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Oxyspirura petrowi infection leads to pathological consequences in Northern Bobwhite (Colinus virginianus)

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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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Oxyspirura petrowi infection leads to pathological consequences in
Northern bobwhite (Colinus virginianus)
Nicholas R. Dunham
a
, Scott Reed
b
, Dale Rollins
c
, Ronald J. Kendall
a
,
*
a
The Wildlife Toxicology Laboratory, The Institute of Environmental and Human Health, Texas Tech University, Box 43290, Lubbock, TX, 79409-3290, USA
b
Texas A&M Veterinary Medical Diagnostic Laboratory, 6610 W. Amarillo Blvd, Amarillo, TX, 79106, USA
c
Rolling Plains Quail Research Ranch, 1262 U.S. Highway 180 W., Rotan, Texas, 79546, USA
article info
Article history:
Received 2 September 2016
Received in revised form
22 September 2016
Accepted 27 September 2016
Keywords:
Colinus virginianus
Eyeworm
Northern bobwhite
Oxyspirura petrowi
Parasitism
Pathology
abstract
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 inuencing their disappearance. Infection by the eyeworm (Oxyspirura petrowi) has been docu-
mented 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.
©2016 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Ocular diseases are commonly reported in avian species with
one of the most common being primary or secondary inammatory
diseases of the eyelids and conjunctiva (Bay
on et al., 2007). Para-
sitic infection of the eye may lead to ocular disease which may be
very debilitating to the host. Visual function in birds is essential for
ying, surviving in the wild, and reproduction (Jezler et al., 2010;
Korbel and Habil, 2011). Even partial impairment of vision caused
by eye disease may have far-reaching consequences because
compensation by other senses is mostly insufcient and/or
impossible (Korbel and Habil, 2011).
Recently, a parasitic eyeworm (Oxyspirura petrowi) has received
increased attention due to the high prevalence detected in native
galliforme populations in the United States (Robel et al., 2003;
Villarreal et al., 2012; Dunham et al., 2016). Specically, the
decline of the Northern bobwhite (Colinus virginianus)inwest
Texas has prompted an investigation of the factors inuencing the
disappearance of these birds. Quail populations are a substantial
part of west Texas hunting culture, and consequently are of eco-
nomic importance for many rural communities throughout the
Rolling Plains (Johnson et al., 2012). With the quail decline
impacting many communities in Texas, researchers began looking
at every possible factor that could be inuencing these populations.
Helminth parasites have been overlooked historically (Lehman,
1984), but eyeworm infections are now considered a possible factor
contributing to the decline of Northern bobwhites in Texas
(Dunham et al., 2014, 2016; Bruno et al., 2015). Oxyspiurura petrowi
is a heteroxenous parasitic nematode reported to infect the eyes of
many avian hosts (Dunham and Kendall, 2016) with species of this
genus being documented in >80 avian species worldwide (Addison
and Anderson, 1969). Eyeworms inhabit the eyelids, nictitating
membrane, nasolacrimal duct, lacrimal gland, Harderian gland, and
intraorbital tissues of its host (Cram, 1937; Addison and Anderson,
1969; Robel et al., 2003; Dunham et al., 2014; Bruno et al., 2015).
There has been interest in studying eyeworm infection in
Northern bobwhite (Colinus virginianus) since recent research
discovered that this parasite is endemic to the Rolling Plains ecor-
egion of Texas and Oklahoma (Dunham et al., 2016). Over the past
few years, eyeworm infection has been documented extensively in
bobwhites throughout the ecoregion and led researchers to
examine the potential inuence that parasites have on their decline
(Villarreal et al., 2012; Xiang et al., 2013; Dunham et al., 2014). The
impact(s) of eyeworms on the host itself is unclear. A few studies
have shown that these parasites do not cause pathological effects or
*Corresponding author.
E-mail address: ron.kendall@ttu.edu (R.J. Kendall).
