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Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web.

INTRODUCTION

How do changes in the productivity of lower trophic levels affect populations at higher levels in a food web? This question is central to the ongoing controversy over how processes that determine population density are distributed across trophic levels in different types of ecosystems (Hairston el al. 1960, Strong 1992, Hairston and Hairston 1993, 1997, Polis and Strong 1996, Polis and Winemiller 1996). A major point of disagreement is whether resource limitation (bottom-up processes) predominate at all trophic levels, or whether top-down processes (limitation of populations by predation) and bottom-up forces alternate in relative strength from one trophic level to the next. The relative contribution of these opposing processes across different trophic levels, and differences in the pattern between ecosystems, likely depend upon numerous factors, e.g., body size, physiology, and foraging modes of primary and higher-order consumers; physical structure of the habitat; abiotic factors; the prevalence of intraguild predation (IGP) and trophic-level omnivory; and whether or not the system is a grazing or detrital food web, or encompasses both (Abrams 1996, Persson et al. 1996).

A major reason for the continuing controversy is not fundamental disagreement over possible mechanisms, but the absence of adequate numbers of experimental studies with a diversity of food webs. Experimentation has been most extensive with grazing webs in aquatic ecosystems, in which enhanced rates of primary production can lead to increased numerical and biomass densities of aquatic herbivores and their predators (Hall et al. 1970, Neill and Peacock 1980, Crowder et al. 1988, Menge and Olson 1990, Ginzburg and Akcakaya 1992, Osenberg and Mittlebach 1996). Although fewer in number, experiments with terrestrial grazing webs have uncovered similar propagating effects of enhanced primary productivity (Hurd et al. 1971, Hurd and Wolf 1974, Vince et al. 1981, Schmitz 1993, 1994). However, not all experiments have yielded a positive response by predators. Long-term fertilization of a Polish meadow increased primary production but failed to elevate the overall density or biomass of spiders, a major arthropod predator in such systems (Kajak 1981). Fertilization of fescue turf led to an increase in staphylinid beetles, but not other major arthropod predators in the system (ants, spiders, and carabid beetles) (Davidson and Potter 1985).

A few resource enhancement experiments have been performed with aquatic and terrestrial detrital food webs (Seastedt et al. 1988, Schaefer 1991, Warren and Spencer 1996, Scheu and Schaefer 1998). In terrestrial ecosystems, a substantial fraction of net primary production enters the decomposition subsystem. In forests, up to 90% of above-ground net primary production may enter primarily detritus-based food webs (Edwards et al. 1970, Crossley 1977, Swift et al. 1979, Peterson and Luxton 1982, Coleman et al. 1983). Thus, processes within the forest floor community are intimately involved with energy flow and nutrient cycling within forest ecosystems.

Although sharing some species with the food web of the underlying soil layers, the leaf litter community is a relatively distinct subsystem (Heal and Dighton 1986). Dead plant materials form the primary energy base of the leaf litter food web. Fungi and bacteria, which as primary decomposers release the majority of energy locked in detritus, are sufficiently specialized to form distinct fungal and bacterial food channels within the entire decomposition food web (Moore and Hunt 1988). The most abundant detritivorous arthropods (i.e., Collembola, many Diptera, and the majority of mites) are primarily fungivorous, because they derive the majority of their energy from fungi associated with detritus (Schaefer 1991, Chen et al. 1996). These arthropod fungivores (for the sake of simplicity, all arthropods that ingest detritus and/or graze fungal mycelia will be referred to as "fungivores") are preyed upon by a wide range of arthropod predators, such as mires, beetles, ants, pseudoscorpions, centipedes, and spiders (Swift et al. 1979). The litter community is well suited for experimental enhancement of the resource base, because its degree of separation from grazing food webs and the large number of trophic interactions within a small area make feasible the creation of replicated, clearly demarcated community units for experimentation.

A previous experiment demonstrated increases in densities of Collembola (springtails), Diptera (primarily fungus gnats), and Acarina (primarily oribatid mites) in response to experimental enhancement of detritus in the litter layer (Chen and Wise 1997). In this earlier study, the resource base was enhanced for 10 wk in 1-[m.sup.2] plots. In order to examine the responses of predators, we (1) expanded our earlier design by making plots 10x larger, in order to include a reasonable number of the larger predators and to reduce edge effects; and (2) increased the duration of the experiment to 15 wk in order to allow more time for predator populations to respond to increased fungivore densities.

