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Evidence of an oxyspirura petrowi epizootic in northern Bobwhites (Colinus Virginianus), Texas, USA

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Abstract We captured 36 Northern Bobwhites (Colinus virginianus) in Mitchell County, Texas in June-September 2013, and examined them for the eyeworm Oxyspirura petrowi. We recovered 334 eyeworms from 28 of 29 adult bobwhites (97%); infections ranged from 1-40 worms and mean (±SD) abundance of 11.9±13.0. Three of seven juveniles were infected, and those infected had one eyeworm each. Prevalence of eyeworms was similar among months. However, mean abundance of eyeworms peaked in July and August (3.3±2.1, 13.5±15.0, and 16.9±15.5), and decreased in September (6.3±3.0). We suggest that several previous studies may underreport prevalence and abundance because in those studies only the eye surface and nictitating membrane were examined, and not eye-associated tissue, ducts, glands, or sinuses.
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EVIDENCE OF AN OXYSPIRURA PETROWI EPIZOOTIC IN NORTHERN
BOBWHITES (COLINUS VIRGINIANUS), TEXAS, USA
Nicholas R. Dunham,
1
Liza A. Soliz,
1,2
Alan M. Fedynich,
2
Dale Rollins,
3
Ronald J. Kendall
1,4
1
The Wildlife Toxicology Laboratory, The Institute of Environmental and Human Health, Texas Tech University, Box
41163, Lubbock, Texas 79409, USA
2
Caesar Kleberg Wildlife Research Institute, Texas A&M University-Kingsville, 700 University Blvd., Kingsville, Texas
78363, USA
3
Texas AgriLife Research, Texas A&M University System, San Angelo, Texas 76901, USA
4
Corresponding author (email: ron.kendall@ttu.edu)
ABSTRACT:
We captured 36 Northern Bobwhites (Colinus virginianus) in Mitchell County, Texas
in June–September 2013, and examined them for the eyeworm Oxyspirura petrowi. We recovered
334 eyeworms from 28 of 29 adult bobwhites (97%); infections ranged from 1–40 worms and mean
(6SD) abundance of 11.9613.0. Three of seven juveniles were infected, and those infected had
one eyeworm each. Prevalence of eyeworms was similar among months. However, mean
abundance of eyeworms peaked in July and August (3.362.1, 13.5615.0, and 16.9615.5), and
decreased in September (6.363.0). We suggest that several previous studies may underreport
prevalence and abundance because in those studies only the eye surface and nictitating membrane
were examined, and not eye-associated tissue, ducts, glands, or sinuses.
Key words: Colinus virginianus, eyeworm, Northern Bobwhite, Oxyspirura petrowi, Rolling
Plains Ecoregion, Texas.
INTRODUCTION
Northern Bobwhites (Colinus virginia-
nus) are declining throughout their range.
The causes are unclear, but many have
pointed to extremes in rainfall patterns,
declining quality of habitat, and habitat
fragmentation (e.g., Guthery et al. 1988;
Duren et al. 2011; Blank 2013). However,
bobwhite populations have declined even
in areas considered good-quality habitat,
such as the Rolling Plains ecoregion of
Texas (Rollins 2007). Historically, bob-
whites thrived throughout the Rolling
Plains ecoregion, producing large num-
bers of harvested quail. Bobwhite popula-
tions in this region now are highly variable
and have continued to decline over the
past two decades (Texas Parks and Wild-
life Department 2013), suggesting other
factors may be contributing to the decline.
Often overlooked is the potential impact
of parasites and diseases, despite studies
in Europe documenting the role of cecal
nematodes in negatively affecting various
population parameters in several species
of free-ranging Galliformes (e.g., Hudson
1986; Draycott et al. 2006).
The eyeworm Oxyspirura petrowi is a
heteroxenous nematode that received re-
cent interest in the role it may play in
negatively affecting game birds (Villarreal
et al. 2012). Eyeworm-infected bobwhites
were found dead after flying into buildings
and other man-made structures (Rolling
Plains Quail Research Ranch, unpubl.
data) and Jackson (1969) reported infected
bobwhites behaving erratically. These
reports led to speculation that eyeworms
may be causing visual obstruction.
Cram (1937) reported O. petrowi and
O. mansoni in several avian species from
North America. However, O. mansoni is
typically found in poultry and can result in
demonstrated pathology (Ruff 1984),
whereas O. petrowi occurs in wild avian
species (Pence 1975), particularly Galli-
formes (e.g., McClure 1949; Landgrebe et
al. 2007), including Northern Bobwhites
in the Rolling Plains ecoregion (Jackson
1969; Villarreal et al. 2012). However,
evidence of pathologic consequences of O.
petrowi is lacking (Villareal et al. 2012)
and most examinations were based solely
on visual inspection.
