Ecology, 84(10), 2003, pp. 2589±2599 ᭧ 2003 by the Ecological Society of America

SPATIAL OF PREDATOR±PREY INTERACTIONS: CORRIDORS AND PATCH SHAPE INFLUENCE SEED

JOHN L. ORROCK,1,4 BRENT J. DANIELSON,1 MOLLY J. BURNS,2 AND DOUGLAS J. LEVEY3 1Ecology and Evolutionary Biology Interdepartmental Graduate Program, 124 Science II, Iowa State University, Ames, Iowa 50011-3221 USA 2Department of Natural Ecology and Management, 124 Science II, Iowa State University, Ames, Iowa 50011-3221 USA 3Department of Zoology, University of Florida, Gainesville, Florida 32611-8525 USA

Abstract. Corridors that connect patches of disjunct may be promising tools for mediating the negative impacts of , but little is known about how corridors affect ecological interactions. In eight 12-ha experimental landscapes, we ex- amined how corridors affect the impact of invertebrate, rodent, and avian seed predators on pokeweed, Phytolacca americana. Over 13 months in 2000 and 2001, we quanti®ed the effects of patch shape, connectivity, and predator type on the number of seeds germinating in the ®eld (germinants), seed removal, and the viability of remaining seeds. Corridors did not affect the number of P. americana germinants in experimental ex- closures or the viability of seeds remaining in exclosures. However, corridors affected the removal of seeds in a predator-speci®c manner: invertebrates removed more seeds in un- connected patches, whereas rodents removed more seeds in connected patches. Seed removal by birds was similar in connected and unconnected patches. Total seed removal by all seed predators was not affected by corridors, because invertebrates removed more seeds where rodents removed fewer seeds, and vice versa. Overall, seed predation signi®cantly reduced the number and viability of remaining seeds, and reduced the number of germinants in 2000 but not in 2001. The of naturally occurring P. americana plants in our experimental patches in 2000 decreased with increasing seed removal from exclosures but was not related to viability or germinants in 2000, suggesting that seed removal may shape the distribution and abundance of this . Complementary patterns of seed removal by rodents and invertebrates suggest that corridors alter the effects of these predator taxa by changing the relative amounts of edge and core (nonedge) in a patch. Because invertebrates and rodents do not completely overlap in the seeds they consume, corridors may change predation pressure on seeds that are primarily consumed by one predator type, with potential consequences for the com- position of plant and seed predator communities. Key words: corridors; patch shape; Phytolacca americana; predator±prey interactions; Savannah River Site, South Carolina (USA); seed predation.

INTRODUCTION serve a target species only to discover that an important predator uses corridors more effectively than the spe- Habitat fragmentation and species loss are occurring cies of concern. on a global scale, yet few experimental studies have By facilitating predator movement, corridors may im- examined the effects of fragmentation on ecological pact prey that rely upon ``predator-free'' space (e.g., Holt communities (Gonzalez et al. 1998, Collinge 2000, De- and Lawton 1993). Moreover, corridors could alter the binski and Holt 2000, Davies et al. 2001). Corridors spatial or temporal asynchrony that promotes the per- connect habitat fragments and are thought to promote sistence of some predator±prey interactions (e.g., Earn population persistence by promoting gene ¯ow, pop- et al. 2000). Empirical work in microcosms reveals that ulation rescue, and increasing abundance (Rosenberg corridors can affect persistence of predator±prey systems et al. 1997). However, corridors have been criticized (Holyoak and Lawler 1996), but also warns that con- because mechanisms underlying purported corridor ef- necting patches can sometimes lead to counterintuitive fects are unknown (Simberloff et al. 1992). Perhaps outcomes (Burkey 1997, Holyoak 2000). We use an ex- more worrisome, the population-level focus of most perimental landscape to evaluate how corridors affect corridor studies neglects the rest of the ecological mi- the ecology of predator±prey interactions. lieu, with largely unknown consequences. For example, imagine the impact of constructing corridors to pre- Study system: corridors, seeds and seed predators