Predator responses were categorized by major taxonomic categories (order or family, depending upon the group), with one exception. Among the spiders (Araneae) we selected the wolf spider Schizocosa (Lycosidae) to examine in more detail. Spiders of the genus Schizocosa are abundant in deciduous forests of eastern North America (Stratton 1991, Wise and Wagner 1992, Martinat et al. 1993). We focused on Schizocosa because other experiments have examined the extent to which top-down forces limit its density (Wagner and Wise 1996, 1997; Wise and Chen, in press; D. H. Wise and B. Chen, unpublished data).

METHODS

The experiment was conducted in Madison County, Kentucky, USA, in an oak-maple forest with a few scattered pine trees (Chen and Wise 1997). Twenty 2 x 5 [m.sup.2] open plots on the forest floor, a minimum of 20 m apart, were randomly assigned to either a Food Enhancement or Control treatment (10 replicates/treatment). Starting 17 June 1995, the resource base was enhanced by adding, at 10- or 14-d intervals through 18 September, 1100 g (fresh mass) chopped commercial mushrooms, 1000 g (fresh mass) chopped potatoes, and 200 g dry, instant Drosophila medium (Formula 4-24, Carolina Biological Supply; Burlington, North Carolina, USA) to each Food Enhancement plot. This combination of nutrients and rate of supplementation ([approximately]20 g/[m.sup.2][multiplied by]d) was chosen because a similar food supplementation increased densities of fungivores within 4 wk in the same forest (Chen and Wise 1997). The added resource was distributed evenly over the surface of the litter.

Over the 3.5 mo of the experiment, each Food Enhancement plot received a total of 446 g/[m.sup.2] dry mass of additional detritus (66 g/[m.sup.2] of mushrooms, 200 g/[m.sup.2] of potatoes, and 180 g/[m.sup.2] of dry, instant Drosophila medium [moisture contents of fresh mushrooms and potatoes were 93.5 [+ or -] 0.6% and 78.4 [+ or -] 1.2%, respectively]). This amount of added detritus approximated the average standing crop (dry mass) of natural litter in the Control plots during the experiment. The majority of this added organic material disappeared, judging by what was visible on the forest floor during the experiment, as well as by the relatively small differences in the mass of all detritus (natural litter plus added resources) in the Food Enhancement plots and natural litter in the Control treatment. After 6 wk, the total amount of detritus in Food Enhancement and Control plots did not differ significantly, and by the end of experiment, the standing crop of detritus in the Food Enhancement treatment was only 30% higher than in the Control plots [ILLUSTRATION FOR FIGURE 1 OMITTED].

Densities of fungivores and predators were determined three times during the experiment: (1) just prior to starting the resource enhancement, in order to determine initial densities of fungivores and predators; (2) after 6 wk, when changes in growth, reproduction and foraging behavior of many fungivores and predators were predicted to have been detectable (approximate midpoint of the experiment); and (3) after 15 wk (end of the experiment). The experiment terminated in early October, just before the start of litter fall and before cooler temperatures prevented accurate censusing of the larger predators by litter sifting. Three different sampling techniques were used.

Sticky traps

The relative abundance of flying insects (Diptera and Hymenoptera) active immediately above the litter layer was determined with vertically oriented 10 x 10 cm pieces of metal insect screening coated on both sides with a tree-banding compound (Tanglefoot Company, Grand Rapids, Michigan, USA). Two sticky traps, set perpendicular to each other 2 m apart along the plot's long axis, were placed in the middle of each plot for 24 h. Traps were set 14 June, 27 July, and 2 October.

Litter extraction

Two 0.05-[m.sup.2] samples of litter (upper and fragmented layers, not including the humus) from each plot were placed for 7 d in a temperature-humidity extraction apparatus (Kempson et al. 1963, Schauermann 1982). Animals were first extracted into 50% ethylene glycol, then washed in 95% EtOH, and finally stored in 80% EtOH for later identification and counting. After the animals had been extracted, the litter samples were oven-dried at 60 [degrees] C for 3 d and then weighed. Litter samples were taken 13 June, 27 July, and 2 October.

