Determinants of Lemming Outbreaks

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Determinants of Lemming Outbreaks Determinants of lemming outbreaks Rolf A. Ims1, Nigel G. Yoccoz, and Siw T. Killengreen Department of Arctic and Marine Biology, University of Tromsø, N-9037 Tromsø, Norway Edited by Stan Boutin, University of Alberta, Edmonton, AB, Canada, and accepted by the Editorial Board December 21, 2010 (received for review August 26, 2010) Population outbreaks in tundra rodents have intrigued scientists large tracts of sub- and low-Arctic Fennoscandian tundra, the for a century as a result of their spectacular appearances and their Norwegian lemming population has erupted only two times since general lessons in ecology. One outstanding question that has led the 1970s, during which time, interestingly, the sympatric gray- to competing hypotheses is why sympatric lemmings and voles sided vole has maintained a regular 5-y population cycle (7, 8). differ in regularity and shape of their outbreaks. Lemming out- Thus, the northern Fennoscandian tundra offers opportunities to breaks may be lost for decades while vole populations maintain elucidate why lemming and vole outbreak trajectories differ and regular population cycles. Moreover, when lemming populations why lemming outbreaks may get lost for long time periods. eventually irrupt, they do so more steeply than the vole popula- Besides the possibility that lemming–plant interactions are tions. Norwegian lemmings exhibited a large-scale outbreak more prone to irregularities (including a more variable outbreak synchronously with gray-sided voles in Finnmark, northern Fen- amplitude) than vole–predator interactions (8), there are two noscandia, during 2006 to 2007 for the first time in two decades. other hypotheses explaining why cyclic lemming outbreaks are Analyses of spatial variability of this outbreak across altitudinal impeded while sympatric voles maintain cycling. One assumes gradients allowed us to identify determinants of the contrasting that lemmings are more sensitive than voles to climate variation lemming and vole dynamics. The steeper lemming outbreak (10, 12). The other emphasizes community processes and pre- trajectories were caused by breeding and population growth dicts that lemming outbreaks are limited by indirect interaction during winter, when nonbreeding vole populations consistently with voles mediated by shared predators (13–15). To our know- declined. The differently shaped lemming and vole outbreaks ledge, no previous study has evaluated the relative merits of appear to result from a particular demographic tactic of lemmings these (not necessarily mutually exclusive) hypotheses. that evolved as an adaptation to the long and cold Arctic–Alpine During 2006 to 2007 a large-scale Norwegian lemming out- winters. The lemming outbreak amplitude increased with altitude break arose in Finnmark, in sub- and low-Arctic Fennoscandia, and vole density, indicating that lemming outbreaks are jointly for the first time in at least two decades. Based on spatially ex- facilitated by low temperatures and apparent mutualism with tensive monitoring of rodent populations at 109 tundra sites voles mediated by shared predators. High sensitivity to variation spanning an area of 10 000 km2, we were able to encompass in climate and predation is likely to be the reasons why lemmings substantial spatial variation in outbreak amplitude along repli- have more erratic population dynamics than sympatric voles. The cated climatic (i.e., altitudinal) gradients in lemmings and gray- combination of continued climatic warming and dampened vole sided voles. Here we provide an analysis of this variation that cycles is expected to further decrease the frequency, amplitude, sheds light on the differences and interrelations between lem- and geographic range of lemming outbreaks in tundra ecosystems. ming and vole dynamics and which factors may impede lemming outbreaks for decades. arctic tundra | climate impact | density dependence | spatial population dynamics Results To visually illustrate the spatiotemporal features of the lemming or centuries, lemmings have caught the attention of natural- outbreak compared with the dynamics of the gray-sided vole in Fists and scientists as a result of their spectacular population the entire monitoring area, we display spatially averaged out- dynamics and keystone functioning in tundra ecosystems (1–4). break trajectories for six separate subregions (Fig. 1). Although Charles Elton (5) was the first to recognize the cyclic nature of all rodent populations simultaneously had converged on very low lemming population outbreaks—a discovery that initiated a last- postoutbreak densities by spring 2008, the incipient stage of the ing research tradition that aims to identify causes of multiannual lemming outbreak differed markedly from that of the gray-sided cycles in animal populations (6). vole. The onset of the lemming irruption was delayed compared Current research on lemmings has been fueled by two recent with the onset of the increase phase of voles. From its onset, the discoveries made in the case of the Norwegian lemming Lemmus lemming outbreak arose