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A Helminth Survey of Northern Bobwhite Quail (Colinus virginianus) and Passerines in the Rolling Plains Ecoregion of Texas

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Abstract

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.
A Helminth Survey of Northern Bobwhite Quail (Colinus
virginianus) and Passerines in the Rolling Plains
Ecoregion of Texas
Authors: Herzog, Jessica L., Lukashow-Moore, Shannon P., Brym,
Matthew Z., Kalyanasundaram, Aravindan, and Kendall, Ronald J.
Source: Journal of Parasitology, 107(1) : 132-137
Published By: American Society of Parasitologists
URL: https://doi.org/10.1645/20-137
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Published 26 February 2021
DOI: 10.1645/20-137
Contents and archives available through www.bioone.org or www.jstor.org
Journal of Parasitology
journal homepage: www.journalofparasitology.org
A HELMINTH SURVEY OF NORTHERN BOBWHITE QUAIL (COLINUS VIRGINIANUS) AND
PASSERINES IN THE ROLLING PLAINS ECOREGION OF TEXAS
Jessica L. Herzog, Shannon P. Lukashow-Moore, Matthew Z. Brym, Aravindan Kalyanasundaram, and Ronald J. Kendall
The Wildlife Toxicology Laboratory, Texas Tech University, Box 43290, Lubbock, Texas 79409-3290.
Correspondence should be sent to Ronald J. Kendall at: ron.kendall@ttu.edu
KEY WORDS ABSTRACT
Passerines
Northern bobwhite
Colinus virginianus
Eyeworms
Oxyspirura petrowi
Rolling Plains
Helminth survey
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.
Over the past several decades, parasites have become increas-
ingly recognized as a potential threat to both wild and domestic
animals (Tompkins et al., 2011; Friend, 2014). Wild avian species,
in particular, may be more susceptible to the effects of parasites,
as the communal behavior and high vagility of many birds could
facilitate both the intensity and spread of infection. Notable
examples of parasites impacting birds include Trichomonas
gallinae,Plasmodium relictum, and Trichostrongylus tenuis, and
these have been associated with declines of greenfinch (Carduelis
chloris) and chaffinch (Fringilla coelebs) (Robinson et al., 2010),
house sparrow (Passer domesticus) (Dadam et al., 2019), and red
grouse (Lagopus lagopus scoticus) (Dobson and Hudson, 1994),
respectively. While these are just a few examples of the numerous
parasite taxa that infect birds, a proliferation of research into this
diverse group is expanding our understanding of their potential
impacts. Helminths are 1 example of the increased interest in
avian parasites, as their potential to cause lethargy, weight loss,
pathology, and even death in their avian hosts has garnered the
attention of researchers (DeRosa and Shivaprasad, 1999;
Nagarajan et al., 2012).
In the Rolling Plains ecoregion of Texas, 2 helminths, the
eyeworm (Oxyspirura petrowi) and cecal worm (Aulonocephalus
pennula), have become increasingly recognized alongside the
many factors potentially contributing to the decline of Northern
bobwhite quail (Colinus virginianus; hereafter ‘‘bobwhite’’) (Vil-
larreal et al., 2012; Bruno et al., 2015; Brym et al., 2018; Henry et
al., 2020), an iconic game bird of substantial economic value to
rural communities in the region (Johnson et al., 2012). Since the
1960s, populations of bobwhite in the Texas Rolling Plains are
documented to have declined at an annual rate of approximately
4% (Sauer et al., 2013), despite regional land-use practices (e.g.,
ranching) which are often conducive toward and include quail
habitat management (Rollins, 2007; Herna
´ndez and Guthery,
2012). This continued decline of bobwhite contributed to the 2010
launch of Operation Idiopathic Decline (OID), a 3-yr collabora-
tive research initiative that examined multiple factors affecting
quail abundance in the Rolling Plains of Texas and Oklahoma.