Litter sifting

For larger spiders, estimating population density by litter extraction is not as accurate as sifting and searching the litter in the field. Densities of spider species whose adult carapace length was [greater than]1.1 mm were estimated by sifting and searching through three 0.2-[m.sup.2] litter samples per plot on 15 June and 14 August, and two samples per plot on the last census, 28 September. For the premanipulation census, spiders were identified to family, and their carapace length was measured in the field. On subsequent censuses the spiders were brought back to the laboratory, where their carapace length was measured and they were weighed to the nearest 0.01 mg, in order to estimate spider biomass density (mg/[m.sup.2]). After being measured, spiders were returned to their plots. Spiders were identified to family level, except that juvenile stages of the wolf spider Schizocosa (Lycosidae) were also analyzed separately.

The two Schizocosa species in our field site, S. ocreata (Hentz) and S. stridulans (Stratton), can be distinguished morphologically only on the basis of traits of mature males (Stratton 1991). We will refer to these two species simply as Schizocosa. This wolf spider has an annual life cycle. Egg sacs are produced in June and early to mid-July, and spiderlings disperse in midsummer. By mid-August most Schizocosa in our study site are recently dispersed spiderlings, with very few adult females ([less than]2% of the population).

Statistical analyses and data presentation

Effects of food supplementation on density were analyzed by ANCOVA of the mean value of density on the two postmanipulation sampling dates, with initial density of the response variable as a covariate. When necessary, data were log-transformed to make variances homogenous. Taxa were grouped for analysis according to whether or not they were fungivorous, mixed (fungivorous, omnivorous, and predaceous species), or strictly predaceous. Because numerous response variables were compared between Food Enhancement and Control treatments, the sequential Bonferroni procedure (Dunn-Sidak method, Sokal and Rohlf 1995) was used to control the table-wide Type I error rate when examining responses of taxa sampled by a particular method within each of the three feeding groups, or when examining taxa within a larger taxon (i.e., families within the Collembola, or the major families of Araneae).

In order to determine if the magnitude of the treatment effect varied over time, we examined the treatment x date interaction in a repeated-measures univariate ANOVA, with initial density as a covariate (rm-ANCOVA; with only two postmanipulation sampling dates, it is not possible to perform a rm-multivariate ANOVA in order to test for a change in treatment response over time). If the treatment x date interaction was significant, the treatment effect was tested for each date separately to clarify the pattern of the interaction.

Statistically significant responses to resource enhancement are first summarized as the average increase, which is calculated as the mean density for the two postmanipulation censuses in the Food Enhancement plots divided by the corresponding mean density in the Control treatment. If the treatment x date interaction is not statistically significant, the statistical significance of the treatment effect is indicated in the table or figure as a single, Bonferroni-adjusted value. If the interaction term is significant, separate Bonferroni-adjusted probabilities for the Food Enhancement vs. Control comparison are given for each date. ANOVA tables are not presented, because most ANOVAs have the same structure: df for covariate (initial density), treatment, date, treatment x date interaction, and error are 1, 1, 1, 1, and 15, respectively. Error df = 16 for ANOVAs of biomass density, which do not incorporate a covariate, because masses were not measured in the pretreatment sampling. All statistical tests are two-tailed, because, in multitrophic systems, negative responses to resource enhancement are possible (Abrams 1993). Data were analyzed by SAS programs (SAS Institute 1990). All values in figures and tables are mean [+ or -] 1 SE.

RESULTS

Densities of all the major groups of arthropod fungivores and predators increased in response to the increased rate of input of detritus, with most groups exhibiting at least a doubling of numbers in the Food Enhancement plots compared to the Control treatment. The results are presented separately by feeding category and sampling method.

Fungivores

Sticky traps. - Diptera represented 66% of the flying insects trapped in the Control plots. Total numbers of Diptera were 2.2x higher in the Food Enhancement plots [ILLUSTRATION FOR FIGURE 2A OMITTED]. The most numerous group, the fungus gnats (Sciaridae and Mycetophilidae), was not significantly elevated after 6 wk, but was 2.7x more abundant in the Food Enhancement plots by the end of the experiment [ILLUSTRATION FOR FIGURE 2B OMITTED].

