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Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from the Rolling Plains Ecoregion of West Texas?

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Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from the Rolling Plains Ecoregion of West Texas?

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The question of whether parasites can significantly influence host population dynamics is complex and debated. Since Anderson and May's groundbreaking theoretical work revealed the potential of parasites to influence host populations, several studies have demonstrated this potential experimentally, leading to an increased consideration of parasites in this regard. One species in which this needs further study is the Northern bobwhite quail (Colinus virginianus), a declining game bird that has been found to exhibit intense parasitic infections in some portions of its range, such as the Rolling Plains of West Texas. As part of a long-term effort monitoring parasitic infection of bobwhite in the Rolling Plains, we received 3 hunter-harvested bobwhite from Mitchell County, Texas in Febru-ary 2018 and 9 bobwhite were captured from a research transect in the same county in March 2018. Eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) burdens for hunter-harvested bobwhite averaged 65 and 830, respectively, while captured bobwhite averaged 49 and 381, respectively. Additionally, an average of 71 trapping sessions were required to capture one bobwhite during March 2018, which was considerably higher than previous reports from this area. These extreme infection levels, as well as the increased effort required to capture a single bobwhite, coincided with widespread reports of dramatically decreased bobwhite abundance. While the sample size presented here is small, the consistency between these observations and recent reports demonstrates the need to continue investigating the effects parasites may be having on bobwhite in the Rolling Plains. Citation: Ronald J Kendall., et al. "Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virgin-ianus) from the The potential of macroparasites to influence host populations has been a longstanding topic of contention amongst researchers. While factors such as resource availability, predator-prey interactions, and competition have typically taken precedence as drivers of population dynamics [1-3], the regulatory capacity of parasites has begun to garner credence in more recent times. In 1978, Anderson and May laid the theoretical groundwork demonstrating that parasites have the potential to impact host population abundance [4,5]. Since then, a number of empirical studies have shown that parasites are indeed capable of affecting host population dynamics [6], including a long-term study by Hudson., et al. [7] which found a helminth to be the underlying cause of cyclical population fluctuations of red grouse (Lagopus lagopus scoticus) on game preserves in Scotland.
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Short Communication
Matthew Z Brym, Cassandra Henry and Ronald J Kendall*
The Wildlife Toxicology Laboratory, Texas Tech University, Box 43290, Lubbock, Texas, 79409-3290, USA
Received: August 20, 2018; Published: August 25, 2018
*Corresponding Author:
Ronald J Kendall, The Wildlife Toxicology Laboratory, Texas Tech University, Box 43290, Lubbock, Texas,
79409-3290, USA.
Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite
Quail (Colinus virginianus) from the Rolling Plains Ecoregion of West Texas?
Abstract

-
 
needs further study is the Northern bobwhite quail (Colinus virginianus

-
Oxyspirura petrowi)
 Aulonocephalus pennula) burdens for hunter-harvested bobwhite averaged 65 and 830, respectively, while cap-
tured bobwhite averaged 49 and 381, respectively. Additionally, an average of 71 trapping sessions were required to capture one




Citation:
Ronald J Kendall., et al.Colinus virgin-
ianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.


Multidisciplinary Advances in Veterinary Science
ISSN: 2573-3435

., et al.
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

-
    
study by Hudson., et alLagopus
lagopus scoticus
Introduction
Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from
the Rolling Plains Ecoregion of West Texas?
407
Citation:
Ronald J Kendall., et al.Colinus vir-
ginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.

