| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Behavioral Ecology Vol. 15 No. 2: 286-289
Behavioral Ecology vol. 15 no. 2 © International Society for Behavioral Ecology 2004; all rights reserved
Scent marking by voles in response to predation risk: a field-laboratory validation
Department of Biology, The University of Memphis, Memphis, TN 38152, USA
Address correspondence to J. O. Wolff. E-mail: jwolff{at}memphis.edu.
Received 15 August 2002; revised 5 May 2003; accepted 8 May 2003.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
Predators use scent to locate their prey, and prey animals often alter their behavior in response to predation risk. I tested the hypothesis that voles would decrease their frequency of scent marking in response to predation risk. I conducted trials in which prairie voles, Microtus ochrogaster, and woodland voles, M. pinetorum, were allowed to scent mark ceramic tiles placed in their runways in the field. The tiles were subjected to one of three treatments: scented with odor from mink, Mustela vison (a rodent predator); rabbit, Oryctolagus cuniculus (a nonpredator mammal control); and no odor (control). No significant differences were found in the frequency of scent marking in response to the three treatments for either species. To validate that voles did not decrease their scent marking in response to predation risk, I brought male prairie voles from the field site into the laboratory and allowed them to scent mark white paper substrate treated with mink odor, rabbit odor, or no odor. No significant differences were found in the frequency of scent marks in response to the three treatments. These results differ from what was predicted based on laboratory studies with other species of rodents that show avoidance, reproductive suppression, decreased activity, and reduced scent marking in response to odors of predators. Voles appear to scent mark different substrates and under a wide variety of social and environmental situations, and this is not influenced by the presence of odor from a predator.
Key words: mink, predation risk, scent marking, vole.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
Scent marking by depositing urine and sebum from anogenital scent glands on substrate is common among mammals, especially rodents (Brown, 1979
; Eisenberg and Kleiman, 1972; Johnston, 1983). The frequency, placement, and quality of this scent provide information about competitive ability, identity, and sexual attractiveness of conspecifics (Brown, 1979; Eisenberg and Kleiman, 1972; Gosling and Roberts 2001; Johnston, 1983). The scent deposited to communicate to conspecifics can have a negative effect by advertising an individual's presence and location to predators. For instance, urine and scent deposited by voles and mice reflect ultraviolet light that can be detected by kestrels, Falco tinnunculus, and hawks, Buteo lagopus (Koivula and Viitala, 1999; Viitala et al., 1995), and odor increases conspicuousness to terrestrial carnivores (Koivula and Korpimäki, 2001). Aerial predators apparently cue in on vole activity by the visual presence of this scent. Predators such as weasels, Mustela nivalis, can detect female deer mice, Peromyscus maniculatus, that are in reproductive condition (Cushing, 1984, 1985), probably using their odor (for voles, see also Koivula and Korpimäki, 2001). However, whether voles alter their social or reproductive behavior in response to this predation risk is unclear. Several laboratory studies have shown that voles reduce reproductive activity and delay the onset of estrus in the presence of terrestrial carnivores or their scent (see Ylönen, 1989; Ylönen and Ronkainen, 1994); however, this has not been documented in the field (Hellstedt et al. 2002; Mappes et al., 1998; Norrdahl and Korpimäki, 2000; Wolff and Davis-Born, 1997). Wolff and Davis-Born (1997) found that gray-tailed voles, Microtus canicaudus, did not show a decrease in reproduction or activity but tended to avoid traps that were scented with feces and urine of mink, Mustela vison. Experimental studies in the laboratory have shown that voles appear to have a general avoidance of the scent of terrestrial carnivores (Jedrzejewski et al., 1993), but whether or not this affects their social or scent-marking behavior in the field is not known (Lambin et al., 1995; Wolff and Davis-Born, 1997).
If scent marking can increase an individual's fitness by advertising its competitive ability or sexual attractiveness yet also decrease fitness by increasing predation risk, natural selection should favor incorporating predation risk into the decision-making process of when and where to scent mark. Similar arguments have been made for foraging behavior (Kotler et al., 1992) and activity and microhabitat use (Abramsky et al., 1996; Hendrie et al., 1998) of rodents. House mice, Mus musculus, apparently alter their scent marking in response to predation risk. Roberts et al. (2001) found that dominant male mice reduced scent marking in the presence of urine from a ferret, Mustela putorius, whereas subordinate mice did not. Roberts et al., (2001) concluded that subordinate mice needed to "try harder" to advertise themselves, whereas the status of a dominant male was less threatened by reducing its scent marking. This laboratory study concluded that mice assessed predation risk and altered their scent marking behavior accordingly. To the best of our knowledge, alterations to the frequency of scent marking by rodents in response to risk by terrestrial predators have not been demonstrated in the field.