Litter extraction. - Springtails (Collembola) accounted for 35% of the arthropods extracted from Control litter samples. Total Collembola abundance averaged 3.0x higher in the Food Enhancement treatment [ILLUSTRATION FOR FIGURE 3 OMITTED]. Except for the Neelidae, each family of Collembola, including subfamilies of Entomobryidae, were all significantly higher in the Food Enhancement plots (Table 1). Mites represented 58% of the arthropods extracted from litter but are discussed in the next section because they include predaceous species. Most other groups of fungivores each accounted for [less than]1% of the total number in the samples.

Mixed groups (fungivores, omnivores, and predators)

Sticky traps. - Hymenoptera accounted for 26% of the flying arthropods caught by sticky traps. Numbers were 2.0x higher in the experimental plots on both postmanipulation censuses (P [less than] 0.01).

Litter extraction. - Mite (Acarina) density doubled in Food Enhancement plots compared to Controls (Table 2). Adult and larval beetles (Coleoptera: Carabidae and Staphylinidae) were several times more abundant in the Food Enhancement treatment, as were densities of Hymenoptera (primarily ants [Formicidae]; Table 2).

Predators

Litter extraction. - Three strictly predaceous groups (the centipedes [Chilopoda], pseudoscorpions [Arachnida: Pseudoscorpionida], and spiders [Arachnida: Araneae]) were nearly twice as abundant in the plots receiving additional detritus (2.0x, 1.7x, and 1.9x, respectively; [ILLUSTRATION FOR FIGURE 4 OMITTED]).

Spiders from 12 families were extracted from the litter samples, but most individuals ([greater than]80%) were from four families. Most spiders in the litter extraction samples were small; either they were juveniles, or they were adults of species with adult carapace length [less than]1.1 mm. The two most abundant spiders were web builders in the families Linyphiidae and Dictynidae, representing 35% and 32% of the total spider catch from Control plots, respectively. Both groups were significantly more abundant in the Food Enhancement plots (2.3x [P [less than] 0.01] and 1.6x [P [less than] 0.05], respectively). The next most abundant species were cursorial spiders in the families Clubionidae and Gnaphosidae, representing 9% and 7% of the total spider catch from Control plots, respectively. Both groups displayed elevated densities, but neither response was statistically significant at the P = 0.05 level.

Litter sifting. - Collecting spiders in sifted, 0.2-[m.sup.2] litter samples revealed that the numerical abundance and biomass density of spiders in the Food Enhancement plots were approximately twice Control values (1.7x and 2.0x, respectively; [ILLUSTRATION FOR FIGURE 5 OMITTED]). Sifting and searching litter samples in the field also yielded 12 spider families, but relative abundances were much different than those determined from extracting spiders in the laboratory from the smaller 0.05-[m.sup.2] samples. The four most abundant spider families in the field-searched samples were the cursorial Gnaphosidae, Lycosidae, and Clubionidae; and the web-building Amaurobiidae, respectively representing 22%, 21%, 18%, and 15% of the spiders found in the Control samples.

Three of the four most abundant families displayed a response to the resource enhancement. The web-building amaurobiids were 2.2x as abundant in the experimental plots (P [less than] 0.01). Densities of the cursorial clubionids were not elevated significantly (P = 0.56), but two other cursorial families, the Gnaphosidae and Lycosidae, both responded to food enhancement. Gnaphosids were twice as abundant, and lycosids were 1.8x as numerous in the Food Enhancement plots as in the Control treatment (P [less than] 0.01 and P [less than] 0.05, respectively).

The wolf spider Schizocosa. - Most lycosids ([greater than]90%) in the litter-sifting samples were Schizocosa. All Schizocosa from the pretreatment sample in June were adults, but in the posttreatment censuses almost all were recently dispersed spiderlings or early-instar juveniles (only 3 out of 216 were adults). Biomass density of Schizocosa responded strongly to an increase in the resource base: total biomass averaged 3.4x higher in Food Enhancement than Control plots [ILLUSTRATION FOR FIGURE 6A OMITTED]. The biomass response of Schizocosa apparently resulted from changes in both numerical density and individual spider size. Schizocosa numerical density was marginally higher (1.7x) in the Food Enhancement plots on both posttreatment censuses ([ILLUSTRATION FOR FIGURE 6B OMITTED]; unadjusted P = 0.031, P [approximately equal to] 0.09 after the Bonferroni adjustment). The magnitude of the effect of resource enhancement on Schizocosa biomass density grew over time, increasing from 2.2x greater than Control values on 14 August to 4.7x larger on 28 September [ILLUSTRATION FOR FIGURE 6A OMITTED]. The increasing effect of food enhancement on Schizocosa biomass density clearly paralleled the changing influence of the food manipulation on individual spider mass [ILLUSTRATION FOR FIGURE 6C OMITTED].

