Journal of Mammalogy, 87(3):440-445, 2006

A CYCLIC RED-BACKED VOLE {CLETHRIONOMYS GAPPERI) POPULATION AND SEEDEALL OVER 22 YEARS IN MAINE

SUSAN P. ELIAS,* JACK W. WITHAM, AND MALCOLM L. HUNTER, JR. Holt Research Forest, University of Maine, Arrowsic, ME 04530, USA (SPE, JWW) Department of Wildlife Ecology, University of Maine, Orono, ME 04469, USA (MLH)

Vole populatioti dynamics are well charactetnzed iti Europe, Fennoscandia, and Japan, but long-term studies of vole dynamics in Noith Ameiica are rare and much needed. Summer relative abundance of southem red-backed voles {Ciethrionomys gapperi) fluctuated periodically during 22 years (1983-2004) at the Holt Research Forest, Maine, suggesting an outbreak or cyclic dynamic. The time series had a 4.4-year period, and 2nd-order lagged relative abundance was significant in an autoregressive model. This was consistent with vole series in Fennoscandia and Japan. Above-average white pine {Pinus strobus) seed crops preceded C. gapperi peaks in 4 of 5 peak phases. In a model including P. strohus seeds, both seeds and 2nd-order lagged abundance terms were significant. Relative importance of P. strohus seeds to this omnivore needs to be established. High and low phases of C. gapperi corresponded with those of sympatric white-footed mice {Peromyscus leucopus). The 2nd- order autoregressive process, 4.4-year periodicity, and synchrony with P. leucopus indicated the C. gapperi dynamic was cyclic. This was a unique finding for the northeastem United States.

Key words: acorns, Ciethrionomys gapperi, cycles, periodicity, Peromyscus leucopus, population dynamics, time-series analysis, southem red-backed voles, white pine seeds, white-footed mice

Population ecologists have a long and continuing fascination behavior (Hansson et al. 2000). Latitude is a correlate of with factors that shape stable, outbreak, and cyclic population cyclic performance; stable to cyclic populations have been dynamics. These halve been particularly well studied for voles observed to grade from south to north in Fennoscandia (C. {Ciethrionomys and Microtus) in Europe, Fennoscandia, and rufocanus), and southwest to northeast in Japan (Bj0mstad Japan. In Europe, stable populations of the bank vole (C. et al. 1995, 1998). glareolus) have relatively constant densities across years in On the Holt Research Forest, a pine-oak forest in midcoastal forests with few mast-producing species, whereas outbreak Maine, the southem red-backed vole (C. gapperi) population populations are distinguished by 6- to 9-year peaks corre- has fluctuated over a 22-year study period. A key question sponding to mast peaks in oak-dominated forests (Hansson is whether this pattem of fluctuation is consistent with an et al. 2000). In Fennoscandia, cyclic dynamics of C. glareolus, outbreak or cyclic dynamic. C. gapperi is the 2nd most gray-sided voles (C. rufocanus), and field voles {M. agrestis) common small mammal species on the Holt Forest after white- are typified by peaks every 3-5 years and very low numbers footed mice {Peromyscus leucopus). Elias et al. (2004) reported in low phases, and have been statistically described using that the periodicity of P. leucopus on the Holt Forest was 4.0 autoregressive, 2nd-order, lagged abundance models (e.g., years, and that the population increased after high acom crops, Bj0mstad et al. 1995; Homfeldt 1994). The same dynamic has but only if the population had been low in the previous 2 years. been described for some populations of C. rufocanus in If C. gapperi numbers also could be modeled as a function of Hokkaido, Japan (Saitoh et al. 1998). Cyclic performance has 2nd-order lagged relative abundance, and were synchronous been attributed theoretically to interactions among food, social with sympatric P. leucopus, it would suggest a cyclic dynamic. behavior, and predation. In regions with strong cyclic Conversely, correspondence only between C. gapperi and dynamics, predation could partially explain synchrony (corre- seedfall would suggest an outbreak dynamic. Although C. lated fluctuation) among species with different diets and gapperi eat greens, fruits, insects, and fungi as well as seeds (Merritt 1981; Vickery 1979), it would be reasonable to expect a numerical response of voles to above-average seedfall, * Correspondent: [email protected] especially autumn crops. Based on these observations, our hypotheses were relative abundance of C. gapperi and © 2006 American Society of Mammalogists P. leucopus would be significantly correlated, indicating syn- www.mammatogy.org chrony; C. gapperi would exhibit strong fluctuation, periodicity

