Spatial and temporal distributions of the Spinose Ear , megnini, within shelters at Fossil Rim Wildlife Center Author(s): Callie J. Price, David H. Kattes, Kristin K. Herrmann, and Christopher L. Higgins Source: The Southwestern Naturalist, 60(2-3):224-230. Published By: Southwestern Association of Naturalists DOI: http://dx.doi.org/10.1894/CUSTJC-81.1 URL: http://www.bioone.org/doi/full/10.1894/CUSTJC-81.1

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. THE SOUTHWESTERN NATURALIST 60(2-3): 224–230 JUNE-SEPTEMBER 2015

SPATIAL AND TEMPORAL DISTRIBUTIONS OF THE SPINOSE EAR TICK, , WITHIN ANIMAL SHELTERS AT FOSSIL RIM WILDLIFE CENTER

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: [email protected]

ABSTRACT—Spinose ear , Otobius megnini, are monoxenous parasites that feed within the ear of ungulates, subjecting them to debilitating conditions. Little is known about the spatial dispersion of spinose ticks in animal shelters or the temporal variation in their abundance. Therefore, the objectives of this study were to: 1) determine the temporal distribution of spinose ear tick abundance within animal shelters, 2) determine the spatial distribution of larvae and adults within animal shelters, and 3) examine the effects of climatic variables on tick abundance. No temporal trend was identified for larval or adult ticks. Larval abundance was highest in quadrats located against the shelter wall while no spatial difference was found in adult abundance. Mean larval tick abundance was significantly correlated with mean temperature while mean adult tick abundance was significantly correlated with mean relative humidity.

RESUMEN—Las garrapatas espinosas del o´ıdo, Otobius megnini, son par´asitos mon´oxenos que obtienen su alimento dentro de los o´ıdos de los ungulados, someti´endolos a condiciones debilitantes. Poco se sabe sobre la dispersi´on de garrapatas espinosas en los refugios de animales o la variaci´on temporal en su abundancia. Por lo tanto, los objetivos de este estudio fueron: 1) determinar la distribuci´on temporal de la abundancia de garrapatas espinosas del o´ıdo dentro de los refugios de animales, 2) determinar la distribuci´on espacial de las larvas y adultos dentro de los refugios de animales, y 3) examinar los efectos de las variables clim´aticas sobre la abundancia de garrapatas . No se identific´o ninguna tendencia temporal en las larvas o adultos de garrapatas. La abundancia de larvas fue mayor en los cuadrantes ubicados cerca de la pared del refugio, mientras que no se encontr´o ninguna diferencia espacial en abundancia de adultos. La media de la abundancia de larvas de garrapatas se correlacion´o significativamente con la media de la temperatura, mientras la media de abundancia de los adultos se correlacion´o significativamente con la media de la humedad relativa.