Journal of Parasitology 2021 107(1) 132–137
ÓAmerican Society of Parasitologists 2021
132
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Because of this effort, helminths were identified as highly
prevalent in bobwhite from the Rolling Plains, with cecal worms
being found in 91% of specimens and eyeworms in 66% (Bruno et
al., 2019).
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 (Kubec
ˇka et al., 2017) and
where cecal worms are consistently reported in 100% of sampled
individuals (Henry et al., 2017; Brym et al., 2018). 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). Contem-
porary 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.
For instance, while much effort has been invested in surveys of
parasites in bobwhite from the Rolling Plains, similar surveys of
sympatric passerines are lacking, despite some of these birds also
being known as hosts to various helminths, including eyeworms
(Pence, 1972; Dunham and Kendall, 2014). This is a potentially
significant oversight since (if passerines are competent hosts of
bobwhite parasites) there is the potential of an interaction in
which bobwhite infection is facilitated and/or exacerbated and
vice versa. Unfortunately, these possibilities remain largely
unexplored due to the lack of comprehensive study into the
helminth communities of passerines in the Rolling Plains.
This possibility of interactions between eyeworm infection in
bobwhite and passerines was considered by Dunham and Kendall
(2014), leading to the opportunistic sampling of passerines during
helminth surveys of bobwhite. Currently, most of the available
data into helminth infection in passerines from the Rolling Plains
is limited to this early work, in which a small number of curve-
billed thrashers (Toxistoma curvirostre), and Northern mocking-
birds (Mimus polyglottos) were sampled (Dunham and Kendall,
2014). Furthermore, only 2 additional helminth surveys were
conducted for Northern cardinals (Cardinalis cardinalis) (Quentin
and Barre, 1976; Rickard, 1985) after cardinals were found to be
eyeworm hosts, while only 1 additional survey exists for Northern
mockingbirds (Evans, 2002). Each of these additional surveys was
conducted outside of Texas, did not entail a comprehensive
assessment of helminth fauna within the host, and used data
obtained from incidentally caught specimens. As such, these
studies likely underrepresent the extent of helminth parasites and
potential range of hosts within passerines and are not represen-
tative of the helminth communities in birds from the Texas
Rolling Plains.
To address the lack of knowledge on helminth communities in
passerines and shared infection between bobwhite and passerines
in the Rolling Plains ecoregion of Texas, we expanded upon
surveys of helminths in bobwhite that have been ongoing since
2013 (Dunham et al., 2014) to include several species of passerines
as well. Examinations for parasites were also extended to include
the eyes, digestive and respiratory tracts, endocrine system, and
muscle tissues to provide a more complete account of potential
helminth infection within hosts. Here we discuss the prevalence of
helminths in bobwhite, scaled quail, and several passerines from
the Rolling Plains ecoregion of Texas, as well as how shared
helminth infection among the different bird species may have
significant effects on infections and parasite–host interactions.
MATERIALS AND METHODS
Study area and sample collection
Sample collection occurred from March to October 2019 in the
Rolling Plains ecoregion of West Texas. The Rolling Plains is a
mesquite-shortgrass savannah dominated by honey mesquite
(Prosopis glandulosa) and juniper (Juniperus pinchotti) (Rollins,
2007). Bobwhite, scaled quail, Northern cardinal, Northern
mockingbird, and curve-billed thrasher were trapped in walk-in
double funnel traps at Matador Wildlife Management Area in
Cottle County (34870300
N, 10082004100
W) and private ranches in
Mitchell (348704500
N, 1008590600
W) and Garza (33812 03200
N,
10181502500
W) counties using methods described by Dunham et
al. (2014). Sunflower (Helianthus annuus) seeds were used as
additional bait in all traps in an attempt to make them more
appealing to the aforementioned passerines. Additionally, extra
traps modified with constricted funnels were deployed in areas
where these passerines were observed in order to increase the
likelihood of capture, since these birds sometimes escape the
wider funnels used in quail traps. A landowner donated another 4
bobwhite from Stonewall County (338110N, 1008150W) 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 20 C, and transported to
TIEHH for processing.