DOI: 10.7589/2013-10-275 Journal of Wildlife Diseases, 50(3), 2014, pp. 000–000
#
Wildlife Disease Association 2014
0
Herein we report three findings made
during a larger, ongoing study known as
Operation Idiopathic Decline, which is a
multiyear collaborative effort to investigate
parasites and diseases occurring in quail
within the Rolling Plains of Texas and
Oklahoma. The first is evidence of a possible
eyeworm epizootic during the summer of
2013. Second is finding eyeworms in eye-
associated ducts and glands and in the nasal
sinuses, which has important implications
for parasitologic studies with the use of data
obtained exclusively from examination of
the eye surface and nictitating membrane.
Lastly, eyeworms were found attached to
tissue and ingesting blood.
MATERIALS AND METHODS
Study area
The study was conducted on a 120,000-ha
privately owned cattle ranch in Mitchell
County, Texas (32u79450N, 100u59960W).
Mean annual daily temperatures in this county
range from 35.6 C in July to 21.1 C in January
with annual precipitation of 50 cm per year
(Texas A&M AgriLife Extension 2013). Dom-
inant vegetation includes honey mesquite
(Prosopis glandulosa), juniper (Juniperus
pinchotti), prickly pear (Opuntia spp.), silver
bluestem (Bothriochloa saccharoides), and
lotebrush (Ziziphus obtusifolia) (Rollins 2007).
Trapping
From June to September 2013, Northern
Bobwhites were trapped and handled accord-
ing to Texas Parks and Wildlife permit SRP-
1098-984 and consistent with Texas A&M
University Acceptable Use Policy 2011-193,
Texas Tech University Animal Care and Use
Committee 11049-07, and Texas Tech Univer-
sity Animal Care and Use Committee 13027-
03. Voucher specimens of O. petrowi (107283)
were deposited in the U.S. National Parasite
Collection, Beltsville, Maryland.
Sixty welded-wire walk-in double funnel
traps (91.4360.9320.3 cm) were placed near
a minimally traveled ranch road (32u109N,
101u559W) at 0.4-km intervals and covered
with clippings from surrounding vegetation.
Traps were left open but baited weekly with
milo (Sorghum bicolor) for 1 mo prior to
trapping. During trapping sessions, traps were
closed until trapping was finished. Closed
traps were monitored daily at 2 hr after
sunrise and 1 hr before sunset or at sunset.
After each trapping session, all traps were
opened. Captured bobwhites were transport-
ed to The Institute of Environmental and
Human Health (TIEHH) Aviary at Texas
Tech University and held in individual
25361-cm cages prior to examination. Bob-
whites were supplied feed (PurinaHGame
Bird Chow; Gray Summit, Missouri, USA),
water, and grit ad libitum while being held.
All bobwhites were held at TIEHH for
#3 days before being euthanized.
Eyeworm examinations
Eyeworms were extracted with the use of
techniques developed during an ongoing study
at TIEHH. Live bobwhites were restrained
manually to reduce struggle, and two drops of
a topical anesthetic (0.5%proparacaine HCl
ophthalmic solution; Alcon Labs, Lake Forest,
Illinois, USA) were applied directly on the eye
to reduce potential discomfort. To ensure the
eye was fully anesthetized, a paintbrush hair
strand was laid over the eye and observed for
eye immobilization or absence of reactivity.
After the eye was fully anesthetized, tissue-
dressing forceps (Sontec 14-4340; Sontec
Instruments, Centennial, Colorado, USA),
lightly lubricated in GenTeal gel (Novartis
Ophthalmics, St. Louis, Missouri, USA) to
provide lubrication and minimize irritation
and the potential for corneal ulcerations, were
used to examine the quail eye. Upper and
lower eyelids were lifted gently and examined
for eyeworms. The nictitating membrane was
pulled gently over the eye for examination
then manipulated gently up and down to
initiate movement of eyeworms that were not
found previously. A magnifying ocular headset
(Donegan DA-5 OptiVisor headband magnifi-
er, 2.53magnification, 20-cm focal length;
Donegan Optical, Lenexa, Kansas, USA) and a
light source helped to facilitate eyeworm
collection. If eyeworms were present and
could not be extracted with forceps, the eye
was flushed with balanced salt solution (BSS,
Alcon Laboratories, Fort Worth, Texas, USA)
with the use of a 22-ga. irrigation cannula.