Manuscript received 22 July 2002; revised 24 January 2003; Seeds can be considered sedentary prey consumed accepted 3 February 2003. Corresponding Editor: E. S. Menges. by vertebrate and invertebrate predators (Janzen 1971, 4 E-mail: [email protected] Hulme 1998). Seed predation can lead to dramatic re- 2589 2590 JOHN L. ORROCK ET AL. Ecology, Vol. 84, No. 10 ductions in the standing crop of seeds and may be the primary determinant of plant distribution in some sys- tems (e.g., Louda 1989, Brown and Heske 1990, Hulme 1998, Howe and Brown 1999, 2000, 2001). By in- creasing the deposition of bird-dispersed seeds (Tewks- bury et al. 2002, Haddad et al. 2003), corridors could have positive impacts on bird-dispersed plants. How- ever, the ultimate effect of corridors on bird-dispersed plants could be negative if corridor-mediated changes in seed predation offset or outweigh corridor-mediated increases in seed deposition. Corridors may affect seed predation by altering the movement of seed predators between connected patch- es of suitable habitat (``corridor effects'') or by making it more likely that an individual moving through an uninhabitable matrix will encounter a suitable patch (``drift-fence effects'' [Rosenberg et al. 1997]). Cor- ridors also add area to a patch, and may affect seed predation by providing more habitat for seed predators (``area effects'' [Haddad and Baum 1999]). Moreover, FIG. 1. Layout of the experimental landscape at the Sa- because corridors tend to be relatively long, linear el- vannah River Site, South Carolina. Eight experimental units were created by clearing mature pine forest. Each experi- ements, they can induce area effects by changing the mental unit consisted of connected (C) and unconnected amount of edge habitat relative to the amount of core patches that were either rectangular (R) or winged (W). All habitat in a patch. Mammals (Bennett 1990, La Polla patches were clearcut habitats separated by 150 m of mature and Barrett 1993, Bennett et al. 1994, Bowne et al. pine forest. Within each patch, one of each exclosure type 1999, Coffman et al. 2001, Haddad et al. 2003), in- was installed around the center of the patch (®nal inset). vertebrates (Haddad 1999, 2000, Haddad and Baum 1999, Collinge 2000), and frugivorous birds respond to corridors (Tewksbury et al. 2002). By affecting the ration of our study allowed us to integrate temporal movement and abundance of a particular type of seed variation in seed predation (Whelan et al. 1991) not predator, corridors could change seed predation by that incorporated in many seed predation studies. (Most predator type. studies last Ͻ4 wk, e.g., Hyatt 1998.) Moreover, the Pokeweed, Phytolacca americana, is a perennial duration of our experiment allowed us to evaluate the plant indigenous to eastern North America that is typ- importance of corridors, patch shape, and seed pre- ically found in early successional habitats (Mitich dation during a critical period of establishment for P. 1994). Phytolacca americana produces berries con- americana in our study system. sumed by many bird species (Mitich 1994), which sub- Our objectives are framed as three questions: (1) Do sequently disperse P. americana seeds (McDonnell et corridors affect seed predation by invertebrates, ro- al. 1984, Mitich 1994). Pokeweed seeds are 2.5±3 mm dents, and birds? (2) Are rates of overall seed predation in size (Radford et al. 1968) and can remain viable in affected by corridors? (3) Is the abundance of naturally the seed bank for at least 40 years (Toole and Brown occurring P. americana plants in our study system re- 1946). Predispersal seed predation is probably mini- lated to rates of seed predation, i.e., is there evidence mal, as rodents reject pokeweed fruits, but readily con- that seed predators affect the distribution of P. amer- sume P. americana seeds (McDonnell et al. 1984, Hyatt icana? 1998), and damage to P. americana fruits by rodents METHODS or invertebrates was never observed during ®eld col- lection of several thousand fruits (J. L. Orrock et al. Experimental design personal observation). Thus, if corridors affect seed Experimental landscape.ÐThe experiment was con- predators, there may be direct consequences for P. ducted in eight replicated experimental units created at americana . the Savannah River Site, a National Environmental Re- We used an experimental landscape composed of search Park (NERP) near Aiken, South Carolina. Each clearcut patches separated by a pine forest matrix to experimental unit consisted of ®ve patches created dur- evaluate the effect of corridors on seed predators and ing the fall and winter of 1999 by clear-cutting mature Phytolacca seeds. For 13 months, we measured three pine forest (the matrix) followed by prescribed burning different metrics to determine the impact of seed pred- (Fig. 1). In each experimental unit, there were three ators on P. americana: the number of seedlings emerg- different patch types: connected, rectangular, and ing (hereafter called germinants), the number of seeds winged (Fig. 1). Connected patches were joined by a removed, and the viability of remaining seeds. The du- 25 m wide corridor that was 150 m in length. Rect- October 2003 CORRIDORS AND SEED PREDATION 2591

TABLE 1. Three effects may lead to the increased predation of seeds in corridors, because corridors change patch shape as well as patch connectivity. Each effect leads to testable predictions for the intensity of seed predation in connected patches (Conn), rectangular patches (Rect), or winged patches (Wing).

