Parasites in Quail in the Rolling Plains Ecoregion of West Texas: Leadership of the Wildlife Toxicology Laboratory
The Rolling Plains Ecoregion of West Texas, an area approximately the size of the State of Michigan, has long been touted as one of the last great strongholds for wild quail hunting left in the United States. In 2010, good spring and summer rains, along with excellent habitat quality, foretold a promising season with abundant quail. However, come opening day, the quail had all but vanished with many landowners estimating a 70-90% decline in wild quail numbers on their properties. This sudden loss of quail captured the attention of many throughout the Rolling Plains, leading to the launch of the research program Operation Idiopathic Decline (OID) to investigate possible causes behind such a precipitous decline in quail populations. With research funding from the Rolling Plains Quail Research Foundation, Park Cities Quail, and Texas A&M AgriLife Extension Service, the OID initiative entailed extensive research on thousands of quail in 2011 and 2012. This initiative engaged multiple investigators from prominent universities throughout Texas to study the potential impacts of environmental contaminants, pesticides, diseases, and parasites on quail of the Rolling Plains. Initially, The Wildlife Toxicology Laboratory (WTL), with tremendous support from Texas Tech University, worked with the OID initiative conducting research on environmental contaminants and pesticides (Baxter et al. 2015; Turaga et al. 2016; Dunham et al. 2017; Pappas, et al. 2017). Then in 2012, the WTL shifted focus to address the question of parasites as a potential mechanism contributing to quail declines in the Rolling Plains.
Head of a parasitic eyeworm
Although parasites had been previously reported in quail of the Rolling Plains prior to OID, their significance was considered largely inconsequential. However, research associated with OID has shed new light on the potential of parasites, particularly the eyeworm (Oxyspirura petrowi), to impact quail populations in the Rolling Plains, and the WTL has been at the forefront of this research. Since 2012, we have implemented extensive and continuous field and laboratory projects to evaluate eyeworm infections in wild quail, which subsequently expanded to include another parasite affecting quail in the region, the caecal worm (Aulonocephalus pennula). Because questions regarding the potential significance of these parasitic infections in wild quail are very complex, the WTL adheres to a meticulous forensics-like approach, termed “weight of evidence”, in order to evaluate the significance of these infections (Henry et al. 2020). As we continue to utilize this method, we build a strong scientific foundation to better understand the role and significance of parasitic infection in wild quail at both the individual and population level by synthesizing data gained from field and laboratory studies and input from landowners and quail hunters, as well as our own personal observations.
As a result of this exhaustive and comprehensive approach, the WTL has documented eyeworms in 3 species of songbirds (Dunham and Kendall 2014; Herzog et al. 2021), Lesser Prairie-Chickens (Tympanuchus pallidicinctus) (Dunham et al. 2014), and Gambel’s (Callipepla gambelii), Scaled (Callipepla squamata), and Northern bobwhite quail (Colinus virginianus) (Dunham and Kendall 2016). Furthermore, Dunham et al. (2016a) has demonstrated the widespread prevalence of eyeworms, as bobwhite from 29 counties in the Rolling Plains were found to be infected with this parasite. The WTL was also the first to document an eyeworm epizootic in wild quail of the Rolling Plains, revealing the alarming speed with which these infections can occur (Dunham et al. 2014). Additionally, the persistence of these infections even when bobwhite populations are low could be perpetuated by the songbirds facilitating transmission to intermediate hosts and thus to the bobwhite.
In our studies, we have also closely investigated the eyes of infected birds. Unlike previous studies that only reported eyeworms on the surface of the eye and under the nictitating membrane, we noted that eyeworms were also concentrated in the intraorbital glands that are important for tear production and immune function, such as the lacrimal duct and Harderian gland (Dunham et al. 2015). These findings spurred subsequent investigation into the pathological consequences of eyeworm infection. During this investigation, the WTL found that infected quail can have severe damage to the eyes and associated tissues (Dunham et al. 2016b). While more work is needed to evaluate the potential impact these infections may have on quail survival, this evidence of damage associated with eyeworm infection supports widespread anecdotal reports of quail flying into objects, such as barns, houses, fences, and trucks, in the Rolling Plains. For those of us familiar with wild quail, we can attest to their incredible ability to navigate seemingly impenetrable brush. This allows them to escape many of their enemies, including formidable aerial predators such as the Cooper’s hawk (Accipiter cooperi). As such, these instances of quail flying at full speed into large and highly visible objects are not only surprising but may also indicate potentially compromised vision.
In the course of this research, we have developed infection level thresholds to gauge the intensity of eyeworm infection in wild quail (Dunham et al. 2017a), and we continue to closely monitor parasite levels in the Rolling Plains. Additionally, this study revealed that another parasitic nematode, the caecal worm, is even more abundant in wild quail from the Rolling Plains than eyeworms. This is an alarming observation considering that similar parasites have been known to negatively affect host nutrition and reproduction. Henry et al. (2017a) hypothesized that the caecal worm may be impairing the caecum function as it has been associated with lower vitamin A and Dunham et al. (2017b) found minimal amounts of digesta within the caecum of infected birds. Dunham further hypothesized that this may impact the survivability of the bobwhite in the winter. Furthermore, little is known about the impacts of multiple parasites and we have found quail in the Rolling Plains to often be heavily infected with both caecal worms and eyeworms.
