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Endure your parasites: sleepy lizard movement is notaffected by their ectoparasites
Journal: Canadian Journal of Zoology
Manuscript ID cjz-2017-0352.R1
Manuscript Type: Article
Date Submitted by theAuthor: 18-Mar-2018
Complete List of Authors: Taggart, Patrick; The University of Adelaide, School of Animaland Veterinary Science; University of AdelaideLeu, Stephan; Macquarie University Department of BiologicalSciencesSpiegel, Orr; Ben Gurion University of the Negev, MitraniDepartment of Desert EcologyGodfery, Stephanie; University of Otago, Department ofZoologySih, Andrew; University of California, Davis, EnvironmentalScience and Policy Dept.Bull, C; Flinders University, College of Science and Engineering
Is your manuscript invitedfor consideration in a
Special Issue?:Not applicable (regular submission)
Keyword: reptile, body-mass index, movement ecology, parasite, gpstracking, host-parasite interaction, spatial behaviour
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1 Endure your parasites: sleepy lizard movement is not affected by their ectoparasites
2
3 Patrick L Taggarta,b, Stephan T Leua,c, Orr Spiegeld, Stephanie S Godfreye, Andrew Sihf and C Michael Bulla
4
5 aCollege of Science and Engineering, Flinders University
6 bcurrent address: School of Animal and Veterinary Science, University of Adelaide
7 ccurrent address: Department of Biological Sciences, Macquarie University
8 dSchool of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel
9 eDepartment of Zoology, University of Otago, Dunedin, New Zealand
10 fDepartment of Environmental Science and Policy, University of California, Davis, U.S.A.
11
12
13 Corresponding author:
14 Patrick Taggart
15 Email: [email protected]
16 Address: University of Adelaide, Veterinary Health Centre, Building E40 Mudla Wirra Rd,
17 Roseworthy SA, 5371
18
19 Author contributions:
20 PLT wrote, drafted and revised manuscript; STL conducted statistical analyses, jointly wrote,
21 drafted and revised manuscript, jointly conceived research questions, and co-supervised project;
22 OS drafted and revised manuscript; SSG collected data, drafted and revised manuscript; AS
23 drafted and revised manuscript; CMB primary supervisor of project, sourced funding and jointly
24 conceived research questions.
25
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26
27
28 Short title:
29 Ectoparasites does not affect lizard movement
30
31 Abstract
32 Movement is often used to indicate host vigour, as it has various ecological and evolutionary
33 implications, and has been shown to be affected by parasites. We investigate the relationship
34 between tick load and movement in the Australian sleepy lizard (Tiliqua rugosa Grey, 1825)
35 using high resolution GPS tracking. This allowed us to track individuals across the entire activity
36 season. We hypothesised that tick load negatively affects host movement (mean distance moved
37 day-1). We used a multivariate statistical model informed by the ecology and biology of the host
38 and parasite, their host-parasite relationship, and known host movement patterns. This allowed
39 us to quantify the effects of ticks on lizard movement above and beyond effects of other factors
40 such as time in the activity season, lizard body condition and stress. We did not find any support
41 for our hypothesis. Instead, our results provide evidence that lizard movement is strongly driven
42 by internal state (sex and body condition independent of tick load), and by external factors
43 (environmental conditions). We suggest that the sleepy lizard has largely adapted to natural
44 levels of tick infection in this system. Our results conform to host-parasite arms race theory,
45 which predicts varying impacts of parasites on hosts in natural systems.
46
47
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48 Keywords: reptile, body-mass index, movement ecology, parasite, gps tracking, host-parasite
49 interaction, spatial behaviour, sleepy lizard, Tiliqua rugosa
50
51
52 Introduction
53 Parasites, by definition, gain their energy resources from their hosts, which negatively impacts
54 the host’s health and vigour (Beyer and Grossman 1997; Fenner and Bull 2008). Such impacts in
55 host-parasite relationships drive selection for host defence mechanisms against parasites and
56 parasite specialisation to overcome host defences, resulting in a host-parasite arm race (Dawkins
57 and Krebs 1979). These opposing selection pressures are key drivers of evolutionary and
58 ecosystem processes within host-parasite interactions (Thomas et al. 1999; Brockhurst et al.
