Introduced Browsing Mammals in New Zealand Natural Forests: Aboveground and Belowground Consequences

Ecological Monographs, 71(4), 2001, pp. 587±614 ᭧ 2001 by the Ecological Society of America

INTRODUCED BROWSING MAMMALS IN NEW ZEALAND NATURAL FORESTS: ABOVEGROUND AND BELOWGROUND CONSEQUENCES

DAVID A. WARDLE,1,5 GARY M. BARKER,2 GREGOR W. Y EATES,3 KAREN I. BONNER,1 AND ANWAR GHANI4 1Landcare Research, P.O. Box 69, Lincoln 8152, New Zealand 2Landcare Research, Private Bag 3127, Hamilton, New Zealand 3Landcare Research, Private Bag 11052, Palmerston North, New Zealand 4AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123, New Zealand

Abstract. Forest dwelling browsing mammals, notably feral goats and deer, have been introduced to New Zealand over the past 220 years; prior to this such mammals were absent from New Zealand. The New Zealand forested landscape, therefore, presents an almost unique opportunity to determine the impacts of introduction of an entire functional group of alien animals to a habitat from which that group was previously absent. We sampled 30 long-term fenced exclosure plots in indigenous forests throughout New Zealand to evaluate community- and ecosystem-level impacts of introduced browsing mammals, emphasizing the decomposer subsystem. Browsing mammals often signi®cantly altered plant community composition, reducing palatable broad-leaved species and promoting other less palatable types. Vegetation density in the browse layer was also usually reduced. Although there were some small but statistically signi®cant effects of browsing on some measures of soil quality across the 30 locations, there were no consistent effects on components of the soil microfood web (com- prising micro¯ora and nematodes, and spanning three consumer trophic levels); while there were clear multitrophic effects of browsing on this food web for several locations, comparable numbers of locations showed stimulation and inhibition of biomasses or populations of food web components. In contrast, all microarthropod and macrofaunal groups were consistently adversely affected by browsing, irrespective of trophic position. Across the 30 locations, the magnitude of response of the dominant soil biotic groups to browsing mammals (and hence their resistance to browsers) was not correlated with the magnitude of vegetation response to browsing but was often strongly related to a range of other variables, including macroclimatic, soil nutrient, and tree stand properties. There were often strong signi®cant effects of browsing mammals on species composition of the plant community, species composition of leaf litter in the litter layer, and composition of various litter-dwelling faunal groups. Across the 30 locations, the magnitude of browsing mammal effects on faunal community composition was often correlated with browser effects on litter layer leaf species composition but never with browser effects on plant community composition. Browsing mammals usually reduced browse layer plant diversity and often also altered habitat diversity in the litter layer and diversity of various soil faunal groups. Across the 30 locations, the magnitude of browser effects on diversity of only one faunal group, humus-dwelling nematodes, was correlated with browser effects on plant diversity. However, browser effects on diversity of diplopods and gastropods were correlated with browser effects on habitat diversity of the litter layer. Reasons for the lack of unidirectional relationships across locations between effects of browsers on vegetation community attributes and on soil invertebrate community attributes are discussed. Browsing mammals generally did not have strong effects on C mineralization but did signi®cantly in¯uence soil C and N storage on an areal basis for several locations. However the direction of these effects was idiosyncratic and presumably re¯ects different mechanisms by which browsers affect soil processes. While our study did not support hypotheses predicting consistent negative effects of browsing mammals on the decomposer subsystem through promotion of plant species with poorer litter quality, our results still show that the introduction of these mammals to New Zealand has caused far-ranging effects at both the community and ecosystem levels of resolution, with particularly adverse effects for indigenous plant communities and populations of most groups of litter-dwelling mesofauna and macrofauna. Key words: alien organisms; browsing; decomposer food web; deer; goats; herbivory; macrofauna; mesofauna; microbial biomass; microfauna; New Zealand forests; plant litter.

Manuscript received 6 June 2000; revised 22 February 2001; accepted 23 February 2001; ®nal version received 16 March 2001. 5 Present address: Department of Animal and Plant Sciences, University of Shef®eld, Shef®eld S10 2TN, UK. E-mail: d.wardle@shef®eld.ac.uk

587 588 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

INTRODUCTION 1998, Suominen 1999, Suominen et al. 1999) although Milchunas et al. (1998) concluded that these effects In terrestrial ecosystems, browsing by herbivores has tended to be small especially when compared with the important indirect effects on belowground properties effects of herbivores on composition of aboveground and processes, in particular the mineralization of soil biota such as plants and birds. C and N (Holland et al. 1992, Molvar et al. 1993, Pastor The in¯uence of herbivory on the diversity (includ- et al. 1993, Frank and Groffman 1998). Several mech- ing taxonomic richness) of consumer groups compris- anisms have been proposed to explain how herbivory ing the decomposer food web remains largely unex- affects soil processes and the organisms that govern plored. Herbivory often increases plant diversity these processes (Bardgett et al. 1998b), but three (Zeevalking and Fresco 1977, Collins et al. 1998), emerge as being consistently important. First, animals probably by reducing competitive exclusion (Grace and return organic matter and nutrients to the soil in rel- Jutila 1999), although both positive and negative ef- atively labile forms as dung and urine, which may stim- fects on diversity are possible depending on the mech- ulate soil activity (Ruess and McNaughton 1987, anisms involved (Olff and Ritchie 1998, Proulx and Bardgett et al. 1998a, Mulder and Ruess 1998). Second, Mazumder 1998). The effects of plant diversity on de- herbivory can affect soil biota by inducing physiolog- composer diversity are poorly understood, although ical changes at the whole-plant level, either by altering reasons can be presented both for and against a rela- the biomass and productivity of the browsed plant tionship between decomposer diversity and plant di- (Ruess et al. 1998; but see McNaughton et al. 1998), versity (Wardle et al. 1999, Hooper et al. 2000). Suo- or by inducing the browsed plant to produce biomass, monen (1999) found gastropod diversity was consis- and subsequently litter, of altered quality and decom- tently reduced by browsing while Leetham and Mil- posability (Seastedt et al. 1988, Tuomi et al. 1988, chunas (1985) and Wall-Freckman and Huang (1998) Kielland et al. 1997, Kaitaniemi et al. 1998). Third, on found no effect of browsing on the diversity of mi- a longer temporal scale, browsing mammals prefer- croarthropods and nematodes, respectively. entially feed upon plant species with a higher resource Despite the dearth of information, the potential ef- quality (Coley et al. 1985, Grime et al. 1996), often fects of browsers on populations of soil organisms and resulting in their replacement in the plant community soil community structure may control ecosystem pro- by species which are better defended but have poorer cesses in the longer term (Milchunas et al. 1998). The resource quality (Augustine and McNaughton 1998, composition of the decomposer food web can operate Ritchie et al. 1998), ultimately causing retardation of as a key regulator of mineralization processes (Ingham soil processes (Pastor et al. 1988, 1993; but see De et al. 1986, Bengtsson et al. 1996), plant nutrient ac- Mazancourt and Loreau 2000). The effects of herbi- quisition (SetaÈlaÈ and Huhta 1991), and ultimately plant vores on soil processes via the above mechanisms are growth (Alphei et al. 1996, Laakso and SetaÈlaÈ 1999). increasingly recognized as important in in¯uencing The indirect in¯uence of browsing on soil communities plant nutrition and plant growth, resulting in major is therefore likely to operate as a critical link in main- feedbacks between the aboveground and belowground taining feedbacks between the soil subsystem and the compartments of ecosystems (McNaughton et al. 1988, plant±herbivore subsystem (e.g., McNaughton et al. De Mazancourt et al. 1998, 1999, Mulder and Ruess 1988, Pastor et al. 1988, De Mazancourt et al. 1998, 1998). Mulder and Ruess 1998). While research on how herbivores affect soil pro- Several species of browsing mammals were liberated cesses is increasing, remarkably little is known about in New Zealand between the 1770s and 1920s, includ- how they in¯uence the components of the soil food ing Capra hircus L. (feral goats) and deer (most notably web which ultimately regulate these processes. How- Cervus elaphus scoticus LoÈnnberg [red deer]); prior to ever, there is evidence that the effects of herbivory on this, forest dwelling browsing mammals were absent the microbial biomass can be positive (Ruess and Sea- from New Zealand. Since their introduction, browsing gle 1994, Bardgett and Leemans 1995, Stark et al. mammals have become widespread and abundant 2000), negative (Pastor et al. 1988), or neutral (Wardle throughout most of the forested landscape of New Zea- and Barker 1997) depending on the system being con- land. Several studies have shown, mainly through the sidered. There is some evidence from the few studies use of fenced exclosures, that introduced browsing available that aboveground herbivory may also in¯u- mammals commonly reduce vegetation density in the ence higher trophic levels of decomposer food webs, browse layer and alter vegetation composition by fa- for example microbe-feeding nematodes (Yeates 1976, voring unpalatable ferns and monocotyledonous spe- Seastedt et al. 1988, Merrill et al. 1994), microarthro- cies at the expense of faster-growing, palatable, broad- pods (Leetham and Milchunas 1985, Bardgett et al. leaved species (Conway 1949, Williams 1955, Wallis 1993), litter-associated gastropods (Suominen 1999), and James 1972, Jane and Pracy 1974, Smale et al. and various soil-associated macrofauna (Suominen et 1995). New Zealand's native megaherbivores, moas al. 1999). Foliar herbivory can also alter the compo- (Aves: Dinornithiformes), became extinct through hu- sition of speci®c groups of soil biota (Milchunas et al. man hunting probably around or before AD 1400 (Hol- November 2001 BROWSING MAMMALS AND DECOMPOSERS 589 daway and Jacomb 2000). While the ecological impact 1980s the former New Zealand Forest Service (NZFS) of these browsers remains unclear, their browsing hab- established several hundred exclosures throughout its were probably very different from those of deer and New Zealand to assess the impacts of introduced deer goats (Atkinson and Greenwood 1989, Caughley 1989) and goats on vegetation in natural forests. With the and the effects of moa browsing on vegetation are be- dissolution of the NZFS in the late 1980s, maintenance lieved to have been considerably less severe than those of the vast majority of these exclosures was discontin- of introduced browsing mammals (McGlone and Clark- ued and many are no longer effective at excluding son 1993). browsing mammals, although it is likely that over 100 There is increasing interest in understanding the eco- still remain in adequate condition. These exlosures logical signi®cance of alien organisms in new envi- have the advantage of being scattered throughout most ronments (Vitousek et al. 1997). The New Zealand for- of New Zealand's forest types and climatic regions, and ested landscape presents an almost unique opportunity are suf®ciently distant from major tracks and routes to to determine the impacts of introducing an entire func- reduce the incidence of human interference; many can tional group of alien organisms (forest-dwelling brows- only be accessed by several hours walking or by he- ing mammals) to an environment from which that group licopter or boat. They represent a unique resource for was absent. In this context, we aimed to test the fol- addressing questions about how the introduction of a lowing four interrelated hypotheses so as to better un- whole functional group of alien animal species can alter derstand the community- and ecosystem-level impacts ecosystem properties. of introduced browsing mammals in New Zealand, with For the present study, we selected 30 exclosures, emphasis on effects of browsers on the biotic com- representing a wide geographic range and encompass- ponents of the decomposer subsystem, through the use ing most of New Zealand's major forest types (Fig. 1, of long term animal exclosure plots: Table 1; all sites subsequently referred to by the codes Hypothesis 1.ÐBrowsing greatly reduces vegetation in the left hand column of Table 1). Only exclosures density in the browse layer and shifts dominance to that were at least 13 yr old were considered. The main unpalatable plant species; this, in turn, adversely af- browsing mammal in most locations was C. elaphus, fects soil chemical properties and various constituents with several locations supporting C. hircus, and with of the decomposer food web. This hypothesis is con- the dominant browser in some areas being Dama dama sistent with the ®ndings of Pastor et al. (1988, 1993) L. (fallow deer), Odocoileus virginianus Zimmerman for boreal forests, and builds upon earlier studies in (white tailed deer), or Macropus eugenii Desmarest New Zealand forests suggesting that browsing mam- (Dama wallaby). These exclosures do not exclude in- mals induce dominance of certain plant functional troduced arboreal browsing mammals such as Tricho- types above others (Wallis and James 1972, Jane and surus vulpecula Kerr (brushtail possum), or introduced Pracy 1974). rodents. Twenty nine of the exclosures were established Hypothesis 2.ÐBrowsing mammals alter plant com- by the NZFS, while one (S21) was set up by the Uni- munity species composition, which, in turn, in¯uences versity of Canterbury's School of Forestry. Most ex- the species composition and quality of litter, and there- closures were ϳ400 m2 or 20 ϫ 20 m (mean Ϯ 1 SE fore the composition of the main taxa of soil organisms. ϭ 431 Ϯ 76 m2). Each exclosure was sampled once This hypothesis predicts that the magnitude of effects between 25 September 1997 and 26 May 1999. While of browsing mammals on soil communities will be de- we acknowledge that a one-time sampling cannot re- termined by the magnitude of effects of browsers on ¯ect temporal trends in our response variables, we re- plant community composition. stricted our sampling to the spring and autumn months Hypothesis 3.ÐBrowsing mammals may induce pos- to avoid any extremes of temperature and moisture that itive or negative changes in plant diversity, and these may have confounded the results. effects are matched by corresponding predictable shifts The exclosures were not initially replicated, a prob- in the diversity of litter types entering the decomposer lem that characterizes the vast majority of published subsystem, and ultimately in the diversity of various exclosure studies (see Stohlgren et al. 1999), particu- components of the belowground biota. larly those that involve older exclosures. However, be- Hypothesis 4.ÐReductions in populations and bio- cause most of the exclosures in our study were rela- masses of soil biota due to browsing will reduce be- tively large and because the focus was on belowground lowground processes such as C mineralization, result- properties effectively sampled over smaller spatial ing in a greater storage of C and N on an areal basis scales, we employed a strati®ed sampling regime (cf., in the litter and humus layers of browsed forests. Stark et al. 2000). For each location we set up four subplots (usually 4 ϫ 4 m) per exclosure, with one METHODS subplot in each corner, and each subplot usually at least 1.5 m away from the fence; adjacent subplots were at System and sampling strategy least 8 m apart in the vast majority of cases. We also Our study utilized a series of long-term, fenced, set up four 4 ϫ 4-m subplots outside the exclosure, browsing mammal exclosures. From the 1950s to the each paired with one of the inside-exclosure subplots 590 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 1. Distribution of the 30 locations that were sampled. Location codes are as for Table 1. and located at least 3 m outside the fence. The four height frequency method (Scott 1965, Dickinson et al. pairs of subplots (each consisting of an inside-exclo- 1992). A 2-m pole marked at 10-cm increments was sure subplot and an outside-exclosure subplot) served positioned vertically, and for each plant species the as the unit of replication for each location. presence of any vegetation intercepting a prescribed For each subplot at each location we measured both cylinder (adjacent to the pole and indicated by hori- browse-layer vegetation (0±2 m height layer) and zontal circular guide rings attached to the pole) of di- ground-layer vegetation (0±10 cm height layer). Den- ameter 5 cm was recorded for each of the twenty 10- sity of browse-layer vegetation was measured using a cm height classes. This pole was positioned twenty November 2001 BROWSING MAMMALS AND DECOMPOSERS 591

