Spatial and temporal distributions of the spinose ear tick, Otobius megnini, within animal shelters at Fossil Rim Wildlife Center.
Otobius megnini have a monoxenous life cycle with four stages: 1) egg, 2) six-legged larva, 3) eight-legged nymph, and 4) eight-legged adult. Ticks developing in temperatures between 21-24[degrees]C typically have oviposition 6-12 d after dropping as nymphs from their hosts. The number of eggs, which are laid in the nesting grounds of potential hosts, can range from 398-1,187 depending on the weight of the female (Nava et al., 2008). Egg incubation ranges from 14-19 d in laboratory studies (Loomis, 1961) and 18-23 d in field studies (Herms, 1917). Once hatching occurs, larvae seek hosts for survival; unfed larvae have been found to survive in the laboratory up to 78 d (Wanchinga and Barker, 1986). Larvae feed on the host for 1-5 wk and then molt into the nymph stage. The majority of nymphs will feed between 2-4 mo (Loomis, 1961) but have been noted to feed up to 6 mo (Wanchinga and Barker, 1986). The nymph will feed until it is completely engorged, exit the ear canal, fall off the host, and seek cover for the last molt into the nonparasitic, eight-legged adult life stage (Hooker, 1908). Adults remain off the host, use stored reserves obtained during the nymph stage (Anonymous, 1991), and can survive up to 2 y (Mayberry, 2003). During this time, adults search for a mate and reproduce. The typical amount of time for O. megnini to complete its life cycle ranges from 62-118 d (Loomis, 1961).
Otobius megnini larvae are the infective stage to the host. Once larvae hatch from the egg, they actively sense information from their environment to detect the presence of a host (Parola and Raoult, 2001). Ticks have a specialized sensory structure, called Haller's organ, that detects the presence of carbon dioxide, temperature, and humidity (Klompen and Oliver, 1993). Haller's organ is a minute cavity at the terminal segment of the first pair of a tick's legs and is composed of a pit and a capsule that contain sensory setae with numerous chemoreceptors designed to target the carbon dioxide (C[O.sub.2]) of exhaling hosts (Klompen and Oliver 1993). Otobius megnini parasitizes domesticated animals, such as cattle, as well as native and exotic wildlife (Becklund, 1968) such as Addax nasomaculatus (addax), Oryx gazella (gemsbok), Tragelaphus angasii (nyala), Hippotragus niger (sable antelope), Giraffa camelopardalis (giraffe), and Equus quagga (zebras). A spinose ear tick has even been reported to parasitize humans (Bishopp and Trembley, 1945; Eads and Campos, 1984), although this is considered to be a rare occurrence.
Otobius megnini is not known to be a vector for disease. However, a study has shown this tick to be infected with Coxiella burnetii, which can cause Q fever (Jellison et al., 1948). Severe irritation in the host can occur due to the tick attaching deep within the internal part of the ear. The irritation to the host promotes scratching that leads to lacerations that may be prone to secondary infections. Ear tick infestations can result in reduced body weight, reduced milk production, and overall lack of vitality (Parish, 1949) or, in some extreme cases, disfigurement or death of the host (Bishopp and Trembley, 1945). These negative effects of tick infestation are a concern for captive breeding programs trying to manage indigenous and exotic species, particularly those focusing on endangered and threatened species.
The ultimate goal of this project was to improve the quality of life for indigenous and exotic animals at Fossil Rim Wildlife Center (FRWC) by better understanding spatial and temporal variation in the abundance of O. megnini. The objectives of this study were to determine the temporal distribution of spinose ear tick abundance within animal shelters, examine the spatial dispersion of adult and larval ticks within animal shelters, and examine the effects of climatic variables on tick abundance. A limited amount of data exists on microhabitat preferences within animal shelters at Fossil Rim WC and patterns of tick abundance; therefore, this research represents a contribution to the scientific literature by examining temporal trends in tick abundance, identifying where these ticks are mostly likely to be found within animal shelters, and determining which environmental factors are most associated with tick abundance.