Contents lists available at ScienceDirect
International Journal for Parasitology:
Parasites and Wildlife
journal homepage: www.elsevier.com/locate/ijppaw
http://dx.doi.org/10.1016/j.ijppaw.2016.09.004
2213-2244/©2016 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
International Journal for Parasitology: Parasites and Wildlife 5 (2016) 273e276
gross lesions (McClure, 1949; Pence, 1972; Ruff and Norton, 1997);
however, Saunders (1935) observed ocular irritation caused by
eyeworm infections. Recently, O. petrowi infections were reported
to cause severe inammation and edema (Dunham et al., 2014,
2015). Bruno et al. (2015) rst reported lesions associated with
eyeworm infection in Northern bobwhites found in the Rolling
Plains of Texas. Eye inammation progressing to destruction of the
eye has been noted in a related eyeworm species (Oxyspirura
mansoni) found commonly in poultry (Ruff and Norton, 1997).
The purpose of this study was to (1) examine the host response
to infection with O. petrowi, (2) determine the extent and incidence
of lesions associated with O. petrowi and (3) discuss the possible
contribution that O. petrowi-associated pathology has on the
decline of Northern bobwhites in the Rolling Plains ecoregion of
Texas and Oklahoma.
2. Materials and methods
2.1. Ethics statement
Animal experiments were approved by Texas Tech University
Animal Care and Use Committee under protocol 13066-08. All quail
were trapped and handled according to Texas Parks and Wildlife
permit SRP-1098-984 and SRP-0715-095.
2.2. Study area
The experimental study area of the present manuscript is
consistent with the study area described in Dunham et al. (2014).
2.3. Quail trapping
All Northern bobwhites were collected from the same trapping
location, in the same manner, and using the same techniques pre-
viously described by Dunham et al. (2014).
2.4. Histological techniques
After euthanasia, the head was removed from the body of each
sample. While holding the head in hand, the lower mandible, neck,
and additional tissues were gently removed. Next the skin and
feathers were carefully excised leaving only the skull, upper
mandible, and eyelids. Heads were xed in 10% neutral buffered
formalin. Each head was xed for a minimum of 4 days. Skulls were
decalcied with 23% w/w hydrochloric acid for 12e16 h. Decalcied
xed heads were then sectioned in 3 mm intervals prior to pro-
cessing. All tissues subsequently were processed routinely in an
automated Shandon Pathcentre
®
histology processor (Thermo
Scientic, Waltham, MA), which dehydrated tissues in progres-
sively increased concentrations of ethanol and cleared in xylene
prior to parafn embedding. Processed tissue was then embedded
in Paraplastparafn wax (VWR, Radnor, PA) to create tissue
blocks for microtomy. Tissue was sectioned at 4
m
thickness with a
microtome and mounted on glass slides for staining. Routine
staining with hematoxylin and eosin (VWR Premium Histology
Stains) was performed, slides were cover-slipped, and specimens
were examined microscopically by a board-certied veterinary
pathologist. Imaging was performed with a Nikon Digital Sight DS-
SM camera (Nikon Instruments Inc., Melville, NY) connected to an
Olympus BX-51 bright eld microscope (Olympus America Inc.,
Center Valley, PA). The Harderian gland, lacrimal gland, cornea,
eyelids, nictitating membrane, and other eye-associated tissues
were adequately sampled for each eye of each sample.
2.5. Pre-preparation for scanning electron microscopy
Eyeworms were removed using techniques described in
Dunham et al. (2015). To prepare eyeworms for scanning electron
microscopy photographs, each eyeworm was dehydrated. The
dehydration started by placing the designated eyeworms in a
deionized water bath for 15 min. Next, eyeworms were placed into
each ethanol solution (30%, 50%, 80%, 90%, and 100%) for 15 min
followed by a 15 min acetone bath. Once nished, each eyeworm
was individually stored in a 5 ml tube with 100% ethanol and sent to
the Tulane Coordinated Instrumentation Facility (New Orleans, LA),
where scanning electron microscopy was performed. Voucher
specimens of O. petrowi (107282) were deposited in the U.S. Na-
tional Parasite Collection, Beltsville, Maryland.
2.6. Parasite identication
Identication of O. petrowi was based on histological and
morphological characteristics, such as spicule and esophagus
length, as described by Addison and Anderson (1969) and Pence
(1972).