TABLE 1. Characteristics of the 30 forest exclosure plots sampled in New Zealand.

Tree January July Year spe- Tree Annual mean mean exposure cies basal Site Mammals Altitude rainfall temp. temp. estab- rich- area code Dominant tree species² excluded³ (m. a.s.l.)§ (mm) (ЊC) (ЊC) lished ness࿣ (m2/ha) S1 Aga. aus., Bei tar. Cap. hir. 250 1974 17.5 9.9 1984 8 114 S2 Bei. tar., Rho. sap., Cya. dea. Cap. hir. 180 2194 17.9 10.5 1984 8 40 S3 Kun. eri. Dam. dam. 110 1377 17.9 9.6 1983 5 31 S4 Aga. aus. Cap. hir. 120 2218 18.3 8.8 1983 4 66 S5 Mel. ram., Cya. med., Kni. exc. Cer. ela., Mac. cug. 310 1739 17.3 7.0 1984 4 35 S6 Bei. taw. Cer. ela. 375 1453 16.9 6.0 1961 8 49 S7 Not. cli. Cer. ela. 400 1476 16.8 5.9 1961 3 28 S8 Dic. squ., Kun. eri., Mel. ram. Cer. ela. 180 2212 18.0 7.4 1968 8 49 S9 Cya. smi., Bei. taw. Cap. hir. 490 2536 16.0 7.3 1983 6 45 S10 Pod. hal., Gri. lit., Phy. alp. Cer. ela. 995 2415 13.4 3.1 1985 6 57 S11 Pod. hal., Cor. ban., Bra. rot. Cap.hir. 900 4742 12.5 4.7 1972 4 7 S12 Kun. eri. Cer. ela. 650 1327 15.5 5.0 1982 4 32 S13 Kun. eri. Cer. ela. 600 1901 15.5 5.2 1982 3 38 S14 Not. cli. Cer. ela. 1090 1605 12.9 2.8 1983 3 98 S15 Several codominant Cer. ela. 590 1708 14.8 5.2 1974 14 19 S16 Myr. sal., Wei. rac., Not. fus. Cap. hir. 340 1249 15.1 7.2 1978 12 70 S17 Not. men., Not. fus., Wei. rac. Cer. ela. 600 1616 14.2 4.5 1975 7 61 S18 Not. sol. Cer. ela. 800 1535 13.8 2.9 1963 5 55 S19 Not. fus., Gri. lit., Car ser. Cer. ela. 560 1615 14.8 3.2 1963 7 55 S20 Not. fus., Not. men. Cer. ela. 710 1565 14.3 2.3 1963 2 33 S21 Not. cli. Cer. ela. 1300 2594 10.4 Ϫ1.0 1970 1 149 S22 Wei. rac., Lib. bid., Pod. tot. Cer. ela. 460 3932 14.5 3.8 1966 7 84 S23 Lib. bid., Pod. hal. Cer. ela. 470 5896 14.2 3.6 1967 11 50 S24 Mel. ram. Cer. ela. 230 2958 14.0 4.0 1968 4 74 S25 Not. cli. Cer. ela. 900 1832 10.4 0.6 1972 1 93 S26 Not. men. Cer. ela. 540 1141 12.7 2.4 1964 3 155 S27 Not. men. Cer. ela. 640 1127 11.9 2.3 1976 1 72 S28 Met. umb., Wei. rac. Odo. vir. 75 1331 12.4 5.4 1979 6 192 S29 Bra. rot., Dic. squ., Car. ser Odo. vir. 35 1329 12.6 5.6 1979 6 36 S30 Wei. rac., Dic. squ., Met. umb. Odo. vir. 75 1331 12.4 5.4 1979 7 81 ² Only tree species that constitute Ͼ10% of total basal area are included. Codes for tree species: Aga. aus. ϭ Agathis australis Salisb.; Bei. tar. ϭ Beischmeidia tarairi (A. Cunn.) Benth & Hook. f. ex Kirk; Bei. taw. ϭ B. tawa (A. Cunn.) Benth. & Hook. f. ex. Kirk; Bra. rot. ϭ Brachyglottis rotundifolia J. R. Forst. & G. Forst.; Car. ser. ϭ Carpodetus serratus J. R. Forst. & G. Forst.; Cor. ban. ϭ Cordyline banksii Hook. f.; Cya. dea. ϭ Cyathea dealbata (Forst. f.) Swartz; Cya. med. ϭ C. medullaris (Forst. f.) Schwartz; Cya. smi. ϭ C. smithii Hook. f.; Dic. squ. ϭ Dicksonia squarrosa (Forst. f.) Swartz; Gri. lit. ϭ Griselinia littoralis Raoul; Kni. exc. ϭ Knightia excelsa R. Br.; Kun. eri. ϭ Kunzea ericoides (A. Ritch.) Joy Thomps.; Lib. bid. ϭ Librocedrus bidwillii Hook. f.; Mel. ram. ϭ Melicytus rami¯orus I. R. Forst. & G. Forst.; Met. umb. ϭ Metrosiderus umbellata Cav.; Myr. sal. ϭ Myrsine salicina Hew. Ex. Hook. f.; Not. cli. ϭ Northofagus solandri var. clifforitioides (Hook. f.). Poole; Not. fus. ϭ N. fusca (Hook. f.) Oerst.; Not. men. ϭ N. menziesii (Hook. f.); Not. sol. ϭ N. solandri var. solandri (Hook. f.) Oerst; Phy. alp. ϭ Phyllocladus alpinus Hook. f.; Pod. hal. ϭ Podocarpus hallii Kirk; Pod. tot. ϭ P. totara G. Benn.; Rho. sap. ϭ Rhopalostylis sapida H. Wendl. & Druce; Wei. rac. ϭ Weinmannia racemosa L. f. ³ Codes for mammal species: Cap. hir. ϭ Capra hircus; Cer. ela. ϭ Cervus elaphus scoticus; Dam. dam. ϭ Dama dama; Odo. vir. ϭ Odocoileus virginianus; Mac. eug. ϭ Macropus eugenii. § Meters above sea level. ࿣ Number of tree species of Ͼ5 cm diameter at 1.3 m height, on a plot of 400 m2. times within each subplot (in a 4 ϫ 5 grid), resulting plot, suf®cient quadrats were sampled to provide in a maximum possible score of 400 intercepts for each enough material for the required analyses and in most species in the browse layer. Ground layer vegetation cases at least three quadrats per subplot were sampled. was assessed in each subplot by using a point intercept All litter was combined within each subplot, as was all method (Goodall 1952). A frame with ®ve points 20 humus. A separate collection of litter from each subplot cm apart was projected downwards and all plant species was made speci®cally for the extraction of soil me- intercepted by each point were recorded. This frame sofauna and macrofauna. Here, litter was collected was positioned twenty times in each subplot, resulting from six circular areas of 34 cm diameter in each sub- in a maximum possible score of 100 intercepts for each plot; all litter was combined for each subplot. species. Humus and litter samples were collected from each Litter and humus analyses subplot for chemical, microbial, and microfaunal anal- Humus and litter sampled using the square quadrats ysis. Several square quadrats (usually 30 ϫ 30 cm) was weighed and the gravimetric moisture content were placed in each subplot and litter and humus were (80ЊC, 24 h) measured to determine the total mass of collected separately within these quadrats. In each sub- litter and humus present in each subplot on an areal 592 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4 basis. Each sample was then homogenized and a rep- Amounts of total soluble C in these extracts were then resentative subsample used to determine C and N con- determined as described above. centrations (using a Leco FP-2000 analyzer; Labora- A preweighed subsample (usually ϳ100 g wet mass) tories Equipment Corporation, St. Joseph, Michigan, of each homogenized humus and litter layer sample USA) and pH. Storage of C and N on an areal basis in was used for microfaunal and enchytraeid determina- the litter and humus layers was determined from these tion by using a tray variant of the Baermann method ®gures. (Southey 1986, Yeates et al. 1993b). Total nematodes, For each litter sample, a representative subsample rotifers, copepods, tardigrades, and enchytraeids were (ϳ100 g wet mass) was hand sorted into leaf litter, twig counted under a stereomicroscope at 40ϫ before being litter and amorphous material. All leaf litter was then killed and ®xed by addition of an equal volume of hand sorted into component species. Oven dry mass boiling 8% formaldehyde. Subsequently, a mean of 126 (80ЊC, 24 h) of all sorted material was then determined. nematode specimens from each sample were identi®ed A subsample of each homogenized sample was se- to nominal genus or family level and placed into six lected for microbial measurements; all samples were functional groupings occupying three trophic levels, stored at 4ЊC until the time of measurement. In the case following Yeates et al. (1993a, b). These trophic group- of humus, this material was sieved to 4 mm while the ings (with component functional groups in brackets) litter layer material was cut into fragments of 1 cm were: microbe feeders (bacterial feeders and fungal whenever necessary. Microbial basal respiration of feeders), predators (top predators and ``omnivores'', each subsample was determined as described by Wardle i.e., predators that feed at more than one trophic level), (1993). This involved adjusting 3 g (dry mass) humus and herbivores (plant parasites and plant associates). or litter to 150% moisture content (dry mass basis), The leaf litter material collected from each subplot placing it in a 130-mL airtight incubation vessel, and for mesofaunal and macrofaunal assessments was extracted in its entirety by placing it in a Tullgren (mod- incubating at 22ЊC. CO2-C evolution between 1 h and 4 h of incubation was then determined by injecting 1- i®ed Berlese) funnel for a period of 6±14 d depending on the bulk and moisture content of the litter. Inver- mL subsamples of headspace gas into an infrared gas tebrates were captured in ethylene glycol and stored in analyzer. Substrate-induced respiration (SIR; a relative 70% ethanol prior to sorting and identi®cation. Fol- measure of active microbial biomass) was determined lowing Tullgren funnel extraction, the samples were using the approach of Anderson and Domsch (1978), sieved and all material passing through a 5-mm mesh as modi®ed by West and Sparling (1986) and Wardle was scanned using a binocular microscope for shells (1993). This was performed as for basal respiration, of gastropod species not extracted in the funnels. The but with an amendment of 10 mg glucose/g material groups of mesofauna enumerated included Collembola at the beginning of the incubation. and Acari (the latter separated into Oribatida, Astig- Total microbial biomass C and N was determined for mata, Mesostigmata, and Prostigmata). Main groups of each humus sample, using the fumigation±extraction macrofauna counted included Coleoptera (identi®ed to procedure described by Wardle and Ghani (1995), mod- family), Staphylinidae (Coleoptera; identi®ed to sub- i®ed from Brookes et al. (1985) and Vance et al. (1987). family), Stratiomyidae (Diptera) larvae, Gastropoda This technique cannot be reliably applied to litter, so (identi®ed to species), Isopoda, Amphipoda, Diplopoda the litter samples were not analyzed using this ap- (identi®ed to family), Chilopoda, Araenida, Pseudo- proach. Brie¯y, duplicate subsamples (5 g dry mass) scorpionidea, and Opiliones. of each humus sample were fumigated with chloroform and a further two were left nonfumigated; these sub- Community-level assessments samples were extracted with 0.5 mol/L K2SO4 for2h For each group of taxa that we assessed (including on an end-over-end shaker. These samples were then litter), we aimed to determine the effects of browsing centrifuged and ®ltered and stored at 4ЊC until analysis on community composition. These groups (and the tax- was complete. Total C in the fumigated and nonfu- onomic resolution to which they were identi®ed) in- migated extracts was determined on a Shimadzu 500 cluded plants in the browse layer (species level), plants TOC analyzer (Shimadzu Corporation, Kyoto, Japan; in the ground layer (species level), leaf litter in the Ghani et al. 1999). These extracts were also analyzed litter layer (species level), litter layer habitat compo- for N using micro-Kjeldahl analysis. Microbial C and sition (separated into twigs, amorphous material, and N were determined by using the differences in C and leaf litter sorted into species), Nematoda in litter (fam- N between the fumigated and nonfumigated subsam- ily level), Nematoda in humus (family level), Gastro- ples with transformation multipliers of 2.22 (Brookes poda in litter (species level), Diplopoda in litter (family et al. 1985, Wu et al. 1990). Water soluble C concen- level), Staphylinidae in litter (subfamily level), and Co- trations were also determined for each humus sample leoptera in litter (family level). To determine the degree as described by Wardle and Ghani (1995) by extracting of dissimilarity of community composition inside vs. 10 g (dry mass; sieved to 4 mm) humus in 20 mL water outside for each exclosure (cf. Milchunas and Lauen- for 30 min using an end-over-end shaker at 20ЊC. roth 1993, Milchunas et al. 1998) for each of these ten November 2001 BROWSING MAMMALS AND DECOMPOSERS 593 groups, we quanti®ed the dissimilarity between each outside exclosure]/[population