The spinose ear tick, Otobius megnini, is a soft-bodied may change temporally in response to seasonal variation tick belonging to the family . Their distribution in environmental conditions. is in the Nearctic and they are most prevalent in arid to Otobius megnini have a monoxenous life cycle with four semiarid regions of the southwestern United States and stages: 1) egg, 2) six-legged larva, 3) eight-legged nymph, northern Mexico (Bishopp and Trembley, 1945; Keirans and 4) eight-legged adult. Ticks developing in tempera- and Pound, 2003). These ticks are less mobile than other tures between 21–248C typically have oviposition 6–12 d species and spend a portion of their life cycle off-host after dropping as nymphs from their hosts. The number (Needham and Teal, 1991). The host-seeking behavior of of eggs, which are laid in the nesting grounds of potential O. megnini exposes them to variable climatic conditions. hosts, can range from 398–1,187 depending on the In many cases, climatic variables (e.g., temperature and weight of the female (Nava et al., 2008). Egg incubation relative humidity) and changes in vegetation can be ranges from 14–19 d in laboratory studies (Loomis, 1961) useful in predicting tick abundance (Cumming, 2002; and 18–23 d in field studies (Herms, 1917). Once Gilbert, 2010). Of course, the exact relationship between hatching occurs, larvae seek hosts for survival; unfed population size and environmental factors is spatially larvae have been found to survive in the laboratory up to variable across its geographic distribution. For example, 78 d (Wanchinga and Barker, 1986). Larvae feed on the the ranges of temperatures that are suitable for ticks in host for 1–5 wk and then molt into the nymph stage. The areas with high humidity may not be the same suitable majority of nymphs will feed between 2–4 mo (Loomis, temperatures for ticks in environments with low humidity 1961) but have been noted to feed up to 6 mo (Estrada-Pena et al., 2010). In addition, tick abundance (Wanchinga and Barker, 1986). The nymph will feed June 2015 Price et al.—Spatial and temporal distributions of the spinose ear tick, Otobius megnini 225 until it is completely engorged, exit the ear canal, fall off tick abundance; therefore, this research represents a the host, and seek cover for the last molt into the contribution to the scientific literature by examining nonparasitic, eight-legged adult life stage (Hooker, 1908). temporal trends in tick abundance, identifying where Adults remain off the host, use stored reserves obtained these ticks are mostly likely to be found within animal during the nymph stage (Anonymous, 1991), and can shelters, and determining which environmental factors survive up to 2 y (Mayberry, 2003). During this time, are most associated with tick abundance. adults search for a mate and reproduce. The typical amount of time for O. megnini to complete its life cycle MATERIALS AND METHODS—Our study location was at the Fossil ranges from 62–118 d (Loomis, 1961). Rim Wildlife Center, located near Glen Rose, Texas. Fossil Rim Otobius megnini larvae are the infective stage to the WC is a not-for-profit, Association of Zoos & Aquariums- accredited facility specializing in captive breeding programs host. Once larvae hatch from the egg, they actively sense for indigenous and exotic endangered and threatened species information from their environment to detect the of (http://www.fossilrim.org). The Fossil Rim WC is presence of a host (Parola and Raoult, 2001). Ticks have approximately 688 ha and supports over 1,000 animals a specialized sensory structure, called Haller’s organ, that consisting of 50 native and nonnative species. This study was detects the presence of carbon dioxide, temperature, and conducted within the main pasture at Fossil Rim WC, which is humidity (Klompen and Oliver, 1993). Haller’s organ is a approximately 172 ha and is occupied by a variety of ungulates minute cavity at the terminal segment of the first pair of a species. These include the addax (A. nasomaculatus), sable tick’s legs and is composed of a pit and a capsule that antelope (H. niger), gemsbok (O. gazelle), fallow deer (D. dama), contain sensory setae with numerous chemoreceptors and white-tailed deer (O. virginianus). The main pasture designed to target the carbon dioxide (CO ) of exhaling contains a total of 11 shelters from which we selected two of 2 similar size and construction (shelter three = 117 m2; shelter hosts (Klompen and Oliver 1993). Otobius megnini four = 126 m2) to include in this study. The shelter numbers parasitizes domesticated animals, such as cattle, as well described in this study were kept consistent with the numbering as native and exotic wildlife (Becklund, 1968) such as scheme assigned to Fossil Rim WC. We subdivided each shelter Addax nasomaculatus (addax), Oryx gazella (gemsbok), into quadrats (1 m · 1 m) for sampling purposes. Quadrats Tragelaphus angasii (nyala), Hippotragus niger (sable ante- were grouped according to those along the wall, those in the lope), Giraffa camelopardalis (giraffe), and Equus quagga middle of the shelter, and those located along the outer edge of (zebras). A spinose ear tick has even been reported to the shelter to characterize the spatial variation within an animal parasitize humans (Bishopp and Trembley, 1945; Eads shelter. We randomly sampled four quadrats within each area of and Campos, 1984), although this is considered to be a a shelter, resulting in a total of 12 quadrats per animal shelter. Both shelters were sampled biweekly from August 2012–July rare occurrence. 2013 to characterize temporal variation in distribution and Otobius megnini is not known to be a vector for disease. abundance of larval and adult spinose ear ticks. However, a study has shown this tick to be infected with Because larvae represent the host-seeking stage of O. megnini, Coxiella burnetii, which can cause Q fever (Jellison et al., they are attracted to CO2 as it provides a proximate cue that a 1948). Severe irritation in the host can occur due to the host is in the area. We therefore used a modified version of the tick attaching deep within the internal part of the ear. compressed CO2 trap developed by Niebuhr et al. (2013) to The irritation to the host promotes scratching that leads capture the larval ticks. The trap consisted of a 2.27-kg to lacerations that may be prone to secondary infections. compressed CO2 tank with a flow regulator coupled to a Ear tick infestations can result in reduced body weight, network of vinyl tubing with an inside diameter of 0.64 cm. The reduced milk production, and overall lack of vitality tubing was split at three points along the main lines to achieve a (Parish, 1949) or, in some extreme cases, disfigurement total of 12 tubes that were placed separately into the 12 sampling quadrats; hose clamps were used to secure tubing at each split. A or death of the host (Bishopp and Trembley, 1945). These 22-ga dissecting needle was used to puncture holes 0.2 m from negative effects of tick infestation are a concern for the end of each tube. The open end of the tubing was sealed captive breeding programs trying to manage indigenous with a 0.64-cm-diameter eyebolt to prevent leakage. Metal and exotic species, particularly those focusing on endan- frames (0.3 m · 0.3 m) covered in white cotton cloth were gered and threatened species. placed over the holes on each tube. For each sampling period, The ultimate goal of this project was to improve the CO2 was released at a rate of 10 psi for 30 min. After 30 min, quality of life for indigenous and exotic animals at Fossil larvae were harvested from the frames using an aspirator and Rim Wildlife Center (FRWC) by better understanding stored in vials containing 70% ethanol to be counted at a later spatial and temporal variation in the abundance of O. time in the laboratory using a dissecting scope. megnini. The objectives of this study were to determine Adult ticks, which represent a nonfeeding stage, are not attracted to the CO released by a potential host and, therefore, the temporal distribution of spinose ear tick abundance 2 were sampled differently than the larvae. To collect adults at within animal shelters, examine the spatial dispersion of each quadrat, we used an uncovered metal frame (0.3 m · 0.3 adult and larval ticks within animal shelters, and examine m) to delineate the space where ground litter was collected. All the effects of climatic variables on tick abundance. A of the litter located within the sampling frame was placed into limited amount of data exists on microhabitat preferenc- plastic bags for laboratory analysis. These sealed bags were sifted es within animal shelters at Fossil Rim WC and patterns of through a series of three screens to reduce the final amount of 226 The Southwestern Naturalist vol. 60, no. 2-3

