Marmots do not consistently use their left eye to respond to an approaching threat but those that did fled sooner

Marmots do not consistently use their left eye to respond to an approaching threat but those that... In many vertebrates, the brain’s right hemisphere which is connected to the left visual field special- izes in the processing of information about threats while the left hemisphere which is connected to the right visual field specializes in the processing of information about conspecifics. This is referred to as hemispheric lateralization. But individuals that are too predictable in their response to preda- tors could have reduced survival and we may expect selection for somewhat unpredictable responses. We studied hemispheric lateralization in yellow-bellied marmots Marmota flaviventer,a social rodent that falls prey to a variety of terrestrial and aerial predators. We first asked if they have lateralized responses to a predatory threat. We then asked if the eye that they used to assess risk influenced their perceptions of risk. We recorded the direction marmots were initially looking and then walked toward them until they fled. We recorded the distance that they responded to our experimental approach by looking, the eye with which they looked at us, and the distance at which they fled (i.e., flight initiation distance; FID). We found that marmots had no eye preference with which they looked at an approaching threat. Furthermore, the population was not comprised of individuals that responded in consistent ways. However, we found that marmots that looked at the approaching person with their left eye had larger FIDs suggesting that risk assessment was influ- enced by the eye used to monitor the threat. These findings are consistent with selection to make prey less predictable for their predators, despite underlying lateralization. Key words: antipredator behavior, behavioral lateralization, flight initiation distance, yellow-bellied marmots. The left and right hemispheres of many vertebrate brains are special- of threatening stimuli (Shibasaki et al. 2014). Mice Mus musculus ized to carry out specific activities (Bisazza et al. 1998; Andrew use their right hemisphere to control observational fear learning 2002). In humans, much research has shown that the left hemisphere (Kim et al. 2012). But not all studies of lateralization find support is generally responsible for interpreting language and the right hemi- for it. For instance, about half the tested population of inbred mice sphere is generally responsible for alert responses (Andrew 2002). Mus molossinus and Mecyclothorax castaneus retrieved food with Hemispheric lateralization controlling the response to threats has their left hand while the other half retrieved food with their right been shown to be an ancestral trait found in a variety of mammals hand (Collins 1985) and several environmental/ecological factors including primates and rodents (Kim et al. 2012). For instance, (CO levels—Domenici et al. 2012; predation risk—Brown et al. Japanese monkeys Macaca fuscata, upon hearing an alarm call, 2004) may modify or eliminate lateralized responses in fishes. looked longer at a picture of a snake with their left eye, a finding The advantage of a lateralized brain is that it helps individuals that suggests right hemispheric dominance during visual processing perform tasks simultaneously (Rogers et al. 2004). For example, V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 lateralized eye use in chickens Gallus gallus permits them to forage experimental approach and measured the following distances (in with 1 eye and be alert to predators with the other eye (Rogers et al. meter): starting distance (first flag to initial position); alert distance (second flag to initial position); and FID (third flag to initial posi- 2004). However, the benefits of lateralization may not come with- tion). In addition, we recorded the number of other marmots within out costs (Chivers et al. 2017). For instance, if individuals respond 10 m of the focal subject, the escape substrate (dirt, stone, talus, in consistent and predictable ways by looking at their predators, low, or high vegetation), slope of the terrain over which the marmot predators can learn how they escape and capitalize on this predict- fled, and the distance to its escape burrow. ability (Vallortigara 2000). Hence, it is possible that eye preference To quantify lateralization, we first noted the closest eye to the varies across individuals within a population (Vallortigara 2000; observer at the start of the experimental approach and quantified Chivers et al. 2017) and, that at a population level, there may be no this as straight (looking with both eyes directly at observer), right evidence for lateralization in how a species responds to threats. (right eye toward observer), left (left eye toward observer), or away Animals perceive approaching humans as predators (Frid and (both eyes facing away from the observer). We recorded the eye Dill 2002) and by walking directly toward an animal, it is possible direction when the marmot alerted to us in the same way (straight, to elicit an antipredator response. Flight initiation distance (FID), right, left, or away). the distance between a predator and its prey at which the prey ini- tiates flight, is a widely used method to quantify risk assessment Statistical analyses (Cooper and Blumstein 2015). When approached by a potential To explain variation in looking direction when alerted, we fitted predator, the prey may change their posture and look toward the generalized linear mixed-effect models (GLMER) with a binomial approaching threat to monitor it. This alert response can be used to error structure, using the following R packages lme4 (Bates et al. study eye preference and hence hemispheric lateralization. 