440 June 2006 ELIAS ET AL.—MAINE CLETHRIONOMYS CYCLES AND SEEDFALL 441

Small mammal trapping.—^We followed guidelines of the American Society of Mammalogists for the capture, handling, and care of mammals (Animal Care and Use Committee 1998). We trapped small mammals in the first 2 weeks of August 1983-2004. We placed 144 stations on 6 parallel, north-south, 400-m transect lines and trapped for 5 consecutive nights during the 1st week of each trapping session ( (Fig. 1). At the beginning of the 2nd week, we placed 140 stations on 2 pairs of 567-m assessment lines. Each pair ran diagonally at 45° to the transect lines (Fig. 1). We trapped assessment lines stations during the 2nd week for 3 consecutive nights. We used this census-assessment line method for efficiency in trapping a large area (O'Farrell and Austin 1978; O'Farrell et al. 1977). Of the 284 trap stations, 219 were in the 23 unharvested blocks. Stations on trap lines were 16.7 m apart (6 stations/100 m). At each station, we baited two 9 x 8 x 23-cm Sherman live traps (H. B. Sherman Traps, Inc., Tallahassee, Florida) with a mixture of rolled oats and peanut butter. We put a 5.1 x 5.1-cm square pad of pressed cotton (Nestlets, Ancare Corporation, Bellmore, New York) in each trap for \ shredding and insulation. We checked traps daily between 0600 and 1000 h; aged, sexed, and weighed the animals; recorded traps snapped but empty; and rebaited traps. We marked P. leucopus with metal ear tags (National Band and Tag Company, Newport, Kentucky). We marked C. gapperi with metal ear tags or by toe-clipping through 1998, and thereafter used passive integrated transponder (PIT) tags (Biomark, Inc., Boise, Idaho), as recommended by the American Society of 1 1 UNHARVESTED Mammalogists (Animal Care and Use Committee 1998). 1 1 HARVESTED Seed collection.—Seedfall was from northem red oak {Quercus 100m ruhra), red spruce {Picea ruhens), white oak {Q. alba), red maple TRANSECT ASSESSMENT {Acer ruhrum), eastern white pine {Pinus strohus), eastern hemlock STATIONS STATIONS {Tsuga canadensis), balsam fir {Abies balsamea), and birches {Betula Fic. 1.—Study area, showing transects for small mammal trapping spp.). We pooled the birches because it was difficult to distinguish and assessment lines on the Holt Research Eorest, Maine, 1983-2004. among seeds of B. alleghaniensis, B. populifolia, and 6. papyrifera. Darker shading indicates 1-ha blocks where timber was harvested. We used 2 methods for collecting seeds. From 1983 to 1990, we Analysis was based on data from unharvested blocks only (lighter randomly located 1 seed trap with a 0.5-m^ opening in each of the 1-ha shading). blocks (23 seed traps in unharvested blocks; total seed trap area = 11.5 m^). Traps were constructed of ultraviolet-resistant nylon net bags suspended from an aluminum ring supported on 1.5-m wooden posts. in the vicinity of 4 years, and significant 2nd-order lagged Traps were emptied and seeds counted once per month to estimate phenology of seedfall and annual seed production. A. rubrum seeds relative abundance in a 2nd-order autoregressive model; dispersed in spring, Betula spp. seeds dispersed in late autumn into C. gapperi would be significantly correlated with any of the January, and seeds of all other species dispersed in autumn. From coniferous seed species and possibly with acorns, suggesting 1988 to 2004, we located a seed trap with a 0.042-m^ opening at each a response to seedfall; and any models of C. gapperi abundance of the small mammal transect-line trap stations (76 seed traps in including a significant seedfall correlate would also include unharvested blocks; total seed trap area = 3.2 m^). These traps were a significant 2nd-order lagged relative abundance term. Con- constructed from net bags suspended within 1.5-m-tall wire tomato firmation of these predictions would indicate a cyclic rather cages and were emptied once per year in May. The magnitude of than outbreak dynamic. This would be a unique finding for Pearson correlation coefficients (pps) between the 2 methods was high a Ciethrionomys population in the northeastem United States (Cohen 1988) in the overlapping 3 years (1988-1990), with pp = 0.73 and provoke new thinking about how geography relates to vole for oaks, pp 0.95 for all other species, and pp = 0.99 for all species population dynamics. combined. McCracken et al. (1999) also concluded that the methods yielded comparable indices of seedfall for the Holt Forest. Therefore, we used the means of the 2 methods for the 3 overlapping years. No MATERtALS AND METHODS evidence of depredation of seed traps was found. The Holt Research Forest is a 120-ha, mature (trees about 70-90 Statistical analyses.—^When time series are used in regression ana- years old), pine-oak forest in Arrowsic, Maine (43°45'N, 69°46'W). lyses, the data are often serially correlated (autocorrelated). Autore- Mean basal area was 30 m^/ha. As part of a long-term forest ecosystem gression is used to diagnose and account for serial correlation between study, we established a study grid of forty 1-ha blocks and conducted values at current time t and values at past lags of t. If the values at t are small mammal trapping within 30 of these (Fig. 1). Seven of the 30 correlated with the values at t — 1, t — 1 is termed a 1 st-order effect and blocks were partially harvested (Kimball et al. 1995) once in winter the series exhibits 1 st-order autocorrelation, and so forth up to n orders. 1987-1988 (shaded in Fig. I). To avoid confounding the time-series In our time-series analyses, the samphng unit was the year. Each analyses with incidental harvest impacts, we used data exclusively year, we calculated N,, the minimum number alive (MNA) of indi- from the twenty-three 1 -ha blocks that were never harvested. viduals per 100 trap nights. This resulted in one 22-year time series each 442 JOURNAL OF MAMMALOGY Vol. 87, No. 3

