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Infection levels of the eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula in the northern bobwhite and scaled quail from the Rolling Plains of Texas

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  • Anastasia Mosquito Control District

Abstract and Figures

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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Infection levels of the eyeworm Oxyspirura
petrowi and caecal worm Aulonocephalus
pennula in the northern bobwhite and
scaled quail from the Rolling Plains of
Texas
N.R. Dunham
1
, S.T. Peper
2
, C. Downing
1
, E. Brake
1
, D. Rollins
3
and R.J. Kendall
1
*
1
The Wildlife Toxicology Laboratory, The Institute of Environmental and
Human Health, Texas Tech University, Box 43290, Lubbock, Texas,
79409-3290, USA:
2
Vector-Borne Zoonoses Laboratory, The Institute of
Environmental and Human Health, Texas Tech University, Box 41163,
Lubbock, Texas 79409-1163, USA:
3
Rolling Plains Quail Research Ranch,
1262 US Highway 180 W., Rotan, Texas, 79546, USA
(Received 12 July 2016; Accepted 23 August 2016)
Abstract
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 to 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 cae-
cal 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 be-
tween 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. pet-
rowi and A. pennula infections to determine if there are individual- and/or popu-
lation-level implications due to parasitic infection.
Introduction
The northern bobwhite (Colinus virginianus) and scaled
quail (Callipepla squamata) are two of the most important
upland gamebird species in Texas because of their
popularity with hunters and also due to their economic
importance to communities (Johnson et al., 2012).
Unfortunately, both species have experienced population
declines, especially since about 1994 (fig. 1) (Texas Parks
and Wildlife Department, 2016). The decline of northern
bobwhite and scaled quail throughout their native range
has been well documented over the past few decades
(Sauer et al., 2013). The Breeding Bird Survey has shown
*E-mail: ron.kendall@ttu.edu
Journal of Helminthology, Page 1 of 9 doi:10.1017/S0022149X16000663
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a yearly decline in northern bobwhites of >4% and scaled
quail have shown a yearly decline of 3% from 1966 to 2013
(Sauer et al., 2013). The decline has been attributed to a
variety of factors, including loss of suitable habitat,
changes in agricultural practices, fragmentation and var-
iations in weather (Bridges et al., 2001; Rollins, 2007;
Hernández et al., 2013). While it is likely that there are sev-
eral inter-related factors causing this decline, the role of
parasitic infections and diseases has not been thoroughly
researched as a potential causal factor. To the contrary,
disease and parasites have long been dismissed as a prob-
lem in quail management (Lehmann, 1984; Peterson,
2007).
In the Rolling Plains ecoregion, the decline of quail has
been especially puzzling considering that habitat condi-
tions have remained relatively stable (Rollins, 2000,
2007). Cantu et al. (2005) noted that the greatest decline
of scaled quail happened in the Rolling Plains ecoregion.
These species typically exhibit a boom and bustlife
cycle that repeats approximately on a 5-year cycle
(Hernández et al., 2007; Lusk et al., 2007). Despite favour-
able weather conditions during the summer of 2010, an
anticipated irruption never occurred. The paucity of
quail left landowners, hunters and researchers looking
for reasons why quail were declining.
The importance of parasites and disease has long been
dismissed as a concern for the management of quail
populations, despite evidence that parasites are capable
of regulating wildlife populations (Lehmann, 1984;
Tompkins et al., 2002). Research addressing parasites of
Texas quail is lacking, with only sporadic efforts since
the 1940s and early 1950s (Peterson, 2007). Without a spe-
cific reason linked to the decline of quail in Texas, the
need for answers sparked a large-scale quail research ini-
tiative. The project, known as Operation Idiopathic
Decline (OID), was a multiyear collaborative effort that in-
vestigated disease, pathogens, contaminants and parasites
in quail living throughout the Rolling Plains ecoregion of
Texas and Oklahoma.
One of the most interesting findings from OID was the
number of quail that were infected with eyeworms
(Oxyspirura petrowi) (Dunham et al., 2016). This is a hetero-
xenous nematode, requiring an intermediate host to com-
plete its life cycle, which inhabits the orbital cavity, nasal
sinuses, the Harderian and lacrimal glands, and under-
neath the eyelids and nictitating membrane of quail
(Saunders, 1935; Addison & Anderson, 1969; Dunham
et al., 2014; Bruno et al., 2015). Oxyspirura spp. were first
reported in bobwhites in the Rolling Plains ecoregion of
Texas in 1965 (Jackson & Green, 1965); however, infection
has been documented in other galliformes including ring-
necked pheasants (Phasianus colchicus), lesser-prairie
chickens (Tympanuchus pallidcinctus) and ruffed grouse
(Bonasas umbellus), to name a few (McClure, 1949;
Fig. 1. Trends in the mean number of (a) northern bobwhite and (b) scaled quail from roadside surveys in the Rolling Plains ecoregion of
Texas from 1978 to 2015; () long-term mean values; (···) long-term population trend (modified from Texas Parks and Wildlife
Department, 2016).
