Of Mice and Men and Trillium: Cascading Effects of Forest Fragmentation

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Of Mice and Men and Trillium: Cascading Effects of Forest Fragmentation Ecological Applications, 13(5), 2003, pp. 1193±1203 q 2003 by the Ecological Society of America OF MICE AND MEN AND TRILLIUM: CASCADING EFFECTS OF FOREST FRAGMENTATION DAVID A. TALLMON,1,5 ERIK S. JULES,2 NIKKI J. RADKE,3 AND L. SCOTT MILLS4 1Division of Biological Sciences, University of Montana, Missoula, Montana 59812 USA 2Department of Biological Sciences, Humboldt State University, Arcata, California 95521 USA 3College of Natural Resources, University of Wisconsin, Stevens Point, Wisconsin 54481 USA 4Wildlife Biology Program, School of Forestry, University of Montana, Missoula, Montana 59812 USA Abstract. 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 ®elds), 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 ®ve 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. Key words: demography; edge effects; habitat fragmentation, direct and indirect effects; land- scape ecology; Paci®c Northwest, USA; Peromyscus maniculatus; plant±animal interactions; popu- lation dynamics; trillium recruitment, southwest Oregon, USA. INTRODUCTION water held behind a new dam. The conversion of the Despite evidence for the general importance of direct former hilltops into small islands in a reservoir has and indirect effects to community dynamics and wide- eliminated predators, allowing herbivore numbers to spread fragmentation of native habitats by humans, expand and then reduce seedling and sapling densities there are few examples of habitat fragmentation leading of a variety of canopy trees (Terborgh et al. 2001). In to important direct and indirect ecological effects. The Argentinian dry forest fragments embedded in an ag- few examples that exist are limited to cases in which ricultural matrix of crop ®elds and pastures, fragmen- the modi®ed habitat matrix is extremely different from tation has reduced pollinator visitation rates to under- the remaining intact habitat fragments. In southern Cal- story plants. This has decreased seed set in several of ifornia, humans have converted coastal sage±scrub these plants, possibly affecting their population dy- habitat into suburban developments and reduced the namics (Aizen and Feinsinger 1994). presence of coyotes (Canis latrans) in habitat frag- Most examples of habitat fragmentation are not as ments surrounded by the suburban matrix. This appears extreme as the aforementioned cases. In forests of the to have released mesopredators, such as housecats (Fel- U.S. Paci®c Northwest, like many regions throughout is catus), from predation risk by coyotes and allowed the world, extensive logging has created patches of these mesopredators to reduce songbird diversity in intact forest reduced in area and surrounded by a matrix habitat fragments (Crooks and Soule 1999). Dramatic of regenerating clearcuts of young trees (Garman et al. shifts in local species compositions have also followed 1999). Fragmented forests are now a dominant feature the isolation of Venezuelan hilltops with a matrix of of the Paci®c Northwest. Although remaining old for- ests show altered physical and biotic characteristics Manuscript received 29 March 2002; revised 24 January 2003; along their edges (Chen et al. 1992, 1995), we do not accepted 15 February 2003. Corresponding Editor: M. G. Turner. know of any examples in which direct demographic 5 Present address: Laboratoire d'Ecologie Alpine, UMR CNRS 5553, Universite Joseph Fourier, F-38041 BP 53 Cedex effects of fragmentation on a single species have trans- 09, Grenoble, France. E-mail: [email protected] lated into indirect impacts on other species in the forest 1193 1194 DAVID A. TALLMON ET AL. Ecological Applications Vol. 13, No. 5 PLATE 1. (Left) Fragmented forest landscape by Erik Jules. (Right) Deer mouse (Peromyscus maniculatus) by Milo Burchman. community. Forests in this region have long been sub- clearcuts. A possible cause for the lack of unity among ject to large-scale disturbances, such as moderate and previous studies is their nearly universal reliance upon stand-replacing ®res (Agee 1993). It is possible that counts or indices of abundance and survival to make the consequences of habitat fragmentation are not as ecological inferences. Demographic indices confound profound in landscapes where the modi®ed matrix is detection probability (the probability of detecting an not completely novel. In these situations, cascading individual that is present) with population parameters ecological effects may not be an important consequence of interest, such as survival or abundance (Nichols and of fragmentation. Pollock 1983). Consequently, demographic indices To understand the direct and indirect effects of hab- provide inaccurate measures of population processes itat fragmentation, it is critical to determine demo- when not all individuals present are detected or detec- graphic responses of single species to fragmentation tion probabilities are not constant across space and across the variety of habitats that compose the frag- time, and should be avoided wherever possible (e.g., mented landscape, as well as how these responses alter Thompson et al. 1998). interspeci®c interactions. Dif®culties in rigorously If deer mice do show demographic responses to measuring within- and among-population demographic clear-cutting and forest fragmentation (see Plate 1), processes have limited most studies to indexing or es- then this may have important implications for forest timating demographic rates in single habitats or pop- plants because mice are important seed predators in ulations (Nichols 1996). Furthermore, information on many communities throughout North America (e.g., movement rates among populations remains anecdotal Sork 1984, Willson and Whelan 1990, Ostfelt et al. or inferred from indirect measures, especially for ver- 1997, Maron and Simms 2001). At some of the same tebrates (Koenig et al. 1996, but see Spendelow et al. sites used in the present study, Jules (1998) found that 1995, Lindberg et al. 1998, Mills et al. 2003). trillium populations in clearcuts and along forest-frag- We sought to examine the relationship between deer ment edges are composed primarily of old individuals mouse (Peromyscus maniculatus rubidus; see Plate 1) that have failed to recruit enough individuals to main- demography and predation of trillium (Trillium ova- tain a stable age structure. Consequently, these popu- tum) seeds in fragmented forests where trillium pop- lations face increased extinction risks. The indirect ef- ulations are known to have reduced recruitment and fects of fragmentation on trillium populations are sub- increased extinction risk (Jules 1998, Jules and Rathcke tle because these populations contain a large proportion 1999). Deer mice have been studied extensively in for- of individuals that successfully produce seeds each year ests of the Paci®c Northwest, but previous studies have (Jules and Rathcke 1999). Jules (1998) reported that not linked deer mouse dynamics across habitats or even densities of trillium populations in fragment edges are reached consensus about the effects of timber harvest not much lower than the estimate provided for our study on habitat-speci®c demographic rates. Most studies area by R. H. Whittaker in 1949, before large-scale have found a positive effect of clear-cutting on deer logging began (Whittaker 1960). Without knowledge mouse populations (e.g., Tevis 1956, van Horne 1981), of the age structures of clearcut and fragment popu- but others have suggested that clearcuts have little de- lations, which can be determined only by counting an- mographic effect (Petticrew and Sadleir 1974), or may nual constrictions on their rhizomes, it would be dif- serve as sinks (Sullivan 1979a). At the same sites used ®cult to discern that these populations have almost no in the present study Mills (1996) found an increase in recruitment and elevated extinction risk. However, the relative abundance of mice along forest edges and counts of annual growth constrictions on trillium rhi- October 2003 CASCADING EFFECTS OF FRAGMENTATION
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