3. Results
A total of 25 of the 28 (89.3%) Northern bobwhites were infected
with O. petrowi. Fourteen of 15 males, 11 of 13 females, 12 of 12
adults, and 13 of 16 juveniles were found to be infected. Eyeworms
were found in the lacrimal gland, Harderian gland, nictitating
membrane, bulbar conjunctive, fornix of the conjunctiva, and
nasolacrimal duct. Histological sections of the Harderian gland
demonstrated lesions, with a varying degree of presumed severity,
associated with the presence of O. petrowi (Figs. 1 and 2). O. petrowi
presence was associated with lymphoplasmacytic Harderian gland
adenitis in all cases. In addition to increasing inammatory cell
inltration associated with infection, there was also increased at-
rophy and corresponding duct dilation.
The intraluminal presence of the O. petrowi was associated with
a moderate to marked Harderian gland adenitis and brosis. In this
study, several birds had corneal epithelial erosions and edema
Fig. 1. Histological section of a Northern bobwhite (Colinus virginianus) Harderian
gland with intraluminal Oxyspirura petrowi parasites in transverse section (indicated
by arrows) and marked heterophilic Harderian adenitis. Hematoxylin and eosin
staining at 100, scale ¼100
m
m*¼marked lymphocyte and heterophilic inam-
matory cell inltrate; C ¼cuticle; HD ¼hypodermis; SM ¼somatic musculature;
LC ¼lateral cords; PC ¼pseudocoelom; A ¼alimentary tract; U ¼uterus containing
embryonated eggs.
N.R. Dunham et al. / International Journal for Parasitology: Parasites and Wildlife 5 (2016) 273e276274
causing corneal edema. Corneas of many infected bobwhites
appeared to be cloudy and have early ulcerative erosions. Eye tis-
sues from the three uninfected quail lacked gland atrophy when
compared to infected birds.
4. Discussion
While many ocular conditions are reported in avian species, the
impact that ocular parasites have on their hosts are not fully un-
derstood. Our results suggest that eyeworms, such as O. petrowi,
negatively impact ocular tissues by causing inammation, brosis,
and adenitis to the host. Past studies with Oxyspirura spp. observed
ocular irritation with no signs of damage in other galliforme spe-
cies, but histological techniques were not implemented (Saunders,
1935; McClure, 1949; Pence, 1972). A closely related eyeworm,
Oxyspirura mansoni, has been associated with damage to the con-
junctiva and lacrimal ducts in poultry (Kobayashi, 1927) and re-
searchers hypothesized that severe infection, coupled with
inammation, would likely lead to blindness (Sanders, 1929). Bruno
et al. (2015) rst documented eye pathology in bobwhites associ-
ated with O. petrowi and infection within the Harderian gland.
Additionally, Dunham et al. (2014, 2015) revealed signicant
inammation and petechial hemorrhaging associated with
O. petrowi infection. This research, along with the present study,
describe a series of detrimental consequences within the Northern
bobwhite host when infected with eyeworms.
Visual acuity is not only necessary for nding/securing food but
also for identifying mates and escaping predators (Jezler et al.,
2010). In the present study, eyeworm infection caused adenitis
(glandular inammation) in both juvenile and adult Northern
bobwhite. Inammation of any kind is commonly associated with
pain due to swelling. The inammation and gland destruction
associated with O. petrowi infection, if allowed to progress, would
lead to gland destruction and functional compromise. Swelling in/
around the eye causes impingement on stretch receptors which
releases cytokines followed by the release of stress hormones. Add
the irritation caused by oscillating and migrating larids, these
quail would be suspected to be signicantly compromised in terms
of foraging and escaping predation.
All avian species possess intraorbital gland which consist of the
lacrimal and Harderian gland (Dimitrov and Genchev, 2011). The
eye requires secretions from the lacrimal and Harderian gland for
moistening, nutrition, and controlling orbital and ocular defense
(Knop and Knop, 2005; Kozlu and Altunay, 2011). In time, the
adenitis would likely result in gland atrophy and brosis, a condi-
tion that was observed in several of the samples in this study. These
conditions cause a deciency in tear production called kerato-
conjuctivitis sicca (KCS), which is commonly known as dry eye.
