Activity Trends and Movement Distances in the Arizona Bark Scorpion (Scorpiones: Buthidae) Author(s): Christopher Stephen Bibbs, Sarah Elizabeth Bengston, and Dawn Heather Gouge Source: Environmental Entomology, 43(6):1613-1620. 2014. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN14148
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BEHAVIOR
Activity Trends and Movement Distances in the Arizona Bark Scorpion (Scorpiones: Buthidae) CHRISTOPHER STEPHEN BIBBS,1,2 SARAH ELIZABETH BENGSTON,3 AND DAWN HEATHER GOUGE4
Environ. Entomol. 43(6): 1613Ð1620 (2014); DOI: http://dx.doi.org/10.1603/EN14148
ABSTRACT The bark scorpion, Centruroides sculpturatus Ewing, is a nocturnal, cryptic, nonburrowing, mobile species that is common in urban landscapes spanning the desert southwest. Bark scorpions are often found in dense localized populations in cities, but the question of whether this is because the species is metabolically movement limited or choose to aggregate has not been addressed. Field observations lead us to believe that the scorpions move very little. Their ability to move is tested here. A circular pacing ring was constructed to observe the distance individuals could move in 2 h under both dark and light conditions. Observations under light motivate the arthropods to move, and signiÞcantly greater distances were observed in light trials, the maximum travel distance being 104.37 m, while the maximum distance in dark trials was 14.63 m. To monitor movement in the Þeld, telemetry tags were used to mark female and male scorpions over 21 d during which relocation distances were recorded daily. Additionally, 12-h and 6-h overnight observational periods took place during which, scorpion movements were recorded hourly. Overall, it was found that scorpions moved signiÞcantly more in the pacing ring than in the Þeld, indicating that Þeld individuals are not moving at their maximum potential. Movement limitation does not explain their distribution pattern. In both the pacing ring and Þeld, gender and pregnancy status had signiÞcant inßuence on distances moved. We conclude that C. sculpturatus is capable of much greater movement than is typically observed in the Þeld. RESUMEN El escorpio´ n de bark, “Centruiroides Sculpturatus” Ewing es un escorpio´ n nocturno (de noche). Es crõ´ptico, sin escavar, y un especie mo´ vil que es comu´ n en los paisajes urbanos que existen en el desierto del suroeste. Se encuentran los escorpio´ nes de bark en las ciudades locales y compactas y que tienen altas populaciones. La pregunta es: ÀPor que´ vienen los escorpiones a estos lugares? ÀEs por que´ el especie es del movimiento metabo´ lico o es por que´ los escorpiones escogan agregarse? Esta pregunta todavõ´a no tiene una respuesta. Las observaciones del campo nos dirigen creer que los escorpiones mueven muy poco. Su abilidad moverse se prueba aquõ´. Un anillo circular de velocidad fue construido para observer la distancia que los escorpiones pueden mover en dos horas segu´ n condiciones de la luz y de la oscuridad. Las observaciones debajo la luz les hacen a los insectos mover, y es una distancia bastante mas larga que en las condiciones de la oscuridad. La distancia ma´xima que movieron debajo la luz fue 104.37 metros, mientras la distancia ma´xima debajo la obsuridad fue 14.63 metros. Para controlar el movimiento en el campo, marcas de telemetrõ´a fueron usadas para distinguir entre los escorpiones femeninos y los ma´sculinos durante los 21 dõ´as en que las distancias de reubicacio´ n fueron recordados diaramente. Tambie´ n, las observaciones de las 12 horas y las 6 horas por noche se realizaron mientras que los moviemientos de los escorpiones fueron recordados cada hora. Segu´ n todo, se encuentra que los escorpiones movieron signiÞcativamente mas en el anillo de velocidad que en el campo. Este nos indica que los insectos del campo no se mueven tanto que tengan la capacidad mover. El lõ´mite del movimiento no explica su manera de distribuirse. En los dos casos del campo y del anillo de velocidad, el ge´ nero y el estado de embarazo tuvieron una inßuencia importante en las distancias que movieron. Terminamos que el escorpio´ n “Centruioides Sculpturatus” Ewing es capa´z de moverse mucho ma´s que fue observado en el campo. KEY WORDS Centruroides, movement, behavior, urban habitat, built environment
Centruroides sculpturatus Ewing, the Arizona bark scorpion, is a generalist predator and native to the desert southwest (Ewing 1928; Stahnke 1956, 1971;
Hadley and Williams 1968; Ennik 1972; Crawford and Krehoff 1975). This species was synonymized with Centruroides exilicauda by Williams (1980), and re-
1 Entomology & Insect Science Program, College of Agriculture and Life Sciences, University of Arizona, 1140 E. South Campus Dr., Forbes 410, Tucson, AZ 85721. 2 Corresponding author, e-mail: [email protected].
3 Department of Ecology & Evolutionary Biology, University of Arizona, P.O. Box 210088, Tucson, AZ 85721-0088. 4 Department of Entomology, University of Arizona, Tucson, AZ 85721.
0046-225X/14/1613Ð1620$04.00/0 䉷 2014 Entomological Society of America
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mained that way until molecular data and venom characterization upheld C. sculpturatus as a distinct species in 2004 (Valdez-Cruz et al. 2004). Like other bark scorpions, C. sculpturatus is cryptic in its native habitat, does not construct its own burrows, and wanders to Þnd resources (Stahnke 1966, 1971; Hadley and Williams 1968). Although desert adapted (Hadley 1974, Polis 1990), the Arizona bark scorpion is preferential of riparian habitats because water availability is one of its limiting factors (Hadley and Williams 1968, Hadley 1971, Polis 1990, Carlson and Rowe 2009). Due to a combination of these preferences and deliberate searching for water to drink (Hadley 1971), the Arizona bark scorpion has become an unexpectedly common concern in urban desert habitats (Smith 1982, Boyer et al. 2001, Gouge and Snyder 2005). Thus, low desert communities may report signiÞcant problems, as this pest is a medically signiÞcant scorpion in the United States (Stahnke 1966, Keegan 1980). C. sculpturatus use plants, rocks, debris, cement walls, storage buildings, and human items as harborage sites (Crawford and Krehoff 1975, Polis 1990, Bibbs et al. 2014) often living in proximity to humans. More importantly, concern over a venomous pest has caused residents and property managers to resort to broadspectrum pesticide applications monthly or as often as every 2 wk, which bring additional concerns about human health impacts due to pesticide exposure. Additionally, pesticides fail to effectively control scorpions (Smith 1982, Roberts and Karr 2013, Trunnelle et al. 2014). Without understanding how this organism behaves in an urban setting, possible solutions such as habitat modiÞcation, exclusion methods, and other nonchemical controls cannot be realized. Bibbs et al. (2014) describe overall preference in refuge type, as well as factors that predict speciÞc preferences; however, many unknowns still prohibit effective population management. One unknown concerns the movement potential of C. sculpturatus. Scorpions, broadly, seem to have poor dispersal ability (Yamashita and Polis 1995, Bryson et al. 2013). Yamashita and Polis (1995) describe dense but localized populations of C. sculpturatus; in a cityscape this appears to be even more evident (D.H.G., unpublished data), but the question of whether this is because the species is metabolically movement limited or that they choose to aggregate has not been addressed. To date, the maximum movement potential is not discussed in any references addressing this species. Field observations lead us to believe that the scorpions move very little, unless disturbed, and then they appear to be capable of signiÞcant relocation. Observations also indicate that C. sculpturatus is mobile, and capable of relocating to varying types of refuges and wandering to Þnd resources. Related work on C. vittatus tested sprinting speeds observed under lab conditions (Shaffer and Formanowicz 1996), but provided no measure of how much distance was voluntarily covered without initiating an exhaustive state. This study investigates whether C. sculpturatus is physically capable of dispersing beyond
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Fig. 1. Movement potential assessment arena. Visible are the acclimation drop box, the marked Plexiglas shields used to control scorpion access, and the circular pacing track the scorpions traveled during timed intervals. (Online Þgure in color.)