-
(Colinus
virginianus




    
Aulonocephalus pennulaOxyspirura petrowi) in quail throughout the region


quail populations.
Materials and Methods

  -

     
      
   -



Results and Discussion

Sorghum bicoloret al
-
ing to Henry., et al     

et al
   et al  
 -

When Henry., et al    

et al




Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from
the Rolling Plains Ecoregion of West Texas?
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Citation:
Ronald J Kendall., et al.Colinus vir-
ginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.
        -
   
       



they are also subject to widespread and intense parasitic infection.
Additionally, we recorded large differences in both parasite loads and trapping effort between our eastern and western trapping

           
of the eastern transect, and the western birds possessed parasite loads less than half that of eastern birds (table 1). The difference for
  

      -

 
-
     

 et al
 -

    -
           



-

Location Sample
Size
Trapping Effort Eyeworms Caecal worms
Trapping
Sessions
Trapping
Session/Bird
Mean
Abundance
Range Mean
Abundance
Range
Total 9 640 71.1 49 23-83 381 109-935
 6 300 50.0 60 23-83 462 170-935
West 3 340 113.3 27 25-30 220 109-350
Table 1: Trapping effort and parasite abundance by location.
Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from
the Rolling Plains Ecoregion of West Texas?
409
Citation:
Ronald J Kendall., et al.      Colinus
virginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.
Figure 1: Caecal worms (n = 1722) extracted from one
Northern bobwhite quail (Colinus virginianus) collected
from Mitchell County, Texas in February 2018.
Figure 2: Comparison of breast tissue of Northern bobwhite
quail (Colinus virginianus) between a (a) typical adult and (b)
heavily parasitized individual collected from Mitchell County,
Texas in February 2018.
   
         -
       
           

  



Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus)
from the Rolling Plains Ecoregion of West Texas?
410
Citation:
Ronald J Kendall., et al.         Colinus
virginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.

 
     

-


-


We thank those at our study ranch for their continued hospitality and for allowing us ranch access. Thank you to all the Wildlife



Acknowledgements
References
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
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 

 et alAuk 118.2 (2001): 290-303.
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 

 

 
16. Sauer JR., et alNorth American
Fauna 79 (2013): 1-32.
Are Helminths Contributing to the Population Fluctuations of Northern Bobwhite Quail (Colinus virginianus) from
the Rolling Plains Ecoregion of West Texas?
411
Citation:
Ronald J Kendall., et al.Colinus vir-
ginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.
        
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Journal of Wildlife Diseases 52.3 (2016): 562-567.
 

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Citation:
Ronald J Kendall., et al.Colinus vir-
ginianusMultidisciplinary Advances in Veterinary Science 2.5 (2018): 406-412.
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 et alIthaca, Cornell University Press (2004).
       