59 2004; Nunn et al. 2004; Martin et al. 2011). The impact parasites have on their hosts varies
60 substantially, ranging from behavioural changes, for instance when parasites manipulate their
61 hosts to increase transmission probability (Poulin 2010, 2013), to population growth regulation
62 (Anderson 1978), substantial reductions in host health (e.g., paralysis (Hamat et al. 2017)),
63 reduced reproductive success (Marzal et al. 2005) and increased mortality (Fraser et al. 2016).
64 Movement, is a measure often used to indicate host vigour (Angelier et al. 2007; Warren et al.
65 2011) and has been shown to be affected by parasite load (Fenner and Bull 2008). Here we
66 investigate the relationship between ectoparasites and vigour in a lizard-tick system.
67
68 Animal movement drives various ecological processes like dispersal, foraging and species-co-
69 existence (Nathan et al. 2008; Hansson and Åkesson 2014). Thus, understanding how parasites
70 affect movement of their host is essential for broad topics in ecology, with implications for
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71 management and conservation (Poulin 2010; Kays et al. 2015; Dougherty et al. 2017).
72 Furthermore, a feedback loop between host movement and parasite infection may exist. Before
73 infection, increased host movement can increase the probability of parasite exposure, particularly
74 for parasites that have a free-living infectious stage in the off-host environment or socially
75 transmitted parasites. For example, dispersal events have been suggested to increase parasite and
76 disease spread in both animals and humans (White et al. 2000; Russell et al. 2005; Viboud et al.
77 2006). Post-infection, parasites can decrease movement by reducing host vigour. For example,
78 O’Dwyer et al. (2014) found a trend towards reduced movements in intertidal snails infected
79 with philophthalmid trematode parasites. Similarly, lizards with experimentally reduced parasite
80 burdens have been shown to move around for longer time periods during observation sessions
81 (Main and Bull 2000; Fenner and Bull 2008). Conversely, there is also evidence that host
82 manipulation by parasites can enhance certain movements or overall activity (Poulin 2013), for
83 example risk taking behaviour in rodents towards cats (Médoc and Beisel 2008) or risky displays
84 by fish infested by trophically transmitted parasites (Lafferty and Morris 1996; Sato et al. 2012).
85 Understanding this feedback between parasite load and host movement within a species (Leung
86 and Koprivnikar 2016) can provide valuable insights into the host-parasite relationship. If there
87 is a negative feedback loop (e.g., where increased movement increases parasite loads, but higher
88 parasite load decreases movement), the system would tend towards intermediate parasite loads,
89 whereas a positive feedback loop (e.g., where increased movement increases parasite loads and
90 parasites cause hosts to move more (e.g., with parasite manipulation of host behaviour (Berdoy
91 et al. 2000), the feedback loop can result in an explosive accumulation of parasites in some hosts.
92
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93 Many of the above mentioned relationships and examples (but not all) have been demonstrated in
94 the laboratory, but not the field. Here, we aim to fill this gap by working in-situ to upscale these
95 findings to a natural population of sleepy lizards (Tiliqua rugosa Gray, 1825). We focus on the
96 effect of parasite load on individual host movement. Working in South Australia, we tracked the
97 movement of free-ranging sleepy lizards infested with two species of parasitic ticks. Previous
98 studies of the effect of parasites in this system supported two complementary hypotheses. Bull
99 and Burzacott (1993) reported a positive relationship between lizard body condition and tick
100 load, and suggested that high quality home ranges simultaneously benefit both lizards and ticks,
101 driving this relationship, and supporting the favourable patch hypothesis. Later, Main and Bull
102 (2000) found evidence for the ‘reduced vigor’ hypothesis by experimentally manipulating lizard
103 tick loads and showing that tick infestation reduced endurance and daily movements in sleepy
104 lizards. While this work demonstrates that heavy tick loads can have a negative effect on lizards,
105 we still do not know whether this effect is present under natural conditions where infestation
106 levels are generally lower, and lizards can compensate for lower vigor by obtaining greater
107 energy resources in high quality home ranges.
