EFFECTS OF PRIOR POPULATION DENSITY ON USE OF SPACE BY MEADOW VOLES, MICROTUS PENNSYLVANICUS

EFFECTS OF PRIOR POPULATION DENSITY ON USE OF SPACE BY MEADOW VOLES, MICROTUS PENNSYLVANICUS STEPHEN R. PUGH AND RICHARD S. OSTFELD University of New Hampshire at Manchester, 220 Hackett Hill Road, Manchester, NH 03102 (SRP) Institute of Ecosystem Studies, Box AB, Millbrook, NY 12545 (RSO) We examined the effect of prior population density on use of space by meadow voles, Microtus pennsyivanicus, by maintaining two replicates each of populations of voles at low, medium, and high density in O.16-ha fenced enclosures in southeastern New York for 20 months. All voles were then removed by live-trapping and equal numbers of new animals were introduced into each enclosure and monitored by biweekly live-trapping for 7 months. We determined patterns of space use of these voles using radiotelemetry. If previous density had a long-lasting effect on habitat quality, voles placed in enclosures that previously maintained high-density populations should have had larger home ranges with greater overlap than individuals in enclosures that previously maintained low-density populations. We found no significant effect of previous density on home-range size and overlap, or interfix movement distance. These results do not support the herbivore-resource mechanism for delayed density-dependence in meadow voles. Key words: Microtus pennsyivanicus, meadow vole, delayed density-dependence, radiotelemetry, use of space, home range Several researchers have suggested that delayed density-dependence may play an important role in the multiannual fluctuations in populations of microtine rodents (Hanski el aj., 1993; OSlfeld el ai., 1993; Turchin and OSlfe1d, 1997). May (1976) developed a model in which populations with a relatively high intrinsic rate of increase (r) would undergo multiannual fluctuations with periods of about 4 years if a delayed density-dependent factor with a time lag of about 9 months was included. However, May (1976) did not propose a biological mechanism for such a time lag. Hornfeldt (1994) documented delayed density dependence with a time lag that approximated May's (1976) 9-month lag in populations of Clethrionomys rufocanus, C. glareolus, and Microtus agrestis in northern Sweden. Hornfeldt's (1994) conclusion was based on a negative correlation between the rate of change in numbers of animals in both summer and winter and density in the previous autumn and spring, respectively. Again, Hornfe1dl (1994) did noi provide support for any particular biological mechanism for this time lag but suggested that predators, food, or disease should be considered. Hanski et al. (1993) evaluated time-series data on several species of Microtus, using a predator-prey model with seasonality and concluded that multiannual fluctuations in Fennoscandian rodents are due to delayed density dependence imposed by mustelid predators. Oslfeld el aj. (1993) and Ostfeld and Canham (1995) described direct density-dependent effects (without a lag) on populations of the meadow vole, Microtus pennsylvanicus, in upstate New York. By maintaining field populations at three different levels of density, they demonstrated that high-density populations showed a reduction in breeding effort, reduction in individual growth rates, increase in size at sexual maturity, and reduction in movement distances relative to low-density populations. They also found a significant reduction in adult survival rates in high-density populations but only after about 16 months at Journal of Mamma/ogy, 79(2):551-557, 199H 551