the tight local populations they are found in around structures. Materials and Methods Scorpions used in the trials were found using UV light ßuorescence and hand collected using 30.48 cm (12 in) forceps at night in southeastern Arizona cities reported to have incidence of bark scorpion activity. These principally include Phoenix, Chandler, Mesa, Tucson, and Vail. All scorpions were kept communally in a ventilated plastic snap lid container containing a single strip of corrugated cardboard harborage and a sponge wetted with water daily. Scorpions were offered house crickets (Acheta domesticus L.) biweekly. Test trials of any kind were restricted to start dates within 2 d of the most recent feeding. This was to decrease the effect of hunger on the behavioral assays and to screen for individuals that were unwilling to feed and therefore deemed unable to participate in the trial. Scorpions used in trials were then randomly selected from containers. Distance Assays. The experimental arena was created (Fig. 1) after testing a series of preliminary conÞgurations; a circular pacing track proved to be the best experimental design. Original designs included a rectangular track. But the corners of the track became inhibitive, as scorpions would often stop all movement for several hours upon reaching a corner. The drop box used in the Þnal assay design, see Fig. 1, was selected because an entirely clear drop box resulted in panic (indicated by frantic, erratic movement or struggling) throughout acclimation periods and led the scorpions to exhaustion with no movement once trials began. This was possibly the result of no refuge in the entire conÞguration. The dark contrast of the box remedied the continuous erratic movement observed during acclimation and allowed data to be recorded. Tape was used to mark the clear Plexiglas shields. The design of the arena limits airßow; without
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it, scorpions were randomly startled or would stop moving once reaching certain sections of the circuit. Inspection found that even the act of the observer breathing near the track when the arena was not adequately sealed resulted in the scorpions being disturbed, forfeiting the continuity of the data. Sealing the track thoroughly allowed the scorpions to proceed while mitigating disturbance from observation. For dark trials, red overhead lighting was selected among the choices of dimly powered white light, total darkness, red light, and UV black light. For dim white light, the observed behavior did not change from the light trials. For total darkness, it was impossible to accurately record observations and movement data given the resources available. For UV black light, the scorpions still showed signs of stress, occasionally darting swiftly as if to escape a stimulus. The red lighting allowed enough visibility for observation and recording without also provoking the darting behavior seen with the UV black light. Scorpion movement distances were recorded using a circular pacing track. Clear vinyl tubing of 2.54 cm (1 in) inner diameter was cut into 30.48-cm (1 foot)long sections and then halved lengthwise, creating 30.48-cm (1 foot)-long clear vinyl half-pipes. This piping was anchored to white foam particle board creating a 193.04-cm circular pacing track; low temperature hot glue (0440, Ad Tech, Oldsmar, FL) was used to seal the pipe to the particle board base and the entire circuit was closed off against external airßow. A Tjunction using a 10.16-cm span of pipe and an additional 20.32-cm section was created, forming a lead into the track. At the end of the junction was a plastic hinged lid box for dropping in scorpions (Fig. 1). Where the T-junction met the track circuit, a section of pipe at both ends of the T-junction was connected to the circuit and a section of the pipe leading to the drop box was cut out to allow the addition of a removable Plexiglas shield. The shields were marked with two vertical strips of tape. When shields were not in use, the slits in the piping were sealed using clear plastic cling wrap (Sku: 2113027001, Safeway Inc, Pleasanton, CA) to maintain the clear design of the circuit. All testing took place in a constant temperature room maintained at 25⬚C and 8 Ð12% relative humidity (RH) with no windows and all external light entry, such as under doorways, blocked using opaque black plastic. Scorpions were labeled with the trial number of the current test using plastic bee tag numbers (#1172, BioQuip, Rancho Dominguez, CA), mounted to the dorsum, using gel super glue (IDH#234790, Rocky Hill, CT). Immediately after each trial the participating scorpions were dried and frozen, weighed and measured laterally from anterior edge of the carapace to the basal connection of the metasoma in millimeters. Plexiglas shields were set in the two lateral sides of the four inch T-junction section linking the circular track, but not in the path leading to the drop point. The scorpion was then admitted to the drop box, the box closed, and the entire set up left in the testing conditions of the trial for an acclimation
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period of 24 h starting at 0800 hours of the day before testing. At the start of the trial at 0800 hours the following day, the shields blocking the circular track were lifted, allowing the scorpion to enter the circuit. A shield closing the entry path was then dropped and a timer started for a 2-h interval as soon as the scorpion entered the track of its own accord. Lap revolutions were recorded along with observations on styles of movement as they differed between males, females, and visibly pregnant females. Males and females were identiÞed based on metasomal segment lengths (indeterminate individuals were not included, but it is possible that juveniles were accidentally included as females). Males were identiÞed according to longer individual metasoma segments that result in being unable to coil the metasoma at rest. Pregnant females for the purposes of this study were those whose ovaries harbored visible embryos by viewing through the ventral cuticle. Two sets of 50 repetition trials were recorded, using one scorpion for a 2-h interval each time. The Þrst set involved the lab room being well lit with the existing overhead ßuorescent light Þxtures. The second set was a dark room design with all lights and light sources turned off or blocked with the exception of a single 60 watt equivalent red ßuorescent bulb centered over the experiment table. In between each usage, regardless of trial type, the track tubing was separated from the base and the board was wiped down with 70% ethanol (to remove uric acid excretions) and allowed to air dry before reassembling. All distances recorded between the two trial types were then summarized for mean, maximum, and minimum distances. Analysis of variance was used to determine if gender and pregnancy held signiÞcance in the movement outcomes. A MannÐWhitney test was used to evaluate disparity between the light and dark trials. All statistical analyses were carried out at a 5% level of probability (␣ ⫽ 0.05). Radio Telemetry. Twenty telemetry tags (Biotrack PicoPIP Ag337 radio transmitter, LoTek, Ontario, Canada) were calibrated to individual frequency channels ranging from 164.048 MHz to 164.978 MHz and labeled using plastic bee tag numbers (#1172, BioQuip, Rancho Dominguez, CA) with the corresponding channel. The frequency channels were stored in the program memory of a telemetry receiver (1 MHz Biotracker, LoTek, Ontario, Canada) Þtted with an antenna (Yagi folding 3-element antenna, LoTek, Ontario, Canada) for directionalized reception boost. All tags were constructed to a mass of 0.29 g. The tag design included a 7-cm antenna, weather resistant coating, 13-millisecond pulse width, and emission of 28 pulses per minute. Scorpions for tagging were found by scanning the Þeld site at night with UV blacklight and grasping them with 30.48-cm (12 in) forceps for placement into an individual container. The tags were mounted at this time to the dorsum of 20 C. sculpturatus, 10 females and 10 males, using gel super glue (IDH#234790, Rocky Hill, CT). Please note, it was impossible in the dark to be absolutely certain of sexual maturity or sex of scorpions collected from the Þeld, tagged and released. Each scorpion was
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Fig. 2. Histogram visualizing the spread of scorpion movement across 50 light trials, each trial recording distances for one scorpion each. X-axis shows total travel distance broken into categories of 5-m increments. Y-axis shows the number of scorpions that traveled a distance that falls into each range.
