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The Parasitic Eyeworm Oxyspirura petrowi as a Possible Cause of Decline in the Threatened Lesser Prairie-Chicken (Tympanuchus pallidicinctus)

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The Parasitic Eyeworm Oxyspirura petrowi as a Possible Cause of Decline in the Threatened Lesser Prairie-Chicken (Tympanuchus pallidicinctus)

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Lesser prairie-chickens (Tympanuchus pallidicinctus) have been declining range wide since the early 1900's despite efforts to establish conservation and improve their habitat. In early 2014, the lesser prairie-chicken was listed as a threatened species under the U.S Endangered Species Act and the need to find out why they are declining is more important than ever. Nine hunter shot lesser prairie-chickens were donated and sampled for the presence or absence of the eyeworm Oxyspirura petrowi, a known parasite that can cause damage to the eye of its host, and common environmental contaminants. Eyeworm infection was found in 7 of 9 birds (78% infection rate) with an infection range between 0-16 O. petrowi per bird. Breast, liver, and fat tissue samples from the lesser prairie-chickens were analyzed for the frequency of 20 organochlorine pesticides. Femurs and livers were also tested on these birds for metal contaminants. Pesticides were found in several samples above the detection limits but were still in the low ng/g range. Notable was the ubiquitous presence of endrin aldehyde across all tissues. One femur showed 5.66 µg/g of lead (Pb) but this is still relatively low. No liver samples had elevated mercury (Hg) above detection limits. The presence of these organochlorines is consistent with the historic use of pesticides in this region. With pesticide and metals found in such low levels and parasitic nematode infections at rather high levels, it is recommended that these parasites be further evaluated as a contributing factor to the decline of the lesser prairie-chicken.
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The Parasitic Eyeworm
Oxyspirura petrowi
as a Possible
Cause of Decline in the Threatened Lesser Prairie-Chicken
(
Tympanuchus pallidicinctus
)
Nicholas R. Dunham, Steven T. Peper, Catherine E. Baxter, Ronald J. Kendall*
The Wildlife Toxicology Laboratory, The Institute of Environmental and Human Health, Texas Tech University, Lubbock, Texas, United States of America
Abstract
Lesser prairie-chickens (Tympanuchus pallidicinctus) have been declining range wide since the early 1900’s despite efforts to
establish conservation and improve their habitat. In early 2014, the lesser prairie-chicken was listed as a threatened species
under the U.S Endangered Species Act and the need to find out why they are declining is more important than ever. Nine
hunter shot lesser prairie-chickens were donated and sampled for the presence or absence of the eyeworm Oxyspirura petrowi,
a known parasite that can cause damage to the eye of its host, and common environmental contaminants. Eyeworm infection
was found in 7 of 9 birds (78% infection rate) with an infection range between 0–16 O. petrowi per bird. Breast, liver, and fat
tissue samples from the lesser prairie-chickens were analyzed for the frequency of 20 organochlorine pesticides. Femurs and
livers were also tested on these birds for metal contaminants. Pesticides were found in several samples above the detection
limits but were still in the low ng/g range. Notable was the ubiquitous presence of endrin aldehyde across all tissues. One
femur showed 5.66 mg/g of lead (Pb) but this is still relatively low. No liver samples had elevated mercury (Hg) above detection
limits. The presence of these organochlorines is consistent with the historic use of pesticides in this region. With pesticide and
metals found in such low levels and parasitic nematode infections at rather high levels, it is recommended that these parasites
be further evaluated as a contributing factor to the decline of the lesser prairie-chicken.
Citation: Dunham NR, Peper ST, Baxter CE, Kendall RJ (2014) The Parasitic Eyeworm Oxyspirura petrowi as a Possible Cause of Decline in the Threatened Lesser
Prairie-Chicken (Tympanuchus pallidicinctus). PLoS ONE 9(9): e108244. doi:10.1371/journal.pone.0108244
Editor: Gregorio Moreno-Rueda, Universidad de Granada, Spain
Received July 7, 2014; Accepted August 26, 2014; Published September 24, 2014
Copyright: ß2014 Dunham et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.
