L. Scott Mills

Challenges in the quest for keystones

Mary E. Power is a professor in the Department of Integrative Biology, University of California, Berkeley, CA 94720. David Tilman is a professor in the Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108. James A. Estes is a wildlife biologist in the National Biological Service, Institute of Marine Science, University of California, Santa Cruz, CA 95064. Bruce A. Menge is a professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. William J. Bond is a professor doctor in the Department of Botany, University of Cape Town, Rondebosch 7700 South Africa. L. Scott Mills is an assistant professor in the Wildlife Biology Program, School of Forestry, University of Montana, Missoula, MT 59812. Gretchen Daily is Bing Interdisciplinary Research Scientist, Department of Biological Science, Stanford University, Stanford, CA 94305. Juan Carlos Castilla is a full professor and marine biology head in Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile. Jane Lubchenco is a distinguished professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. Robert T. Paine is a professor in the Department of Zoology, NJ-15, University of Washington, Seattle, WA 98195. ? 1996 American Institute of Biological Sciences. A keystone species is

The Keystone-Species Concept in Ecology and ConservationManagement and policy must explicitly consider the complexity of interactions in natural systems

1Will the extinction of a single species in a community cause the loss of many others? Can we identify a set of species that are so important in determining the ecological functioning of a community that they warrant special conservation efforts? The answer to these questions hinges on the existence of a limited number of species whose loss would precipitate many further extinctions; these species have often been labeled keystone species. The term keystone species has enjoyed an enduring popularity in the ecological literature since its introduction by Robert T. Paine in 1969: Paine (1969) was cited in more than 92 publications from 1970 to 1989; an earlier paper (Paine 1966), which introduced the phenomenon of keystone species in intertidal systems but did not use the term, was cited more than 850 times during the same period. As used by Paine and other ecologists, there are two hallmarks of keystone species. First, their presence is crucial in maintaining the organization and diversity of their ecological communities. Second, it is implicit that these species are exceptional, relative to the rest of the community, in their importance.

LIFE STAGE SIMULATION ANALYSIS: ESTIMATING VITAL-RATE EFFECTS ON POPULATION GROWTH FOR CONSERVATION

We developed a simulation method, known as life-stage simulation analysis (LSA) to measure potential effects of uncertainty and variation in vital rates on population growth (λ) for purposes of species conservation planning. Under LSA, we specify plausible or hypothesized levels of uncertainty, variation, and covariation in vital rates for a given population. We use these data under resampling simulations to establish random combinations of vital rates for a large number of matrix replicates and finally summarize results from the matrix replicates to estimate potential effects of each vital rate on λ in a probability-based context. Estimates of potential effects are based on a variety of summary statistics, such as frequency of replicates having the same vital rate of highest elasticity, difference in elasticity values calculated under simulated conditions vs. elasticities calculated using mean invariant vital rates, percentage of replicates having positive population growth, and variation in λ explained ...

Sensitivity analyses of the life cycle of midcontinent mallards

Relationships between vital rates and population growth rate (λ) are critical to understanding and managing population dynamics. Considerable study of the midcontinent mallard (Anas platyrhynchos) population has been directed to understanding how vital rates respond to environmental fluctuations and management, but inference to the relative importance of specific vital rates to λ remains weak. We used analytic and simulation-based sensitivity analyses of a stage-based matrix model of female midcontinent mallards to compare the relative importance of vital rates to λ. For each vital rate, we estimated mean values and process variation (biological variation across space and time) for females breeding on sites of approximately 70 km 2 in the Prairie Pothole Region (PPR) of the United States (Montana, North Dakota, South Dakota, Minnesota) and Canada (Saskatchewan, Manitoba, Alberta). We conducted perturbation analyses (i.e., analytic sensitivities and elasticities) to predict the relative influence of changes in vital rates on λ. We conducted variance decomposition analyses to assess the proportion of spatial and temporal variation in λ explained by process variation in each vital rate. At mean values of vital rates, analytic sensitivity of λ was highest to nest success and survival of adult females during the breeding season and non-breeding season; hence, equal absolute changes in these vital rates would be predicted to result in the largest Δλ, relative to other vital rates. Variation in sensitivities and elasticities across process variation in vital rates was primarily explained by variation in nest success and survival of ducklings. Process variation in breeding parameters was driving variation in λ: vital rates explaining the most variation were nest success (43%), survival of adult females during the breeding season (19%), and survival of ducklings (14%). Survival of adult females outside the breeding season accounted for only 9% of variation in λ. Our analyses suggested that predation processes on the breeding grounds were the primary proximate factors limiting population growth.

