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Population Cycles in Voles and Lemmings: State of the 4 Mammal Review ISSN 0305-1838 1 REVIEW 2 3 Population cycles in voles and lemmings: state of the 4 5 science and future directions Journal Name No. Manuscript of 14 pages: No. S. Amul PE: 6 Madan K. OLI* Department of Wildlife Ecology and Conservation, University of Florida, MAM 12156 7 1 8 110 Newins-Ziegler Hall, Gainesville, FL 32611, USA. Email: olim@ufl.edu 9 10 11 2 Keywords ABSTRACT 12 Arvicoline rodents, consumer–resource 13 dynamics, maternal effects, population cycles, 1. Despite nearly a century of research, the causes of population cycles in 14 predator–prey dynamics Arvicoline rodents (voles and lemmings) in northern latitudes are not yet 15 fully understood. Theory tells us that delayed density-dependent feedback 16 *Correspondence author. mechanisms are essential for rodent population cycles, suggesting vegetation– 17 Submitted: 19 October 2018 rodent, rodent–parasite or rodent–predator interactions as the most likely 18 Returned for revision: 11 December 2018 drivers of population cycles. Dispatch: 13-4-2019 Dispatch: R Madhumitha CE: 19 Revision accepted: 5 February 2019 2. However, food provisioning, carried out either indirectly through fertilisation 20 Editor: DR treatments of the habitat or directly through food supplementation, has failed 21 to alter population cycles substantially, suggesting that variation in food sup- doi: 10.1111/mam.12156 22 ply by itself is not necessary or sufficient to cause cyclic fluctuations in 23 abundance. 24 3. Predator exclusion experiments conducted in Fennoscandia have succeeded 25 in slowing population crashes and increasing autumn densities, implicating 26 predation as the most likely cause of rodent cycles in this region. However, 27 experimental removal of specialist predators in northern England had no 28 discernible effect on a cyclic vole population, casting doubt on the notion 29 that predation is a necessary explanation of rodent population cycles. 30 4. Population cycle research has contributed substantially to our current under- 31 standing of the dynamics, regulation and persistence of biological populations, 32 but we do not yet know with certainty what factors or processes cause multi- 33 annual population fluctuations or if population cycles are driven by the same 34 mechanisms everywhere. Recent theoretical and empirical studies suggest that 35 extrinsic factors (primarily food supply and predator abundance) may interact 36 with population intrinsic processes (e.g. dispersal, social behaviour, stress re- 37 sponse) to cause multiannual population fluctuations and to explain biological 38 attributes of rodent population cycles. 39 5. Solving the enigma of population cycles may necessitate identifying factors 40 and processes that cause phase-specific demographic changes, and performing 41 conclusive experiments to ascertain the mechanisms that generate multiannual 42 density fluctuations. 43 44 3 INTRODUCTION lemmings and voles. He suggested that the causes of popu- 45 lation cycles in lemmings ‘lie either with the lemmings 46 Although periodic outbreaks in rodent numbers have been themselves or with their environment’, but that the cause 47 observed throughout recorded history, Elton (1924) was of periodicity must ‘lie with the environment’, in light of 48 the first to scrutinise the phenomenon of multiannual the spatial synchrony in lemming cycles. A careful reading 49 population fluctuations scientifically. In this exceptionally of his paper reveals that Elton envisioned many of the 50 insightful paper, Elton (1924) not only synthesised infor- modern ideas in animal ecology, including the concept of 51 mation on cyclic fluctuations in abundance of many animal population regulation, prey switching, trophic interactions 52 species, but also extensively explored causes and conse- and cascades, and climatic forcing. In essence, Elton’s (1924, 53 quences of population cycles with a particular focus on 1942) work on population cycles laid the foundation of Mammal Review (2019) © 2019 The Mammal Society and John Wiley & Sons Ltd 1 Mammalian population cycles M. K. Oli 1 the ‘Eltonian’ tradition of animal ecology, and influenced for convenience (e.g. Stenseth 1999, Hanski et al. 2001, 2 generations of ecologists. Nearly a century has elapsed since Turchin 2003), but most field studies show that these bio- 3 the publication of Elton’s seminal work, but population logical changes are nearly ubiquitous and indispensable 4 cycles remain enigmatic even today. components of rodent populations that exhibit cyclic or 5 The often contentious history of population cycle re- otherwise large- scale population fluctuations. Other features 6 search has been thoroughly discussed in the literature, of cyclic populations include latitudinal gradients in