Necropsy and helminth collection
Necropsies for helminth collection were performed immediately
after euthanasia of live-caught birds or after donated birds had
thawed completely. The eyes and ocular tissues, intestines, ceca,
stomach, liver, gonads, kidneys, heart, lungs, crop, trachea, and
major and minor right pectoralis were removed and examined for
helminths. Because of the time required to perform a complete
necropsy, any tissues not immediately examined for parasites were
stored in 70% ethanol to prevent deterioration. 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. Any helminths found were counted and
HERZOG ET AL.—A HELMINTH SURVEY OF NORTHERN BOBWHITE QUAIL 133
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stored in 70% ethanol at room temperature until processed.
However, Raillietina spp. and Mesocestoides spp. tetrathyridia
were not counted due to high infections and scolex deterioration,
which is a common problem encountered in surveys of these
parasites (Dancak et al., 1982; Villarreal, 2012; Olsen, 2014).
Helminth processing and identification
Acanthocephalans and cestodes were chemically treated as
described by Sepulveda and Kinsella (2013). Representative
helminths were either temporarily wet mounted in 20% lacto-
phenol (cestodes and nematodes) or stained with Semichon’s
Aceto-Acid Carmine, dehydrated in a series of concentrations of
ethanol, and permanently mounted in Damar Balsam mountant
on a microscope slide (cestodes and acanthocephalans) (Sepulve-
da and Kinsella, 2013; Olsen, 2014). Mounted helminths were
identified based on morphological characteristics using an
Olympus BX 50 microscope. Eyeworm identification was based
on characteristics for O. petrowi described by Pence (1972), and
characteristics reported by Chandler (1935) and Inglis (1958) were
used to distinguish cecal worms. The identity of eyeworms
recovered from passerines was also confirmed by PCR and
sequencing using ITS2 primers for O. petrowi as outlined by
Kistler et al. (2016). Physaloptera spp. were identified according
to descriptions from Dixon and Roberson (1967), Boggs et al.
(1990), Taton-Allen and Cheney (2001), Gonza
´lez and Hamann
(2012), and Mohamadain and Ammar (2012). Any other
helminths were identified using published keys from Khalil et al.
(1994) and Anderson et al. (2009), as well as reference slides from
the Museum of Texas Tech University. Helminths that could not
be identified were sent to Texas Veterinary Medical Diagnostics
Laboratory (College Station, Texas) and Dr. Mike Kinsella
(Ph.D., Missoula, Montana) for identification.
RESULTS
Of the 54 birds sampled, 51 (94.4%) were infected with
helminths, and a total of 5,459 helminths representing at least 10
species were recovered (Table I). Bobwhite harbored the highest
parasite diversity of all the birds sampled, with 9 of the 10
helminth species being found in bobwhite. Overall, eyeworms
were the most prevalent helminths encountered, with 85.3% of
bobwhite, 50% of scaled quail, 42.9% of Northern cardinals,
85.7% of Northern mockingbirds, and 100% of curve-billed
thrashers surveyed being infected. All eyeworms recovered
conformed to characteristics for O. petrowi described by Pence
(1972), and specimens from all passerine species tested positive for
O. petrowi ITS2 specific primers, with gravid eyeworms being
found in a Northern cardinal (Fig. 1). Cecal worms were also
commonly found, and these parasites had the highest intensities
of all helminths in our sample. However, cecal worm infections
were limited to bobwhite and scaled quail, in which the prevalence
of cecal worms was 100% for both species, with infection intensity
ranging from 1 to 336 and 60 to 162, respectively. The prevalence
of all other helminth species, excluding eyeworms and cecal
worms, was considerably lower, with Tetrameres sp., as well as
unidentified nematodes and acanthocephalans, being unique to
the passerines in the sample. Infection with multiple species of
helminths was also noted, with 34 of 54 (63.0%) birds having
coinfections. The majority of coinfections (20 of 34, 58.8%) were
eyeworms and cecal worms, and most of these (19 of 20) occurred
in bobwhite. All coinfections in this sample involved either the
eyeworm, cecal worm, or both.