N.R. Dunham et al.2
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Erickson et al., 1949; Robel et al., 2003). Prior to OID, little
was known about O. petrowi in bobwhites from the
Rolling Plains, except that infected birds had been docu-
mented behaving erratically and flying into stationary ob-
jects such as fences and buildings (Jackson, 1969). These
observations, coupled with the high prevalence and inten-
sities noted, led to speculation that O. petrowi infection
may be more of a problem than previously thought.
This finding has led to further investigations to determine
if O. petrowi poses a health or fitness problem in infected
quail. Subsequent studies confirmed that O. petrowi infec-
tions result in inflammation, oedema, acinar atrophy, con-
junctivitis, and damage to the cornea and eye ducts/
glands of northern bobwhites from Texas (Dunham
et al., 2014; Bruno et al., 2015).
During the summer of 2013, an O. petrowi epizootic was
documented in Mitchell County, Texas, with infection in
adult bobwhites ranging from 91 to 100% throughout
the entire summer (Dunham et al., 2014). These eyeworm
infections were much higher than the 6179% (Jackson &
Green, 1965) and 57% (Villarreal et al., 2012) previously
documented in quail in the Rolling Plains. Subsequent re-
search has also suggested that O. petrowi is now endemic
throughout the region, with infections being documented
in 29 counties throughout the Rolling Plains of Texas and
Oklahoma (Dunham et al., 2016).
The caecal worm (Aulonocephalus pennula) is another
parasitic nematode of concern in the Rolling Plains. It is
an intestinal parasite found in the intestines and caeca
of its host (Chandler, 1935; Peterson, 2007). Intestinal
parasites, much like A. pennula, have been documented
to cause inflammation of the caecal mucosa, inactivity,
weight loss, reduced growth and even death in game
birds (DeRosa & Shivaprasad, 1999; Nagarajan et al.,
2012). Caecal worms have not been studied extensively
and little is known about the potential consequences
that caecal worm infections pose for quail species in
west Texas. Rollins (1980) observed evidence of gross
pathological changes in the caeca of quail with >100 cae-
cal worms. Additionally, drought has been suggested to
increase the intensity of caecal worm infection in quail
(Lehmann, 1984), which is alarming considering that the
Rolling Plains experienced a long-term drought during
20102013. While few studies have looked at caecal
worm infections in quail, they did document high caecal
worm infections (>80% prevalence, mean intensities >80
worms) in both northern bobwhite and scaled quail
(Lehmann, 1984; Rollins, 2007; Landgrebe et al., 2007).
The aim of the present study was to monitor helminth
infections in quail in Mitchell County, Texas, to gain a bet-
ter understanding of O. petrowi infection dynamics as well
as monitor A. pennula infection in the same populations.
Given the potential damage that these parasites can
cause to their host, it is imperative that we monitor
them in the long term to assess how they may influence
quail inhabiting the Rolling Plains.
Materials and methods
Study area
The study area was a 120,000-ha privately owned ranch
in Mitchell County, Texas (32°745N, 100°596W) that
lies within the Rolling Plains ecoregion. The primary
interest of the ranch is cattle production, with some
focus on oil production and wind energy. Mitchell
County has a mean annual daily temperature that ranges
from 35.6°C in July to 1.1°C in January, with an annual
precipitation of 50 cm/year (Texas A&M AgriLife
Extension, 2016). Much of the Rolling Plains ecoregion is
comprised of rangelands that are dominated by juniper
(Juniperus pinchotti), prickly pear (Opuntia spp.) and
honey mesquite (Prosopis glandulosa); grassland species
such as silver bluestem (Bothriochloa saccharoides), sideoats
grama (Bouteloua curtipendula) and buffalo grass (Buchloe
dactyloides); and woody species such as sand shinnery
oak (Quercus havardii), netleaf hackberry (Celtis reticulata),
catclaw (Acacia spp.) and lotebush (Ziziphus obtusifolia)
(Rollins, 2007).