steeply to reach sharp peaks simulta- lemmus, the most renowned lemming species (3). The first is that neously across the study region in fall 2007, although with large its outbreak trajectory is differently shaped from that of the gray- spatial variation in outbreak amplitude (i.e., peak densities; Fig. 1). sided vole (Myodes rufocanus), the often codominant rodent spe- Peak densities also varied in voles, but were reached more cies, which always exhibits population peaks synchronously with gradually, and the dynamics were more spatially asynchronous the lemming. Specifically, the lemming population erupts more than in lemmings. steeply than the vole population. This discrepancy in “outbreak To provide a quantitative, comparative assessment of pop- topology” has been suggested to result from different trophic ulation trajectories and their potential determinants in lemmings interactions; the “sharp” lemming outbreaks from an interaction and voles, we analyzed site-specific seasonal (winter and summer) with food plants, the “blunt” vole peaks from an interaction with growth rates during the lemming outbreak period (fall 2006 to fall predators (7, 8). However, there are still contrasting views on which factors regulate lemming populations (4, 6, 9). The other issue renewing ecologists’ search for circumstances Author contributions: R.A.I. and N.G.Y. designed research; R.A.I. and S.T.K. performed causing cyclic population outbreaks is the recent emergence of research; N.G.Y. analyzed data; and R.A.I. wrote the paper. collapsed cycles in several species (10). One well documented The authors declare no conflict of interest. case of a recent absence of outbreaks is that of a local Norwegian This article is a PNAS Direct Submission. S.B. is a guest editor invited by the Editorial lemming population in alpine southern Norway, where cyclic Board. outbreaks at regular 3- to 4-y intervals prevailed until the past Freely available online through the PNAS open access option. 15 y (11). However, this recent incident is not unprecedented. In 1To whom correspondence should be addressed. E-mail: [email protected]. 1970–1974 | PNAS | February 1, 2011 | vol. 108 | no. 5 www.pnas.org/cgi/doi/10.1073/pnas.1012714108 Downloaded by guest on October 1, 2021 8 72–288m 6 N=24 8 4 160–323m 6 N=18 2 Individuals per site Individuals 4 0 2004 2005 2006 2007 2008 2 8 Individuals per site 125 –341m 0 6 N=24 2004 2005 2006 2007 2008 71oN 4 n in la k su rd 2 in o per site Individuals n N e p 0 d 2004 2005 2006 2007 2008 r Norwegian lemming o i f Ba Grey-sided vole a re an n T tsSe Va rang er p a enin 02040 km sula 8 225–346m 6 N=18 Va 4 ran ger fio 8 2 rd 30– 80m Individuals per site Individuals N=14 0 6 2004 2005 2006 2007 2008 8 220–240m 4 6 N=11 2 4 per site Individuals 0 2 2004 2005 2006 2007 2008 Individuals per site Individuals 0 2004 2005 2006 2007 2008 Fig. 1. Population trajectories of Norwegian lemmings (L. lemmus) and gray-sided voles (M. rufocanus) displayed for six separate tundra subregions in eastern Finnmark, northernmost Fennoscandia. Population trajectories are based on the mean number of individuals caught per site (with SE bars) in spring and fall in each year. One individual/site corresponds to 4.17 individuals and 100 trap-nights. Small squares on the map denote the position of the trapping sites in each region. The number of trapping sites per subregion and the altitude range they spanned are provided in the panel for each subregion. 2007). On average, the Norwegian lemming had positive winter (Table 1). Indirect community interactions were indicated by growth rates, whereas they were consistently negative in the gray- a positive effect of density of voles on lemming growth rate sided vole (Table 1 and Fig. 1). Summer growth rates in lemmings during the winter. and voles were positive, although somewhat lower in the lemmings (Table 1). The degree of spatial coherence in growth rates was Discussion assessed by computing Moran I statistics. Also, this spatial aspect Our spatially extensive seasonal monitoring, which happened to of the seasonal dynamics differed between the lemming and the encompass the now rare event of a proper lemming outbreak in vole. Lemming growth rates exhibited spatial autocorrelation in northern Fennoscandia, allowed us to provide a detailed com- winter, but not in summer, whereas the gray-sided vole had the parison of the topology of the lemming outbreak with the si- opposite seasonal difference (Table 1). multaneous dynamics of the gray-sided vole. In accordance with We used linear state-space models (Methods) to estimate the previous studies (7, 8), the lemming exhibited a steeper increase effect of the following potential predictors of seasonal growth phase than that of the vole. However, the previous studies based rates (all model coefficients are provided in Table 1): direct their analysis of population growth rates taken at an annual time density dependence, altitude (as a proxy of climatic variation), scale (fall to fall); i.e., the population dynamics were not sepa- and density of voles (to estimate the effect of community inter- rated into seasonal components.
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