DISCUSSION
This study contributes data to the very limited helminth surveys
of passerines that have been conducted in Texas thus far. To our
knowledge, this is only the second study to report Mesocestoides
in North American bobwhite (Kubec
ˇka et al., 2018), as well as the
first report of any acanthocephalan species in Northern mock-
ingbirds. We also documented considerable prevalence (42.9%)
of eyeworms in all of the bird species examined, which was
consistent with a previous survey that reported eyeworms in all
Northern mockingbirds and curve-billed thrashers sampled
(Dunham and Kendall, 2014). While the number of passerines
examined in this study is limited, our findings of highly prevalent
eyeworm infections in passerines suggest that shared infection
Table I. Prevalence and range of infection of helminths in sampled avian species. NI¼the number infected, % ¼percent infected, R ¼range of infection.
Helminth
Northern
bobwhite quail
(n ¼34)
Scaled quail
(n ¼2)
Northern cardinal
(n ¼7)
Northern
mockingbird
(n ¼7)
Curve-billed
thrasher
(n ¼4)
Total
(n ¼54)
NI % R NI % R NI % R NI % R NI % R NI %
Aulonocephalus pennula 34 100 1–336 2 100 60–162 0 0 0 0 0 0 0 0 0 36 66.7
Oxyspirura petrowi 29 85.3 0–40 1 50 0–7 3 42.9 0–8 6 85.7 0–6 4 100 1–5 43 79.6
Physaloptera sp. 4 11.8 0–5 0 0 0 0 0 0 0 0 0 0 0 0 4 7.4
Subulura brumpti 1 2.9 0–1 0 0 0 0 0 0 0 0 0 0 0 0 1 1.9
Tetrameres pattersoni 2 5.9 0–2 0 0 0 0 0 0 0 0 0 0 0 0 2 3.7
Tetrameres sp. 0 0 0 0 0 0 1 14.3 0–3 0 0 0 0 0 0 1 1.9
Unidentified nematodes* 0 0 0 0 0 0 0 0 0 0 0 0 1 25 0–1 1 1.9
Raillietina sp. 4 11.8 N/A 0 0 0 0 0 0 0 0 0 0 0 0 4 7.4
Mesocestoides sp. tetrathyridium 1 2.9 N/A 0 0 0 0 0 0 0 0 0 0 0 0 1 1.9
Mesocestoides canislagopodis 2 5.9 0–2 0 0 0 0 0 0 0 0 0 0 0 0 2 3.7
Oncicola canis 1 2.9 0–3 0 0 0 0 0 0 0 0 0 0 0 0 1 1.9
Unidentified acanthocephalans* 0 0 0 0 0 0 0 0 0 1 14.3 0–1 1 25 0–4 2 3.7
* The features necessary for identification of these samples were damaged during processing, rendering these specimens unidentifiable.
134 THE JOURNAL OF PARASITOLOGY, VOL. 107, NO. 1, FEBRUARY 2021
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between bobwhite and passerines may be a common occurrence in
the Rolling Plains ecoregion of Texas. Additionally, our
observation of gravid eyeworms in Northern cardinal (Fig. 1)
supports the possibility that passerines may serve as competent
hosts of O. petrowi, which may have important implications
regarding the transmission dynamics of this parasite.
Shared eyeworm infection in bobwhite and passerines is likely
due to the birds’ diets incorporating the insect intermediate hosts
of this parasite, especially during breeding season when the
increased protein demands of egg-laying and chick-rearing must
be met (Fischer, 1981; Brennan, 1999). Because insect intermedi-
ate hosts are used by various helminth taxa (Rausch, 1983), the
possibilities of shared host–helminth associations between quail
and passerines may also span the cestode, nematode, acantho-
cephalan, and trematode groups (Sepulveda and Kinsella, 2013).