Funding: The authors have no support or funding to report.
Competing Interests: The authors have declared that no competing interests exist.
* Email: ron.kendall@ttu.edu
Introduction
Historically, lesser prairie-chickens (Tympanuchus pallidicinc-
tus) have thrived throughout much of the southern United States
but since the early 1900’s their population and range have been
diminished by over 90% [1]. Arguably much of their decline has
been blamed on anthropogenic factors including habitat loss due
to agriculture or habitat fragmentation [2]. In early 2014, the
lesser prairie-chicken was placed as a threatened species under the
U.S Endangered Species Act which means if proper conservation
and management isn’t established the lesser prairie-chicken will
become an endangered species in the foreseeable future under the
law [3]. Recent reports of lesser prairie-chickens flying into
stationary objects and other anecdotal reports of these birds flying
into objects, as large as vehicles and barns, have led us to wonder if
these birds have vision problems or other neurological problems.
These problems are often caused through either parasitic
infections, contamination by organochlorine pesticides, or metal
toxicity which will be examined in this manuscript. With their
recent listing as threatened under the Endangered Species Act, the
need to find out why they are declining and increased conservation
measures are needed now more than ever.
Oxyspirura petrowi has been receiving increased attention due
to its potential role in negatively impacting gamebirds [4]. This
parasite, known as the eyeworm, is a nematode that lives on the
surface of and/or behind the eyeball in the lacrimal duct and its
associated glands. Eyeworm sizes can range from microscopic egg
to well over 15 mm in length [5]. While the lifecycle is not
completely known, it has been suggested that the lifecycle of O.
petrowi is likely similar to Oxyspirura mansoni which is known to
infect poultry [6]. The lifecycle of O. mansoni starts when a gravid
female deposits embryonated eggs in the eyes of the host, which
are then washed down the naso-lacrimal ducts to the mouth,
swallowed, and finally excreted into the feces where they are then
ingested by an intermediate host [7]. Research is still underway to
determine which arthropods are intermediate hosts for the
eyeworm.
Research by Dunham et al. (2014a) on northern bobwhites
(Colinus virginianus) revealed damage to tissues behind the
eyeball and in the nasal-lacrimal glands causing localized
hemorrhaging and swelling by these blood-feeding parasites.
Increased eyeworm infections could cause severe hemorrhaging
and swelling behind the eye, which applies pressure to the optic
nerve, probably compromising the bird’s vision. Visual impair-
ments could impact their ability to forage, fly efficiently when
escaping predators, and reproduce successfully, all of which could
ultimately decrease their survivability in the wild.
The eyeworm O. petrowi has been previously found in
lesser prairie-chickens in Texas [8] and Kansas [1]. A related
species of eyeworm (O. lumsdeni) has been documented in lesser
PLOS ONE | www.plosone.org 1 September 2014 | Volume 9 | Issue 9 | e108244
prairie-chickens in Oklahoma [9]. However, little research has
been conducted on the impact that eyeworms could have on the
decline of the lesser prairie-chicken.
Most pesticides of the organochlorine class have been banned or
restricted for years; however, they are often still very persistent in
soil and can be harmful to birds when they are exposed [10].
Organochlorines in avian species can lead to toxic effects such as
lethargy, convulsions, and emaciation with more commonly
known effects like eggshell thinning and reproductive inhibition
[11]. Additionally both lead (Pb) and mercury (Hg) are commonly
found throughout the environment and have well established
detrimental effects on wildlife health. Lead and mercury are
released into the environment by anthropogenic processes such as
spent lead ammunition or by-products of the combustion of fossil
fuels, and can lead to behavioral and neurological abnormalities.
This manuscript examines the influence of parasitic infections,
organochlorine pesticides, and metal toxicity as a potential
contributor to the lesser prairie-chicken decline.