inside exclosure]; see subplot inside the exclosure and the corresponding sub- Milchunas and Lauenroth 1993) across all 30 locations. plot outside the exclosure, using the community dis- These independent variables included plant browse lay- similarity index of Whittaker (1952). This index in- er biomass and community characteristics, and litter creases with increasing dissimilarity of community and humus chemical properties (and effects of browsers composition, and ranges from 0 (community compo- on each of these variables), as well as such factors as sition identical between the two subplots) to 1 (com- site macroclimate, forest stand properties, altitude, lat- munity composition mutually exclusive between the itude, and age of exclosure. Macroclimatic variables subplots). were determined for each location using climate-sur- To determine the effect of browsing on community face models (Leathwick and Stephens 1998) and in- diversity, the Shannon-Weiner diversity index was cal- cluded mean annual rainfall; mean July, January, and culated for each subplot for each of these ten groups; annual air temperature; mean annual humidity; mean the index based on the litter habitat composition of the solar radiation; and mean annual potential evapotrans- litter layer was used as a measure of microhabitat di- piration. Forest stand properties included tree species versity (i.e., litter habitat diversity). Taxonomic rich- richness, diversity (Shannon-Weiner index), and basal ness, i.e., number of taxa noted for each subplot, was area for all trees with diameter Ͼ5 cm at 1.3 m height, also determined for each of the groups except for litter measured on a 400 m2 plot at each location. Correlation layer habitat composition. and multiple stepwise regression analysis were also used to determine whether community dissimilarity Statistical analyses (between inside and outside exclosure) of each soil Our study enabled us to assess the effects of brows- animal group (Nematoda, Staphylinidae, Coleoptera, ing mammals on response variables at two contrasting Diplopoda, Gastropoda) across the 30 locations was scales: within each location and across all 30 locations. more closely related to community dissimilarity of At the within-location scale, the effect of browsing browse layer plants and/or litter across these locations, mammals on each response variable was assessed by or was instead related to some of the independent var- paired t tests in which the four subplots inside each iables mentioned above. Similar analyses were per- exclosure were compared with the corresponding four formed to determine whether effects of browsing on subplots outside it; data was transformed by log, square diversity of these animal groups across locations were root, or ranking whenever necessary to satisfy as- related to browsing effects on plant, leaf litter, and litter sumptions for parametric analysis. For the community layer habitat diversity; or whether other variables in- dissimilarity index data, it was not possible to test di- stead emerged as being of importance. rectly for statistical signi®cance of exclosure effects because each datum includes information from both RESULTS inside and outside the exclosure. Therefore, to test Plant responses whether community composition of each of the ten groups of taxa mentioned earlier differed signi®cantly Plant density in the browse layer (i.e., pole intercept between inside and outside the exclosure for each lo- frequency) was greater inside than outside the exclo- cation, Principal Components Analysis (PCA) was used sures for 25 of the 30 locations, and these effects were to derive principal components scores for each of the signi®cant at P ϭ 0.05 for 13 locations (Fig. 2). Further, eight subplots at that location which summarized the when the data for all 30 locations were pooled, plant overall community composition data for that group. density in the browse layer was signi®cantly greater Paired t tests were then used to determine whether the inside than outside the exclosures (Fig. 3). In contrast, principal component scores for the main two axes, de- for the 16 locations in which some ground layer veg- termined for each subplot, differed signi®cantly be- etation was present, there were several instances in tween inside the exclosure and outside it, and therefore which density in the ground layer was greater outside whether the community composition of that group sig- than inside the exclosure, and these effects were signi®cantly differed inside vs. outside the exclosure (see ni®cant at P ϭ 0.05 for ®ve locations (Fig. 2). There Wardle et al. 1999). were no overall signi®cant differences in the vegetation At the across-location scale, paired t tests were also density of the ground layer between inside and outside used for testing effects of browsing on the various re- exclosures when data were pooled for all locations (Fig. sponse variables that we measured, but with each of 3). the 30 locations serving as a single unit of replication. Browsing mammals affected the relative importance In addition, correlation and multiple stepwise regres- of different plant species in the browse layer, and there sion were used to evaluate the possible in¯uence of a were clear differences in composition inside vs. outside range of independent variables on the magnitude of for several exclosures (Fig. 4). At 12 locations, several effect of browsing mammals on the populations (or larger leafed plant species were very abundant inside biomasses) of various groups of soil organisms (cal- the exclosure and effectively absent outside it. Species culated as [population inside exclosure Ϫ population that were frequently severely reduced by browsers in- 594 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 2. Plant density and soil chemical properties inside and outside of 30 browsing mammal exclosure plots. I, inside exclosure; O, outside exclosure. For each panel, locations are arranged in order of decreasing effect of browsers on the density of plants in the browse layer (calculated as [density inside exclosure Ϫ density outside exclosure]/[density inside November 2001 BROWSING MAMMALS AND DECOMPOSERS 595 cluded Geniostoma rupestre J. R. Forst. & G. Forst., there were no overall effects of browsing mammals on Astelia spp., Griselinia littoralis Raoul, and Coprosma C or N storage in litter or humus, and the magnitude spp. (especially C. grandifolia Hook. f.). However, of the effect of browsers on C and N storage was not there were instances in which some plant species were signi®cantly correlated with the magnitude of effect of clearly promoted by browsing, and these tended to in- browsers on either vegetation density or vegetation clude smaller-leaved shrubs [i.e., Cyathodes juniperina composition (dissimilarity index data) across sites. J. R. Forst. and G. Forst., Leucopogon fasciculatus (G. Forst.) A. Rich], and some fern species [e.g., Blechnum Components of the soil microfood web spp., Polystichum vestitum (Forst. F.)]. Browsing mam- Our measurements enabled us to assess the effects mals also induced large changes in the vegetation com- of browsing mammals on the soil microfood web, position of the ground layer (Fig. 5); browsing signif- which includes the micro¯ora and microfauna, and icantly enhanced the cover of sedges (Uncinia spp.) at which spans at least three consumer trophic levels (Fig. ®ve sites and the grass Microlaena avenacea (Raoul) 8). The soil microbial biomass responded signi®cantly Hook. f. and ®lmy ferns (Hymenophyllum spp.) at two to browsers at several locations, whether measured by sites. fumigation±extraction or SIR (Fig. 8). There were also several instances of signi®cant effects of browsers on Humus and litter chemical properties the C to N ratio of the microbial biomass (Fig. 8). In nearly all of the 30 locations there was no sig- Microbial basal respiration, indicative of C minerali- ni®cant effect of browsing mammals on either N con- zation rate, was less strongly in¯uenced by browsing centration or C to N ratio of the litter layer (data not mammals, with ®ve and four locations showing sig- presented), although when the data were averaged ni®cant responses in the litter and humus layers re- across all 30 locations, the C to N ratio was marginally spectively (data not presented). signi®cantly lower inside (50.0) than outside (53.6) the Analysis of the within-exclosure data across the 30 exclosures (t ϭ 2.08, P ϭ 0.043; Fig. 3). Seven lo- locations revealed that microbial biomass in the humus cations showed signi®cant effects of browsers on hu- was most closely correlated with substrate N concen- mus N concentration although the direction of this re- tration (for both the SIR and fumigation±extraction sponse varied among locations (Fig. 2); only four data) while microbial biomass in the litter layer was showed signi®cant effects on humus C to N ratio (data most closely related to substrate pH (Table 2). Micro- not presented) and there were no signi®cant effects bial biomass showed little consistent relationship with when data were averaged across all 30 locations (Fig. most climatic or forest stand properties across locations 6). Ten and 11 locations showed signi®cant effects of (Table 2 and data not presented). Further, all microbial browsers on pH in the litter and humus layers, respec- parameters showed idiosyncratic responses to brows- tively, roughly equal numbers of locations showed ers, with both strong positive and negative effects being stimulation and reduction of pH by browsers, and when detected, and with no net effect of browsers on any the data were averaged across all 30 locations there microbial variable when the data from all 30 locations were no signi®cant differences inside vs. outside ex- were averaged (Figs. 3 and 6). The magnitude of effects closures (Figs. 3 and 6). Over a quarter of the locations of browsing mammals on the micro¯ora was not sig- also showed signi®cant effects of browsers on humus ni®cantly related to the magnitude of effects of brows- soluble organic C concentrations (Fig. 2), and, aver- ers on vegetation density or composition (quanti®ed aged across the 30 locations, concentrations were sig- using dissimilarity indices), or age of exclosures, ni®cantly greater inside (422 ␮g C/g humus) than out- across locations. However, the response of microbial side (351 ␮g C/g humus) exclosures (t ϭ 2.16, P ϭ biomass (fumigation±extraction) to browsers was high- 0.040; Fig. 6). ly positively correlated with the effects of browsers on For many of the 30 locations, browsing mammals humus N concentration across the 30 sites (R2 ϭ 0.323, signi®cantly affected C and N storage on an areal basis P ϭ 0.003). in the humus and (to a lesser extent) litter layers (Fig. The effects of browsing mammals on the soil mi- 7). Despite the strength of these effects in several cases, crofood web were clearly multitrophic in nature for the direction of browser effects was highly idiosyn- several locations; populations of microbe-feeding and cratic, with browsers signi®cantly promoting seques- predaceous nematodes were signi®cantly affected by tration of C and N in some cases and having the reverse browsers in both the humus and litter layers in nearly effect in others. When averaged across all 30 locations half the sites (Fig. 8). There were also frequent sig-

