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2018 SOUTHEASTERN NATURALIST 17(4):554–559
Host Specificity of Oxyspirura petrowi in Wild Turkey
Bradley W. Kubečka1,*, Andrea Bruno1, and Dale Rollins1
Abstract - The Rolling Plains ecoregion of Texas hosts the highest known prevalence and
intensity of the eyeworm Oxyspirura petrowi among Colinus virginianus (Northern Bobwhite)
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.
Introduction
Host specificity is defined as the number of host species that are used by a
parasite population (Poulin et al. 2011). High host specificity is demonstrated in
parasites utilizing a single or few host(s) to complete a life cycle, whereas low
host-specificity is described as a parasite infecting multiple definitive hosts. Collectively,
host diversity and parasite specificity dictate whether a parasite can persist
when a host becomes locally extirpated or scarce, and whether a parasite has the
potential to colonize new areas (Lafferty 2012, Poulin et al. 2011). Therefore, understanding
the susceptibility of various host species to a parasite offers insight into
the life cycles and extinction risks of parasites themselves (S trona 2015).
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. 2014, 2016a, 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). Wild Turkeys and Bobwhites have similar diets (i.e., facultative
insectivores), overlapping ranges, and phylogenetic relatedness (i.e.,
Galliformes); thus, we expected Wild Turkeys sympatric with an infected population
of Bobwhites would also host eyeworms.
1Rolling Plains Quail Research Foundation, Roby, TX 79543. *Corresponding author -
bkubecka@talltimbers.org.
Manuscript Editor: Roger Applegate
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Field-site Description
This study was conducted on a 27,530-ha area in Roberts County, TX (35°56'1''N,
100°52'33''W) where Bobwhites and Wild Turkeys inhabit similar vegetation communities
(Guthery et al. 2005). Annual precipitation averages 590 mm and the area
is characterized by a native plant community of Andropogon hallii Hack. (Sand
Bluestem), Schizachyrium scoparium Michx. (Little Bluestem), Panicum virgatum
L. (Switchgrass), Artemsia filifolia Torr. (Sand Sagebrush), Prunus angustifolia
Marsh. (Sand Plum), and Rhus trilobata Nutt. (Skunkbush Sumac) (NRCS 2017,
US Climate Data 2017).
Methods
We solicited hunter-donated Bobwhites (n = 50) during October 2014–February
2015. We opportunistically solicited Wild Turkey heads (n = 104) from hunters and
researchers conducting a study of Wild Turkey diets in the area during April–July
2014. Researchers flash-froze Wild Turkey heads immediately upon harvest using
ethyl alcohol and dry ice to mitigate the possibility of eyeworms migrating from
the orbital cavity. For convenience of quail hunters and lack of research personnel
on site during hunts, hunter-harvested Bobwhite samples were not flash frozen but
conventionally frozen. We stored all heads frozen in individual, labeled, plastic
bags until dissection.
For both host species, we examined under the eyelids and nictitating membranes
before removing the eyes and examining the nasal-lacrimal sinuses, Harderian
glands, and lacrimal ducts (Bruno et al. 2015, Dunham et al. 2014). Although
eyeworms are apparent to the naked eye, we used a stereo zoom microscope (7X–
45X) and a 3-diopter (1.75X) magnifying lens with LED illumination to assure
detection. We compared host prevalence by sex using Fisher’s exact test (PROC
FREQ) and mean abundance and mean intensity with a Kruskal–Wallis test
(PROC NPAR1WAY) in SAS Studio (SAS Institute Inc., Cary, NC).
Parasitological terms presented herein adhere to definitions suggested by Bush
et al. (1997), where ‘‘prevalence’’ describes percent of infected individuals in a
sample; ‘‘mean abundance’’ describes average number of eyeworms among all
samples (i.e., infected and non-infected), and ‘‘mean intensity’’ describes the average
number of eyeworms within the subset of infected individuals. Descriptive
statistics herein are presented as the mean ± 1 standard error (SE).
Results
Twenty-nine of the 50 Bobwhites (58%) hosted eyeworms, with a mean abundance
of 7.6 ± 1.8 and mean intensity of 13.1 ± 2.7. Prevalence was similar between
male (n = 25, 64%) and female (n = 25, 52%) Bobwhites (P = 0.57). Mean
abundance was similar between males (8.8 ± 2.6) and females (6.4 ± 2.5; P = 0.53);
mean intensity between males (13.7 ± 3.5) and females (12.4 ± 4.3) did not differ
(P = 0.71). Only 1 of the 104 Wild Turkeys (female) hosted a single eyeworm.
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2018 Vol. 17, No. 4
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Discussion
We examined 104 Wild Turkeys (n = 63 females, 41 males) and 50 Bobwhites
(n = 25 females, 25 males) for eyeworms during 2014–2015. Age composition of
our Bobwhite sample was 32 juveniles, 3 adults, and 15 birds of unknown age. We
did not obtain specific ages for female Wild Turkeys, but all were after-hatch-year
(AHY) individuals. Male age composition included 15 juveniles (i.e., 1-y old), 18
adults (>1-y old), and 8 of unknown age. We were unable to evaluate the effect of
host age on eyeworm prevalence or abundance for either species, though eyeworm
prevalence and abundance in Bobwhites tends to be greater in adults than juveniles
(Bruno et al. 2018, Dunham et al. 2016a). Thus, given the large proportion of juveniles
in the sample, our estimate for mean abundance and intensity for Bobwhites
is likely a conservative one. No evidence currently exists for developed resistance
to eyeworm with host age. Rather, time-related accumulation seems to occur from
prolonged exposure to infective stages of eyeworm (Bruno et al. 2018, Dunham et
al. 2016a, Villareal et al. 2016).