The objective of this study was to determine if two species of voles, prairie voles, Microtus ochrogaster, and woodland voles, M. pinetorum, reduce their scent marking in the presence of predation risk in the field. Voles were exposed to three treatments, odor (urine) of mink; odor (fecal pellets) of rabbit, Oryctolagus cuniculus; and a control (no odor). If scent marking exposes voles to predation risk, voles should decrease their frequency of scent marking in the presence of odor from a predator, such as a mink, but not that of a rabbit or no odor. After conducting an experiment in the field, I brought the same animals that were exposed to the three treatments in the field into the laboratory and repeated the experiment under controlled conditions.
|
EXPERIMENT 1 |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
Methods
Prairie voles
To determine if the presence of a predator decreased the rate at which voles scent marked, I placed ceramic tiles along vole runways in three 20 x 30-m rodent enclosures and recorded the frequency of marking in response to the scent of mink (predator), rabbit (neutral nonpredator control mammal), and no scent (control). The enclosures contained natural vole habitat and had been used for previous experimental field studies (see Mahady and Wolff, 2002
). Twenty 5 x 5-cm white ceramic tiles were distributed in a haphazard pattern covering all home range areas in each of three enclosures. Average spacing between tiles was approximately 5 m. Preliminary trials showed that voles typically mark strange objects in their runways. Tiles were left in place for 24 h. For the predator treatment, 10–20 drops of mink urine (Minnesota Trapline Products) were dripped in the runway within 20 cm on either side of the tile. For the rabbit scent, two to three fecal pellets were placed in the runway within 20 cm on either side of the tile. No scent was administered to the control tiles. Tiles were handled with latex gloves. All 20 tiles for any one treatment were placed in the same enclosure on any given night. The treatments were rotated among the enclosures such that each treatment was run in each enclosure three times over a 3-month period from May–July 2002. The order of treatments for the three enclosures was selected at random such that all voles were not exposed to treatments in the same order. Tiles were placed in the same home range areas for all trials, but in different runways or locations to avoid habituation and previous scents. Trials were conducted 4–7 days apart, which should have been sufficient for any prior scent to dissipate. Replicate treatments in the same enclosures were approximately 3 weeks apart. Based on livetrapping, I estimated about 20 animals were in each enclosure. Each enclosure had six to eight adult males distributed in a regular pattern such that three or four tiles were placed in the home range area of each male.
Woodland voles
The same procedure as above was used for woodland voles, except the study was conducted in open habitat in a peach orchard 20 km from the prairie vole site in Shelby County, western Tennessee. Woodland voles were distributed in what appeared to be independent family units under one or two trees (spaced at approximately 5–7-m intervals with open mowed habitat between trees). Two tiles were placed in active runways under each of 60 trees (20 mink, 20 rabbit, and 20 control). Home ranges of woodland voles may occupy more than one tree site, so some individuals may have had access to more than one set of tiles on a given night. However, not all trees were active sites, so tiles were often placed two or three trees apart. Therefore, each tree was considered an independent unit. Each treatment was replicated nine times in different portions of the habitat using 20 tiles for each replicate.
After 24 h for prairie voles and 48 h for woodland voles, tiles were collected and brought to the laboratory for observation. Woodland voles are primarily fossorial and do not come to the surface as often as do prairie voles, and thus, they took longer to mark the tiles. Tiles were observed under a long-wave ultraviolet lamp (Desjardins et al., 1973; urine and scent marks of voles fluoresce under ultraviolet light). If a tile was scent marked, the amount of scent was similar on all tiles, so I recorded scent as present or absent for each tile. In preliminary trials, about 50–75% of tiles were marked with scent or urine in 24 (or 48) h, and marks were relatively evenly deposited in a streak down the center of each tile from end to end. After scoring, the tiles were washed and disinfected and allowed to air dry.
Data analysis
For the prairie vole field data, each treatment was replicated three times in each enclosure, so I used a repeated-measures ANOVA to test for treatment effect. For the woodland voles, tiles were placed at new sites for each trial, so I used a one-way ANOVA to test among treatments (N = 9 replicates per treatment).