Extracted eyeworms were placed in physio-
logic saline solution at 37 C (Schwabe 1951).
Bobwhites were euthanized approximately
1 day after initial examination with the use of a
carbon dioxide chamber (Kent Scientific
Corp., Torrington, Connecticut, USA) fol-
lowed by cervical dislocation. Once euthaniza-
tion had taken place, the lower eyelid was
lifted, reexamined, and removed with the use
of scissors. The upper eyelid was lifted and
reexamined and the nictitating membrane was
0 JOURNAL OF WILDLIFE DISEASES, VOL. 50, NO. 3, JULY 2014
located and pulled over the eye to initiate
movement of eyeworms not found previously.
The eyeball was removed with the use of
scissors and forceps so the orbital area,
lacrimal gland and ducts, and nasal cavity
could be examined for eyeworms. Excised
eyeworms were placed in physiologic saline
solution at 37 C. All eyeworms were visually
examined with a magnifying ocular headset
immediately after extraction.
It was difficult to remove some eyeworms
because of their strong attachment to the
tissues of the eye. When eyeworms released
from the tissue and were removed, blood
was seen around the point of attachment,
around the mouth of the parasite, and inside
the body of the parasite. This condition was
witnessed multiple times over the examination
process. Eyeworm blood ingestion was con-
firmed visually with a magnifying ocular
headset and by using phase-contrast micros-
copy. The phase contrast allowed us to see the
blood-meal contents of the intestinal tract and
to confirm that eyeworms were ingesting
blood.
Statistical analyses and terminology
We conducted chi-square analyses to com-
pare the prevalence of eyeworms between host
gender and host age classes. Prevalence of
eyeworms was not analyzed because it was
similar among all months. Because our para-
site data were not normally distributed and our
sample size was small, we used a standard
1,000 bootstrap method on our mean abun-
dance data. We then performed a Welch’s
two-sample t-test on the output. Significance
was inferred at P#0.05 level.
Parasitologic terminology follows that of
Bush et al. (1997). Prevalence refers to the
number of bobwhites infected with O. petrowi
in the sample divided by total bobwhites
examined in the sample, and mean abundance
is the number of O. petrowi found in the
bobwhite sample divided by the total number
of bobwhites examined.
RESULTS
Presence of eyeworms
The surface of the eye, nictitating mem-
brane, and eye-associated ducts, glands, and
nasal sinus of 36 Northern Bobwhites (29
adults, 7 juveniles; 21 males and 15 females)
were examined for O. petrowi.Ofthe29
adult bobwhites, 28 were infected with 1–
40 eyeworms and averaged 11.9613.0
[SD]. Prevalence was consistent among
months, ranging from 91–100%,andmean
abundance of eyeworms increased from
June (3.362.1), peaked in August (16.96
15.5), and decreased in September
(6.363.0) (Table 1). These bobwhites were
captured along the same trap-transect line
throughout the duration of the study.
Three of seven juveniles were infected
with one eyeworm each. Higher mean
abundance of eyeworms occurred in adult
males than juvenile males (12.3613.5 and
1.061.7, respectively; P,0.0001) and in
adult females than juvenile females (10.56
12.6 and 1.061.4, respectively; P,0.0001).
Mean abundance of eyeworms between
sexes was similar (male: 9.6612.7, female
9.3612.2, P50.8027). Although females
appeared to have a higher prevalence of
infection compared to males, the difference
was not significant (93.3%vs. 80.9%,re-
spectively; x
2
1
51.12, P50.29). Adult
bobwhites had a significantly greater prev-
alence compared to juveniles (96.5%vs.
42.8%, respectively (x
2
1
513.6, P,0.0001)
(Table 2). Cumulative monthly rainfall to-
tals increased from May and June and
peaked in July, respectively, before drop-
ping in August and September (Fig. 1).
Eyeworm recovery
The number of eyeworms collected from
the eye surface and nictitating membrane
of live birds during the initial examination
was fewer than the number of eyeworms
collected from the nasal–lacrimal–sinus
T
ABLE
1. Prevalence, abundance, and number of
eyeworms (Oxyspirura petrowi) collected in adult
Northern Bobwhites (Colinus virginianus) captured
in Mitchell County, Texas, USA during June–
September 2013.