FIG. 1—Adult and larval tick abundance (2012-2013) measured biweekly in shelters at Fossil Rim Wildlife Center. Dashed line corresponds to larval tick abundance and solid line corresponds to adult tick abundance. litter that needed to be searched to locate adults. The screens seasonal peaks in abundance. Overall, there was neither a are sized in such a way that the adults passed through the first net decrease nor a net increase in abundance over time and second screen but did not pass through the third screen (1st for both larval (F = 0.299; df = 1, 68; P = 0.586) and adult 2 2 screen = 1.27 cm , 2nd screen = 0.64 cm , 3rd screen = 0.32 = = = 2 ticks (F 1.764; df 1, 68; P 0.189). There was no cm ). The third screen was then exposed to a black light for difference in larval tick abundance between the two approximately 20 min; the black light exposes the fluorescing shelters (F = 0.687; df = 1, 45; P = 0.412) as well as no legs of the adults to help aid in detection. difference in adult abundance between the two shelters (F The environmental data collected included temperature and = 2.628; df = 1, 45; P = 0.112). relative humidity. A Kestrelt 3,000 handheld weather station = (Kestrel Meters, Birmingham, Michigan) was used to gather Because there was no difference in temperature (F temperature and relative humidity data once per shelter during 0.445; df = 1, 45; P = 0.508) and relative humidity (F = each sampling period; both temperature and relative humidity 0.505; df = 1, 45; P = 0.481) between the two shelters over were recorded at ground level in the middle of the shelter. We time, we used the mean between the two shelters as used SPSS software (https://www-01.ibm.com/software/ estimates of environmental conditions. Mean larval tick analytics/spss/) to generate sequence charts for adult and abundance was significantly correlated with mean tem- larval tick abundances within each animal shelter (dependent perature (r = 0.408; P = 0.048; Fig. 2) but not variables) as well as for each of the two environmental factors significantly correlated with mean relative humidity (r = (independent variables). An analysis of covariance was used to 0.130; P = 0.544; Fig. 3). Mean adult tick abundance was statistically compare the abundance of larval and adult ticks not significantly correlated with mean temperature (r = between the two animal shelters; time was used as a covariate. 0.202; P = 0.343; Fig. 2) but was significantly correlated We quantified the degree of dispersion within each shelter using with mean relative humidity (r = 0.443; P = 0.030; Fig. 3). Morisita’s index (Morisita, 1971), which characterizes the spatial Larval tick collection numbers were highest in quad- distribution as being consistent with aggregated, uniform, or random patterns. We also used an analysis of covariance to rats located in the sampling area directly against the determine whether quadrats along the wall, those in the middle shelter wall (F = 5.319; df = 2, 68; P = 0.007). There was of the shelter, or those located along the outer edge of the no difference found in adult tick abundance among the shelter contained the most individuals; time was used as a three areas of the shelter (F = 0.773; df = 2, 68; P = covariate. Linear regression was used to predict the abundance 0.466). Larval ticks demonstrated the following overall of ticks as a function of environmental conditions. spatial patterns for shelter three: aggregated = 80%, uniform = 20%, random = 0%; shelter four: aggregated RESULTS—The abundance of O. megnini varied over = 74%, uniform = 17%, random = 9%. Adult ticks time with multiple peaks in spring, summer, and fall demonstrated the following spatial patterns for shelter months; ticks were collected during winter months but in three: aggregated = 61%, uniform = 33%, random = 6%; low abundances (Fig. 1). Adult abundances were consid- shelter four: aggregated = 8%, uniform = 50%, and erably lower than larval abundances but both exhibited random = 42%. Degree of aggregation was found to be June 2015 Price et al.—Spatial and temporal distributions of the spinose ear tick, Otobius megnini 227