108
109 Due to the wealth of knowledge surrounding the sleepy lizard – tick system, and following the
110 results of Main and Bull (2000), it is unlikely that ticks increase lizard movement to facilitate
111 their transmission. Consequently, we formulate three predictions: 1) under natural conditions
112 ticks negatively affects lizard movement activity; 2) the effects of ticks on lizard movement
113 increases with decreasing host body condition (Beldomenico et al. 2008; Beldomenico and
114 Begon 2010), such as later in the season when individuals experience particularly harsh
115 environmental conditions (hot and dry) and food resources have dried out; and 3) tick abundance
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116 in the environment, and hence tick load on the lizard, increases over time, further enhancing the
117 influence of ticks on lizard movement later in the season. To test these predictions, we followed
118 the movement behaviour of 55 adult sleepy lizards using GPS tracking devices and
119 simultaneously quantified their naturally occurring tick loads on a fortnightly basis. We then
120 built a multivariate statistical model that incorporated tick-host relationships known from
121 previous studies in this species (and which we detail below) to address these predictions.
122
123
124 Methods
125 Study site
126 This study was conducted in a 1.5km2 study site near Bundy Bore station in South Australia’s
127 mid-north (33°54’16”S, 139°20’43”E) (Figure 1(A)). This semi-arid region receives an average
128 annual rainfall of about 250 mm (Bull and Baghurst 1998) and its vegetation consists primarily
129 of chenopod shrubland (Bull and Pamula 1998; Leu et al. 2011a). Average monthly high
130 temperatures in winter are ~15 oC and in summer ~32 oC. Winter temperatures regularly drop
131 below 10 oC and summer temperatures regularly climb above 40 oC. In 2009, when our study
132 was conducted, monthly winter and summer temperatures were above average, but annual
133 rainfall equal to the average for the region.
134
135 Host parasite system
136 The host species, the sleepy lizard is a large scincid lizard, with adult snout to vent lengths of up
137 to 350 mm and body mass of up to 1000 g (Bull and Pamula 1996). Adult lizards maintain stable
138 home ranges of approximately 4 ha, with little spatial shift over time (Bull 1995; Bull and
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139 Baghurst 1998; Bull and Freake 1999; Kerr and Bull 2006a). Lizards in the focal population use
140 bushes (Maireana sedifolia, and other species), coarse woody or human (corrugated iron sheets)
141 debris, wombat and rabbit warrens as overnight refuges and to avoid adverse weather conditions
142 (Kerr et al. 2003; Leu et al. 2011a).
143
144 At our study site, the sleepy lizard is parasitised by two ectoparasitic tick species, Amblyomma
145 limbatum Neumann, 1899 and Bothriocroton hydrosauri Denny, 1843 (Figure 1(C)). Both tick
146 species are three host ticks, with each life stage, larvae, nymphs and adults, requiring a host
147 individual. All life stages (except adult males) engorge with blood and or lymph while they are
148 attached to their host (Bull and Sharrad 1980). When ticks are fully engorged they detach from
149 their hosts, mostly in the lizards refuges, to moult into the next life stage (Petney et al. 1983;
150 Chilton and Bull 1993b; Kerr and Bull 2006b). Favourable environmental conditions in these
151 host refuges reduce the risks of desiccation for both tick species (Bull et al. 1988; Chilton and
152 Bull 1993a, b). Larvae and nymphs take some time to moult (8-72 days depending on
153 temperature and relative humidity) into the next life stage, during which they are not infectious,
154 before attaching to the next host individual (Chilton et al. 2000). Both tick species rely on host
155 movement and their reuse of refuges to attach to subsequent hosts and do not actively seek out
156 hosts (Petney et al. 1983). Subsequent hosts may be the same or different individuals that use the
157 same refuge. Sleepy lizards repeatedly use a set of overnight refuges, where ticks are transmitted.