TABLE 1.—Summary statistics for red-backed voles {Ciethrionomys 25-1 gapperi), white-footed mice {Peromyscus teucopus), and seedfall at - Clettirionomys gapperi the Holt Research Forest, Arrowsic, Maine, 1983-2004. Sample size • Peromyscus leucopus (n) is the number of years in the time series. The seed series was c shorter than the mammal series for autumn-dispersing species because Q. a seedfall before 1983 was unknown. Pearson correlation coefficients - 15 are for C. gapperi versus P. leucopus and each of the 8 seedfall series.

Species n r SE Minimum Maximum Minimun number alive per 100 trap nights C. gapperi 22 4.2 0.47 0.1 8.3 P. leucopus 22 8.5 1.57 0.0 24.0 0.66*** Seedfall (kg/ha) 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 Year Quercus ruhra 21 111.0 A 19.76 0.0 269.2 0.25 Picea ruhens 21 23.0 B 9.75 O.I 198.8 -0.06 FIG. 2.—Time series of red-backed vole {Ciethrionomys gapperi) Quercus alba 21 19.5 B 5.26 0.0 84.8 -0.11 and white-footed mouse {Peromyscus leucopus) relative abundance Acer ruhrum 22 4.8 C 0.75 0.0 13.9 0.22 (minimum number alive per 100 trap nights) on the Holt Research Pinus strobus 21 4.5 C 1.60 0.0 24.2 0.55** Forest, Maine, 1983-2004. Tsuga canadensis 21 0.9 D 0.31 0.0 5.6 0.14 Betula spp. 21 0.6 D 0.17 0.0 3.1 0.06 Abies' balsamia 21 0.2 D 0.09 0.0 1.6 -0.04 abundance plus seedfall, 1 model per seed series. The lagged relative abundance model took the form " Seedfall means with different lettei^ are different at F < 0.05 (Wilcoxon rank- sum test). '' Two asterisks (**) indicate 0.01 < 0.001 and 3 asterisks (*•*) indicate P < 0.0001. Nt = Po + -9lV,-l -(p2V,-2 -f E and the lagged relative abundance/seed models took the form for C. gapperi and P. leucopus. We did attempt to obtain an estimate of Nt = Po + Pi (seeds) 4- -(P|V,_| -(p2V,_2 -I- s population size {N) using several mark-recapture estimators, but with so few captures in low phases and low recapture rates within all trap where N, is MNA/100 trap nights, PQ is the intercept coefficient. Pi is sessions, population estimates were grossly inaccurate. However, with the seed coefficient, v,_i and v,_2 represent lags of N,, —cpi and —92 fixed sampling protocol and site, catch per unit effort represents are their coefficients, and s is unexplained error. We used the Akaike population trends as well as, or better than, N derived from statistical information criterion (AIC) to assess model fit and rank models models (Hopkins and Kennedy 2004; Slade and Blair 2000). (Hurvich and Tsai 1989). For each of the models, we bootstrapped the Accounting for the area trapped for seeds and using published seed C. gapperi series 1,000 times. We modeled each of the 1,000 series, weights (United States Department of Agriculture, Forest Service holding the actual seed series as a fixed input (seed models) and using 1974), we calculated seedfall as kilograms per hectare per year by the 1st value of the C. gapperi series as the starting value, and species. This resulted in a 22-year series for A. ruhrum and 21-year outputting a distribution of AIC scores. If the original AIC score fell series for the 6 other species and birch group, because seedfall before within the 5th percentile of the AIC distribution, we considered P^nt < 1983 for the autumn-winter dispersers was not known. 