Month Prevalence Abundance
Number of
eyeworms
June 3 of 3 3.362.1 10
July 6 of 6 13.5615.0 81
August 10 of 11 16.9615.5 186
September 9 of 9 6.363.0 57
DUNHAM ET AL.—OXYSPIRURA PETROWI IN BOBWHITES 0
area upon necropsy 1 day later. Addition-
ally, live bobwhites that had eyeworms
removed during the initial examination of
the eye surface and nictitating mem-
branes were found to be infected in the
same locations upon examination during
necropsy. In bobwhites with .10 eye-
worms, a majority of the worms were
found inhabiting and tightly packed into
the lacrimal duct with a maximum of 30
eyeworms found in one duct. In these
cases, the lacrimal duct was visually larger
and inflamed with distinct petechial
hemorrhaging as compared to bobwhites
with no eyeworms recovered (Fig. 2).
Eyeworms varied visually in size, color,
and shape, indicating the presence of both
juvenile and adult worms. It was common
to find both adult and juvenile eyeworms
inhabiting the same areas of the eye in the
same Northern Bobwhite. Juvenile eye-
worms were much shorter and thinner,
and appeared transparent, whereas adult
eyeworms were much longer and thicker,
and more opaque in color. Female eye-
worms were examined under a microscope
to look for eggs. If eggs were seen they
were considered gravid and adult, other-
wise they were considered juveniles
(Fig. 3).
DISCUSSION
Many studies reporting O. petrowi
relied on donated, hunter-shot birds killed
F
IGURE
1. Bar graph represents monthly precipitation totals and line graph represents mean abundance
6SD of eyeworms (Oxyspirura petrowi) found in adult Northern Bobwhites (Colinus virginianus) from a
study area in Mitchell County, Texas, USA, May 2013–September 2013.
T
ABLE
2. Prevalence, abundance, and number of eyeworms (Oxyspirura petrowi) by host age and sex from
Northern Bobwhites (Colinus virginianus) captured in Mitchell County, Texas, USA, from June–
September 2013.
Sample size
Prevalence
Abundance No. of eyewormsNo. quail infected %infected
Male
Adults 16 15 93.8 12.3613.5 197
Juveniles 5 2 40 1.0061.7 5
Total 21 17 81.0 9.6612.7 202
Female
Adults 13 13 100 10.5612.6 137
Juveniles 2 1 50 1.061.4 2
Total 15 14 93.3 9.3612.2 139
0 JOURNAL OF WILDLIFE DISEASES, VOL. 50, NO. 3, JULY 2014
during the fall and winter (e.g., Erickson
et al. 1949; Pence et al. 1980) or during
periods before the breeding season (Da-
vidson et al. 1991). Davidson et al. (1991)
examined bobwhites collected in February
from 1971 to 1984 in northern Florida and
found only 3 bobwhites in 700 to be
infected with one Oxyspirura matogrosen-
sis (likely O. petrowi, based on Pence
1972). Because these studies with the use
of hunter-shot birds are reporting ‘‘survi-
vors’’ (i.e., individuals still remaining in
the population to be sampled) of various
biotic and abiotic insults encountered
during the breeding season, it is likely
that eyeworm prevalence and abundance
is underreported during the winter if
eyeworms have a direct or indirect impact
on bird survival. Unfortunately, little is
known regarding O. petrowi transmission,
infection, and population dynamics during
summer. McClure (1949) sampled Ring-
necked Pheasants (Phasianus colchicus)
during the summer, but only averaged
four eyeworms per bird with a gross
infection of 40%, whereas Robel et al.
(2003) recorded 95%infection with an
average of 14 eyeworms per Lesser
Prairie-Chicken (Tympanuchus pallidi-
cinctus) sampled, which is comparable to
our present study. However, it is unclear if
either McClure (1949) or Robel et al.
(2003) examined all the tissues where O.
petrowi can occur in a host, as done in our
study. We found high overall prevalence
and increased numbers of juvenile O.
petrowi as we continued to trap through-
out the summer. During June and July,
trapping was difficult because insects
deterred Northern Bobwhites from forag-
ing in our milo-baited traps. In addition,
all eyeworms collected from bobwhites in
June were immature but, by July, the
majority of eyeworms collected were
mature based on their size, and gravid
females were present. These observations
F
IGURE
2. (A) Front view of an eyeball of a Northern Bobwhite (Colinus virginianus) captured in
Mitchell County, Texas, USA, showing inflamed lacrimal duct associated with an infection of eyeworms
(Oxyspirura petrowi). (B) Top view of the same eyeball of a bobwhite showing an inflamed lacrimal duct.