Collection and examination of quail
Northern bobwhites and scaled quail were trapped
from March to October in both 2014 and 2015 along the
same 9.6-km transect that was used to document an O.
petrowi epizootic in the study of Dunham et al. (2014).
This area was chosen because it had suitable quail habitat
and was near a minimally travelled gravel ranch road.
Forty-five welded-wire walk-in double funnel traps
(91.4 × 60.9 × 20.3 cm) were placed near and/or alongside
a minimally travelled ranch road (32°10N, 101°55W) at
intervals of 0.40.8 km. All traps were set next to a tree
or bush and covered with available vegetation to ensure
they were properly shaded. Each trap was left open and
baited using milo (Sorghum bicolor) for a minimum of 2
weeks prior to trapping. During trapping sessions, all
traps were monitored daily from 2 h after sunrise to 1 h
before, or at, sunset. All captured quail were transported
to The Institute of Environmental and Human Health
(TIEHH) aviary at Texas Tech University and held in 25 ×
61-cm cages for a maximum of 10 days prior to examin-
ation. Quail were provided milo, grit and water ad
libitum while being held. During their 10-day holding per-
iod, all quail were aged, sexed, weighed, cloacal swabbed,
and faeces and blood were collected. Cloacal swabs, fae-
ces and blood were collected for additional research
needs, not suitable for this manuscript, which is the rea-
son quail were held for 10 days. By day 10, all quail
were euthanized and examined for O. petrowi and A. pen-
nula infection. Voucher specimens of O. petrowi (northern
bobwhite: 1420519; scaled quail: 1420520) and A. pennula
(northern bobwhite: 1420521; scaled quail: 1420522)
were deposited in the Smithsonian Museum of Natural
History (Suitland, Maryland, USA).
During the months of NovemberFebruary in 2014 and
2015, we also collected bobwhite and scaled quail via
hunter-donations from the same study ranch where
quail were trapped. All quail were hunted using a dog
and harvested with a shotgun. After being shot, the
head and one wing from each donated quail were re-
moved and placed into individually numbered plastic
bags. The caeca were also removed from each quail and
placed in a separate plastic bag. All bags were then prop-
erly labelled, frozen and provided to the Wildlife
Toxicology Laboratory for analysis of eyeworm and caecal
worm infection. Quail were aged (adult vs. juvenile)
Eye and caecal worm infections in quail from Texas 3
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according to the presence or absence of buffed tips on the
primary wing coverts, whereas gender was determined
based on the coloration of the feather on the head and
plumage of the face and throat (Wallmo, 1956; Lyons
et al., 2012).
Parasite examinations
Eyeworms were extracted using a modified technique
developed at TIEHH (Dunham et al., 2014). After euthan-
asia and/or after hunter-donated specimens were proper-
ly thawed, the examination started for all quail by first
lifting each eyelid with forceps and looking underneath
for O. petrowi. Next, the nictitating membrane was located
and examined using forceps. After the surface examin-
ation of both eyes, the eyelids, beak and excess tissue
were removed to allow the eyeball, associated ducts/
glands and tissues to be removed. The eyeball and excised
tissues were placed into a Petri dish filled with Ringers
solution (Sigma-Aldrich, St. Louis, Missouri, USA). Both
the lacrimal and Harderian gland, along with the excised
tissues, were removed from the eyeball, teased apart and
examined using a magnifying ocular headset (Donegan
DA-5 OptiVisor headband magnifier, 2.5 × magnification,
20 cm focal length; Donegan Optical, Lenexa, Kansas,
USA) because immature eyeworms can be difficult to
see without magnification. Once all of the glands, ducts
and tissues had been examined, the head of the quail
was dipped several times in the Ringers solution, which
causes any potential eyeworms that are still attached
within the orbital cavity to release and fall to the bottom
of the Petri dish.
Aulonocephalus pennula were extracted by carefully re-
moving the caeca out of the quail and/or by thawing
the donated caeca and placing them on a 20-mesh sieve.
Next, the caeca were cut into several smaller sections
and examined by slowly teasing apart the tissues and cae-
cal contents, and looking for parasites. To help in the re-
covery, an ocular headset, light and water squirt bottle
were used. The squirt bottle was used to flush the
organics and parasites out of the caeca and the sieve
was used to filter out the faeces and expose only the caecal
worms. After all of the small sections of caecum were ex-
amined, A. pennula were transferred into a Petri dish filled
with Ringers solution and counted. Once the examination
was complete, all parasites were placed in a 70% ethanol
with 8% glycerol solution for storage.