MATERIALS AND METHODS--Our study location was at the Fossil Rim Wildlife Center, located near Glen Rose, Texas. Fossil Rim WC is a not-for-profit, Association of Zoos & Aquariums-accredited facility specializing in captive breeding programs for indigenous and exotic endangered and threatened species of animals (http://www.fossilrim.org). The Fossil Rim WC is approximately 688 ha and supports over 1,000 animals consisting of 50 native and nonnative species. This study was conducted within the main pasture at Fossil Rim WC, which is approximately 172 ha and is occupied by a variety of ungulates species. These include the addax (A. nasomaculatus), sable antelope (H. niger), gemsbok (O. gazelle), fallow deer (D. dama), and white-tailed deer (O. virginianus). The main pasture contains a total of 11 shelters from which we selected two of similar size and construction (shelter three = 117 [m.sup.2]; shelter four = 126 [m.sup.2]) to include in this study. The shelter numbers described in this study were kept consistent with the numbering scheme assigned to Fossil Rim WC. We subdivided each shelter into quadrats (1m x 1 m) for sampling purposes. Quadrats were grouped according to those along the wall, those in the middle of the shelter, and those located along the outer edge of the shelter to characterize the spatial variation within an animal shelter. We randomly sampled four quadrats within each area of a shelter, resulting in a total of 12 quadrats per animal shelter. Both shelters were sampled biweekly from August 2012-July 2013 to characterize temporal variation in distribution and abundance of larval and adult spinose ear ticks.
Because larvae represent the host-seeking stage of O. megnini, they are attracted to C[O.sub.2] as it provides a proximate cue that a host is in the area. We therefore used a modified version of the compressed C[O.sub.2] trap developed by Niebuhr et al. (2013) to capture the larval ticks. The trap consisted of a 2.27-kg compressed C[O.sub.2] tank with a flow regulator coupled to a network of vinyl tubing with an inside diameter of 0.64 cm. The tubing was split at three points along the main lines to achieve a total of 12 tubes that were placed separately into the 12 sampling quadrats; hose clamps were used to secure tubing at each split. A 22-ga dissecting needle was used to puncture holes 0.2 m from the end of each tube. The open end of the tubing was sealed with a 0.64-cm-diameter eyebolt to prevent leakage. Metal frames (0.3 m x 0.3 m) covered in white cotton cloth were placed over the holes on each tube. For each sampling period, C[O.sub.2] was released at a rate of 10 psi for 30 min. After 30 min, larvae were harvested from the frames using an aspirator and stored in vials containing 70% ethanol to be counted at a later time in the laboratory using a dissecting scope.
Adult ticks, which represent a nonfeeding stage, are not attracted to the C[O.sub.2] released by a potential host and, therefore, were sampled differently than the larvae. To collect adults at each quadrat, we used an uncovered metal frame (0.3 m x 0.3 m) to delineate the space where ground litter was collected. All of the litter located within the sampling frame was placed into plastic bags for laboratory analysis. These sealed bags were sifted through a series of three screens to reduce the final amount of litter that needed to be searched to locate adults. The screens are sized in such a way that the adults passed through the first and second screen but did not pass through the third screen (1st screen = 1.27 [cm.sup.2], 2nd screen = 0.64 [cm.sup.2], 3rd screen = 0.32 [cm.sup.2]). The third screen was then exposed to a black light for approximately 20 min; the black light exposes the fluorescing legs of the adults to help aid in detection.
[FIGURE 1 OMITTED]
The environmental data collected included temperature and relative humidity. A Kestrel[R] 3,000 handheld weather station (Kestrel Meters, Birmingham, Michigan) was used to gather temperature and relative humidity data once per shelter during each sampling period; both temperature and relative humidity were recorded at ground level in the middle of the shelter. We used SPSS software (https://www-01.ibm.com/software/ analytics/spss/) to generate sequence charts for adult and larval tick abundances within each animal shelter (dependent variables) as well as for each of the two environmental factors (independent variables). An analysis of covariance was used to statistically compare the abundance of larval and adult ticks between the two animal shelters; time was used as a covariate. We quantified the degree of dispersion within each shelter using Morisita's index (Morisita, 1971), which characterizes the spatial distribution as being consistent with aggregated, uniform, or random patterns. We also used an analysis of covariance to determine whether quadrats along the wall, those in the middle of the shelter, or those located along the outer edge of the shelter contained the most individuals; time was used as a covariate. Linear regression was used to predict the abundance of ticks as a function of environmental conditions.