2017), lmerTest (Kuznetsova et al. 2016), and optimx (Nash and Although evidence for hemispheric lateralization has been Varadhan 2011). We used gplot2 (Wickham and Chang 2016)to studied in many species, there are relatively few studies of rodents plot residuals and predicted values. We focused on those marmots (Kim et al. 2012), especially in the field. However, we know that that either responded by looking left or right (5 adults for which we rodents have lateralized brain function (Glick et al. 1977). Thus, our were not certain of the eye directed at us were not analyzed). We aim was to study hemispheric lateralization in a free-living rodent. then modeled the direction they looked in response to our approach We focused on yellow-bellied marmots Marmota flaviventer that are (looking direction when alerted) as a function of their initial looking prey to a variety of terrestrial and aerial predators (Van Vuren direction (left, right, straight, or away) and sex (male or female). We 2001) and asked 2 related questions. First, when approached by a included a random effect of individual marmot because most mar- human, did marmots respond by looking at us with their left eye. mots were approached more than once. We tested for individual Second, did the eye with which they looked at us influence the dis- consistency by comparing a model with and without the random tance at which they fled. effect of individual with a likelihood ratio test and by fitting a model with only individual marmot as a fixed effect. We plotted residuals Materials and Methods versus predicted values and generated qq-plots to evaluate distribu- tional assumptions. Study site and subjects To study variation in FID, we fitted linear mixed-effects models Between 5 June 2017 and 23 July 2017, we measured responses of and modeled FID as a function of alert distance, the eye with which adult yellow-bellied marmots (2 years old) to an approaching they looked at us during the experimental approach, sex, and the human. We studied marmots in the upper East River Valley in and 2-way interactions between alert distance and sex and alert distance around the Rocky Mountain Biological Laboratory (RMBL; and looking direction. Again, marmot identity was included as a 38 77’N, 106 50’W) in Gothic, Colorado, the site of a long-term random effect, and we re-plotted residuals versus predicted values study (Blumstein 2013; Armitage 2014). All marmots are regularly and generated qq-plots to evaluate distributional assumptions. live-trapped and individually marked with ear tags, for permanent Because risk perception may be influenced by other factors, but identification, and we use fur dye to mark each individual with a because our sample size was somewhat limited and we did not wish unique dorsal mark that permits identification from afar (Armitage to over-fit the model by including them all at once, we systematically 1982). added distance to burrow, escape substrate (stone, dirt, talus, low vegetation, or high vegetation), and escape incline, along with their Quantifying lateralization using FID 2-way interaction with alert distance, to our basic linear model. We assumed that marmots treated humans as predators (Frid and Dill 2002) and studied lateralization while measuring FID Results (Blumstein et al. 2015). Observers were trained to approach mar- mots at a standardized velocity of 0.5 m/s (Blumstein et al. 2004; We conducted 104 flushes on 39 unique adults (mean 2.8; range 1–9 Runyan and Blumstein 2004; Petelle et al. 2013). If more than 1 flushes) that either looked left or right in response to our approach marmot was at a location, we focused on a single subject. (58 of these approaches generated a look with their left eye, 46 Once a subject was identified, we waited at least 10 min to approaches generated a look with their right eye). The random effect ensure it was in a relaxed state, which we defined as foraging, look- of identity explained no variation in looking direction when alerted ing, standing and looking, or lying down and looking, before we (Table 1; likelihood ratio test comparing a general linear model with approached it. We dropped flags at the location we started the the mixed effects model containing initial head position to a mixed experimental approach, the location where the marmot moved its effects model with only head position, P ¼ 0.666; the models with head and looked toward the approaching person, and the location sex and initial position were also not significantly different, where it fled by either walking or running to their burrow. We then P ¼ 0.424). We also found no effect of prior looking direction, or of walked to the location where the animal was when we began the the marmot’s sex on looking direction when alerted (Table 2). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Blumstein et al.  Marmot lateralization 3 Table 1. Generalized linear mixed-effect models fitted in R to explain variation in looking direction and to test for random effects of individ- ual marmot on lateralized eye use Description Model AIC Model with only random effect Looking direction  (1juid) 146.4 Mixed-effect model Looking direction  Initial head position þ sex þ (1juid) 149.7 Fixed-effect only model Looking direction  Initial head position 146.5 Fixed-effect only model Looking direction  Initial head position þ sex 148.3 Table 2. Results from linear mixed-effects model explaining varia- Table 3. Results of linear mixed-effects model explaining variation tion in looking direction in flight initiation distance as a function of eye use Variable Estimate (SE) zP-value Variable Estimate (SE) df P-value A) Intercept 0.0004 (0.517) 0.001 0.999 Intercept 3.812 (3.197) 38.48 0.240 Initial head (L) 1.065 (0.650) 1.638 0.101 Looking head (R) 3.997 (3.706) 78.56 0.284 Initial head (R) 0.039 (0.575) 0.067 0.947 Sex (M) 7.629 (5.434) 28.19 0.171 Initial head (S) 0.021 (0.850) 0.024 0.981 Alert distance 0.668 (0.057) 65.62 <2e16 Sex (M) 0.104 (0.533) 0.195 0.845 Looking head (R)  Alert distance 0.158 (0.072) 94.16 0.030 B) Intercept 0.035 (0.487) 0.072 0.942 Sex (M)  Alert distance 0.199 (0.097) 57.53 0.045 Initial head (L) 1.080 (0.647) 1.669 0.095 Main effects only are presented (N ¼ 104 on 39 unique individuals). Initial head (R) 0.039 (0.577) 0.067 0.947 Initial head (S) 0.002 (0.848) 0.002 0.998 lateralization is not fixed but can change based on environmental Initial direction includes: left (L), right (R), straight (S) or away (the reference pressures over development (e.g., Andrew 2002) and with changes category). The first mixed-effects model (A) included sex and initial head posi- in the environment (Chiandetti et al. 2005). Nonetheless, this lack tion. The second model (B) included only initial head position (N ¼ 104 on 39 of a visual bias is striking because many studies (Hook-Costigan and unique individuals for both models) Rogers 1998; Santi et al. 2002) have reported hemispheric lateraliza- tion of antipredator responses, even if it was for a subset of antipre- However, we found that for a given alert distance, marmots dator behaviors (Lippolis et al. 2002). that responded to an approaching person by looking at them with Although we found no lateralization in the eye used, we found a their left eye, fled at greater distances (Table 3, Figure 1), and we consequence