Hypothesized strength of infection
Since 2010, there has been a considerable amount of ef-
fort to understand the dynamics of O. petrowi and A. pen-
nula in the Rolling Plains ecoregion of Texas and
Oklahoma. Northern bobwhite and scaled quail have
been collected throughout the region and we have noticed
that infection levels vary greatly between the samples.
Recent studies have documented eye pathology in quail
infected with parasites (Dunham et al., 2014; Bruno et al.,
2015), which has led to speculation that parasite infection
can influence the quail population. Using data from
Dunham et al. (2014,2016) and data collected from the
present study, we have begun to hypothesize mild, strong
and extreme infection strength for both O. petrowi and A.
pennula (fig. 2). Due to the added burden that parasites
can have on their host, less-infected quail would be ex-
pected to live longer. We expect that as the level of para-
site infection increases there is a likelihood that these quail
have reduced survivability.
Data analysis
Prevalence, mean abundance, mean intensity and range
of O. petrowi and A. pennula infection were calculated for
both northern bobwhite and scaled quail. Analysis was
conducted on the combined total of captured and hunter-
donated quail for each species. To determine if parasite
abundance was influenced during times of precipitation,
rainfall data were collected from our study location,
being recorded daily by the ranch manager using multiple
rain gauges spread throughout the study ranch. A
Fig. 2. Hypothesized strength (mild, strong and extreme) of eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula
infection in the northern bobwhite inhabiting the Rolling Plains ecoregion of Texas, 20142015.
N.R. Dunham et al.4
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KruskalWallis test was used to determine if there was a
significant difference in mean abundance of infection
between years, sex and age of both species of quail
(R Development Core Team, 2015). Prevalence of infection
is defined as the number of quail infected with the para-
site divided by total number of quail examined (Bush
et al., 1997). Mean abundance refers to the number of para-
sites found in the quail examined divided by the total
number of quail examined, whereas mean intensity is de-
fined as the average number of the parasites of interest in
infected quail (Bush et al., 1997). Significance was deter-
mined at P0.05 and means are reported as mean ± SE.
Results
Between 2014 and 2015, a total of 208 of the 219 cap-
tured/hunter-donated northern bobwhites examined for
O. petrowi (95%) and 210 of the 213 examined for A. pen-
nula (99%) were infected. A maximum of 107 O. petrowi
(approximately 50% immature) and 562 A. pennula were
documented in a single bobwhite. Northern bobwhites
averaged 19.6 ± 1.8 eyeworms (95%) and 98.6 ± 8.2 caecal
worms (98%) in 2014 and 23.5 ± 2.1 eyeworms (95%)
and 129.9 ± 10.7 caecal worms (99%) in 2015. Adult bob-
whites had on average more eyeworms and caecal
worms than juveniles in both 2014 and 2015 (table 1).
There was no significant difference in eyeworm
(χ
2
61
= 53.8, P= 0.73) and caecal worm (χ
2
147
= 144.4,
P= 0.55) infection between sexes.
From 2014 to 2015, a total of 73 of the 101 captured/
hunter-donated scaled quail examined for O. petrowi
(72%) and 96 of the 97 examined for A. pennula (99%)
were infected. A maximum of 52 O. petrowi and 255 A.
pennula were found in single scaled quail. Scaled quail
had on average 4.8 ± 1.0 eyeworms (72%) and 50 ± 6.8 cae-
cal worms (99%) in 2014 and 5.7 ± 1.3 eyeworms (73%)
and 38.1 ± 7.1 (100%) caecal worms in 2015. Eyeworm
and caecal worm infection was similar across adult and
juvenile scaled quail in both years (table 2). There was
no significant difference in eyeworm (χ
2
20
= 9.2, P= 0.98)
and caecal worm (χ
2
59
= 52.4, P= 0.72) infection between
the sexes in scaled quail.
There was a significant difference in eyeworm infection
between northern bobwhite and scaled quail (χ
2
62
= 113.7,
P< 0.001) but no significant difference in caecal worm in-
fection between these species of quail (χ
2
172
= 185.2,
P= 0.23). Since 2013, there has been a gradual increase
in average O. petrowi mean abundance and range of infec-
tion in adult and juvenile bobwhites throughout our
study area (Dunham et al., 2014)(fig. 3). Both eyeworm
and caecal worm mean abundances in bobwhites peaked
during late the summer months then decreased by the late
autumn and winter months, corresponding with the cu-
mulative monthly rainfall totals in both 2014 and 2015
(fig. 4). Both O. petrowi and A. pennula infection varied
from month to month in both years for scaled quail.
