Concepts & Synthesis
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CONCEPTS & SYNTHESIS EMPHASIZING NEW IDEAS TO STIMULATE RESEARCH IN ECOLOGY Ecology, 86(10), 2005, pp. 2568±2577 q 2005 by the Ecological Society of America PARADOXICAL AVOIDANCE OF ENRICHED HABITATS: HAVE WE FAILED TO APPRECIATE OMNIVORES? DOUGLAS W. M ORRIS1 Department of Biology and Faculty of Forestry and the Forest Environment, Lakehead University, Thunder Bay, Ontario P7B 5E1 Canada Abstract. Omnivores have not ®gured prominently in our understanding of food webs and prey dynamics even though they can have substantial direct and indirect effects on the structure of ecological communities and on the dynamics of interacting species. The im- portant role of omnivores is implicated by the paradoxical results of a food-supplementation experiment. The experiment was designed to test theories that predict how habitat change affects the distribution of habitat-selecting species. According to theories of habitat selec- tion, a quantitative change in habitat (as caused by supplemental food) should increase consumer population size and alter habitat selectivity. Related theories of patch use predict that consumers should increase their use of enriched patches. A two-year experiment on two species of small mammals in Canada's boreal forest failed to alter population densities of red-backed voles, but did cause a dramatic shift in vole habitat use. Rather than increasing their use of feeding stations as predicted by classical theory, voles avoided them. Deer mice did not respond to the experimental treatments. The paradoxical results occurred because omnivorous black bears altered prey behavior by increasing predation risk at feeding stations. Revised theory con®rms the indirect omnivore effect, and demonstrates that the behavioral paradox is far more likely for omnivores than for other types of predators. The behavioral paradox of enrichment highlights not only important new, and potentially sta- bilizing, roles for omnivores, but also the pervasive in¯uences of behavior and habitat selection on population dynamics and regulation. Key words: boreal forest; competition; deer mice, ecology of fear; food web; habitat selection; ideal-free distribution; omnivore; paradox of enrichment; population regulation; predation risk; red- backed voles. INTRODUCTION zero. The result was anathema to those ecologists who believed that competition could be estimated from On occasion, great ecological insights emerge from niche (and habitat) overlap. Rosenzweig (1979) had a ``failed'' experiments. Perhaps the most famous ex- better idea. The species are in fact strong competitors; ample is Schroder and Rosenzweig's (1975) reciprocal so strong that the persistent threat of competition cre- removal experiment on two competing kangaroo rats. ates the very habitat preferences that eliminate our abil- When Schroder and Rosenweig removed Dipodomys ity to measure their competitive interaction. Rosen- ordii from its preferred desert grassland, they expected invasion by the closely related D. merriami. Instead, zweig's invention of isoleg theory proved the point, the grids were quickly repopulated by Ord's kangaroo and his clever metaphor to the ghost of competition rats. When they removed D. merriami from its favored cemented the concept ®rmly in the minds of community desert scrub, the area was reinvaded by Merriam's kan- ecologists. garoo rats. Even though the two seed-eating rodent I report on a similar ``failed'' experiment in Canada's species are similar, the experiment revealed stereotyped boreal forest that also reveals an extremely interesting habitat preferences that reduced competition to near and potentially widespread effect. My assistants and I enriched habitats exploited by red-backed voles (Cleth- rionomys gapperi). Study plots contained an equal mix- Manuscript received 31 May 2004; revised 8 December 2004; ture of ``shrub'' and ``moss'' habitat. We added sun- accepted 7 February 2005; ®nal version received 24 March 2005. Corresponding Editor: B. J. Danielson. ¯ower seed and rodent chow on different plots at sta- 1 E-mail: [email protected] tions representing either shrub, moss, or a mixture of 2568 October 2005 ON THE IMPORTANCE OF OMNIVORES 2569 the two. In the second year of the experiment we re- dix C). We used pretreatment vole data to measure versed the treatments. Voles avoided the enriched habitat preference along the habitat gradient so that we patches. When we reversed the treatments, voles re- could de®ne, for each plot, two equal groups of stations versed their preferences. We think we know why. Om- representing preferred (shrub), and less preferred nivorous black bears foraged extensively on the en- (moss) habitat. riched patches and increased the risk of predation to We estimated habitat use by trapping small mammals small mammals. with ``Longworth'' live traps for several trapping pe- I begin by describing the context and design of the riods (each station trapped over three consecutive ®eld experiment. I demonstrate how the experiment's nights) in 1991 through 1994 (Appendix B). We com- paradoxical