The sample presented herein illustrates this possibility, since at
least 10 helminth species representing nematodes, cestodes, and
acanthocephalans were recovered from birds collected in the
Texas Rolling Plains. However, our sample is insufficient to
reliably determine overall helminth communities and instances of
shared parasites because it is small (n ¼54), consists predom-
inantly of quail (n ¼36), and includes relatively few Northern
cardinals (n ¼7), Northern mockingbirds (n ¼7), and curve-billed
thrashers (n ¼4). This discrepancy between quail and passerines
in our sample is likely due to our trapping techniques being biased
toward the collection of quail. Supplementing surveys of helminth
communities in quail from the Rolling Plains with those more
specialized for the collection of passerines (e.g., mist netting) are
thus strongly encouraged, since these would provide a more
representative assessment of the helminth communities and
instances of shared infection in the region. Nevertheless, this
study is among the first preliminary assessments of avian helminth
communities in the Texas Rolling Plains and thus provides a
useful baseline for future research.
Our findings of shared eyeworm infection between bobwhite
and passerines, coupled with an instance of gravid eyeworms in
one of these passerines, also emphasize the need to consider the
potential role of shared infections in the transmission dynamics of
this parasite. For instance, bobwhite populations in the Rolling
Plains typically fluctuate between periods of abundance and
scarcity (boom and bust) (Lusk et al., 2007), and passerines may
maintain the life cycle of eyeworms when bobwhite populations
are low by serving as competent hosts for these parasites.
Passerines may be especially well suited to the role of maintaining
the eyeworm life cycle, since their longer lifespans and compar-
atively lower eyeworm intensities, relative to bobwhite, may lead
to less pathology and allow eyeworms to persist for longer in the
environment. Furthermore, because passerines are typically more
vagile than bobwhite, they may transmit eyeworms across a larger
area,andthiscouldleadtoinfectionofnaı
¨ve bobwhite
populations or reinfection of populations in which the eyeworm
life cycle has been broken. Alternatively, quail may harbor
helminths that use passerines as definitive hosts, and during years
of plentiful quail populations, the incidence and intensity of these
infections in passerines may likewise increase due to an
amplification effect from quail.
While hypothetical, the aforementioned examples of potential
consequences of shared helminth infection between bobwhite and
passerines illustrate the potential significance of this interaction.
Unfortunately, the lack of research into this topic hinders our
Figure 1. Gravid Oxyspirura petrowi recovered from a Northern
cardinal (Cardinalis cardinalis) in Mitchell County, Texas.
HERZOG ET AL.—A HELMINTH SURVEY OF NORTHERN BOBWHITE QUAIL 135
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understanding of the potential consequences of these infections
and how they may affect populations of both bobwhite and
passerines within the Rolling Plains. Expanding upon the research
of helminth communities and shared infection of birds in the
Rolling Plains through comprehensive surveys may thus provide
greater insight into the interactions within these systems and lead
to a better understanding of the effect of helminths on avian
populations.
ACKNOWLEDGMENTS
This study was approved by Texas Tech University Animal
Care and Use Committee under protocols 16071-08 and 19015-02.
All birds were trapped and handled according to Texas Parks and
Wildlife permit SRP-0715-095, United States Fish and Wildlife
Permits MB88764B-0 and MB88764B-1, and Federal Bird
Banding Permit 22590. Funding for this project was provided
by Park Cities Quail Coalition, the Texas Tech University
Graduate School, Lubbock, Texas, and the AFO-WOS Travel
Award Committee and AFO-WOS Student Travel Grant
Committee, Cape May, New Jersey. The authors would like to
thank those at Dalby, Morrison, Ribelin, and Spade Ranches, as
well as the staff of the Matador Wildlife Management Area for
their hospitality and support of this work. We would also like to
express our gratitude to Caroline Ellison, Heath Garner, Joe
Luksovsky, Dr. Mike Kinsella, and members of the Wildlife
Toxicology Laboratory for their contributions and assistance.
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... Quail chicks also consume fire ants, but this reduces quail survival and weight gain (Myers et al. 2014). Numerous species of ectoparasites have been collected from bobwhite quail, but none appear to cause significant impacts on quail population levels (Bergstrand and Klimstra 1964, Doster et al. 1980, Teel et al. 1998, Herzog 2020. ...
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