Only 4% of sampled quail had a level of infection rated
as extremefor both O. petrowi and A. pennula, while
roughly 80% of all quail in our study area had only a
mild to limited strong infection level (fig. 2).
Discussion
A recent surge in parasite studies in bobwhite and
scaled quail has raised speculation in terms of parasite in-
fluence on quail. Parasites have long been dismissed as a
problem in quail; however, recent documentation of
heavy parasitic infection concomitant with quail decline
suggests a possible causal relationship. The results of this
study confirm that northern bobwhite and scaled quail in-
habiting our study area are heavily infected with both O.
petrowi and A. pennula. Within our study area, northern
bobwhites were significantly more infected with O. petro-
wi than scaled quail (northern bobwhite >90%, scaled
quail >70%). Despite infection being so prevalent
throughout the region, with some parasites reaching epi-
zootic levels in certain areas, the knowledge base on
these two parasites remains relatively low due to the
lack of parasite studies in quail.
Both O. petrowi and A. pennula are prevalent in bob-
white and scaled quail throughout the Rolling Plains eco-
region of Texas and western Oklahoma. Approximately
15% of bobwhites sampled in the present study averaged
>40 O. petrowi per bird, with only 4% averaging more than
Table 1. Prevalence (%), mean abundance (± SE), and range of eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula)by
host age and sex from the northern bobwhite (Colinus virginianus) captured in Mitchell County, Texas, USA 20142015.
Northern bobwhite
Eyeworm Caecal worm
Sample size % Mean abundance Range Sample size % Mean abundance Range
2014
Overall 94 94.7 19.6 ± 1.8 192 90 97.8 98.6 ± 8.2 2307
Adult 77 94.8 21.6 ± 1.9 192 73 97.3 101.7 ± 8.9 2286
Juvenile 17 94.1 10.5 ± 3.2 150 17 100 85.3 ± 19.1 12307
Male 48 93.8 19.2 ± 2.2 151 46 100 99.7 ± 11.7 286
Female 46 95.7 19.9 ± 2.7 192 44 95.5 97.5 ± 11.3 4307
2015
Overall 125 95.2 23.5 ± 2.1 1107 123 99.2 129.9 ± 10.7 8562
Adult 100 98 26.1 ± 2.1 1107 98 98.9 150.0 ± 10.4 8562
Juvenile 25 84 12.8 ± 5.0 173 25 100 50.8 ± 18.1 11177
Male 64 96.9 27.6 ± 3.1 1107 62 98.4 129.1 ± 14.3 17562
Female 61 93.4 19.1 ± 2.2 179 61 100 130.7 ± 11.6 8372
Eye and caecal worm infections in quail from Texas 5
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60. As many as 107 eyeworms (approx. 50% immature)
were found in a single bobwhite and 52 eyeworms in a
single scaled quail, both of which were the highest re-
corded O. petrowi infections documented in these species
of quail. High levels of A. pennula were also found in
both species of quail, with more than 500 found in a single
northern bobwhite and more than 250 in a single scaled
quail from our study ranch. Given the documented pro-
blems related to A. pennula infections, and with a heavy
infection being documented in both northern bobwhite
and scaled quail, this parasite may be as hazardous to
quail as significant O. petrowi infections. Examination of
the pathology of the caeca was out of the scope of the pre-
sent project and pathology observations of A. pennula in-
fection were not undertaken. However, Rollins (1980)
did observe haemorrhaging in the caeca of bobwhites har-
bouring >100 caecal worms.
Eyeworm and caecal worm infections in bobwhites
peaked during the summer months in both 2014 and
2015 then decreased by late autumn, which corresponds
with the rise in precipitation. Peak transmission of many
nematodes with a heteroxenous life cycle typically coin-
cides with the wet season (MayJune in the Rolling
Plains) when intermediate hosts are most plentiful
(Davidson et al., 1980). With the potential increase in inter-
mediate host availability, due to the rise in precipitation,
there is also an increased chance for quail to become in-
fected. Cumulative monthly rainfall totals during our ex-
periment increased from April to May then slowly
dropped off throughout the summer months, before in-
creasing again in the early autumn, which coincided
with our infection data (fig. 4).
While we have been collecting data from both O. petrowi
and A. pennula, most of the focus has been on O. petrowi
infection in the northern bobwhite. Given the difference
in parasite infection in both quail species, we speculate
that the primary host of these parasites is the northern
bobwhite. Rollins (1980) reported greater infections of cae-
cal worms in scaled quail that were sympatric with bob-
whites than allopatric populations of scaled quail.