Predicted predation Effect Description intensity Area effects Corridors increase total amount of habitat and also in- crease edge relative to core habitat in patch. Effects differ depending upon predator's response to edge: Edge-selecting predators Conn Ͼ Rect; Conn ഠ Wing Edge-neutral predators Conn ഠ Rect ഠ Wing Edge-avoiding predators Rect Ͼ Conn; Conn ഠ Wing Corridor effects Predator abundance is increased because movement be- Conn Ͼ Wing; Wing ഠ Rect tween connected patches dampens effects of stochastic events on predator populations. Predators may also har- vest more seeds by moving between connected patches. Drift-fence effects Predators moving through the matrix encounter the corri- Wing ഠ Conn; Wing Ͼ Rect dor and follow it into the patch. angular patches consisted of a 1-ha square patch with Seed predation.ÐWe used exclosures to determine 0.375 ha of additional area, representing the area added the effect of different types of seed predators on P. by the corridor (Fig. 1). Winged patches consisted of americana seeds. All exclosures were cylindrical wire a 1-ha square patch with two extending ``drift-fence'' cages ϳ32 cm in diameter and 16 cm high. The four sections, each 75 m long and 25 m wide (Fig. 1). Two treatment types were: (1) access by no seed predators connected patches were in each experimental unit. Four (hereafter referred to as NONE); (2) access by inver- of the experimental units had two rectangular patches tebrates (I); (3) access by invertebrates and rodents and one winged patch, whereas the other four experi- (IR); (4) access by invertebrates, rodents, and birds mental units had two winged patches and one rectan- (ALL). To exclude all seed predators, NONE treatments gular patch, yielding a total of 12 winged patches, 12 used exclosures with walls of 1.5-cm2 mesh hardware rectangular patches, and 16 connected patches. cloth covered with ®berglass window screen (Ͻ1-mm2 Dissecting the role of corridor, drift-fence, and area mesh); although smaller ants could enter these exclo- effects.ÐOur design allowed us to determine the rel- sures, they could not remove seeds. Exclosures with ative importance of corridor, drift-fence, and area ef- sides constructed of hardware cloth with 1.5-cm2 open- fects on seed predation because each type of effect ings were used to exclude birds and rodents for inver- makes a speci®c prediction (Table 1). It is important tebrate-access treatments (I). IR treatments used ex- to note that, although patches were of similar area, each closures with walls constructed of hexagonal poultry patch type differed in the relative amounts of edge and wire with 4-cm2 openings. ALL treatments used ex- area habitat because of changing patch shape. This is closures with sides constructed of wire fencing with simply illustrated by the area/perimeter ratio for each 20-cm2 openings. Each exclosure had a top constructed patch type: 22.62 for connected patches, 19.64 for of ®berglass window screen that excluded most seed winged patches, and 28.95 for rectangular patches. If rain, including seeds of P. americana. seed predation is affected by edge, then edge-neutral, We randomly placed one of each exclosure type edge-selecting, and edge-avoiding seed predators along a central 8-m square within each of the 40 patches should display different patterns (Table 1) in response to the changing perimeter (because area is relatively (Fig. 1), yielding 160 total exclosures (4 exclosures per constant) among patch types. patch in 40 patches). At each exclosure site, leaf litter, Winged and rectangular patches had the same area debris, and resident plants were removed and the top (1.375 ha), whereas connected patches had slightly less 7 cm of soil was mixed to standardize conditions among area than unconnected patches because they shared a exclosures. A weighed portion of ®eld-collected P. corridor (central patch area plus half of the corridor ϭ americana seeds (mean Ϯ 1 SE ϭ1.98 Ϯ 0.01 g; equiv- 1.1875 ha). The small difference in total area between alent to 312 Ϯ 3.7 seeds) was placed on the soil surface, connected and unconnected patches does not change and the exclosure was placed over the seeds. This the qualitative order of our predictions (Table 1). Rath- amount of seeds approximates the number of seeds that er, it provides a more stringent test of the importance collects under isolated perches at our site (D. J. Levey, of movement through corridors as a means for preda- unpublished data). A 4-cm galvanized steel ring was tors to exploit seeds. If seed predation is greatest in pushed into the soil around the edge of each exclosure connected patches, despite the slightly reduced overall so that 1 cm was above the soil surface. This did not area and drift fence in connected patches, we have a prevent access to the exclosure by seed predators (ants stronger case for movement-mediated changes in seed readily traversed the ring), but reduced the likelihood predation. of seeds washing or blowing into or out of the exclo- 2592 JOHN L. ORROCK ET AL. Ecology, Vol. 84, No. 10 sures. The base of the exclosure and the retaining ring P. americana is rarely found in the understory of ma- were anchored into the soil with 15-cm steel turf stakes. ture pine forest, plants counted in our census almost Once established in June 2000, exclosures were vis- certainly established from seed after our plots were ited twice per month during the growing season cleared seven months earlier. (March±September). Germinants of P. americana were counted and removed during each visit. Germinants of Statistical analyses all other species were removed. During the course of Corridors and seed predation by invertebrates, ro- the experiment, small anthills were observed within dents, and birds.ÐWe used multivariate analysis of two NONE exclosures. Ant-repellent granules (Spec- covariance (MANCOVA, Scheiner 2001) to accom- trum Brands, St. Louis, Missouri, USA) sprinkled modate the inherent dependencies among exclosure around the outside of the exclosures eliminated this treatments: rodents and invertebrates could forage from problem. At the conclusion of the seed predation trials in July 2001, all seeds were exhumed from exclosures more than one exclosure type, interactions among pred- to a depth of 7 cm by one person to minimize any bias ators could alter among exclosures, and the in soil collection techniques. Pokeweed seeds were recovery rate of seeds may have differed among patch- sieved from the soil and counted. es. A separate MANCOVA was used for each metric Because local habitat characteristics can affect seed of seed predation: number of germinants, seed removal, predation (Reader and Beisner 1991, Hulme 1997, and seed viability. Each MANCOVA had four depen- Manson and Stiles 1998), substrate and dent variables corresponding to the values obtained characteristics were measured ina1mradius extending from the four different exclosure treatments (NONE, from the center of all exclosures open to predators (i.e., I, IR, and ALL). Because preliminary analyses indi- I, IR, and ALL treatments) in late July 2000. For con- cated signi®cant differences in ®eld germination be- sistency, only two investigators quanti®ed habitat char- tween 2000 and 2001 (paired t test, t ϭ 3.60, df ϭ 39, acteristics, visually estimating the percent cover of P Ͻ 0.001), we performed two MANCOVA analyses downed woody debris, woody plant material, vegeta- for ®eld germination, one for each year of germination tive plant material, bare soil, and leaf litter. data. Seed viability.ÐWe used germination trials to test Our models speci®ed experimental unit and the type the viability of exhumed seeds. This estimate of via- of patch (connected, rectangular, or winged) as ®xed bility may be conservative because dormancy and sen- effects (random effects cannot be modeled with MAN- sitivity to environmental factors varies seasonally and COVA, Scheiner 2001). Substrate and vegetation data annually in P. americana (Baskin and Baskin 2001). were examined as possible covariates. Comparing the As such, seeds removed from the ®eld in July may be number of remaining seeds (our second metric of seed less likely to germinate than seeds collected during predation) assumes that the number of germinants was optimal germination times earlier in the year (Baskin constant among treatments. Although the qualitative and Baskin 2001). outcome of our analyses would be the same if this For each exclosure, we ®lled a 5 ϫ 5 ϫ 6-cm com- assumption were not met, comparison of germinants partment of a standard plastic seedling ¯at with heat- over the entire sampling period supports this assump- sterilized sand and placed recovered P. americana tion (paired t tests, df ϭ 39, t Ͻ 0.77, P Ͼ 0.44; see seeds on the surface of the sand. Seedling ¯ats were also Table 2). placed in a growth chamber with a 14:10 light:dark If signi®cant patch type effects were found in MAN- photoperiod and a 31Њ:27ЊC temperature regime (Farm- COVAs, we used planned pairwise multivariate con- er and Hall 1970). Seeds were watered daily from 1 trasts of patch type effects (Scheiner 2001) to test the September to 31 October 2001, with the exception of predictions that distinguish corridor, drift-fence, and one day due to logistic dif®culties. Germinants were area effects (Table 1). We follow the multivariate con- counted and removed weekly. The remaining seeds trasts with univariate ANCOVAs that use the difference were sieved from the sand and counted. between exclosure types as the dependent variable Surveys of naturally recruiting P.americana.ÐPoke- (Scheiner 2001) to determine if the relationship be- weed plants were censused in nine 25 ϫ 25-m plots in tween exclosure treatments changed with patch type. all patches in September of 2000. The nine plots were For example, if rodents removed more seeds than in- ina3ϫ 3 array that was centered in each patch, leaving vertebrates in one patch type, but not in another, the a buffer strip of 12.5 m along patch edges that was not univariate ANCOVA would detect a signi®cant effect censused. Within each plot, we walked four equally of patch type on the difference between I and IR ex- spaced transects, ϳ6 m wide, and recorded all P. amer- closures. This approach also allows us to assess the icana plants that were visible and easily identi®ed with- contribution of each predator type to overall seed pre- out squatting. In essence, this technique provided an dation in each patch type. These analyses were all estimate of established plants because we were rarely planned, i.e., we did not perform tests in an exploratory able to detect small seedlings. Stems that appeared fashion. As such, we did not adjust ␣ for multiple tests joined at the base were counted as single plants. Since (Day and Quinn 1989), although such an adjustment October 2003 CORRIDORS AND SEED PREDATION 2593

