Lecture Outline: Population Cycles

1. Lecture Outline: Population Cycles • Some history: beautiful hypotheses and ugly facts • How common are population cycles? • Components of cycles: periods and amplitudes • Questions and hypotheses • Case study: Snowshoe hares (Kluane Project) • Case study: Specialist predator hypothesis and vole cycles • Parasites and red grouse cycles

2. In early 1900s, wildlife biologists analyzed the fur trading records of the Hudson’s Bay Company, including those for the Canadian lynx. Population cycles—The “holy grail” of ecology • Long history of investigation without consensus regarding mechanisms. • Hope is that understanding population cycles will provide insight into more general issues of population regulation and dynamics. • Archbishop of Uppsala, Sweden published two reports on cyclic fluctuations of northern small rodents in mid-sixteenth century.

3. Elton established Bureau of Animal Population as unit within Department of Zoology and Comparative Anatomy at Oxford University. • Elton wrote famous textbook “Animal Ecology”. Charles Elton’s classic paper1 initiated scientific investigation of population cycles that continues today. 1Elton, C. 1924. Periodic fluctuations in number of animals: their causes and effects. Br. J. Exp. Biol. 2:119-163.

4. The difficulty of unraveling the mysteries of population cycles can be gleaned from the subtitle of a book by Dennis Chitty (trained in Elton’s Lab). • Chitty spent much of his career trying to explain periodic population fluctuations of small mammals but (like many others) had only limited success. The Chitty hypothesis proposed that the demographic changes occurring in vole and lemming cycles are mediated by natural selection operating on the genetic-behavioral composition of the population. • Populations consist of ‘docile’ and ‘aggressive’ types whose fitness varies with population density. • At high density, selection favors aggressive types that are good survivors but poor breeders. Population decreases. • At low density, selection favors docile type that are good breeders. Population increases.

5. Cycles were most common in mammal and fish populations. How common are population cycles? • Analyzed nearly 700 time series (25+ years) of animal populations for large-scale patterns in cycles. • Overall, nearly 30% of time series were cyclic. Kendall, BE et al. 1998. The macroecology of population dynamics: taxonomic and biogeographic patterns in populations cycles. Ecology Letters 1:160-164.

6. Proportion of cyclic populations increased with latitude (all data were from northern hemisphere), but pattern was driven by mammals. Mammals How common are population cycles? • However, studies were not random sample of species. North American fur-bearing carnivores dominated the mammal data, and most fish species were commercially harvested. • For birds, cycles seem to be more common for grouse than for other groups.

7. Components of cycles: period and amplitude • Period is amount of time it takes population to go through complete cycle. • Amplitude can be defined as difference between maximum population size and population size at midpoint, but some researchers refer to peak-to-trough amplitudes. • In general, periods tend to be fairly consistent for a particular cyclic population, whereas amplitudes are more variable.

8. Within a species, some populations are cyclic and others are not. • However, often broad spatial synchrony (70 – 1500 km) in population dynamics across a region where cycles occur. Some classic population cycles Species Period (yrs) Peak (no./ ha) Trough (no./ha) • Snowshoe hare 10 (9 – 11) 1-5 <0.01 • Northern voles 4 (3 – 5) 50 -300 <0.5 • Northern lemmings 4 (3 – 5) 10 – 200 <0.1 • Red grouse 4-10

9. Spatial synchrony among pairs of lynx time series

10. General questions • What stops population growth at peak densities? • What causes ensuing decline? • What causes recovery of population growth? • What affects the seasonal timing of decline? • What determines cycle length and amplitude?

11. Categories of hypotheses for population cycles • Abiotic (weather, sunspots) • Biotic intrinsic (genotypic-phenotypic physiological and behavioral changes) • Biotic extrinsic (food, predation, parasites, disease) • Much debate on whether any single-factor hypothesis will be adequate to explain cycles or whether multi-factor hypotheses are necessary. • Multiple factors could be from same category (e.g., predation-food quality) or from different categories (e.g., food quantity-genotypic/behavioral changes). • As usual, many ecologists advocate field experiments to test hypotheses, but these are logistically difficult to conduct for multi-factor hypotheses.

12. Which factors should be manipulated in experiment? (from Chitty 1996)

13. Nutrient Recovery Hypothesis (from Pitelka & Batzli 2007)

14. Case study: Snowshoe hare cycles • Non-territorial herbivore of boreal forest with 10-yr cycle • Reproduction: 3-4 litters per summer and average litter size of 5 leverets. Always first breed when 1-yr old, so age at sexual maturity is fixed. • Reproductive output reaches peak early in the phase of population increase, falls rapidly while population is still rising, and reaches lowest point during peak density or 1-2 years afterwards. Krebs, CJ. et al. 2001. What drives the 10-year cycle of snowshoe hares? BioScience 51:25-35.

15. Pattern of reproductive output in snowshoe hares

16. Pattern of survival in snowshoe hares • Survival begins to decline during the increase phase of the cycle before peak densities are reached (same as for reproduction) • Hence, maximal survival and reproduction occur early in increase phase.