Head of a parasitic caecal worm
We have also been able to document some very interesting situations with parasitic infection. For instance, on a research transect we have been working on for almost six years, we noted a precipitous decline in wild quail in the spring of 2017 concurrent with an increase in parasitic infection (Henry et al. 2017b). Additionally, landowners donated multiple quail to the WTL in 2017 after witnessing them fly into stationary objects, killed by a predator, or in a weakened state. Parasites were found in all of these samples, and while it is unknown whether parasites are responsible for these examples, it is an important possibility that must be considered (Brym et al. 2018a). We also received hunter-shot specimens from December 2017 – February 2018. In these samples, we found some of the highest average eyeworm and caecal worm burdens observed and documented the highest caecal worm burden ever recorded (1722). This observation was followed by a decrease in parasite loads in these same areas, as well as hunters reporting increased difficulty in finding coveys of bobwhite and an apparent dramatic drop in quail numbers (Brym et al. 2018b; Brym et al. 2018c). Because these parasites are long-lived and are not excreted after infecting quail, this suggests that highly infected bobwhite were dropping out of the population. Furthermore, we documented an increase in the muscle worm, Physaloptera sp., amidst the elevated burdens of eyeworms and caecal worms (Kalyanasundaram et al. 2018a). In 2018, we were also able to document that bobwhite had persistently high parasite burdens and began to decline well before the breeding season (Commons et al. 2019).
Needless to say, 2017 was a tough year for bobwhite. Based on Texas Parks and Wildlife Department’s (TPWD) Quail Roadside Counts, bobwhite went from a record high in 2016 to less than half of those numbers in 2017. In 2018, this decline would only get worse as TPWD reported the third lowest numbers of bobwhite on record since their surveys began in 1978. But how could we go from such high numbers of quail in 2016 to a record low just three years later? With extensive field monitoring by WTL personnel, involving literally thousands of hours of field trapping and surveillance of wild bobwhite quail in the Rolling Plains, we identified a major loss of bobwhite in the early spring period of 2018, which substantially reduced the breeding capital of wild bobwhite going into the summer of 2018 (Commons et al 2019). Additionally, the caecal worm and eyeworm infection levels of 2018 were higher than or similar to levels in the previous years after which there was a crash in local quail populations. This pattern of high parasitic infection immediately preceding a crash in wild quail populations is one which the WTL has observed over the years on our field research transects. Following these population crashes, tremendous effort is required to trap, see, or even hear even one quail, highlighting the potential severity of these events. While this is just one piece of the puzzle to understand the factors driving quail populations in the RP, it does suggest the importance of including parasites in the equation.
Caecal worms collected from one wild bobwhite quail
Considering the widespread prevalence and pathological consequences of these parasitic infections in wild quail of the Rolling Plains, as well as the predators and harsh environmental conditions that these birds must overcome on a daily basis, it is essential to understand how these parasites factor into the complex equation that governs quail survival. To address some of these factors, the WTL has successfully designed a Mobile Research Laboratory (MRL) in the Rolling Plains that utilizes state-of-the-art molecular techniques (Kistler et al. 2016; Kalyanasundaram et al. 2018b). During a pilot study, it was demonstrated that the MRL had the same accuracy and efficiency as a typical laboratory (Blanchard et al. 2018), and we have continued to implement the MRL and standardize the techniques. By doing this, we can now better determine infection level based on the qPCR results (Blanchard et al. 2019a). This will provide widespread non-lethal surveillance for parasitic infection in quail and will be invaluable for evaluating the epidemiology of these parasitic infections in our quail populations. These molecular techniques are also being implemented to predict seasonal infection of these parasites, and our recent paper demonstrates that temperature and precipitation can influence caecal worm and eyeworm reproduction, as well as caecal worm infection intensity (Blanchard et al. 2019b).
As the story of these parasites continues to unfold, phylogenetic studies conducted by WTL will contribute to our understanding of the potential effects these parasites may have on bobwhite. These studies have revealed that the muscle worm is closely related to Wuchereria bancrofti (78%), a roundworm that causes lymphatic filariasis in humans and is known to increase susceptibility to other infections (Kalyanasundaram et al. 2018a). In addition, the eyeworm is closely related to the central African human eyeworm, Loa loa (96% at the genomic level) and the European/eastern Asian human and carnivore eyeworm, Thelazia callipaeda (92%) (Kalyanasundaram et al. 2018c). Both eyeworms reportedly cause severe visual impairment and inflammation in the eyes of their hosts, which elevates our concern for the quail eyeworm. Furthermore, the caecal worm is more than 90% related to the ascarid, or roundworm, of dogs and cats (Kalyanasundaram et al. 2017). We have also begun evaluating the impacts of these parasites on the immune system of bobwhite. The preliminary study evaluated changes in 6 immune response genes when bobwhite were challenged with eyeworm and caecal worm glycoproteins, in which there was a measurable immune reaction (Kalyanasundaram et al. 2019b). For future work, housekeeping genes are being further evaluated to better understand the immune response across several tissues (Kalyanasundaram et al. 2021), as well as identifying additional genes.