This KCS condition is likely to lead to corneal ulcerations and a
reduction in vision. In addition the inammatory condition itself
would be expected to cause signicant morbidity resulting from
pressure, swelling, and likely lead to pain associated with inamed
glands. Inammation was witnessed in all quail samples that were
infected.
Several cornea samples appeared cloudy and had signs of early
erosions. Corneal damage is often very painful and debilitating
when compromised in any manner. The cornea is the most
important structure of the ocular surface for the maintenance of
visual function (Knop and Knop, 2005) hence, corneal damage may
be painful and debilitating. With the Northern bobwhites having an
average life span of approximately six months (Hern
andez and
Peterson, 2007) and with the negative impacts of eyeworm infec-
tion, it is likely that bobwhites that survive longer harboring these
parasites have more inammation and eye pathology. Additional
studies are warranted to determine if pain is associated with
inammation and swelling in bobwhites infected with eyeworms.
Dunham et al. (2015) revealed that eyeworms have a unique
mouth structure that we speculate likely enables them to attach
Fig. 2. Histological section of Northern bobwhite (Colinus virginianus) Harderian glands with a varying degree of pathological response associated with Oxyspirura petrowi infection.
Scale bar ¼200
m
m.
N.R. Dunham et al. / International Journal for Parasitology: Parasites and Wildlife 5 (2016) 273e276 275
and potentially feed. The potential implications of attaching eye-
worms, along with a high prevalence of infection found within
individual quail, would be expected to cause localized tissue
trauma and inammation. To strengthen this hypothesis, Fig. 3
shows the rst ever image of an O. petrowi mouth structure. If
eyeworms do attach to tissues it is likely detrimental to the host;
however, determining damage caused by mouth parts was out of
the scope of the present study and additional research is needed.
The present study supports the recent data suggesting that
O. petrowi infection may impact the Northern bobwhite host.
Although cause and effect are not proved, we saw a varying degree
of lesion severity within the Harderian gland associated with
O. petrowi infection suggesting a causal relationship, which wasn't
previously documented in related studies. While the results of this
study cannot determine if O. petrowi infection leads to visual
impairment, it is likely that the pathological damage associated
with infection negatively impacts the eye function and reduces
survival. Additional research is needed to determine if O. petrowi
infections decrease vision and play a role in the tness, hence
survival, of Northern bobwhites.
Acknowledgments
We thank Park Cities Quail and the Rolling Plains Quail Research
Foundation for their continued nancial support of our quail
research. We thank the Texas A&M Veterinary Medical Diagnostic
Laboratory (Amarillo, TX) and Comparative Ocular Pathology Lab-
oratory of Wisconsin (Madison, WI) for performing the pathology
evaluation on our quail samples. We thank the owners and em-
ployees of our study ranch for allowing access and providing lod-
ging. Lastly we thank members of the Wildlife Toxicology
Laboratory for their eld and laboratory assistance.
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N.R. Dunham et al. / International Journal for Parasitology: Parasites and Wildlife 5 (2016) 273e276276
... 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]. ...
... 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 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]. ...
... 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. ...
Article
Full-text available
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].
... Despite their high prevalence, it is currently not completely understood how these parasites affect the survival of bobwhite. It has been proposed that heavy infection by caecal worms could lead to malnutrition in bobwhite (Dunham et al., 2017b), which may hinder survival, whereas eyeworms, which are found in the tissues around the eye, can cause cellular damage to the eye tissues, as well as scarring and interstitial keratitis of the cornea (Bruno et al., 2015;Dunham et al., 2016). Bobwhite infected with eyeworms have therefore been hypothesized to have impaired vision, which is supported by anecdotal reports of abnormal behavior like bobwhite flying into large structures (Brym et al., 2018a). ...
... After euthanasia, bobwhite were immediately necropsied following procedures from Dunham et al. (2016Dunham et al. ( , 2017b. Caecal and eyeworms were identified via morphological traits (Dunham et al., 2016;Kalyanasundaram et al., 2017). ...
... After euthanasia, bobwhite were immediately necropsied following procedures from Dunham et al. (2016Dunham et al. ( , 2017b. Caecal and eyeworms were identified via morphological traits (Dunham et al., 2016;Kalyanasundaram et al., 2017). Caecal worms were collected from both arms of the caecum and a portion of the ileum. ...