Results--The abundance of O. megnini varied over time with multiple peaks in spring, summer, and fall months; ticks were collected during winter months but in low abundances (Fig. 1). Adult abundances were considerably lower than larval abundances but both exhibited seasonal peaks in abundance. Overall, there was neither a net decrease nor a net increase in abundance over time for both larval (F = 0.299; df = 1, 68; P = 0.586) and adult ticks (F = 1.764; df = 1, 68; P = 0.189). There was no difference in larval tick abundance between the two shelters (F = 0.687; df = 1, 45; P = 0.412) as well as no difference in adult abundance between the two shelters (F = 2.628; df = 1, 45; P = 0.112).
Because there was no difference in temperature (F = 0.445; df = 1, 45; P = 0.508) and relative humidity (F = 0.505; df = 1, 45; P = 0.481) between the two shelters over time, we used the mean between the two shelters as estimates of environmental conditions. Mean larval tick abundance was significantly correlated with mean temperature (r = 0.408; P = 0.048; Fig. 2) but not significantly correlated with mean relative humidity (r = 0.130; P = 0.544; Fig. 3). Mean adult tick abundance was not significantly correlated with mean temperature (r = 0.202; P = 0.343; Fig. 2) but was significantly correlated with mean relative humidity (r = 0.443; P = 0.030; Fig. 3).
Larval tick collection numbers were highest in quadrats located in the sampling area directly against the shelter wall (F = 5.319; df = 2, 68; P = 0.007). There was no difference found in adult tick abundance among the three areas of the shelter (F = 0.773; df = 2, 68; P = 0.466). Larval ticks demonstrated the following overall spatial patterns for shelter three: aggregated = 80%, uniform = 20%, random = 0%; shelter four: aggregated = 74%, uniform = 17%, random = 9%. Adult ticks demonstrated the following spatial patterns for shelter three: aggregated = 61%, uniform = 33%, random = 6%; shelter four: aggregated = 8%, uniform = 50%, and random = 42%. Degree of aggregation was found to be positively correlated with abundance in both the larval (r = 0.815; P < 0.001; Fig. 4a) and adult (r = 0.726; P < 0.001; Fig. 4b) samples.
[FIGURE 2 OMITTED]
DISCUSSION--Temporal Trends in Abundance--The abundance of O. megnini varied over time with multiple peaks throughout the seasons. There was no overall trend in abundance across the year-long study, coinciding with other studies examining temporal trends in abundance of O. megnini (Dreyer et al., 1998; Nava et al., 2008). Nava et al. (2008) found seasonal peaks in abundance, but the timing of the peaks differed from year to year, with highest larval abundance occurring in April-May and August-October consecutively. Dreyer et al. (1998) found similar nymph abundance data as compared to adult abundance in our study, which showed no distinct trend over time. Neither of these studies reported environmental conditions, specifically temperature or relative humidity, which could help explain the variability in seasonal peaks. Otobius megnini exhibit endophilic behavior during nonparasitic stages in that they burrow into the ground, rocks, nest of host, etc. in an effort to avoid unfavorable environmental conditions (Estrada-Pena et al., 2010). Understanding the link between the environment and the behavior of this species is important when trying to identify temporal distributions. Previous studies demonstrated that various life stages may be differentially affected by environmental conditions such that peaks in abundance of different life stages occur during different seasons (Ostfeld et al., 1996).
[FIGURE 3 OMITTED]
[FIGURE 4 OMITTED]
Environmental Conditions--Larval tick abundances were positively correlated with temperature; no significant relationship existed for relative humidity. Egg hatchment has been found to be linked to temperature, with ovipositon occurring between 20-30[degrees]C (Loomis, 1961; Sweatman, 1967; Wanchinga and Barker, 1986). Abundance of larvae in our study started to increase in March as temperatures approached 20[degrees]C and was highest at 26[degrees]C, supporting previous findings of egg hatchment. Another study measured the effects of temperature and relative humidity on questing of larval ticks and found that temperature affected distance traveled and amount of time spent questing but that relative humidity had no effect (Vail and Smith, 2002). Adult female ticks secrete a wax covering over their eggs to protect them from desiccation in dry habitats (Booth, 1989). Resistance of eggs to fluctuating relative humidity, along with abundance patterns of larvae, supports our findings of no significant relationship being found between larval abundance and relative humidity.