Severe pathological implications have been documented
in quail with infections ranging from 1 to 61 O. petrowi
(Bruno et al., 2015); however, significant inflammation
and haemorrhaging within the nasal-lacrimal and eye
gland/ducts was observed in northern bobwhites with
as few as 40 eyeworms (Dunham et al., 2014,2015).
Finding O. petrowi in all the months sampled, and with
their range in size, suggests that these parasites have the
potential to live inside the host for long periods of time,
indicating that infection is continuous in nature and likely
cumulative until the host dies.
The primary areas where O. petrowi is encountered in
birds are open fields, submarginal grasslands and marsh-
lands, suggesting that infection is probably dependent on
Table 2. Prevalence (%), mean abundance ( ± SE) and range of eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula)by
host age and sex from the scaled quail (Callipepla squamata) captured in Mitchell County, Texas, USA, 20142015.
Scaled quail
Eyeworm Caecal worm
Sample size % Mean abundance Range Sample size % Mean abundance Range
2014
Overall 68 72.1 4.8 ± 1.0 152 67 98.5 50 ± 6.8 1255
Adult 59 77.9 5.3 ± 0.9 152 58 100 54.5 ± 7.6 2255
Juvenile 9 33.3 1.1 ± 5.4 15 9 88.9 21.2 ± 13.2 147
Male 47 74.5 4.6 ± 1.2 152 47 97.8 52.3 ± 8.4 1255
Female 21 66.6 5.1 ± 2.0 140 20 100 44.6 ± 11.4 2208
2015
Overall 33 72.7 5.7 ± 1.3 130 30 100 38.1 ± 7.1 4177
Adult 31 70.9 5.7 ± 1.4 130 28 100 37.2 ± 7.6 4177
Juvenile 2 100 5.0 ± 2.8 19 2 100 51 ± 0 5151
Male 25 72 5.6 ± 1.5 130 24 100 37.9 ± 8.6 4177
Female 8 75 5.9 ± 2.9 126 6 100 38.7 ± 8.6 768
Fig. 3. The mean abundance (± SE) of Oxyspirura petrowi in adult
(clear bars) and juvenile (grey bars) northern bobwhite from
Mitchell County, Texas, USA; (...) trend in mean abundances
from 2013 to 2015 (Dunham et al., 2014).
N.R. Dunham et al.6
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the occurrence of intermediate hosts that are restricted to a
particular habitat (Pence, 1972). With O. petrowi infection
being documented at epizootic levels in particular areas,
as well as in 29 counties throughout the ecoregion, it is
likely that the prevalence of infection will increase.
Friend et al. (2001) suggested that parasites can reduce
host abundance during epizootic events that have high
host mortality. Additionally, parasite eggs and infective-
stage larvae have been documented to remain viable in
the environment for several months, which further in-
creases the chance of infection as parasites would be pre-
sent in these locations for long periods of time (Lund,
1960; Draycott et al., 2000). Recent research by Kistler
et al. (2016) revealed that one intermediate host can
carry as many as 90 L3 infective-stage O. petrowi larvae,
suggesting that consumption of only one or two infected
arthropods would be enough to lead to a strong or even
extreme infection. The transmission of parasites from
one organism to another depends on host availability,
so by increasing the host density the likelihood for trans-
mission increases (Hudson & Dobson, 1988).
Given the increased infection in the present study and
evidence presented in recently published manuscripts
(Dunham et al., 2014,2016; Bruno et al., 2015), we believe
that these quail are experiencing similar, if not more, irri-
tation and/or damage from their increased parasite infec-
tion. In terms of strength of O. petrowi and A. pennula
infection in quail inhabiting this ecoregion, we believe
that our hypothesized infection levels are a plausible re-
flection of what is happening. With <4% of samples of
quail having an extreme infection for both parasites dur-
ing this study, the results strongly suggest that heavily in-
fected quail are likely dropping out of the population.
Roughly 70% of all quail sampled had a mild to strong
level of parasite infection, which was expected because
they may have fewer problems associated with eye path-
ology and a higher parasite tolerance; however, as infec-
tion levels rise, their chances of surviving are most
likely reduced (fig. 2).