DNA reveals high dispersal synchronizing the population dynamics of Canada lynx

Population dynamics of Canada lynx (Lynx canadensis) have been of interest to ecologists for nearly sixty years. Two competing hypotheses concerning lynx population dynamics and large-scale spatial synchrony are currently debated. The first suggests that dispersal is substantial among lynx populations, and the second proposes that lynx at the periphery of their range exist in small, isolated patches that maintain cycle synchrony via correlation with extrinsic environmental factors. Resolving the nature of lynx population dynamics and dispersal is important both to ecological theory and to the conservation of threatened lynx populations: the lack of knowledge about connectivity between populations at the southern periphery of the lynxs geographic range delayed their legal listing in the United States. We test these competing hypotheses using microsatellite DNA markers and lynx samples from 17 collection sites in the core and periphery of the lynxs geographic range. Here we show high gene flow despite separation by distances greater than 3,100 km, supporting the dispersal hypothesis. We therefore suggest that management actions in the contiguous United States should focus on maintaining connectivity with the core of the lynxs geographic range.

OF MICE AND MEN AND TRILLIUM: CASCADING EFFECTS OF FOREST FRAGMENTATION

Cascading ecological effects of anthropogenic habitat fragmentation have been studied primarily in extreme cases (e.g., the isolation of habitat fragments in a novel habitat matrix such as suburban developments, reservoirs, or agricultural fields), with less attention to more subtle and widespread cases, such as habitat fragmentation due to timber harvest. Few studies have used rigorous demographic data to demonstrate the direct and indirect effects of habitat fragmentation. We trapped deer mice (Peromyscus maniculatus) at five sites over two years in southwest Oregon, USA, and used multi-state capture- recapture models to estimate deer mouse survival and movement in clearcuts, forest-frag- ment edges, forest-fragment interiors, and contiguous forests. We also estimated deer mouse densities in fragmented and unfragmented forests and combined deer mouse demographic studies with trillium (Trillium ovatum) seed predation trials to link deer mouse changes to reduced trillium recruitment previously observed at the same study sites. Mouse survival was highest in clearcuts, intermediate in forest fragments, and lowest in unfragmented (control) forests. Mouse movement among clearcuts, forest edges, and forest interiors was common over short time intervals. Collectively, demographic rates led to mouse densities that were 3-4 times higher at forest-fragment sites than at unfragmented sites. Trillium seeds were ;3 times more likely to be depredated in areas of elevated relative mouse abundance than in areas of lower relative abundance. Forest fragmentation has favored mouse populations, resulting in increased seed predation that may decrease recruitment rates and increase local extinction risks for trillium.

Identifying lynx and other North American felids based on MtDNA analysis

As part of a program to identify the distribution of Canada lynx (Lynx canadensis) across the U.S. using hair snags, we have developed a protocol to distinguish among all four felid species of northern North America (lynx, bobcat [Lynx rufus], cougar [Felis concolor], and domestic cat [Felis catus]) using mtDNA. Our tests were designed to be time and cost-efficient, and applicable to low-quantity or degraded DNA samples. Although it is possible to identify species using microsatellite DNA (e.g. Ernest et al. 2000), we favor mtDNA because of the greater copy number and because allele size constraints limit interspecific ranges of microsatellite DNA, potentially leading to allele frequency overlap (Nauta and Weissing 1996). Because mtDNA is highly conserved among tissue types within an individual, and because tissue samples amplify more consistently than hair, we developed and validated our protocol using both tissue and hair samples. For hair samples, 5–10 follicles with shafts were typically used in extraction, although in some cases we successfully used single hairs with or without follicles (see below). Genomic DNA was extracted using standard protocols for tissues (Dneasy tissue kit; Qiagen Inc.), with overnight incubation in lysis buffer and Proteinase K on a rocker at 60 • C. Elution of DNA was in 50 µl of buffer. To distinguish felid species from one another and from other species, we used the Polymerase Chain Reaction (PCR) to amplify two portions of the mito-chondrial genome (Figure 1). One region includes the control region, amplified using conserved, universal primers L16007 and H16498 (Kocher et al. 1989; Shields and Kocher 1991). Twenty-µl PCR reactions contained 50–100 ng DNA, 1× reaction buffer (Perkin-Elmer), 2.5 mM MgCl 2 , 200 µM each dNTP, 0.3 mg/ml BSA, 1 µM each primer, and 1 U Taq polymerase (Perkin-Elmer). After initial incubation at 94 • C for 5 min, the PCR profile was 35 cycles of 94 • C for 1 minute, 55 • C for 1 minute, and 72 • C for 1.5 minutes. PCR products were run in a 2.0% agarose gel (Asubel et al. 1989). The control region primers produced a PCR product of approximately 700 bp in all felid samples (Figure 1). This is the same region amplified by Foran et al. (1997a, b), except that primer L16007 results in a product 200 bp smaller, which we find amplifies with greater consistency. Felids have a 80–82 bp monomer within this region that …