← exclosure]). For each location in each panel, the shaded bar is the larger of the two. Location codes correspond to Table 1. The symbols ϩ, *, **, and *** indicate that the inside and outside values differ at P ϭ 0.10, 0.05, 0.01, and 0.001, respectively. NA ϭ statistical test not performed because samples for all replicates needed to be combined to provide suf®cient humus for analysis; ND ϭ not determined. 596 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 3. Box-and-whisker plots summarizing data for the response to browsing mammals of autotrophs and components of the decomposer food web in the litter layer for all 30 locations. The index V (Wardle 1995), determined for each response variable for each location, becomes increasingly negative if the value is increasingly greater outside the exclosure relative to inside it, and increasingly positive if it becomes increasingly greater inside the exclosure than outside it; the index ranges from Ϫ1toϩ1, with 0 indicating no difference. For each variable, the box encompasses the middle half of the data (values of V) between the ®rst and third quartiles, the bisecting line is at the value of the median, and the horizontal line outside the box represents the typical range of data values. Asterisks indicate outlier values. P values are for paired t tests comparing the signi®cance of the difference between the value of the variable inside the exclosure and that outside the exclosure across the 30 locations. For each variable, locations with values of or very close to 0 both inside and outside the exclosure are not included. November 2001 BROWSING MAMMALS AND DECOMPOSERS 597