Article
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The Northern bobwhite quail (Colinus virginianus) is an important gamebird among hunters that has been experiencing a nationwide decline for N 50 yr. In West Texas, one of the last regions to experience this downward trend, research on bobwhite populations has focused on habitat variables and, increasingly, on parasitic infection. In bobwhite, two of the most common parasites are the caecal worm (Aulonocephalus pennula) and eyeworm (Oxyspirura petrowi). To better document the state of bobwhite populations in the Rolling Plains Ecoregion, trapping , summer rooster counts, fall covey counts, and parasitic infection assessments were conducted in three counties during 2018. These efforts were compared with previous years for a longitudinal perspective. In 2018, bobwhite populations experienced a widespread decline, although some counties surveyed fared slightly better than others. More effort was required to trap fewer total bobwhite, and fewer roosters and coveys were counted than in previous years. In addition, in 2018, parasitic infection levels of caecal and eyeworms were higher than or similar to levels in previous years. Additional research is necessary to understand which factors influence bob-white populations in allopatric locations and over time.
... The heteroxenous eyeworm is typically found under the nictitating membrane, lacrimal ducts and glands, and the orbital cavity of the bobwhite (Saunders, 1935;Addison and Anderson, 1969;Robel et al., 2003;Dunham et al., 2014;Bruno et al., 2015;Dunham and Kendall, 2017). Pathological investigations by Dunham et al. (2016a) and Bruno et al. (2015) found inflammation in the lacrimal duct and lesions on the Harderian gland. This is of great concern when considering these two tissues' importance to saturation of the eye (Holly and Lemp, 1977) and immune response (Payne, 1994), respectively. ...
... Euthanasia and necropsies were performed as described in Dunham et al. (2014). Eyeworms were extracted from the eyes by removing the eyeball and associated tissues into a petri dish as outlined in Dunham et al. (2016a). Caecal worm collection followed protocols described in Dunham et al. (2017b) where caeca were removed and placed in a 20mesh sieve, then cut into smaller sections to assess caecal worm count. ...
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The northern bobwhite quail (Colinus virginianus) is a popular gamebird in the Rolling Plains Ecoregion of West Texas. However, there has been a population decline in this area over recent decades. Consistent reports indicate a high prevalence of the eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula), which may be of major influence on the bobwhite population. While research has suggested pathological consequences and genetic relatedness to other pathologically significant parasites, little is known about the influence of climate on these parasites. In this study, we examined whether seasonal temperature and precipitation influences the intensity of these parasites in bobwhite. We also analyzed quantitative PCR results for bobwhite feces and cloacal swabs against temperature and precipitation to identify climatic impacts on parasite reproduction in this region. Multiple linear regression analyses were used for parasite intensity investigation while binary logistic regression analyses were used for parasite reproduction studies. Our analyses suggest that caecal worm intensity, caecal worm reproduction, and eyeworm reproduction are influenced by temperature and precipitation. Temperature data was collected 15, 30, and 60 days prior to the date of collection of individual bobwhite and compared to qPCR results to generate a temperature range that may influence future eyeworm reproduction. This is the first preliminary study investigating climatic influences with predictive statistics on eyeworm and caecal worm infection of northern bobwhite in the Rolling Plains.
... Since OID, additional studies have confirmed pathological consequences associated with eyeworm infection [20][21][22]. There have also been suspicions of caecal worms leading to decreased vitamin A levels and malnutrition [22,23]. ...
... Since OID, additional studies have confirmed pathological consequences associated with eyeworm infection [20][21][22]. There have also been suspicions of caecal worms leading to decreased vitamin A levels and malnutrition [22,23]. However, because there are a multi- tude of variables that affect bobwhite survival in the Rolling Plains [13], isolating and quantifying the effects parasites may have on wild bobwhite population dynamics continues to challenge researchers. ...
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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.