of the eye marmots used to monitor the approaching found that for a given alert distance, males fled at a greater dis- human. Marmots that used their left eye to monitor an approaching tance than females (Table 3, Figure 2). The 3 covariates tested had threat presumably assessed a higher risk and fled sooner. And this significant interactions between alert distance and distance to bur- second finding suggests that marmots have lateralized antipredator row (P ¼ 0.029), escape substrate (P ¼ 0.008), and escape incline behavior. Taken together these results are striking because while we (P ¼ 0.021), but all models retained the significant interaction might expect selection against animals being too predictable in their between look direction and alert distance (P ¼ 0.004, 0.004, and escape behavior (Briffa 2013), we might expect that there is rela- 0.046, respectively). Furthermore, when added one at a time to tively less cost to predictably looking at a predator and relatively our basic model, there was an effect of social group size more cost to predictably escaping from it. Given that predators may (P ¼ 0.045), vegetation height (P ¼ 0.032), and the day of data col- learn any bias in how individual prey respond to their attacks and lection on FID (P ¼ 0.020) on FID. Thus, while other variables use this to their advantage, we expect strong selection on prey to explain some variation in FID, we can conclude that the eye with respond to predators in an unpredictable manner, which is consis- which marmots looked at the approaching human was always a tent with the nonsignificant repeatability. In marmots, it may be significant factor. that the costs of predictably using 1 specific eye outweigh the bene- fits and perhaps variation in the relative costs and benefits explains Discussion some of the variation in lateralization seen across species (Chivers et al. 2016, 2017). Male marmots fled at greater distances once alerted than did Yellow-bellied marmots at our study site are preyed upon by a females, but we found no support that marmots overall preferen- variety of predators, a finding that given the Brown et al. (2004) tially used their left eye to monitor approaching humans. Although results, made us expect that marmots should have lateralized eye it is possible that with a substantially larger data set we would have use. Marmots are preyed upon by a variety of terrestrial predators detected individual consistency in the eye marmots used to monitor (coyotes Canis latrans, badgers Taxidea taxus, American martens an approaching threat, we did not detect it in our data set that Martes americana, black bears Ursus americanus, and long-tailed included an average of 3 (and up to 9) repeated approaches on indi- viduals. It is also possible that our predator manipulation was insuf- weasels Mustela frenata, Van Vuren 2001), as well as aerial preda- ficiently risky to generate the expected lateralized response. Levels tors (golden eagles Aguila chrysaetos, red-tailed hawks Buteo jamai- censis, Swainson’s hawks Buteo swainsoni, and goshawks Accipiter of predator exposure influence lateralization in fishes, where indi- viduals with the greatest risk of predation exhibited the most lateral- gentilis, Van Vuren 2001). It is possible that vulnerability to a vari- ized behavior (Heuts 1999; Ferrari et al. 2015; Chivers et al. 2017; ety of different and presumably cognitively sophisticated predators Lucon-Xiccato et al. 2017) and populations with very low predation has increased the cost of marmots responding predictably with 1 eye risk may lose lateralized eye use (Brown et al. 2004). Thus, and hence has selected for unpredictable eye use. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Figure 1. Relationship between alert distance and FID as a function of eye used when looking at approaching human. The plus sign indicates the right eye and dots the left eye. For any given distance, individuals monitoring approach with their right eye (thick line) had a shorter FID than those who monitored approach with their left eye (thin line). processing of risk-related stimuli. Therefore, when the right eye was used for risk assessment we expected that marmots would tolerate closer approaches. Our results suggest that more information on the relative costs of the looking with each eye is warranted. Do marmots respond the same way to humans as they do their more “natural” predators? Are occasions when marmots look with their right eye and tolerate closer approaches more likely to end in a costly escape? And, the broader question of whether individuals are less likely to have later- alized antipredator responses when they deal with cognitively sophisticated predators remains to be determined. 0 20 40 60 80 100 120 140 Alert Distance (m) Acknowledgments Figure 2. Relationship between alert distance and FID as a function of sex. We thank 2017 Team Marmot for logistical help in the field: Gabriela Pinho, Triangles indicate females and dots indicate males. For any given alert dis- Dana Williams, Sarah Heissenberger, Jazmine Uy, Gina Johnson, and tance, females (thick line) tolerated closer approach compared with males Madeline Standen. We thank 2 anonymous reviewers and the editor for a set (thin line). of astute comments that have helped us improve the paper. Studies in other taxa have reported that predictable prey may be more vulnerable to predation. For instance, proactive jumping spi- Funding ders Portia labiate captured more prey that responded predictably than unpredictable prey while docile spiders captured more unpre- D.T.B. was supported by the National Science Foundation (grant 1557130). dictable prey (Chang et al. 2017). Furthermore, hermit crabs A.D. was an NSF REU fellow supported by DBI 1226713 (to the Rocky Mountain Biological Laboratory). L.Y. was supported by China Scholarship Paguroidea bernhardus that fled in response to a predator Carcinus Counsel and Peking University. maenas had unpredictable re-emergence times, a finding consistent with this random response being an antipredator adaptation (Briffa 2013). Such unpredictable behavior may be the best method against References predators that are able to learn sequential patterns in their prey Andrew R, 2002. Development of lateralization. In: Rogers LJ, Andrew RJ, (Bednekoff and Lima 2002). editors. Comparative Vertebrate Lateralization. Oxford: Oxford University Despite marmots responding unpredictably to an approaching Press, 157–205. predator, our results are also consistent with hemispheric lateraliza- Armitage KB, 1982. Yellow-bellied marmot. In: Davis DE, editor. CRC tion of marmots’ escape behavior. The eye marmots used to monitor Handbook of Census Methods for Terrestrial Vertebrates. Boca Raton (FL): an approaching predator was associated with the distance at which CRC Press, Inc, 148–149. they fled the approaching predator. Because lateralized eye use Armitage KB, 2014. Marmot Biology: Sociality, Individual Fitness, and seems to be an ancestral and wide spread trait for risk perception in Population Dynamics. Cambridge (NY): Cambridge University Press. vertebrates (fishes—Bisazza et al. 1998; birds—Andrew 2002; Bates D, Maechler M, Bolker B, Walker S, 2017. Lme4: linear mixed-effects rodents—Kim et al. 2012; and primates—Shibasaki et al. 2014), we models using ‘eigen’ and S4. R Package Version 1.1-13 [cited 2017 July 1]. expected to see a greater FID when the left eye monitored approach Available from: https://github.com/lme4/lme4/ http://lme4.r-forge.r-project. because this was the eye that was associated with right hemispheric org/. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Flight Iniaon Distance (m) Blumstein et al.  Marmot lateralization 5 Bednekoff PA, Lima SL, 2002. Why are scanning patterns so variable? An Frid A, Dill LM, 2002. Human-caused disturbance stimuli as a form of preda- overlooked question in the study of anti-predator vigilance. J Avian Biol 33: tion risk. Conserv Ecol 6:11. [cited 2017 July 1] Available from: http:// 143–149. www.consecol.org/vol6/iss1/art11. Bisazza A, Rogers LR, Vallortigara G, 1998. The origins of cerebral asymme- Glick SD, Zimmerberg B, Jerussi TP, 1977. Adaptive significance of laterality try: a review of evidence of behavioural and brain lateralization in fishes, in the rodent. Ann NY Acad Sci 299:180–185. reptiles and amphibians. Neurosci Biobehav Rev 22:411–426. Heuts BA, 1999. Lateralization of trunk muscle volume, and lateralization of Blumstein DT, 2013. Yellow-bellied marmots: insights from an emergent view swimming turns of fish responding to external stimuli. Behav Proc 47: of sociality. Phil Trans R Soc Lond B 368:20120349. 113–124. Blumstein DT, Flores G, Munoz NE, 2015. Does locomotor ability influence Hook-Costigan MA, Rogers LJ, 1998. Lateralized use of the mouth in produc- flight initiation distance in yellow-bellied marmots? Ethology 121:434–441. tion of vocalizations by marmosets. Neuropsychologia 36:1265–1273. Blumstein DT, Runyun A, Seymour M, Nicodemus A, Ozgul A et al., 2004. Kim S, Matyas F, Lee S, Acsady L, Shin H, 2012. Lateralization of observatio- Locomotor ability and wariness in yellow-bellied marmots. Ethology 110: nal fear learning at the cortical but not thalamic level in mice. Proc Natl 615–634. Acad Sci USA 109:15497–15501. Briffa M, 2013. Plastic proteans: reduced predictability in the face of predation Kuznetsova A, Brocknoff PB, Christensen BRH, 2016. lmerTest in linear risk in hermit crabs. Biol Lett 9:2013592. mixed effects models. R package version 3.3.3 [cited 2017 July 1]. Available Brown C, Gardner C, Braithwaite VA, 2004. Population variation in lateral- from: https://CRAN.Rproject.org/package¼lmerTest. ized eye use in the pociliid Brachyraphis episcopi. Proc R Soc Lond B Lippolis G, Bisazza A, Rogers L, Vallortigara G, 2002. Lateralisation of 271(Suppl):S455–S457. predator avoidance responses in three species of toads. Laterality 7: Chang C, Teo HY, Norma-Rashid Y, Li D, 2017. Predator personality and 163–183. prey behavioural predictability jointly determine foraging performance. Sci Lucon-Xiccato T, Chivers DP, Mitchell MD, Ferrari MCO, 2017. Prenatal Rep 7:40734. exposure to predation affects predator recognition learning via lateraliza- Chiandetti C, Regolin L, Rogers LJ, Vallortigara G, 2005. Effect of light stim- tion plasticity. Behav Ecol 28:253–259. ulation of embryos on the use of position-specific and object-specific cues in Nash JC, Varadhan R, 2011. Unifying optimization algorithms to aid software binocular and monocular domestic chicks Gallus gallus. Behav Brain Res system users: optimx for R. J Stat Softw 43:1–14. 163:10–17. Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT, 2013. Chivers DP, McCormick MI, Allan BJM, Mitchell MD, Gonc¸alves EJ et al., Development in boldness and docility in yellow-bellied marmots. Anim 2016. At odds with the group: changes in lateralization and escape per- Behav 86:1147–1154. formance reveal conformity and conflict in fish schools. Proc R Soc B Rogers LJ, Zucca P, Vallortigara G, 2004. Advantages to having a lateralized 283:1127. brain. Proc R Soc B 217: S420–S422. Chivers DP, McCormick MI, Warren DT, Allen BJ, Ramasamy RA et al., Runyan AM, Blumstein DT, 2004. Do individual differences influence flight 2017. Competitive superiority versus predation savvy: the two sides of initiation distances? J Wildl Manag 68:1124–1129. behavioural lateralization. Anim Behav 130:9–15. Santi A, Bisazza A, Vallortigara G, 2002. Complementary left and right eye Collins RL, 1985. On the inheritance of direction and degree of asymmetry. use during predator inspection and shoal-mate scrutiny in minnows. J Fish In: Glick SD, editor. Cerebral Lateralization in Nonhuman Species. New Biol 60:1116–1125. York (NY): Academic Press, 41–69. Shibasaki M, Nagumo S, Koda H, 2014. Japanese monkeys Macaca fuscata Cooper WE Jr, Blumstein DT, 2015. Escape behavior: importance, scope, and spontaneously associate alarm calls with snakes appearing in the left visual variables. In: Cooper WE Jr, Blumstein DT, editors. Escaping from field. J Comp Psych 128:332–335. Predators: An Integrative View of Escape Decisions. Cambridge (UK): Vallortigara G, 2000. Comparative neuropsychology of the dual brain: a stroll Cambridge University Press, 3–12. through animals’ left and right perceptual worlds. Brain Lang 73:189–219. Domenici P, Allan B, McCormick MI, Munday PL, 2012. Elevated carbon Van Vuren DH, 2001. Predation on yellow-bellied marmots Marmota flavi- dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8: ventris. Am Midl Nat 145:94–100. 78–81. Wickham H, Chang W, 2016. ggplot2: create elegant data visualisations using Ferrari MCO, McCormick MI, Allan BJM, Choi RB, Ramasamy RA et al., the grammar of graphics. R Package Version 2.2.1 [cited 2017 July 1]. 2015. The effect of background risk on behavioural lateralization in a coral Available from: http://ggplot2.tidyverse.org, https://github.com/tidyverse/ reef fish. Funct Ecol 29:1553–1559. ggplot2. 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Marmots do not consistently use their left eye to respond to an approaching threat but those that did fled sooner

