Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination and common genet cues

Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination... In nature, animals are exposed to a broad range of threats imposed by predators, which may strongly influence the ecology of prey species directly or indirectly by affecting their behavior via fear of predation. Here, we studied wood mice Apodemus sylvaticus behavioral and physiological responses to simulated predation risk. Risk avoidance was analyzed by live trapping with control traps and traps treated with feces of common genet Genetta genetta (direct cue of risk) under new moon nights and following by simulated full moon conditions (indirect cue). The time devoted to foraging behavior and capture time were analyzed by video recording mice activity around traps. Food intake was calculated based on the amount of bait remaining in each trap. Fecal cortico- sterone metabolites (FCMs) were measured by enzyme-immunoassay as indicators of physio- logical stress responses. Fewer wood mice were captured during full moon, yet only non-breeding adult males clearly avoided common genet odor. Mice were captured sooner at night during the simulated full moon conditions and later in predator-treated traps. Foraging activity was lower when individuals faced predator’s feces, but neither food intake nor FCM levels were affected by predation risk cues. Direct and indirect cues of predation risk selectively affected wood mice behav- ior, although behavioral responses seem to be modulated by different costs–benefit balances related to the individual’s perception of risk. The lack of physiological responses to predation risk cues suggests that wood mice did not perceive them as reliable stressors or the response was too small or transient to be measured by FCM. Key words: common genet, fecal predator cues, feeding, foraging, moonlight, predator avoidance. Predation represents one of the most important causes of death for or avoid predation risk (Lima and Dill 1990; Kats and Dill 1998; small mammals and it strongly influences prey ecology directly Lima 1998). Thus, prey are attuned to respond in a number of be- through mortality (Brown et al. 1999; Hanski et al. 2001)or havioral and physiological ways to cues associated with predation through indirect effects on prey demographic and behavioral re- risk that can be direct (signals associated to predators: presence, sponses to predators (Lima and Dill 1990; Apfelbach et al. 2005; urine, feces, or sounds) or indirect (e.g., habitat complexity or envir- Dı´az et al. 2005; Zanette et al. 2011; Navarro-Castilla and Barja onmental conditions) (Eilam et al. 1999; Orrock et al. 2004; Wro´ bel 2014a, 2014b). Because animals are exposed to a wide range of dan- and Bogdziewicz 2015). gers imposed by predators, they have developed a variety of preda- Most carnivores use secretions from glands, urine, and feces to tor detection mechanisms and antipredatory responses to minimize mark their territory (Hutchings and White 2000; Barja and List V C The Author (2017). 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/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 2 Current Zoology, 2017, Vol. 00, No. 00 2006; Barja 2009; Martı´n et al. 2010; Pineiro ~ et al. 2012) and mul- we studied whether these cues of increased predation risk affected: tiple studies have revealed that several rodent species are sensitive to (1) wood mouse behavior (i.e., avoidance of predator-treated traps the scent of potential predators, avoiding such chemical signals and foraging activity), (2) food intake, and (3) physiological stress without needing other cues (Stoddart 1982; Dickman and Doncaster response in wood mice. Further, the influence of individual charac- 1984; Calder and Gorman 1991; Jedrzejewski et al. 1993; Navarro- teristics (i.e., sex, reproductive activity, and age) on these responses Castilla and Barja 2014a, 2014b). Furthermore, prey species often was also evaluated. The common genet is an important threat for alter their behavior in response to the auditory, visual, and chemo- small mammals, especially for wood mice (Hamdine et al. 1993; sensory cues from predators (Lima and Dill 1990; Kats and Dill Virgo´ s et al. 1999). Since variation in predation risk affects foraging 1998; Eilam et al. 1999; Zanette et al. 2011; Clinchy et al. 2013; decisions (Lima and Bednekoff 1999), we predicted that wood mice Tortosa et al. 2015). Thus, in that prey species are at risk of preda- would alter their foraging behavior when confronted with common tion while performing daily activities, there are tradeoffs between genet feces and they would also avoid entering the predator-treated antipredator behavior and other fundamental activities like foraging traps, especially under high illumination (simulated full moon). and feeding (Sih 1980; Brown et al. 1988; Brown 1988; Orrock Further, wood mice were expected to vary food intake in response et al. 2004; Gallego et al. 2017; Sa´nchez-Gonza´lez et al. 2017). to their perceived predation risk prior to entering the trap (owing In addition, antipredatory behavior can be strongly influenced by both to increased illumination and the presence of predator feces), the environment. Thus, increased predation risk perception but also because of the likely detection of common genet fecal odor through lower habitat complexity or higher visibility has revealed by individuals within treated traps. Finally, we expected that expos- that rodent species will avoid open areas and decrease activity on ure to increased illumination and to common genet feces would nights with a full moon (Kaufman and Kaufman 1982; Kotler evoke physiological stress responses in wood mice as measured by et al. 1988; Wolfe and Summerlin 1989; Kotler et al. 1994; Brown fecal GC metabolites. et al. 2001; Kotler et al. 2002; Eilam 2004; Kotler et al. 2010). Few studies have attempted to determine whether prey responses to predation risk situations are influenced by individual character- Materials and Methods istics (e.g., sex, breeding condition, and age of individuals) Study area (Dickman and Doncaster 1984; Jedrzejewski and Jedrzejewska Field work was carried out in the savanna-like holm oak Quercus 1990). ilex woodlands of the National Park of Cabaneros ~ (Central Spain, Responses to predation risk should not be restricted only to be- 30S 385450, UTM 4353479). In this system, large oak trees grow havioral responses because, under certain risky situations, prey may scattered (mean tree density is 14 ha ) on a grassland matrix with display physiological responses which are not translated into a almost no shrub cover (<1%; see Pulido et al. 2001; Dı´az et al. modification of behavior (Eilam et al. 1999). When animals are sub- 2011). jected to a stressor, the hypothalamus releases corticotrophin releas- ing hormone inducing the anterior pituitary to secrete the Experimental design: live trapping and simulation of adrenocorticotropic hormone (ACTH) which signals the adrenal cortex to release glucocorticoids (GC) to help the individuals to predation risk cope with the stressful situation (Sapolsky et al. 2000). Thus, GC Prior to the beginning of the experimental study, to determine which concentrations can be used as a hormonal measure of physiological trees were occupied by wood mice and to allow mice to acclimate to stress responses (Wingfield and Romero 2001; Mo¨stl and Palme traps, Sherman traps were placed beneath trees (n ¼ 170) in 2 study 2002). In fact, GC metabolites in feces have been reported in several sites (separated by 1,500 m) over a 3-day period. Afterward, during vertebrate species as a useful non-invasive technique for assessing the experimental study (Figure 1), Sherman traps (n ¼ 2/tree) were adrenocortical function (Mo¨stl and Palme 2002; Monclu´ s et al. placed in those trees (n ¼ 40) confirmed to be occupied by wood 2006; Lepschy et al. 2007; Dantzer et al. 2010; Barja et al. 2012; mice. Since predator’s odors have been previously shown to evoke Pineiro ~ et al. 2012; Zwijacz-Kozica et al. 2013; Navarro-Castilla antipredatory responses in small mammals (Dickman and Doncaster et al. 2014a, 2014b). In mammals, GC plays an important role in re- 1984; Navarro-Castilla and Barja 2014a, 2014b), we manipulated sponding to diverse factors such as social conflicts and human dis- the direct perception of predation risk through predator odor from turbances (Sapolsky et al. 2000; Romero 2002; Barja et al. 2007; one of the main rodent predators in the study area, the common Navarro-Castilla et al. 2014a, 2014b). Since stressful situations usu- genet G. genetta. To examine the effect of predator odor, nearby ally evoke an increase in GC production, predators could induce occupied trees were randomly paired and treatments (traps treated physiological responses in their prey by a physical attack but also by with predator odor) and control (untreated traps) were assigned to making them fearful of an imminent attack (Boonstra et al. 1998; one tree of each pair at random. Mean distance between predator- Eilam et al. 1999; Hirschenhauser et al. 2000; Korte 2001; Monclu´s treated and paired control trees was 42.79 m (range 8.20–80.36 m). et al. 2005; Clinchy et al. 2013; Zanette et al. 2014). Similarly, Predator treatment consisted in fresh feces of common genet col- increased illumination could act as a potential stressor for noctur- ~ lected from captive animals of the Canada Real Open Center nally active prey species. However, few studies have previously eval- (Madrid, Spain). To prevent volatile compounds variation in rela- uated its effect on the physiological stress response (Navarro- tion to seasonal or individual factors (Andreolini et al. 1987; Castilla and Barja 2014b). Jemiolo et al. 1991; Hayes et al. 2006; Scordato et al. 2007; Martı´n In the present study, we tested whether wood mice Apodemus et al. 2010), all collected feces were mixed to obtain a homogeneous sylvaticus showed behavioral and physiological changes due to mixture avoiding possible bias in our results. Predator treatment increased predation risk due to moonlight (i.e., natural new moon was made following methods by Navarro-Castilla and Barja and simulated full moon conditions) and exposure to predator odor (2014a), 100 g of homogenized fecal sample was mixed with from an invasive species, the common genet Genetta genetta. Thus, 100 mL of distilled water obtaining a mixture similar to real fresh Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 3 Figure 1. Flow chart of the experimental study. feces. Predator presence was simulated by leaving an equal amount tripod 60 cm tall located 1 m away and focused on Sherman traps, (5 g) of feces at the entrance of treated traps and it was renewed covering a field of vision of 1 m . Video-cameras were provided every day at dusk. with ELRO dvr32 card-based recorders (settings 5 frames/s and To test the effect of moonlight, the above mentioned experimen- using 16 GB recording cards replaced each day). Both the recording tal design was carried out during 5 consecutive new moon nights and the illumination devices were fully autonomous since they were (20–24 March 2012); afterward, the following 5 nights we simu- powered by car batteries (70 Ah, lead-acid) attached to solar panels lated full moon light conditions at the same sites by means of artifi- (ono-silicon erial P_20; 20 w). However, they were turned on each cial illumination. The illumination device (composed of 3 white and day at dusk, before opening traps and renewing predator odor. Mice 3 blue led lights grouped behind a diffusion screen simulating a dif- foraging behavior, recorded as the time (s) since individuals ap- fuse light with the spectral composition of moonlight) was hung peared in the image until they went inside the trap closing it, was down from the tree canopy at a height of 2 m to simulate a light in- videotaped during trapping sessions. We also recorded at what time tensity of 1 lux at ground level (measured by means of a TES-1332A of the night each individual was captured allowing us to know the luxometer). Light intensity of 1.0 lux approximately corresponds to time spent by each individual inside traps. the maximum moonlight intensity expected during full moon nights To determine the amount of food eaten, bait remains were oven- in this region (Bu¨ nning and Moser 1969). dried at 50 C (Selecta, model CONTERM 2000208) and weighed Sherman traps were activated at dusk, and trap checks were car- (Giros PG-500; precision 0.01 g). Body weight of individuals was ried out 10–12 h later (at dawn) to minimize the time that animals positively correlated with food intake (r ¼ 0.67, P ¼ 0.002); there- were kept. Nest material (raw wool with natural lanolin) was used as fore, food intake by an individual was divided by its body weight to bedding inside traps. All traps were baited with 4 g of toasted corn. control the effect of body weight on food intake. Captured individuals were identified to species. Sex and reproductive condition was determined from external characteristics (Gurnell and Feces collection and fecal corticosterone Flowerdew 1994); adult males with enlarged testicles descended into metabolites quantification the scrotal sac and females showing noticeable nipples and/or the va- Fresh feces were collected from traps where individuals were cap- ginal membrane perforated were classified as reproductively active. tured, if urine was detected fecal samples were excluded in order to In addition, a 100 g hand-held scale was employed to measure body avoid cross contamination (Touma et al. 2003). To avoid the effects weight which was used to estimate relative age following Navarro- of environmental conditions and microorganisms proliferation on Castilla and Barja (2014a) (juveniles: <13 g; sub-adults: from 13 g to fecal corticosterone metabolite (FCM) levels (Washburn and <20 g; adults: 20 g). Individuals were marked in non-conspicuous Millspaugh 2002; Millspaugh et al. 2003), only fresh feces (i.e., with areas with harmless paints (red food coloring: Ponceau-4R E124) for a soft texture and not dried) were collected. Fecal samples were col- individual identification and to control for recaptures. Animals were lected between sunrise and 2 h after; thus, by only collecting fresh quickly handled (<1 min) and then released at the same point of cap- feces during the early morning we avoided circadian rhythm effects ture. Manipulations of animals were done in compliance with the on excretion patterns (Touma et al. 2003). Corticosterone peak con- European Communities Council Directive 86/609/EEC for animal centrations have been observed in wood mice feces on average at experiments and were carried out under the permit of the Cabaneros 10 h after ACTH injection (range: 8–12 h; see the “results” section); National Park authorities. therefore, fecal samples from individuals trapped >8 h were rejected to avoid any possible effect of the capture in FCM levels. Fecal sam- Mice foraging behavior and food intake ples were stored in the freezer at 20 C until analysis. To control For recording wood mice foraging behavior, video-cameras for potential observer bias, we used blind observation by coding (OmniVision CMOS 380 LTV, 3.6 mm lens) were mounted on a samples before laboratory analysis of FCM concentrations. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 4 Current Zoology, 2017, Vol. 00, No. 00 Extraction of FCM from fecal samples was done according to Table 1. Results of the fit of a log-linear model analyzing the effects of individual and predation risk factors on the capturability of the modified method of Touma et al. (2003). Fecal samples were un- wood mice frozen and dried in the heater until constant weight. We placed 0.05 g of dry feces in assay tubes with 0.5 mL of phosphate buffer 2 Effect df G P and 0.5 mL of 80% methanol, then, they were shaken for 16 h and Sex/age 2 7.38 0.025 supernatants were centrifuged at 2,500  g for 15 min. Pellets were Breeding condition 1 10.68 0.001 discarded and the fecal extracts were stored at 20 C until ana- Sex/age * breeding condition 1 6.66 0.010 lyzed. Quantification was achieved using a commercial cortico- Treatment 1 0.36 0.548 sterone enzyme immunoassay (EIA) (Demeditec Diagnostics GmbH, Moonlight 1 12.35 0.000 Kiel, Germany) previously validated for measuring FCM in mice Moonlight * sex/age 2 3.03 0.220 species (Abelson et al. 2016; Navarro-Castilla et al. 2017). Moonlight * breeding condition 1 0.15 0.695 Parallelism, accuracy, and precision tests were done to validate the Treatment * moonlight 1 0.04 0.843 EIA (Goymann et al. 1999; Young et al. 2004). Parallelism was per- Treatment * sex/age 2 1.94 0.379 formed with serial dilutions of fecal extracts (1:32, 1:16, 1:8, 1:4, Treatment * breeding condition 1 0.21 0.644 1:2, 1:1) resulting in a curve parallel to the standard. Accuracy (re- Treatment * moonlight * sex/age 2 0.42 0.809 Treatment * moonlight * breeding condition 1 0.14 0.712 covery) was 118.66 31.7% (n ¼ 6). Precision was tested through Treatment * sex/age * breeding condition 1 6.54 0.011 intra- and inter-assay coefficients of variation for 3 biological sam- Moonlight * sex/age * breeding condition 1 1.01 0.316 ples, being 4.7% (n ¼ 6) and 8.2% (n ¼ 3), respectively. In each Treatment * moonlight * sex/age * breeding condition 1 0.97 1.000 assay, we used a standard, whose corticosterone concentration was known, included in the Demeditec kit. The assay was excluded and samples were reanalyzed if standard corticosterone concentrations deviated >10% from the expected value. The assay detection limit (except age factor) and we included the time that each individual (sensitivity) for corticosterone metabolites was 4.1 ng/mL. spent inside the trap as covariate. Finally, variation in FCM was Furthermore, a biological validation was carried out to confirm the analyzed by GLMs, including moon phase, treatment, sex, breeding suitability of the EIA for wood mouse fecal samples. Thus, following condition, and recapture as fixed factors and body weight of individ- the procedure by Touma et al. (2004), we injected a high dose uals was included as covariate. Foraging behavior and FCM were (60 mg/100 g of body weight) of synthetic ACTH (Synacthen Depot, log-transformed as needed to normalize the distributions of Novartis, Germany) into 5 captive individuals (2 females and 3 residuals. males). Samples of each of the 5 individuals were collected within The GLMs included the main effects of the factors studied and minutes after defecation and immediately stored in Eppendorfs at their 2-way interactions. Results were considered significant at 20 C until analysis. Sampling times were: 0, 2, 4, 6, 8, 10, 12, 14, a< 0.05. The probability of committing table-wise type-I errors was 18, 22, and 26 h post-injection. FCM levels are expressed as nano- judged low (ca. 18%; 4 comprehensive test made at a ¼ 0.05; grams per gram dry feces. Streiner and Norman 2011), so that we did not perform adjustments Higher FCM concentrations detected in the present study are for multiple comparisons to avoid the risk of committing type-II similar to those analyzed using the same methodology in another errors (Rothman 1990; Feise 2002). Results are given as closely related rodent species, the Algerian mouse (Mus spretus), mean6 standard error (SE). We used the SPSS 15.0 statistical soft- inhabiting the same study area (Navarro-Castilla et al. 2017). ware (SPSS Inc., Chicago, IL, USA). This may be attributable to the very low limit of detection (553 pg/ mL) of the Demeditec kit, which is known to detect higher FCM concentrations than other available commercial kits (see Abelson Results et al. 2016). Risk avoidance by wood mice Overall, 153 wood mice (71 new captures and 82 recaptures) were Data analysis captured. The study population was dominated by adults (80.3% Capture frequencies according to odor and moonlight treatments, as vs. 19.7%), females (56.1% vs. 43.9% males), and reproductively well as their interactions with individual characteristics (sex, age, active females (53% vs. 20% reproductively active males; Table 1). and breeding condition) were analyzed by fitting log-linear models Regarding predation risk factors, simulated full moon conditions to the 5-way contingency table generated by the factors odor (con- decreased the number of captures compared with the natural new trol/common genet feces), moonlight (new moon/simulated full moon phase (36.5% vs. 63.5%, respectively) while predator treat- moon), sex/age (adult male, adult female, or juvenile), breeding con- ment did not significantly decrease wood mice captures (46.5% vs. dition (active or not), and presence/absence of capture, taking into 53.5% control traps) (Table 1 and Figure 2A). Nevertheless, we account the structural zeros resulting from the impossibility of find- found a significant interaction between treatment * sex/ ing sexually active juveniles (Dı´az et al. 1999; Mora´n-Lo´ pez et al. age * breeding condition (Table 1) showing that non-breeding adult 2015). Recaptures were not taken into account in the captures fre- males clearly avoided common genet feces (v ¼ 7.04, df ¼ 1, quencies tests to maintain data independence. P ¼ 0.008; Figure 2B). None of the interactions among predator risk We used general linear models (GLMs) to analyze differences in factors were significant (Table 1). foraging behavior due to moonlight (natural new moon/simulated full moon), treatment (control/fecal odor), sex (male/female), breed- ing condition (breeding/non-breeding), age (juveniles/sub-adults/ Mice foraging behavior and food intake adults), and recapture (new capture/recapture). We also employed Wood mice were captured sooner at night during simulated full moon 0 0 GLMs to test variation in food intake (corrected by animal’s body conditions (5 h 1 6 34 after trap activation) than during new moon 0 0 weight); fixed factors were the same as in the foraging activity model nights (6 h 45 6 34)(F ¼ 5.77, P¼ 0.019). Further, individuals 1,76 Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 5 Figure 3. Effect of treatment (control vs. common genet) on wood mice forag- ing behavior (s, mean6 SE). Significant differences are indicated by asterisks (*P< 0.05). Table 3. Food intake by wood mice in relation to predation risk and Figure 2. Percentage of wood mice captured in relation to direct (common individual factors genet feces) and indirect (moonlight) cues of predation risk (A). Percentage of captures according to treatment, sex/age, and breeding condition (B). Factor df FP Asterisks indicate significant differences between the analyzed groups (**P< 0.01; ***P< 0.001). Moonlight 1 3.579 0.065 Treatment 1 1.432 0.238 Sex 1 0.019 0.890 Table 2. Results of GLMs testing for the effects of predation risk Breeding condition 1 8.486 0.006 and individual factors on wood mice foraging behavior Recapture 1 6.563 0.231 Time inside trap 4 2.608 0.114 Factor df FP Error 55 Moonlight 1 0.301 0.587 Treatment 1 6.945 0.013 Sex 1 1.176 0.286 Breeding condition 1 2.554 0.120 to 40,420 ng/g feces. In the 5 individuals, the corticosterone EIA de- Relative age 1 1.680 0.202 tected an average increase in FCM concentrations ranging from Recapture 1 1.366 0.271 116% to 247% within 8–12 h of the injection event. Subsequent to Error 59 that, a downward trend toward baseline FCM values was detected within 12–18 h, validating the corticosterone EIA for the analysis of wood mouse fecal samples. 0 0 were captured sooner in control traps (at 5 h 5 6 34 ) compared with FCM levels were analyzed in 107 fresh fecal samples. Neither traps treated with common genet feces in which individuals were cap- moonlight nor predator odor emerged as significant factors influenc- 0 0 tured later during the night (6 h 40 6 34)(F ¼ 4.66, P ¼ 0.034). 1,76 ing FCM levels. Factors explaining the variation found in FCM con- Treatment was the only significant factor explaining the variation centrations are presented in Table 4. Body weight of individuals was found in foraging behavior before entering traps (Table 2); individuals positively correlated with FCM levels (Table 4). Overall, FCM levels spent less time foraging when they were subjected to predator were lower in males (130,6956 53,407 ng/g dry feces) than in fe- fecal cues (24.566 2.60 s) than when they faced control traps males (138,7626 41,306 ng/g dry feces) and individuals showed (31.546 4.67 s; Table 2 and Figure 3). The amount of food consumed lower FCM levels when they were recaptured (84,9286 35,891 ng/g was not related to the amount of time that animals spent inside traps, dry feces) than when they were captured for the first time or by their previous capture history. Further, neither common genet (165,0026 47,982 ng/g dry feces). However, the only significant feces nor illumination influenced food intake. Only breeding condition interaction between sex * recapture revealed that significant differ- emerged as a significant factor (Table 3), with breeding individuals ences in FCM were between females captured for the first time and having a significantly lower food intake (0.0916 0.008 g/g) than non- recaptured males (Table 4 and Figure 4). breeding individuals (0.1746 0.013 g/g). Interactions among factors were not statistically significant. Discussion Physiological stress response Risk avoidance by wood mice In the biological validation experiment, measured FCM baseline lev- A decrease in activity during full moon conditions has been els (prior to injection) for each tested individual ranged from 13,120 described as a generalized antipredatory behavior in prey species Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 6 Current Zoology, 2017, Vol. 00, No. 00 Table 4. Results of a general lineal model testing the effects of indi- significantly different from random expectations for non-breeding vidual and predation risk factors on fecal glucocorticoid metabol- adult males only. Coincident with these results, Dickman and ites in wood mice Doncaster (1984) showed that male wood mice exhibited a higher avoidance of predator feces than females did. However, in our case, Factor df FP breeding males did not show such avoidance. Their social, sexual, Moonlight 1 2.690 0.105 and territorial-related behaviors during the breeding season Treatment 1 0.025 0.875 (Montgomery and Gurnell 1985) and their attraction to new objects Sex 1 0.177 0.675 (Brown 1969) could be possible explanations for the results. Similar Breeding condition 1 0.170 0.681 differences in response to predator cues due to sex and breeding con- Recapture 1 1.235 0.270 dition were also found in bank voles Clethrionomys glareolus by Body weight 1 5.660 0.020 Jedrzejewski and Jedrzejewska (1990). Therefore, sex and breeding Sex * recapture 1 4.178 0.044 condition differences in the responses to predation risk suggest that Error 90 gonadal hormones may be involved in the mediation of the antipre- datory responses (Perrot-Sinal et al. 1999). On the other hand, young mammals typically devote less time to predator detection (Arenz and Leger 2000) which could explain why juveniles were equally captured although predation risk cues increased. Therefore, while indirect risk cues (moonlight) seem to be perceived by most in- dividuals as a more reliable indicator of enhanced predation risk (Orrock et al. 2004), responses to direct cues (predator feces) are not generalized, but vary among individuals according to the indi- vidual’s characteristics and in all likelihood, their previous experi- ence (Lima