returned to its point of discovery immediately after the telemetry tag was securely mounted (the process taking 2Ð3 min). The site selected for monitoring bordered an elementary school campus in Mesa, a city on the east side of the Phoenix valley area. Coordinates were 33⬚ 27⬘41⬙ N, 111⬚ 45⬘47⬙ W, centered on an ⬇100-m stretch of hollow, 15.24 cm ⫻ 20.32 cm ⫻ 40.64 cm (6 in ⫻ 8 in ⫻ 16 in) normal-weight cinderblock, capped cement wall. The north face met a stand of ornamental and fruiting trees. The south face of the same wall formed the perimeter wall of the 25, 211-square meter campus. The last known location of each scorpion per day was marked with colored ßags annotated with the corresponding frequency of the tag used at that location, henceforth indicative of that individual. Using the receiver, scorpions were located daily at midday when movement was least likely. Each subsequent location was marked with a different colored ßag to indicate consecutive day locations. First data recordings began on 1 August 2013 and concluded 21 August 2013. The moon was in the third quarter (23.4% illumination) on August Þrst and was full August 21st (99.7% illumination). Absolute distances between consecutive days harborage were recorded in a straight line from one marker to the next. Additional tracking distances were recorded during one 12-h period and two 6-h periods starting at 1900 hours and repeated hourly to observe nighttime movement activity. Observations were recorded and related to the daily distance readings. Tracking concluded 21 d after tagging in approximation of the battery life deadline. Distance information was then summarized for mean, maximum, and minimum for the daily recordings and each hourly night time tracking stint. A general additive model (GAM) was used to explore whether individual preference, estimated
gender, pregnancy status, temperatures, humidity, and wind were predictive of the movement outcomes. Linear regression between both 6-h overnight intervals was used to check for patterns of movement attributable to 24-h rhythms. A MannÐWhitney U test was performed to see how the Þeld movement differed from the lab recorded movements. All statistical analyses were carried out at ␣ ⫽ 0.05 signiÞcance level using “R” statistical software, v2.14.2 with Tinn-R Editor graphic user interface. Observational notes regarding trends in activity throughout a night are also reported. Results Distance Assays. During the light trials, the minimum travel distance was 19.74 m; the median travel distance was 70.38 m; the maximum travel distance was 104.37 m; the mean travel distance was 70.12 m (Fig. 2). One-way ANOVA supported that gender (F ⫽ 12.95, df ⫽ 1, P ⬍ 0.001) and pregnancy (F ⫽ 11.75, df ⫽ 2, P ⬍ 0.001) affected the travel distance. Males on average traveled farther than females at a mean value of 74 m. Females that were not pregnant averaged lower travel distances of 63 m. Females that were pregnant averaged the lowest travel distances of 47 m. During the dark trials, the minimum travel distance was 0 m; the median travel distance was 0.55 m; the maximum travel distance was 14.63 m; the mean travel distance was 2.15 m (Fig. 3a and b). The data did not follow a normal distribution, so a MannÐWhitney U test was performed to determine that gender (P ⫽ 0.337) had no discernible effect on the recorded movement distances. A KruskalÐWallis test was used to determine if pregnancy status affected distance and was found to have no signiÞcance (P ⫽ 0.465). Males traveled an average of 2.80 m. Females that were not
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Fig. 3. Histogram visualizing the spread of scorpion movement across 50 dark trials, each trial recording distances for one scorpion each. (a) X-axis shows total travel distance broken into categories of 0.5-m increments. Y-axis shows the number of scorpions that traveled a distance that falls into each range. (b) Distribution of scorpion movement within the 0Ð0.5 m category with categories reassigned at 0.05-m increments. Axis labels are shared with overall graph. (Online Þgure in color.)
pregnant traveled an average of 1.50 m. Females that were pregnant traveled an average of 3.10 m. A MannÐ Whitney U test indicated that scorpion travel distances varied signiÞcantly between light trials and dark trials (U ⫽ 2500, z ⫽ 8.617, P ⬍ 0.001). Radio Telemetry. The daily recorded Þeld data are summarized as a mean relocation distance of 1.25 m, a minimum distance of 0 m, and a maximum distance of 31.57 m. A general additive model on the daily relocation measurements indicated that individual preference (P ⬍ 0.001), high temperature (P ⬍ 0.001), low temperature (P ⬍ 0.001), high humidity (P ⬍ 0.001), low humidity (P ⬍ 0.1), maximum wind speed (P ⬍ 0.001), and average wind speed (P ⬍ 0.1) held no predictive power over scorpion movement distances, but gender (P ⬍ 0.010) and to a lesser extent pregnancy status (P ⬍ 0.050) did. A line graph for this daily data (Fig. 4) demonstrates what seem to be erratic bursts of relocation. The 12-h overnight tracking stint where distances were recorded hourly is summarized as a mean travel distance of 0.425 m, a minimum distance of 0 m, and a maximum distance of 16.46 m. A line graph of this interval (Fig. 5) indicates this movement was primarily from one individual. A GAM of these data indicated that individual preference (P ⬍⬍ 0.001), gender (P ⬍⬍ 0.001), hourly temperature (P ⬍⬍ 0.001), hourly humidity (P ⬍⬍ 0.001), and hourly
wind speed (P ⬍⬍ 0.001) were not predictive of the distances traveled. It should be noted that the outlier visible in the line graph (Fig. 5) is a male. In a paired t-test between the daily data set and the 12-h data set, movement rate per hour was assessed by apportioning the data to separate treatments. The results suggest the daily period reßected more movement than the 12-h interval with an hourly period (P ⫽ 0.041, T ⫽ 2.21). For the Þrst 6-h overnight interval on 20 August 2013 where distances were recorded hourly, movement is summarized as a mean of 0.29 m, a minimum of 0 m, and a maximum of 8.53 m. For the second 6-h overnight interval on 21 August 2013 where distances were recorded hourly, movement is summarized as a mean of 0.188 m, a minimum distance of 0 m, and a maximum distance of 8.53 m. General additive models for both of these 6-h intervals also indicated that individual preference (P ⬍⬍ 0.001), gender (P ⬍⬍ 0.001), hourly temperature (P ⬍⬍ 0.001), hourly humidity (P ⬍⬍ 0.001), and hourly wind speed (P ⬍⬍ 0.001) were not predictive of the distances traveled. A linear regression between the two 6-h data sets suggests there was no consistency between the movement data sets over a 24-h period given the time scale of the data (P ⫽ 0.593, R2 ⫽ 0.0029). Comparison of the in-lab movement trials and the telemetry Þeld data using a MannÐWhitney U test indicated that scorpion travel distances varied signif-
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Fig. 4. Line graph representing all scorpion movement recorded at a daily time interval for all tagged scorpions; 21-d tracking period. X-axis represents the tracking day. Y-axis represents distance traveled in meters. Legend indicates telemetry tag channel number; 1Ð10 are females, and 11Ð20 are males. (Online Þgure in color.)
icantly between the lab and the Þeld (U ⫽ 900, z ⫽ 6.25543, 2-tailed P ⫽ 3.96416e⫺10). Discussion Bark scorpion distances recorded in circular pacing track tests were much greater than expected. The disparity between the distances traveled in continuous light versus dark showed that the scorpions were motivated to move; it is assumed they are seeking harborage. However, scorpion movement did not appear to be that of panic. In unrecorded trials during the optimization of the experimental set up, stressed scorpions would dart swiftly in a dash. The design and acclimation interval were altered to ensure that scorpions would not be in a state of stress. That kind of behavior was not observed in any of the trials recorded. The Þnding that males traveled on average farther than females is consistent with the idea that male scorpions maintain higher activity levels as they search for mates (Steinmetz et al. 2004). In light trials, males maintained a more elevated walking stance.
Movement patterns consisted of short, quick bursts followed by brief rest intervals of about 2 min. Males were also highly exploratory, pinching at the experimental set up, pushing on gaps, and attempting to wedge themselves under the Plexiglas shields. Females kept a lower walking stance with a shallow gap between the venter and substrate. Their movement pattern had fairly consistent stride, but they seemed not to move as quickly as the males. This was tempered by females tending to walk fairly continuously and not taking many rest periods. When the females did rest, it was often for ⬇20 min. They were also not as exploratory as males, ignoring continuity differences in the experimental apparatus and not attempting to move the Plexiglas. Additionally, scorpions of different pregnancy status also differed. For females with internal brood, these observations were consistent, but rest periods were observed more often than with nonpregnant females. By contrast, in the dark trials there was relatively little movement. All scorpions were still active, despite not traveling around the ring. Frequent observations of grooming, hunting postures, and elevating the venter from the substrate indicated
Fig. 5. Line graph representing all scorpion movement recorded at a 12-h overnight interval for all tagged scorpions; interval from 1900 to 0700 hours the next morning. X-axis represent the tracking hour. Y-axis represents distance traveled in meters. Legend indicates telemetry tag channel number; 1Ð10 are females, and 11Ð20 are males. (Online Þgure in color.)