... As such, high cecal worm and eyeworm infection are likely endemic in bobwhite from the West Texas Rolling Plains, and researchers suspect that these infections may play an important role in affecting regional bobwhite population dynamics (Commons et al., 2019). Contemporary research is also expanding our knowledge into the pathological consequences of eyeworm and cecal worm infection, as well as their potential impact on bobwhite populations (Bruno et al., 2015;Dunham et al., 2016;Henry et al., 2020). However, due to the complexity of parasite-host interactions, achieving a comprehensive understanding of how helminths affect bobwhite in the Rolling Plains is a formidable challenge, and substantial knowledge gaps remain. ...
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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.
... Anecdotal accounts of eyeworm infected bobwhite from the Rolling Plains exhibiting erratic behavior (Jackson, 1969) spurred concerns that these parasites may be causing visual impairment by damaging structures within the eyes of infected individuals. Later, researchers conducted pathological assessments of the eyes of infected bobwhite and confirmed inflammation and damage to the eye tissues and cornea of bobwhite hosts, as well as hemorrhaging of nasolacrimal ducts (Bruno et al., 2015;Dunham et al., 2015Dunham et al., , 2016bHunter, 2016). Because bobwhite are highly dependent on their sense of vision when foraging, navigating their environment, and evading predators, the potential effects of impaired vision may be substantial. ...
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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.
... Oxyspirura petrowi was first reported in bobwhite from Texas in 1961, with a prevalence of 49% (Jackson, 1969), but since then this parasite has frequently been found with a prevalence of 90-100% in bobwhite of the Rolling Plains Henry et al., 2017;Commons et al., 2019). Researchers have also documented O. petrowi in songbirds , conducted phylogenetic analysis (Kalyanasundaram et al., 2018), and demonstrated pathological changes in the eye of birds infected with this parasite (Bruno et al., 2015;Dunham et al., 2016b). ...
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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.
... en Cryptosporidium spp. en myiasis (Abrams et al., 2002;Dubey, 2002;Elias et al., 2008;Lopez et al., 2010;Church et al., 2013;Dunham et al., 2016). Veel van deze parasieten komen echter zelden voor in West-Europa en infecties worden vaak uitsluitend waargenomen bij in het wild levende dieren of in het wild gevangen dieren. ...
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A five-year-old, female scaly-sided merganser was presented with a chronic recurrent conjunctivitis of the left eye. Physical examination showed a caseous nodular lesion at the palpebral conjunctiva associated with excessive tearing. Necropsy revealed caseous necrotic debris at the left conjunctiva and infra-orbital sinus, but also multiple granuloma in several internal organs. Histological examination showed granulomatous splenitis, hepatitis, arteritis, fibrinonecrotic enteritis and conjunctivitis, and also amyloidosis of liver and spleen. Bacterial and molecular tests of a conjunctival swab in the live animal showed the presence of a multiresistant Escherichia coli strain and Chlamydia psittaci, respectively. These bacteria had only a secondary pathogenic role. No premortem cytological examination or Ziehl-Neelsen (ZN) staining of the histological section of the conjunctiva biopt or additional tests, such as blood test and radiographs, were performed. Finally, a Mycobacterium avium infection of the conjunctiva and internal organs was confirmed following necropsy by ZN staining and PCR analysis. Local and systemic antimicrobial treatments with fluoroquinolones, tetracyclines and aminoglycosides were unsuccessful.
... Colinus virginianus L. (Northern Bobwhite, hereafter, Bobwhite) and Meleagris gallopavo L. (Wild Turkey) are among the most pursued game birds in Texas and occur sympatrically across most of their range. Recent studies in the Rolling Plains ecoregion of Texas have considered the role of disease in population regulation of Bobwhite, with heightened interest on the eyeworm Oxyspirura petrowi (Cobbold) (Brym et al. 2018;Dunham et al. 2014Dunham et al. , 2016aDunham et al. , 2016b. The highest known prevalence and intensity of eyeworms among Bobwhites in the US occurs in the Rolling Plains ecoregion of northwest Texas and western Oklahoma (Kubečka et al. 2017). ...