552 JOURNAL OF MAMMALOGY Vol. 79, No.2 high density, suggesting that there may be a lag in the effect of density on adult survival. In addition, in an experiment in which growth of vole populations was monitored for 7 months in areas that had been subject to different densities of voles during the previous 20 months, Ostfeld et ai. (1993) found no evidence for delayed density dependence influencing population density or growth rates. Severa1 mechanisms for delayed density dependence have been suggested, including predator-prey interactions, food or habitat quality (herbivore-resource interactions), disease, maternal effects, and behavioral polymorphism (Hanski et ai., 1993; Homfeldt, 1994; Krebs and Myers, 1974; Mihok and Boonstra, 1992; Ostfeld et ai., 1993). OUf purpose is to evaluate the herbivoreresource mechanism of delayed density dependence in meadow voles by examining how previous density affects use of space, movement patterns, and home-range size and overlap. High population density could result in an overexploitation of grasses and forbs. which are the principal food of meadow voles. Such overexploitation could then trigger a population decline. After the crash, populations could experience a delay in the onset of the increase phase resulting from a lag in recovery by the plant community from heavy exploitation. We used the same populations of voles studied by Ostfeld et a1. (1993) and monitored use of space using radiotelemetry. We predicted that if previous density had a long-lasting effect on habitat quality (quantity or quality of food and cover), voles on grids that previously maintained high-density populations would have to range further to meet their nutritional requirements and would have larger horne ranges with greater overlap than individuals on grids that previously maintained lower-density populations. MATERIALS AND METHODS Study area and trapping protocol.-our study was conducted at the Institute of Ecosystem Studies in Millbrook (Dutchess Co.), New York. In June 1990, we built nine 40 by 40 m (0.16 ha) fenced enclosures in a grassy old field (Ostfeld and Canham, 1995). Fences were constructed of galvanized hardware cloth and extended from 0.5 m below ground to 0.8 m aboveground. Live-trapping grids established in each enclosure consisted of 25 trap stations in a five by five array with 7.5 m between trap stations. initially, one Longworth live trap was placed at each trap station. Whenever ;:::80% of traps were occupied on a given night, we placed an additional trap at each station. Trapping was conducted biweekly from June 1990 through April 1992. Traps were set for 2 consecutive nights and checked the following mornings. AU animals were given individually numbered ear tags at first capture. For all captures, we recorded tag number, gender, trap location, mass, and reproductive condition. Density of voles was manipulated in the enc~osures beginning in June 1990 by removing subadult voles (Ostfeld and Canham, 1995). Three levels of density were maintained. On low-density grids, subadults were removed whenever five or more adult and subadult voles were captured on the first day of trapping. On medium-density grids animals were removed whenever ;::: 15 adult and subadult voles were captured. No voles were removed from highdensity grids. With this technique, we successfully maintained three replicates each of grids at high (ca. 380 voleslha), medium (ca. 180 voles! ha), and low density (ca. 70 voles/ha). In April 1992. all voles were removed from each grid by live trapping and released elsewhere. This removal was timed to coincide with annual spring declines typically observed in this species (Boonstra and Rood, 1983; Krebs and Myers, 1974). One week later two pairs of voles, trapped 2 km away, were introduced into each enclosure. One week later, missing voles were replaced to equalize sex and age composition in the nine enclosures. Populations of voles on all nine grids were allowed to grow freely and were monitored by biweekly live trapping unti1 November 1992 (Ostfeld et al., 1993). Radiotelemetry.-In July and August 1992, we monitored movement and use of space of adult voles on six of the nine grids using radiotelemetry. Two grids (C and I) were previously maintained at high density, two (B and H) at medium density, and two (A and G) at low density. We placed radiocollars (AVM Instrument