and Bednekoff 1999). Mice foraging behavior and food intake Predation risk perception may influence animal daily decision mak- ing to choose when, where, and how long to forage. According to Lima and Bednekoff (1999), under high risk situations prey reduce time spent in daily activities to optimize the energy spent on antipre- datory behavior. Several studies have reported that under high levels of risk, individuals decreased mobility and concentrated foraging ac- tivity in safer habitats (Lima and Dill 1990; Dı´az 1992; Kotler et al. 2002). Our results also showed predation risk influencing foraging behavior. Thus, when traps were treated with common genet feces, Figure 4. Log-transformed concentrations (mean6 SE) of fecal glucocorticoid wood mice apparently delayed foraging close to these traps and metabolites (FCM, ng/g dry feces) in males and females in relation to new were captured later at night. Despite that delay, once individuals captures or recaptures. were detected in the vicinity of a trap, they devoted less time to for- aging, entering feces-treated traps more rapidly than control traps. In relation to moonlight, wood mice were trapped sooner during (Kotler et al. 2010; Penteriani et al. 2013). This common behavioral simulated full moon conditions, but no effect of moonlight was response could explain why fewer wood mice were captured during found on foraging behavior. These results perfectly match those of the simulated full moon conditions, matching this result with the Dı´az et al. (2005), who found that wood mice reduced foraging be- moonlight avoidance found in wood mice under natural full moon havior in response to the presence or activity of common genets but nights (Navarro-Castilla and Barja 2014b). The number of newly there was no effect of moonlight on foraging activity. Apart from ef- captured individuals during the full moon treatment could also have fects of the different nature and meaning of both predation risk cues been influenced by the design of our study, because it was carried (direct cues indicate predator presence nearby, whereas indirect cues out after the new moon treatment and had a smaller pool of poten- just general levels of danger), results may be also explained by tem- tial new animals to catch. However, the reduction in the number of poral variation in their intensity. Predator odor intensity surely both newly captured and recaptured individuals supported the over- decreased through the night, so that wood mice delayed foraging all negative effect of increased illumination on wood mice foraging. and foraged more rapidly when facing predator feces, consistent Therefore, moonlight can indicate a higher risk of predation since with this decreasing intensity of the direct cue. However, moonlight an individual’s vulnerability to a predator depends partly upon visi- intensity was constant over the night, so that perception of risk, and bility. On the other hand, predator odor might provide direct infor- hence responses, did not decrease. According to Lima and Bednekoff mation on predation risk even when the predator is absent at the (1999), animals under longer periods of high risk (e.g., full moon time of detection. In this study, the number of captures decreased in nights) are forced to decrease antipredatory behavior and forage to traps treated with common genet feces, coincident with several stud- meet their energy demands. This hypothesis could explain why al- ies where avoiding areas marked by predators was common in small though moonlight is supposed to increase perceived predation risk mammals (Dickman and Doncaster 1984; Calder and Gorman and wood mice were expected to decreased food intake we did not 1991; Russell and Banks 2007). However, this antipredatory re- find significant differences. Alternatively, as the full moon experi- sponse varied depending on individual characteristics, being ment was carried out after the new moon sampling, this might be an Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 7 effect of treatment order (i.e., first new moon directly following by between the benefits of safety from predation and the costs associ- the full moon experiments) and previous experience. Thus, as a re- ated with missing opportunities for foraging or reproduction sult of being repeatedly captured during both moon phases, wood (Abrams 1986; Lima and Dill 1990; Brown et al. 1999; Brown and mice may have become accustomed and would have valued the Kotler 2004). Besides being an invasive species, common genets benefits of obtaining food over the risk perceived via illumination. defecate in latrines, so their feces may be less indicative of their pres- Regarding individual factors, only breeding condition led to signifi- ence or movement patterns, and therefore, a generalized antipreda- cant differences in food intake. Overall, prey have to trade off food tory response would not lead to survival benefits that would and safety under each situation, but they also have to prioritize outweigh the cost of lost foraging opportunities. Thus, wood mice between different daily activities. In this regard, we conservatively are expected to exhibit different antipredatory responses only when speculate that breeding individuals could be more careful they have an accurate assessment of the current predation risk, and under risky situations reducing feeding and allocating more time to making decisions, choosing those behavioral options which maxi- survive and breed. mize their fitness, for example, delaying and reducing foraging activ- ity when facing common genet fecal cues. Nevertheless, behavioral responses seem to depend on context, past experience, and individ- Physiological stress response ual variation (Gorman and Trowbridge 1989). The apparent ab- Generally, short-term GC secretion last only a few hours and pro- sence of a GC stress responses to factors that are presumably related motes successful adaptive responses to a stressful stimulus to predation risk (i.e., moonlight and predator odor) suggests that (Wingfield and Romero 2001), whereas chronic stress occurs when these factors are not perceived as reliable stressors by wood mice. individuals experienced either multiple, frequent exposure to stres- So, making decisions by altering behavioral responses seem to be sors, and/or long-term continuous exposure to stressors which gen- better, faster, and a more useful option to maximize fitness. erates elevated and prolonged high GC levels exceeding the individual level of beneficial adaptation and leading to pathological consequences (Mo¨ stl and Palme 2002; Sapolsky 2002; Romero Author Contributions 2004). Physiological responses due to simulated predation risk by owl calls were previously found for voles and mice (Eilam et al. Conceptualization: A.N.C., I.B., and M.D.; Methodology: A.N.C.; 1999). However, studies where predation risk was simulated with Data analysis: A.N.C., I.B., and M.D.; Writing—original draft prep- predator odor did not evoke any physiological response in different aration: A.N.C.; Writing—review and editing: A.N.C., I.B., and rodent species (bank voles and weasels: Ylo¨ nen et al. 2006; meadow M.D.; and Funding acquisition: A.N.C., I.B., and M.D. voles and weasels: Fletcher and Boonstra 2006). In the present The authors are very grateful to Miguel Ferna´ndez, Vero´ nica study, neither moonlight nor exposure to predator feces had any in- Alonso, David Lo´ pez, and Javier Jime´nez for their help during field fluence on FCM in wood mice, a result similar to the lack of effect work. They thank the authorities and staff of the Cabaneros ~ of natural moonlight conditions and red fox fecal odor on the National Park who allowed them to develop their studies there. physiological stress response of wood mice found by Navarro- They also thank Dr Vincenzo Penteriani for their generous help in Castilla and Barja (2014b). Thus, perceived predation risk does not reviewing a previous version of this manuscript, and Dr James Hare appear to be sufficient to elicit increased FCM levels in the wood and 2 anonymous reviewers for their useful comments and sugges- mouse. Both the delay in approaching feces-treated traps and tions to improve the present work. reduced foraging behavior when in proximity to such traps could re- duce the individual’s perceived predation risk so as to preclude a physiological stress response, or diminish that response in magni- Funding tude or duration to the point that it escaped detection by our FCM This work was partially supported by the project RISKDISP (CGL2009- assay. Alternatively, inter-individual variation in FCM levels could 08430/BOS) and Comunidad de Madrid together with the European Social result in insufficient statistical power to detect significant differences Fund and Universidad Auto´noma de Madrid (CCG10-UAM/AMB-5325). among predation risk treatments. Regarding the effect of individual This study is a contribution to the projects MONTES [CSD2008-00040], factors, we found that body weight of individuals, which is closely RISKDISP [CGL2009-08430], and VULGLO [CGL2010-22180-C03-03], related to the age of individuals (Gurnell and Flowerdew 1994), was funded by the Spanish Ministerio de Ciencia e Innovacio´n; 096/2002 and positively correlated with FCM levels. Adults may have exhibited 003/2007, funded by the Organismo Auto´nomo Parques Nacionales; and higher FCM levels as a consequence of their breeding condition, that ANASINQUE [PGC2010-RNM-5782], funded by the Junta de Andalucı´a. is, changes due to pregnancy and lactancy (Bauman 2000; Strier A.N.-C. was supported by a FPU scholarship [AP2008-03430] from the Ministerio de Educacio´n y Ciencia of Spain. et al. 2003; Reeder and Kramer 2005), as well as to social inter- actions among adult males (Rogovin et al. 2003). Alternatively, indi- viduals might simply display age-related physiological responses to References cope with stressors (Hauger et al. 1994). The interaction between Abelson KSP, Kalliokoski O, Teilmann AC, Hau J, 2016. Applicability of sex * recapture also showed a significant influence on FCM levels, commercially available ELISA kits for the quantification of faecal immunor- which could also indicate a greater stress response by females to the eactive corticosterone metabolites in mice. In Vivo 30:739–744. novel testing environment. Higher GC levels in females have been Abrams PA, 1986. Is predator–prey coevolution an arms race? Trends Ecol previously found in this and other rodent species (Touma et al. Evol 1:108–110. 2004; Navarro-Castilla et al. 2014a, 2014b), which could be attrib- Andreolini F, Jemiolo B, Novotny M, 1987. Dynamics of excretion of urinary uted primarily to differences in the metabolism and/or excretion of chemosignals in the house mouse Mus musculus during the natural estrous GCs between both sexes (Touma et al. 2003). cycle. Experientia 43:998–1002. Overall, wood mice behavioral changes found under the preda- Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS, 2005. tion risk situations studied likely reduced the probability of an en- The effects of predator odors in mammalian prey species: a review of field counter with a predator, but they imply important trade-offs and laboratory studies. Neurosci Biobehav Rev 29:1123–1144. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 8 Current Zoology, 2017, Vol. 00, No. 00 Arenz CL, Leger DW, 2000. Antipredator vigilance of juvenile and adult Feise RJ, 2002. Do multiple outcome measures require P-value adjustment? thirteen-lined ground squirrels and the role of nutritional need. Anim Behav BMC Med Res Methodol 2:8. 59:535–541. Fletcher QE, Boonstra R, 2006. Do captive male meadow voles experience Barja I, 2009. Decision making in plant selection during the faecal-marking be- acute stress in response to weasel odour? Can J Zool 84:583–588. haviour of wild wolves. Anim Behav 77:489–493. Gallego D, Mora´n-Lo´ pez T, Torre I, Navarro-Castilla A, Barja I et al., 2017. Barja I, Escribano G, Lara C, Virgo´s E, Benito J et al., 2012. Non-invasive Context dependence of acorn handling by the Algerian mouse Mus spretus. monitoring of adrenocortical activity in European badgers Meles meles and Acta Oecol 8:1–7. effects of sample collection and storage on faecal cortisol metabolite concen- Gorman ML, Trowbridge BJ, 1989. The role of odor in the social lives of car- trations. Anim Biol 62:419–432. nivores. In: Gittleman JL, editor. Carnivore Behavior, Ecology, and Barja I, List R, 2006. Faecal marking behaviour in ringtails Bassariscus astutus Evolution. New York: Cornell University Press, 57–88. during the non-breeding period: spatial characteristics of latrines and single Goymann W, Mo¨ stl E, Van’t Hof T, East ML, Hofer H, 1999. Noninvasive faeces. Chemoecology 16:219–222. fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen Barja I, Silva´n G, Rosellini S, Pineiro ~ A, Gonza´lez-Gil A et al., 2007. Stress Comp Endocrinol 114:340–348. physiological responses to tourist pressure in a wild population of European Gurnell J, Flowerdew JR, 1994. Live Trapping Small Mammals: A Practical pine marten. J Steroid Biochem 104:136–142. Guide. 