F
IGURE
3. Juvenile and adult female eyeworms
(Oxyspirura petrowi) removed from Northern Bob-
whites (Colinus virginianus) captured in Mitchell
County, Texas, USA. Maturity of the eyeworm was
determined by size, color, and shape and a phase-
contrast microscope was used to determine the
presence or absence of eggs.
DUNHAM ET AL.—OXYSPIRURA PETROWI IN BOBWHITES 0
seemed to occur as a result of increased
rainfall on the study area from early June
to September, which in turn caused an
explosion of intermediate hosts. An in-
creasing number of intermediate hosts
would likely facilitate eyeworm transmis-
sion during summer, evidenced by in-
creased O. petrowi abundance and differ-
ent developmental stages within individual
bobwhites. Villarreal (2011) examined the
helminth community of 51 (juvenile,
n529, 6–10 wk old; adult, n522) bob-
whites in Fisher County, Texas (Rolling
Plains ecoregion) during drought condi-
tions of summer (August) 2010 and
reported O. petrowi prevalence, intensity,
and abundance of 33%, 4.060.8 (SE), and
1.060.4, respectively. In addition, of the
juveniles examined, only two were infect-
ed with three eyeworms. Those results are
substantially lower than our findings. It is
possible that the rainfall events on our
study area triggered new vegetation
growth, thereby triggering expansive pop-
ulation growth of intermediate hosts of O.
petrowi, which were then exploited by
foraging bobwhites. Alternatively, it is
possible that wetter conditions, relieving
previous drought conditions on the study
area, may increase O. petrowi egg survival
within the environment prior to ingestion
by intermediate hosts. Further examina-
tion is needed to elucidate the relationship
between rainfall and host infection rates.
Sanders (1928) and Schwabe (1950)
reported severe pathologic effects from O.
mansoni in domestic poultry, including
inflammatory response, corneal opacity,
nasal discharge, damage to the eye, and
eventual blindness. However, little is known
about the negative effects of O. petrowi on
individuals or populations of bobwhites.
Based on our finding of eyeworms in the
nasal–lacrimal–orbital tissue and observing
eyeworms connected to orbital tissue in-
gesting blood, high numbers of O. petrowi
can cause inflammation and localized pete-
chiae/spot hemorrhaging to the lacrimal
duct.
Several studies on O. petrowi are
unclear in their descriptions of how birds
were examined for eyeworms (e.g., Erick-
son et al. 1949; Villarreal et al. 2012),
whereas others were clearly explained
(e.g., Sanders 1928; Schwabe 1951). Such
inconsistencies in the methods or report-
ing of methods make it difficult to
determine if the results are reflective of
the true infection. Inconsistent methods
may also result in a substantial number of
worms being missed, which could result in
lower estimates of prevalence, intensity,
and abundance. Insufficient examinations
may result in erroneous conclusions that
infections are inconsequential when they
could be more consequential than previ-
ously thought.
There are many other factors that need
to be looked at when determining the
impact of eyeworms on Northern Bob-
whites. Infection could render the host
susceptible to impaired respiratory func-
tion, visual obstruction leading to an
inability to find/secure food or escape
predators, and increased energy expendi-
ture. Additional studies are warranted to
determine whether infections caused by
O. petrowi could lead (directly or indi-
rectly) to increased host susceptibility to
other infections or influence predator–
prey dynamics. Negative impacts of O.
petrowi may be worse than previously
believed. More in-depth investigations are
needed to assess the consequences of
eyeworm infections.
ACKNOWLEDGMENTS
Funding for this research was provided by
the Rolling Plains Quail Research Foundation.
We thank the Rolling Plains Quail Research
Ranch, Sara Pappas, Brad Thomas, Adric
Olson, and Galen Austin for laboratory and
field assistance. We also thank Steve White
and Randy Bullard for their continuous hospi-
tality and access to our study ranch.
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DUNHAM ET AL.—OXYSPIRURA PETROWI IN BOBWHITES 0
... While parasites have long been known to infect bobwhite of the Rolling Plains, their significance in terms of bobwhite conservation has remained largely obscure. However, contemporary investigations of parasites in the region have revealed epizootic events, a high prevalence, and the potential of two helminths, A. pennula and O. petrowi, contributing to the declines of local bobwhite populations (Bruno, 2014;Dunham et al., 2014a;Bruno et al., 2019a). Evidence exists of parasites like Loa and Thelazia callipaeda, which are closely related to O. petrowi (Xiang et al., 2013;Kalyanasundaram et al., 2018a), causing irritation and impaired vision in their hosts (Otranto et al., 2004;Barua et al., 2005;Nayak et al., 2016). ...