Results
The numbers of tiles marked for any one trial ranged from nine to 19 of 20 for prairie voles and six to 15 of 20 for woodland voles. The mean numbers of tiles marked by voles did not differ significantly among the three treatments for prairie voles (F2,12 = 0.345, p =.714) or for woodland voles (F2,24 = 0.157, p =.856) (Figure 1). The amount of scent deposited on tiles was visually comparable among treatments. These results suggest that neither prairie voles nor woodland voles altered their scent marking behavior in response to the threat of predation.
|
|
EXPERIMENT 2 |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
After completing the field study, I removed 13 male prairie voles from the field enclosures and brought them into the laboratory. Males were removed from home range areas in which tiles had been placed in the field, assuming these males were primary markers on the tiles. Animals were housed individually in polycarbonate cages (29 x 18 x 13 cm) and maintained on a 14-h light/10-h dark illumination cycle to simulate field conditions. Food and water were provided ad libitum, and room temperature was maintained at 21 ± 1°C.
Each animal was tested once with each of the same mink, rabbit, and control treatments as in the field. Trials were conducted on three consecutive days, starting the day after animals were brought in from the field. The order of the treatments was randomized to control for a time effect. Individual voles were placed in a 25 x 45 x 25 cm Plexiglas arena and allowed to scent mark on clean white copy paper for 10 min. This apparatus and method for scent marking have been used in previous experiments (Thomas and Wolff, 2002; Wolff et al., 2002). The substrate was treated with one of the following treatments: four drops of mink urine distributed throughout the arena, four rabbit pellets, or no odor (control). By using this procedure, prairie voles typically scent mark by depositing sebum from anogenital glands and rarely urinate or defecate. The sizes of scent marks vary but typically are 2–4 mm wide and 3–10 cm long. To standardize the area marked, I counted the number of scent marks covered by 0.5-cm squares on a transparency grid that was laid over the scent marks (for details, see Thomas and Wolff, 2002). Trials were conducted from 0700–0800 h.
Because the numbers of scent marks deposited by a given individual are highly variable, I standardized the relative number of marks for the three treatments by dividing the number for the greatest frequency of scent marks into the other two values for each individual. The frequencies of scent marking are presented as relative values, with 1.0 set as the value for the variable with the greatest number of marks for that individual for each trial. Data were arcsine/square-root transformed and analyzed with one-way ANOVA with the relative proportion of scent marks per treatment as the response variable.
Results
Scent marking occurred in 37 of 39 trials for the three treatments for all 13 individuals (one individual did not mark in the rabbit treatment and one in a control treatment). The range of scent marks for the other 37 trials was three to 492 and was comparable for all treatments. The mean numbers of scent marks (0.5-cm squares containing a scent mark) placed by male prairie voles on paper substrate was variable and ranged from 66 for controls to 109 for the rabbit treatment (Figure 2a). The mean relative proportion of scent marks placed by voles on the paper did not differ significantly among the mink, rabbit, and control treatments (F = 1.466, p =.244) (Figure 2b). Only one of 13 individuals deposited fewer scent marks in the mink treatment than in the other two treatments. There was no indication that animals attempted to avoid the drops of mink urine, as scent marks often ran through the mink scent.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
I failed to provide any evidence that voles decrease their frequency of scent marking in the field or in the laboratory in response to odor of a mammalian predator. The frequencies of depositing scent on tiles in the field or on paper in the laboratory were comparable in the presence of odor from mink, rabbits, or no odor. These results were not expected in light of previous studies that concluded voles reduce reproductive activity (Ylönen and Ronkainen, 1994
), delay sexual maturation (Heikkilä et al., 1993), and, in general, decrease activity or attempt to avoid predators (Korpimäki et al., 1996, but see Mappes et al. 1998). In addition, one field study demonstrated that when vole scent was added to vole habitat, predation by small mustelid predators increased compared with that in control habitats (Koivula and Korpimäki, 2001). Koivula and Korpimäki concluded that odor from vole scent posed a greater risk to voles than did ultraviolet visibility by avian predators. My results, however, are consistent with a field study in which gray-tailed voles did not alter their reproduction, sexual development, activity (Wolff and Davis-Born, 1997), or spacing (Jonsson et al. 2000) after exposure to heavy application of urine and feces of mink. Mappes et al. (1998) likewise showed that odors from weasels, Mustela nivalis, had no significant affect on the number of breeding females, time to sexual maturation, litter size, pup weight, or sex ratio of bank voles, Clethrionomys glareolus, in the field. Similar results were found for a field study with field voles, Microtus agrestis, in which the presence of weasels and their odor had no effect on demography or reproduction (Hellstedt et al. 2002). The results are also consistent with those of Pusenius and Ostfeld (2000), in which meadow voles did not reduce foraging activity in the presence of predation risk by a stoat, Mustela erminea. Voles can detect and may even avoid the odor of mink and other predators (Jedrzejewski et al., 1993; Parsons and Bondrup-Nielsen, 1996; Wolff and Davis-Born, 1997), and predators apparently cue in on vole odor (Koivula and Korpimäki, 2001), but this does not seem to affect their scent marking behavior.