3rd edn. London: The Mammal Society. Bauman DE, 2000. Regulation of nutrient partitioning during lactation: Hamdine W, The´venot M, Sellami M, De Smet K, 1993. Re´gime alimentaire homeostasis and homeorhesis revisited. In: Cronje´ PB, editor. Ruminant de la genette (Genetta genetta Linne´, 1758) dans le Parc national du Physiology: Digestion, Metabolism, Growth and Reproduction. New York: Djurdjura, Alge´rie. Mammalia 57:9–18. CAB Publishing, 311–327. Hanski I, Henttonen H, Korpima¨ki E, Oksanen L, Turchin P, 2001. Boonstra R, Hik D, Singleton GR, Tinnikov A, 1998. The impact of Small-rodent dynamics and predation. Ecology 82:1505–1520. predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79: Hauger R, Thrivikraman K, Plotsky P, 1994. Age-related alterations of 371–394. hypothalamic–pituitary–adrenal axis function in male Fischer rats. Brown JS, 1988. Patch use as an indicator of habitat preference, predation Endocrinology 134:1528–1536. risk, and competition. Oecologia 22:37–47. Hayes RA, Morelli TL, Wright PC, 2006. Volatile components of lemur scent Brown JS, Kotler BP, 2004. Hazardous duty pay and the foraging cost of pre- secretions vary throughout the year. Am J Primatol 68:1202–1207. dation. Ecol Lett 7:999–1014. Hirschenhauser K, Mo¨ stl E, Wallner B, Dittami J, Kotrschal K, 2000. Brown JS, Kotler BP, Bouskila A, Bouskila A, 2001. The ecology of fear and Endocrine and behavioural responses of male greylag geese Anser anser to the foraging game between owls and gerbils. Ann Zool Fenn 38:71–87. pairbond challenges during the reproductive season. Ethology 106:63–77. Brown JS, Kotler BP, Smith RJ, Wirtz WO, 1988. The effects of owl predation Hutchings MR, White PCL, 2000. Mustelid scent-marking in managed ecosys- on the foraging behavior of heteromyid rodents. Oecologia 76:408–415. tems: implications for population management. Mamm Rev 30:157–169. Brown JS, Laundre´ JW, Gurung M, 1999. The ecology of fear: optimal forag- Jedrzejewski W, Jedrzejewska B, 1990. Effect of a predator’s visit on the spa- ing, game theory, and trophic interactions. J Mammal 80:385–399. tial distribution of bank voles: experiments with weasels. Can J Zool 68: Brown LE, 1969. Field experiments on the movements of Apodemus sylvaticus 761–824. L. using trapping and tracking techniques. Oecologia 2:198–222. Jedrzejewski W, Rychlik L, Jedrzejewska B, 1993. Responses of bank voles to Bu¨nning E, Moser I, 1969. Interference of moonlight with the photoperiodic odours of seven species of predators: experimental data and their relevance measurement of time by plants, and their adaptive reaction. Proc Natl Acad to natural predator–vole relationships. Oikos 68:251–257. Sci USA 62:1018–1022. Jemiolo B, Xie TM, Andreolini F, Baker AEM, Novotny M, 1991. The t com- Calder CJ, Gorman ML, 1991. The effects of red fox Vulpes vulpes faecal plex of the mouse: chemical characterization by urinary volatile profiles. odours on the feeding behaviour of Orkney voles Microtus arvalis. J Zool J Chem Ecol 17:353–367. 224:599–606. Kats LB, Dill LM, 1998. The scent of death: chemosensory assessment of pre- Clinchy M, Sheriff MJ, Zanette LY, 2013. Predator-induced stress and the dation risk by prey animals. Ecoscience 5:361–394. ecology of fear. Funct Ecol 27:56–65. Kaufman DW, Kaufman GA, 1982. Effect of moonlight on activity and micro- Dantzer B, McAdam AG, Palme R, Fletcher QE, Boutin S et al., 2010. Fecal habitat use by Ord’s kangaroo rat Dipodomys ordii. J Mammal 63: cortisol metabolite levels in free-ranging North American red squirrels: 309–312. assay validation and the effects of reproductive condition. Gen Comp Korte SM, 2001. Corticosteroids in relation to fear, anxiety and psychopath- Endocrinol 167:279–286. ology. Neurosci Biobehav Rev 25:117–142. Dı´az M, 1992. Rodent seed predation in cereal crop areas of central Spain: ef- Kotler BP, Ayal Y, Subach A, 1994. Effects of predatory risk and resource re- fects of physiognomy, food availability, and predation risk. Ecography 15: newal on the timing of foraging activity in a gerbil community. Oecologia 77–85. 100:391–396. Dı´az M, Alonso CL, Arroyo L, Bonal R, Munoz ~ A et al., 2011. Desarrollo de Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A, 2010. Moonlight un protocolo de seguimiento a largo plazo de los organismos clave para el avoidance in gerbils reveals a sophisticated interplay among time allocation, funcionamiento de los bosques mediterra´neos. In: Ramı´rez L, Asensio B, vigilance and state-dependent foraging. Proc R Soc B 277:1469. editors. Proyectos de Investigacio ´ n en Parques Nacionales: 2007–2010. Kotler BP, Brown JS, Dall SRX, Gresser S, Ganey D et al., 2002. Foraging Madrid: Organismo Auto´nomo Parques Nacionales, 47–75. games between gerbils and their predators: temporal dynamics of resource Dı´az M, Santos T, Tellerı´a JL, 1999. Effects of forest fragmentation on the depletion and apprehension in gerbils. Evol Ecol Res 4:495–518. winter body condition and population parameters of an habitat generalist, Kotler BP, Brown JS, Smith RJ, Wirtz WO, 1988. The effects of morphology the wood mouse Apodemus sylvaticus: a test of hypotheses. Acta Oecol 20: and body size on rates of owl predation on desert rodents. Oikos 53:145–152. 39–49. Lepschy M, Touma C, Hruby R, Palme R, 2007. Non-invasive measurement Dı´az M, Torre I, Peris A, Tena L, 2005. Foraging behavior of wood mice as of adrenocortical activity in male and female rats. Lab Anim 41:372–387. related to presence and activity of genets. J Mammal 86:1178–1185. Lima SL, 1998. Stress and decision making under the risk of predation: recent Dickman CR, Doncaster CP, 1984. Responses of small mammals to red fox developments from behavioral, reproductive, and ecological perspectives. Vulpes vulpes odour. J Zool 204:521–531. Adv Stud Behav 27:215–290. Eilam D, 2004. Locomotor activity in common spiny mice Acomys cahirinuse: Lima SL, Bednekoff PA, 1999. Temporal variation in danger drives antipreda- the effect of light and environmental complexity. BMC Ecol 4:16. tor behavior: the predation risk allocation hypothesis. Am Nat 153: Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G et al., 1999. 649–659. Differential behavioural and hormonal responses of voles and spiny mice to Lima SL, Dill LM, 1990. Behavioral decisions made under the risk of preda- owl calls. Anim Behav 58:1085–1093. tion: a review and prospectus. Can J Zool 68:619–640. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 9 Martı´n J, Barja I, Lo´pez P, 2010. Chemical scent constituents in feces of wild Russell BG, Banks PB, 2007. Do Australian small mammals respond to native Iberian wolves Canis lupus signatus. Biochem Syst Ecol 38:1096–1102. and introduced predator odours? Aust J Ecol 32:277–286. Millspaugh JJ, Washburn BE, Milanick MA, Slotow R, van Dyk G, 2003. Sa´nchez-Gonza´lez B, Barja I, Navarro-Castilla A, 2017. Wood mice modify Effects of heat and chemical treatments on fecal glucocorticoid measure- food intake under different degrees of predation risk: influence of acquired ments: implications for sample transport. Wildl Soc B 31:399–406. experience and degradation of predator’s faecal volatile compounds. Monclu´s R, Ro¨ del HG, Palme R, Von Holst D, de Miguel J, 2006. Chemoecology 27:115–122. Non-invasive measurement of the physiological stress response of wild rab- Sapolsky RM, Romero LM, Munck AU, 2000. How do glucocorticoids influ- bits to the odour of a predator. Chemoecology 16:25–29. ence stress responses? Integrating permissive, suppressive, stimulatory, and Monclu´s R, Ro¨ del HG, Von Holst D, de Miguel J, 2005. Behavioural and preparative actions. Endocr Rev 21:55–89. physiological responses of naı¨ve European rabbits to predator odour. Anim Sapolsky RM, 2002. Endocrinology of the stress-response. In: Becker JB, Behav 70:753–761. Breedlove SM, Crews D, McCarthy MM, Editors. Behavioral Endocrinology. Montgomery WI, Gurnell J, 1985. The behaviour of Apodemus. Symp Zool Cambridge: MIT Press, 409–450. Soc Lond 55:89–115. Scordato ES, Dubay G, Drea CM, 2007. Chemical composition of scent marks Mora´n-Lo´pez T, Ferna´ndez M, Alonso CL, Flores-Renterı´a D, Valladares F in the ringtailed lemur Lemur catta: glandular differences, seasonal vari- et al., 2015. Effects of forest fragmentation on the oak-rodent mutualism. ation, and individual signatures. Chem Senses 32:493–504. Oikos 124:1482–1491. Sih A, 1980. Optimal behavior: can foragers balance two conflicting demands? Mo¨ stl E, Palme R, 2002. Hormones as indicators of stress. Domest Anim Science 210:1041–1043. Endocrinol 23:67–74. Stoddart DM, 1982. Demonstration of olfactory discrimination by the Navarro-Castilla A, Barja I, 2014a. Antipredatory response and food intake in short-tailed vole Microtus agrestis L. Anim Behav 30:293–294. wood mice Apodemus sylvaticus under simulated predation risk by resident Streiner DL, Norman GR, 2011. Correction for multiple testing: is there a and novel carnivorous predators. Ethology 120:90–98. resolution? Chest 140:16–18. Navarro-Castilla A, Barja I, 2014b. Does predation risk, through moon phase Strier KB, Lynch JW, Ziegler TE, 2003. Hormonal changes during the mating and predator cues, modulate food intake, antipredatory and physiological and conception seasons of wild northern muriquis Brachyteles arachnoides responses in wood mice Apodemus sylvaticus? Behav Ecol Sociobiol 68: hypoxanthus. Am J Primatol 61:85–99. 1505–1512. Tortosa FS, Barrio IC, Carthey AJR, Banks PB, 2015. No longer naı¨ve? Navarro-Castilla A, Barja I, Olea PP, Pineiro ~ A, Mateo-Toma´s P et al., 2014a. Generalized responses of rabbits to marsupial predators in Australia. Behav Are degraded habitats from agricultural crops associated with elevated fae- Ecol Sociobiol 69:1649–1655. cal glucocorticoids in a wild population of common vole Microtus arvalis? Touma C, Palme R, Sachser N, 2004. Analyzing corticosterone metabolites in Mammal Biol 79:36–43. fecal samples of mice: a noninvasive technique to monitor stress hormones. Navarro-Castilla A,Dı´az M, Barja I, 2017. Does ungulate disturbance Horm Behav 45:10–22. mediate behavioural and physiological stress responses in Algerian mice Touma C, Sachser N, Mo¨stl E, Palme R, 2003. Effects of sex and time of day Mus spretus? A wild exclosure experiment. Hystrix J. doi: on metabolism and excretion of corticosterone in urine and feces of mice. 10.4404/hystrix-28.2-12332. Gen Comp Endocrinol 130:267–278. Navarro-Castilla A, Mata C, Ruiz-Capillas P, Palme R, Malo JE et al., 2014b. Virgo´s E, Llorente M, Corte´s Y, 1999. Geographical variation in genet Are motorways potential stressors of roadside wood mice Apodemus sylva- (Genetta genetta L.) diet: a literature review. Mamm Rev 29:117–126. ticus populations? PLoS One 9:e91942. Washburn BE, Millspaugh JJ, 2002. Effects of simulated environmental condi- Orrock JL, Danielson BJ, Brinkerhoff RJ, 2004. Rodent foraging is affected by tions on glucocorticoid metabolite measurements in white-tailed deer feces. indirect, but not by direct, cues of predation risk. Behav Ecol 15:433–437. Gen Comp Endocrinol 127:217–222. Penteriani V, Kuparinen A, del Mar Delgado M, Palomares F, Lo´pez-Bao JV Wingfield JC, Romero LM, 2001. Adrenocortical responses to stress and their et al., 2013. Responses of a top and a meso predator and their prey to moon modulation in free-living vertebrates. In: McEwen BS, Goodman HM, edi- phases. Oecologia 173:753–766. tors. Handbook of Physiology—Coping with the Environment: Neural and Perrot-Sinal T, Kavaliers M, Ossenkopp KP, 1999. Changes in locomotor ac- Endocrine Mechanisms. New York: Oxford University Press, 211–234. tivity following predator odor exposure are dependent on sex and repro- Wolfe JL, Summerlin CT, 1989. The influence of lunar light on nocturnal ac- ductive status in the meadow vole. In: Johnston RE, Mu¨ller-Schwarze D, tivity of the old-field mouse. Anim Behav 37:410–414. Sorensen PW, editors. Advances in Chemical Signals in Vertebrates. New Wro´bel A, Bogdziewicz M, 2015. It is raining mice and voles: which weather York: Kluber Academic/Plenum Publishers, 497–504. conditions influence the activity of Apodemus flavicollis and Myodes glareo- Pineiro ~ A, Barja I, Silva´n G, Illera JC, 2012. Effects of tourist pressure and re- lus?. Eur J Wildl Res 61:475–478. production on physiological stress response in wildcats: management impli- Ylo¨ nen H, Eccard JA, Jokinen I, Sundell J, 2006. Is the antipredatory response cations for species conservation. Wildl Res 39:532–539. in behaviour reflected in stress measured in faecal corticosteroids in a small Pulido FJ, Dıaz M, Hidalgo SJ, 2001. Size structure and regeneration of rodent? Behav Ecol Sociobiol 60:350–358. Spanish holm oak Quercus ilex forests and dehesas: effects of agroforestry use Young KM, Walker SL, Lanthier C, Waddell WT, Monfort SL et al., 2004. on their long-term sustainability. Forest Ecol Manage 146:1–13. Noninvasive monitoring of adrenocortical activity in carnivores by fecal Reeder DM, Kramer KM, 2005. Stress in free-ranging mammals: integrating glucocorticoid analyses. Gen Comp Endocrinol 137:148–165. physiology, ecology, and natural history. J Mammal 86:225–235. Zanette LY, White AF, Allen MC, Clinchy M, 2011. Perceived predation risk Rogovin K, Randall JA, Kolosova I, Moshkin M, 2003. Social correlates of reduces the number of offspring songbirds produce per year. Science 334: stress in adult males of the great gerbil Rhombomys opimus in years of high 1398–1401. and low population densities. Horm Behav 43:132–139. Zanette LY, Clinchy M, Suraci JP, 2014. Diagnosing predation risk effects on Romero LM, 2002. Seasonal changes in plasma glucocorticoid concentrations demography: can measuring physiology provide the means? Oecologia 176: in free-living vertebrates. Gen Comp Endocrinol 128:1–24. 637–651. Romero LM, 2004. Physiological stress in ecology: lessons from biomedical Zwijacz-Kozica T, Selva N, Barja I, Silva´n G, Martı´nez-Ferna´ndez L et al., research. Trends Ecol Evol 19:249–255. 2013. Concentration of fecal cortisol metabolites in chamois in relation to Rothman KJ, 1990. No adjustments are needed for multiple comparisons. tourist pressure in Tatra National Park (South Poland). Acta Theriol 58: Epidemiology 1:43–46. 215–222. 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Foraging, feeding, and physiological stress responses of wild wood mice to increased illumination and common genet cues