Our Wild Turkey sample appears to be the first conclusive report of eyeworm
in Meleagris gallopavo ssp. intermedia Sennett (Rio Grande Wild Turkey). We deposited
the eyeworm voucher specimen from the Wild Turkey in the Sam Houston
State University Parasite Museum (SHSUP), Sam Houston State University, Huntsville,
TX (SHSUP 001599). Though eyeworms are not commonly reported to infect
Wild Turkeys, Addison and Prestwood (1978) documented prevalence of Oxyspirura
turcottei Addison in 8% of M. g. silvestris (Viellot) (Eastern Wild Turkey)
collected in West Virginia. Infections of O. petrowi are reported in a wide range
of galliforms, except for Wild Turkeys, in the Great Plains. For example, Robel et
al. (2003) documented 95% prevalence among Tympanuchus pallidicinctus (Ridgway)
(Lesser Prairie Chicken) in western Kansas. Likewise, Phasianus colchicus
(L.) (Ring-necked Pheasant) and Callipepla squamata (Vigors) (Scaled Quail) are
also susceptible hosts with prevalence of 39% and 72%, respectively (Bedford
2015, Dunham et al. 2017, McClure 1949). Pence (1972) recovered eyeworms
from 21 species of birds from across multiple taxonomic orders. In regards to host
specificity, Pence (1972:27) stated, “O. petrowi exhibits little host specificity and
is encountered primarily in birds found in open fields, submarginal grasslands, and
marsh lands. Its presence in a number of species of avian hosts representing several
families, but all occupying comparable ecological niches, indicates that host
specificity is not dependent on definitive host physiology. Rather, it is probably
dependent on the occurrence of the intermediate host(s) which is restricted to a
particular habitat.”
The overlapping diets and range of Bobwhite and Wild Turkeys from this study
suggest that intermediate hosts may not be the only limiting factor for O. petrowi
development. Wild Turkeys are opportunistic foragers with diets similar to Bobwhites
(Glover and Bailey 1949, Peterson 2007). A compositional analysis of
Wild Turkey diets from our sample revealed at least 74% of individual s consumed
arthropods across 9 taxonomic orders including: Araneae, Blatarria, Coleoptera,
Hemiptera, Homoptera, Hymenoptera, Lepidoptera, Mantodea, and Orthoptera
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(Rolling Plains Quail Research Ranch, Roby, TX , unpubl. data). It is likely that all
Wild Turkeys consumed arthropods during the study, but these estimates are a function
of sampling bias (i.e., crop, gizzard-content analysis). By documenting DNA
from O. petrowi in various species of cockroaches, crickets, and grasshoppers,
Almas et al. (2018) identified arthropods of these groups as potential intermediate
hosts. Successful in vitro infection of Bobwhites has been demonstrated using
Brachystola magna Girard, C. (Plains Lubber Grasshoppers; Kistler et al. 2016),
but their occurrence in Bobwhite diets has not been documented. However, Plains
Lubber Grasshoppers were noted in the diet of Wild Turkeys from our sample.
Nonetheless, we presume that Wild Turkeys in this study were consuming arthropods
infected with O. petrowi larvae.
Peak mean abundance of eyeworms for Bobwhites in the region occurs during
May–July, which coincided with our Wild Turkey collection period (Dunham et
al. 2017, Jackson and Green 1964). Thus, the probability of detecting infection of
O. petrowi in Wild Turkeys should have been the highest during our sampling period.
Further, our hunter-harvested sample (October–February) of Bobwhite likely
provides conservative estimates of Bobwhite infection. Anatomical differences,
i.e., greater distance and stronger physical gradient from crop to lacrimal ducts in
Wild Turkeys (~20 cm), may preclude immigration by eyeworm larvae. However,
Wild Turkey poults would not be subject to this limitation. As documented in various
mammals (Villalba et al. 2014), there is also a possibility that Wild Turkeys
have the ability to self-medicate by consuming natural anthelmintics from plants
not available to Bobwhite. For example, 9% of Wild Turkeys from our sample were
documented consuming Equisetum spp. (horsetails)—plants containing silica that
could serve as an anthelmintic (Wiewióra et al. 2015). However, this retroductive
hypothesis does not appear to ubiquitously explain lack of eyeworm documentation
in the literature, and the proportion of individuals consuming notable plants in this
study was low.
A survey of 35 sites across the Rolling Plains indicated that our study site
had one of the highest prevalence rates of eyeworms in Bobwhites during
2011–2013 (Bruno 2014, Dunham et al. 2016a). Our results are limited to 1 area
and 1 year, but we feel that the sample size was sufficient to document prevalence
of O. petrowi in Wild Turkeys. Coupled with the lack of documentation
in the literature, Wild Turkeys do not appear to be suitable hosts for O. petrowi.
Understanding why Wild Turkeys are rarely infected by O. petrowi, despite
numerous infections of other galliforms in the same region may help better understand
the life cycle of O. petrowi.
Acknowledgments
We acknowledge the Mesa Vista Ranch for their hospitality for accommodating this
study. Special thanks go to K. Boone and C. Goertz, who assisted in collection and preservation
of Wild Turkey specimens. We appreciate B. Ruzicka and multiple anonymous
reviewers for their helpful criticism in the development of this manuscript. This study
was funded with the help of the Rolling Plains Quail Research Foundation and Park Cities
Quail Coalition.
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