0.05 and concluded the process to be nonrandom (Efron and We calculated simple summary statistics for N, and seedfall. We Tibshirani 1993). obtained Pearson correlation coefficients (pps) between C. gapperi and P. leucopus, and between C. gapperi and seedfall (the current year's for A. rubrum; previous year's for all other tree species). For C. gapperi RESULTS we calculated the index of fluctuation {s) according to Henttonen et al. Sympatric C. gapperi and P. leucopus made up 81% of the (1985). Hansson and Henttonen (1985) considered s > 0.50 characteristic of a strongly fluctuating population. We did a spectral 8,366 individual small mammals captured in 41,682 trap nights analysis (Priestley 1981) to estimate the oscillation period of the over 22 years at the Holt Forest. Fifty-six percent (4,669) of C. gapperi series. individual captures were P. leucopus and 25% (2,091) were We prepared the data for time-series analysis by scaling (adding C. gapperi. P. leucopus relative abundance (N,) averaged 8.5 1 and log-transforming) the seed data, checking for trend in the re- per 100 trap nights and C. gapperi averaged 4.2 per 100 trap sponse (C gapperi) and input (seed) series, and checking for auto- nights (Table 1). correlation in the input series. Trend in the response can generate The 5 peak and 6 low phases of C. gapperi and P. leucopus spurious significant 2nd-order effects in a model (Saitoh et al. 1997), corresponded visually (Fig. 2) and the 2 series were signif- but the C. gapperi series exhibited no trend. A spurious significant icantly correlated (pp = 0.66; Table 1), indicating synchrony. 2nd-order effect in a population model may arise from autocorrelation Relative abundance of C. gapperi ranged from 0.06 to 8.27 in an input series (Williams and Leibhold 1995). First-order auto- voles per 100 trap nights (Table 1), a 138-fold difference. The correlation was detected only in the P. strobus series. Using autoregression (PROC AUTOREG—SAS Institute Inc. index of fluctuation {s) was 0.88, indicating a strong fluctuation 1999) with maximum likelihood, we specified nine 2nd-order in this population. The estimated oscillation period was 4.4 autogressive models. In the 1st, we tested the significance of lagged years. When the C. gapperi time series was fit to a 2nd-order relative abundance up to 2 lags (N,_| N,_2) as predictors of N,. For the lagged relative abundance model (r^ = 0.31), relative remainder of models, we tested the significance of lagged relative abundance from 2 summers previous (Nt_2) was a significant June 2006 ELIAS ET AL.—MAINE CLETHRIONOMYS CYCLES AND SEEDFALL 443