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wakefulness. Behavioral activities where not methodically recorded during these tests, but future studies could track the amounts of time males, gravid females, and nongravid females spend walking, resting, grooming, etc. In the Þeld, we expected a correlation with humidity, temperature, or both, given that water seeking is so important in the biology of C. sculpturatus. While this was not found, the GAM did indicate gender and pregnancy status as predictors of movement distance. This could be due to gender-based behavioral differences, like mate seeking on the part of the male. However, inspection of the line graph shows that females were more consistent in their movement, having relatively regular relocation in 3-d spurts. Males had relatively low but frequent movement, with occasional bursts, and in the case of one individual an extended high level of movement over several days. It is reported by Steinmetz et al. (2004) that Centruroides males change their behavior depending on the presence of females. Before being near females, males had erratic bursts of activity. After being exposed to evidence of females, the males would change to short, controlled, search-oriented movement. What Figs. 4 and 5 may be showing is that the male group being tracked is concentrating its presence in a small area, thus not showing much obvious movement. The outlier scorpion may be an example of the erratic searching behavior. Steinmetz et al. (2004) also note that males do not demonstrate this change in behavior through all seasons. It would be beneÞcial to follow up with another tracking effort during an earlier part of summer, before the onset of seasonal rains in the desert southwest (and triggering of mate-seeking behavior). Because the daily period yielded more variability and between the two 6-h intervals no consistent pattern could be seen, it must be stressed that the tracking results did not address activity outside of the particular instances recorded. Additionally, in lab assessments, scorpions were active without necessarily moving to new locations. During the night time observations, scorpions were found grooming, poised for prey capture, or otherwise patrolling tight areas that were not large enough to lead the scorpion a reasonable measuring distance away from its last position. During Þeld tracking intervals the following pattern of activity was observed: scorpions began activity at the onset of dusk; at the tracking location and dates this was approximately starting at 1900 hours. During the 12-h tracking interval, active wakefulness was observed for approximately the Þrst 4 h. By midnight, scorpions no longer appeared to be grooming or in ready postures. A period of low activity lasted for approximately 3 h; after 0300 hours, the scorpions became easily agitated by minimal disturbance and began retreating to nearby harborage. During the two 6-h tracking intervals (both 1900 Ð 0100 hours), the same activity trend was observed. These observations match up with the Þndings of Crawford and Krehoff (1975) who explored activity patterns of scorpions, including C. sculpturatus. Their experiments indicated that C. sculpturatus were ini-
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tially active with the onset of darkness, followed by inactive periods later on. Annotations were also recorded on unmarked scorpion activity during night time observations. During both of the 6-h intervals, a dust storm and a full moon occurred; these may have been inßuential events affecting movement data. Despite the fact that both well-lit nights and weather phenomena are reported as deterrents to scorpion activity (Hadley and Williams 1968), ⬎70 unmarked scorpions were observed in each 6-h interval moving outside of harborage. Scorpions near to irrigation sources ignored the moonlight and weather to drink standing water. These otherwise unfavorable conditions may not function as a strong deterrent to activity in the urban landscape, particularly if a water source is available. It was also more usual to observe scorpions (tagged or untagged) within several centimeters of at least one other scorpion. Although C. sculpturatus can survive as and is sometimes considered a solitary organism, tolerance to conspeciÞcs leads scorpions living in dense populations even outside of winter time, when they are known to gather together in hibernacula. The contrast of how far scorpions were capable of moving in the lab compared with how far they actually moved in the Þeld supports the theory that C. sculpturatus is not found within densely populated pockets strictly because they are movement limited. The tracked scorpions did not have need to relocate outside of the proximal resources, as the tracking site contained ample harborage, insect prey, and a regular water source. If the Arizona bark scorpion was motivated to relocate due to water source or harborage needs, it is suggested that they are more than capable of moving to habitation sites farther than we assumed based on previous literature (Hadley and Williams 1968). Animals with low metabolic rates are not exclusively poor dispersers. The Atlantic blue crab, Callinectes sapidus, succeeds at necessary incidents of dispersal due to efÞciency in locomotor activities rather than having higher oxygen uptake or a special mechanism of dispersal (Booth and McMahon 1992). An important consideration to make is how often C. sculpturatus may need to relocate in an urbanized landscape. Cityscapes are heavily disturbed and events such as construction, landscaping, or ßooding (due to poor water retention on land with paved surface) may all result in temporarily migrant populations of C. sculpturatus. The argument of low vagility might lead one to consider that movement across a landscape is multigenerational, as a population may shift with a new generation spreading out further from an epicenter (Yamashita and Polis 1995, Bryson et al. 2013). However, a disturbed population of C. sculpturatus is certainly capable of dispersing further into an urban landscape to Þnd resources. This may result in relatively mobile populations, rather than just individuals. Given the multiyear life span of scorpions (Polis 1990), this is important to consider as we modify habitats around and within the built environment.
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ENVIRONMENTAL ENTOMOLOGY Acknowledgments
Jude McNally is thanked for his representation of this projectÕs interests to the funding associates allied with Rare Disease Therapeutics, Inc. in the southwestern region of the United States. Information leading to scorpion acquisition was provided by the Tucson Poison and Drug Information Center courtesy of afÞliates Keith Boesen, Jude McNally, and Dan Massey. We thank Mike Ellsworth for Spanish translation of the abstract. The funding for this project was provided by Rare Disease Therapeutics, Inc.
References Cited Bibbs, C. S., S. E. Bengston, and D. H. Gouge. 2014. Exploration of refuge preference in Centruroides sculpturatus (Scorpiones: Buthidae). J. Environ. Entomol. 43: 1345Ð 1353. Booth, C. E., and B. R. McMahon. 1992. Aerobic capacity of the Blue Crab, Callinectes sapidus. Physiol. Zool. 65: 1074Ð 1091. Boyer, L., K. Heubner, J. McNally, and P. Buchanan. 2001. Death from Centruroides scorpion sting allergy. J. Toxicol. Clin. Toxicol. 39: 561Ð562. Bryson, R. W., B. R. Riddle, M. R. Graham, B. T. Smith, and L. Prendini. 2013. As old as the hills: montane scorpions in Southwestern North America reveal ancient associations between biotic diversiÞcation and landscape history. PLoS ONE 8: 1Ð11. Carlson, B. E., and M. P. Rowe. 2009. Temperature and desiccation effects on the antipredator behavior of Centruroides vittatus (Scorpiones: Buthidae). J. Arachnol. 37: 321Ð330. Crawford, C. S., and R. C. Krehoff. 1975. Diel activity in sympatric populations of the scorpions Centruroides sculpturatus (Buthidae) and Diplocentrus spitzeri (Diplocentridae). J. Arachnol. 2: 195Ð204. Ennik, F. 1972. A short review of scorpion biology, management of stings, and control. Cal. Vector Views 19: 69 Ð80. Ewing, H. E. 1928. The scorpions of the western part of the United States, with notes on those occurring in northern Mexico. Proc. U.S. Nat. Mus. 73: 1Ð23. Gouge, D. H., and J. L. Snyder. 2005. Parasitism of bark scorpions Centruroides exilicauda (Scorpiones: Buthidae) by entomopathogenic nematodes (Rhabditida: Steinernematidae; Heterorhabditidae). J. Econ. Entomol. 98: 1486Ð1493. Hadley, N. F. 1971. Water uptake by drinking in the scorpion, Centruroides sculpturatus (Buthidae). Southwest. Nat. 15: 504Ð505.