However, adult tick abundances were positively correlated with relative humidity. The differential effects of environmental variables on abundance of varying life stages suggest biological differences in body structure or function between larvae and adults. Previous studies indicate that older life stages have higher humidity requirements than do the younger life stages (Hafez et al., 1970; Rodgers et al., 2007). As ticks feed and molt into later life stages, their cuticle thins as body size increases (Hackman, 1975). As a nymph, no additional wax is added to the cuticle to account for the increased body size until after molting into an adult (Yoder et al., 1997). Also in this stage, water is lost to allow for increased blood consumption from the host (Needham and Teal, 1991). This would suggest that because of the nymph's sensitivity to moisture they would be prone to fluctuations in humidity, resulting in adult abundances that are correlated with relative humidity values.
Spatial Distribution--The spatial dispersion of larval ticks was aggregated for the majority of the samples collected. An aggregated distribution was found during periods of higher larval abundance whereas a uniform distribution was found in samples of lower larval abundances. The behavior of newly hatched larvae remaining near the egg clutch and demonstrating an ambush strategy for host attachment can result in an aggregated distribution (Stafford, 1992). Previous work has documented a relationship demonstrating that the degree of aggregation is higher in larval stages with higher densities and decreases over time as the density decreases due to the dispersion of the ticks by the hosts (Ostfeld et al., 1996). We observed a higher degree of aggregation in the larval stage than in the adult form, supporting the idea that there is a higher degree of aggregation in earlier life stages and that the degree of aggregation decreases over time (Daniels and Fish, 1990). As nymphs fall off-host to molt into adults, the spatial pattern could appear aggregated due to synchronous detachment of nymphs (Oliver, 1989; Ostfeld et al., 1996). Highest larval abundance was found in the sampling area located directly against the wall while adult abundances did not differ statistically among the three areas of the animal shelter.
Management--Direct application of acaricides into the ears of hosts has been shown to reduce O. megnini abundances on-host (Drummond et al., 1967; Mayberry, 2003) while other methods such as application of systemic biocides have not been shown to reduce tick abundance (Nava and Guglielmone, 2009). Direct application into the ears can be costly and time consuming, as frequent reapplication is necessary due to continuous infestation of ticks. in addition, this method may be impractical in wildlife facilities, such as Fossil Rim WC, that adopt more of a hands-off approach in their management strategies to mimic natural processes as much as possible. Based on results from this study, we suggest that effective management strategies should target specific microhabitats heavily used by ticks while off-host. Within the shelters, our results suggest control efforts should be concentrated along the walls where larvae abundance was significantly higher than other areas. Not only does this decrease the amount of interaction with the host, but it also focuses eradication efforts where tick populations tend to be concentrated.
In addition to the application of acaricides to the outer edge of animal shelters, the complete removal of animal bedding in early spring could reduce tick populations by reducing suitable tick habitat. Replacement of bedding should not occur until immediately before the first winter freeze. Of course, the timing of this particular control method is key to its success. This management strategy could especially be useful to wildlife areas that need ways to control parasites off-host, minimizing interactions with threatened and endangered wildlife. By better understanding spatial and temporal dynamics of tick abundance, as well as the environmental drivers of those dynamics, we can implement more-effective and less-invasive management strategies.
We would like to thank C. J. Vavra, S. L. Musick, A. C. Ford Jones, P. J. Steerle III, B. W. Kubecka, and A. L. Kimmel for their assistance in field and laboratory studies. We would also like to recognize Tarleton State University for providing financial support through an Organized Research Grant. Special appreciation is extended to Fossil Rim Wildlife Center for their enthusiasm, time, and support of this research.
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Submitted 20 February 2014.
Acceptance recommended by Jerry L. Cook, 25 February 2015.
Callie J. Price, * David H. Kattes, Kristin K. Herrmann, and Christopher L. Higgins
Department of Biological Sciences, Box T-0100, Tarleton State University, Stephenville, TX 76402 (CJP, KKH, CLH)
Department of Wildlife, Sustainability, and Ecosystem Sciences, Box T-0050, Tarleton State University, Stephenville, TX 76402 (DHK)
* Correspondent: firstname.lastname@example.org
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|Author:||Price, Callie J.; Kattes, David H.; Herrmann, Kristin K.; Higgins, Christopher L.|
|Date:||Jun 1, 2015|
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