 Limnology and Oceanography 44.3.2 (1999):
925-931.
... The West Texas Rolling Plains is also considered to be a stronghold of bobwhite hunting [5], which provides an important source of seasonal revenue for many local communities [8]. Unfortunately, bobwhite populations throughout the West Texas Rolling Plains have been declining, with O. petrowi infection being purported as a potential mechanism contributing to this decline [9][10][11]. ...
... In the Rolling Plains, there have been extensive studies investigating the effects of O. petrowi on bobwhite and surveys have identified it to be highly prevalent throughout the ecoregion [7,12]. For instance, Dunham et al. [13] found 58.7% of adult bobwhite across 29 counties in the Rolling Plains to be infected with O. petrowi, while others have found some areas with a prevalence of 100% [10,11]. Oxyspirura petrowi is typically found on the surface of the eye, under the nictitating membrane, as well as in the lacrimal ducts and other glands of the eye [9]. ...
... Oxyspirura petrowi is typically found on the surface of the eye, under the nictitating membrane, as well as in the lacrimal ducts and other glands of the eye [9]. Oxyspirura petrowi infections have been correlated with inflammation of the lacrimal ducts, keratitis and lesions on the Harderian gland [9,14], leading to suspicions that infection may adversely affect bobwhite [9][10][11]. Pathological investigations have further increased concerns of O. petrowi infection, as the Harderian gland is associated with immune function [15]; although more research is needed to elucidate links between infection and these immune system processes. ...
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Background: Oxyspirura petrowi (Spirurida: Thelaziidae), a heteroxenous nematode of birds across the USA, may play a role in the decline of the northern bobwhite (Colinus virginianus) in the Rolling Plains Ecoregion of West Texas. Previous molecular studies suggest that crickets, grasshoppers and cockroaches serve as potential intermediate hosts of O. petrowi, although a complete study on the life-cycle of this nematode has not been conducted thus far. Conse-quently, this study aims to improve our understanding of the O. petrowi life-cycle by experimentally infecting house crickets (Acheta domesticus) with O. petrowi eggs, feeding infected crickets to bobwhite and assessing the life-cycle of this nematode in both the definitive and intermediate hosts.Methods: Oxyspirura petrowi eggs were collected from gravid worms recovered from wild bobwhite and fed to house crickets. The development of O. petrowi within crickets was monitored by dissection of crickets at specified intervals. When infective larvae were found inside crickets, parasite-free pen-raised bobwhite were fed four infected crickets each. The maturation of O. petrowi in bobwhite was monitored through fecal floats and bobwhite necropsies at specified intervals.Results: In this study, we were able to infect both crickets (n = 45) and bobwhite (n = 25) with O. petrowi at a rate of 96%. We successfully replicated and monitored the complete O. petrowi life-cycle in vivo, recovering embryonated O. petrowi eggs from the feces of bobwhite 51 days after consumption of infected crickets. All life-cycle stages of O. petrowi were confirmed in both the house cricket and the bobwhite using morphological and molecular techniques.Conclusions: This study provides a better understanding of the infection mechanism and life-cycle of O. petrowi by tracking the developmental progress within both the intermediate and definitive host. To our knowledge, this study is the first to fully monitor the complete life-cycle of O. petrowi and may allow for better estimates into the potential for future epizootics of O. petrowi in bobwhite. Finally, this study provides a model for experimental infection that may be used in research examining the effects of O. petrowi infection in bobwhite. (PDF) Life-cycle of Oxyspirura petrowi (Spirurida: Thelaziidae), an eyeworm of the northern bobwhite quail (Colinus virginianus). Available from: https://www.researchgate.net/publication/337430813_Life-cycle_of_Oxyspirura_petrowi_Spirurida_Thelaziidae_an_eyeworm_of_the_northern_bobwhite_quail_Colinus_virginianus [accessed Nov 22 2019].
... Following the hunting season of 2017-2018, Brym et al. (2018c) also reported difficulty in trapping bobwhite, reinforcing previous reports suggesting a scarcity of birds that may have resulted from the consistently elevated parasite burdens documented throughout the region. Commons et al. (2019) likewise documented difficulty trapping amidst high parasite burdens compared with previous years. ...
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The potential of parasites to affect host abundance has been a topic of heated contention within the scientific community for some time, with many maintaining that issues such as habitat loss are more important in regulating wildlife populations than diseases. This is in part due to the difficulty in detecting and quantifying the consequences of disease, such as parasitic infection, within wild systems. An example of this is found in the Northern bobwhite quail (Colinus virginanus), an iconic game bird that is one of the most extensively studied vertebrates on the planet. Yet, despite countless volumes dedicated to the study and management of this bird, bobwhite continue to disappear from fields, forest margins, and grasslands across the United States in what some have referred to as “our greatest wildlife tragedy”. Here, we will discuss the history of disease and wildlife conservation, some of the challenges wildlife disease studies face in the ever-changing world, and how a “weight of evidence” approach has been invaluable to evaluating the impact of parasites on bobwhite in the Rolling Plains of Texas. Through this, we highlight the potential of using “weight of the evidence” to better understand the complex effects of diseases on wildlife and urge a greater consideration of the importance of disease in wildlife conservation.