results can be interpreted in the light of plemented our habitat-use data from live-trapping with increased predation risk from omnivorous predators. I counts of rodent tracks (an estimate of ``activity den- develop a simple theory that links the behavioral par- sity''; Kotler 1985; Appendix B). adox of enrichment to theories of habitat selection. I We collected control data on small-mammal abun- then use the theory to evaluate the relative roles of dance during three trapping periods in 1991. We col- predators vs. omnivores on prey habitat use and pop- lected experimental data in 1992 and 1993 (nine trap- ulation regulation, as well as their respective in¯uences ping periods each year) followed by a second control on the structure of food webs. year in 1994 (eight trapping periods). Each ®eld season began in mid-May and ended in early September. I CONTEXT OF THE EXPERIMENT estimated population densities and recruitment for each Theories of habitat selection predict that the spatial plot during each trapping period (Appendix B). distribution of individuals should re¯ect the ®tness that Beginning in 1992, I randomly assigned the eight they can expect to achieve in different habitats (Fre- ®eld plots to four treatment groups for supplemental twell and Lucas 1969, Rosenzweig 1981, Morris 1988, feeding in the 1992 and 1993 ®eld seasons. Two plots Concepts & Synthesis 2003; Appendix A). Fitness will depend on resource (1 and 6) served as natural controls. The controls re- levels (e.g., Sutherland 1983, Pulliam and Caraco 1984, ceived no supplement in either year. Plots 4 and 7 Fagen 1987, Morris 1994), on the ef®ciency of har- served as ``quantitative'' controls. I selected nine sta- vesting those resources (Morris 1988), and on the risks tions at random from each of the shrub and moss hab- associated with their harvest (Brown 1988). I attempted itats. The 18 stations received supplemental food in to test the theory with a multi-year experiment using 1992. The other 18 stations on plots 4 and 7 received red-backed voles as the primary model organism. The food in 1993. The remaining plots received ``qualita- experiment was centered on food-supplementation tive'' treatments. Plots 2 and 5 received supplemental treatments (increased resource), that allocated those food in the ``shrub'' habitat. All 18 shrub stations on supplements differentially to preferred (shrub), less each plot received supplemental food in 1992. Plots 3 preferred (moss), or a shrub±moss mixture of habitats. and 8 received supplemental food in the ``moss'' hab- According to current theory and intuition, vole den- sities should have increased in treated plots relative to itat. I reversed the treatments in 1993 (plots 2 and 5 controls, and the increase should have been greater in received food in the moss habitat, plots 3 and 8 received preferred habitat (with its associated high foraging ef- food in the shrub habitat). We trapped all plots again ®ciency and low risk of mortality) than in secondary in 1994 for comparison with the pretreatment data col- or mixed treatments. lected in 1991 (temporal control). The six treatment plots received the twice-weekly METHODS food supplements. We calculated the expected ener- Several assistants and I manipulated habitat richness getic needs of voles when at maximum density (30 in a large homogeneous fragment of boreal forest in voles per plot from the 1991 data; mean August density northwestern Ontario, Canada (488559 N, 898559 W; 5 29.125 voles), then doubled that value (Appendix Appendix B). In 1991 we established eight 1-ha rep- D). We broadcast two forms of resources, sun¯ower licate study plots, arranged with two columns and four seeds and rodent chow (to ensure access to both energy rows. We separated each 100 3 100 m plot from its and essential nutrients), at the calculated rate (totaling neighbors by an intervening equal-sized, 1-ha area that four times the energetic requirements of voles). we avoided during the entire study. The outside margin I compared vole population numbers, habitat selec- of the ``checkerboard'' was at least 200 m from the tivity, and recruitment on treatment plots with the nat- edge of disturbed habitat (roads and small cutblocks). ural controls to assess the in¯uence of supplemental Each study plot was composed of a 6 3 6 sampling food (Table 1). I compared ``shrub and moss treat- grid with 20-m spacing between the 36 sample points. ments'' with the quantitative controls to evaluate pos- We began by measuring habitat and vegetation at all sible differences in foraging ef®ciency or risk associ- sampling stations, and then summarized the data with ated with food located in alternative habitats. I repeated principal-components analysis to create a single com- the tests with deer mice, the second most abundant posite variable representing habitat variation (Appen- rodent species. 2570 DOUGLAS W. MORRIS Ecology, Vol. 86, No. 10 TABLE 1. A brief summary of key predictions and results from a ®eld experiment that supplemented food for red-backed voles in preferred and less preferred habitats in boreal forest located in northern Ontario, Canada.