Camouflage mismatch in seasonal coat color due to decreased snow duration

Most examples of seasonal mismatches in phenology span multiple trophic levels, with timing of animal reproduction, hibernation, or migration becoming detached from peak food supply. The consequences of such mismatches are difficult to link to specific future climate change scenarios because the responses across trophic levels have complex underlying climate drivers often confounded by other stressors. In contrast, seasonal coat color polyphenism creating camouflage against snow is a direct and potentially severe type of seasonal mismatch if crypsis becomes compromised by the animal being white when snow is absent. It is unknown whether plasticity in the initiation or rate of coat color change will be able to reduce mismatch between the seasonal coat color and an increasingly snow-free background. We find that natural populations of snowshoe hares exposed to 3 y of widely varying snowpack have plasticity in the rate of the spring white-to-brown molt, but not in either the initiation dates of color change or the rate of the fall brown-to-white molt. Using an ensemble of locally downscaled climate projections, we also show that annual average duration of snowpack is forecast to decrease by 29–35 d by midcentury and 40–69 d by the end of the century. Without evolution in coat color phenology, the reduced snow duration will increase the number of days that white hares will be mismatched on a snowless background by four- to eightfold by the end of the century. This novel and visually compelling climate change-induced stressor likely applies to >9 widely distributed mammals with seasonal coat color.

Population-specific vital rate contributions influence management of an endangered ungulate.

To develop effective management strategies for the recovery of threatened and endangered species, it is critical to identify those vital rates (survival and reproductive parameters) responsible for poor population performance and those whose increase will most efficiently change a populations trajectory. In actual application, however, approaches identifying key vital rates are often limited by inadequate demographic data, by unrealistic assumptions of asymptotic population dynamics, and of equal, infinitesimal changes in mean vital rates. We evaluated the consequences of these limitations in an analysis of vital rates most important in the dynamics of federally endangered Sierra Nevada bighorn sheep (Ovis canadensis sierrae). Based on data collected from 1980 to 2007, we estimated vital rates in three isolated populations, accounting for sampling error, variance, and covariance. We used analytical sensitivity analysis, life-stage simulation analysis, and a novel non-asymptotic simulation approach to (1) identify vital rates that should be targeted for subspecies recovery; (2) assess vital rate patterns of endangered bighorn sheep relative to other ungulate populations; (3) evaluate the performance of asymptotic vs. non-asymptotic models for meeting short-term management objectives; and (4) simulate management scenarios for boosting bighorn sheep population growth rates. We found wide spatial and temporal variation in bighorn sheep vital rates, causing rates to vary in their importance to different populations. As a result, Sierra Nevada bighorn sheep exhibited population-specific dynamics that did not follow theoretical expectations or those observed in other ungulates. Our study suggests that vital rate inferences from large, increasing, or healthy populations may not be applicable to those that are small, declining, or endangered. We also found that, while asymptotic approaches were generally applicable to bighorn sheep conservation planning; our non-asymptotic population models yielded unexpected results of importance to managers. Finally, extreme differences in the dynamics of individual bighorn sheep populations imply that effective management strategies for endangered species recovery may often need to be population-specific.

PELLET COUNT INDICES COMPARED TO MARK–RECAPTURE ESTIMATES FOR EVALUATING SNOWSHOE HARE DENSITY

Abstract Snowshoe hares (Lepus americanus) undergo remarkable cycles and are the primary prey base of Canada lynx (Lynx canadensis), a carnivore recently listed as threatened in the contiguous United States. Efforts to evaluate hare densities using pellets have traditionally been based on regression equations developed in the Yukon, Canada. In western Montana, we evaluated whether or not local regression equations performed better than the most recent Yukon equation and assessed whether there was concordance between pellet-based predictions and mark–recapture density estimates of hares. We developed local Montana regression equations based on 224 data points consisting of mark-recapture estimates and pellet counts, derived from 38 sites in 2 different areas sampled for 1 to 5 years using 2 different pellet plot shapes. We evaluated concordance between estimated density and predicted density based on pellet counts coupled with regression equations at 436 site-area-season combinations different from those used to develop the regression equations. At densities below 0.3 hares/ha, predicted density based on pellets tended to be greater than for mark–recapture; the difference was usually <1 hare per ha on an absolute scale, but at low densities this translated to proportional differences of 1,000% or greater. At densities above 0.7 hares/ha, pellet regressions tended to predict lower density than mark–recapture. Because local regression equations did not outperform the Yukon equation, we see little merit in further development of local regression equations unless a study is to be conducted in a formal double-sampling framework. We recommend that widespread pellet sampling be used to identify areas with very low hare densities; subsequent surveys using mark–recapture methodology can then focus on higher density areas where density inferences are more reliable.