158 Furthermore, Leu et al. (2010b) and Wohlfiel et al. (2013) showed that transmission networks
159 based on asynchronous refuge sharing among neighbours predicts individual tick load.
160
161 Movement and tick infestation
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162 We captured most of the resident adult lizards (29 males and 26 females) in our study site, and
163 observed their movement throughout the main activity period (Bull and Baghurst 1998),
164 September 2009 – January 2010. We attached a data logger to the dorsal surface of each lizard’s
165 tail using surgical adhesive tape (Leu et al. 2010b) (Figure 1(B)). Data loggers included a GPS
166 unit to record lizard movement, a radio transmitter to allow the recapture of lizards and regular
167 tick counts, and a step counter. GPS locations were recorded every 10 mins when lizards were
168 active and moving, that is when they took at least one step in the previous 10 min. The GPS
169 devices had a median horizontal accuracy of +/- 6m (Leu et al. 2010a). Each data logger (GPS,
170 radio transmitter and step counter units) weighed 37 g, representing 4.9 % of an average 750 g
171 adult lizard body mass. Based on the GPS data, we calculated for each individual, the total
172 distance moved per day (sum of all distances between consecutive locations on that day) and
173 subsequently for each lizard the mean daily distance moved per fortnight (Figure 1(D)). Sleepy
174 lizard movement has previously been quantified by a number of different measures, including
175 steps taken per day (Leu and Bull 2016); daily activity (total number of 10 min intervals during
176 which lizards were recorded active divided by the number of days observed) and daily distance
177 moved (total distance moved in metres divided by the number of days observed) (Leu et al.
178 2016a); movement activity (distance between consecutive GPS locations) and duration (Leu et
179 al. 2011b); and cotton spooling, sprint speed, endurance, active/inactive behaviour (Main and
180 Bull 2000), all of which measure different aspects of lizard activity. Here our focus was on the
181 mean daily distance moved by lizards on active days, similar to previous studies (Leu et al.
182 2016a), hence we excluded days on which lizards did not move, i.e. either no steps were taken
183 and hence no GPS locations were recorded, or the total daily distance travelled was 0 m.
184
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185 Individual lizards could be identified by their unique radio transmitter frequency. We recaptured
186 lizards once every fortnight to record tick loads (number, species and life stage), take
187 morphological measurements and download GPS data. Lizard handling periods (a standard two
188 hour period) were excluded from the GPS data, and lizards released at their point of capture.
189 Handling periods accounted for the period of time lizards were actively handled (~30 mins) and
190 the period of time over which lizard movement was expected to be impacted as a consequence of
191 handling (~1 hour (Kerr et al. 2004)). Larvae, nymphs and adult females have an increasing
192 impact on the hosts because they draw increasing amounts of blood and lymph. Males do not
193 engorge with blood. Following Main (1999), we quantified the differential impact of each life
194 stage and converted each lizard’s fortnightly tick load to a larvae equivalent index. One nymph
195 equalled ten larvae, one adult female equalled 250 larvae, and one adult male equalled one larva
196 (Main 1999). Fortnightly morphological measurements included lizard mass (to the nearest 5 g),
197 and snout-vent length (to the nearest 5 mm). We log transformed these fortnightly morphological
198 measures and used them in a mass on snout-vent length linear regression. We then used the
199 unstandardized residuals from this regression analysis as a measure of each lizard’s fortnightly
200 body condition (Moore et al. 2009). These morphological measures were regressed in one
201 analysis including all lizards and all fortnights, as this provided a better perspective of body
202 condition across the activity season and population.
203
204 The first time lizards were captured we also determined each individual’s sex by assessing head
205 morphology, males have substantially longer jaws and broader heads than females (Bull and
206 Pamula 1996). Male sex was confirmed by gently everting their hemipenes where possible.
207
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208 After the study we removed all data loggers and released all lizards. We observed no damage or
209 irritation to the skin where data loggers were attached and lizards naturally shed their skin in the
210 following months. All lizards were treated using procedures formally approved by the Flinders
211 University Animal Welfare Committee in compliance with the Australian Code of Practice for
212 the Use of Animals for Scientific Purposes and conducted under the South Australian
213 Department of Environment and Natural Resources Permit to Undertake Scientific Research.
214
215 Model construction
216 We constructed our multivariate statistical model informed by previous knowledge of the
217 ecology of the sleepy lizard and its ecto-parasitic ticks as well as their host-parasite relationship.