Methods
The bodies of nine hunter-harvested lesser prairie-chickens from
Kansas were donated to the Wildlife Toxicology Laboratory at
The Institute of Environmental and Human Health (TIEHH),
Texas Tech University for extensive evaluation for the presence of
eyeworms, organochlorine pesticides, and toxic metals. These
lesser prairie-chickens were harvested by hunters in Kansas during
a limited hunting season. Specimens were salvaged from a
registered taxidermist in the taxidermy specimen preparation
process. Prior to processing by the taxidermists, each eyeball and
its associated lacrimal ducts and tissues were removed and put into
separate 70% ethanol vials. The eye sockets were examined for
any remaining eyeworms and they were placed into their
respective vials. In coordination with samples supplied by
registered taxidermists, we were allocated the eyes and their
associated ducts and glands, femur, liver, and breast muscle.
Eyeworm Examination
Each bird was thawed and examined for eyeworms. The
examination started by removing the lacrimal duct, gland, and
tissue from the eyeball and teasing them apart to look for
eyeworms. Any eyeworms that were found during the examination
process were placed in a physiological saline holding media. When
all the examinations were complete, eyeworms were then
transferred into a 70% ethanol+8% glycerin vial for preservation.
Voucher parasite specimens of O. petrowi (USNPC No. 108249)
were deposited in the U.S. National Parasite Collection, Beltsville,
Maryland. Prevalence refers to the number of lesser prairie-
chickens infected with O. petrowi in the sample divided by total
number of lesser prairie-chickens examined in the sample, and
mean is the number of O. petrowi found in the lesser prairie-
chickens sampled by the total number of lesser prairie-chickens
examined [12].
Contaminant Analysis
Samples of breast muscle, liver, and fat from the lower breast
were taken from all nine donated birds. These tissues were
extracted using a general QuEChERS method and analyzed by
GC-ECD for 20 organochlorine pesticides and metabolites:
hexachlorocyclohexane (HCH; alpha, beta, gamma (lindane),
and delta isomers), alpha and gamma chlordane, heptachlor and
heptachlor epoxide, DDT, DDE, DDD, methoxychlor, aldrin,
dieldrin, endrin, endrin aldehyde, endrin ketone, endosulfan I,
endosulfan II, and endosulfan sulfate [13]. The QuEChERS
method started by taking approximately 3 g wet weight tissue that
was then freeze dried and added to a 50 mL centrifuge tube
containing 4,000 mg anhydrous magnesium sulfate and 1,000 mg
anhydrous sodium chloride (United Chemical Technologies,
Bristol, PA, USA). To this tube 15–20 mL acetonitrile was added
with tetrachloro-m-xylene as an internal standard. After vortexing
and centrifugation (3,000 rpm for 10 min), the extract was
decanted and transferred into a 15 mL QuEChERS cleanup
centrifuge tube containing 900 mg anhydrous magnesium sulfate,
300 mg primary-secondary amine (PSA) exchange material, and
150 mg endcapped C18 (United Chemical Technologies, Bristol,
PA, USA).
Samples were analyzed on a Hewlett-Packard 6890 gas
chromatograph equipped with two Agilent columns (primary:
DB-17 ms: 30 m60.32 mm60.25 mm; secondary: DB-XLB:
30 m60.32 mm60.50 mm) and two mECD detectors. Inlet and
detector temperatures were 220uC and 300uC (both detectors),
respectively. A volume of 2 mL was injected in pulsed splitless
mode with a pulse pressure of 40.0 psi, pulse time of 0.20 min,
purge flow of 44.8 mL/min and purge time of 1.00 min. Each
standard was made by spiking chicken breast extract with a
certified OC pesticide mixture (Restek, Belafonte, PA, USA) and
TCMX (Accustandard, New Haven, CT, USA).
Additionally, livers and a portion of each femur were extracted
from all lesser prairie-chickens and sent to Trace Analysis Inc.