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Northern bobwhite quail (Colinus virginianus) are a highly sought-after game bird in the Rolling Plains of West Texas. Unfortunately, bobwhite populations in this area are subject to dramatic fluctuations and have been steadily decreasing over the past several decades. While many factors have been investigated as potential mechanisms of cyclic and declining bobwhite numbers, the effect of parasites on bobwhite populations has historically been undervalued. Between December 2017 and February 2018, we received 21 hunter-shot bobwhite from Garza and Mitchell counties in Texas and found peak caecal worm (Aulonocephalus pennula) and eyeworm (Oxyspirura petrowi) burdens averaging 599 and 44, respectively. These represent the highest average parasite loads we have documented in bobwhite from the Rolling Plains thus far and are coincident with widespread reports of declining bobwhite abundance. These elevated infections also followed a high point in bobwhite populations in the Rolling Plains, and our observations of infection dynamics during this time reflect other instances of potential parasite-induced host mortality. While the sample discussed in this communication is small, our findings highlight the need for additional research into how parasites may affect bobwhite population fluctuations in this region.
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Aulonocephalus pennula is a heteroxenous nematode that commonly infects a declining game bird, the northern bobwhite quail ( Colinus virginianus ). There is a lack of information on the life cycle of A. pennula and the potential effects of infection on bobwhites. In order to better understand the life cycle of this parasite, various species from the order Orthoptera were collected from a field site in Mitchell County, Texas. Using polymerase chain reaction (PCR), nine potential intermediate hosts were identified from the 35 orthopteran species collected. Later, ten live specimens were collected to identify larvae within the potential intermediate hosts. Larvae were present in three of these and were sent for sequencing. Similarly, the presence of larvae was confirmed from extra tissues of samples identified as positive with PCR. This was the first study to document potential intermediate hosts, but future studies are needed to confirm that these species are capable of transmitting infection to bobwhite. However, this study demonstrates that PCR has increased sensitivity and may be a valuable tool when determining intermediate hosts.
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To determine potential intermediate hosts of Oxyspirura petrowi, a common nematode eyeworm of wild gallinaceous birds, various arthropod species including red harvester ants, beetles, wood cockroaches, crickets, grasshoppers, katydids, and desert termites were screened for the presence of O. petrowi using specific polymerase chain reaction (PCR) primers targeting the internal transcribed spacer 2 region (ITS2) of the eyeworm ribosomal deoxyribonucleic acid (rDNA). This is the first study to investigate the intermediate hosts of O. petrowi utilizing molecular techniques. We determined 38% (13/34) of the cockroaches, 27% (3/11) of the crickets, and 23% (68/289) of the grasshoppers which were positive for O. petrowi. Identifying potential intermediate hosts of O. petrowi is essential to better understanding the epizoology of the eyeworm's transmission mechanics and to controlling infections in wild gallinaceous birds.
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Anecdotal reports of Northern bobwhite quail (Colinus virginianus) exhibiting strange behavior have raised suspicions of parasite induced host mortality (PIHM) in the Rolling Plains of West Texas. In 2017, we received 11 bobwhite carcasses associated with such reports and found parasites in all of these specimens. While further research is needed to evaluate the impact of parasites on bobwhite, these reports provide a valuable supplement to on-going investigations of PIHM in bobwhite from the Rolling Plains of West Texas.
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We have been monitoring wild Northern bobwhite quail (Colinus virginianus) on a research transect in Mitchell County, Texas. We captured a total of 51 bobwhites in March-May of 2016 and 2017 and examined them for eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) infections. In March 2017, bobwhites averaged 15 ± 10 eyeworms and 269 ± 90 caecal worms, and by mid-April averages had increased to 18 ± 13 eyeworms and 372 ± 144 caecal worms. These averages were much higher than those observed in March 2016 (11 ± 13 eyeworms and 160 ± 57 caecal worms) and April 2016 (12 ± 12 and 216 ± 56, respectively). We observed a precipitous decline in quail numbers by late April 2017, and average infection had dropped to 7 ± 2 eyeworms and 252 ± 109 caecal worms. The number of trapping sessions needed to capture one bobwhite also increased from 14.26 in 2016 to 36.46 in 2017. These observations warrant further investigation into the effects these helminth parasites may have on bobwhites and their populations within the Rolling Plains.