DISCUSSION

Our experiment revealed substantial bottom-up effects propagating through a major terrestrial decomposition food web. Experimentally enhancing the food base elevated populations of arthropod fungivores, which reduced food limitation of the arthropod predators and caused their densities to increase. All trophic levels of the arthropod food web displayed marked and relatively rapid positive responses to enhancement of the resource base. In this system high degrees of intraguild [TABULAR DATA FOR TABLE 1 OMITTED] predation (IGP) and trophic-level omnivory likely occur, leading one to predict that indirect effects eventually would alter the pattern of responses over time, until new equilibria have been attained (Bender et al. 1984, Yodzis 1988, 1996). Osenberg and Mittelbach (1996) define the change in equilibrium level that results from the net impact of direct and indirect effects acting over periods longer than a generation to be a measure of bottom-up control. They define the degree of resource limitation to be the magnitude of the short-term, within-generation response to a resource perturbation. Our experiment has demonstrated significant bottom-up limitation of predaceous arthropods in the leaf litter food web; establishing the actual degree of bottom-up control would require a perturbation experiment lasting several years.

The fungivore response

Enhancing the resource base slowed the decline in Collembola numbers that occurred from June through early October in the Control plots. Our previous experiment, which was conducted from April through mid-June in the same forest, found that supplementing the food base increased rates of reproduction and/or juvenile survival of Entomobryidae and decreased the [TABULAR DATA FOR TABLE 2 OMITTED] activity of most springtail families. Thus, it is reasonable to conclude that, in our current experiment, adding high-quality detritus directly enhanced Collembola fecundity, and/or survival, and possibly reduced rates of emigration. In addition, lowered activity rates could have indirectly improved Collembola survival by lessening their exposure to predators, an interaction that would tend to weaken the response of the predator trophic level to resource enhancement. The pattern of relative change of fungus gnat numbers repeated that of the earlier experiment (Chen and Wise 1997): numbers were not different in Food Enhancement and Control plots after a month of food supplementation, but had significantly increased by the end of the study. Apparently the major component of the response by fungus gnats is not attraction of adults to the added food, but higher rates of egg laying and/or larval survival in plots with an enhanced resource base (Chen and Wise 1997).

Possible mechanisms underlying the response of predators to increased densities of their prey

Because the plots were open, a reduced rate of emigration in the presence of higher fungivore densities is a likely component of the response of predators. This is particularly the case for the larger, more active species (cursorial spiders and centipedes). Experiments have shown that centipedes, wolf spiders and some web-building spiders switch to a less active foraging mode when prey are more abundant (Ford 1978, Olive 1982, Rypstra 1985, Rubenstein 1987, Formanowicz and Bradley 1987, Persons and Uetz 1996, Wagner and Wise 1997). Several studies have also demonstrated that a limited food supply limits growth and reproduction of cursorial and web-building spiders (Wise 1993). Collembola are a major prey in the diet of pseudoscorpions, centipedes, and wolf spiders (Edgar 1969, Weygoldt 1969, Lewis 1981). Field observations reveal that Collembola and Diptera constitute a major proportion of the diet of small, ground-dwelling web spiders (Nyffeler and Benz 1988). Spiders and centipedes also will prey on each other and will prey upon pseudoscorpions (Jones 1975, Lewis 1981; D. H. Wise and B. Chen, unpublished data). Thus, it is reasonable to hypothesize that increased growth and fecundity due to enhanced densities of fungivorous and other types of prey, and improved survival due to reduced cannibalism and IGP, also contributed to higher predator numbers and biomass densities in the Food Enhancement plots.

Most previous studies of food limitation in spiders have documented responses of individual spiders, usually web builders, to experimental supplementation of their diet in the field, or have compared growth rates in the field and laboratory (Wise 1993). Our experiment improves our quantitative understanding of the degree to which a limited food supply affects spider densities, across the entire range of spider foraging modes, in one community. What is striking about our results is the widespread, approximate doubling of density of the major spider groups in response to elevated densities of their natural prey species. Such a consistent, widespread response has not been demonstrated in previous experiments, which were not designed to uncover such patterns.