(Lubbock, TX, USA). Livers were analyzed for elevated mercury
levels and femurs were analyzed for elevated lead levels. Livers
were tested for mercury using modified EPA method SW-846
7471B. [14]. First 5 mL of DI water was added to a 0.5–0.6 g
portion of well-homogenized, freeze-dried sample. This mixture
was heated for 2 minutes at 9563uC. After cooling, an additional
50 mL of DI water was added, followed by 15 mL of potassium
permanganate solution, and each sample was allowed to sit for a
minimum of 15 minutes. Samples were mixed thoroughly and
then heated at 9563uC for 30 minutes. After cooling, 6 mL of
sodium chloride hydroxylamine sulfate solution was added to each
sample. These samples were then analyzed using a CETAC M-
6100 Cold Vapor Atomic Absorbance mercury analyzer. Absor-
bance for Hg was measured at 253.7 nm. Femur samples were
prepared for Pb analysis using a slightly modified version of
modified EPA method SW-846 3050B [15]. Freeze dried femurs
were digested for one hour at room temperature using 5 mL of
HNO
3
. An additional 5 mL of HNO
3
was added to each sample;
samples were then heated to 100uC. The heating process
continued until samples were completely digested and the
digestant appeared clear. Once the digestion was complete, the
samples were cooled and 10 mL of 30% H
2
O
2
was added.
Samples were then heated again until foaming subsided. At this
point, 10 mL of concentrated HCl was added and samples were
heated until the volume was reduced to 5 mL. Samples were
subsequently diluted to 50 mL using DI water. Analysis of femurs
for lead followed EPA method SW-846 6010C using a Perkin
Optima 8300 Duel View Inductively Coupled Plasma-Optical
Emission Spectrometer. Lead was measured at a wavelength of
220.353 nm in axial mode.
Method detection limits (MDLs) ranged from 8.0 ng/g for
heptachlor epoxide to 70 ng/g for methoxychlor. In general, most
MDLs are approximately10 ng/g. Generally speaking, organo-
chlorine pesticide residues in the tissues of lesser prairie-chickens
were relatively low to barely detectable. Standard detection limits
for lead was 0.263 mg/g and mercury’s was 0.00354 mg/g.
Factors Impacting Lesser Prairie Chickens
PLOS ONE | www.plosone.org 2 September 2014 | Volume 9 | Issue 9 | e108244
Results
Of the 9 lesser prairie-chickens examined, 7 were found to be
infected with a total of 49 eyeworms. Prevalence of infection was
78% with a mean abundance of 5.4466.02 [range:0–16]. Endrin
aldehyde was detected but could not be quantitated due to partial
removal in the QuEChERS cleanup step. The poor recovery of
endrin aldehyde could have been a result of removal by PSA in the
extraction step. Nevertheless, endrin aldehyde was detected on the
primary column. Figure 1 shows the detection frequencies of each
pesticide by tissue. Most residues were below method detection
limits. The range and averages for pesticides above detection limits
was recorded in Table 1. Even those pesticides found above
detection limits are in the low ng/g range, which means it’s
unlikely that these levels pose a direct threat to lesser prairie-
chicken health. Notable is the ubiquitous presence of endrin
aldehyde across all tissues. Endrin aldehyde as well as DDE are
common metabolites found in many birds including lesser prairie-
chickens [16]. The presence of these organochlorines in low
concentrations is consistent with the historic (and not recent) use of
pesticides in the region.
Lead levels in the nine femur samples averaged 0.86 mg/g and
only one of the femur samples was found to have lead above
detection limits at 5.66 mg/g. This amount of lead is relatively low
and not consistent with toxic lead exposure ranging between
2–8 mg/g [17,18]. Liver samples averaged 0.04 mg/g of mercury
and no samples had mercury above the 0.263 mg/g detection
limit.
Discussion
While our sample size is relatively low, it appears that lesser
prairie-chickens in Kansas are not being exposed to a large
number of organochlorines or two metals which are common
throughout the environment. Since organochlorine pesticides have
been banned or restricted, the likelihood of them exerting toxicity
is being reduced daily. These pesticides are constantly being
degraded in the environment and exposure is unlikely. However,
this study only measured a subsample of potential organochlorine
pesticides and didn’t look at both organophosphate and carbamate
pesticides, which means pesticides shouldn’t be completely
discarded as potential dangers to lesser prairie-chickens.