218 This allowed us to investigate the effects of ticks on lizard movement above and beyond effects
219 of other factors that are known to affect movement. For each fortnight, we calculated the mean
220 daily distance travelled by each lizard, which was our dependent variable. This variable was
221 square root transformed to meet model assumptions (normality, homoscedasticity). Then, to test
222 our first prediction we included total larvae equivalent as a measure of tick load and as one of
223 our independent variables into the model.
224
225 Lizard movement activity first increases, then decreases over the course of the season (Firth and
226 Belan 1998; Kerr and Bull 2006c). At the beginning and end of the activity season lizard
227 movement is low due to cool ambient temperatures and low food resources, respectively. We
228 accounted for this non-linear relationship by including a time variable, fortnight, and fortnight2
229 into our model (both continuous). Lizard sex was included as a fixed categorical factor, because
230 male sleepy lizards have been demonstrated to have higher levels of movement activity than
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231 females (Leu et al. 2011b). Movement activity also varies with body condition (Leu and Bull
232 2016), which we included in our model. We also included a random intercept and slope for each
233 individual, (fortnight | lizard id), to account for individual differences in movement activity
234 (intercept), as well as individual differences in movement change over time (slope).
235
236 In the sleepy lizard, tick load is known to vary with body condition (Bull and Burzacott 1993),
237 and hence we included the interaction term total larvae equivalent x body condition to test our
238 second prediction that the impact of ticks on lizard movement increases with decreasing host
239 condition. Lastly, we included the interaction term total larvae equivalent x fortnight to test our
240 third prediction that lizard movement is more strongly affected late in the season because tick
241 abundance in the environment and hence tick load on the lizard increases over time. All
242 continuous independent variables were centred and scaled to allow us to determine their
243 importance relative to one another in the statistical model. We used the “vif.mer” function (Frank
244 2011) to check for collinearity using variance inflation factors (VIFs), which were generally very
245 low (< 1.07) and below a pre-selected threshold (Zuur et al. (2010) suggest a cut-off of 3). As
246 expected, VIFs were higher for fortnight (20.33) and fortnight2 (20.36), due to the polynomial
247 structure of the model, with a clear relationship between the two variables.
248
249 Our final model was as follows:
250 √mean daily distance = sex + fortnight + fortnight2 + total larvae equivalent + body condition +
251 total larvae equivalent x body condition + total larvae equivalent x fortnight + (fortnight | lizard
252 id)
253
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254 All statistical analyses and data manipulation was conducted in IMB SPSS Statistics 22 (Corp
255 2013), or R (R Core Team 2016), using mostly lme4 (Bates et al. 2015), lmerTest (Kuznetsova et
256 al. 2016), and ggplot2 (Wickham 2009) to produce graphs.
257
258
259 Results
260 Over the duration of this study, the mean number of location records per lizard was 1728 (95%
261 CI 1617-1838), with lizards monitored for a mean of 5.42 (95% CI 5.08-5.8) fortnights over the
262 duration of the season. On average lizards moved a mean daily distance of 215 m (95% CI 203-
263 228m) in a given fortnight over the duration of the season. Mean daily distance moved in a given
264 fortnight ranged from 3-745m/day. Lizard tick loads varied by fortnight, ranging from 0-801
265 larval units, with a mean of 64 (95% CI 47-81).