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Abstract

In many vertebrates, the brain’s right hemisphere which is connected to the left visual field special- izes in the processing of information about threats while the left hemisphere which is connected to the right visual field specializes in the processing of information about conspecifics. This is referred to as hemispheric lateralization. But individuals that are too predictable in their response to preda- tors could have reduced survival and we may expect selection for somewhat unpredictable responses. We studied hemispheric lateralization in yellow-bellied marmots Marmota flaviventer,a social rodent that falls prey to a variety of terrestrial and aerial predators. We first asked if they have lateralized responses to a predatory threat. We then asked if the eye that they used to assess risk influenced their perceptions of risk. We recorded the direction marmots were initially looking and then walked toward them until they fled. We recorded the distance that they responded to our experimental approach by looking, the eye with which they looked at us, and the distance at which they fled (i.e., flight initiation distance; FID). We found that marmots had no eye preference with which they looked at an approaching threat. Furthermore, the population was not comprised of individuals that responded in consistent ways. However, we found that marmots that looked at the approaching person with their left eye had larger FIDs suggesting that risk assessment was influ- enced by the eye used to monitor the threat. These findings are consistent with selection to make prey less predictable for their predators, despite underlying lateralization. Key words: antipredator behavior, behavioral lateralization, flight initiation distance, yellow-bellied marmots. The left and right hemispheres of many vertebrate brains are special- of threatening stimuli (Shibasaki et al. 2014). Mice Mus musculus ized to carry out specific activities (Bisazza et al. 1998; Andrew use their right hemisphere to control observational fear learning 2002). In humans, much research has shown that the left hemisphere (Kim et al. 2012). But not all studies of lateralization find support is generally responsible for interpreting language and the right hemi- for it. For instance, about half the tested population of inbred mice sphere is generally responsible for alert responses (Andrew 2002). Mus molossinus and Mecyclothorax castaneus retrieved food with Hemispheric lateralization controlling the response to threats has their left hand while the other half retrieved food with their right been shown to be an ancestral trait found in a variety of mammals hand (Collins 1985) and several environmental/ecological factors including primates and rodents (Kim et al. 2012). For instance, (CO levels—Domenici et al. 2012; predation risk—Brown et al. Japanese monkeys Macaca fuscata, upon hearing an alarm call, 2004) may modify or eliminate lateralized responses in fishes. looked longer at a picture of a snake with their left eye, a finding The advantage of a lateralized brain is that it helps individuals that suggests right hemispheric dominance during visual processing perform tasks simultaneously (Rogers et al. 2004). For example, V C The Author(s) (2018). Published by Oxford University Press. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 2 Current Zoology, 2018, Vol. 0, No. 0 lateralized eye use in chickens Gallus gallus permits them to forage experimental approach and measured the following distances (in with 1 eye and be alert to predators with the other eye (Rogers et al. meter): starting distance (first flag to initial position); alert distance (second flag to initial position); and FID (third flag to initial posi- 2004). However, the benefits of lateralization may not come with- tion). In addition, we recorded the number of other marmots within out costs (Chivers et al. 2017). For instance, if individuals respond 10 m of the focal subject, the escape substrate (dirt, stone, talus, in consistent and predictable ways by looking at their predators, low, or high vegetation), slope of the terrain over which the marmot predators can learn how they escape and capitalize on this predict- fled, and the distance to its escape burrow. ability (Vallortigara 2000). Hence, it is possible that eye preference To quantify lateralization, we first noted the closest eye to the varies across individuals within a population (Vallortigara 2000; observer at the start of the experimental approach and quantified Chivers et al. 2017) and, that at a population level, there may be no this as straight (looking with both eyes directly at observer), right evidence for lateralization in how a species responds to threats. (right eye toward observer), left (left eye toward observer), or away Animals perceive approaching humans as predators (Frid and (both eyes facing away from the observer). We recorded the eye Dill 2002) and by walking directly toward an animal, it is possible direction when the marmot alerted to us in the same way (straight, to elicit an antipredator response. Flight initiation distance (FID), right, left, or away). the distance between a predator and its prey at which the prey ini- tiates flight, is a widely used method to quantify risk assessment Statistical analyses (Cooper and Blumstein 2015). When approached by a potential To explain variation in looking direction when alerted, we fitted predator, the prey may change their posture and look toward the generalized linear mixed-effect models (GLMER) with a binomial approaching threat to monitor it. This alert response can be used to error structure, using the following R packages lme4 (Bates et al. study eye preference and hence hemispheric lateralization. 