But, this is not the case when it comes to being exposed to
potential eyeworm infection. Our eyeworm infection findings in
the present study are considerably high and comparable to Robel
et al. (2003) infection rates of O. petrowi in lesser prairie-chickens
(95% infection), considering a further reduced population today.
A continuing presence of eyeworms is being reported in lesser
prairie-chicken which could indicate that this parasite could
potentially be a contributing factor to lesser prairie-chicken decline
and have deeper implications than what was previously known.
Previous research on the red grouse (Lagopus lagopus scoticus)in
Figure 1. Percent frequencies of organochlorine pesticide detections, including pesticides above and below method detection
limits, in lesser prairie-chickens (
Tympanuchus pallidicinctus
) by tissue type, Kansas, USA.
*
Method detection limits for heptachlor epoxide
were 8 ng/g, 70 ng/g for methoxychlor, and 10 ng/g for all other organochlorines.
doi:10.1371/journal.pone.0108244.g001
Factors Impacting Lesser Prairie Chickens
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Scotland has shown that high parasite burdens can ultimately
make a host more susceptible to predation [19]. Additional studies
have also shown that increased parasite loads can correlate with
the host population decline and reduced parasite loads throughout
the populations correlate with an upward trend in the host
population [20]. Eyeworm infection rates in northern bobwhites of
the Rolling Plains region of Texas have been reported at greater
than 90% in sampled birds and there is concern that the
population of bobwhites is declining [4].
The infection rate throughout this region was much higher than
what was previously thought which suggests that either the
infection may have increased or was underestimated and this
could be similar to what is happening in Kansas. However,
because these birds are hunter shot, there may be some bias that
these lesser prairie-chickens were more susceptible to being shot
because of their increased parasitism than a lesser prairie-chicken
that was eyeworm infection free.
The erratic behavior of lesser prairie-chickens flying into
stationary objects is very similar to that of other gallinaceous or
ground feeding birds, which have been found to be infected with
the parasitic eyeworm Oxyspirura petrowi [21,22]. Eyeworms are
known blood feeding nematodes that can cause inflammation and
edema behind the eyes of other gallinaceous birds. A heavy
infection of eyeworm may render lesser prairie-chickens suscep-
tible to vision problems which may impair their ability to find food
or escape from predators, and a heavy infection likely causes
increased energy expenditure.
Despite efforts to restore habitat and limit hunting in areas
where lesser prairie-chickens are commonly found, much of the
population is steadily declining to the point where they are now
threatened. Parasites like the eyeworm, which we believe has been
underestimated as a factor, could silently be impacting the
population by compromising vision which is a necessity for
predator avoidance and finding/securing food. Additionally, new
conservation practices by biologists and landowners have been to
add fence signs and/or colored marking tape on fences to help
reduce bird/fence collisions. The idea of this practice is to enable
the lesser prairie-chicken to see the fence lines; however, this
conservation practice may be counterintuitive. Marking the fences
with signs provides no net benefit to the lesser prairie-chickens by
being there and may actually provide targets with increased
probability of impact by visually impaired birds. Further research
needs to be conducted on the eyeworm and the impact they have
on their infected host, including lesser prairie-chickens, so better
management practices can be established.
Acknowledgments
We would like to thank all of the hunters who donated lesser prairie-
chickens in support of this project. We thank Trace Analysis Inc. for their
support in analyzing our samples for metal contamination. We would like
to thank all of the Wildlife Toxicology Lab members for their laboratory
support. Lastly, we would like to thank all of the reviewers of this
manuscript for all of their time and guidance in getting this manuscript
published.
Author Contributions
Conceived and designed the experiments: ND RK. Performed the
experiments: ND SP CB. Analyzed the data: ND RK. Contributed
reagents/materials/analysis tools: ND SP CB RK. Contributed to the
writing of the manuscript: ND SP CB RK.
References
1. Robel RJ, Walker TL, Hagen CA, Ridley RK, Kemp KE, et al. (2003) Helminth
parasites of Lesser Prairie-chicken Tympanuchus pallidicinctus in southwestern
Kansas: Incidence, burdens and effects. Wildl Biol 9:341–349.