FIG. 2—Correlation between mean tick abundance and mean temperature (2012-2013) measured biweekly in shelters at Fossil Rim Wildlife Center. positively correlated with abundance in both the larval (r timing of the peaks differed from year to year, with = 0.815; P < 0.001; Fig. 4a) and adult (r = 0.726; P < highest larval abundance occurring in April–May and 0.001; Fig. 4b) samples. August–October consecutively. Dreyer et al. (1998) found similar nymph abundance data as compared to adult DISCUSSION—Temporal Trends in Abundance—The abun- abundance in our study, which showed no distinct trend dance of O. megnini varied over time with multiple peaks over time. Neither of these studies reported environmen- throughout the seasons. There was no overall trend in tal conditions, specifically temperature or relative humid- abundance across the year-long study, coinciding with ity, which could help explain the variability in seasonal other studies examining temporal trends in abundance of peaks. Otobius megnini exhibit endophilic behavior during O. megnini (Dreyer et al., 1998; Nava et al., 2008). Nava et nonparasitic stages in that they burrow into the ground, al. (2008) found seasonal peaks in abundance, but the rocks, nest of host, etc. in an effort to avoid unfavorable

FIG. 3—Correlation between mean tick abundance and mean relative humidity (2012-2013) measured biweekly in shelters at Fossil Rim Wildlife Center. 228 The Southwestern Naturalist vol. 60, no. 2-3