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Debilitating ocular diseases are often reported in avian species. By and large, helminth parasites have been overlooked in avian diseases and regarded as inconsequential. The decline of Northern bobwhite quail (Colinus virginianus) in the Rolling Plains ecoregion of Texas has prompted an investigation of the factors influencing their disappearance. Infection by the eyeworm (Oxyspirura petrowi) has been documented in many avian species; however, the effect it has on its host is not well understood. Heavy eyeworm infection has been documented in Northern bobwhites throughout this ecoregion, leading to eye pathology in this host species. The present study further documents and supports the pathological changes associated with O. petrowi in bobwhites.
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Northern bobwhite (Colinus virginianus) and scaled quail (Callipepla squamata) have experienced chronic declines within the Rolling Plains ecoregion of Texas. Parasitic infection, which has long been dismissed as a problem in quail, has not been studied thoroughly until recently. A total of 219 northern bobwhite and 101 scaled quail from Mitchell County, Texas were captured and donated from 2014-2015, and examined for eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) infections. In 2014, bobwhites averaged 19.6±1.8 eyeworms and 98.6±8.2 caecal worms and 23.5±2.1 eyeworms and 129.9±10.7 caecal worms in 2015. Scaled quail averaged 4.8±1.0 eyeworms and 50±6.8 caecal worms in 2014 and 5.7±1.3 eyeworms and 38.1±7.1 caecal worms in 2015. This study expands the knowledge of parasitic infection in quail inhabiting the Rolling Plains of Texas. A significant difference was documented in O. petrowi infection between species but there was no significant difference in A. pennula between quail species. No significant difference was detected in parasite infection between the sexes of both northern bobwhite and scaled quail. This study also documented the highest reported O. petrowi infection in both species of quail. Additional research is needed on the life history and infection dynamics of O. petrowi and A. pennula infections to determine if there are individual and/or population level implications due to parasitic infection. .
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Oxyspirura petrowi is a heteroxenous parasitic nematode that has been reported in high prevalences from birds in the Order Galliformes experiencing population declines in the USA. There is a paucity of information regarding the natural history O. petrowi, including the life cycle and effects of infection on wild bird populations. In order to study the life cycle of this parasite, we collected plains lubber grasshoppers (Brachystola magna) from a field location in Mitchell County, Texas. We found third-stage larvae (L3) in 37.9% (66/174) B. magna. We determined that they were O. petrowi through morphological comparison of L3 from experimentally infected Acheta domesticus and by sequence analysis. Then, we showed that B. magna are a potential intermediate hosts for O. petrowi infections in northern bobwhites (Colinus virginianus) in a laboratory setting by experimental infection. We first detected shedding of eggs in feces using a fecal float technique 52 days post infection. In addition, we recovered 87 O. petrowi from experimentally infected northern bobwhites. Although we detected shedding in feces, recovery of eggs was low (>5 eggs/g). Future work is needed to understand shedding routes and shedding patterns of northern bobwhites infected with O. petrowi.
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The Northern Bobwhite ( Colinus virginianus ) has been steadily declining throughout much of its historic range for decades. The Rolling Plains ecoregion of Texas and western Oklahoma, historically rich with wild bobwhites and one of the last remaining quail strongholds, also has a declining population. During August and October in 2011-2013, 348 Northern Bobwhites from the Rolling Plains were examined for eyeworms (Oxyspirura petrowi). Of these 348 Northern Bobwhites, 144 (41.4%) were infected with 1,018 total eyeworms. Eyeworm abundance (mean±SE) was 2.9±0.4 (range 0-64), with an intensity (mean±SE) of 7.1±0.6. Eyeworm prevalence was significantly higher in adult Northern Bobwhites (58.7%) than in juveniles (35.4%). Recent research suggests that eyeworms have the potential to cause cellular tissue damage to the eye, but it is unknown how these worms affect host survivability. This study further expands the regional distribution of O. petrowi in Northern Bobwhites in the Rolling Plains ecoregion and assesses the prevalence and abundance of infection across host age, host sex, and year. Further research is warranted on the life history of O. petrowi and assessing the impacts of eyeworms on their definitive host at individual and population levels.