FIG. 4. Density of plant species in the browse layer inside and outside of 30 browsing mammal exclosure plots. All units are mean numbers of intercepts per 400 points (see Methods: System and sampling strategy). Only plant species with a mean score of three intercepts either inside or outside the exclosure are included. I, inside exclosure; O, outside exclosure. For each location in each panel, the shaded bar is the larger of the two. Location codes correspond to Table 1. The symbols ϩ, *, **, and *** indicate that the inside and outside values differ at P ϭ 0.10, 0.05, 0.01, and 0.001, respectively. Species abbreviations are as for Table 1 and additional ones are as follows: Ack. ros. ϭ Ackama rosifolia A. Cunn.; Asp. bul. ϭ Asplenium bulbiferum Forst. f.; Ast. tri. ϭ Astelia trivervia Kirk; Ast. sp. ϭ Astelia sp.; Ble. dis. ϭ Blechnum discolor (Forst. f.) Keys; Ble. fra. ϭ B. fraseri (Cunn.) Luerssen; Ble. mon. ϭ B. montanum Chambers and Farrant; Ble. nov. ϭ B. novae- zealandiae Chambers and Farrant; Bra. rep. ϭ Brachyglottis repanda J. R. Forst. and G. Forst.; Car. arb. ϭ Carmichaelia arborea (G. Forst.) Druce; Cop. arb. ϭ Coprosma arborea Kirk; Cop. cil. ϭ C. ciliata Hook. f.; Cop. foe. ϭ C. foetidissima J. R. Forst and G. Forst; Cop. gra. ϭ C. grandifolia Hook. f.; Cop. lin. ϭ C. linariifolia Hook. f.; Cop. luc. ϭ C. lucida J. R. et G. Forst.; Cop. mic. ϭ C. microcarpa Hook. f.; Cop. par. ϭ C. parvi¯ora Forst f.; Cop. pro. ϭ C. propinqua A. Cunn.; Cop. rha. ϭ C. rhamnoides A. Cunn.; Cop. rot. ϭ C. rotundifolia A. Cunn.; Cop. s. t. ϭ Coprosma sp. (t) as in Eagle, A.; Cop. ten. ϭ C. tenuifolia Cheeseman; Cya. jun. ϭ Cyathodes juniperina (J. R. Forst. and G. Forst.) Druce; Fre. bau. ϭ Freycinetia baueriana Endl.; Gah. pau. ϭ Gahnia pauci¯ora Kirk; Gen. rup. ϭ Geniostoma rupestre J. R. Forst. and G. Forst.; Heb. str. ϭ Hebe stricta (Benth.); Hed. arb. ϭ Hedycarya arborea J. R. Forst. and G. Forst.; His. inc. ϭ Histiopteris incisa (Thunb). J. Smith; Leu. fas. ϭ Leucopogon fasciculatus (G. Forst.) A. Rich; Lyc. deu. ϭ Lycopodium deuterodensum Herter; Lyc. vul. ϭ L. volubile Forst. f.; Myr. aus. ϭ Myrsine australis (A. Rich.) Allan; Neo. ped. ϭ Neomyrtus pedunculata (Hook. f.); Ole. ran. ϭ Olearia rani A. Cunn.; Phy. tri. ϭ Phyllocladus trichomanoides D. Don; Pim. sp. ϭ Pimelia sp.; Pit. ten. ϭ Pittosporum tenuifolium Sol. Ex. Gaertn.; Pol. ves. ϭ Polystichum vestitum (Forst. f.); Pse. axi. ϭ Pseudowintera axillaris (J. R. et. G. Forst.); Pse. col. ϭ P. colorata (Raoul) Dandy; Pse. les. ϭ Pseudopanax lessonii (D. C.) C. Koch; Pse. sim. ϭ P. simplex (G. Forst.) Philipson; Rip. sca. ϭ Ripogonum scandens J. R. & G. Forst.; Rub. cis. ϭ Rubus cissoides A. Cunn.; Sch. dig. ϭ Schef¯era digitata J. R. and G. Forst. ni®cant effects of browsers on the ratio of bacterial overall signi®cant effect of browsers on nematode pop- feeding to fungal feeding nematodes, and therefore on ulations across the 30 locations (Figs. 3 and 6). Similar the relative importance of the bacterial vs. fungal en- patterns were also noted for other, less numerous, soil ergy channels. Again the effects of browsing mammals microfood web components, i.e., tardigrades, cope- on all nematode variables were idiosyncratic, with no pods, and rotifers (Figs. 3 and 6). 598 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 5. Density of plant species in the ground layer inside and outside of the 16 browsing mammal exclosure plots in which a ground layer vegetation was present. All units are mean total numbers of intercepts per 100 points (see Methods: System and sampling strategy). Only plant species with a mean score of two intercepts either inside or outside the exclosure are included. I, inside exclosure; O, outside exclosure. For each location in each panel, the shaded bar is the larger of the two. Location codes correspond to Table 1. The symbols ϩ, *, **, and *** indicate that the inside and outside values differ at P ϭ 0.10, 0.05, 0.01, and 0.001, respectively. Species abbreviations are as for Table 1 and Fig. 4; additional ones are as follows: Ble. cha. ϭ Blechnum chambersii; Ble. ®l. ϭ B. ®liforme (Cunn.) Ettingsh; Ble. ¯u. ϭ B. ¯uviatile (R. Br.) Salomon; Hym. dem. ϭ Hymenophyllum demissum (Forst. f.) Swartz; Hym. dil. ϭ H. dilatatum (Forst. f.) Swartz; Hym. mul. ϭ H. multi®dum (Forst. f.) Swartz; Hym. san. ϭ H. sanguinolentum (Forst. f.) Swartz; Hym. sp. ϭ Hymenophyllum sp.; Lyc. vol. ϭ Lycopodium volubile Forst. f.; Met. rob. ϭ Metrosideros robusta A. Cunn.; Mic. ave. ϭ Microlaena avenacea (Raoul) Hook. f.; Phy. pus. ϭ Phymatosorus pustulus (Forst. f.) Large, Braggins and Green; Unc. cla. ϭ Uncinia clarata KuÈk; Unc. sp. ϭ Uncinia sp.; Unc. unc. ϭ U. uncinata (L. f.) KuÈk.

Analysis of the within-exclosure data across the 30 Mesofaunal and macrofaunal responses locations found that nematode populations often Browsing did not affect the abundance of enchy- showed signi®cant relationships with soil chemical traeids within locations (data not presented), and across properties (e.g., substrate pH, N concentration, and soil the 30 locations there was no signi®cant overall effect C on an areal basis), and in the case of microbe-feeding of browsers on enchytraeid abundance (Fig. 3). How- nematodes, total annual precipitation (Table 2). How- ever, the other groups of mesofauna (all microarthro- ever, there was no relationship between the magnitude pods) showed consistent and very clear responses to of effects of browsers on nematode populations and the browsers (Fig. 9), regardless of trophic position. Ef- magnitude of effects of browsers on vegetation density, fects of browsers on abundances of microarthropods vegetation composition, or age of exclosure across the were negative for all but one of the 63 instances in 30 locations. However, multiple stepwise regression which a signi®cant effect at P ϭ 0.05 was detected analysis revealed that a signi®cant proportion of the (Fig. 9). Across the 30 locations for the within-exclo- total variation across the 30 locations for the effects of sure data, all mesofaunal groups except the Mesostig- browsers on nematode abundance could be explained mata showed signi®cant relationships with some sub- in terms of several other independent variables includ- strate and macroclimatic variables (Table 2), but not ing substrate properties, tree stand characteristics and with forest stand variables (data not presented). Further, effects of browsers on organisms of lower trophic lev- when the results were averaged over all 30 locations els (Table 3). This was especially apparent for microbe- the effects of browsers on microarthropod populations feeding nematodes in litter and predaceous nematodes were highly signi®cant for all groups (Fig. 3). The mag- in humus, for which 50% and 64% of the total variation nitude of effects of browsers on microarthropod pop- could be explained, respectively. ulations did not re¯ect the magnitude of effects of November 2001 BROWSING MAMMALS AND DECOMPOSERS 599

FIG. 6. Box-and-whisker plots summarizing data for the response to browsing of components of the decomposer food web in the humus layer, and autotrophs, for all 30 locations. See Fig. 3 legend for further explanation of plot. browsers on vegetation density, vegetation composi- to the effect of browsers on browse-layer vegetation tion, or age of exclosure across the 30 locations. How- density or composition, nor to age of exclosure. How- ever, multiple stepwise regression analysis showed that ever, for eight of the most abundant macrofaunal groups signi®cant amounts of variation across the 30 sites in a statistically signi®cant proportion of the variation the effects of browsers on various microarthropod across the 30 locations with regard to their population groups could be effectively explained by macroclimatic response to browsing could be explained by combi- variables, density of browse layer vegetation inside the nations of variables re¯ecting soil chemical, litter com- exclosure, and the effects of browsers on soil chemical positional, forest stand, and macroclimatic properties. properties including soil storage of C and N (Table 3). (Table 3). For the Gastropoda, Diplopoda, and Am- Responses in abundance of macrofauna to browsing phipoda, over 50% of the variation across locations in mammals were similar to those of mesofauna, and terms of response to browsers could be explained by again there were consistent, and often very strong, re- combinations of variables such as litter properties, ductions of all the dominant macrofaunal groups by browser effects on areal storage of C and N, and lo- browsers (Fig. 10); all but one of the 138 effects de- cation altitude (Table 3). picted in Fig. 10 which were signi®cant at P ϭ 0.05 involved reductions of abundance by browsers. For the Community dissimilarity within-exclosure data across the 30 locations, popu- The community dissimilarity analyses revealed that lations of ®ve of the eight macrofaunal groups were community structure differed signi®cantly between in- signi®cantly correlated with mean January tempera- side and outside of the exclosure plots for several lo- ture, and some also showed signi®cant relationships cations, and for ®ve groups of organisms (plants in the with substrate quality variables (Table 2); there were, browse layer, nematodes in humus, nematodes in litter, however, few relationships with forest stand variables diplopods, and gastropods) at least 60% of all sites across locations. When averaged across all 30 loca- showed signi®cant differences between inside and out- tions, populations of all 13 macrofaunal groups tested side the exclosure (Fig. 11). Across the 30 locations, were signi®cantly reduced by browsing mammals (Fig. there were no animal groups for which community dis- 3), irrespective of trophic position. The magnitude of similarity was signi®cantly related to plant community macrofaunal population response to browsers across dissimilarity (Table 4). Further, dissimilarity measures the 30 locations was generally not signi®cantly related for litter species composition were not signi®cantly re- 600 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 7. Storage of C and N on an areal basis in the humus and litter layers inside and outside of 30 browsing mammal exclosure plots. Symbols and legend are as for Fig. 2, and locations are arranged in the same rank order for each panel as for Fig. 2. lated to those for plants. However, dissimilarity indices was greater outside the exclosure. Averaged across all for litter nematodes, gastropods, and diplopods were 30 locations, diversity indices were signi®cantly re- all signi®cantly related to dissimilarity indices for spe- duced by browsers for vegetation in the browse layer cies composition of litter across the 30 sites, and litter but not in the ground layer (Table 5). Diversity indices nematode dissimilarity was very strongly correlated calculated for litter species, litter habitat, nematodes, with litter habitat dissimilarity (Table 4). Over 60% of diplopods, and gastropods were also often affected by variation across locations with regard to dissimilarity browsers but these effects were idiosyncratic with indices for litter could be explained by stepwise mul- roughly equal numbers of cases of stimulation and re- tiple regression relationships incorporating various site duction by browsing (Fig. 12); diversity indices were variables including tree diversity at the site (Table 5). not signi®cantly in¯uenced by browsing mammals for Stepwise multiple regression relationships could also these groups when averaged across all 30 locations explain Ͼ40% of the total variation across sites for (Table 6). However, diversity indices calculated for co- community dissimilarity for three of the faunal groups leopteran families and staphylinid subfamilies were, (litter nematodes, gastropods, and diplopods) in terms when signi®cantly in¯uenced by browsers, usually of combinations of independent variables such as litter greater outside the exclosure (Fig. 12). Averaged across dissimilarity indices, soil chemical properties, tree bas- all 30 locations, there was a signi®cant increase in di- al area, and macroclimatic properties (Table 5). versity of both these groups by browsers (Table 6). Plant species richness responses to browsers generally Community diversity paralleled those for plant diversity indices, with a mean In most locations browsing mammals reduced plant reduction by browsers of species richness across all diversity (Shannon-Weiner index) in the browse layer; locations of 38% in the browse layer (Table 6). Dip- diversity was greater inside the exclosure than outside lopod family richness was only signi®cantly affected for all but three locations and for half the locations the by browsers for two locations (data not presented) but effects were signi®cant at P ϭ 0.05 (Fig. 12). However, when the data were averaged across locations there was this trend did not occur for the ground layer vegetation a statistically signi®cant, although small, reduction in and in the majority of instances diversity in this layer richness (Table 6). Gastropod species richness was sig- November 2001 BROWSING MAMMALS AND DECOMPOSERS 601

