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.
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, which we have termed “weight of the evidence”, in order to evaluate the significance of these infections. 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 songbirds (Dunham and Kendall 2014), 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 wide spread 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, in our studies, we have 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 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.
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. At the same time, we saw an increase in parasitic infection and reported this in the scientific literature (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 many hunter-shot specimens from December 2017 – February 2018. In these samples, we found the highest average eyeworm and caecal worm burdens observed and was followed by a decrease in parasite loads in these same areas, as well as hunters reporting increased difficulty in finding coveys of bobwhite(Brym et al. 2018b). The results of our trapping effort in March of 2018 continue to follow this trend, with increased trapping effort required to catch a single bird and a decrease in parasite loads (Brym et al. 2018c). Because these parasites are long lived and are not excreted through feces, 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).
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, implemented, and deployed a Mobile Research Laboratory (MRL) in the Rolling Plains that will utilize state-of-the-art molecular techniques (Kistler et al. 2016; Kalyanasundaram et al., 2018b). A recent pilot study deployed the MRL and determined its accuracy and efficiency to be the same as that of a typical laboratory (Blanchard et al., 2018). 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. Furthermore, identification of the intermediate hosts for these parasites may be an important factor to consider as parasitic infection may be precipitated by certain environmental conditions and availability of the intermediate host (Henry et al., 2018). The WTL has been addressing this factor, and Kistler et al. (2016) and Henry et al. (2018) have identified various grasshoppers as potential intermediate hosts for both parasites.
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). As all of us that have hunting dogs know that 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 to register a medicated feed treatment that will be safe for quail and for the environment. Although the results to date have been very promising, all of this takes time and extensive research in both the laboratory and the field.
An eye was removed from a deceased and parasitized Northern bobwhite (Colinus virginianus) quail and placed in solution in a petri dish. Note the number of eyeworms (Oxyspirura petrowi) exiting the ducts, including the lacrimal duct and Harderian gland, of the quail. This was from a wild Northern bobwhite collected in the Rolling Plains of West Texas in January 2018.
Here are caecal worms (Aulonocephalus pennula) removed from the intestines of a wild northern bobwhite (Colinus virginianus) quail. This number of caecal worms were infecting one wild quail. This wild Northern bobwhite was collected from the Rolling Plains of West Texas in January 2018.
Note here eyeworms (Oxyspirura petrowi) on the surface or just under the nictitating membrane of this deceased wild Northern bobwhite (Colinus virginianus) quail collected from the Rolling Plains of West Texas. Sometimes we do see eyeworms under the nictitating membrane but most of the time the worms are located in the rear of the eye, particularly in the lacrimal duct and the Harderian gland, where we believe they are feeding, and we have evidence of eye pathology.
1. Caecal worm (Aulonocephalus pennula) infection in the intestines of a wild northern bobwhite (Colinus virginianus) quail collected in the Rolling Plains of West Texas.
2. From an eyeball of a wild northern bobwhite (Colinus virginianus) quail. Note the exiting of eyeworms (Oxyspirura petrowi) from ducts at the rear of the eye.
3. The head structure of the caecal worm (Aulonocephalus pennula) is well-developed. Note the structure of the mouth parts.
4. Another angle of the head and mouth parts of the caecal worm (Aulonocephalus pennula) obtained from the intestines of a wild northern bobwhite (Colinus virginianus) quail collected in the Rolling Plains of West Texas.
5. This is a picture of the head and mouth parts of the female caecal worm (Aulonocephalus pennula) collected from the intestines of a wild northern bobwhite (Colinus virginianus) quail from the Rolling Plains of West Texas.
6. The eyeworm (Oxyspirura petrowi) has a well-defined head structure, including highly developed mouth parts and sensors that detect light. This eyeworm was extracted from the eye of a wild northern bobwhite (Colinus virginianus) quail collected from the Rolling Plains of West Texas.
7. The head structure of the eyeworm (Oxyspirura petrowi) is noted with light sensors as well as a well-developed mouth structure for feeding. In this series of pictures, note in picture A the mouth and esophagus of the eyeworm (Oxyspirura petrowi). In picture B, note the structure of the head and light sensors. Picture C is, again, a close-up view of the head and light sensors in the eyeworm and D is a very close-up picture of the mouth structure of the eyeworm. All of these worms were collected from the eyes of wild northern bobwhite (Colinus virginianus) quail from the Rolling Plains of West Texas.
8. The female eyeworm (Oxyspirura petrowi) is packed with eggs for distribution to facilitate wide-scale infections in birds, particularly the wild northern bobwhite (Colinus virginianus) quail in the Rolling Plains of West Texas.
9. The female caecal worm (Aulonocephalus pennula) is an enormous egg producer for the distribution, which facilitates widespread infection in wild northern bobwhite (Colinus virginianus) quail in the Rolling Plains ecoregion of West Texas.
10. Staff from the Wildlife Toxicology Laboratory at Texas Tech University are operating a Mobile Research Laboratory to facilitate non-lethal detection of parasitic infection in wild quail using molecular techniques.
11. The MRL being operated by the WTL at TTU can literally go anywhere in the Rolling Plains ecoregion of West Texas to detect and monitor parasitic infections in wild northern bobwhite (Colinus virginianus) quail.