May 1998 PUGH AND OSTFELD-SP ACE USE IN VOLES 553 Co., Livennore, CAl on all adult voles ;?::32 g. Each radio weighed <3 g and transmitted a signal at a unique frequency. Following the radiotelemetry protocol of Ostfeld (1986), we determined the location (fix) of each radiocollared vole (to the nearest meter) two to six times per day between OSOO and 2200 h for 13-1S days using a 4-m probe antenna connected to a multichannel receiver. We monitored 17 individuals on grids G (2 males, S females), H (2 males, 1 female), and I (2 males, S females) from 8 to 22 July 1992 and 16 individuals on grids A (2 males, 3 females), B (3 males, 3 females), and C (4 males, 1 female) from 7 to 19 August 1992. Twelve individuals (6 male and 6 female) were monitored on grids that previously held bighdensity populations, 9 individuals (S males and 4 females) on grids that previously held medium-density populations, and 12 individuals (4 males and 8 females) on grids that previously held low-density populations. Mean number of fixes detennined per individual was 43.S ::!: 0.43 SE and ranged from 36 to 46. Radiotelemetry coordinates of each individual were used to determine sizes of minimum-convex-polygon (Mep) home ranges using the com~ puter program RANGES IV (R. Kenward, Institute of Terrestrial Ecology, Wareham, UK). We used SO% MCP home ranges to represent core areas and 9S% MCP home ranges to represent core plus peripheral areas. These were calculated by excluding fixes that were the furthest from the harmonic mean of all coordinate points determined for an individual vole. We calculated an index of home range overlap between each pair of voles on a grid using the overlap index (01,,) of Ostfeld (1986), Ol'i = O.OS (PIIo9s) (P/J o.9s) + O.S (QIIo.9s). (QIJ o.so) + O.S (RfIo50) (RlJ O.95) + 0.9S (SIlo.50) (S/Jo. 50 ) where 10.95 = 9S% MCP home range area for individual I; 10.50 = SO% MCP home range area for individual I; and similarly for individual J; P = area of overlap between the 9S% MCP area of I and the 9S% MCP area of J; Q = area of overlap between the 9S% MCP area of I and the SO% Mep area of J; R = area of overlap between the SO% MCP area of I and the 9S% MCP area of J; S = area of overlap between the SO% MCP area of I and the SO% Mep area of J. The factors O.OS, O.S and 0.9S were employed to place greater weight on overlap in core than in peripheral areas (Ostfeld, 1986). We summed the overlap index value between each vole and any overlapping neighbors to derive a cumulative overlap index value (toi;). We also calculated average interfix distances for each individual as a measure of movement patterns. Homerange size, cumulative overlap index values, and interfix distances were compared using nonparametric statistical techniques (Kruskal-Wallis H and Mann-Whitney U tests-sakal and Rohlf, 1981) to determine if there were any significant (P < O.OS) differences among prior-density treatments or between females and males. RESULTS We observed no significant effect of previous density on either core (50% MCP) or core plus peripheral (95% MCP) homerange size of males or females (core home ranges of males-h ~ 3.28, d.! ~ 2, P ~ 0.19; core plus peripheral home ranges of males-h ~ 4.64, d.f ~ 2, P ~ 0.09; core home ranges of females-h = 0.26, dj = 2, P = 0.88; core plus peripheral home ranges of females-h ~ 0.01, d.f ~ 2, P = 0.99; Fig. 1). When density treatments were combined, home ranges of males were larger than home ranges of females (core home ranges-u = 238, P < 0.001; core plus peripheral home ranges-v = 239, P < 0.001; Table I). We observed no effect of previous density on either intrasexual or intersexual overlap of males or females (males, intrasexual overlap-h ~ 1.71, d.f ~ 2, P ~ 0.42; males, intersexual overlap-h = 1.39, d.f ~ 2, P ~ 0.50; females, intrasexual overlap-h ~ 3.13, d.f ~ 2, P ~ 0.21; females, intersexual overlap--h = 1.64, d.f ~ 2, P ~ 0.44; Fig. 2, Table 1). When density treatments were combined, there were no differences between indices of home-range overlap of males and females (intrasexual overlap--u = 181, 0.20 > P > 0.10; intersexual overlap--v = 159, P > 0.20, Table I). There were no significant effects of density on interfix movement distances for either males or females (males-h = 4.06, P ~ 0.13; females-h ~ 0.29, P ~ 0.86).

554 JOURNAL OF MAMMALOGY Vol. 79, No. 2 o Grid A (Low Density) Grid B (Medium Density) Grid C (High Density) ~D E ~ Grid G (Low Density) Grid H (Medium Density) Grid I (High Density) FIG. I.-Home range maps (95% minimum convex polygons) of male and female meadow voles in grids maintained previously at low- (grids A and G), medium- (grids B and H), and high (grids C and I) density. When density treatments were combined, males moved greater distances between radiotelemetry fixes than females (U = 249.5, P < 0.001, Table I). DISCUSSION We predicted that if overexploitation of resources was the proximate mechanism for delayed density dependence, voles inhabiting enclosures that previously held highdensity populations should have larger home ranges with greater overlap and should move greater distances than voles in enclosures that previously held low- or medium-density populations. This prediction was not supported. We found no significant

May 1998 PUGH AND OSTFELD-SP ACE USE IN VOLES 555 09 08 0.7 c 0.5 " rr ~ 0.4 ~ 0.3 o Male-Male Female-Female o Male-Female 0.6 0.2 0.1 0 0-0.09 0.1-0.19 0.2-0.29 0.3-0.39 0.4-0.49 0.5-0.59 > 0.6 Index of overlap FIG. 2.-Frequency distribution of indices of home-range overlap for meadow voles; all density treatments combined. effect of previous density on home-range size, inter- and intrasexual home-range overlap, or movement distances. Female meadow voles are territorial during the breeding season, whereas males are nonterritorial (Madison, 1980). In this experiment, we found similar results in the two sexes despite differences in spacing behavior. Our results are consistent with the demographic results of Ostfeld et a1. (1993), who reported no significant effects of previous density on density or growth rate of populations. In contrast, direct effects of density (without a lag) were quite significant. Highdensity populations experienced a reduction in breeding effort, individual growth rates, and intertrap movement distances (Ostfeld and Canham, 1995; Ostfeld et ai., 1993). Quantity of food was reduced in the highdensity enclosures, but this effect was ephemeral. The plant community recovered during the second year of the density manipulations, even in the high-density enclosures (Ostfeld, 1994). While shorter intertrap movement distances (an indication of smaller home ranges) were observed in TABLE l.-minimum convex polygon (MCP) home range (m2), cumulative overlap index, and average inter fix distance (m) of meadow voles in enclosures that previously held low-, medium-, or high-density populations (mean ~ SE). Average Intrasexual Intersexual interfix S" Density n 50% MCP 95% MCP overlap overlap distance Male Low density 4 152 ~ 60 596 :!:: 80 0.024 :!:: 0.007 0.266 ::': 0.230 12.3 :!:: 0.8 Medium density 5 178 :!: 52 804 :::':: 65 0.013 ± 0.008 0.093 :!: 0.076 12.2 ± 0.9 High density 6 90 ::': 26 485 :!:: 152 0.153 :!:: 0.098 0.195 :::':: 0.159 9.8 :!: 0.8 Female Low density 8 41 :!: 13 223 ~ 43 0.042 ± 0.026 0.133 ± 0.084 7.2 :!: 0.7 Medium density 4 39 ~ 11 200 ::': 42 0.001 :!: 0.001 0.128 :!:: 0.088 7.6 ± 0.7 High density 6 32 :!: 12 270 ~ 79 0.011 ± 0.005 0.195 :!: 0.064 7.0::': 1.0