Responses of predators in other experiments that enhanced the detrital resource base of the leaf litter food web

All major groups of fungivores and predators responded positively to the resource enhancement. This result does not necessarily follow from theoretical arguments. Although some lines of reasoning lead to the conclusion that detrital food webs should exhibit strong donor control (Pimm 1982), examination of the complexity of possible trophic interactions leads to the prediction that either an increase, no change, or even a decrease in predators is a possible outcome to enhancement of the resource base of a detritus-based web (Abrams 1993, Persson et al. 1996).

Experiments with the leaf litter community mirror some of this complexity of response, though the variable pattern of results may primarily reflect the different approaches used to increase the resource base. One technique is to introduce additional leaf litter. This approach has produced no change in numbers of centipedes and a decrease in pseudoscorpions (David et al. 1991), an increase in centipedes (Poser 1990), and an increase in spider densities (Stippich 1987). The latter two studies were part of a single large-scale experiment (Schaefer 1991). Because treatments were not spatially replicated in these three studies, it is difficult to compare the strength and magnitude of responses with our results. In a replicated litter manipulation experiment, Uetz (1979) found an effect of litter depth on species diversity, but not spider numbers. Manipulating litter produces results that can be difficult to interpret strictly in terms of resource limitation, because changes in litter amount, depth, and structure can significantly affect densities of arthropods independently of changes in the rate of input of energy and nutrients (Uetz 1991).

In order to increase the resource base by increasing productivity of the microflora without altering litter structure or amount, Scheu and Schaefer (1998) added sources of carbon, nitrogen, or phosphorus. At the end of their experiment, the number of litter-dwelling centipedes was [approximately]2x higher in plots receiving supplemental N; centipedes showed no clear response to the other additions.

Because the resource that we added was finely chopped or consisted of dry flakes, it is unlikely that it substantially changed litter structure in a manner that would have directly affected predator behavior or density. Our manipulation procedure produced no noticeable increase in litter mass when applied for 10 wk earlier in the season (Chen and Wise 1997), and had produced no statistically significant increase after 6 wk in our current experiment. By 3.5 mo the litter amount was higher, but only by 30%.

Other experimental enhancements of the resource base of the leaf litter food web have not produced increases in predator densities as rapid or as consistently positive as we observed. Some differences in results likely reflect differences in duration and whether the plots were open or fenced. One major cause of variation in the magnitude and rapidity of system responses is the difference in resource quality between added leaves or elemental nutrients and the high-quality detritus we added. The dry mass of resource that we added was approximately equal to the dry mass of leaf litter on the forest floor, but the nutrient quality was undoubtedly higher, particularly because of the absence of structural materials such as lignin. In this respect, our manipulation was similar to that of Scheu and Schaefer (1998), but differed from theirs in that our technique provided a resource directly available to Collembola and other fungivores.

It should be emphasized that the primary goal of our experiment was to reveal the extent to which predators responded to increases in densities of their prey. Our addition of high-quality detritus was designed to increase fungivore numbers, but was not designed to test resource limitation of the microflora growing on the litter, like the experiment of Scheu and Schaefer. Because our manipulation did not substantially modify litter structure, our results are directly relevant to making inferences about the degree to which variations in factors affecting the productivity of the resource base of fungivores influence higher trophic levels.

Insights from effects on the wolf spider Schizocosa

Our experiment revealed strong bottom-up limitation of juvenile Schizocosa. Increasing the input of detritus to the system increased the biomass density of immature Schizocosa almost fivefold by the end of the experiment. Several mechanisms likely contributed to this response: (1) The fecundity of females may have increased in the Food Enhancement plots. Collembola numbers had doubled by the end of July, so it is possible that females producing egg sacs during July had higher fecundities in the experimental plots. (2) The survival of hatchlings and younger instars may have improved in the experimental plots due to reduced mortality from cannibalism at higher levels of Collembola, Diptera, and other prey (Wagner and Wise 1996, 1997). (3) Survival may have improved due to reduced mortality from IGP. This is a possibility, but may not be a major explanation, because other predators (centipedes, other spiders) were also more abundant in the Food Enhancement plots. (4) Emigration of Schizocosa may have decreased at higher prey densities. The presence of prey reduces the foraging activity and emigration rate of Schizocosa in laboratory experiments (Persons and Uetz 1996, Wagner and Wise 1997). (5) Growth rates may have increased at higher prey densities. The dramatic increase in Schizocosa mass in plots open to migration suggests strong food limitation. This result confirms previous conclusions that negative effects of Schizocosa density on growth rates in field experiments with fenced plots were due to exploitative competition for prey (Wise and Wagner 1992, Wagner and Wise 1996).