My results differ from those of Roberts et al. (2001), who found that dominant, but not subordinate, laboratory mice decreased their frequency of scent marking when exposed to the scent of ferrets, Mustela putorius. I did not know the dominance relationships among voles in this study, but only one of 13 males tested in the laboratory showed a decrease in scent marking in the presence of mink urine in both trials. My experimental design differed from that of Roberts et al., who looked at the frequency of counter-marking by one individual in response to the scent of another individual in the presence of predation risk, whereas I looked at scent marking on a clean substrate, independent of any social context. In the field, however, I assume that voles were encountering dominant and subordinate individuals, involved in sexual activity, and defending mates and/or space. Thus, in this natural social environment, voles did not alter their scent marking behavior in response to predation risk. I did not know which individuals were scent marking in the field, but based on laboratory studies (Thomas, 2002; Thomas and Wolff, 2002), I assumed that males were the predominant scent markers. In addition, we ran a few trials in the field after we removed males from a couple of enclosures and the frequency of scent marking declined considerably in those enclosures. Scent marking resumed when males were returned.
Voles may be inherently different than mice or other rodents with respect to scent marking in that they seem to mark everything, everywhere, and most of the time. However, scent marking by mice has not been studied in the field, so we do not know if they would respond differently than in the laboratory or than did voles. Also, previous studies on response of rodents to stimuli in the laboratory may be artificial, presented in super stimulus quantities and in situations in which rodents do not have the opportunity to avoid it, making the results equivocal and unnatural (Lambin et al. 1995; Norrdahl and Korpimäki, 2000; Wolff, 2003). In several related studies in our laboratory, I concluded that prairie voles and meadow voles, Microtus pennsylvanicus, commonly scent mark bare substrate, their own previously scented areas, and areas scented by conspecific males and females to self-advertise their identity and presence in an area (Thomas, 2002; Thomas and Wolff 2002; Wolff et al. 2002). In conjunction with the field study on mink odor, I placed 60 tiles that had been rubbed across the ventral and genital region of a bullsnake, Pituophis melanoleucus, in runways as described above. Forty-nine of the 60 tiles (82%) were marked compared with 13 of 25 (65%) control tiles. Thus, voles did not avoid scent marking in the presence of scent from a sit-and-wait snake predator either. These results along with those of the current study suggest that voles are motivated to scent mark and are not inhibited from doing so by the odor of predators. Voles are relatively short-lived and during the reproductive season devote considerable effort to reproduction. The results from this study suggest that scent marking has greater benefits, perhaps in the form of developing a presence in an area, reproductive competition, or sexual advertisement than it does costs of increasing predation risk.
|
ACKNOWLEDGEMENTS |
|---|
I thank C. Roberts, S. Thomas, and two anonymous reviewers for helpful comments on the manuscript. Lee Wood and Juanita Jones kindly granted me permission to study woodland voles on their peach orchard. Bill Gutzke provided the snake odor. This research was funded in part by a grant from NSF.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENT 1EXPERIMENT 2DISCUSSIONREFERENCES |
|---|
Abramsky Z, Strauss E, Subach A, Kotler BP, Ricchman A, 1996. The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and Gerbillus pyramidum. Oecologia 105:213-319.
Brown RE, 1979. Mammalian social odors: a critical review. Adv Study Behav 10:103-162.
Cushing BS, 1984. A selective preference by least weasels for oestrous versus diestrous urine of prairie deer mice. Anim Behav 32:1263-1265.[CrossRef]
Cushing BS, 1985. Estrous mice and vulnerability to weasel predation. Ecology 66:1976-1978.[CrossRef]
Desjardins C, Maruniak JA, Bronson FH, 1973. Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939-941.
Eisenberg JF, Kleiman DG, 1972. Olfactory communication in mammals. Ann Rev Ecol Syst 3:1-32.[CrossRef]
Gosling LN, Roberts SC, 2001. Scent-marking in male mammals: cheat-proof signals of competitors and mates. Adv Study Behav 30:169-217.[CrossRef]
Heikkilä J, Kaarsalo K, Mustonen O, Pekkarinen P, 1993. Influence of predation risk on early development and maturation in three species of Clethrionomys voles. Ann Zool Fenn 30:153-161.