2. Hagen CA, Jamison BE, Giesen KM, Riley TZ (2004) Guidelines for managing
lesser prairie-chicken populations and their habitats. Wildl Soc Bull 32:69–82.
3. United States Fish and Wildlife Service (2014) Endangered and Threatened
Wildlife and Plants; Determination of Threatened Status for the lesser prairie-
chicken; Final Rule. Federal Register 79: 10 April 2014. Available: http://www.
gpo.gov/fdsys /pkg/FR-2014-04-10/pdf/201 4-07302.pdf. A ccessed 15 May
2014.
Table 1. Average and range of select pesticides found in lesser prairie-chickens (Tympanuchus pallidicinctus) tissues (ng/g wet
weight)*, from Kansas, USA.
Pesticide Breast Muscle (n= 9) Liver (n = 9) Breast Fat (n= 8)
Alpha-HCH 14 (n = 1)
Beta-HCH 10 (n = 1) 21 (11–32) (n = 3) 17 (n = 1)
Gamma-HCH 32 (13–64) (n= 3)
Alpha Chlordane 17 (n = 1)
Gamma Chlordane 12 (n = 1)
Heptachlor 11 (9.9–13) (n = 4) 18 (9–39) (n = 6) 43 (16–120) (n = 8)
Heptachlor Epoxide 20 (8–33) (n= 2)
DDD 35 (n = 1)
DDE 27 (n = 1)
DDT 35 (13–74) (n= 3)
Aldrin 42 (n = 1)
Endrin 21 (20–21) (n = 2) 43 (n = 1)
Endrin Ketone 35 (16–57) (n= 5)
Endosulfan I 27 (n = 1)
Endosulfan Sulfate 31 (24–38) (n= 2)
*Values and pesticides shown are only those above detection limits. Endrin aldehyde could not be quantitated.
Note: Method detection limits for heptachlor epoxide were 8 ng/g, 70 ng/g for methoxychlor, and 10 ng/g for all other organochlorines.
doi:10.1371/journal.pone.0108244.t001
Factors Impacting Lesser Prairie Chickens
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4. Dunham NR, Soliz LA, Fedynich AM, Rollins D, Kendall RJ (2014a) Evidence
of an Oxyspirura petrowi epizootic in Northern Bobwhites (Colinus virginianus).
J Wildl Dis 50: 552–558.
5. Dunham NR, Soliz LA, Brightman A, Rollins D, Fedynich AM, Kendall RJ
(2014b) Live eyeworm (Oxyspirura petrowi) extraction, in-vitro culture, and
transfer for experimental studies. J Parasitol: Published Online.
6. Ruff MD (1984) Nematodes and acanthocephalan s. In: Diseases of poultry. 8
th
Ed, Hofstand MS, Calnek BW, Helmboldt CF, Reid WM, Yoder Jr HW, editor.
Iowa State University Press, Ames, Iowa, pp. 614–648.
7. Schwabe CW (1951) Studies on Oxyspirura mansoni, the tropical eyeworm of
poultry. II. Life history. Pac Sci 5:18–35.
8. Pence DB, Sell DL (1979) Helminths of the lesser prairie chicken, Tympanuchus
pallidicinctus (Ridgway) (Tetraonidae), from the Texas panhandle. P Helm Soc
Wash 46: 146–149.
9. Addison EM, Anderson RC (1969) Oxyspirura lumsdeni n. sp. (Nematoda:The-
laziidae) from Tetraonidae in North America. Can J of Zool 47:1223–1227.
10. Hellou J, Lebeuf M, Rudi M (2012) Review on DDT and metabolites in birds
and mammals of aquatic ecosystems. Environ Rev 21:53–69.
11. Fimreite N (1984) Effects of lead shot ingestion in willow ptarmi gan. Bull of
Environ Contam Toxicol 33:121–126.
12. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology
in its own terms: Margolis et al. revisted. J Parasitol 83:575–583.
13. Cies
´lik E, Sadowska-Rociek A, Ruiz JMM, Surma-Zadora M (2011) Evaluation
of QuEChERS method for the determination of organochlorine pesticide
residues in selected groups of fruits. Food Chem 125:773–778.