556 JOURNAL OF MAMMALOGY Vol. 79, No.2 high-density enclosures, these were probably caused by direct effects of crowding at high density and not by a reduction in food availability, which would have increased movement distances. In any case, effects of high density on habitat quality did not persist into the subsequent growing season. Therefore, a model of delayed density dependence based on a lag in recovery of resource quality or quantity was not supported in this study. OUf results are not consistent with a similar study on the field vole (Microtus agrestis) in southern Scandinavia by Agrell et ai. (1995), who observed a response by field vole populations to previous density. Reproduction, recruitment rates, and individual growth rates were reduced in areas that had been exposed to high density for the 2 previous months. In addition, home-range size was larger and more exclusive, and interlix movement distances were greater on trapping grids that previously held highdensity populations. As in our study, all voles were removed at the end of the period of density manipulation, and new voles were introduced. This procedure eliminates the possibility that maternal effects, directly transmitted disease, or behavioral polymorphism were proximate causes of delayed effects of density on demography and spacing behavior. Both studies were done on similar-sized grids (0.1 ha-agrell et ai., 1995; our study--o.16 ha) that were larger than mean individual home ranges. Agrell et ai. (1995) suggested that female voles on grids that previously held high-density populations were postponing reproductive effort until the next reproductive season, but, they described only minimal effects of density on resources. No effects of previous density on vegetative composition or biomass were detected. They suggested that food quality (protein levels or phenolic content) rather than food quantity may have been involved. Satisfactory explanations for disparate results of these two studies are difficult to generate. Ostfeld (1994) suggested that a delayed effect of high density on subsequent population growth expressed through resource quality was unlikely if primary productivity was high, because the plant community likely would recover quickly after overexploitation by consumers. Moderately productive communities were hypothesized to be more likely candidates for resource-based density dependence. We suggest that the higher productivity in fields in New York allowed the plant community to respond to exploitation quickly, eliminating a mechanism for delayed density dependence. Lower productivity in southern Scandinavia may have prevented a similar rapid recovery in the experiments by Agrell et ai. (1995). Another factor that has been suggested as a proximate cause of delayed density dependence is predation by specialist predators (Hanski et ai., 1993). Neither our study nor that of Agrell et al. (1995) controlled for or monitored predation rates. More detailed studies on delayed density dependence that also monitor or control predation may be necessary before a satisfactory explanation can be determined. ACKNOWLEDGMENTS We thank K. Price for help in radiotelemetry and O. Wilhelm and numerous field assistants for help in trapping. R. H Tamarin provided useful comments on an early draft of this paper. S. R. Pugh was supported by a Summer Research Fellowship from the Mary Flagler Cary Charitable Trust. Funding was from Central Hudson Gas and Electric Corporation, Empire State Electric Energy Research Corporation, General Reinsurance Corporation, and the Mary Flagler Cary Charitable Trust. LITERATURE CITED AGRELL, J., S. ERLINGE, J. NELSON. C. NILSSON. AND 1. PERSSON. 1995. Delayed density-dependence in a small-rodent population. Proceedings of the Royal Society of London, Series B, Biological Sciences, 262:65-70. BOONSTRA, R., AND E H. ROOD. 1983. Regulation of breeding density in Microtu.\ pennsyivanicus. The Journal of Animal Ecology, 52:757-780. HANSKI, I., P. TURCHIN, E. KORPIMAKI, AND H. HENT TONEN. 1993, Population oscillations of boreal rodents: regulation by mustelid predators leads to chaos. Nature, 364:232-235.

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