... In subsequent studies, Bruno et al. (2019b) found 40% of bobwhite sampled from 2011 to 2013 to be infected with O. petrowi, while 73% were infected with A. pennula. However, Dunham et al. (2014a) suspected previous surveys underreported eyeworm prevalence as those studies only examined the nictitating membrane and the surface of the eye. By examining eye-associated tissues as well, Dunham et al. (2014a) found 97% of bobwhite infected with O. petrowi. ...
... However, Dunham et al. (2014a) suspected previous surveys underreported eyeworm prevalence as those studies only examined the nictitating membrane and the surface of the eye. By examining eye-associated tissues as well, Dunham et al. (2014a) found 97% of bobwhite infected with O. petrowi. Today, the Rolling Plains is considered to be the epicenter of caecal worm and eyeworm infection in bobwhite (Kubečka et al., 2017), and surveys regularly yield infection rates approaching 100% with infection levels averaging >400 A. pennula and >30 O. petrowi (Henry et al., 2017;Brym et al., 2018b;RPQRF, 2019). ...
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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.
... Two helminths, eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula, have been demonstrated to have high prevalence of 66% and 91%, respectively, in wild bobwhite in the Rolling Plains ecoregion of Texas [12]. A number of studies have been published in relation to prevalence and diagnostic techniques of these parasitic infections in wild bobwhite [13][14][15][16][17]. However, the available knowledge on host parasite interaction in this species is limited due to very few studies having utilized histological or proteomic approaches to assess the host response to these parasites [12,18]. ...
... The experimental study area of the present manuscript is consistent with the study area described in Dunham et al. [13]. The broader range of application (e.g., Rolling Plains) was described by Rollins [7]. ...
... The broader range of application (e.g., Rolling Plains) was described by Rollins [7]. Wild bobwhite were collected in July of 2019 from the same study area, in the same manner, and using the same techniques previously described by Dunham et al. [13]. ...
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Many recent studies have been focused on prevalence and impact of two helminth parasites, eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula, in the northern bobwhite quail (Colinus virginianus). However, few studies have attempted to examine the effect of these parasites on the bobwhite immune system. This is likely due to the lack of proper reference genes for relative gene expression studies. Glyceraldehyde 3-phosphate dehydrogenase (GAPDH) is a glycolytic enzyme that is often utilized as a reference gene, and in this preliminary study, we evaluated the similarity of bobwhite GAPDH to GAPDH in other avian species to evaluate its potential as a reference gene in bobwhite. GAPDH was identified in the bobwhite full genome sequence and multiple sets of PCR primers were designed to generate overlapping PCR products. These products were then sequenced and then aligned to generate the sequence for the full-length open reading frame (ORF) of bobwhite GAPDH. Utilizing this sequence, phylogenetic analyses and comparative analysis of the exon–intron pattern were conducted that revealed high similarity of GAPDH encoding sequences among bobwhite and other Galliformes. Additionally, This ORF sequence was also used to predict the encoded protein and its three-dimensional structure which like the phylogenetic analyses reveal that bobwhite GAPDH is similar to GAPDH in other Galliformes. Finally, GAPDH qPCR primers were designed, standardized, and tested with bobwhite both uninfected and infected with O. petrowi, and this preliminary test showed no statistical difference in expression of GAPDH between the two groups. These analyses are the first to investigate GAPDH in bobwhite. These efforts in phylogeny, sequence analysis, and protein structure suggest that there is > 97% conservation of GADPH among Galliformes. Furthermore, the results of these in silico tests and the preliminary qPCR indicate that GAPDH is a prospective candidate for use in gene expression analyses in bobwhite.
... Common methods of assessing parasite prevalence in bobwhite have largely consisted of necropsies (e.g. [3,4,6,7]) which can involve time, money, and intense labor. Similar problems arise when using fecal floats as a nonlethal alternative, with the additional risk of potentially misidentifying parasite species' eggs [8]. ...
... The mobile research laboratory was deployed to three locations in the Rolling Plains Ecoregion including Cottle, Garza, and Mitchell Counties. Bobwhite sample collection occurred between March and October of 2018 following the procedures described in Dunham et al. [7] with an additional trap check in the afternoon for a total of 3 trap checks per day. Upon collection, bobwhites were banded, aged, sexed, weighed, given a body condition score, and a cloacal swab was taken. ...