However, adult tick abundances were positively corre- lated 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 corre- lated 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 FIG. 4—Correlation between degree of aggregation and adult abundances. The behavior of newly hatched larvae tick abundance (2012-2013) measured biweekly in shelters at remaining near the egg clutch and demonstrating an Fossil Rim Wildlife Center. ambush strategy for host attachment can result in an aggregated distribution (Stafford, 1992). Previous work has documented a relationship demonstrating that the environmental conditions (Estrada-Pena et al., 2010). degree of aggregation is higher in larval stages with Understanding the link between the environment and higher densities and decreases over time as the density the behavior of this species is important when trying to decreases due to the dispersion of the ticks by the hosts identify temporal distributions. Previous studies demon- (Ostfeld et al., 1996). We observed a higher degree of strated that various life stages may be differentially aggregation in the larval stage than in the adult form, affected by environmental conditions such that peaks in supporting the idea that there is a higher degree of abundance of different life stages occur during different aggregation in earlier life stages and that the degree of seasons (Ostfeld et al., 1996). aggregation decreases over time (Daniels and Fish, 1990). Environmental Conditions—Larval tick abundances were As nymphs fall off-host to molt into adults, the spatial positively correlated with temperature; no significant pattern could appear aggregated due to synchronous relationship existed for relative humidity. Egg hatchment detachment of nymphs (Oliver, 1989; Ostfeld et al., has been found to be linked to temperature, with 1996). Highest larval abundance was found in the ovipositon occurring between 20–308C (Loomis, 1961; sampling area located directly against the wall while adult Sweatman, 1967; Wanchinga and Barker, 1986). Abun- abundances did not differ statistically among the three dance of larvae in our study started to increase in March areas of the animal shelter. as temperatures approached 208C and was highest at Management—Direct application of acaricides into the 268C, supporting previous findings of egg hatchment. ears of hosts has been shown to reduce O. megnini Another study measured the effects of temperature and abundances on-host (Drummond et al., 1967; Mayberry, relative humidity on questing of larval ticks and found 2003) while other methods such as application of systemic that temperature affected distance traveled and amount biocides have not been shown to reduce tick abundance of time spent questing but that relative humidity had no (Nava and Guglielmone, 2009). Direct application into the effect (Vail and Smith, 2002). Adult female ticks secrete a ears can be costly and time consuming, as frequent wax covering over their eggs to protect them from reapplication is necessary due to continuous infestation desiccation in dry habitats (Booth, 1989). Resistance of of ticks. In addition, this method may be impractical in eggs to fluctuating relative humidity, along with abun- wildlife facilities, such as Fossil Rim WC, that adopt more dance patterns of larvae, supports our findings of no of a hands-off approach in their management strategies to significant relationship being found between larval mimic natural processes as much as possible. Based on abundance and relative humidity. results from this study, we suggest that effective manage- June 2015 Price et al.—Spatial and temporal distributions of the spinose ear tick, Otobius megnini 229 ment strategies should target specific microhabitats heavily ESTRADA-PENA, A., S. NAVA,I.G.HORAK, AND A. A. GUGLIELMONE. used by ticks while off-host. Within the shelters, our results 2010. Using ground-derived data to assess the environmental suggest control efforts should be concentrated along the niche of the spinose ear tick, Otobius megnini. Entomologia walls where larvae abundance was significantly higher than Experimentalis et Applicata 137:132–142. other areas. Not only does this decrease the amount of GILBERT, L. 2010. Altitudinal patterns of tick and host abun- dance: a potential role for climate change in regulating tick- interaction with the host, but it also focuses eradication borne diseases? Oecologia 162:217–225. efforts where tick populations tend to be concentrated. HACKMAN, R. H. 1975. Expanding abdominal cuticle in the bug In addition to the application of acaricides to the outer Rhodnius and the tick Boophilus. Journal of Insect Physiology edge of animal shelters, the complete removal of animal 21:1613–1623. bedding in early spring could reduce tick populations by HAFEZ, M., S. EL-ZIADY, AND T. H EFNAWY. 1970. 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