Hellstedt P, Kalske T, Hanski I., 2002. Indirect effects of least weasel presence on field vole behaviour and demography: a field experiment. Ann Zool Fenn 39:257-264.
Hendrie CA, Weiss SM, Eilam D., 1998. Behavioral responses of wild rodents to the calls of an owl: a comparative study. J Zool 245:439-446.[CrossRef]
Jedrzejewski W, Rychlik L, Jedrzejewski B, 1993. Responses of bank voles to odours of seven species of predators: experimental data and their relevance to natural predator-prey relationships. Oikos 68:251-257.[CrossRef]
Johnston RE, 1983. Chemical signals and reproductive behavior. In: Pheromones and reproduction in mammals. (Vandenbergh JG, ed.). Orlando,Florida: Academic Press; 3–37.
Jonsson P, Koskela E, Mappes T., 2000. Does risk of predation by mammalian predators affect the spacing behaviour of rodents? Oecologia 122:487-492.[CrossRef]
Koivula M, Korpimäki E, 2001. Do scent marks increase predation risk of microtine rodents? Oikos 97:275-281.[CrossRef]
Koivula M, Viitala J, 1999. Rough-legged buzzards use vole scent marks to assess hunting areas. J Avian Biol 30:329-332.
Korpimäki E, Koivunenn V, Hakkarainen H, 1996. Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation? Behav Ecol 7:30-34.
Kotler BP, Blaustein I, Brown JS, 1992. Predator facilitation: the combined effects of snakes and owls on the foraging behavior of gerbils. Ann Zool Fenn 29:199-206.
Lambin X, Ims RA, Steen H, Yoccoz N, 1995. Vole cycles. Trends Ecol Evol 10:204.
Mahady S, Wolff JO, 2002. A field study of the Bruce effect in prairie voles. Behav Ecol Sociobiol 52:31-37.
Mappes T, Koskela E, Ylönen H, 1998. Breeding suppression in voles under predation risk of small mustelids: laboratory or methodological artifact? Oikos 82:365-369.[CrossRef]
Norrdahl K, Korpimäki E, 2000. The impact of predation risk from small mustelids on prey populations. Mamm Rev 30:147-156.
Parsons GJ, Bondrup-Nielsen S, 1996. Experimental analysis of behaviour of meadow voles (Microtus pennsylvanicus) to odours of the short-tailed weasel (Mustela erminea). Ecoscience 3:63-69.
Pusenius J, Ostfeld RS, 2000. Effects of stoat's presence and auditory cues indicating its presence on tree seedling predation by meadow voles. Oikos 91:123-130.[CrossRef]
Roberts SC, Gosling LM, Thornton EA, McClung J, 2001. Scent-marking by male mice under the risk of predation. Behav Ecol 12:698-705.
Thomas SA, 2002. Scent marking and mate choice in the prairie vole (Microtus ochrogaster). Anim Behav 63:1121-1127.[CrossRef]
Thomas SA, Wolff JO, 2002. Scent marking in voles: a reassessment of counter marking, over marking, and self-advertisement. Ethology 108:51-62.[CrossRef]
Viitala J, Korpimäki E, Palokangas P, Koivula M, 1995. Attraction of kestrels to vole scent marks visible in ultraviolet light. Nature 373:425-427.[CrossRef]
Wolff JO., 2003. Laboratory studies with rodents: facts or artifacts. Bioscience 53:421-427.[CrossRef]
Wolff JO, Davis-Born R, 1997. Response of gray-tailed voles to odours of a mustelid predator: a field test. Oikos 79:543-548.[CrossRef]
Wolff JO, Mech SG, Thomas SA, 2002. Scent marking in female prairie voles: a test of alternative hypotheses. Ethology 108:483-494.[CrossRef]
Ylönen H, 1989. Weasels, Mustela nivalis, suppress reproduction in cyclic bank voles Clethrionomys glareolus. Oikos 5:138-140.[CrossRef]
Ylönen H, Ronkainen H, 1994. Breeding suppression in the bank vole as an antipredatory adaptation in a predictable environment. Evol Ecol 8:658-666.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  F. Rosell and J. Sanda Potential risks of olfactory signaling: the effect of predators on scent marking by beavers Behav. Ecol., November 1, 2006; 17(6): 897 - 904. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||