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The Rolling Plains ecoregion of Texas hosts the highest known prevalence and intensity of the eyeworm Oxyspirura petrowi among Colinus virginianus (Northern Bob-white) in the US. Meleagris gallopavo (Wild Turkey) and the Northern Bobwhite have a similar diet (i.e., facultative insectivore), overlapping ranges, and phylogenetic relatedness (i.e., Galliformes); thus, we expected Wild Turkeys sympatric with an infected population of wild Northern Bobwhites to also host eyeworms. In 2014, we dissected 104 Wild Turkey and 50 Northern Bobwhite heads from a 27,530-ha area in Roberts County, TX. Only 1 turkey (female) was infected with a single eyeworm. Prevalence, mean abundance (± SE), and mean intensity (± SE) among Northern Bobwhites on the same area was 58%, 7.6 ± 1.8, and 13.1 ± 2.7, respectively. Eyeworm prevalence between Northern Bobwhite males (n = 25, 64%) and females (n = 25, 52%) was not statistically different (P = 0.57). Mean abundance (± SE) was similar between males (8.8 ± 2.6) and females (6.4 ± 2.5; P = 0.53), and mean intensity between males (13.7 ± 3.5) and females (12.4 ± 4.3) did not differ (P = 0.71). Wild Turkeys do not appear to be suitable hosts for O. petrowi.
Article
Helminths were examined from 145 scaled quail ( Callipepla squamata ) collected during the 2012–2013, 2013–2014 and 2014–2015 hunting seasons from a semi-arid region of Texas that spans four ecoregions. Helminth infracommunities were species poor, averaging 1.7 (range 1–4) species. Six species occurred within the component community of which one ( Oxyspirura petrowi ) is known to be pathogenic to quail. Aulonocephalus pennula was most abundant (9991 individuals, 95% of total) followed by O. petrowi (391 individuals, 4%). Each of the remaining four species was rare (≤21% prevalence) and contributed few individuals (<1%). In the High Plains ecoregion, prevalence of O. petrowi was higher in host collections made during the 2013–2014 hunting season than either hunting seasons 2012–2013 or 2014–2015 and was higher in the High Plains ecoregion than the Edwards Plateau ecoregion during the 2013–2014 hunting season. Mean abundance of A. pennula and O. petrowi was higher in scaled quail from the High Plains ecoregion than the Edwards Plateau ecoregion. Our results provide new information about helminth fauna in scaled quail, persistence of indirect lifecycle helminth species within a semi-arid region, and the occurrence of pathogenic helminth species within this host species.
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Northern bobwhite ( Colinus virginianus ) and Scaled quail ( Callipepla squamata ) have been declining steadily throughout much of their historical range over the past few decades. Even the Rolling Plains of Texas, historically rich with wild quail and one of the last remaining quail strongholds, has been suffering a population decline, most notably since 2010. Gambel's quail ( Callipepla gambelii ) have also been experiencing their own decline throughout their respective range, but not as significant as that of other species of quail. Eyeworms ( Oxyspirura petrowi ) in quail have been recognized for years but not thoroughly studied until recently. New research reveals that O. petrowi infection can cause inflammation, oedema, and cellular damage to the eye of the quail host. The objective of this research was to better understand the prevalence of the eyeworm infection in different quail species, expand on known distribution, and determine if there is a relationship between location and species infected with eyeworms. Northern bobwhite, Scaled quail and Gambel's quail were hunter-donated from one county within Texas, New Mexico and Arizona, and examined for the prevalence, mean abundance and mean intensity of eyeworm infection from November 2013 to February 2014. Quail from every location were found to have individuals with a varying degree of eyeworm infection. This is the first study to document eyeworm infection in Gambel's quail and in quail in New Mexico and Arizona, and reports the highest eyeworm infection found in Northern bobwhite and Scaled quail.
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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.
Article
The present investigation was performed on 80 intraorbital glands (40 lacrimal and 40 Harderian) obtained from 20 sexually mature clinically healthy Japanese quails (10 males and 10 females) of the Manchurian Golden and Pharaoh breeds. Prior to fixation, the weight and metric dimensions of glands were determined. In both quail breeds studied, a clear sexual dimorphism with regard to live body weight was observed with female birds being heavier than males. The body weight of birds did not correlate with the weight of either gland. There was neither a correlation between the three morphometric parameters and quails' sex and breed.