TABLE 2.—Linear autoregressive models of the relationship between red-backed vole {Ciethrionomys gapperi) minimum number alive per 100 trap nights (N,), eastern white pine {Pinus strobus) seedfall in the previous autumn, and N, at past lags on the Holt Research Forest, Arrowsic, Maine, 1983-2004. Livetrapping data are from 2-week, early-August trapping sessions conducted annually for 22 years (model « = 21 because seedfall before autumn 1983 was unknown). AICc = Akaike information criterion, corrected for small sample sizes.

Seeds N,-, N,_2 Model fit

Model P, SE P SE P 'P2 SE P Seeds r^ Total r^ AICc N, {{Pinus strobus, N,_i, N,_2;)" 0.86 0.22 0.00 -0.14 0.19 0.48 0.69 0.19 0.003 0.49 0.63 83.58 <0.001 N, 0.07 0.21 0.74 0.56 0.21 0.02 0.00 0.31 96.03 0.04 ' N, = Po + |5|(seeds) H—(piV|_|—(P2V|_2 + e . where v,_i and v,_2 are lags of N,. ' N, = Po H—9iV,_i-(p2V,_2 + e, where v,_i and v,_2 are lags of N,. predictor of curretit N,, and the series was consistent with a 2nd- DISCUSSION order autoregressive rather than random process (Table 2). Cyclic dynamic.—The C. gapperi population fiuctuation Over the 21 years seedfall was collected on the Holt Forest, pattem in Holt Research Forest was consistent with a cyclic seed mass of Q. rubra was roughly 5 times greater than that of dynamic based on the combined features of a 4.4-year P. rubens and Q. alba, and 26 times greater than that of A. periodicity, strong fluctuation, a significant 2nd-order lagged rubum and P. strobus (Table 1). C. gapperi N, was significantly relative abundance term in the autoregression models, and correlated only with P. strobus seedfall (pp = 0.60; Table 1). synchrony with sympatric P. leucopus. The estimated period- Above-average P. strobus seedfall preceded 4 out of 5 C. icity for P. leucopus on the Holt Forest was 4.0 years (Elias et al. gapperi peak phases (1985-1986, 1993-1994, 1997, and 2004). In Fennoscandia, periodicity of C. glareolus, C. 2001-2002) but 1 peak phase (1990) followed below-average rufocanus, and northem red-backed voles (C. rutilus) ranged P. strobus seedfall (Fig. 3). from 2.9 to 3.9 years in Fennoscandia's "transition zone" (60.5- Among 2nd-order lagged relative abundance models in- 64°N), and from 4.4 to 4.8 years above 67°N (Bj0mstad et al. cluding seedfall mass, only the P. strobus seed term was 1995). In cycling C. rufocanus populations in Hokkaido, Japan significant (Table 2). The 2nd-order autoregressive model (between 4rN and 45°N), periodicity was 3^ years (Bj0mstad including P. strobus seeds fit the data better than the simple et al. 1998). Gilbert and Krebs (1991) found that a southwestem 2nd-order autoregressive