TABLE 2. Effect of patch type (connected, rectangular, winged) and experimental unit (EU) on three different metrics of seed predation.

Metric of predation Factor Pillai's trace F df P Field germination 2000 patch type 0.49 1.14 8, 28 0.37 EU 1.29 1.10 28, 64 0.37 patch type ϫ EU 1.91 1.04 56, 64 0.43 Field germination 2001 patch type 0.27 0.54 8, 28 0.82 EU 0.99 0.76 28, 64 0.79 patch type ϫ EU 1.55 0.72 56, 64 0.89 Number of seeds remaining patch type 0.94 2.88 8, 26 0.02 EU 1.48 1.53 28, 60 0.21 patch type ϫ EU 2.30 1.45 56, 60 0.09 woody debris 0.78 10.46 4, 12 Ͻ0.01 Multivariate contrasts Conn vs. Wing 0.20 0.74 4, 12 0.58 Conn vs. Rect 0.72 7.58 4, 12 Ͻ0.01 Rect vs. Wing 0.71 7.26 4, 12 Ͻ0.01 Viability of remaining seeds patch type 0.62 1.45 8, 26 0.23 EU 1.55 1.35 28, 60 0.16 patch type ϫ EU 2.19 1.29 56, 60 0.16 leaf litter 0.69 6.39 4, 12 Ͻ0.01 Notes: Each metric of predation is composed of four dependent variables representing data from NONE, I, IR, and ALL exclosures in connected (Conn), rectangular (Rect), and winged (Wing) patches. If signi®cant, covariates describing micro- habitat in a 1-m radius around exclosures were included (e.g., woody debris). If signi®cant patch type effects were found, we conducted multivariate contrasts to compare patch types. would not change the signi®cance of our comparisons that any effect of each predator is additive (generally at ␣ϭ0.05. supported for IR and ALL treatments, see Results). We Corridors and overall seed predation.ÐWe use used backward selection to identify which variables MANCOVA to examine the net effect of all seed pred- were most related to the abundance of naturally re- ators on the number of germinants in 2000 and 2001, cruiting P. americana plants. seed removal, and viability. For these analyses, the Analyses were performed with SAS version 8.1 (SAS dependent variables were the values from NONE and Institute 2000). Germinant counts were square-root ALL treatments (analogous to Hotelling's T 2 test transformed and counts of P. americana plants were [Scheiner 2001]). Our model was otherwise the same log-transformed (Zar 1999). as used for examining predator-speci®c effects, in- cluding covariates. If signi®cant effects were found due RESULTS to patch type, we conducted planned pairwise contrasts to examine the predictions that distinguish the effects Corridors and seed predation by invertebrates, ro- of corridors (Table 1), as with our predator-speci®c dents, and birds.ÐCorridors did not affect the number models. If signi®cant differences were not found due of germinants in each exclosure type in 2000 or 2001 to patch type, we used paired t tests for each measure (Table 2). Corridors and patch type affected the number of seed predation to determine if overall predator ef- of seeds removed by each predator type, and downed fects were signi®cant. woody debris was a signi®cant covariate (Table 2, Fig. Seed predation and the distribution of P. ameri- 2). Examination of standardized canonical coef®cients cana.ÐWe used multiple regression to examine the re- suggests that more seeds were removed from treatment lationship between the abundance of naturally recruit- I (coef®cient ϭ 1.29) and fewer seeds were removed ing P. americana in our study system and our exper- from treatments IR and ALL as woody debris increased imental measures of seed predation (changes in ger- (coef®cients ϭϪ0.92 and Ϫ0.79, respectively). The minants, seeds remaining, and viability). As with the magnitude of the coef®cients indicates that treatments ANCOVAs, we used the difference between exclosure I and IR were most responsible for the signi®cance of treatments to partition the effects of each predator type. woody debris as a covariate (Scheiner 2001). The vi- For example, the reduction in seed number due to ro- ability of remaining seeds in each treatment did not dents was obtained by subtracting the number of seeds differ among patch types (Table 2), although leaf litter recovered from I treatments from the number of seeds was a signi®cant covariate in the analysis. The signif- recovered from IR treatments. In this way, we gener- icance of leaf litter was mostly attributable to a positive ated nine variables, representing the change in ger- relationship between leaf litter and viability in treat- minants in 2000, seed removal, and viability due to ments I and ALL (coef®cients ϭ 1.06 and 1.37, re- invertebrates, rodents, and birds. Because the calcu- spectively) rather than a weaker negative relationship lations for rodent and bird effects include more than between viability and leaf litter in treatment IR (co- one predator type, the rodent and bird estimates assume ef®cient ϭϪ0.83). 2594 JOHN L. ORROCK ET AL. Ecology, Vol. 84, No. 10