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Abstract

In nature, animals are exposed to a broad range of threats imposed by predators, which may strongly influence the ecology of prey species directly or indirectly by affecting their behavior via fear of predation. Here, we studied wood mice Apodemus sylvaticus behavioral and physiological responses to simulated predation risk. Risk avoidance was analyzed by live trapping with control traps and traps treated with feces of common genet Genetta genetta (direct cue of risk) under new moon nights and following by simulated full moon conditions (indirect cue). The time devoted to foraging behavior and capture time were analyzed by video recording mice activity around traps. Food intake was calculated based on the amount of bait remaining in each trap. Fecal cortico- sterone metabolites (FCMs) were measured by enzyme-immunoassay as indicators of physio- logical stress responses. Fewer wood mice were captured during full moon, yet only non-breeding adult males clearly avoided common genet odor. Mice were captured sooner at night during the simulated full moon conditions and later in predator-treated traps. Foraging activity was lower when individuals faced predator’s feces, but neither food intake nor FCM levels were affected by predation risk cues. Direct and indirect cues of predation risk selectively affected wood mice behav- ior, although behavioral responses seem to be modulated by different costs–benefit balances related to the individual’s perception of risk. The lack of physiological responses to predation risk cues suggests that wood mice did not perceive them as reliable stressors or the response was too small or transient to be measured by FCM. Key words: common genet, fecal predator cues, feeding, foraging, moonlight, predator avoidance. Predation represents one of the most important causes of death for or avoid predation risk (Lima and Dill 1990; Kats and Dill 1998; small mammals and it strongly influences prey ecology directly Lima 1998). Thus, prey are attuned to respond in a number of be- through mortality (Brown et al. 1999; Hanski et al. 2001)or havioral and physiological ways to cues associated with predation through indirect effects on prey demographic and behavioral re- risk that can be direct (signals associated to predators: presence, sponses to predators (Lima and Dill 1990; Apfelbach et al. 2005; urine, feces, or sounds) or indirect (e.g., habitat complexity or envir- Dı´az et al. 2005; Zanette et al. 2011; Navarro-Castilla and Barja onmental conditions) (Eilam et al. 1999; Orrock et al. 2004; Wro´ bel 2014a, 2014b). Because animals are exposed to a wide range of dan- and Bogdziewicz 2015). gers imposed by predators, they have developed a variety of preda- Most carnivores use secretions from glands, urine, and feces to tor detection mechanisms and antipredatory responses to minimize mark their territory (Hutchings and White 2000; Barja and List V C The Author (2017). 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/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 2 Current Zoology, 2017, Vol. 00, No. 00 2006; Barja 2009; Martı´n et al. 2010; Pineiro ~ et al. 2012) and mul- we studied whether these cues of increased predation risk affected: tiple studies have revealed that several rodent species are sensitive to (1) wood mouse behavior (i.e., avoidance of predator-treated traps the scent of potential predators, avoiding such chemical signals and foraging activity), (2) food intake, and (3) physiological stress without needing other cues (Stoddart 1982; Dickman and Doncaster response in wood mice. Further, the influence of individual charac- 1984; Calder and Gorman 1991; Jedrzejewski et al. 1993; Navarro- teristics (i.e., sex, reproductive activity, and age) on these responses Castilla and Barja 2014a, 2014b). Furthermore, prey species often was also evaluated. The common genet is an important threat for alter their behavior in response to the auditory, visual, and chemo- small mammals, especially for wood mice (Hamdine et al. 1993; sensory cues from predators (Lima and Dill 1990; Kats and Dill Virgo´ s et al. 1999). Since variation in predation risk affects foraging 1998; Eilam et al. 1999; Zanette et al. 2011; Clinchy et al. 2013; decisions (Lima and Bednekoff 1999), we predicted that wood mice Tortosa et al. 2015). Thus, in that prey species are at risk of preda- would alter their foraging behavior when confronted with common tion while performing daily activities, there are tradeoffs between genet feces and they would also avoid entering the predator-treated antipredator behavior and other fundamental activities like foraging traps, especially under high illumination (simulated full moon). and feeding (Sih 1980; Brown et al. 1988; Brown 1988; Orrock Further, wood mice were expected to vary food intake in response et al. 2004; Gallego et al. 2017; Sa´nchez-Gonza´lez et al. 2017). to their perceived predation risk prior to entering the trap (owing In addition, antipredatory behavior can be strongly influenced by both to increased illumination and the presence of predator feces), the environment. Thus, increased predation risk perception but also because of the likely detection of common genet fecal odor through lower habitat complexity or higher visibility has revealed by individuals within treated traps. Finally, we expected that expos- that rodent species will avoid open areas and decrease activity on ure to increased illumination and to common genet feces would nights with a full moon (Kaufman and Kaufman 1982; Kotler evoke physiological stress responses in wood mice as measured by et al. 1988; Wolfe and Summerlin 1989; Kotler et al. 1994; Brown fecal GC metabolites. et al. 2001; Kotler et al. 2002; Eilam 2004; Kotler et al. 2010). Few studies have attempted to determine whether prey responses to predation risk situations are influenced by individual character- Materials and Methods istics (e.g., sex, breeding condition, and age of individuals) Study area (Dickman and Doncaster 1984; Jedrzejewski and Jedrzejewska Field work was carried out in the savanna-like holm oak Quercus 1990). ilex woodlands of the National Park of Cabaneros ~ (Central Spain, Responses to predation risk should not be restricted only to be- 30S 385450, UTM 4353479). In this system, large oak trees grow havioral responses because, under certain risky situations, prey may scattered (mean tree density is 14 ha ) on a grassland matrix with display physiological responses which are not translated into a almost no shrub cover (<1%; see Pulido et al. 2001; Dı´az et al. modification of behavior (Eilam et al. 1999). When animals are sub- 2011). jected to a stressor, the hypothalamus releases corticotrophin releas- ing hormone inducing the anterior pituitary to secrete the Experimental design: live trapping and simulation of adrenocorticotropic hormone (ACTH) which signals the adrenal cortex to release glucocorticoids (GC) to help the individuals to predation risk cope with the stressful situation (Sapolsky et al. 2000). Thus, GC Prior to the beginning of the experimental study, to determine which concentrations can be used as a hormonal measure of physiological trees were occupied by wood mice and to allow mice to acclimate to stress responses (Wingfield and Romero 2001; Mo¨stl and Palme traps, Sherman traps were placed beneath trees (n ¼ 170) in 2 study 2002). In fact, GC metabolites in feces have been reported in several sites (separated by 1,500 m) over a 3-day period. Afterward, during vertebrate species as a useful non-invasive technique for assessing the experimental study (Figure 1), Sherman traps (n ¼ 2/tree) were adrenocortical function (Mo¨stl and Palme 2002; Monclu´ s et al. placed in those trees (n ¼ 40) confirmed to be occupied by wood 2006; Lepschy et al. 2007; Dantzer et al. 2010; Barja et al. 2012; mice. Since predator’s odors have been previously shown to evoke Pineiro ~ et al. 2012; Zwijacz-Kozica et al. 2013; Navarro-Castilla antipredatory responses in small mammals (Dickman and Doncaster et al. 2014a, 2014b). In mammals, GC plays an important role in re- 1984; Navarro-Castilla and Barja 2014a, 2014b), we manipulated sponding to diverse factors such as social conflicts and human dis- the direct perception of predation risk through predator odor from turbances (Sapolsky et al. 2000; Romero 2002; Barja et al. 2007; one of the main rodent predators in the study area, the common Navarro-Castilla et al. 2014a, 2014b). Since stressful situations usu- genet G. genetta. To examine the effect of predator odor, nearby ally evoke an increase in GC production, predators could induce occupied trees were randomly paired and treatments (traps treated physiological responses in their prey by a physical attack but also by with predator odor) and control (untreated traps) were assigned to making them fearful of an imminent attack (Boonstra et al. 1998; one tree of each pair at random. Mean distance between predator- Eilam et al. 1999; Hirschenhauser et al. 2000; Korte 2001; Monclu´s treated and paired control trees was 42.79 m (range 8.20–80.36 m). et al. 2005; Clinchy et al. 2013; Zanette et al. 2014). Similarly, Predator treatment consisted in fresh feces of common genet col- increased illumination could act as a potential stressor for noctur- ~ lected from captive animals of the Canada Real Open Center nally active prey species. However, few studies have previously eval- (Madrid, Spain). To prevent volatile compounds variation in rela- uated its effect on the physiological stress response (Navarro- tion to seasonal or individual factors (Andreolini et al. 1987; Castilla and Barja 2014b). Jemiolo et al. 1991; Hayes et al. 2006; Scordato et al. 2007; Martı´n In the present study, we tested whether wood mice Apodemus et al. 2010), all collected feces were mixed to obtain a homogeneous sylvaticus showed behavioral and physiological changes due to mixture avoiding possible bias in our results. Predator treatment increased predation risk due to moonlight (i.e., natural new moon was made following methods by Navarro-Castilla and Barja and simulated full moon conditions) and exposure to predator odor (2014a), 100 g of homogenized fecal sample was mixed with from an invasive species, the common genet Genetta genetta. Thus, 100 mL of distilled water obtaining a mixture similar to real fresh Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 3 Figure 1. Flow chart of the experimental study. feces. Predator presence was simulated by leaving an equal amount tripod 60 cm tall located 1 m away and focused on Sherman traps, (5 g) of feces at the entrance of treated traps and it was renewed covering a field of vision of 1 m . Video-cameras were provided every day at dusk. with ELRO dvr32 card-based recorders (settings 5 frames/s and To test the effect of moonlight, the above mentioned experimen- using 16 GB recording cards replaced each day). Both the recording tal design was carried out during 5 consecutive new moon nights and the illumination devices were fully autonomous since they were (20–24 March 2012); afterward, the following 5 nights we simu- powered by car batteries (70 Ah, lead-acid) attached to solar panels lated full moon light conditions at the same sites by means of artifi- (ono-silicon erial P_20; 20 w). However, they were turned on each cial illumination. The illumination device (composed of 3 white and day at dusk, before opening traps and renewing predator odor. Mice 3 blue led lights grouped behind a diffusion screen simulating a dif- foraging behavior, recorded as the time (s) since individuals ap- fuse light with the spectral composition of moonlight) was hung peared in the image until they went inside the trap closing it, was down from the tree canopy at a height of 2 m to simulate a light in- videotaped during trapping sessions. We also recorded at what time tensity of 1 lux at ground level (measured by means of a TES-1332A of the night each individual was captured allowing us to know the luxometer). Light intensity of 1.0 lux approximately corresponds to time spent by each individual inside traps. the maximum moonlight intensity expected during full moon nights To determine the amount of food eaten, bait remains were oven- in this region (Bu¨ nning and Moser 1969). dried at 50 C (Selecta, model CONTERM 2000208) and weighed Sherman traps were activated at dusk, and trap checks were car- (Giros PG-500; precision 0.01 g). Body weight of individuals was ried out 10–12 h later (at dawn) to minimize the time that animals positively correlated with food intake (r ¼ 0.67, P ¼ 0.002); there- were kept. Nest material (raw wool with natural lanolin) was used as fore, food intake by an individual was divided by its body weight to bedding inside traps. All traps were baited with 4 g of toasted corn. control the effect of body weight on food intake. Captured individuals were identified to species. Sex and reproductive condition was determined from external characteristics (Gurnell and Feces collection and fecal corticosterone Flowerdew 1994); adult males with enlarged testicles descended into metabolites quantification the scrotal sac and females showing noticeable nipples and/or the va- Fresh feces were collected from traps where individuals were cap- ginal membrane perforated were classified as reproductively active. tured, if urine was detected fecal samples were excluded in order to In addition, a 100 g hand-held scale was employed to measure body avoid cross contamination (Touma et al. 2003). To avoid the effects weight which was used to estimate relative age following Navarro- of environmental conditions and microorganisms proliferation on Castilla and Barja (2014a) (juveniles: <13 g; sub-adults: from 13 g to fecal corticosterone metabolite (FCM) levels (Washburn and <20 g; adults: 20 g). Individuals were marked in non-conspicuous Millspaugh 2002; Millspaugh et al. 2003), only fresh feces (i.e., with areas with harmless paints (red food coloring: Ponceau-4R E124) for a soft texture and not dried) were collected. Fecal samples were col- individual identification and to control for recaptures. Animals were lected between sunrise and 2 h after; thus, by only collecting fresh quickly handled (<1 min) and then released at the same point of cap- feces during the early morning we avoided circadian rhythm effects ture. Manipulations of animals were done in compliance with the on excretion patterns (Touma et al. 2003). Corticosterone peak con- European Communities Council Directive 86/609/EEC for animal centrations have been observed in wood mice feces on average at experiments and were carried out under the permit of the Cabaneros 10 h after ACTH injection (range: 8–12 h; see the “results” section); National Park authorities. therefore, fecal samples from individuals trapped >8 h were rejected to avoid any possible effect of the capture in FCM levels. Fecal sam- Mice foraging behavior and food intake ples were stored in the freezer at 20 C until analysis. To control For recording wood mice foraging behavior, video-cameras for potential observer bias, we used blind observation by coding (OmniVision CMOS 380 LTV, 3.6 mm lens) were mounted on a samples before laboratory analysis of FCM concentrations. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 4 Current Zoology, 2017, Vol. 00, No. 00 Extraction of FCM from fecal samples was done according to Table 1. Results of the fit of a log-linear model analyzing the effects of individual and predation risk factors on the capturability of the modified method of Touma et al. (2003). Fecal samples were un- wood mice frozen and dried in the heater until constant weight. We placed 0.05 g of dry feces in assay tubes with 0.5 mL of phosphate buffer 2 Effect df G P and 0.5 mL of 80% methanol, then, they were shaken for 16 h and Sex/age 2 7.38 0.025 supernatants were centrifuged at 2,500  g for 15 min. Pellets were Breeding condition 1 10.68 0.001 discarded and the fecal extracts were stored at 20 C until ana- Sex/age * breeding condition 1 6.66 0.010 lyzed. Quantification was achieved using a commercial cortico- Treatment 1 0.36 0.548 sterone enzyme immunoassay (EIA) (Demeditec Diagnostics GmbH, Moonlight 1 12.35 0.000 Kiel, Germany) previously validated for measuring FCM in mice Moonlight * sex/age 2 3.03 0.220 species (Abelson et al. 2016; Navarro-Castilla et al. 2017). Moonlight * breeding condition 1 0.15 0.695 Parallelism, accuracy, and precision tests were done to validate the Treatment * moonlight 1 0.04 0.843 EIA (Goymann et al. 1999; Young et al. 2004). Parallelism was per- Treatment * sex/age 2 1.94 0.379 formed with serial dilutions of fecal extracts (1:32, 1:16, 1:8, 1:4, Treatment * breeding condition 1 0.21 0.644 1:2, 1:1) resulting in a curve parallel to the standard. Accuracy (re- Treatment * moonlight * sex/age 2 0.42 0.809 Treatment * moonlight * breeding condition 1 0.14 0.712 covery) was 118.66 31.7% (n ¼ 6). Precision was tested through Treatment * sex/age * breeding condition 1 6.54 0.011 intra- and inter-assay coefficients of variation for 3 biological sam- Moonlight * sex/age * breeding condition 1 1.01 0.316 ples, being 4.7% (n ¼ 6) and 8.2% (n ¼ 3), respectively. In each Treatment * moonlight * sex/age * breeding condition 1 0.97 1.000 assay, we used a standard, whose corticosterone concentration was known, included in the Demeditec kit. The assay was excluded and samples were reanalyzed if standard corticosterone concentrations deviated >10% from the expected value. The assay detection limit (except age factor) and we included the time that each individual (sensitivity) for corticosterone metabolites was 4.1 ng/mL. spent inside the trap as covariate. Finally, variation in FCM was Furthermore, a biological validation was carried out to confirm the analyzed by GLMs, including moon phase, treatment, sex, breeding suitability of the EIA for wood mouse fecal samples. Thus, following condition, and recapture as fixed factors and body weight of individ- the procedure by Touma et al. (2004), we injected a high dose uals was included as covariate. Foraging behavior and FCM were (60 mg/100 g of body weight) of synthetic ACTH (Synacthen Depot, log-transformed as needed to normalize the distributions of Novartis, Germany) into 5 captive individuals (2 females and 3 residuals. males). Samples of each of the 5 individuals were collected within The GLMs included the main effects of the factors studied and minutes after defecation and immediately stored in Eppendorfs at their 2-way interactions. Results were considered significant at 20 C until analysis. Sampling times were: 0, 2, 4, 6, 8, 10, 12, 14, a< 0.05. The probability of committing table-wise type-I errors was 18, 22, and 26 h post-injection. FCM levels are expressed as nano- judged low (ca. 18%; 4 comprehensive test made at a ¼ 0.05; grams per gram dry feces. Streiner and Norman 2011), so that we did not perform adjustments Higher FCM concentrations detected in the present study are for multiple comparisons to avoid the risk of committing type-II similar to those analyzed using the same methodology in another errors (Rothman 1990; Feise 2002). Results are given as closely related rodent species, the Algerian mouse (Mus spretus), mean6 standard error (SE). We used the SPSS 15.0 statistical soft- inhabiting the same study area (Navarro-Castilla et al. 2017). ware (SPSS Inc., Chicago, IL, USA). This may be attributable to the very low limit of detection (553 pg/ mL) of the Demeditec kit, which is known to detect higher FCM concentrations than other available commercial kits (see Abelson Results et al. 2016). Risk avoidance by wood mice Overall, 153 wood mice (71 new captures and 82 recaptures) were Data analysis captured. The study population was dominated by adults (80.3% Capture frequencies according to odor and moonlight treatments, as vs. 19.7%), females (56.1% vs. 43.9% males), and reproductively well as their interactions with individual characteristics (sex, age, active females (53% vs. 20% reproductively active males; Table 1). and breeding condition) were analyzed by fitting log-linear models Regarding predation risk factors, simulated full moon conditions to the 5-way contingency table generated by the factors odor (con- decreased the number of captures compared with the natural new trol/common genet feces), moonlight (new moon/simulated full moon phase (36.5% vs. 63.5%, respectively) while predator treat- moon), sex/age (adult male, adult female, or juvenile), breeding con- ment did not significantly decrease wood mice captures (46.5% vs. dition (active or not), and presence/absence of capture, taking into 53.5% control traps) (Table 1 and Figure 2A). Nevertheless, we account the structural zeros resulting from the impossibility of find- found a significant interaction between treatment * sex/ ing sexually active juveniles (Dı´az et al. 1999; Mora´n-Lo´ pez et al. age * breeding condition (Table 1) showing that non-breeding adult 2015). Recaptures were not taken into account in the captures fre- males clearly avoided common genet feces (v ¼ 7.04, df ¼ 1, quencies tests to maintain data independence. P ¼ 0.008; Figure 2B). None of the interactions among predator risk We used general linear models (GLMs) to analyze differences in factors were significant (Table 1). foraging behavior due to moonlight (natural new moon/simulated full moon), treatment (control/fecal odor), sex (male/female), breed- ing condition (breeding/non-breeding), age (juveniles/sub-adults/ Mice foraging behavior and food intake adults), and recapture (new capture/recapture). We also employed Wood mice were captured sooner at night during simulated full moon 0 0 GLMs to test variation in food intake (corrected by animal’s body conditions (5 h 1 6 34 after trap activation) than during new moon 0 0 weight); fixed factors were the same as in the foraging activity model nights (6 h 45 6 34)(F ¼ 5.77, P¼ 0.019). Further, individuals 1,76 Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 5 Figure 3. Effect of treatment (control vs. common genet) on wood mice forag- ing behavior (s, mean6 SE). Significant differences are indicated by asterisks (*P< 0.05). Table 3. Food intake by wood mice in relation to predation risk and Figure 2. Percentage of wood mice captured in relation to direct (common individual factors genet feces) and indirect (moonlight) cues of predation risk (A). Percentage of captures according to treatment, sex/age, and breeding condition (B). Factor df FP Asterisks indicate significant differences between the analyzed groups (**P< 0.01; ***P< 0.001). Moonlight 1 3.579 0.065 Treatment 1 1.432 0.238 Sex 1 0.019 0.890 Table 2. Results of GLMs testing for the effects of predation risk Breeding condition 1 8.486 0.006 and individual factors on wood mice foraging behavior Recapture 1 6.563 0.231 Time inside trap 4 2.608 0.114 Factor df FP Error 55 Moonlight 1 0.301 0.587 Treatment 1 6.945 0.013 Sex 1 1.176 0.286 Breeding condition 1 2.554 0.120 to 40,420 ng/g feces. In the 5 individuals, the corticosterone EIA de- Relative age 1 1.680 0.202 tected an average increase in FCM concentrations ranging from Recapture 1 1.366 0.271 116% to 247% within 8–12 h of the injection event. Subsequent to Error 59 that, a downward trend toward baseline FCM values was detected within 12–18 h, validating the corticosterone EIA for the analysis of wood mouse fecal samples. 0 0 were captured sooner in control traps (at 5 h 5 6 34 ) compared with FCM levels were analyzed in 107 fresh fecal samples. Neither traps treated with common genet feces in which individuals were cap- moonlight nor predator odor emerged as significant factors influenc- 0 0 tured later during the night (6 h 40 6 34)(F ¼ 4.66, P ¼ 0.034). 1,76 ing FCM levels. Factors explaining the variation found in FCM con- Treatment was the only significant factor explaining the variation centrations are presented in Table 4. Body weight of individuals was found in foraging behavior before entering traps (Table 2); individuals positively correlated with FCM levels (Table 4). Overall, FCM levels spent less time foraging when they were subjected to predator were lower in males (130,6956 53,407 ng/g dry feces) than in fe- fecal cues (24.566 2.60 s) than when they faced control traps males (138,7626 41,306 ng/g dry feces) and individuals showed (31.546 4.67 s; Table 2 and Figure 3). The amount of food consumed lower FCM levels when they were recaptured (84,9286 35,891 ng/g was not related to the amount of time that animals spent inside traps, dry feces) than when they were captured for the first time or by their previous capture history. Further, neither common genet (165,0026 47,982 ng/g dry feces). However, the only significant feces nor illumination influenced food intake. Only breeding condition interaction between sex * recapture revealed that significant differ- emerged as a significant factor (Table 3), with breeding individuals ences in FCM were between females captured for the first time and having a significantly lower food intake (0.0916 0.008 g/g) than non- recaptured males (Table 4 and Figure 4). breeding individuals (0.1746 0.013 g/g). Interactions among factors were not statistically significant. Discussion Physiological stress response Risk avoidance by wood mice In the biological validation experiment, measured FCM baseline lev- A decrease in activity during full moon conditions has been els (prior to injection) for each tested individual ranged from 13,120 described as a generalized antipredatory behavior in prey species Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 6 Current Zoology, 2017, Vol. 00, No. 00 Table 4. Results of a general lineal model testing the effects of indi- significantly different from random expectations for non-breeding vidual and predation risk factors on fecal glucocorticoid metabol- adult males only. Coincident with these results, Dickman and ites in wood mice Doncaster (1984) showed that male wood mice exhibited a higher avoidance of predator feces than females did. However, in our case, Factor df FP breeding males did not show such avoidance. Their social, sexual, Moonlight 1 2.690 0.105 and territorial-related behaviors during the breeding season Treatment 1 0.025 0.875 (Montgomery and Gurnell 1985) and their attraction to new objects Sex 1 0.177 0.675 (Brown 1969) could be possible explanations for the results. Similar Breeding condition 1 0.170 0.681 differences in response to predator cues due to sex and breeding con- Recapture 1 1.235 0.270 dition were also found in bank voles Clethrionomys glareolus by Body weight 1 5.660 0.020 Jedrzejewski and Jedrzejewska (1990). Therefore, sex and breeding Sex * recapture 1 4.178 0.044 condition differences in the responses to predation risk suggest that Error 90 gonadal hormones may be involved in the mediation of the antipre- datory responses (Perrot-Sinal et al. 1999). On the other hand, young mammals typically devote less time to predator detection (Arenz and Leger 2000) which could explain why juveniles were equally captured although predation risk cues increased. Therefore, while indirect risk cues (moonlight) seem to be perceived by most in- dividuals as a more reliable indicator of enhanced predation risk (Orrock et al. 2004), responses to direct cues (predator feces) are not generalized, but vary among individuals according to the indi- vidual’s characteristics and in all likelihood, their previous experi- ence (Lima and Bednekoff 1999). Mice foraging behavior and food intake Predation risk perception may influence animal