14. United States Environmental Protection Agency (US EPA) (2007) SW-846,
Method 7471B, Mercury in Solid or Semisolid Waste (Manual Cold Vapor
Technique). Washington, DC.
15. United States Environmental Protection Agency (US EPA) (1996) SW-846,
Method 3050B, Acid Digestion of Sediments, Sludges, and Soils. Washington,
DC.
16. Mackay D, Shiu W-Y, Ma KC (1997) Illustrated handbook of physical-chemical
properties and environmental fate for organic chemicals: Pesticide Chemicals.
CRC press Boca Raton, FL, USA.
17. Friend M, Franson CJ (1999) Field manual of wildlife disease: general field guide
procedures and disease of birds. United States Geological Survey, Washington,
DC, pp.295–305.
18. Kendall RJ, Lacker TE, Bunck C, Daniel B, Driver C, et al. (1996) An ecological
risk assessment of lead shot exposure in non-waterfowl avian species: Upland
game birds and raptors. Environ Toxicol Chem 15:4–20.
19. Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable
to predation? J Anim Ecol 61:681–692.
20. Cattadori IM, Haydon DT, Hudson PJ (2005) Parasites and climate synchronize
red grouse populations. Nature 433:737–741.
21. Erickson AB, Highby PR, Carlson CE (1949) Ruffed Grouse populations in
Minnesota in relation to blood and intestinal parasitism. J Wildl Manage
13:188–194.
22. McClure HE (1949) The eyeworm, Oxyspirura petrowi, in Nebraska pheasants.
J of Wildl Manage 13:304–307.
Factors Impacting Lesser Prairie Chickens
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... Oxyspirura petrowi has a broad host range and has been reported infecting birds in the order Passeriformes and Galliformes [2,[4][5][6]. Particularly, O. petrowi has been detected in high prevalences in northern bobwhites (Colinus virginianus) in western Texas [3], and lesser prairie chickens (Tympanuchus pallidicinctus) in southwestern Kansas [2,7]. Over the last century northern bobwhite and lesser prairie chicken populations have been going experiencing declines [8,9]. ...
... Over the last century northern bobwhite and lesser prairie chicken populations have been going experiencing declines [8,9]. The cause of these decline has been largely attributed to habitat loss, habitat fragmentation, and climatic variables [10][11][12] with the role of disease only recently being investigated [3,7]. ...
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Oxyspirura petrowi is a parasitic nematode that infects wild birds. This parasite has a broad host range, but has recently been reported in high prevalences from native Galliformes species in the United States. In order to better understand the impact O. petrowi has on wild bird populations, we developed a quantitative PCR protocol to detect infections in wild northern bobwhites (Colinus virginianus). We used paired fecal and cloacal swab samples from wild caught and experimentally infected northern bobwhites and matching fecal float data from experimentally infected birds to validate our assay. Overall we detected more positive birds from fecal samples than the paired cloacal swabs and there was strong agreement between the qPCR results from fecal samples and from fecal flotation (84%; κ = 0.69 [0.53–0.84 95% CI]). We also detected O. petrowi DNA in ten replicates of samples spiked with one O. petrowi egg. This qPCR assay is an effective assay to detect O. petrowi infections in wild birds. Our results suggest that fecal samples are the most appropriate sample for detecting infections; although, cloacal swabs can be useful for determining if O. petrowi is circulating in a population.
... 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. ...
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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.
... 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].
... As parasites can have significant influences on the conservation of threatened and endangered species (e.g., Dunham, Peper, Baxter, & Kendall, 2014;Godfrey, Moore, Nelson, & Bull, 2010;Thompson, Lymbery, & Smith, 2010), it is important to consider the role that parasite diversity can play in exacerbating or mitigating the impact of disease outbreaks in host populations. Additionally, there is a growing recognition regarding the significance of taking co-extinctions, such as that of parasites, into account when prioritizing conservation targets (Gómez & Nichols, 2013;Spencer & Zuk, 2016;Strona, 2015). ...
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