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Hadley, N. F. 1974. Adaptational biology of desert scorpions. J. Arachnol. 2: 11Ð23. Hadley, N. F., and S. C. Williams. 1968. Surface activities of some North American scorpions in relation to feeding. Ecology 49: 726 Ð734. Keegan, H. L. 1980. Scorpions of medical importance, p. 140. University Press of Mississippi, Jackson, MS. Polis, G. A. 1990. Ecology, pp. 247Ð293. In G. A. Polis (ed.), The biology of scorpions. Stanford University Press, Stanford, CA. Roberts, J. R., and C. J. Karr. 2013. Policy statement: pesticide exposure in children. Pediatrics 130: 1757Ð1764. Shaffer, L. R., and D. R. Formanowicz, Jr. 1996. A cost of viviparity and parental care in scorpions: reduced sprint speed and behavioural compensation. Anim. Behav. 51: 1017Ð1024. Smith, R. L. 1982. Venomous animals of Arizona, p.134. College of Agriculture Cooperative Extension of University of Arizona, Tucson, AZ. Stahnke, H. L. 1956. Scorpions, p. 36. Poisonous animals research laboratory of arizona state college, Tempe, AZ. Stahnke, H. L. 1966. Some aspects of scorpion behavior. Bull. So. Cal. Acad. Sci. 65: 65Ð 80. Stahnke, H. L. 1971. Some observations of the genus Centruroides (Buthidae, Scorpionida), Entomol. News 82: 218 Ð307. Steinmetz, S. B., K. S. Bost, and D. D. Gaffin. 2004. Response of male Centruroides vittatus (Scorpiones: Buthidae) to aerial and substrate-borne chemical signals. Euscorpius 12: 3Ð 6. Trunnelle, K. J., D. H. Bennett, N. S. Tulve, M. S. Clifton, M. D. Davis, A. M. Calafat, R. Moran, D. J. Tancredi, and I. Hertz-Picciotto. 2014. Urinary pyrethroid and chlorpyrifos metabolite concentrations in northern California families and their relationship to indoor residential insecticide levels, part of the Study of Use of Products and Exposure Related Behavior (SUPERB). Environ. Sci. Technol. 48: 1931Ð1939. Valdez-Cruz, N. A., S. Da´ vila, A. Licea, M. Corona, F. Z. Zamudio, J. Garcı´a-Valdes, L. Boyer, and L. D. Possani. 2004. Biochemical, genetic and physiological characterization of venom components from two species of scorpions: Centruroides exilicauda Wood and Centruroides sculpturatus Ewing. Biochimie 86: 387Ð396. Williams, S. C. 1980. Scorpions of Baja California, Mexico, and adjacent islands. Occ. Pap. Calif. Acad. Sci. 135: 1Ð127. Yamashita, T., and G. A. Polis. 1995. A test of the centralmarginal model using sand scorpion populations (Paruroctonus mesaensis, Vaejovidae). J. Arachnol. 23: 60 Ð 64. Received 26 May 2014; accepted 24 September 2014.
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BEHAVIOR
Activity Trends and Movement Distances in the Arizona Bark Scorpion (Scorpiones: Buthidae) CHRISTOPHER STEPHEN BIBBS,1,2 SARAH ELIZABETH BENGSTON,3 AND DAWN HEATHER GOUGE4
Environ. Entomol. 43(6): 1613Ð1620 (2014); DOI: http://dx.doi.org/10.1603/EN14148
ABSTRACT The bark scorpion, Centruroides sculpturatus Ewing, is a nocturnal, cryptic, nonburrowing, mobile species that is common in urban landscapes spanning the desert southwest. Bark scorpions are often found in dense localized populations in cities, but the question of whether this is because the species is metabolically movement limited or choose to aggregate has not been addressed. Field observations lead us to believe that the scorpions move very little. Their ability to move is tested here. A circular pacing ring was constructed to observe the distance individuals could move in 2 h under both dark and light conditions. Observations under light motivate the arthropods to move, and signiÞcantly greater distances were observed in light trials, the maximum travel distance being 104.37 m, while the maximum distance in dark trials was 14.63 m. To monitor movement in the Þeld, telemetry tags were used to mark female and male scorpions over 21 d during which relocation distances were recorded daily. Additionally, 12-h and 6-h overnight observational periods took place during which, scorpion movements were recorded hourly. Overall, it was found that scorpions moved signiÞcantly more in the pacing ring than in the Þeld, indicating that Þeld individuals are not moving at their maximum potential. Movement limitation does not explain their distribution pattern. In both the pacing ring and Þeld, gender and pregnancy status had signiÞcant inßuence on distances moved. We conclude that C. sculpturatus is capable of much greater movement than is typically observed in the Þeld. RESUMEN El escorpio´ n de bark, “Centruiroides Sculpturatus” Ewing es un escorpio´ n nocturno (de noche). Es crõ´ptico, sin escavar, y un especie mo´ vil que es comu´ n en los paisajes urbanos que existen en el desierto del suroeste. Se encuentran los escorpio´ nes de bark en las ciudades locales y compactas y que tienen altas populaciones. La pregunta es: ÀPor que´ vienen los escorpiones a estos lugares? ÀEs por que´ el especie es del movimiento metabo´ lico o es por que´ los escorpiones escogan agregarse? Esta pregunta todavõ´a no tiene una respuesta. Las observaciones del campo nos dirigen creer que los escorpiones mueven muy poco. Su abilidad moverse se prueba aquõ´. Un anillo circular de velocidad fue construido para observer la distancia que los escorpiones pueden mover en dos horas segu´ n condiciones de la luz y de la oscuridad. Las observaciones debajo la luz les hacen a los insectos mover, y es una distancia bastante mas larga que en las condiciones de la oscuridad. La distancia ma´xima que movieron debajo la luz fue 104.37 metros, mientras la distancia ma´xima debajo la obsuridad fue 14.63 metros. Para controlar el movimiento en el campo, marcas de telemetrõ´a fueron usadas para distinguir entre los escorpiones femeninos y los ma´sculinos durante los 21 dõ´as en que las distancias de reubicacio´ n fueron recordados diaramente. Tambie´ n, las observaciones de las 12 horas y las 6 horas por noche se realizaron mientras que los moviemientos de los escorpiones fueron recordados cada hora. Segu´ n todo, se encuentra que los escorpiones movieron signiÞcativamente mas en el anillo de velocidad que en el campo. Este nos indica que los insectos del campo no se mueven tanto que tengan la capacidad mover. El lõ´mite del movimiento no explica su manera de distribuirse. En los dos casos del campo y del anillo de velocidad, el ge´ nero y el estado de embarazo tuvieron una inßuencia importante en las distancias que movieron. Terminamos que el escorpio´ n “Centruioides Sculpturatus” Ewing es capa´z de moverse mucho ma´s que fue observado en el campo. KEY WORDS Centruroides, movement, behavior, urban habitat, built environment
Centruroides sculpturatus Ewing, the Arizona bark scorpion, is a generalist predator and native to the desert southwest (Ewing 1928; Stahnke 1956, 1971;
Hadley and Williams 1968; Ennik 1972; Crawford and Krehoff 1975). This species was synonymized with Centruroides exilicauda by Williams (1980), and re-
1 Entomology & Insect Science Program, College of Agriculture and Life Sciences, University of Arizona, 1140 E. South Campus Dr., Forbes 410, Tucson, AZ 85721. 2 Corresponding author, e-mail: [email protected].
3 Department of Ecology & Evolutionary Biology, University of Arizona, P.O. Box 210088, Tucson, AZ 85721-0088. 4 Department of Entomology, University of Arizona, Tucson, AZ 85721.