FIG. 8. Properties of litter and humus microfood web components (micro¯ora and nematodes) inside and outside of 30 browsing mammal exclosure plots. FE ϭ fumigation±extraction method; SIR ϭ substrate induced respiration; mf ϭ microbe feeders; bf ϭ bacterial feeders; ff ϭ fungal feeders. Other symbols and legend are as for Fig. 2, and locations are arranged in the same rank order for each panel as for Fig. 2. ni®cantly reduced by browsers in nine locations (and duced by a mean of 13% by browsing, corresponding no signi®cant positive effects of browsers were found; to a loss of 2.4 species per location (Table 6). data not presented), and when the data were averaged When the within-exclosure data for the 30 locations across locations species richness was signi®cantly re- was considered, diversity indices of most groups were 602 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

TABLE 2. Pearson's correlation coef®cients between soil organism biomasses (microbial data) or populations (faunal data) and selected soil chemical and macroclimatic variables, for n ϭ 30 locations.

Storage Substrate N of C in Mean Mean Mean annual concentra- litter (areal annual January solar Size class Organism group Substrate pH tion basis) rainfall࿣ temperature radiation Micro¯ora³ Microbial biomass (SIR; humus) 0.148 0.364* 0.104 Ϫ0.083 Ϫ0.291 Ϫ0.158 Microbial biomass (SIR; litter) 0.437* 0.313² Ϫ0.031 Ϫ0.167 Ϫ0.244 Ϫ0.148 Microbial biomass (FE; humus) 0.282* 0.662** Ϫ0.158 0.438* 0.151 0.194 Microfauna Microbe-feeding Nematoda 0.104 0.461** Ϫ0.158 0.367* 0.236 Ϫ0.428* (humus) Microbe-feeding Nematoda 0.433* 0.495** Ϫ0.353* 0.588*** Ϫ0.045 0.089 (litter)࿣ Predaceous Nematoda (humus) Ϫ0.536** 0.279 0.233 Ϫ0.242 Ϫ0.430* Ϫ0.440* Predaceous Nematoda (litter) 0.164 0.541** Ϫ0.346* 0.205 Ϫ0.216 Ϫ0.194 Mesofauna Collembola 0.402* 0.317² Ϫ0.427* Ϫ0.126 0.521** 0.520** Oribatida 0.333² 0.241 Ϫ0.313² Ϫ0.137 0.470** 0.459** Mesostigmata 0.109 0.031 0.031 0.077 0.000 0.130 Protostigmata 0.419* 0.308² Ϫ0.151 Ϫ0.167 0.328² 0.420* Macrofauna Gastropoda 0.327² 0.420* Ϫ0.288 Ϫ0.154 0.408* 0.189 Isopoda 0.339² 0.134 Ϫ0.256 Ϫ0.122 0.546** 0.158 Diplopoda 0.207 0.161 Ϫ0.309² Ϫ0.104 0.527** 0.339² Amphipoda 0.392* 0.380* Ϫ0.362* 0.187 0.400* 0.200 Staphylinidae (predaceous) 0.197 0.236 Ϫ0.100 Ϫ0.262 0.242 0.228 Araenida 0.426* 0.330² Ϫ0.256 0.031 0.482* 0.204 Opiliones 0.488** 0.342² 0.248 0.000 0.070 0.154 Chilopoda 0.432* 0.134 Ϫ0.371* 0.054 0.282 0.161 Note: Only inside-exclosure data were included in analyses. ², *, **, *** Correlation coef®cient statistically signi®cant to 0 at P ϭ 0.10, 0.05, 0.01, and 0.001, respectively. ³ SIR ϭ substrate induced respiration method; FE ϭ fumigation±extraction method. ࿣ Log-transformed variable.

TABLE 3. Results of stepwise multiple regression analysis relating the magnitude of browsing effects on soil faunal populations to external environmental factors, for n ϭ 30 locations.

Size class Reduction by browsing of:² Independent variables in relationship³ R2 P Microfauna Microbe-feeding Nematoda (humus) ln(ASIRH) (Ϫ) 0.236 0.006 Microbe-feeding Nematoda (litter) TSH (Ϫ); DDOC (ϩ); NOR (ϩ) 0.504 Ͻ0.001 Predaceous Nematoda (humus) NLI (Ϫ); TNSP (Ϫ); DMF (ϩ) 0.641 Ͻ0.001 Predaceous Nematoda (litter) DMIC (ϩ); ln(RP) (Ϫ) 0.348 0.007 Mesofauna Collembola DNAREA (ϩ); JULT (ϩ); PCOV (ϩ) 0.463 0.001 Oribatida ACAREA (Ϫ); JULT (ϩ); PCOV (ϩ) 0.445 Ϫ0.002 Mesostigmata DNAREA (ϩ); APHH (Ϫ) 0.541 Ͻ0.001 Prostigmata SOLRAD (Ϫ) 0.323 0.001 Macrofauna Gastropoda DNAREA (ϩ); ͙ALTIT (Ϫ); CNLI (Ϫ) 0.596 Ͻ0.001 Isopoda STAREA (ϩ); ͙ALTIT (Ϫ) 0.458 Ͻ0.001 Diplopoda PHHI (ϩ); LDIS (ϩ); ln(ANL) (Ϫ) 0.522 Ͻ0.001 Amphipoda DCAREA (ϩ); CNLI (Ϫ); ͙ALTIT (Ϫ) 0.596 Ͻ0.001 Staphylinidae (predaceous) NHI (ϩ); PDIS (ϩ) 0.262 0.017 Araenida DNAREA (ϩ); LDIS (ϩ) 0.345 0.005 Opiliones PHLI (ϩ); SOLRAD (Ϫ) 0.358 0.003 Chilopoda STAREA (ϩ); APCOV (Ϫ) 0.422 Ͻ0.001 Note: Only terms that explain a statistically signi®cant proportion of the variation of the response variable at P ϭ 0.05 are included in each relationship. ² Expressed as ([population inside exclosure] Ϫ [population outside exclosure])/(population inside exclosure). ³(ϩ)or(Ϫ) after a variable indicates a positive or negative relationship between the independent variable and the response variable. Abbreviations are as follows: ACAREA, ANL, APCOV, APHH, ASIRH ϭ absolute value of proportional reduction by browsing, i.e., ([value inside exclosure] Ϫ [value outside exclosure])/[value inside exclosure] of humus C storage per unit area, N concentration of litter, density of browse layer vegetation, humus pH, and humus SIR, respectively; ALTIT ϭ altitude (meters above sea level), CNLI ϭ C-to-N ratio of litter inside exclosure; DDOC, DCAREA, DMF, DMIC, DNAREA ϭ proportional reduction by browsing of humus soluble C, humus C storage on an areal basis, populations of microbe- feeding nematodes, humus microbial biomass (fumigation±extraction), and humus N storage on an areal basis; JULT ϭ mean July temperature (ЊC); LDIS ϭ dissimilarity index D for plant litter species composition (inside vs. outside exclosure); NHI, NLI ϭ concentration of N (%) inside exclosure for litter and humus, respectively; NOR ϭ northing (relative scale based on latitude of site); PDIS ϭ dissimilarity index D for plant species composition of browse layer (inside vs. outside exclosure); PCOV ϭ density of browse layer vegetation inside exclosure (intercepts per 200 points); PHHI, PHLI ϭ pH inside exclosure of humus and litter, respectively; RP ϭ ratio of rainfall to potential evapotranspiration; SOLRAD ϭ solar radiation (mJ´mϪ2´dϪ1); STAREA ϭ tree stem density (no./ha); TNSP ϭ tree species richness per 400 m2; TSH ϭ tree species diversity (Shannon-Weiner diversity index). November 2001 BROWSING MAMMALS AND DECOMPOSERS 603

FIG. 9. Populations of microarthropod groups in litter inside and outside of 30 browsing mammal exclosure plots. Symbols and legend are as for Fig. 2, and locations are arranged in the same rank order for each panel as for Fig. 2. signi®cantly related to few forest stand or substrate and R2 ϭ 0.191, P ϭ 0.017, respectively). The mag- variables, but diversity of several groups was signi®- nitude of response of diplopod diversity to browsers cantly correlated with mean January temperature (i.e., was best predicted by a multiple regression relationship the Shannon-Weiner diversity values for litter species incorporating mean January temperature and the effect [R2 ϭ 0.151, P ϭ 0.042], staphylinid beetles [R2 ϭ of browsers on habitat diversity in the litter layer (R2 0.257, P ϭ 0.005], humus nematodes [R2 ϭ 0.144, P ϭ 0.550, P Ͻ 0.001). ϭ 0.033], and litter nematodes [R2 ϭ 0.244, P ϭ 0.006], and species richness for gastropods [R2 ϭ 0.257, P Ͻ DISCUSSION 0.001]). Across the locations, the effects of browsers Plant and soil food web responses on diversity of humus nematodes, but not of any other faunal group, was signi®cantly related to the response The response of the plant community to browsing of browse layer vegetation diversity to browsers (Table was generally consistent with our ®rst hypothesis; 7). Meanwhile, the effect of browsers on gastropod browsing usually reduced vegetation density and often diversity was signi®cantly related to the effect of severely reduced palatable, larger-leaved (notophyl- browsers on leaf species diversity in the litter layer, lous, sensu Raunkiaer [1934], Webb [1956]) species and browser effect on diplopod diversity was signi®- causing domination by unpalatable small-leaved (nan- cantly related to browser effect on litter layer habitat ophyllous and leptophyllous, sensu Raunkiaer [1934]) diversity (Table 7). With one exception there were no species, ferns, and ground layer monocotyledonous signi®cant correlations between the effects of browsers plants. This is consistent with studies showing shifts on any two groups of animal taxa (Table 7). Stepwise in the relative abundance of different plant functional multiple regression revealed few relationships between types following browsing in New Zealand forests (Wal- browser effects on diversity of faunal groups and in- lis and James 1972, Jane and Pracy 1974) and else- dependent site variables across the 30 locations. How- where (Augustine and McNaughton 1998, Virtanen ever, the magnitude of browser effects on gastropod 1998). The increases in abundance of unpalatable spe- diversity across sites was signi®cantly related to site cies often observed outside the exclosures was pre- humidity (R2 ϭ 0.339, P Ͻ 0.001), and browser effects sumably due to release from competition with palatable on coleopteran and staphylinid diversity were both sig- species, as well as improved light levels at the ground ni®cantly related to the effects of browsers on humus layer (Ritchie et al. 1998, Huisman et al. 1999, Suom- C storage on an areal basis (R2 ϭ 0.279, P ϭ 0.003 inen et al. 1999). Plant species with larger leaves and 604 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