266
267 We found no evidence to support any of our three predictions on tick load effects; tick load did
268 not affect lizard movement; the effect of tick load on lizard movement was not host condition
269 dependent; and the effect of tick load on lizard movement did not depend on the time in the
270 lizard activity season (Table 1). Our model accounted for lizard ID and fortnight as random
271 effects (intercept and slope (fortnight | lizard id)). Lizard ID explained twice as much of the
272 variance in the intercept than fortnight in the slope (0.15 and 0.08, respectively), suggesting
273 lizards differed from each other more strongly (intercept) than their observed temporal variation
274 (slope) over the duration of the season. Consistent with previous studies, lizard movement varied
275 over the course of the activity season (Table 1). Fortnight had a positive effect, and fortnight2 a
276 negative effect, implying lower movement at the start of the season and that lizards also walked
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277 less as the season progressed. Lizard movement increased with body condition (Table 1). Female
278 lizards additionally moved shorter mean distances per day than males (Table 1 and Figure 2).
279 Interaction effects included in the model were not significant (Table 1).
280
281
282 Discussion
283 Summary of main result
284 Our study is based on a rich dataset using GPS data loggers attached to lizards which recorded
285 host movement in greater detail than previous studies investigating similar questions, and
286 combining this with repeated measures of lizard tick loads. In contrast to our predictions, we
287 found no evidence that tick load negatively affected lizard travel distance, and the effect of tick
288 load was not dependent on host condition or the time in the lizard activity season. Our
289 interpretation of this results is that lizards have adapted to the natural level of tick infection, and
290 that the average intensity (number of individual ticks on a given lizard) of ticks is too low to
291 have a measurable effect on movement patterns. Chronic stress is known to negatively impact
292 immune system function (Dhabhar 2014). Consequently, we predicted that lizard vigour
293 (movement) is more strongly affected during periods of chronic stress, for example at low body
294 conditions or high tick loads, which may occur later in the season due to harsh environmental
295 conditions, poorer quality food resources and increased tick abundance in the environment.
296 However, we found no evidence for these predictions. A possible explanation for the lack of tick
297 effects shown in our study could be that both ticks and lizards are affected by environmental
298 conditions in a similar manner (both negatively affected by harsh and positively affected by good
299 environmental conditions). For example, increased temperature and decreased humidity shortens
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300 the time to desiccation for ticks and decreases tick survival when waiting for the next host (Bull
301 et al. 1988; Chilton and Bull 1993a, b). Similarly, temperature and humidity have been shown to
302 influence sleepy lizard activity and movement (Firth and Belan 1998; Kerr and Bull 2006c).
303
304 Comparison with earlier findings from the sleepy lizard – tick model system
305 Our results, demonstrating no impact of ticks on the movement activity of lizard hosts, contrast
306 previous work by Main and Bull (2000) who experimentally manipulated lizard tick load in the
307 field and laboratory, and monitored lizard movements and activity levels. The conclusion of their
308 study was that ticks reduced the daily distance lizards moved, home range size, endurance and
309 sprint speed, and altered basking/active behaviour. However, these effects could not be
310 consistently identified across study sites, lizard age classes, or years (Main and Bull 2000). We
311 argue that increasing tick loads beyond natural levels may increase the level of stress
312 experienced by lizards in a similar manner to a reduction in body condition and food resource
313 availability, as ticks consume host resources. Thus, although the results of Main and Bull (2000)
314 are not consistent with ours or across seasons and sites in their study, their conclusions conform
315 to our original predictions. Whilst the work by Main and Bull (2000) suggests that under some
316 circumstances ticks can impact on lizard movement, our results suggest that overall, under
317 natural conditions, this is not the case.
318
319 Parasite effects on movement in other systems
320 Several studies in other systems also found no effect of parasites on host movement (Hillegass et
321 al. 2010; Mayer et al. 2015; Nelson et al. 2015). For example, Mayer et al. (2015) found no
322 difference in swimming speed of adult keelback snakes (Tropidonophis mairi Jan, 1863) before
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323 and after the removal of the gastrointestinal nematode Tanqua anomala Linstow, 1904.