There were signi®cant multivariate differences in seed removal between connected and rectangular patches, between winged and rectangular patches, but not between winged and connected patches (Table 2, Fig. 2). Univariate ANCOVA on the difference be- tween treatments NONE and I found no signi®cant dif-

ferences due to patch type (F2,15 ϭ 1.52, P ϭ 0.25; Fig. 2b). The difference between NONE and I treatments was signi®cantly different from zero in winged (t ϭ 3.04, df ϭ 15, P Ͻ 0.01) and rectangular (t ϭ 3.25, df ϭ 15, P Ͻ 0.01) patches (Fig. 2a). In winged and rect- angular patches, invertebrates removed 29% and 45% more seeds relative to NONE treatments, but inverte- brates did not remove a signi®cant number of seeds in connected patches (t ϭ 1.38, df ϭ 15, P ϭ 0.19). Uni- variate ANCOVA on the difference between treatments I and IR found signi®cant effects due to patch type

(F2,15 ϭ 8.59, P Ͻ 0.01; Fig. 2b). In rectangular patches, 36% more seeds were removed from treatment I rela- tive to treatment IR (t ϭϪ2.38, df ϭ 15, P ϭ 0.01), suggesting that seed predation by invertebrates increas- es with area, speci®cally as the amount of area relative to perimeter increases (Table 1). In connected patches, rodents and invertebrates removed 33% more seeds than invertebrates alone (t ϭ 3.72, df ϭ 15, P Ͻ 0.01), suggesting that rodents are responding to corridor ef- FIG. 2. Seed removal from exclosure treatments located in connected (Conn), rectangular (Rect), and winged (Wing) fects (Table 1). Rodents and invertebrates did not re- patches. (a) Mean number of P. americana seeds remaining move more seeds than invertebrates alone in winged (and 95% con®dence intervals) in treatments exposed to no patches (t ϭ 1.50, df ϭ 15, P ϭ 0.15). Regardless of seed predators (NONE), invertebrates only (I), invertebrates patch type, allowing birds access to seeds did not result and rodents (IR), and invertebrates, rodents, and birds (ALL). (b) The effect of adding a particular predator type, as re¯ected in a signi®cant increase in seed removal, i.e., the dif- by the mean difference between exclosure treatments that ference between treatments IR and ALL did not differ differ by only one predator type. due to patch type (F2,15 ϭ 0.09, P ϭ 0.91; Fig. 2b), and was not different from zero (t Ͻ 0.25, df ϭ 15, P Ͼ 0.81 for all patch types). However, rodents, birds, and invertebrates (ALL) combined to remove signi®cantly more seeds than invertebrates alone in winged patches (paired t test, t ϭ 2.52, df ϭ 11, P ϭ 0.03; Fig. 2a).

TABLE 3. Effect of patch type (connected, rectangular, winged) and experimental unit (EU) on three different metrics of seed predation.