model. Previous autumn P. strobus Yukon population of C. rutilus followed a 3- to 4-year cycle. seedfall explained 48%, and the 2nd-order autoregressive term Therefore, periodicity of the time series for C. gapperi on the 15%, of the variation in Nt, for a total r^ of 0.63 (Table 2). The Holt Forest corresponds to the high end of the transition zone serially correlated input (seeds) may have infiated the co- ranges of the Yukon, Hokkaido, and Fennoscandia, and at the efficient of the 2nd-order lagged relative abundance term (0.69 low end of the northem Fennoscandian range. compared to 0.56; Table 2), as predicted by Williams and The C. gapperi fluctuation on the Holt Forest {s index = Leibhold (1995). Fortunately, we didn't face a situation where 0.88) was strong (>0.50) and greater than that of Hokkaidan C. the input elevated the 2nd-order term from insignificance rufocanus (0.42—Saitoh et al. 1998). Based on minimum to to significance, because the 2nd-order term in the simple maximum differences, the Holt Forest vole fluctuation (138- 2nd-order autoregressive model was significant {P = 0.02). fold) fell between that of Hokkaidan voles («> 18-fold—Saitoh et al. 1998) and Fennoscandian voles (C. glareolus, C. 25 T rufocanus, and M. agrestis, averaging 200-fold for each 1^ P/nus strobus species—Homfeldt 1994). The 2nd-order dynamic, found in -^ Ciethrionomys gapperi 20 - Holt Forest C. gapperi, was characteristic of approximately 80% of vole time series above 60.5°N in Fennoscandia (Bj0mstad et al. 1995) and of approximately 30% of vole populations in northeastem and central Hokkaido (Bj0mstad et al. 1998; Saitoh et al. 1998). The synchronicity observed between C. gapperi and P. leucopus has been reported among other rodent species in Fennoscandia. Homfeldt (1994) reported synchrony among C. glareolus, C. rufocanus, and M. agrestis in Sweden. Fluctua- 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 00 01 02 03 04 tions in C. glareolus in Fennoscandia were synchronized with Year at least 4 other microtine and 2 shrew {Sorex) species (Henttonen 1985; Henttonen and Hansson 1984; Henttonen FIG. 3.—^Time series of eastern white pine {Pinus strobus) seedfall (kg/ha) and red-backed vole {Ciethrionomys gapperi) relative et al. 1977). However, synchrony between Hokkaidan C. abundance (minimum number alive per 100 trap nights) on the Holt rufocanus and 2 field mouse species {Apodemus speciosus and Research Forest, Maine, 1983-2004. Seedfall mass for a given year A. argenteus) was weak (pp = 0.2 [Saitoh et al. 1999], versus was the crop of the previous autumn. PP = 0.66 in this study). 444 JOURNAL OF MAMMALOGY Vol. 87. No. 3