324 Similarly, Nelson et al. (2015) found no relationship between a range of movement measures
325 (distance travelled per minute, voluntary movements, movements towards prey items, sprint
326 speed and endurance) and lungworm (Rhabdias hylae Johnston and Simpson, 1942) infection in
327 multiple anuran species (Rhinella marina Linnaeus, 1758, Cyclorana Australis Gray, 1842,
328 Limnodynastes convexiusculus MacLeay, 1877 and Litoria nasuta Gray, 1842). The host-parasite
329 arms race clearly suggests that the effects of parasites on their hosts in natural systems are on a
330 scale from large to small (Dawkins and Krebs 1979). Consequently, studies reporting no impact
331 of parasites on hosts are important as they suggest that in some systems hosts have adapted to
332 natural levels of parasite infection (Mayer et al. 2015; Nelson et al. 2015), at least with regard to
333 the measure of interest.
334
335 Nevertheless there are studies which have clearly shown that parasites can reduce host
336 movements. For example, Garrido and Pérez-Mellado (2013) found haemogregarine blood
337 parasite infestation to reduce sprint speed in wild caught Lilford’s wall lizards (Podarcis lilfordi
338 Günther, 1874). They suggested that this is the result of the blood parasite reducing haemoglobin
339 concentrations and subsequently lowering the lizards’ capacity for oxygen transportation to
340 muscle tissues, thereby reducing sprint speed (Garrido and Pérez-Mellado 2013). In contrast,
341 there are also reports of parasites increasing host movement. Médoc and Beisel (2008) found that
342 acanthocephalan (Polymorphus minutus Goeze, 1782) infection increased both swimming speed
343 and distance covered at the beginning of an escape attempt (first 0.5 sec) in male amphipods
344 (Gammarus roeseli Gervais, 1835). They suggested that the acanthocephalan parasite
345 manipulates its host’s vigour to enhance its transmission to a suitable avian definitive host by
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346 increasing the ability of G. roeseli to avoid other crustacean predators (Médoc and Beisel 2008).
347 Together the relationships in these studies suggest that the effect of parasite infections on host
348 movement is largely dependent on the host-parasite system and type of movement/behaviour
349 being observed or measured.
350
351 Other drivers of sleepy lizard movement
352 Whilst tick load did not appear to impact movement activity in the sleepy lizard, we did identify
353 three other drivers of lizard movement. Lizard movement changed over the lizard activity season
354 (change over time) in a non-linear fashion. This is consistent with earlier findings (Kerr and Bull
355 2006c; Spiegel et al. 2015) and is driven by ambient conditions, predominately temperature
356 (Firth and Belan 1998) and food availability. Movement activity in the sleepy lizard increases
357 from the beginning of the active season, when nights are cold and lizards bask longer to reach
358 suitable body temperatures before they start moving. Following its peak, movement activity
359 decreases again towards the end of the activity season, as ambient temperatures become too hot
360 and food availability is scarce. Lizard sex was a second major driver of movement, with males
361 moving greater daily distances than females and covering larger home ranges (Spiegel et al.
362 accepted). Leu et al. (2011b) found similar differences between sexes and suggested that greater
363 male movement is due to males seeking extra pair matings and/or additional foraging
364 opportunities because costs of pair living are higher for males, or due to males investing more in
365 home range guarding activities such as patrolling it more or marking their home range more
366 frequently than females (Leu et al. 2016b; Sih et al. 2017). Thirdly, we showed movement to
367 increase with lizard body condition. Earlier studies suggested that lizard body condition and tick
368 loads are related (Bull and Burzacott 1993). Here, we included lizard body condition, tick load
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369 and their interaction in our model and did not find a significant interaction effect nor any
370 collinearity between these variables. Based on this, we were able to distinguish between the
371 effect of both factors and clearly identified body condition as a strong driver of movement in the
372 sleepy lizard. Whilst not demonstrated in our study, social interactions are also known to
373 influence behaviour and movement in the sleepy lizard, for example in monogamous lizard pairs,
374 where pair partners remain in close proximity for extended periods of time (Leu et al. 2015), or
375 in social networks, where individuals actively associate with or avoid individual neighbours (Leu
376 et al. 2010a; Spiegel et al. 2016). Ectoparasitic ticks also have the potential to influence the
377 relationship between social interaction and movement both directly, by changing host behaviours
378 such as the frequency of refuge reuse (Leu et al. 2010b), or indirectly by affecting how
379 conspecific lizards respond to infected individuals (Bull 1990).