daily decision mak- ing to choose when, where, and how long to forage. According to Lima and Bednekoff (1999), under high risk situations prey reduce time spent in daily activities to optimize the energy spent on antipre- datory behavior. Several studies have reported that under high levels of risk, individuals decreased mobility and concentrated foraging ac- tivity in safer habitats (Lima and Dill 1990; Dı´az 1992; Kotler et al. 2002). Our results also showed predation risk influencing foraging behavior. Thus, when traps were treated with common genet feces, Figure 4. Log-transformed concentrations (mean6 SE) of fecal glucocorticoid wood mice apparently delayed foraging close to these traps and metabolites (FCM, ng/g dry feces) in males and females in relation to new were captured later at night. Despite that delay, once individuals captures or recaptures. were detected in the vicinity of a trap, they devoted less time to for- aging, entering feces-treated traps more rapidly than control traps. In relation to moonlight, wood mice were trapped sooner during (Kotler et al. 2010; Penteriani et al. 2013). This common behavioral simulated full moon conditions, but no effect of moonlight was response could explain why fewer wood mice were captured during found on foraging behavior. These results perfectly match those of the simulated full moon conditions, matching this result with the Dı´az et al. (2005), who found that wood mice reduced foraging be- moonlight avoidance found in wood mice under natural full moon havior in response to the presence or activity of common genets but nights (Navarro-Castilla and Barja 2014b). The number of newly there was no effect of moonlight on foraging activity. Apart from ef- captured individuals during the full moon treatment could also have fects of the different nature and meaning of both predation risk cues been influenced by the design of our study, because it was carried (direct cues indicate predator presence nearby, whereas indirect cues out after the new moon treatment and had a smaller pool of poten- just general levels of danger), results may be also explained by tem- tial new animals to catch. However, the reduction in the number of poral variation in their intensity. Predator odor intensity surely both newly captured and recaptured individuals supported the over- decreased through the night, so that wood mice delayed foraging all negative effect of increased illumination on wood mice foraging. and foraged more rapidly when facing predator feces, consistent Therefore, moonlight can indicate a higher risk of predation since with this decreasing intensity of the direct cue. However, moonlight an individual’s vulnerability to a predator depends partly upon visi- intensity was constant over the night, so that perception of risk, and bility. On the other hand, predator odor might provide direct infor- hence responses, did not decrease. According to Lima and Bednekoff mation on predation risk even when the predator is absent at the (1999), animals under longer periods of high risk (e.g., full moon time of detection. In this study, the number of captures decreased in nights) are forced to decrease antipredatory behavior and forage to traps treated with common genet feces, coincident with several stud- meet their energy demands. This hypothesis could explain why al- ies where avoiding areas marked by predators was common in small though moonlight is supposed to increase perceived predation risk mammals (Dickman and Doncaster 1984; Calder and Gorman and wood mice were expected to decreased food intake we did not 1991; Russell and Banks 2007). However, this antipredatory re- find significant differences. Alternatively, as the full moon experi- sponse varied depending on individual characteristics, being ment was carried out after the new moon sampling, this might be an Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 7 effect of treatment order (i.e., first new moon directly following by between the benefits of safety from predation and the costs associ- the full moon experiments) and previous experience. Thus, as a re- ated with missing opportunities for foraging or reproduction sult of being repeatedly captured during both moon phases, wood (Abrams 1986; Lima and Dill 1990; Brown et al. 1999; Brown and mice may have become accustomed and would have valued the Kotler 2004). Besides being an invasive species, common genets benefits of obtaining food over the risk perceived via illumination. defecate in latrines, so their feces may be less indicative of their pres- Regarding individual factors, only breeding condition led to signifi- ence or movement patterns, and therefore, a generalized antipreda- cant differences in food intake. Overall, prey have to trade off food tory response would not lead to survival benefits that would and safety under each situation, but they also have to prioritize outweigh the cost of lost foraging opportunities. Thus, wood mice between different daily activities. In this regard, we conservatively are expected to exhibit different antipredatory responses only when speculate that breeding individuals could be more careful they have an accurate assessment of the current predation risk, and under risky situations reducing feeding and allocating more time to making decisions, choosing those behavioral options which maxi- survive and breed. mize their fitness, for example, delaying and reducing foraging activ- ity when facing common genet fecal cues. Nevertheless, behavioral responses seem to depend on context, past experience, and individ- Physiological stress response ual variation (Gorman and Trowbridge 1989). The apparent ab- Generally, short-term GC secretion last only a few hours and pro- sence of a GC stress responses to factors that are presumably related motes successful adaptive responses to a stressful stimulus to predation risk (i.e., moonlight and predator odor) suggests that (Wingfield and Romero 2001), whereas chronic stress occurs when these factors are not perceived as reliable stressors by wood mice. individuals experienced either multiple, frequent exposure to stres- So, making decisions by altering behavioral responses seem to be sors, and/or long-term continuous exposure to stressors which gen- better, faster, and a more useful option to maximize fitness. erates elevated and prolonged high GC levels exceeding the individual level of beneficial adaptation and leading to pathological consequences (Mo¨ stl and Palme 2002; Sapolsky 2002; Romero Author Contributions 2004). Physiological responses due to simulated predation risk by owl calls were previously found for voles and mice (Eilam et al. Conceptualization: A.N.C., I.B., and M.D.; Methodology: A.N.C.; 1999). However, studies where predation risk was simulated with Data analysis: A.N.C., I.B., and M.D.; Writing—original draft prep- predator odor did not evoke any physiological response in different aration: A.N.C.; Writing—review and editing: A.N.C., I.B., and rodent species (bank voles and weasels: Ylo¨ nen et al. 2006; meadow M.D.; and Funding acquisition: A.N.C., I.B., and M.D. voles and weasels: Fletcher and Boonstra 2006). In the present The authors are very grateful to Miguel Ferna´ndez, Vero´ nica study, neither moonlight nor exposure to predator feces had any in- Alonso, David Lo´ pez, and Javier Jime´nez for their help during field fluence on FCM in wood mice, a result similar to the lack of effect work. They thank the authorities and staff of the Cabaneros ~ of natural moonlight conditions and red fox fecal odor on the National Park who allowed them to develop their studies there. physiological stress response of wood mice found by Navarro- They also thank Dr Vincenzo Penteriani for their generous help in Castilla and Barja (2014b). Thus, perceived predation risk does not reviewing a previous version of this manuscript, and Dr James Hare appear to be sufficient to elicit increased FCM levels in the wood and 2 anonymous reviewers for their useful comments and sugges- mouse. Both the delay in approaching feces-treated traps and tions to improve the present work. reduced foraging behavior when in proximity to such traps could re- duce the individual’s perceived predation risk so as to preclude a physiological stress response, or diminish that response in magni- Funding tude or duration to the point that it escaped detection by our FCM This work was partially supported by the project RISKDISP (CGL2009- assay. Alternatively, inter-individual variation in FCM levels could 08430/BOS) and Comunidad de Madrid together with the European Social result in insufficient statistical power to detect significant differences Fund and Universidad Auto´noma de Madrid (CCG10-UAM/AMB-5325). among predation risk treatments. Regarding the effect of individual This study is a contribution to the projects MONTES [CSD2008-00040], factors, we found that body weight of individuals, which is closely RISKDISP [CGL2009-08430], and VULGLO [CGL2010-22180-C03-03], related to the age of individuals (Gurnell and Flowerdew 1994), was funded by the Spanish Ministerio de Ciencia e Innovacio´n; 096/2002 and positively correlated with FCM levels. Adults may have exhibited 003/2007, funded by the Organismo Auto´nomo Parques Nacionales; and higher FCM levels as a consequence of their breeding condition, that ANASINQUE [PGC2010-RNM-5782], funded by the Junta de Andalucı´a. is, changes due to pregnancy and lactancy (Bauman 2000; Strier A.N.-C. was supported by a FPU scholarship [AP2008-03430] from the Ministerio de Educacio´n y Ciencia of Spain. et al. 2003; Reeder and Kramer 2005), as well as to social inter- actions among adult males (Rogovin et al. 2003). Alternatively, indi- viduals might simply display age-related physiological responses to References cope with stressors (Hauger et al. 1994). The interaction between Abelson KSP, Kalliokoski O, Teilmann AC, Hau J, 2016. Applicability of sex * recapture also showed a significant influence on FCM levels, commercially available ELISA kits for the quantification of faecal immunor- which could also indicate a greater stress response by females to the eactive corticosterone metabolites in mice. In Vivo 30:739–744. novel testing environment. Higher GC levels in females have been Abrams PA, 1986. Is predator–prey coevolution an arms race? Trends Ecol previously found in this and other rodent species (Touma et al. Evol 1:108–110. 2004; Navarro-Castilla et al. 2014a, 2014b), which could be attrib- Andreolini F, Jemiolo B, Novotny M, 1987. Dynamics of excretion of urinary uted primarily to differences in the metabolism and/or excretion of chemosignals in the house mouse Mus musculus during the natural estrous GCs between both sexes (Touma et al. 2003). cycle. Experientia 43:998–1002. Overall, wood mice behavioral changes found under the preda- Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS, 2005. tion risk situations studied likely reduced the probability of an en- The effects of predator odors in mammalian prey species: a review of field counter with a predator, but they imply important trade-offs and laboratory studies. Neurosci Biobehav Rev 29:1123–1144. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 8 Current Zoology, 2017, Vol. 00, No. 00 Arenz CL, Leger DW, 2000. Antipredator vigilance of juvenile and adult Feise RJ, 2002. Do multiple outcome measures require P-value adjustment? thirteen-lined ground squirrels and the role of nutritional need. Anim Behav BMC Med Res Methodol 2:8. 59:535–541. Fletcher QE, Boonstra R, 2006. Do captive male meadow voles experience Barja I, 2009. Decision making in plant selection during the faecal-marking be- acute stress in response to weasel odour? Can J Zool 84:583–588. haviour of wild wolves. Anim Behav 77:489–493. Gallego D, Mora´n-Lo´ pez T, Torre I, Navarro-Castilla A, Barja I et al., 2017. Barja I, Escribano G, Lara C, Virgo´s E, Benito J et al., 2012. Non-invasive Context dependence of acorn handling by the Algerian mouse Mus spretus. monitoring of adrenocortical activity in European badgers Meles meles and Acta Oecol 8:1–7. effects of sample collection and storage on faecal cortisol metabolite concen- Gorman ML, Trowbridge BJ, 1989. The role of odor in the social lives of car- trations. Anim Biol 62:419–432. nivores. In: Gittleman JL, editor. Carnivore Behavior, Ecology, and Barja I, List R, 2006. Faecal marking behaviour in ringtails Bassariscus astutus Evolution. New York: Cornell University Press, 57–88. during the non-breeding period: spatial characteristics of latrines and single Goymann W, Mo¨ stl E, Van’t Hof T, East ML, Hofer H, 1999. Noninvasive faeces. Chemoecology 16:219–222. fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen Barja I, Silva´n G, Rosellini S, Pineiro ~ A, Gonza´lez-Gil A et al., 2007. Stress Comp Endocrinol 114:340–348. physiological responses to tourist pressure in a wild population of European Gurnell J, Flowerdew JR, 1994. Live Trapping Small Mammals: A Practical pine marten. J Steroid Biochem 104:136–142. Guide. 