the 7 and the scientific progress has been reviewed periodically degree of cyclicity (e.g. populations in northern Europe 8 (e.g. Krebs et al. 1973, Tamarin 1978, Lidicker 1988, Batzli tend to be more cyclic than southern ones) and a broad 9 1992, Krebs 1996, Stenseth 1999, Berryman 2002, Hanski range of spatial synchrony within and among species 10 & Henttonen 2002, Lambin et al. 2002, Turchin 2003, (Stenseth 1999, Krebs 2013). Spatial patterns in cyclic dy- 11 Kelt et al. 2018). Here, I provide a thorough review of namics range from travelling waves (e.g. Lambin et al. 1998) 12 published research on rodent population cycles, highlight to highly synchronous fluctuations over large geographic 13 interesting features of cyclic rodent populations, review areas (e.g. Angerbjörn et al. 2001). Thus, any hypothesis 14 progress, discuss the possible reasons for our failure to attempting to explain population cycles must explain phase- 15 ascertain causes of population cycles, and identify knowl- specific changes in population characteristics as well as 16 edge gaps that must be filled to identify necessary and broader spatial and temporal patterns in abundance that 17 sufficient causes of population cycles. define population cycles. 18 19 CHARACTERISING RODENT POPULATION THEORETICAL FOUNDATIONS 20 CYCLES 21 The theoretical impetus for population cycle research has 22 The most prominent feature of cyclic populations are multi- been provided by two complementary ecological theories: 23 annual fluctuations in abundance with cyclic phases (increase, the theory of population regulation and the theory of preda- 24 peak, decrease and low phases) occurring every 3–5 years tor–prey (or, more broadly, consumer- resource) dynamics. 25 (Krebs 2013). Various statistical approaches have been used The former embodies the ‘density paradigm’, and the latter 26 to characterise population cycles, including the s-index, the ‘mechanistic paradigm’ of population ecology proposed 27 wavelet analysis, and time- series analysis (see Appendix S1 by Krebs (2002). The theory of population regulation pro- 28 for details). Field evidence shows that most, if not all, cyclic vides a conceptual foundation for our understanding of 29 rodent populations are characterised by phase-related changes how biological populations are regulated, and attempts to 30 in body mass, social behaviours, age structure, age at sexual explain why populations fluctuate as they do. Factors or 31 maturation, survival and reproductive rates (Chitty 1952, processes that prevent unlimited population growth have 32 1960, Krebs et al. 1973, Krebs & Myers 1974, Boonstra & long been debated in the literature (Nicholson 1933, 33 Krebs 1979, Boonstra 1994, Prevot- Julliard et al. 1999, Andrewartha & Birch 1954, White 2001, Turchin 2003), 34 Norrdahl & Korpimäki 2002); together, they constitute the but population regulation theory suggests that density- 35 ‘biological definition’ of population cycles (Krebs 1996). At dependent feedback mechanisms that permit populations 36 high densities, sexual maturation is delayed, the length of to grow at faster rates at low densities but reduce popula- 37 breeding season shortens, and juvenile survival rates and tion growth rates at high density are necessary and often 38 reproductive rates are reduced, the proportion of young sufficient for preventing unlimited population growth 39 animals in the population declines, and the mean age of (Royama 1992, Turchin 1999, 2003). Although the impor- 40 reproductive females increases; these changes precede and/ tance of abiotic (density- independent) factors in limiting 41 or accompany population crashes (Krebs et al. 1973, Boonstra populations is widely recognised, Royama (1992) argued 42 1994, Krebs 1996, Prevot- Julliard et al. 1999, Ergon et al. that population regulation necessarily implies density- 43 2001a, b, Norrdahl & Korpimäki 2002). At low densities, dependence, and that unregulated populations cannot persist. 44 these patterns are reversed. Another feature of cyclic popu- The structure of density-dependence determines the pattern 45 lations is the phase- related changes in body mass: individuals of population fluctuations (Royama 1992). Direct (or first- 46 are substantially heavier (up to 30% heavier) during the order) density- dependence typically leads to stable equilib- 47 high- density phase, and this is often referred to as the rium whereas delayed (or second- order) density- dependence 48 ‘Chitty effect’ (Chitty & Chitty 1962, Oli 1999). Also, social can generate a variety of dynamical patterns, including cyclic 49 behaviour may be affected (animals in high-density phases fluctuations, depending on the strength of direct and delayed 50 are much more aggressive than those in low- density phases; density- dependence. The primary
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