0046-225X/14/1613Ð1620$04.00/0 䉷 2014 Entomological Society of America
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mained that way until molecular data and venom characterization upheld C. sculpturatus as a distinct species in 2004 (Valdez-Cruz et al. 2004). Like other bark scorpions, C. sculpturatus is cryptic in its native habitat, does not construct its own burrows, and wanders to Þnd resources (Stahnke 1966, 1971; Hadley and Williams 1968). Although desert adapted (Hadley 1974, Polis 1990), the Arizona bark scorpion is preferential of riparian habitats because water availability is one of its limiting factors (Hadley and Williams 1968, Hadley 1971, Polis 1990, Carlson and Rowe 2009). Due to a combination of these preferences and deliberate searching for water to drink (Hadley 1971), the Arizona bark scorpion has become an unexpectedly common concern in urban desert habitats (Smith 1982, Boyer et al. 2001, Gouge and Snyder 2005). Thus, low desert communities may report signiÞcant problems, as this pest is a medically signiÞcant scorpion in the United States (Stahnke 1966, Keegan 1980). C. sculpturatus use plants, rocks, debris, cement walls, storage buildings, and human items as harborage sites (Crawford and Krehoff 1975, Polis 1990, Bibbs et al. 2014) often living in proximity to humans. More importantly, concern over a venomous pest has caused residents and property managers to resort to broadspectrum pesticide applications monthly or as often as every 2 wk, which bring additional concerns about human health impacts due to pesticide exposure. Additionally, pesticides fail to effectively control scorpions (Smith 1982, Roberts and Karr 2013, Trunnelle et al. 2014). Without understanding how this organism behaves in an urban setting, possible solutions such as habitat modiÞcation, exclusion methods, and other nonchemical controls cannot be realized. Bibbs et al. (2014) describe overall preference in refuge type, as well as factors that predict speciÞc preferences; however, many unknowns still prohibit effective population management. One unknown concerns the movement potential of C. sculpturatus. Scorpions, broadly, seem to have poor dispersal ability (Yamashita and Polis 1995, Bryson et al. 2013). Yamashita and Polis (1995) describe dense but localized populations of C. sculpturatus; in a cityscape this appears to be even more evident (D.H.G., unpublished data), but the question of whether this is because the species is metabolically movement limited or that they choose to aggregate has not been addressed. To date, the maximum movement potential is not discussed in any references addressing this species. Field observations lead us to believe that the scorpions move very little, unless disturbed, and then they appear to be capable of signiÞcant relocation. Observations also indicate that C. sculpturatus is mobile, and capable of relocating to varying types of refuges and wandering to Þnd resources. Related work on C. vittatus tested sprinting speeds observed under lab conditions (Shaffer and Formanowicz 1996), but provided no measure of how much distance was voluntarily covered without initiating an exhaustive state. This study investigates whether C. sculpturatus is physically capable of dispersing beyond
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Fig. 1. Movement potential assessment arena. Visible are the acclimation drop box, the marked Plexiglas shields used to control scorpion access, and the circular pacing track the scorpions traveled during timed intervals. (Online Þgure in color.)
the tight local populations they are found in around structures. Materials and Methods Scorpions used in the trials were found using UV light ßuorescence and hand collected using 30.48 cm (12 in) forceps at night in southeastern Arizona cities reported to have incidence of bark scorpion activity. These principally include Phoenix, Chandler, Mesa, Tucson, and Vail. All scorpions were kept communally in a ventilated plastic snap lid container containing a single strip of corrugated cardboard harborage and a sponge wetted with water daily. Scorpions were offered house crickets (Acheta domesticus L.) biweekly. Test trials of any kind were restricted to start dates within 2 d of the most recent feeding. This was to decrease the effect of hunger on the behavioral assays and to screen for individuals that were unwilling to feed and therefore deemed unable to participate in the trial. Scorpions used in trials were then randomly selected from containers. Distance Assays. The experimental arena was created (Fig. 1) after testing a series of preliminary conÞgurations; a circular pacing track proved to be the best experimental design. Original designs included a rectangular track. But the corners of the track became inhibitive, as scorpions would often stop all movement for several hours upon reaching a corner. The drop box used in the Þnal assay design, see Fig. 1, was selected because an entirely clear drop box resulted in panic (indicated by frantic, erratic movement or struggling) throughout acclimation periods and led the scorpions to exhaustion with no movement once trials began. This was possibly the result of no refuge in the entire conÞguration. The dark contrast of the box remedied the continuous erratic movement observed during acclimation and allowed data to be recorded. Tape was used to mark the clear Plexiglas shields. The design of the arena limits airßow; without
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BIBBS ET AL.: MOBILITY TRENDS IN THE ARIZONA BARK SCORPION
it, scorpions were randomly startled or would stop moving once reaching certain sections of the circuit. Inspection found that even the act of the observer breathing near the track when the arena was not adequately sealed resulted in the scorpions being disturbed, forfeiting the continuity of the data. Sealing the track thoroughly allowed the scorpions to proceed while mitigating disturbance from observation. For dark trials, red overhead lighting was selected among the choices of dimly powered white light, total darkness, red light, and UV black light. For dim white light, the observed behavior did not change from the light trials. For total darkness, it was impossible to accurately record observations and movement data given the resources available. For UV black light, the scorpions still showed signs of stress, occasionally darting swiftly as if to escape a stimulus. The red lighting allowed enough visibility for observation and recording without also provoking the darting behavior seen with the UV black light. Scorpion movement distances were recorded using a circular pacing track. Clear vinyl tubing of 2.54 cm (1 in) inner diameter was cut into 30.48-cm (1 foot)long sections and then halved lengthwise, creating 30.48-cm (1 foot)-long clear vinyl half-pipes. This piping was anchored to white foam particle board creating a 193.04-cm circular pacing track; low temperature hot glue (0440, Ad Tech, Oldsmar, FL) was used to seal the pipe to the particle board base and the entire circuit was closed off against external airßow. A Tjunction using a 10.16-cm span of pipe and an additional 20.32-cm section was created, forming a lead into the track. At the end of the junction was a plastic hinged lid box for dropping in scorpions (Fig. 1). Where the T-junction met the track circuit, a section of pipe at both ends of the T-junction was connected to the circuit and a section of the pipe leading to the drop box was cut out to allow the addition of a removable Plexiglas shield. The shields were marked with two vertical strips of tape. When shields were not in use, the slits in the piping were sealed using clear plastic cling wrap (Sku: 2113027001, Safeway Inc, Pleasanton, CA) to maintain the clear design of the circuit. All testing took place in a constant temperature room maintained at 25⬚C and 8 Ð12% relative humidity (RH) with no windows and all external light entry, such as under doorways, blocked using opaque black plastic. Scorpions were labeled with the trial number of the current test using plastic bee tag numbers (#1172, BioQuip, Rancho Dominguez, CA), mounted to the dorsum, using gel super glue (IDH#234790, Rocky Hill, CT). Immediately after each trial the participating scorpions were dried and frozen, weighed and measured laterally from anterior edge of the carapace to the basal connection of the metasoma in millimeters. Plexiglas shields were set in the two lateral sides of the four inch T-junction section linking the circular track, but not in the path leading to the drop point. The scorpion was then admitted to the drop box, the box closed, and the entire set up left in the testing conditions of the trial for an acclimation
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period of 24 h starting at 0800 hours of the day before testing. At the start of the trial at 0800 hours the following day, the shields blocking the circular track were lifted, allowing the scorpion to enter the circuit. A shield closing the entry path was then dropped and a timer started for a 2-h interval as soon as the scorpion entered the track of its own accord. Lap revolutions were recorded along with observations on styles of movement as they differed between males, females, and visibly pregnant females. Males and females were identiÞed based on metasomal segment lengths (indeterminate individuals were not included, but it is possible that juveniles were accidentally included as females). Males were identiÞed according to longer individual metasoma segments that result in being unable to coil the metasoma at rest. Pregnant females for the purposes of this study were those whose ovaries harbored visible embryos by viewing through the ventral cuticle. Two sets of 50 repetition trials were recorded, using one scorpion for a 2-h interval each time. The Þrst set involved the lab room being well lit with the existing overhead ßuorescent light Þxtures. The second set was a dark room design with all lights and light sources turned off or blocked with the exception of a single 60 watt equivalent red ßuorescent bulb centered over the experiment table. In between each usage, regardless of trial type, the track tubing was separated from the base and the board was wiped down with 70% ethanol (to remove uric acid excretions) and allowed to air dry before reassembling. All distances recorded between the two trial types were then summarized for mean, maximum, and minimum distances. Analysis of variance was used to determine if gender and pregnancy held signiÞcance in the movement outcomes. A MannÐWhitney test was used to evaluate disparity between the light and dark trials. All statistical analyses were carried out at a 5% level of probability (␣ ⫽ 0.05). Radio Telemetry. Twenty telemetry tags (Biotrack PicoPIP Ag337 radio transmitter, LoTek, Ontario, Canada) were calibrated to individual frequency channels ranging from 164.048 MHz to 164.978 MHz and labeled using plastic bee tag numbers (#1172, BioQuip, Rancho Dominguez, CA) with the corresponding channel. The frequency channels were stored in the program memory of a telemetry receiver (1 MHz Biotracker, LoTek, Ontario, Canada) Þtted with an antenna (Yagi folding 3-element antenna, LoTek, Ontario, Canada) for directionalized reception boost. All tags were constructed to a mass of 0.29 g. The tag design included a 7-cm antenna, weather resistant coating, 13-millisecond pulse width, and emission of 28 pulses per minute. Scorpions for tagging were found by scanning the Þeld site at night with UV blacklight and grasping them with 30.48-cm (12 in) forceps for placement into an individual container. The tags were mounted at this time to the dorsum of 20 C. sculpturatus, 10 females and 10 males, using gel super glue (IDH#234790, Rocky Hill, CT). Please note, it was impossible in the dark to be absolutely certain of sexual maturity or sex of scorpions collected from the Þeld, tagged and released. Each scorpion was
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Fig. 2. Histogram visualizing the spread of scorpion movement across 50 light trials, each trial recording distances for one scorpion each. X-axis shows total travel distance broken into categories of 5-m increments. Y-axis shows the number of scorpions that traveled a distance that falls into each range.