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Over the last few decades, there has been a decline in Northern bobwhite quail (Colinus virginianus) throughout their native range. While there are various factors that may be influencing this decline, it is suggested that parasites should be taken into consideration as a potential contributor in the Rolling Plains Ecoregion. High prevalence of the eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) in bobwhite of this region, coupled with a continuous decline, creates a need to assess infection through alternative methods for regional surveillance. Previous studies have developed a qPCR method and mobile research laboratory as an option for nonlethal procedures. However, there is still a need for standardization of these techniques. Therefore, this study builds on previous protocols to develop an application that considers factors that may influence qPCR results. In this study, cloacal swabs are collected from bobwhite in three locations throughout the Rolling Plains and scaled based on amount of feces present on the swab. This data is compared to qPCR standards as a limit of quantification for both eyeworm and caecal worm to define parasitic infection levels. Binary logistic regressions confirm that the probability of detection increases for both eyeworm (Odds Ratio: 2.3738; 95% Confidence Interval: [1.7804, 3.1649]) and caecal worm (Odds Ratio: 2.8516; 95% Confidence Interval: [2.2235, 3.6570]) as swab score increases. Infection levels for eyeworm and caecal worm are based on the generated cycle threshold value averages of qPCR standards. Based on the results of this study, this method can be applied in the mobile research laboratory to quantitatively assess regional parasitic infection in bobwhite throughout the Rolling Plains.
... Such circumstances have caused people to question why bobwhites have declined despite large tracts of habitat and what could have caused such a rapid decline. A popular hypothesis is disease (Dunham et al. 2014). However, I wonder whether a tipping point exists for quail regarding the amount of habitat necessary for population persistence and whether such tipping point has been crossed in the region. ...
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Humans engage in 2 modes of thinking: an associative mode and a reasoning mode. Institutions and scientific education primarily have focused on reasoning, even though the associative mode is linked to creativity and has been actively nurtured and used by influential scientists. The inattentiveness by scientific institutions toward associative thinking is such that it has been called the forgotten half of scientific thinking, and few opportunities exist for its professional exercising. I was fortunate to have been granted such an opportunity through an invitation to speak at a symposium honoring the retirement of a noted quail scientist. The symposium directive was simple: complete intellectual freedom to explore any quail topic as long as it was grounded in science. These were ideal and welcomed conditions for engaging in associative thought and nurturing dual thinking—that is, thinking engaging both association and reasoning. Here I provide my scientific reflections. The general themes range from psychology to chaos to dialectical philosophy. Although the topics may seem far removed from quail, I highlight their potential relevancy. I offer these reflections in the spirit of stimulating scientific curiosity in the natural world, as an encouragement to push the boundaries of quail science, and, ultimately, with the hope of encouraging further opportunities for dual thinking in science. © 2021 The Wildlife Society. Humans engage in 2 modes of thought: association and reasoning. Dual thinking, or the use of both modes, is integral for creativity and has been used by some of the most influential scientists. Unfortunately, scientific institutions have focused on reasoning and shunned association leaving scientists with little opportunity to engage in creative, dual thought. Here I illustrate the value of dual thinking and present 3 case studies linking quail ecology to unconventional themes (psychology, chaos, and dialectical philosophy) with the goal of stimulating scientific curiosity in the natural world and encouraging dual thinking in science.
... Pathogenicity findings revealed disseminated pruritic erythema in the skin of the infected humans (Dung et al., 2020). Northern bobwhites infected with O. petrowi also showed signs of inflammation, along with distinct petechial hemorrhaging, corneal scarring, conjunctivitis, and keratitis was observed in the lacrimal ducts, eyelid, nictitating membrane, and in the conjunctival sac (Dunham et al., 2014;Bruno et al., 2015). Our recent O. petrowi glycoprotein challenge study using host cytokines showed a measurable immune reaction in experimental bobwhites (Kalyanasundaram et al., 2019a). ...
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Based on sequence homology and phylogenetic tree results, the first report of eyeworm Oxyspirura species larvae has been confirmed in a human patient from Vietnam. However, important information related to Oxyspirura larvae was not presented in the case study. This comment provides a more detailed comparison of the Oxyspirura larvae found in the human case study to the avian eyeworm Oxyspirura petrowi.
... Pathogenicity findings revealed disseminated pruritic erythema in the skin of the infected humans (Dung et al., 2020). Northern bobwhites infected with O. petrowi also showed signs of inflammation, along with distinct petechial hemorrhaging, corneal scarring, conjunctivitis, and keratitis was observed in the lacrimal ducts, eyelid, nictitating membrane, and in the conjunctival sac (Dunham et al., 2014;Bruno et al., 2015). Our recent O. petrowi glycoprotein challenge study using host cytokines showed a measurable immune reaction in experimental bobwhites (Kalyanasundaram et al., 2019a). ...