3rd edn. London: The Mammal Society. Bauman DE, 2000. Regulation of nutrient partitioning during lactation: Hamdine W, The´venot M, Sellami M, De Smet K, 1993. Re´gime alimentaire homeostasis and homeorhesis revisited. In: Cronje´ PB, editor. Ruminant de la genette (Genetta genetta Linne´, 1758) dans le Parc national du Physiology: Digestion, Metabolism, Growth and Reproduction. New York: Djurdjura, Alge´rie. Mammalia 57:9–18. CAB Publishing, 311–327. Hanski I, Henttonen H, Korpima¨ki E, Oksanen L, Turchin P, 2001. Boonstra R, Hik D, Singleton GR, Tinnikov A, 1998. The impact of Small-rodent dynamics and predation. Ecology 82:1505–1520. predator-induced stress on the snowshoe hare cycle. Ecol Monogr 79: Hauger R, Thrivikraman K, Plotsky P, 1994. Age-related alterations of 371–394. hypothalamic–pituitary–adrenal axis function in male Fischer rats. Brown JS, 1988. Patch use as an indicator of habitat preference, predation Endocrinology 134:1528–1536. risk, and competition. Oecologia 22:37–47. Hayes RA, Morelli TL, Wright PC, 2006. Volatile components of lemur scent Brown JS, Kotler BP, 2004. Hazardous duty pay and the foraging cost of pre- secretions vary throughout the year. Am J Primatol 68:1202–1207. dation. Ecol Lett 7:999–1014. Hirschenhauser K, Mo¨ stl E, Wallner B, Dittami J, Kotrschal K, 2000. Brown JS, Kotler BP, Bouskila A, Bouskila A, 2001. The ecology of fear and Endocrine and behavioural responses of male greylag geese Anser anser to the foraging game between owls and gerbils. Ann Zool Fenn 38:71–87. pairbond challenges during the reproductive season. Ethology 106:63–77. Brown JS, Kotler BP, Smith RJ, Wirtz WO, 1988. The effects of owl predation Hutchings MR, White PCL, 2000. Mustelid scent-marking in managed ecosys- on the foraging behavior of heteromyid rodents. Oecologia 76:408–415. tems: implications for population management. Mamm Rev 30:157–169. Brown JS, Laundre´ JW, Gurung M, 1999. The ecology of fear: optimal forag- Jedrzejewski W, Jedrzejewska B, 1990. Effect of a predator’s visit on the spa- ing, game theory, and trophic interactions. J Mammal 80:385–399. tial distribution of bank voles: experiments with weasels. Can J Zool 68: Brown LE, 1969. Field experiments on the movements of Apodemus sylvaticus 761–824. L. using trapping and tracking techniques. Oecologia 2:198–222. Jedrzejewski W, Rychlik L, Jedrzejewska B, 1993. Responses of bank voles to Bu¨nning E, Moser I, 1969. Interference of moonlight with the photoperiodic odours of seven species of predators: experimental data and their relevance measurement of time by plants, and their adaptive reaction. Proc Natl Acad to natural predator–vole relationships. Oikos 68:251–257. Sci USA 62:1018–1022. Jemiolo B, Xie TM, Andreolini F, Baker AEM, Novotny M, 1991. The t com- Calder CJ, Gorman ML, 1991. The effects of red fox Vulpes vulpes faecal plex of the mouse: chemical characterization by urinary volatile profiles. odours on the feeding behaviour of Orkney voles Microtus arvalis. J Zool J Chem Ecol 17:353–367. 224:599–606. Kats LB, Dill LM, 1998. The scent of death: chemosensory assessment of pre- Clinchy M, Sheriff MJ, Zanette LY, 2013. Predator-induced stress and the dation risk by prey animals. Ecoscience 5:361–394. ecology of fear. Funct Ecol 27:56–65. Kaufman DW, Kaufman GA, 1982. Effect of moonlight on activity and micro- Dantzer B, McAdam AG, Palme R, Fletcher QE, Boutin S et al., 2010. Fecal habitat use by Ord’s kangaroo rat Dipodomys ordii. J Mammal 63: cortisol metabolite levels in free-ranging North American red squirrels: 309–312. assay validation and the effects of reproductive condition. Gen Comp Korte SM, 2001. Corticosteroids in relation to fear, anxiety and psychopath- Endocrinol 167:279–286. ology. Neurosci Biobehav Rev 25:117–142. Dı´az M, 1992. Rodent seed predation in cereal crop areas of central Spain: ef- Kotler BP, Ayal Y, Subach A, 1994. Effects of predatory risk and resource re- fects of physiognomy, food availability, and predation risk. Ecography 15: newal on the timing of foraging activity in a gerbil community. Oecologia 77–85. 100:391–396. Dı´az M, Alonso CL, Arroyo L, Bonal R, Munoz ~ A et al., 2011. Desarrollo de Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A, 2010. Moonlight un protocolo de seguimiento a largo plazo de los organismos clave para el avoidance in gerbils reveals a sophisticated interplay among time allocation, funcionamiento de los bosques mediterra´neos. In: Ramı´rez L, Asensio B, vigilance and state-dependent foraging. Proc R Soc B 277:1469. editors. Proyectos de Investigacio ´ n en Parques Nacionales: 2007–2010. Kotler BP, Brown JS, Dall SRX, Gresser S, Ganey D et al., 2002. Foraging Madrid: Organismo Auto´nomo Parques Nacionales, 47–75. games between gerbils and their predators: temporal dynamics of resource Dı´az M, Santos T, Tellerı´a JL, 1999. Effects of forest fragmentation on the depletion and apprehension in gerbils. Evol Ecol Res 4:495–518. winter body condition and population parameters of an habitat generalist, Kotler BP, Brown JS, Smith RJ, Wirtz WO, 1988. The effects of morphology the wood mouse Apodemus sylvaticus: a test of hypotheses. Acta Oecol 20: and body size on rates of owl predation on desert rodents. Oikos 53:145–152. 39–49. Lepschy M, Touma C, Hruby R, Palme R, 2007. Non-invasive measurement Dı´az M, Torre I, Peris A, Tena L, 2005. Foraging behavior of wood mice as of adrenocortical activity in male and female rats. Lab Anim 41:372–387. related to presence and activity of genets. J Mammal 86:1178–1185. Lima SL, 1998. Stress and decision making under the risk of predation: recent Dickman CR, Doncaster CP, 1984. Responses of small mammals to red fox developments from behavioral, reproductive, and ecological perspectives. Vulpes vulpes odour. J Zool 204:521–531. Adv Stud Behav 27:215–290. Eilam D, 2004. Locomotor activity in common spiny mice Acomys cahirinuse: Lima SL, Bednekoff PA, 1999. Temporal variation in danger drives antipreda- the effect of light and environmental complexity. BMC Ecol 4:16. tor behavior: the predation risk allocation hypothesis. Am Nat 153: Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G et al., 1999. 649–659. Differential behavioural and hormonal responses of voles and spiny mice to Lima SL, Dill LM, 1990. Behavioral decisions made under the risk of preda- owl calls. Anim Behav 58:1085–1093. tion: a review and prospectus. Can J Zool 68:619–640. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018 Navarro-Castilla et al. Wood mouse behavioral and physiological stress responses to predation risk 9 Martı´n J, Barja I, Lo´pez P, 2010. Chemical scent constituents in feces of wild Russell BG, Banks PB, 2007. Do Australian small mammals respond to native Iberian wolves Canis lupus signatus. Biochem Syst Ecol 38:1096–1102. and introduced predator odours? Aust J Ecol 32:277–286. Millspaugh JJ, Washburn BE, Milanick MA, Slotow R, van Dyk G, 2003. Sa´nchez-Gonza´lez B, Barja I, Navarro-Castilla A, 2017. Wood mice modify Effects of heat and chemical treatments on fecal glucocorticoid measure- food intake under different degrees of predation risk: influence of acquired ments: implications for sample transport. Wildl Soc B 31:399–406. experience and degradation of predator’s faecal volatile compounds. Monclu´s R, Ro¨ del HG, Palme R, Von Holst D, de Miguel J, 2006. Chemoecology 27:115–122. Non-invasive measurement of the physiological stress response of wild rab- Sapolsky RM, Romero LM, Munck AU, 2000. How do glucocorticoids influ- bits to the odour of a predator. Chemoecology 16:25–29. ence stress responses? Integrating permissive, suppressive, stimulatory, and Monclu´s R, Ro¨ del HG, Von Holst D, de Miguel J, 2005. Behavioural and preparative actions. Endocr Rev 21:55–89. physiological responses of naı¨ve European rabbits to predator odour. Anim Sapolsky RM, 2002. Endocrinology of the stress-response. In: Becker JB, Behav 70:753–761. Breedlove SM, Crews D, McCarthy MM, Editors. Behavioral Endocrinology. Montgomery WI, Gurnell J, 1985. The behaviour of Apodemus. Symp Zool Cambridge: MIT Press, 409–450. Soc Lond 55:89–115. Scordato ES, Dubay G, Drea CM, 2007. Chemical composition of scent marks Mora´n-Lo´pez T, Ferna´ndez M, Alonso CL, Flores-Renterı´a D, Valladares F in the ringtailed lemur Lemur catta: glandular differences, seasonal vari- et al., 2015. Effects of forest fragmentation on the oak-rodent mutualism. ation, and individual signatures. Chem Senses 32:493–504. Oikos 124:1482–1491. Sih A, 1980. Optimal behavior: can foragers balance two conflicting demands? Mo¨ stl E, Palme R, 2002. Hormones as indicators of stress. Domest Anim Science 210:1041–1043. Endocrinol 23:67–74. Stoddart DM, 1982. Demonstration of olfactory discrimination by the Navarro-Castilla A, Barja I, 2014a. Antipredatory response and food intake in short-tailed vole Microtus agrestis L. Anim Behav 30:293–294. wood mice Apodemus sylvaticus under simulated predation risk by resident Streiner DL, Norman GR, 2011. Correction for multiple testing: is there a and novel carnivorous predators. Ethology 120:90–98. resolution? Chest 140:16–18. Navarro-Castilla A, Barja I, 2014b. Does predation risk, through moon phase Strier KB, Lynch JW, Ziegler TE, 2003. Hormonal changes during the mating and predator cues, modulate food intake, antipredatory and physiological and conception seasons of wild northern muriquis Brachyteles arachnoides responses in wood mice Apodemus sylvaticus? Behav Ecol Sociobiol 68: hypoxanthus. Am J Primatol 61:85–99. 1505–1512. Tortosa FS, Barrio IC, Carthey AJR, Banks PB, 2015. No longer naı¨ve? Navarro-Castilla A, Barja I, Olea PP, Pineiro ~ A, Mateo-Toma´s P et al., 2014a. Generalized responses of rabbits to marsupial predators in Australia. Behav Are degraded habitats from agricultural crops associated with elevated fae- Ecol Sociobiol 69:1649–1655. cal glucocorticoids in a wild population of common vole Microtus arvalis? Touma C, Palme R, Sachser N, 2004. Analyzing corticosterone metabolites in Mammal Biol 79:36–43. fecal samples of mice: a noninvasive technique to monitor stress hormones. Navarro-Castilla A,Dı´az M, Barja I, 2017. Does ungulate disturbance Horm Behav 45:10–22. mediate behavioural and physiological stress responses in Algerian mice Touma C, Sachser N, Mo¨stl E, Palme R, 2003. Effects of sex and time of day Mus spretus? A wild exclosure experiment. Hystrix J. doi: on metabolism and excretion of corticosterone in urine and feces of mice. 10.4404/hystrix-28.2-12332. Gen Comp Endocrinol 130:267–278. Navarro-Castilla A, Mata C, Ruiz-Capillas P, Palme R, Malo JE et al., 2014b. Virgo´s E, Llorente M, Corte´s Y, 1999. Geographical variation in genet Are motorways potential stressors of roadside wood mice Apodemus sylva- (Genetta genetta L.) diet: a literature review. Mamm Rev 29:117–126. ticus populations? PLoS One 9:e91942. Washburn BE, Millspaugh JJ, 2002. Effects of simulated environmental condi- Orrock JL, Danielson BJ, Brinkerhoff RJ, 2004. Rodent foraging is affected by tions on glucocorticoid metabolite measurements in white-tailed deer feces. indirect, but not by direct, cues of predation risk. Behav Ecol 15:433–437. Gen Comp Endocrinol 127:217–222. Penteriani V, Kuparinen A, del Mar Delgado M, Palomares F, Lo´pez-Bao JV Wingfield JC, Romero LM, 2001. Adrenocortical responses to stress and their et al., 2013. Responses of a top and a meso predator and their prey to moon modulation in free-living vertebrates. In: McEwen BS, Goodman HM, edi- phases. Oecologia 173:753–766. tors. Handbook of Physiology—Coping with the Environment: Neural and Perrot-Sinal T, Kavaliers M, Ossenkopp KP, 1999. Changes in locomotor ac- Endocrine Mechanisms. New York: Oxford University Press, 211–234. tivity following predator odor exposure are dependent on sex and repro- Wolfe JL, Summerlin CT, 1989. The influence of lunar light on nocturnal ac- ductive status in the meadow vole. In: Johnston RE, Mu¨ller-Schwarze D, tivity of the old-field mouse. Anim Behav 37:410–414. Sorensen PW, editors. Advances in Chemical Signals in Vertebrates. New Wro´bel A, Bogdziewicz M, 2015. It is raining mice and voles: which weather York: Kluber Academic/Plenum Publishers, 497–504. conditions influence the activity of Apodemus flavicollis and Myodes glareo- Pineiro ~ A, Barja I, Silva´n G, Illera JC, 2012. Effects of tourist pressure and re- lus?. Eur J Wildl Res 61:475–478. production on physiological stress response in wildcats: management impli- Ylo¨ nen H, Eccard JA, Jokinen I, Sundell J, 2006. Is the antipredatory response cations for species conservation. Wildl Res 39:532–539. in behaviour reflected in stress measured in faecal corticosteroids in a small Pulido FJ, Dıaz M, Hidalgo SJ, 2001. Size structure and regeneration of rodent? Behav Ecol Sociobiol 60:350–358. Spanish holm oak Quercus ilex forests and dehesas: effects of agroforestry use Young KM, Walker SL, Lanthier C, Waddell WT, Monfort SL et al., 2004. on their long-term sustainability. Forest Ecol Manage 146:1–13. Noninvasive monitoring of adrenocortical activity in carnivores by fecal Reeder DM, Kramer KM, 2005. Stress in free-ranging mammals: integrating glucocorticoid analyses. Gen Comp Endocrinol 137:148–165. physiology, ecology, and natural history. J Mammal 86:225–235. Zanette LY, White AF, Allen MC, Clinchy M, 2011. Perceived predation risk Rogovin K, Randall JA, Kolosova I, Moshkin M, 2003. Social correlates of reduces the number of offspring songbirds produce per year. Science 334: stress in adult males of the great gerbil Rhombomys opimus in years of high 1398–1401. and low population densities. Horm Behav 43:132–139. Zanette LY, Clinchy M, Suraci JP, 2014. Diagnosing predation risk effects on Romero LM, 2002. Seasonal changes in plasma glucocorticoid concentrations demography: can measuring physiology provide the means? Oecologia 176: in free-living vertebrates. Gen Comp Endocrinol 128:1–24. 637–651. Romero LM, 2004. Physiological stress in ecology: lessons from biomedical Zwijacz-Kozica T, Selva N, Barja I, Silva´n G, Martı´nez-Ferna´ndez L et al., research. Trends Ecol Evol 19:249–255. 2013. Concentration of fecal cortisol metabolites in chamois in relation to Rothman KJ, 1990. No adjustments are needed for multiple comparisons. tourist pressure in Tatra National Park (South Poland). Acta Theriol 58: Epidemiology 1:43–46. 215–222. Downloaded from https://academic.oup.com/cz/advance-article-abstract/doi/10.1093/cz/zox048/4060528 by Ed 'DeepDyve' Gillespie user on 08 June 2018

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