FIG. 10. Populations of macrofaunal groups in litter inside and outside of 30 browsing mammal exclosure plots. Symbols and legend are as for Fig. 2, and locations are arranged in the same rank order for each panel are as for Fig. 2. November 2001 BROWSING MAMMALS AND DECOMPOSERS 605 speci®c leaf areas are often less well defended and have browsing mammals. Although the direction of these higher nutrient concentrations when compared with results is consistent with our ®rst hypothesis, this is species that produce smaller, longer lived, leaves (see unlikely to re¯ect changes in litter quality by browsers; Grime 1979, Coley et al. 1985, Cornelissen et al. 1999), the soil microfood web components, which are far more meaning that these larger leaved species are both more intimately associated with the resource than are most likely to be palatable to herbivores and produce litter of these organisms, did not show a unidirectional re- of superior quality for decomposers (Cornelissen et al. sponse. Further, reduction of mesofaunal and macro- 1999). The signi®cantly lower litter layer C to N ratio faunal groups occurred even for those locations in and higher humus soluble C content inside exclosures which browsers increased the quality of the resource across all 30 locations is consistent both with this trend base (e.g., sites S3, S5, and S9). The consistently ad- and with our ®rst hypothesis, and is presumably due verse effects of browsing mammals on these organisms to superior litter quality of those plant species domi- is therefore more likely to re¯ect the physical effects nating inside the exclosure (see Grime et al. 1996). of browsers, for example disturbance caused by tram- This effect is, however, relatively small and may there- pling and scuf®ng. The intensity of scuf®ng and tread- fore be insuf®cient to exert detectable effects on the ing (and resultant disturbance, compaction, and re- soil biota. duced substrate porosity) caused by hoof pressure from Our ®rst hypothesis was not supported when the deer and goats can be considerable, and is likely much components of the belowground microfood web were more severe than that caused by the extinct species of considered; for each of the three consumer trophic lev- browsing moas (Duncan and Holdaway 1989). In this els (microbes, microbe-feeders, predators), as many lo- context, it is signi®cant that, when data were pooled cations showed reduction as showed stimulation by across all 30 locations (Fig. 3), browsers had no overall browsers (Fig. 8). This means that, while browsing effect on any of those faunal groups that occupy the mammals had mostly unidirectional effects above- aqueous component of the litter layer and which are ground, these were not necessarily matched below- intimately associated with the leaf substrate, and had ground. The idiosyncratic response of microbes and adverse overall effects on all free living faunal groups micro¯ora to browsing mammals presumably re¯ects that are more exposed to external environmental fac- the range of mechanisms through which browsers can tors. This is consistent with studies showing that larger, affect belowground biota and which sometimes have free-living, soil animals are less resistant than smaller directly opposite consequences (Bardgett et al. 1998b); ones to exogenous disturbances (Wardle 1995). At it is the relative balance of these mechanisms which some sites, reduction of mesofaunal and macrofaunal determines the observed response of belowground or- groups may have also resulted from effects of browsers ganisms. For example, dung and urine return by brows- on plant properties allowing increased light incidence ers could positively affect the belowground biota (see at the ground layer (Suominen et al. 1999) and unfa- Ruess and McNaughton 1987, Mulder and Ruess 1998), vorable microclimatic changes (Kielland and Bryant while plant compositional changes (as per our hypoth- 1998). However, this was clearly not the case in all esis) may have the reverse effect. It is also apparent instances, because some locations that demonstrated that the effects of browsers on the soil microfood web strong responses to browsers of several faunal groups are tritrophic; frequently the highest trophic level (i.e., (e.g., sites S1, S4, and S29) showed no detectable effect the predatory nematodes which occupy the tertiary con- of browsing on vegetation density or composition. sumer trophic level) responded (either positively or Across the 30 locations, we failed to ®nd signi®cant negatively) to browsers when the lower ones did not, relationships between the magnitude of effect of brows- and vice versa. This is consistent with earlier experi- ers on browse layer vegetation density or composition mental and theoretical work suggesting that different (dissimilarity index data), and the magnitude of effect components of the soil microfood web are affected dif- of browsers on the abundance of any group of soil biota. ferentially by top-down vs. bottom-up forces following This is inconsistent with our ®rst hypothesis. Our mul- manipulation of the resource base (Wardle and Yeates tiple regression analyses (Table 3) suggest that the re- 1993, De Ruiter et al. 1995, Mikola and SetaÈlaÈ 1998). sistance of soil biota to browsers is instead determined Browsing mammals also changed the composition of by a suite of other factors. For many faunal groups, individual trophic levels within the microfood web; over half of the across-location variation for the effects frequently signi®cant (although idiosyncratic) effects of browsers on their densities could be explained by were noted both for the microbial C to N ratio and for combinations of other site-based factors such as be- the ratio of fungal feeding to bacterial feeding nema- lowground nutrient status, macroclimate, forest stand todes. This latter result indicates that browsers can in- properties, and the responses of lower trophic levels duce important shifts between the bacterial-based and and nutrients to browsers. This is consistent with pre- fungal-based energy channels in soil food webs (see vious studies indicating that habitat characteristics Moore and Hunt 1988, Bardgett et al. 1998b). (e.g., nutrient status of the system, C availability, mac- All mesofaunal groups (except Enchytraeidae) and roclimate) can determine the resistance, and other com- all macrofaunal groups were consistently reduced by ponents of stability, of populations and biomasses of 606 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4 November 2001 BROWSING MAMMALS AND DECOMPOSERS 607 organisms in a wide range of ecological communities aboveground vegetation; the absence of a link between (McNaughton 1985, De Angelis 1992, Closs and Lake the two with regard to the magnitude of dissimilarity 1994, Wardle 1998, McCauley et al. 1999). across locations can only be explained by the magnitude of browsing-induced effects either on above- Community dissimilarity ground production (and hence litterfall), or on litter Browsing mammals strongly affected the dissimi- quality and associated decomposition rates of resident larity of communities inside vs. outside exclosures for litter, also differing across locations. several locations and for all groups of organisms considered. However, there was no evidence that the com- Community diversity munity dissimilarity of any faunal group was signi®- There were large shifts in plant diversity due to cantly related to plant community dissimilarity across browsing mammals, consistent with our third hypoth- the 30 locations, in direct contrast to the predictions esis. These effects were usually negative, although a of our second hypothesis. Dissimilarity indices for small subset of locations did show signi®cant increases three litter-dwelling animal groups were instead sig- in plant diversity in the ground layer. Several earlier ni®cantly correlated with dissimilarity indices for litter studies have detected enhanced plant diversity due to composition across the locations, suggesting that aboveground mammalian herbivory, particularly in browsing mammals can alter community composition grasslands (Zeevalking and Fresco 1977, Collins et al. of some faunal groups through altering community 1998) probably through a reduction in competitive ex- composition of litter in the litter layer. This implies a clusion (Grace and Jutila 1999), an increased incidence level of speci®city of resources for the component or- of inedible plant species (Milchunas et al. 1988), and ganisms of these three groups. All three faunal groups disturbance effects (Olff and Ritchie 1998). However, that showed this relationship are mainly either microbe- in nutrient-poor ecosystems, diversity may reduce graz- feeders or microbidetritivores. Different types of litter ing because limited resources prevents vegetation re- support different communities of microorganisms growth after grazing (Pandey and Singh 1991, Proulx (Widden 1986, Carreiro and Koske 1992) and litter- and Mazumder 1998). Our exclosure sites were prob- dwelling fauna which feed on microbes (in particular ably quite nutrient poor in relation to those used for fungi) show distinct feeding speci®city (Visser and most other comparable studies (for our 30 locations, Whittaker 1977, Klironomas et al. 1992). Further, as C-to-N ratios in the litter layer ranged from 30 to 108 was the case for the belowground faunal population and in the humus layer from 16 to 46), and may be data, community dissimilarity inside vs. outside exclo- within the range for which browsing would be expected sures for these three groups was highly signi®cantly to reduce diversity (Proulx and Mazumder 1998). Fur- related to combinations of various site variables (Table ther, unlike other exclosure studies, New Zealand for- 5), indicating that site factors also govern resistance of ests did not evolve in the presence of the browsing belowground animals to browsing mammals at the mammals being investigated, and the extinct mega- community level. herbivores (moas) would not have exerted effects of The second hypothesis did not hold because, while comparable intensity (McGlone and Clarkson 1993). browser effects on community structure of some be- Plant species of New Zealand's forests may therefore lowground faunal groups were related to browser ef- not have evolved to thrive under high mammalian fects on the composition of their habitat in the litter browsing pressure, such as is the case for other ¯oras layer across the 30 locations, the magnitude of browser (Westoby 1989). effects on litter species composition clearly did not We found that the magnitude of effect of browsing re¯ect the magnitude of browser effects on plant com- mammals on diversity of only one animal group, hu- munity composition. The effect of browsers on litter mus-dwelling nematodes, was signi®cantly correlated compositional dissimilarity inside vs. outside exclo- with the magnitude of effect of browsers on browse- sures was instead strongly related to other, independent layer vegetation diversity across the 30 locations. Re- site variables (Table 5). Browsing mammals clearly in- duction of browse-layer plant species richness was duced changes in the community composition of dead matched by reduced richness of gastropod species and leaves in the litter layer, and these effects must have diplopod families across all 30 sites, but the magnitude ultimately resulted from changes in the composition of of reduction of richness of these animal groups was

←

FIG. 11. Community dissimilarity indices for various groups of organisms (including litter), indicating degree of dissimilarity of community structure inside vs. outside browsing mammal exclosure plots. For each panel, locations are arranged in order of decreasing dissimilarity between inside and outside exclosure for plant species in the browse layer. Location codes correspond to Table 1. The symbols ϩ, *, **, and *** indicate that community structure differs signi®cantly between inside and outside the exclosure at P ϭ 0.10, 0.05, 0.01, and 0.001, respectively, as determined by paired t tests on principal axes derived by Principal Components Analysis (see Methods: Statistical analyses). ND ϭ not determined; N ϭ no ground layer vegetation present. 608 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

TABLE 4. Pearson's correlation coef®cients between different groups of taxa (including plant litter) with regard to the community dissimilarity index D calculated for inside vs. outside exclosures, across n ϭ 30 locations.