Metric of predation Factor Pillai's trace F df P Field germination 2000 patch type 0.06 0.23 4, 32 0.91 EU 0.80 1.52 14, 32 0.16 patch type ϫ EU 0.89 0.91 28, 32 0.59 Field germination 2001 patch type 0.13 0.57 4, 32 0.69 EU 0.67 1.15 14, 32 0.34 patch type ϫ EU 0.92 0.98 28, 32 0.52 Number of seeds remaining patch type 0.21 0.89 4, 30 0.48 EU 0.82 1.50 14, 30 0.17 patch type ϫ EU 2.18 1.04 28, 30 0.41 woody debris 0.05 0.35 2, 14 0.71 Viability of remaining seeds patch type 0.28 1.51 4, 30 0.33 EU 0.84 1.55 14, 30 0.15 patch type ϫ EU 1.16 1.47 28, 30 0.15 leaf litter 0.44 5.44 2, 14 0.02 Notes: Each metric of predation is composed of two dependent variables representing data from NONE and ALL exclosures collected in connected (Conn), rectangular (Rect), and winged (Wing) patches. If signi®cant in the previous MANCOVA model, covariates describing microhabitat in a 1-m radius around exclosures were included (e.g., woody debris). October 2003 CORRIDORS AND SEED PREDATION 2595

duced the number and viability of remaining seeds, and reduced the number of ®eld germinants in 2000 (t ϭ 2.33, df ϭ 39, P ϭ 0.03; Fig. 3a), but not the number of ®eld germinants in 2001 (t ϭ 0.13, df ϭ 39, P ϭ 0.89; Fig. 3a). Averaged across all patch types, seed predators removed 49% of the available P. americana seeds (t ϭ 8.00, df ϭ 39, P Ͻ 0.001; Fig. 3b), and remaining seeds were only 36% as viable as seeds from NONE treatments not available to predators (t ϭ 5.46, df ϭ 39, P Ͻ 0.001; Fig. 3c). Seed predation and the distribution of P. ameri- cana.ÐThe number of P. americana plants was neg- atively related to seed removal by invertebrates, ro- dents, and birds (Table 4). Changes in viability and the number of germinants in 2000 were not retained in the ®nal model. Standardized partial regression coef®- cients suggest that seed removal by rodents was most related to reduced abundance of naturally recruiting Phytolacca americana, followed by seed removal by invertebrates and seed removal by birds (Table 4). Col- linearity did not affect the selection or interpretation of the ®nal model, as the largest condition index value was 4.31, below the value of 30 indicative of collin- earity (Hair et al. 1998).

DISCUSSION Corridors altered large-scale predator±prey interac-

FIG. 3. Mean effects (and 95% con®dence intervals) of tions in a manner most consistent with area effects, and seed predators across all patch types as measured by exclosure perhaps corridor effects (for rodents), rather than drift- treatments allowing access by no seed predators (NONE) or fence effects. However, there was no net effect over access by invertebrate, rodent, and bird seed predators (ALL). the entire landscape because the effects of corridors on Effects of seed predators are measured using (a) the number of P. americana seeds germinating in the ®eld in 2000 and predator taxa were antagonistic: when corridors led to 2001, (b) the number of P. americana seeds remaining in increased rodent seed predation, this was accompanied experimental exclosures, and (c) the proportion of remaining by reduced invertebrate seed predation, and vice versa P. americana seeds that were viable. (Table 3, Fig. 2). We suspect that there was no net corridor effect on prey (seeds) because P. americana Corridors and overall seed predation.ÐAlthough seeds are readily consumed by both (Hyatt corridors affected predator-speci®c seed removal, cor- 1998) and mammals (McDonnell et al. 1984, Hyatt ridors did not change the overall impact of seed pred- 1998). Overall seed removal from exclosures and the ators on P. americana: there was no effect of patch abundance of naturally occurring P. americana plants type on overall seed predation (Table 3, Fig. 2). Re- in the same patch were negatively correlated, suggest- gardless of patch type, seed predation signi®cantly re- ing that seed predators may affect the distribution of

TABLE 4. Relationship between the total number of P. americana plants (after log transfor- mation) found in each patch and seed predation in each of 40 patches.

Partial correlation Source df MS coef®cient FR2 P Model 3 12.93 8.22 0.41 Ͻ0.001 Invertebrate seed removal 1 20.18 Ϫ0.54 12.83 0.26 Ͻ0.001 Rodent seed removal 1 35.44 Ϫ0.79 22.53 0.38 Ͻ0.001 Bird seed removal 1 15.76 Ϫ0.48 10.02 0.22 0.003 Error 36 1.57 Notes: Independent variables for each predator type were derived by subtracting treatments with the predator from treatments without the predator. Values of F and R2 for individual predator effects are partial values that describe the effects of each predator while accounting for all others in the model. Adjusted R2 for the entire model was 0.36. 2596 JOHN L. ORROCK ET AL. Ecology, Vol. 84, No. 10