returned to its point of discovery immediately after the telemetry tag was securely mounted (the process taking 2Ð3 min). The site selected for monitoring bordered an elementary school campus in Mesa, a city on the east side of the Phoenix valley area. Coordinates were 33⬚ 27⬘41⬙ N, 111⬚ 45⬘47⬙ W, centered on an ⬇100-m stretch of hollow, 15.24 cm ⫻ 20.32 cm ⫻ 40.64 cm (6 in ⫻ 8 in ⫻ 16 in) normal-weight cinderblock, capped cement wall. The north face met a stand of ornamental and fruiting trees. The south face of the same wall formed the perimeter wall of the 25, 211-square meter campus. The last known location of each scorpion per day was marked with colored ßags annotated with the corresponding frequency of the tag used at that location, henceforth indicative of that individual. Using the receiver, scorpions were located daily at midday when movement was least likely. Each subsequent location was marked with a different colored ßag to indicate consecutive day locations. First data recordings began on 1 August 2013 and concluded 21 August 2013. The moon was in the third quarter (23.4% illumination) on August Þrst and was full August 21st (99.7% illumination). Absolute distances between consecutive days harborage were recorded in a straight line from one marker to the next. Additional tracking distances were recorded during one 12-h period and two 6-h periods starting at 1900 hours and repeated hourly to observe nighttime movement activity. Observations were recorded and related to the daily distance readings. Tracking concluded 21 d after tagging in approximation of the battery life deadline. Distance information was then summarized for mean, maximum, and minimum for the daily recordings and each hourly night time tracking stint. A general additive model (GAM) was used to explore whether individual preference, estimated
gender, pregnancy status, temperatures, humidity, and wind were predictive of the movement outcomes. Linear regression between both 6-h overnight intervals was used to check for patterns of movement attributable to 24-h rhythms. A MannÐWhitney U test was performed to see how the Þeld movement differed from the lab recorded movements. All statistical analyses were carried out at ␣ ⫽ 0.05 signiÞcance level using “R” statistical software, v2.14.2 with Tinn-R Editor graphic user interface. Observational notes regarding trends in activity throughout a night are also reported. Results Distance Assays. During the light trials, the minimum travel distance was 19.74 m; the median travel distance was 70.38 m; the maximum travel distance was 104.37 m; the mean travel distance was 70.12 m (Fig. 2). One-way ANOVA supported that gender (F ⫽ 12.95, df ⫽ 1, P ⬍ 0.001) and pregnancy (F ⫽ 11.75, df ⫽ 2, P ⬍ 0.001) affected the travel distance. Males on average traveled farther than females at a mean value of 74 m. Females that were not pregnant averaged lower travel distances of 63 m. Females that were pregnant averaged the lowest travel distances of 47 m. During the dark trials, the minimum travel distance was 0 m; the median travel distance was 0.55 m; the maximum travel distance was 14.63 m; the mean travel distance was 2.15 m (Fig. 3a and b). The data did not follow a normal distribution, so a MannÐWhitney U test was performed to determine that gender (P ⫽ 0.337) had no discernible effect on the recorded movement distances. A KruskalÐWallis test was used to determine if pregnancy status affected distance and was found to have no signiÞcance (P ⫽ 0.465). Males traveled an average of 2.80 m. Females that were not
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Fig. 3. Histogram visualizing the spread of scorpion movement across 50 dark trials, each trial recording distances for one scorpion each. (a) X-axis shows total travel distance broken into categories of 0.5-m increments. Y-axis shows the number of scorpions that traveled a distance that falls into each range. (b) Distribution of scorpion movement within the 0Ð0.5 m category with categories reassigned at 0.05-m increments. Axis labels are shared with overall graph. (Online Þgure in color.)
pregnant traveled an average of 1.50 m. Females that were pregnant traveled an average of 3.10 m. A MannÐ Whitney U test indicated that scorpion travel distances varied signiÞcantly between light trials and dark trials (U ⫽ 2500, z ⫽ 8.617, P ⬍ 0.001). Radio Telemetry. The daily recorded Þeld data are summarized as a mean relocation distance of 1.25 m, a minimum distance of 0 m, and a maximum distance of 31.57 m. A general additive model on the daily relocation measurements indicated that individual preference (P ⬍ 0.001), high temperature (P ⬍ 0.001), low temperature (P ⬍ 0.001), high humidity (P ⬍ 0.001), low humidity (P ⬍ 0.1), maximum wind speed (P ⬍ 0.001), and average wind speed (P ⬍ 0.1) held no predictive power over scorpion movement distances, but gender (P ⬍ 0.010) and to a lesser extent pregnancy status (P ⬍ 0.050) did. A line graph for this daily data (Fig. 4) demonstrates what seem to be erratic bursts of relocation. The 12-h overnight tracking stint where distances were recorded hourly is summarized as a mean travel distance of 0.425 m, a minimum distance of 0 m, and a maximum distance of 16.46 m. A line graph of this interval (Fig. 5) indicates this movement was primarily from one individual. A GAM of these data indicated that individual preference (P ⬍⬍ 0.001), gender (P ⬍⬍ 0.001), hourly temperature (P ⬍⬍ 0.001), hourly humidity (P ⬍⬍ 0.001), and hourly
wind speed (P ⬍⬍ 0.001) were not predictive of the distances traveled. It should be noted that the outlier visible in the line graph (Fig. 5) is a male. In a paired t-test between the daily data set and the 12-h data set, movement rate per hour was assessed by apportioning the data to separate treatments. The results suggest the daily period reßected more movement than the 12-h interval with an hourly period (P ⫽ 0.041, T ⫽ 2.21). For the Þrst 6-h overnight interval on 20 August 2013 where distances were recorded hourly, movement is summarized as a mean of 0.29 m, a minimum of 0 m, and a maximum of 8.53 m. For the second 6-h overnight interval on 21 August 2013 where distances were recorded hourly, movement is summarized as a mean of 0.188 m, a minimum distance of 0 m, and a maximum distance of 8.53 m. General additive models for both of these 6-h intervals also indicated that individual preference (P ⬍⬍ 0.001), gender (P ⬍⬍ 0.001), hourly temperature (P ⬍⬍ 0.001), hourly humidity (P ⬍⬍ 0.001), and hourly wind speed (P ⬍⬍ 0.001) were not predictive of the distances traveled. A linear regression between the two 6-h data sets suggests there was no consistency between the movement data sets over a 24-h period given the time scale of the data (P ⫽ 0.593, R2 ⫽ 0.0029). Comparison of the in-lab movement trials and the telemetry Þeld data using a MannÐWhitney U test indicated that scorpion travel distances varied signif-
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Fig. 4. Line graph representing all scorpion movement recorded at a daily time interval for all tagged scorpions; 21-d tracking period. X-axis represents the tracking day. Y-axis represents distance traveled in meters. Legend indicates telemetry tag channel number; 1Ð10 are females, and 11Ð20 are males. (Online Þgure in color.)