2017), lmerTest (Kuznetsova et al. 2016), and optimx (Nash and Although evidence for hemispheric lateralization has been Varadhan 2011). We used gplot2 (Wickham and Chang 2016)to studied in many species, there are relatively few studies of rodents plot residuals and predicted values. We focused on those marmots (Kim et al. 2012), especially in the field. However, we know that that either responded by looking left or right (5 adults for which we rodents have lateralized brain function (Glick et al. 1977). Thus, our were not certain of the eye directed at us were not analyzed). We aim was to study hemispheric lateralization in a free-living rodent. then modeled the direction they looked in response to our approach We focused on yellow-bellied marmots Marmota flaviventer that are (looking direction when alerted) as a function of their initial looking prey to a variety of terrestrial and aerial predators (Van Vuren direction (left, right, straight, or away) and sex (male or female). We 2001) and asked 2 related questions. First, when approached by a included a random effect of individual marmot because most mar- human, did marmots respond by looking at us with their left eye. mots were approached more than once. We tested for individual Second, did the eye with which they looked at us influence the dis- consistency by comparing a model with and without the random tance at which they fled. effect of individual with a likelihood ratio test and by fitting a model with only individual marmot as a fixed effect. We plotted residuals Materials and Methods versus predicted values and generated qq-plots to evaluate distribu- tional assumptions. Study site and subjects To study variation in FID, we fitted linear mixed-effects models Between 5 June 2017 and 23 July 2017, we measured responses of and modeled FID as a function of alert distance, the eye with which adult yellow-bellied marmots (2 years old) to an approaching they looked at us during the experimental approach, sex, and the human. We studied marmots in the upper East River Valley in and 2-way interactions between alert distance and sex and alert distance around the Rocky Mountain Biological Laboratory (RMBL; and looking direction. Again, marmot identity was included as a 38 77’N, 106 50’W) in Gothic, Colorado, the site of a long-term random effect, and we re-plotted residuals versus predicted values study (Blumstein 2013; Armitage 2014). All marmots are regularly and generated qq-plots to evaluate distributional assumptions. live-trapped and individually marked with ear tags, for permanent Because risk perception may be influenced by other factors, but identification, and we use fur dye to mark each individual with a because our sample size was somewhat limited and we did not wish unique dorsal mark that permits identification from afar (Armitage to over-fit the model by including them all at once, we systematically 1982). added distance to burrow, escape substrate (stone, dirt, talus, low vegetation, or high vegetation), and escape incline, along with their Quantifying lateralization using FID 2-way interaction with alert distance, to our basic linear model. We assumed that marmots treated humans as predators (Frid and Dill 2002) and studied lateralization while measuring FID Results (Blumstein et al. 2015). Observers were trained to approach mar- mots at a standardized velocity of 0.5 m/s (Blumstein et al. 2004; We conducted 104 flushes on 39 unique adults (mean 2.8; range 1–9 Runyan and Blumstein 2004; Petelle et al. 2013). If more than 1 flushes) that either looked left or right in response to our approach marmot was at a location, we focused on a single subject. (58 of these approaches generated a look with their left eye, 46 Once a subject was identified, we waited at least 10 min to approaches generated a look with their right eye). The random effect ensure it was in a relaxed state, which we defined as foraging, look- of identity explained no variation in looking direction when alerted ing, standing and looking, or lying down and looking, before we (Table 1; likelihood ratio test comparing a general linear model with approached it. We dropped flags at the location we started the the mixed effects model containing initial head position to a mixed experimental approach, the location where the marmot moved its effects model with only head position, P ¼ 0.666; the models with head and looked toward the approaching person, and the location sex and initial position were also not significantly different, where it fled by either walking or running to their burrow. We then P ¼ 0.424). We also found no effect of prior looking direction, or of walked to the location where the animal was when we began the the marmot’s sex on looking direction when alerted (Table 2). Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Blumstein et al.  Marmot lateralization 3 Table 1. Generalized linear mixed-effect models fitted in R to explain variation in looking direction and to test for random effects of individ- ual marmot on lateralized eye use Description Model AIC Model with only random effect Looking direction  (1juid) 146.4 Mixed-effect model Looking direction  Initial head position þ sex þ (1juid) 149.7 Fixed-effect only model Looking direction  Initial head position 146.5 Fixed-effect only model Looking direction  Initial head position þ sex 148.3 Table 2. Results from linear mixed-effects model explaining varia- Table 3. Results of linear mixed-effects model explaining variation tion in looking direction in flight initiation distance as a function of eye use Variable Estimate (SE) zP-value Variable Estimate (SE) df P-value A) Intercept 0.0004 (0.517) 0.001 0.999 Intercept 3.812 (3.197) 38.48 0.240 Initial head (L) 1.065 (0.650) 1.638 0.101 Looking head (R) 3.997 (3.706) 78.56 0.284 Initial head (R) 0.039 (0.575) 0.067 0.947 Sex (M) 7.629 (5.434) 28.19 0.171 Initial head (S) 0.021 (0.850) 0.024 0.981 Alert distance 0.668 (0.057) 65.62 <2e16 Sex (M) 0.104 (0.533) 0.195 0.845 Looking head (R)  Alert distance 0.158 (0.072) 94.16 0.030 B) Intercept 0.035 (0.487) 0.072 0.942 Sex (M)  Alert distance 0.199 (0.097) 57.53 0.045 Initial head (L) 1.080 (0.647) 1.669 0.095 Main effects only are presented (N ¼ 104 on 39 unique individuals). Initial head (R) 0.039 (0.577) 0.067 0.947 Initial head (S) 0.002 (0.848) 0.002 0.998 lateralization is not fixed but can change based on environmental Initial direction includes: left (L), right (R), straight (S) or away (the reference pressures over development (e.g., Andrew 2002) and with changes category). The first mixed-effects model (A) included sex and initial head posi- in the environment (Chiandetti et al. 2005). Nonetheless, this lack tion. The second model (B) included only initial head position (N ¼ 104 on 39 of a visual bias is striking because many studies (Hook-Costigan and unique individuals for both models) Rogers 1998; Santi et al. 2002) have reported hemispheric lateraliza- tion of antipredator responses, even if it was for a subset of antipre- However, we found that for a given alert distance, marmots dator behaviors (Lippolis et al. 2002). that responded to an approaching person by looking at them with Although we found no lateralization in the eye used, we found a their left eye, fled at greater distances (Table 3, Figure 1), and we consequence of the eye marmots used to monitor the approaching found that for