17. ‘Food hypothesis’ has two forms: food quantity and food quality. • Food quality could be related to increase in secondary chemical compounds (tannins and resins) by plants in response to browsing by hares • Little general evidence that overall food quantity is limiting at any time. • Only 3% of hare mortalities directly attributed to starvation . • Food addition experiment (rabbit chow) resulted in 2-3 fold increase in density (mostly immigration) but hare cycle continue unchanged. • Second food addition experiment involved natural food (white spruce) Causes of cycle • Mostly like explanations involve three main factors—food, predation, and social interactions—that might act singly or in combination. Krebs, CJ. et al. 2001. What drives the 10-year cycle of snowshoe hares? BioScience 51:25-35.

18. Natural food addition experiment • Concluded that food shortage by itself is not explanation for hare cycle.

19. Predation hypothesis • Cause of death of 95% of radio-collared hares was predation (lynx, coyotes, goshawks, great horned owls). • All predators showed strong numerical changes that lagged behind hare cycle 1-2 years. • Lynx and coyotes killed more hares per day in peak and decline phase than during increase. • Conducted predator exclusion experiment in Yukon (“Kluane Experiment”) in which they kept mammalian predators out of two areas (1 km2 each) using electric fencing. • Also added food to one of the predator reduction treatments (note that these fence treatments were not replicated, whereas the controls were).

20. Predation hypothesis • Removal of mammalian predators increased survival rates. Again, food seemed to have a relatively minor effect. • Cannot pinpoint the role of any particular predator species and emphasize that cycle is not strictly a lynx-hare cycle.

21. Still unclear what might be driving changes in reproduction during cycle. • Suggested the “Stress Hypothesis” in which chronic stress is related to signs of predators (odor, tracks, unsuccessful chases) and thus predator density. • Likewise, reasons for the low phase that lasts for 2-4 years after decline are not well understood. • Nevertheless, Krebs et al. conclude that the 10-year hare cycle is a result of the interaction between predation and food supplies. Predation is dominant process; food effects are indirect. Cyclicity is caused by “time lag in both the indirect effects and the direct effects of predation”.

22. The Specialist Predator Hypothesis and Vole Cycles in Fennoscandia field vole (Microtus agrestis) least weasel (Mustela nivalis) “The Specialist”

23. Resident specialists are strongly coupled with prey, which leads to a delayed numerical response of predators to changes in prey population size and thus destabilizing delayed density-dependent mortality of rodents. • Predation by specialist predators might be a sufficient cause for rodent declines. The Predation Hypothesis and Vole Cycles Three types of predators: resident specialists, nomadic specialists, and generalists. • Generalist predators can prevent vole cycles by switching to prey upon voles when their density is high. They can cause direct density-dependent mortality. (Hanski et al. 1991. J. Animal Ecology 60:353-367. Hanski et al. 2001. Ecology 82:1505-1520)

24. The Predation Hypothesis and Vole Cycles • Other factors slow population growth of prey at high densities such as resource competition, social interactions (territoriality & infanticide), and generalist and nomadic specialist predators. • Nomadic specialistsinclude owls and diurnal raptors that track small mammal populations over large areas (i.e. ‘spatial switching’ instead of prey switching). Hence, the predation hypothesis predicts that generalist and nomadic predators have a stabilizing effect on rodent dynamics, whereas resident specialist predators drive population cycles.

25. In Fennoscandia, there is an increase in resident generalists and nomadic specialists as you move from north to south.

26. Degree of population fluctuations and cycle length are related to latitude for rodents in Fennoscandia.

27. Cycle amplitude versus latitude for field voles

28. Experimental support for the Predation Hypothesis? • Korpimaki and colleagues conducted predator manipulation experiments in large unfenced areas. • In first experiment, they manipulated breeding density of raptors that caused a short-term but not long-term change in dynamics of voles. • Conducted second experiment in western Finland during decline phase of voles. • Removal of just least weasels had no effect, whereas removal of all main predators resulted in densities that were 3-fold higher compared to control areas.

29. Experimental support for the Predation Hypothesis? • Replicated predator manipulation experiment in northern England. • Three control sites and three weasel removal sites (unfenced). • Density of weasels reduced via continuous livetrapping. • Weasel removal resulted in ~8% increase in adult survival. • Surprisingly, weasel removal resulted in lower juvenile survival. • All control and removal populations experienced a cyclic decline during winter. • Concluded that the impact of weasel predation on field-vole survival was neither necessary nor sufficient to drive population cycles. Graham, IM and X Lambin. 2002. J. Animal Ecology 71:946-956

30. Population cycles in red grouse • Two main competing hypotheses derived from studies in different geographical regions. • Parasite hypothesis (gut nematode) in England. • Territoriality hypothesis (aggressiveness and spacing behavior of males) in Scotland. See assigned reading for latest piece of the puzzle: Redpath et al. 2006. Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters 9:410-418.

31. The holy grail of population ecology is still out there. Beautiful hypotheses and ugly facts or Practical difficulties in designing field experiments?