... Moreover, this is the first study to monitor and document the complete life-cycle of O. petrowi in the laboratory from egg to reproductive maturity, providing a clearer understanding of the timeframe associated with O. petrowi development in both of its hosts. The time points of infection reported herein may allow for better estimates into the potential for future epizootic events, as previously reported in the Rolling Plains Ecoregion [30]. Finally, this study adds to the increasing body of knowledge regarding the consequences of O. petrowi infection by providing a model for experimental infection to systematically examine the consequences of this parasite in bobwhite. ...
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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].
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The Northern bobwhite quail (Colinus virginianus) is a popular game bird that has been experiencing a well-documented decline throughout Texas since the 1960s. While much of this decline has been attributed to habitat loss and fragmentation, recent studies have identified other factors that may also contribute to decreasing quail populations. Parasites, in particular, have become increasingly recognized as possible stressors of quail, and some species, particularly the eyeworm (Oxyspirura petrowi) and cecal worm (Aulonocephalus pennula) are highly prevalent in Texas quails. Eyeworm infection has also been documented in some passerines, suggesting helminth infection may be shared between bird species. However, the lack of comprehensive helminth surveys has rendered the extent of shared infection between quail and passerines in the ecoregion unclear. Thus, helminth surveys were conducted on bobwhite, scaled quail (Callipepla squamata), Northern mockingbirds (Mimus polyglottos), curve-billed thrashers (Toxistoma curvirostre), and Northern cardinals (Cardinalis cardinalis) to contribute data to existing parasitological gaps for birds in the Rolling Plains ecoregion of Texas. Birds were trapped across 3 counties in the Texas Rolling Plains from March to October 2019. Necropsies were conducted on 54 individuals (36 quail and 18 passerines), and extracted helminths were microscopically identified. Nematode, cestode, and acanthocephalan helminths representing at least 10 helminth species were found. Specifically, A. pennula and O. petrowi had the highest prevalence, and O. petrowi was documented in all of the study species. This research adds to the body of knowledge regarding parasitic infections in quail and passerines of the Rolling Plains ecoregion and highlights the potential consequences of shared infection of eyeworms among these bird species.
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Recently, the heteroxenous eyeworm, Oxyspirura petrowi, has gained attention due to its prevalence in the declining game bird, Northern bobwhite (Colinus virginianus), but the intermediate hosts of many nematodes remain unknown. However, identifying the intermediate host of O. petrowi with traditional techniques would be difficult and time-consuming, especially considering there are more than 80 potential orthopteran hosts just in Texas. To screen a large number of samples quickly and effectively, primers for nested PCR (nPCR) were developed using the internal transcribed spacer 1(ITS1) region. Then the nPCR was used to identify which of the 35 species collected from the Order Orthoptera were potential intermediate hosts of O. petrowi. With this technique, 18 potential intermediate hosts were identified. Later, we collected live specimens of species that tested positive to confirm the presence of larvae, but larvae were not found in the live specimens, nor in the extra tissue of the species that had tested positive for O. petrowi DNA. Despite this, this study demonstrated that nPCR is more sensitive than traditional techniques and can be a valuable tool in determining the intermediate hosts of parasites.
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We conducted a 3-year study of helminth parasites to assess their effect on the lesser prairie-chicken Tympanuchus pallidicinctus. Helminth parasites were found in most of the examined wild prairie chicken carcasses: 95% had eye worm Oxyspirura petrowi, 92% had stomach worm Tetrameres sp., and 59% had caecal worm Subulura sp. Few parasite burdens or incidences of infection were related to prairie chicken body mass, gender, age or season of collection. Droppings from transmitter-equipped prairie chickens were examined for parasite eggs and the data were used to determine which free-ranging prairie chickens harboured parasites. Telemetry data from 46 heavily parasitized and 52 lightly parasitized or parasite-free prairie chickens indicated no difference between mean daily movements, monthly home ranges, clutch sizes, nest success or survival. No adverse impacts were evident in the lesser prairie-chicken population from the incidences or burdens of the helminth parasites found in our study.
Chapter
The Rolling Plains have historically provided some of the best opportunities to hunt northern bobwhite (Colinus virginianus) populations anywhere. Historically, scaled quail (Callipepla squamata) have been common to abundant over much of the Rolling Plains, but the populations decreased dramatically in the late 1980s and have been slow to reclaim their historic range. Copyright © 2007 by Leonard Alfred Brennan Manufactured in the United States of America All rights reserved.
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