P. americana in the landscape by reducing the number Dark-eyed Juncos (Junco hymenalis), Chipping Spar- of available seeds (Table 4). rows (Spizella passerina), White-throated Sparrows Corridors and seed predation by invertebrates, ro- (Zonotrichia albicolis), Northern Cardinals (Cardinalis dents, and birds.ÐCorridors did not in¯uence the num- cardinalis), and Eastern Towhees (Pipilo erythro- ber of P. americana germinants or the viability of re- phthalmus) (P. Champlin, personal communication). maining seeds, but corridors did affect patterns of seed We suspect that seed predation by avian granivores did removal (Tables 2 and 3, Fig. 2). Moreover, seed re- not exhibit a corridor effect in our study due to the moval and viability were signi®cantly related to the scale of our experimental patches. Avian granivores amount of woody debris and leaf litter within a 1-m forage over relatively large areas, concentrating on radius, emphasizing the importance of local microhab- high-density patches of seeds (Thompson et al. 1991). itat characteristics in affecting seed risk (Reader and As such, although birds contributed to the removal of Beisner 1991, Hulme 1997, Manson and Stiles 1998). seeds (Fig. 2), the small scale of our experimental Patterns of seed removal by invertebrates were con- patches relative to the scale of foraging by avian gran- sistent with the hypothesis that invertebrate seed pred- ivores probably precluded any corridor effects on avian ators avoid edges and are affected by corridors pri- seed removal. Moreover, the nested design of our ex- marily as area effects (Tables 1 and 2, Fig. 2). The closure treatments may have made corridor effects shape of rectangular patches yields the most amount more dif®cult to detect for avian granivores because of core habitat relative to the amount of edge habitat, rodents and ants also had access to ALL treatments that even though overall area is nearly equal among rect- allowed bird access. If rodents and invertebrates com- angular, connected, and winged patches (see Methods, pensate for corridor-mediated changes in avian seed Fig. 1). The increased core habitat in rectangular patch- predation, such changes may not be readily detected es may represent increased high-quality habitat for ear- by measuring the number of remaining seeds. However, ly successional invertebrate seed predators. For ex- the signi®cant partial correlation between bird seed re- ample, ®re ants (Solenopsis spp.) only establish in hab- moval from our experimental exclosures and the abun- itats where direct sunlight reaches the soil (Stiles and dance of naturally recruiting P. americana plants (Ta- Jones 1998). Moreover, colony growth, abundance, and ble 4) suggests that there was a detectable ``signal'' of foraging are positively related to soil temperature and avian foraging after accounting for seed losses to in- insolation (Porter and Tschinkel 1987, Porter 1988). vertebrates and rodents. Thus, although corridors may The occurrence and abundance of carabid beetles and be important short-term foraging conduits for frugiv- harvester ants (Pogonomyrmex spp.) also respond to orous birds (Tewksbury et al. 2002), corridors do not changes in temperature, edge, and core area (Didham appear to affect the impact of avian granivores on P. et al. 1998, Crist and Ahern 1999, MacMahon et al. americana seeds in the long term. 2000, Davies et al. 2001). Gonzalez et al. (1998) found Corridors and overall seed predation.ÐCorridors that corridors promote population rescue for moss- led to changes in the ef®cacy of invertebrate and rodent dwelling arthropods. Our data suggest that the distri- seed predators (Fig. 2), but corridors did not affect total bution of invertebrate seed predators may be limited seed predation when all predators had access to seeds more by habitat quality and availability than by the (Table 3, Fig. 2). Overall, seed predators signi®cantly ability of invertebrates to colonize a patch, and support reduced the number of P. americana germinants in the conclusion of Collinge (2000) that corridor effects 2000, reduced the number and viability of remaining per se may be weak or nonexistent for ground-dwelling seeds, but did not affect the number of germinants in invertebrates. 2001 (Fig. 3). Greater seed removal by rodents in connected and The similar levels of overall seed removal among winged patches may arise because corridors affect ro- patches contrast with predator-speci®c patterns caused dent movement and behavior. Old-®eld mice (Pero- by patch shape (Fig. 2), and suggest that compensation myscus polionotus) and cotton mice (P. gossypinus) occurs between seed predators, primarily rodents and were the primary rodent species in our experimental invertebrates, as has been noted in other studies (Brown patches (R. J. Brinkerhoff et al., unpublished manu- and Davidson 1977, Reichman 1979). Moreover, the script), and both consume a variety of seeds (Gentry difference between connected and rectangular patches and Smith 1968, Cothran et al. 1991). Corridors may provides evidence that patch shape may affect inter- increase patch residency time of female P. polionotus actions between seed predators. In rectangular patches, (Danielson and Hubbard 2000), and may also serve as invertebrates removed a signi®cant amount of seeds movement conduits for P. polionotus (Haddad et al. when they had exclusive access to seeds. When rodents 2003; R. J. Brinkerhoff et al., unpublished manuscript); were also allowed access, seed removal was no longer both effects could increase seed removal by P. polion- signi®cantly different from NONE treatments (Fig. 2a). otus in connected patches. This suggests that some reciprocal interaction was oc- We found no evidence that corridors affect avian curring, at least in rectangular patches. If invertebrates seed predation. The most common avian granivores in negatively affected rodents, but not vice versa, seed our system were Mourning Doves (Zenaida macroura), removal should have been equal in I and IR exclosures October 2003 CORRIDORS AND SEED PREDATION 2597 in rectangular patches, which it was not (Fig. 2a). Al- (Table 4). Rodent seed predators may have more in¯u- though we cannot be certain of the mechanism, the ence on P. americana than invertebrate seed predators potential for corridor-mediated interactions exists: in- because rodents detect and exhume buried seeds vertebrates can alter rodent foraging (Holtcamp et al. (Reichman 1979, Abramsky 1983). Because avian seed 1997) and can occur between ro- predators forage across large scales and target high- dents and invertebrates (Gentry and Smith 1968, Dan- density seed patches, their impact may be to reduce ielson and Hubbard 2000). Although additional studies spatial variation in seed density rather than dramati- are required to determine if corridors affect cally reduce total seed density (Thompson et al. 1991). in time and space, our data provide evidence that there Moreover, each experimental unit may receive a frac- may be little truly ``predator-free'' space from the per- tion of foraging by avian granivores compared to in- spective of Phytolacca americana. vertebrate and rodent granivores because the latter for- Why were signi®cant reductions in viability and the age almost exclusively within each experimental unit. number of seeds re¯ected in the number of germinants Although avian seed predators generally removed few- in 2000 but not 2001? Several mechanisms may be at er seeds than rodents and invertebrates (Fig. 2), the work. First, we may have failed to detect germinants signi®cant relationship between seed removal by birds that were lost to desiccation or herbivory between our and the abundance of naturally occurring P. americana sampling sessions. However, the lack of evidence of (Table 4) suggests that avian granivores may still have herbivory in the ®eld (e.g., clipped seedlings) and the important effects on P. americana . consistency of germination among all treatment types Corridors, predators, and prey.ÐCorridors may (Table 2, Fig. 3) do not support this explanation. Sec- have several bene®cial effects that make them ame- ond, P. americana germination may have been affected nable to conservation (Rosenberg et al, 1997, Haddad by precipitation differences between 2000 and 2001. 1999, Tewksbury et al. 2002). However, our results However, this explanation is not supported by ®eld demonstrate that corridors also affect multiple species data, as there was no signi®cant difference in precip- in different ways within a given . Gener- itation during the study in 2000 and 2001 (t test, t ϭ ally, our results suggest that corridors are most likely 0.72, df ϭ 233, P ϭ 0.48). Third, P. americana seed- to alter predator±prey interactions when predators dif- lings may exhibit density-dependent germination in- fer greatly in their response to corridors and in their hibition via allelopathy, as extracts from mature P. impacts on prey. For example, seeds that are consumed americana are known to inhibit germination (Edwards only by a particular predator type would be more likely et al. 1988), and seedlings may become microsite lim- to exhibit a net effect due to corridors. Hence, large- ited when many emerge during pulses of germination seeded, early successional species, such as Prunus spp., (Maron and Simms 1997). Although we removed ger- that are primarily consumed by rodents (Whelan et al. minants as soon as we found them, our rate of removal 1991), may bene®t from lower predation in rectangular may not have been suf®cient to avoid germination in- patches, whereas the converse may be true for seeds hibition of remaining seeds. Because P. americana ger- primarily consumed by invertebrates. Moreover, by me- mination is expected to be greatest during the spring diating interactions among seed predators, corridors (Baskin and Baskin 2001), density-dependent allelo- could differentially affect seed banks in fragmented pathic effects would be most likely to occur during the landscapes and thus shape the resulting plant com- spring phase of our study (i.e., in 2001), in agreement munity. with the greater number of germinants we observed ACKNOWLEDGMENTS from March to July 2001 compared to June±September 2000 (see Methods, Fig. 3a). This study was made possible by J. Blake, E. Olson, and other members of the USDA Forest Service Savannah River, Seed predation and the distribution of P. ameri- who were instrumental in the construction of the experimental cana.ÐWe observed a signi®cant negative relationship landscape. We thank N. Haddad for leadership in establishing between the abundance of naturally recruiting P. amer- the experimental patches. We are indebted to A. Weldon for icana and seed removal from our experimental exclo- help with data collection. We also thank E. Damschen and the poke posse: D. Kue¯er, E. Koenig, and J. Mayer, for sures. It is possible that the relationship between the tireless help with collecting, sifting, and counting seeds. P. number of seeds remaining and the number of naturally Townsend, J. Tewksbury, C. Brooks, J. Brinkerhoff, and D. recruiting P. americana is spurious, because we sur- Corbett also provided ®eld assistance. T. Ciravolo and K. veyed plants in 2000, but collected seed-removal and McLeod at the Savannah River Ecology Lab kindly provided viability data in 2001. However, the strength of the the growth chamber and logistical support. D. Catlett pro- vided critical materials and advice on exclosure construction. relationship between seed removal and naturally re- The manuscript was improved by comments from T. J. Ben- cruiting plants was strong, as seed removal explained son, R. J. Brinkerhoff, D. Coyle, E. Damschen, N. Haddad, 41% of the variance in P. americana abundance (Table C. Kwit, J. Tewksbury, and A. Weldon. Funding and support 4). were provided by the Department of Energy-Savannah River Operations of®ce through the U.S. Forest Service Savannah Although seed removal by rodents was most related River under Interagency Agreement DE-IA09-00SR22188. to the overall abundance of P. americana plants, re- Funding was also provided by an NSF Research Experience moval by invertebrates and birds was also important for Undergraduates Grant to B. J. Danielson and M. J. Burns, 2598 JOHN L. ORROCK ET AL. Ecology, Vol. 84, No. 10 an NSF Grant to B. J. Danielson (DEB-9907365) and D. J. pokeweed (Phytolacca americana) I. Laboratory tech- Levey (DEB-9815834), and a Grant-in-Aid of Research to J. niques and autotoxicity. American Journal of Botany 75: L. Orrock from the American Society of Mammalogists. 1794±1802. Farmer, R. E., Jr., and G. C. Hall. 1970. 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