As all of us that have hunting dogs know, regular treatment for ascarids is necessary to maintain their performance and prevent death. Should we not have similar concerns then for a highly related worm, the quail caecal worm? While there are abundant treatment options for parasites infecting cats and dogs, there are no options for wild quail. However, we are well on our way to developing a solution for these parasitic infections in wild quail and are working closely with the Food and Drug Administration (FDA). We are contributing data to support FDA-requested scientific information to register a suitable treatment for parasite infection in wild northern bobwhite quail. Although the results to date have been very promising, all of this takes time and extensive research in both the laboratory and the field.
Dr. Ron Kendall
Since 2012, Dr. Ron Kendall at the Wildlife Toxicology Lab (WTL) at Texas Tech University has worked to assess the impacts of eyeworms (Oxyspirura petrowi) and caecal worms (Aulonocephalus pennula) on quail. The WTL has greatly expanded the knowledge for what we know and what we think; the WTL continues to work tirelessly address what we don’t know and to answer the questions for where we’re headed.
What We Know
These are two adult female and two adult male eyeworms removed from a wild northern bobwhite quail from the Rolling Plains of West Texas. If the size of these eyeworms in a wild quail were extrapolated to infection in the eye of a human, they would approach toothpick size. This is why we are so concerned about these eyeworm infections in our wild bobwhites.
- Very common throughout the Rolling Plains with 80-90% of birds infected (up to 100% in some areas)
- Worms are longer than a dime
- Over 1700 worms have been found in a single bird
- Has been associated with gross pathology, distension of the caeca, and lack of digesta; thus providing a mechanism for reduced fitness, including weight loss
- 90% related at the DNA level to the Ascarid, or roundworm, of dogs and cats which if left untreated can cause weight loss, malnutrition, and eventual death
- 13 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 caecal worm infection
- Caecal worm glycoproteins elicited an immune response in bobwhite
- Epizootic event in 2013 demonstrated the potential for rapid spread of infection
- Very common throughout the Rolling Plains with 50-70% of birds infected (up to 100% in some areas)
- Rolling Plains is the hot spot for infection; often 8X more prevalent in bobwhite from Rolling Plains vs South Texas Plains
- Worms are large (longer than a penny)
- 107 worms found in a single bird
- Feed on tissues and glands within the eyes and nasal sinuses
- Cause scarring of the cornea as well as damage to other eye tissues; thus providing a mechanism for reduced vision and/or fitness and explains reports of quail flying into stationary objects
- 24 potential intermediate hosts have been identified from grasshoppers, crickets, katydids, and cockroaches
- Takes 51-56 days to complete its life cycle within the bobwhite
- 96% related at the DNA level to the Loa loa, a central African human eyeworm known to cause blindness
- New molecular techniques are available to allow for on-site, non-lethal sampling of quail to detect eyeworm infection
- Eyeworm glycoproteins elicited an immune response in bobwhite
What We Think
- Eyeworms reduce vision and likely predispose quail to predators, flying into objects (e.g., barns, fences, trees), and difficulty finding food.
- Caecal worms deplete nutrients and may lead to malnutrition, energy loss, reduced breeding potential, increase susceptibility to extreme environmental conditions, and impair their ability to evade predators
- Parasitic infection suppresses the immune system which may leave quail susceptible to secondary infections
- Because parasites are long-lived, over time an infection may increase until it is eventually fatal, ultimately reducing populations
- Even low infections may tip the scales against quail in an already challenging environment, e.g. Cooper’s Hawk predation
- Implementation of a medicated feed (“Quail Guard”) twice annually (Spring and Late Summer) will reduce parasitic infection in wild quail populations and allows for sustainable/huntable quail population
- Based on the “weight of the evidence” as well as field and laboratory data, we believe that quail are impaired by parasitic infection and their reproduction and survival are reduced
Top: Healthy bobwhite quail breast; Bottom: Heavily parasitized and emaciated bobwhite quail breast
What We Don’t Know (At This Point)
- How many parasites can a quail harbor before they are impaired? Is it a linear relationship or is it dependent on the bird, like people and alcohol consumption?
- How does the availability of infected intermediate hosts vary from one year to the next?
- Is there an effect on the immune system of quail? Do high infections leave them more susceptible to other diseases?
- Can the “boom and bust” cycles of quail be reduced by addressing parasite-related concerns?
- What are the consequences of multiple parasite species?
Where we’re headed
- A medicated feed has been developed which we hope earns FDA approval soon and becomes available in the near future
- WTL has deployed a Mobile Research Laboratory and will continue to monitor parasitic infection in quail throughout the Rolling Plains
- WTL is developing new molecular techniques for rapid non-lethal assessment for parasitic infection in quail
- WTL is conducting studies to evaluate bobwhite immune response to parasitic infection
- WTL will continue to add to the “weight of the evidence” supporting the hypothesis that parasites are affecting wild quail, and we recently published a scientific paper to support our “weight of the evidence” approach