Other experiments have revealed top-down control of juvenile Schizocosa populations, but top-down effects are not as consistent as responses to changes in prey abundance. Reducing predation pressure from vertebrate predators for 1.3 yr had no impact on Schizocosa densities (Wise and Chen, in press). In contrast, arthropod IGP can exert significant mortality on juvenile Schizocosa, but the pattern is complex (Wagner and Wise 1996, 1997; D. H. Wise and B. Chen, unpublished data). Schizocosa mortality during the first 2 mo of life is high ([greater than]70%), yet experimentally reducing IGP does not significantly improve survival of the youngest instars, most likely because of increased mortality from cannibalism. In an experiment conducted in the same forest as the current study, reducing IGP improved Schizocosa survival by [approximately]70% during the second month of life in some, but not all, habitat patches (D. H. Wise and B. Chen, unpublished data). Mortality rates of older Schizocosa juveniles were positively correlated with densities of two families of cursorial spiders (Gnaphosidae and Ctenidae).

It might appear from this pattern of results that bottom-up forces exert stronger effects on Schizocosa populations than top-down processes. Such a conclusion, however, would be premature. Older juvenile stages and adult Schizocosa might exhibit different patterns, and, in addition, indirect effects involving other generalist predators could have a large impact on Schizocosa densities. Long-term experiments of several years are needed to determine whether the strong resource limitation shown by juvenile Schizocosa is expressed as consistent resource control, once new equilibria have been established at elevated rates of resource input. Furthermore, the most direct way to assess the relative strength of bottom-up and top-down control processes is to manipulate predation intensity and resource levels both singly and simultaneously (Schmitz 1993, 1994, Osenberg and Mittelbach 1996). Thus, long-term, multifactorial experiments should prove fruitful in assessing the relative strength of bottom-up and top-down forces affecting Schizocosa populations.

Comparison with variation in spider densities in another type of detritus-based system

Densities of spiders in coastal habitats can be strongly influenced by insect populations that breed in marine detritus that has washed ashore. Differences in spider numbers between islands in the Gulf of California can be attributed to differing rates of detrital input from the marine environment (Polis and Hurd 1995, 1996, Polis et al. 1998). On small islands, the relatively high input of allochthonous energy from the marine food web is correlated with densities of web-building spiders up to two orders of magnitude higher than on larger islands. Within an island, spider densities can be 6x higher along the shore than inland, due to enhanced prey populations from the marine detritus. In an experiment conducted on the mainland California coast, Spiller (1992) increased densities of an orb web spider. 3x by augmenting the amount of kelp that had washed up on the beach. In our experiment overall spider densities increased [approximately]2x, and Schizocosa biomass increased [approximately]5x, in response to enhanced input of detritus. Thus, the responses we observed in the leaf litter community are similar in magnitude to the variation in spider densities observed in marine coastal situations in which comparisons are made within a single landscape and not between isolated habitats of widely differing area.

It would be worthwhile to determine whether or not several-fold variation in densities of spiders and other predaceous arthropods within the leaf litter of a particular forest, or between different forest types, can be explained largely by differences in productivity of the detrital resource base. Continued experimentation with the leaf litter food web will help to answer this question and will furnish insights into the interplay between bottom-up and top-down control processes in terrestrial decomposition systems.

ACKNOWLEDGMENTS

We would like to thank Berea College for permission to use the study site. We thank Keith Erny, Jarrod True, Erica Wise, and Keith Day for field assistance; and James Wagner, Kendra Lawrence, Ricardo Bessin, Rolando Lopez, Anthony Joern, and two anonymous reviewers for helpful comments on the manuscript. This research was supported by NSF grant DEB-9306692 and USDA/KAES Hatch Project KY-00711 to D. H. Wise. This is publication #97-08-95 from the Kentucky Agricultural Experimental Station.

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Date:Apr 1, 1999
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