380
381 Concluding remarks
382 Parasites are defined as having adverse impacts on their hosts. Nevertheless, several studies have
383 described exceptions to this (Mayer et al. 2015; Nelson et al. 2015; Taggart 2016; Taggart and
384 Schultz 2016). Here, we describe another exception in a lizard-tick host-parasite system which
385 extends our understanding of the complex relationships between hosts, parasites and the
386 environment by including detailed previous knowledge, frequently unavailable in other systems.
387 In this study, we chose a single index of vigour, however, it is possible that other aspects of the
388 lizards’ movement are impacted by tick loads, such as area covered or duration of activity, as
389 well as non-movement measures. The host-parasite arms race clearly predicts that some parasites
390 have little or no impact on their host while others have great impacts depending on the state of
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391 the arms race (Dawkins and Krebs 1979). This system is another example of a parasite having
392 little effect on its host.
393
394
395 Acknowledgments:
396 This research was supported by funds from the Australian Research Council. We thank Ron and
397 Leona Clark for allowing access to their land, Geoff Cottrell for maintaining the data loggers,
398 and Dale Burzacott for logistical support at the field site. We also extend our thanks to Jana
399 Bradley and Caroline Wohlfeil their tireless efforts collecting the data. O.S. was supported by the
400 Israeli Ministry of Science and Technology 'Shamir Postdoctoral Fellowship'.
401
402
403 References:
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565 White, A., Watt, A.D., Hails, R.S., and Hartley, S.E. 2000. Patterns of spread in insect-pathogen systems: 566 the importance of pathogen dispersal. Oikos, 89(1): 137-145.567 Wickham, H. 2009. ggplot2: Elegant graphics for data analysis. Springer-Verlag New York.568 Wohlfiel, C.K., Leu, S.T., Godfrey, S.S., and Bull, C.M. 2013. Testing the robustness of transmission 569 network models to predict ectoparasite loads. One lizard, two ticks and four years. Int. J. Parasitol: 570 Parasites and Wildlife, 2: 271-277.571 Zuur, A.F., Ieno, E.N., and Elphick, C.S. 2010. A protocol for data exploration to avoid common statistical 572 problems. Methods in Ecology and Evolution, 1(1): 3-14.573
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594 Table 1: Linear mixed model summary showing the effects of sleepy lizard (Tiliqua rugosa) sex,
595 body condition, tick load and time in the activity season on the average daily movement of
596 lizards.
597 SE = standard error
598 DF = degrees of freedom
Fixed-effects Estimate SE DF T-value P-valueInterceptMale 15.12 0.27 84.18 56.70 <0.001SexFemale -2.03 0.39 86.33 -5.22 <0.001Fortnight 6.93 0.86 283.19 8.09 <0.001Fortnight2 -7.66 0.86 217.16 -8.96 <0.001Total larvae equivalent -0.10 0.19 226.12 -0.54 0.590Body condition 0.87 0.19 194.89 4.45 <0.001Total larvae equivalent x body condition -0.08 0.25 282.65 -0.31 0.760Total larvae equivalent x fortnight 0.06 0.21 217.08 0.26 0.790
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618 Figure 1: Sleepy lizards (Tiliqua rugosa) and our study site: (A) the location of our study site in
619 South Australia; (B) adult sleepy lizard with GPS unit and radio transmitter taped to tail, note
620 permanent marker pen adjacent lizard for scale; (C) ticks attached to lizard; and (D) movement
621 tracks of a single tagged lizard over the duration of the activity season (green lines), showing
622 example of our dependent variable, the total daily distance moved (red line). Map source data
623 were provided by the Department of Environment, Water and Natural Resources.
624
625 Figure 2: Effect of lizard sex on the mean daily movement of male and female sleepy lizards
626 (Tiliqua rugosa).
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