Relationships to seedfall.—In this study, C. gapperi was with 2nd-order terms have been attributed to specialist predator correlated with P. strobus seedfall and associated with P. strobus response (e.g., Boonstra et al. 1998; Hanski et al. 1991; Krebs seedfall in a 2nd-order autoregressive model. Vole-pine asso- 1996; Stenseth et al. 1996). In Chile, 2nd-order feedback in ciations have been found in other contexts. Swedish C. glareolus population dynamics of the leaf-eared mouse {Phyllotis was associated with pine {P. silvestris) seeds in a 2nd-order darwini) was related to bam owl {Tyto alba) predation (Lima autoregressive model (Homfeldt 1994); Abbott and Quink et al. 2002). Significant 1 st-order lagged abundance terms were (1970) reported presence of P. strohus seed caches where not obtained in this or the P. leucopus study (Elias et al. 2004), C. gapperi were trapped; and in a laboratory food trial with but in any case, synchrony in voles and mice would be difficult animals from the Holt Forest, C. gapperi ate 93% of P. strobus to explain given different food habits and social behavior. seeds offered compared to 17% of g. rubra acoms (Plucinski Therefore, assuming similar vulnerability to predation, the and Hunter 2001). However, the question of spurious correlation vole-mouse synchrony and significant 2nd-order lagged arises. In this study, above-average P. strobus seedfall did not relative abundance in both species' models suggested a numer- precede the 1990 vole peak, and in Connecticut, C. gapperi did ical or functional response of predators with a time delay. not respond numerically to P. strobus seeds (Schnurr et al. A new geographic gradient.—Geographic gradients in the 2002). Thus, the literature appears equivocal about the bi- cycling dynamic have been described in depth for Fennoscandia ological importance of P. strobus seeds to Ciethrionomys. and Japan. Fennoscandian C. glareolus grade from stable to Lack of response to A. balsamea was consistent with the cyclic from south to north and Japanese C. rufocanus from rejection of those seeds in food trials by Abbott (1962). Lack of southwest to northeast on the island of Hokkaido (Bj0mstad response to T. canadensis may have been an artifact of low et al. 1995, 1998). According to the Koppen climate classi- seed mass, but lack of response to P. rubens in a species that fication system (Blair 1942; Trewartha and Hom 1980), Maine, evolved in boreal conditions (Cook et al. 2003) was enigmatic. southeastem Scandinavia, eastem Europe, and Hokkaido share C. glareolus was associated with spmce seed crop in both the same climate: moderate summers, long winters with spells of Sweden (Homfeldt 1994) and Norway (Selds et al. 2002). Lack clear, cold weather, and a 90- to 130-day growing period. Given of response to A. rubrum does not seem surprising because its a choice between refining analyses of known gradients or seeds disperse in spring, when plenty of herbs and insects are finding new ones, Hansson and Henttonen (1998) recommended available. In contrast, a short-term study of 3 years by Schnurr that new ones be found. We suggest that the northeastem United et al. (2002) found that increased C. gapperi abundance States and southeastem Canada are promising places to look. followed higher A. rubrum seedfall. Given the high nutritional content of acoms, the lack of correlation between C. gapperi and acoms on the Holt Forest ACKNOWLEDGMENTS was puzzling. In Connecticut, Schnurr et al. (2002) also were We are grateful for the help of our field assistants during the more surprised to observe no link between acoms and C. gapperi. C. than 20 years of research at the Holt Research Forest. We thank the glareolus outbreaks in Europe are mast-dependent in oak and reviewers for excellent suggestions that improved the manuscript. The Holt Woodland Research Foundation supported this research. This is oak-beech forests, and in laboratory and field tests, C. glareolus Maine Agricultural and Forest Experiment Station Paper 2808. preferred oak and beech to smaller seeds (Hansson et al. 2000). Ggbczyriska (1976) found that European C. glareolus diet was I % tree seeds in spring and summer compared to 36% tree seeds LITERATURE CITED in fall and winter. C. gapperi populations from east of the ABBOTT, H. G. 1962. Tree seed preferences of mice and voles in the Mississippi River are difficult to distinguish from and closely Northeast. Joumal of Forestry 60:97-99. related genetically to C. glareolus (Cook et al. 2003), which ABBOTT, H. G., AND T. F. QUINK. 1970. Ecology of eastem white pine suggests C. gapperi should be able to eat acoms. However, C. seed caches made by small forest mammals. Ecology 51:271-278. gapperi may not have adapted to the size, hardness, and ANIMAL CARE AND USE COMMITTEE. 1998. Guidelines for the capture, secondary plant compounds of Q. rubra acoms. Merritt (1981) handling, and care of mammals as approved by the American has (rather ambiguously) described the skull and dentition of C. Society of Mammalogists. Joumal of Mammalogy 79:1416-1431. BJ0RNSTAD, O. N., W. FALCK, AND N. C. STENSETH. 1995. A geo- gapperi as "weak," suggesting that C. gapperi may not easily graphic gradient in small rodent density fluctuations: a statistical break the seed coat of an acom. Secondary plant compounds modelling approach. Proceedings of the Royal Society of London, influenced forage preferences of 3 Arctic microtines (Jung and B. Biological Sciences 262:127-133. Batzli 1981) and similarly may limit acom consumption by C. BJ0RNSTAD, O. N., N. C. STENSETH, T. SAITOH, AND O. C. LINJ/ERDE. gapperi. Clearly, a closer look at geographical and seasonal 1998. Mapping the regional transition to cyclicity in Ciethrionomys C. gapperi food preferences is needed. rufocanus: spectral densities and functional data analysis. Re- Underlying mechanisms of dynamics.—Increases in vole searches on Population Ecology 40:77-84. numbers associated with food surplus are short-term (e.g., BLAIR, T. A. 1942. Climatology, general and regional. 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