a given alert distance, males fled at a greater dis- human. Marmots that used their left eye to monitor an approaching tance than females (Table 3, Figure 2). The 3 covariates tested had threat presumably assessed a higher risk and fled sooner. And this significant interactions between alert distance and distance to bur- second finding suggests that marmots have lateralized antipredator row (P ¼ 0.029), escape substrate (P ¼ 0.008), and escape incline behavior. Taken together these results are striking because while we (P ¼ 0.021), but all models retained the significant interaction might expect selection against animals being too predictable in their between look direction and alert distance (P ¼ 0.004, 0.004, and escape behavior (Briffa 2013), we might expect that there is rela- 0.046, respectively). Furthermore, when added one at a time to tively less cost to predictably looking at a predator and relatively our basic model, there was an effect of social group size more cost to predictably escaping from it. Given that predators may (P ¼ 0.045), vegetation height (P ¼ 0.032), and the day of data col- learn any bias in how individual prey respond to their attacks and lection on FID (P ¼ 0.020) on FID. Thus, while other variables use this to their advantage, we expect strong selection on prey to explain some variation in FID, we can conclude that the eye with respond to predators in an unpredictable manner, which is consis- which marmots looked at the approaching human was always a tent with the nonsignificant repeatability. In marmots, it may be significant factor. that the costs of predictably using 1 specific eye outweigh the bene- fits and perhaps variation in the relative costs and benefits explains Discussion some of the variation in lateralization seen across species (Chivers et al. 2016, 2017). Male marmots fled at greater distances once alerted than did Yellow-bellied marmots at our study site are preyed upon by a females, but we found no support that marmots overall preferen- variety of predators, a finding that given the Brown et al. (2004) tially used their left eye to monitor approaching humans. Although results, made us expect that marmots should have lateralized eye it is possible that with a substantially larger data set we would have use. Marmots are preyed upon by a variety of terrestrial predators detected individual consistency in the eye marmots used to monitor (coyotes Canis latrans, badgers Taxidea taxus, American martens an approaching threat, we did not detect it in our data set that Martes americana, black bears Ursus americanus, and long-tailed included an average of 3 (and up to 9) repeated approaches on indi- viduals. It is also possible that our predator manipulation was insuf- weasels Mustela frenata, Van Vuren 2001), as well as aerial preda- ficiently risky to generate the expected lateralized response. Levels tors (golden eagles Aguila chrysaetos, red-tailed hawks Buteo jamai- censis, Swainson’s hawks Buteo swainsoni, and goshawks Accipiter of predator exposure influence lateralization in fishes, where indi- viduals with the greatest risk of predation exhibited the most lateral- gentilis, Van Vuren 2001). It is possible that vulnerability to a vari- ized behavior (Heuts 1999; Ferrari et al. 2015; Chivers et al. 2017; ety of different and presumably cognitively sophisticated predators Lucon-Xiccato et al. 2017) and populations with very low predation has increased the cost of marmots responding predictably with 1 eye risk may lose lateralized eye use (Brown et al. 2004). Thus, and hence has selected for unpredictable eye use. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 4 Current Zoology, 2018, Vol. 0, No. 0 Figure 1. Relationship between alert distance and FID as a function of eye used when looking at approaching human. The plus sign indicates the right eye and dots the left eye. For any given distance, individuals monitoring approach with their right eye (thick line) had a shorter FID than those who monitored approach with their left eye (thin line). processing of risk-related stimuli. Therefore, when the right eye was used for risk assessment we expected that marmots would tolerate closer approaches. Our results suggest that more information on the relative costs of the looking with each eye is warranted. Do marmots respond the same way to humans as they do their more “natural” predators? Are occasions when marmots look with their right eye and tolerate closer approaches more likely to end in a costly escape? And, the broader question of whether individuals are less likely to have later- alized antipredator responses when they deal with cognitively sophisticated predators remains to be determined. 0 20 40 60 80 100 120 140 Alert Distance (m) Acknowledgments Figure 2. Relationship between alert distance and FID as a function of sex. We thank 2017 Team Marmot for logistical help in the field: Gabriela Pinho, Triangles indicate females and dots indicate males. For any given alert dis- Dana Williams, Sarah Heissenberger, Jazmine Uy, Gina Johnson, and tance, females (thick line) tolerated closer approach compared with males Madeline Standen. We thank 2 anonymous reviewers and the editor for a set (thin line). of astute comments that have helped us improve the paper. Studies in other taxa have reported that predictable prey may be more vulnerable to predation. For instance, proactive jumping spi- Funding ders Portia labiate captured more prey that responded predictably than unpredictable prey while docile spiders captured more unpre- D.T.B. was supported by the National Science Foundation (grant 1557130). dictable prey (Chang et al. 2017). Furthermore, hermit crabs A.D. was an NSF REU fellow supported by DBI 1226713 (to the Rocky Mountain Biological Laboratory). L.Y. was supported by China Scholarship Paguroidea bernhardus that fled in response to a predator Carcinus Counsel and Peking University. maenas had unpredictable re-emergence times, a finding consistent with this random response being an antipredator adaptation (Briffa 2013). Such unpredictable behavior may be the best method against References predators that are able to learn sequential patterns in their prey Andrew R, 2002. Development of lateralization. In: Rogers LJ, Andrew RJ, (Bednekoff and Lima 2002). editors. Comparative Vertebrate Lateralization. Oxford: Oxford University Despite marmots responding unpredictably to an approaching Press, 157–205. predator, our results are also consistent with hemispheric lateraliza- Armitage KB, 1982. Yellow-bellied marmot. In: Davis DE, editor. CRC tion of marmots’ escape behavior. The eye marmots used to monitor Handbook of Census Methods for Terrestrial Vertebrates. Boca Raton (FL): an approaching predator was associated with the distance at which CRC Press, Inc, 148–149. they fled the approaching predator. Because lateralized eye use Armitage KB, 2014. Marmot Biology: Sociality, Individual Fitness, and seems to be an ancestral and wide spread trait for risk perception in Population Dynamics. Cambridge (NY): Cambridge University Press. vertebrates (fishes—Bisazza et al. 1998; birds—Andrew 2002; Bates D, Maechler M, Bolker B, Walker S, 2017. Lme4: linear mixed-effects rodents—Kim et al. 2012; and primates—Shibasaki et al. 2014), we models using ‘eigen’ and S4. R Package Version 1.1-13 [cited 2017 July 1]. expected to see a greater FID when the left eye monitored approach Available from: https://github.com/lme4/lme4/ http://lme4.r-forge.r-project. because this was the eye that was associated with right hemispheric org/. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zoy003/4798834 by Ed 'DeepDyve' Gillespie user on 12 July 2018 Flight Iniaon Distance (m) Blumstein et al.  Marmot lateralization 5 Bednekoff PA, Lima SL, 2002. Why are scanning patterns so variable? An Frid A, Dill LM, 2002. Human-caused disturbance stimuli as a form of preda- overlooked question in the study of anti-predator vigilance. J Avian Biol 33: tion risk. Conserv Ecol 6:11. [cited 2017 July 1] Available from: http:// 143–149. www.consecol.org/vol6/iss1/art11. Bisazza A, Rogers LR, Vallortigara G, 1998. The origins of cerebral asymme- Glick SD, Zimmerberg B, Jerussi TP, 1977. Adaptive significance of laterality try: a review of evidence of behavioural and brain lateralization in fishes, in the rodent. Ann NY Acad Sci 299:180–185. reptiles and amphibians. Neurosci Biobehav Rev 22:411–426. Heuts BA, 1999. Lateralization of trunk muscle volume, and lateralization of Blumstein DT, 2013. Yellow-bellied marmots: insights from an emergent view swimming turns of fish responding to external stimuli. Behav Proc 47: of sociality. Phil Trans R Soc Lond B 368:20120349. 113–124. Blumstein DT, Flores G, Munoz NE, 2015. Does locomotor ability influence Hook-Costigan MA, Rogers LJ, 1998. Lateralized use of the mouth in produc- flight initiation distance in yellow-bellied marmots? Ethology 121:434–441. tion of vocalizations by marmosets. Neuropsychologia 36:1265–1273. Blumstein DT, Runyun A, Seymour M, Nicodemus A, Ozgul A et al., 2004. Kim S, Matyas F, Lee S, Acsady L, Shin H, 2012. Lateralization of observatio- Locomotor ability and wariness in yellow-bellied marmots. Ethology 110: nal fear learning at the cortical but not thalamic level in mice. Proc Natl 615–634. Acad Sci USA 109:15497–15501. Briffa M, 2013. Plastic proteans: reduced predictability in the face of predation Kuznetsova A, Brocknoff PB, Christensen BRH, 2016. lmerTest in linear risk in hermit crabs. Biol Lett 9:2013592. mixed effects models. R package version 3.3.3 [cited 2017 July 1]. Available Brown C, Gardner C, Braithwaite VA, 2004. Population variation in lateral- from: https://CRAN.Rproject.org/package¼lmerTest. ized eye use in the pociliid Brachyraphis episcopi. Proc R Soc Lond B Lippolis G, Bisazza A, Rogers L, Vallortigara G, 2002. Lateralisation of 271(Suppl):S455–S457. predator avoidance responses in three species of toads. Laterality 7: Chang C, Teo HY, Norma-Rashid Y, Li D, 2017. Predator personality and 163–183. prey behavioural predictability jointly determine foraging performance. Sci Lucon-Xiccato T, Chivers DP, Mitchell MD, Ferrari MCO, 2017. Prenatal Rep 7:40734. exposure to predation affects predator recognition learning via lateraliza- Chiandetti C, Regolin L, Rogers LJ, Vallortigara G, 2005. Effect of light stim- tion plasticity. Behav Ecol 28:253–259. ulation of embryos on the use of position-specific and object-specific cues in Nash JC, Varadhan R, 2011. Unifying optimization algorithms to aid software binocular and monocular domestic chicks Gallus gallus. Behav Brain Res system users: optimx for R. J Stat Softw 43:1–14. 163:10–17. Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT, 2013. Chivers DP, McCormick MI, Allan BJM, Mitchell MD, Gonc¸alves EJ et al., Development in boldness and docility in yellow-bellied marmots. Anim 2016. At odds with the group: changes in lateralization and escape per- Behav 86:1147–1154. formance reveal conformity and conflict in fish schools. Proc R Soc B Rogers LJ, Zucca P, Vallortigara G, 2004. Advantages to having a lateralized 283:1127. brain. Proc R Soc B 217: S420–S422. Chivers DP, McCormick MI, Warren DT, Allen BJ, Ramasamy RA et al., Runyan AM, Blumstein DT, 2004. Do individual differences influence flight 2017. Competitive superiority versus predation savvy: the two sides of initiation distances? J Wildl Manag 68:1124–1129. behavioural lateralization. Anim Behav 130:9–15. Santi A, Bisazza A, Vallortigara G, 2002. Complementary left and right eye Collins RL, 1985. On the inheritance of direction and degree of asymmetry. use during predator inspection and shoal-mate scrutiny in minnows. J Fish In: Glick SD, editor. Cerebral Lateralization in Nonhuman Species. New Biol 60:1116–1125. York (NY): Academic Press, 41–69. Shibasaki M, Nagumo S, Koda H, 2014. Japanese monkeys Macaca fuscata Cooper WE Jr, Blumstein DT, 2015. Escape behavior: importance, scope, and spontaneously associate alarm calls with snakes appearing in the left visual variables. In: Cooper WE Jr, Blumstein DT, editors. Escaping from field. J Comp Psych 128:332–335. Predators: An Integrative View of Escape Decisions. Cambridge (UK): Vallortigara G, 2000. Comparative neuropsychology of the dual brain: a stroll Cambridge University Press, 3–12. through animals’ left and right perceptual worlds. Brain Lang 73:189–219. Domenici P, Allan B, McCormick MI, Munday PL, 2012. Elevated carbon Van Vuren DH, 2001. Predation on yellow-bellied marmots Marmota flavi- dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8: ventris. Am Midl Nat 145:94–100. 78–81. Wickham H, Chang W, 2016. ggplot2: create elegant data visualisations using Ferrari MCO, McCormick MI, Allan BJM, Choi RB, Ramasamy RA et al., the grammar of graphics. R Package Version 2.2.1 [cited 2017 July 1]. 2015. The effect of background risk on behavioural lateralization in a coral Available from: http://ggplot2.tidyverse.org, https://github.com/tidyverse/ reef fish. Funct Ecol 29:1553–1559. ggplot2. 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Current ZoologyOxford University Press

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