858-860.

Kubečka, B.W., A. Bruno, and D. Rollins. 2017. Geographic Survey of Oxyspirura petrowi Among Wild Northern Bobwhites in the United States,” National Quail Symposium Proceedings: Vol. 8, Article 84. Available at: http://trace.tennessee.edu/nqsp/vol8/iss1/84

Kubecka, B.W., N. J. Traub, V. V. Tkach, T.R. Shirley, D. Rollins, and A. M. Fedynich. 2018. Mesocestoides sp. in Wild Northern Bobwhite (Colinus virginianus) and Scaled Quail (Callipepla squamata). Journal of Wildlife Diseases, 54(3): In press.

Su, H., J. McKelvey, D. Rollins, M. Zhang,, D.J. Brightsmith, et al. 2014. Cultivable Bacterial Microbiota of Northern Bobwhite (Colinus virginianus): A New Reservoir of Antimicrobial Resistance? PLoS ONE 9(6): e99826. doi:10.1371/journal.pone.0099826

Villarreal, S.M., Fedynich, A., L. A. Brennan, and D. Rollins. (2012) “Parasitic Eyeworm (Oxyspirura petrowi) in Northern Bobwhites from the Rolling Plains of Texas, 2007–2011,” National Quail Symposium Proceedings: Vol. 7, Article 95.

Villarreal, S.M., A. Bruno, A.M. Fedynich, L.A. Brennan, and D. Rollins. 2016. Helminth Infections Across a Northern Bobwhite (Colinus virginianus) Annual Cycle in Fisher County, Texas. Western North American Naturalist 76(3):275-280.

Parasite FAQ

How do quail become infected with eyeworms?

Quail must consume an infected “intermediate host” (e.g., grasshopper, cricket, cockroach).  Once inside the quail’s crop, eyeworm larvae from the intermediate host escape, make their way into the esophagus, and move up to the lacrimal ducts, then migrate up into the eye.  This process can occur in less than 30 minutes.

Are these eyeworms only in quail?

No, they have been found in pheasants, lesser prairie chickens, mockingbirds, and several other species. Interestingly, we surveyed for their presence in wild turkeys on a site that had “high” infection rates of eyeworms. While the turkeys were eating arthropods (presumably infected with eyeworm larvae), only 1 of 104 turkeys had an eyeworm. Explain that discrepancy?

Read Host Specificity of Oxyspirura petrowi in Wild Turkey

Is the eyeworm native to North America?

Parasites aren’t typically classified as native or exotic. Skrjabin (1929) first characterized O. petrowi in Northeastern Europe, and early reports in the U.S. date back to the 1940s.

I've only heard of this in Texas—is it limited to there or does it occur elsewhere?

While the Rolling Plains ecoregion of Texas appears to have the highest infection rates, we have also found them in bobwhites from AL, OK, and VA.  They likely occur in KS and NE but we have not examined birds from those states.

Do eyeworms cause blindness in an infected quail?

They can irritate (i.e., cause inflammation) to the optic nerve and associated glands situated behind the eyes.  They can also produce scarring of the cornea.  Such pathology likely affects the quail’s vision.  Odds are it would be preyed upon before it became “blind.”

What percentage of bobwhites have eyeworms?

Since we began studying them in 2009, we typically find that 50-60 percent of the bobwhites harbor eyeworms.  Some sites have upwards of 80 percent infection.  Infections in the Rolling Plains are about 8X greater than bobwhites from south Texas.  Adult quail typically have greater infections than juvenile birds.

Are the birds okay for human consumption if they have eyeworms?

Yes, no concerns for human consumption . . . most of us don’t eat the heads anyway!

How do I know if my quail have eyeworms?

For initial inspection in the field, see Joe Crafton’s technique above (https://youtu.be/VSfwWONuU0Y ).  Also watch the video “How to Search for Eyeworms in Quail”.  Be aware however that both of these techniques underestimate the number of eyeworms, as many (probably most) reside behind the eyeball itself.  A complete dissection of the head is needed to get an accurate count.

So do you think eyeworms are worse now than in times past or is it just that we are aware that they exist now and know how to check for them?

We’ve known about eyeworms since early 1960s in bobwhites; they were noted in pheasants in the Midwest earlier than that. Information about them in quail essentially lay “dormant” for the past 50 years, because most parasite studies don’t look at/in/around the eyes–looking typically in the GI tract. Our “Operation Idiopathic Decline” study (initiated in 2011; see video at https://www.youtube.com/watch?v=xUfqw8dGk5E ) resulted in newfound interest in eyeworms.

Is there any credibility to the rumor that wild hogs assist in the spread of eyeworms?

I am not aware of any connection/rumor of feral hogs being involved in transmission of eyeworms–I don’t see any connection between the 2.

What’s the answer?

We are working with the Wildlife Toxicology Lab at Texas Tech to develop a medicated feed that will kill the eyeworms and cecal worms. Hope to have it commercially available in 2022.

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