icantly between the lab and the Þeld (U ⫽ 900, z ⫽ 6.25543, 2-tailed P ⫽ 3.96416e⫺10). Discussion Bark scorpion distances recorded in circular pacing track tests were much greater than expected. The disparity between the distances traveled in continuous light versus dark showed that the scorpions were motivated to move; it is assumed they are seeking harborage. However, scorpion movement did not appear to be that of panic. In unrecorded trials during the optimization of the experimental set up, stressed scorpions would dart swiftly in a dash. The design and acclimation interval were altered to ensure that scorpions would not be in a state of stress. That kind of behavior was not observed in any of the trials recorded. The Þnding that males traveled on average farther than females is consistent with the idea that male scorpions maintain higher activity levels as they search for mates (Steinmetz et al. 2004). In light trials, males maintained a more elevated walking stance.
Movement patterns consisted of short, quick bursts followed by brief rest intervals of about 2 min. Males were also highly exploratory, pinching at the experimental set up, pushing on gaps, and attempting to wedge themselves under the Plexiglas shields. Females kept a lower walking stance with a shallow gap between the venter and substrate. Their movement pattern had fairly consistent stride, but they seemed not to move as quickly as the males. This was tempered by females tending to walk fairly continuously and not taking many rest periods. When the females did rest, it was often for ⬇20 min. They were also not as exploratory as males, ignoring continuity differences in the experimental apparatus and not attempting to move the Plexiglas. Additionally, scorpions of different pregnancy status also differed. For females with internal brood, these observations were consistent, but rest periods were observed more often than with nonpregnant females. By contrast, in the dark trials there was relatively little movement. All scorpions were still active, despite not traveling around the ring. Frequent observations of grooming, hunting postures, and elevating the venter from the substrate indicated
Fig. 5. Line graph representing all scorpion movement recorded at a 12-h overnight interval for all tagged scorpions; interval from 1900 to 0700 hours the next morning. X-axis represent the tracking hour. Y-axis represents distance traveled in meters. Legend indicates telemetry tag channel number; 1Ð10 are females, and 11Ð20 are males. (Online Þgure in color.)
December 2014
BIBBS ET AL.: MOBILITY TRENDS IN THE ARIZONA BARK SCORPION
wakefulness. Behavioral activities where not methodically recorded during these tests, but future studies could track the amounts of time males, gravid females, and nongravid females spend walking, resting, grooming, etc. In the Þeld, we expected a correlation with humidity, temperature, or both, given that water seeking is so important in the biology of C. sculpturatus. While this was not found, the GAM did indicate gender and pregnancy status as predictors of movement distance. This could be due to gender-based behavioral differences, like mate seeking on the part of the male. However, inspection of the line graph shows that females were more consistent in their movement, having relatively regular relocation in 3-d spurts. Males had relatively low but frequent movement, with occasional bursts, and in the case of one individual an extended high level of movement over several days. It is reported by Steinmetz et al. (2004) that Centruroides males change their behavior depending on the presence of females. Before being near females, males had erratic bursts of activity. After being exposed to evidence of females, the males would change to short, controlled, search-oriented movement. What Figs. 4 and 5 may be showing is that the male group being tracked is concentrating its presence in a small area, thus not showing much obvious movement. The outlier scorpion may be an example of the erratic searching behavior. Steinmetz et al. (2004) also note that males do not demonstrate this change in behavior through all seasons. It would be beneÞcial to follow up with another tracking effort during an earlier part of summer, before the onset of seasonal rains in the desert southwest (and triggering of mate-seeking behavior). Because the daily period yielded more variability and between the two 6-h intervals no consistent pattern could be seen, it must be stressed that the tracking results did not address activity outside of the particular instances recorded. Additionally, in lab assessments, scorpions were active without necessarily moving to new locations. During the night time observations, scorpions were found grooming, poised for prey capture, or otherwise patrolling tight areas that were not large enough to lead the scorpion a reasonable measuring distance away from its last position. During Þeld tracking intervals the following pattern of activity was observed: scorpions began activity at the onset of dusk; at the tracking location and dates this was approximately starting at 1900 hours. During the 12-h tracking interval, active wakefulness was observed for approximately the Þrst 4 h. By midnight, scorpions no longer appeared to be grooming or in ready postures. A period of low activity lasted for approximately 3 h; after 0300 hours, the scorpions became easily agitated by minimal disturbance and began retreating to nearby harborage. During the two 6-h tracking intervals (both 1900 Ð 0100 hours), the same activity trend was observed. These observations match up with the Þndings of Crawford and Krehoff (1975) who explored activity patterns of scorpions, including C. sculpturatus. Their experiments indicated that C. sculpturatus were ini-
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tially active with the onset of darkness, followed by inactive periods later on. Annotations were also recorded on unmarked scorpion activity during night time observations. During both of the 6-h intervals, a dust storm and a full moon occurred; these may have been inßuential events affecting movement data. Despite the fact that both well-lit nights and weather phenomena are reported as deterrents to scorpion activity (Hadley and Williams 1968), ⬎70 unmarked scorpions were observed in each 6-h interval moving outside of harborage. Scorpions near to irrigation sources ignored the moonlight and weather to drink standing water. These otherwise unfavorable conditions may not function as a strong deterrent to activity in the urban landscape, particularly if a water source is available. It was also more usual to observe scorpions (tagged or untagged) within several centimeters of at least one other scorpion. Although C. sculpturatus can survive as and is sometimes considered a solitary organism, tolerance to conspeciÞcs leads scorpions living in dense populations even outside of winter time, when they are known to gather together in hibernacula. The contrast of how far scorpions were capable of moving in the lab compared with how far they actually moved in the Þeld supports the theory that C. sculpturatus is not found within densely populated pockets strictly because they are movement limited. The tracked scorpions did not have need to relocate outside of the proximal resources, as the tracking site contained ample harborage, insect prey, and a regular water source. If the Arizona bark scorpion was motivated to relocate due to water source or harborage needs, it is suggested that they are more than capable of moving to habitation sites farther than we assumed based on previous literature (Hadley and Williams 1968). Animals with low metabolic rates are not exclusively poor dispersers. The Atlantic blue crab, Callinectes sapidus, succeeds at necessary incidents of dispersal due to efÞciency in locomotor activities rather than having higher oxygen uptake or a special mechanism of dispersal (Booth and McMahon 1992). An important consideration to make is how often C. sculpturatus may need to relocate in an urbanized landscape. Cityscapes are heavily disturbed and events such as construction, landscaping, or ßooding (due to poor water retention on land with paved surface) may all result in temporarily migrant populations of C. sculpturatus. The argument of low vagility might lead one to consider that movement across a landscape is multigenerational, as a population may shift with a new generation spreading out further from an epicenter (Yamashita and Polis 1995, Bryson et al. 2013). However, a disturbed population of C. sculpturatus is certainly capable of dispersing further into an urban landscape to Þnd resources. This may result in relatively mobile populations, rather than just individuals. Given the multiyear life span of scorpions (Polis 1990), this is important to consider as we modify habitats around and within the built environment.
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ENVIRONMENTAL ENTOMOLOGY Acknowledgments
Jude McNally is thanked for his representation of this projectÕs interests to the funding associates allied with Rare Disease Therapeutics, Inc. in the southwestern region of the United States. Information leading to scorpion acquisition was provided by the Tucson Poison and Drug Information Center courtesy of afÞliates Keith Boesen, Jude McNally, and Dan Massey. We thank Mike Ellsworth for Spanish translation of the abstract. The funding for this project was provided by Rare Disease Therapeutics, Inc.
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