The population of quail declined steadily in the Rolling
Plains ecoregion from 2007 to 2014. In the midst of this de-
cline, the Rolling Plains has experienced a long-term
drought, which has been suggested to increase caecal
worm intensity in quail (Lehmann, 1984). Undoubtedly,
a sustained drought had a major impact on quail abun-
dance, but our studies documented a concurrent O. petro-
wi epizootic event that may have exacerbated the impact
of the drought (Dunham et al., 2016). In 2015 there was
an increase in quail populations throughout the Rolling
Plains ecoregion, which we speculate was due to the de-
crease in the availability of potential intermediate hosts
because drought conditions likely suppressed them. We
hypothesize that decreasing the availability of intermedi-
ate hosts likely reduces the chances of obtaining a parasit-
ic infection, thus leading to an increase in the quail
populations.
Our study continued to reveal that northern bobwhite
and scaled quail inhabiting the Rolling Plains ecoregion
are heavily infected with both eyeworm and caecal
worm parasites. The present study also documented the
most O. petrowi ever found in both northern bobwhite
and scaled quail. Additional studies are under way to con-
tinue to monitor O. petrowi infection dynamics, in order to
determine their role in the latest quail irruption, as well as
to understand O. petrowi and A. pennula infection dynam-
ics throughout the entire boombust cycle of northern
bobwhite and scaled quail. More research is warranted
to study the infection dynamics and life history of these
parasites, in an effort to determine whether either (or
both) parasite species have the ability to influence both
Fig. 4. Monthly precipitation (grey bars) and mean abundances (± SE) of (a) the eyeworm Oxyspirura petrowi and (b) the caecal worm
Aulonocephalus pennula in the northern bobwhite from Mitchell County, Texas, USA in 2014 and 2015.
Eye and caecal worm infections in quail from Texas 7
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individual- and population-level abundance of quail
throughout the Rolling Plains ecoregion of Texas.
Acknowledgements
We thank the Rolling Plains Quail Research
Foundation for funding this project. We thank the em-
ployees of our study site for providing lodging and
ranch access, and all of the quail hunters who donated
specimens for our examinations. Thank you to the
Wildlife Toxicology Laboratory personnel for their field
and laboratory assistance. Lastly, we thank the reviewers
for their time, comments and consideration of this
manuscript.
Financial support
This work was supported by the Rolling Plains Quail
Research Foundation.
Conflict of interest
None.
Ethical standards
All quail were trapped and handled according to Texas
Parks and Wildlife permit SRP-1098-984 and Texas Tech
University Animal Care and Use protocol 13066-08.
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... While these helminths have been documented in bobwhite from the West Texas Rolling Plains before (Jackson and Green, 1965), the high prevalence reported during OID led to calls for more study into the impacts of parasites and resulted in a surge of research into the topic (Bruno et al., 2015;Dunham et al., 2017;Henry et al., 2017). Recent studies suggest that helminth prevalence in bobwhite from the Rolling Plains continues to be high (Commons et al., 2019), especially in Texas, where eyeworm infection is higher than other regions (Kubecˇka et al., 2017) and where cecal worms are consistently reported in 100% of sampled individuals (Henry et al., 2017;Brym et al., 2018). ...
... A landowner donated another 4 bobwhite from Stonewall County (33811 0 N, 100815 0 W) that were included in this study as well. Wild-caught birds were transported to The Institute of Environmental and Human Health (TIEHH) at Texas Tech University, where they were euthanized via CO 2 chamber and necropsied as detailed by Dunham et al. (2017). Donated birds were frozen, stored at À20 C, and transported to TIEHH for processing. ...
... Tissues stored in this manner were kept at room temperature and examined for parasites as soon as possible, but always within 2 weeks from the initial date of necropsy to reduce the potential of damage to parasites. The eyes and ocular tissues were examined by teasing the tissues apart in a petri dish with deionized water, whereas the ceca were examined by cutting the ceca open and flushing the contents with deionized water through a VWR USA Standard 150 lm testing sieve as per Dunham et al. (2017). All other tissues were examined by carefully pulling the tissues apart in a Petri dish with deionized water. ...
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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.
... Oxyspirura petrowi have also been documented in wild turkey (Meleagris gallopavo; Kubečka et al., 2018), songbirds (Dunham and Kendall, 2014), lesser prairie-chickens (Tympanuchus pallidicinctus; Dunham et al., 2014b), Gambel's (Callipepla gambelii), and scaled quail (Callipepla squamata) (Dunham and Kendall, 2017), while A. pennula have been found in scaled quail (Dunham et al., 2017a) and wild turkey (Hon et al., 1975). The wide range of hosts for O. petrowi and A. pennula highlights the possibility that these parasites may be more widely distributed that previously thought, and if bobwhite populations recover the parasites may remain in reservoir hosts and be capable of infecting bobwhite in the future. ...
... While the widespread incidence of O. petrowi in the Rolling Plains may have exposed a large proportion of bobwhite to infection, it is also important to consider the intensity of these infections, as even highly pathogenic organisms may have negligible effects on their hosts if present only in low numbers (Fredensborg et al., 2004). Consequently, Dunham et al. (2017a) developed infection level thresholds to provide a systematic way of gauging the intensity of parasitic infection in bobwhite; during which, a large proportion of bobwhite (48%) were found to have lower eyeworm infections (<20 O. petrowi), while relatively few (15%) were heavily parasitized (>40 O. petrowi). Dunham et al. (2017a) hypothesized that this was due to highly infected individuals suffering reduced fitness, which ultimately led to mortality, and this is consistent with models of populations experiencing PIHM discussed in section 4.3. ...
... Consequently, Dunham et al. (2017a) developed infection level thresholds to provide a systematic way of gauging the intensity of parasitic infection in bobwhite; during which, a large proportion of bobwhite (48%) were found to have lower eyeworm infections (<20 O. petrowi), while relatively few (15%) were heavily parasitized (>40 O. petrowi). Dunham et al. (2017a) hypothesized that this was due to highly infected individuals suffering reduced fitness, which ultimately led to mortality, and this is consistent with models of populations experiencing PIHM discussed in section 4.3. ...
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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.
... This species exhibits a 5-year "boom and bust" cycle, but the cause of these "booms" and "busts" is unknown (Guthery 2002;Hernández et al. 2002). However, the expected "boom" in the summer of 2010 did not occur despite stable habitat conditions (Dunham et al. 2017a). This sparked increasing interest from hunters, landowners, and researchers as to other possible causes. ...
... During a collaborative effort to investigate potential contributors to the bobwhite decline, eyeworm (Oxyspirura petrowi Skrjabin, 1929) and caecal worm (Aulonocephalus pennula Chandler, 1935) were found to be abundant and widespread in the Rolling Plains (Dunham et al. 2014;Bruno et al. 2018). Subsequent surveys continued to identify high prevalence of both parasites throughout the Rolling Plains, with some areas having 100% of infected bobwhite individuals (Dunham et al. 2017a;Henry et al. 2017;Brym et al. 2018). ...
... Furthermore, phylogenetic analyses performed by Kalyanasundaram et al. (2018) found the eyeworm to be related to the human eyeworm (Loa loa) and the human and carnivore eyeworm (Thelazia callipaeda). Both eyeworm species have been associated with vision impairment and irritation (Nayak et al. 2016;Barua et al. 2005) which may correlate with reports of bobwhite flying into stationary objects (Jackson 1969;Dunham et al. 2017a;Brym et al. 2018). ...
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... This decline has received increasing attention in the Rolling Plains Ecoregion of West Texas, considered one of the last strongholds of this popular gamebird [2]. In this region, parasites have been an especially notable concern due to the prevalence of two heteroxenous nematodes, the eyeworm (Oxyspirura petrowi Skrjabin, 1929) and caecal worm (Aulonocephalus pennula Chandler, 1935), infecting bobwhite [3][4][5][6]. ...
... 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]. ...
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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.
... In the USA, it was first reported in Galliformes and Passeriformes in Michigan during 1937 [1]. Since then, it has been identified in numerous other species from these orders, including the lesser-prairie chicken (Tympanuchus pallidicinctus) [2], northern cardinal (Cardinalis cardinalis) [3], northern mockingbird (Mimus polyglottos), curve-billed thrasher (Toxostoma curvirostre) [4], Gambel's quail (Callipepla gambelii) [5], scaled quail (Callipepla squamata) and northern bobwhite quail (Colinus virginianus; hereafter, bobwhite) [6]. Oxyspirura petrowi has gained particular notoriety in the Rolling Plains Ecoregion of West Texas, as this area is reported to be the epicenter of infection [7]. ...
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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].
... In this brief communication, we report an instance of a greater roadrunner capturing a wild quail chick in the Rolling Plains ecoregion of Texas. Since 2013, the Wildlife Toxicology Laboratory at Texas Tech University has conducted surveys of parasite abundance in Northern bobwhite quail (Colinus virginianus; hereafter bobwhite) on a privately owned ranch in Mitchell County, Texas (3287 0 45 00 N, 100850 0 6 00 W; Dunham et al., 2014Dunham et al., , 2017. These surveys encompassed extensive time in the field during which we frequently observed both quail and roadrunner activity. ...
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