Dissimilarity index (inside vs. outside exclosure) for: Dissimilarity index (inside Plants Litter Litter vs. outside (browse (leaf (habitat Nematoda Nematoda Staphylini- exclosure) for: layer) species) diversity) (humus) (litter) Gastropoda Diplopoda dae Litter (leaf species) Ϫ0.270 Litter (habitat diversity) 0.047 ND² Nematoda (humus) 0.152 0.110 Ϫ0.021 Nematoda (litter) 0.223 0.398* 0.570*** 0.116 Gastropoda 0.058 0.401* 0.236 0.160 0.148 Diplopoda 0.050 0.371* 0.148 0.077 0.094 0.442* Staphylinidae Ϫ0.093 0.161 0.183 0.344 0.157 0.601*** 0.167 Coleoptera 0.037 0.162 0.290 0.224 0.148 0.460* 0.178 0.870*** Note: Dissimilarity indices were calculated using families for Nematoda, Diplopoda, and Coleoptera; subfamilies for Staphylinidae; and species for Gastropoda. *, **, *** Correlation coef®cient is signi®cantly different from 0 at P ϭ 0.05, 0.01, and 0.001, respectively. ² Not determined on the basis of representing a spurious correlation. not correlated with the magnitude of reduction of plant in these groups more than others. In most instances, species richness across locations. The level of reduc- our third hypothesis was not supported because the tion of gastropod species richness by browsers was magnitude of effects of browsers on vegetation diver- comparable to that observed by Suominen (1999) for sity across the 30 locations did not correlate with the a series of browsing mammal exclosures in Scandi- magnitude of browser effects on soil animal diversity. navia. Our ®nding that the magnitude of response to This is probably in part because effects of browsers on browsing of gastropod and diplopod diversity was cor- plant diversity did not cause corresponding predictable related with the magnitude of browser effects on leaf shifts in habitat diversity. These results are consistent litter species diversity or litter layer habitat diversity with the ®ndings of Wardle et al. (1999) that loss of across all exclosures is consistent with earlier studies plant species from a plant community can either cause showing microarthropod diversity to be in¯uenced by increases or decreases in the diversity of soil organ- microhabitat diversity (Anderson 1978, Sulkava and isms, depending on the plant species removed, and sug- Huhta 1998). Even though browsing mammals reduced gests that different plant species may have substantially vegetation diversity in the browse layer across all 30 different effects on overall belowground habitat diver- locations, diversity of both coleopteran subfamilies and sity (Hooper et al. 2000). staphylinid subfamilies was enhanced by browsers (Ta- ble 6). Given that taxonomic richness of these groups Soil processes was not affected by browsers, this means that browsers In contrast to our fourth hypothesis, browsing mam- consistently reduced the population sizes of some taxa mals did not consistently reduce C mineralization (litter

TABLE 5. Multiple regression relationships relating values of the dissimilarity index D (calculated for determining dissimilarities of community structures inside vs. outside exclosures) for various taxa (including plant litter) to external environmental variables, across n ϭ 30 locations.

Dependent variables Independent variables in relationship² R2 P Litter (leaf species) TSH (ϩ); CNHI (Ϫ); PCOV (ϩ) 0.650 Ͻ0.001 Litter (habitat) TSH (ϩ); ͙ALTIT (Ϫ); BASAR (Ϫ) 0.621 Ͻ0.001 Humus Nematoda (families) SIR (Ϫ) 0.210 0.014 Litter Nematoda (families) ln(RP) (Ϫ); ACNL (Ϫ); LDISH (ϩ) 0.575 Ͻ0.001 Gastropoda (species) ln(RAIN) (Ϫ); SOLRAD (Ϫ); LDIS (ϩ) 0.531 Ͻ0.001 Diplopoda (families) DCLAREA (ϩ); BASAR (Ϫ) 0.407 0.001 Notes: Only terms that explain a statistically signi®cant proportion of the variation of the response variable at P ϭ 0.05 are included in each relationship. Coleopteran and Staphylinid relationships are not presented because no relationships were signi®cant at P ϭ 0.05. ²(ϩ)or(Ϫ) after a variable indicates a positive or negative relationship between the independent variable and the response variable. Abbreviations are as for Table 3; additional ones include: ACNL ϭ absolute value of proportional reduction by browsing of litter CN ratio; BASAR ϭ tree basal area (m2/ha); CNHI ϭ C-to-N ratio of humus inside exclosure; DCLAREA ϭ proportional reduction by browsing of litter C storage on an areal basis; LDIS, LDISH ϭ dissimilarity index (inside vs. outside exclosure) for litter leaf species community structure and litter habitat, respectively; RAIN ϭ mean annual precipitation (mm); SIR ϭ humus SIR inside exclosure. November 2001 BROWSING MAMMALS AND DECOMPOSERS 609

FIG. 12. Diversity indices for various groups of organisms (including litter) inside and outside of 30 browsing mammal exclosure plots. Symbols and legend are as for Fig. 2, but, for each panel, locations are arranged in order of decreasing effect of browsers on the diversity of plants in the browse layer (calculated as [(diversity inside exclosure) Ϫ (diversity outside exclosure)]/[diversity inside exclosure]). 610 DAVID A. WARDLE ET AL. Ecological Monographs Vol. 71, No. 4

TABLE 6. Diversity of plants, litter, and soil biota inside and outside exclosure plots, averaged across all 30 locations.

Shannon-Weiner diversity index Richness Biota Inside Outside t value P Inside Outside t value P Plant species (browse layer) 1.97 1.29 5.92 Ͻ0.001 6.45 3.99 5.77 Ͻ0.001 Plant species (ground layer) 0.89 0.88 0.08 0.935 2.36 2.36 0.01 0.989 Leaf litter species 1.89 1.80 1.50 0.144 5.46 5.51 0.18 0.861 Litter habitat diversity 1.29 1.19 1.45 0.145 ND ND ND ND Nematode families (humus) 2.16 2.14 0.47 0.643 15.3 14.9 0.86 0.396 Nematode families (litter) 2.12 2.05 1.16 0.254 14.4 13.8 1.58 0.125 Gastropod species (litter) 2.58 2.56 0.45 0.653 19.0 16.6 5.47 Ͻ0.001 Diplopod families (litter) 1.32 1.33 0.22 0.824 5.11 4.80 2.97 0.006 Staphylinid subfamilies (litter) 2.26 2.47 4.33 Ͻ0.001 8.04 7.98 0.56 0.581 Coleopteran families (litter) 2.35 2.58 4.12 Ͻ0.001 12.4 12.4 0.20 0.841 Notes: The t values were determined using paired t tests with n ϭ 30 locations (i.e., 29 df) except for the plant species (ground layer) in which only the 14 locations with a vegetated ground layer present were used. ND ϭ not determined. and humus respiration); indeed, relatively few locations ferent plant species which are eaten out by deer and showed signi®cant effects and the overall effect of goats across sites vary in their effects on storage of C browsers across the 30 locations was not signi®cant. and N. Earlier studies have shown that browsing effects on C and N mineralization can be negative (e.g., Pastor et Conclusions al. 1988, 1993; see also Ritchie et al. 1998), positive Our study failed to entirely support any of our four (e.g., McNaughton et al. 1988, Kielland et al. 1997), hypotheses, indicating that while the mechanisms pro- or neutral (e.g., Molvar et al. 1993, Burke et al. 1999), posed by Pastor et al. (1988, 1993) may have applied probably because of the varied ways in which browsers in some locations they clearly did not in others, and may affect soil organisms, especially those in the soil when the data was averaged across all 30 locations microfood web (Bardgett et al. 1998b and this study). there was little support for these hypotheses at least In this light, we also found no consistent effect of with regard to belowground processes and mechanisms. browsing mammals on litter or humus C and N storage Although browsing mammals had generally predictable on an areal basis. Although there were strong statis- effects aboveground, browser effects on the soil mi- tically signi®cant effects at several locations, these ef- crofood web and soil processes were idiosyncratic, and fects were idiosyncratic, again pointing to a range of the directions of effects were presumably governed by mechanisms with opposing effects on net soil C and N the balance of different mechanisms by which browsers sequestration. These mechanisms involve the effects of can potentially in¯uence the belowground system (see browsers on both soil biological properties and plant Bardgett et al. 1998b). The unidirectional response of species composition. There is evidence that forest plant the litter mesofauna and macrofauna to browsing, al- species can differ tremendously in their effects on be- though consistent with our hypotheses, is more likely lowground soil C and N storage (Binkley and Giardina to re¯ect physical effects of browsers than browsing- 1998, Finzi et al. 1998) and it is conceivable that dif- induced shifts in resource quality.

TABLE 7. Pearson's correlation coef®cients between taxa (including plant litter) with regard to browsing effects on the Shannon-Weiner diversity index, across n ϭ 30 locations.

Effect of browsing on diversity index of: Plants Litter Litter Effect of browsing on (browse (leaf (habitat Nematoda Nematoda Staphylini- diversity index of: layer) species) diversity) (humus) (litter) Gastropoda Diplopoda dae Litter (leaf species) Ϫ0.055 Litter (habitat diversity) 0.245 ND² Nematoda (humus) 0.466** 0.153 Ϫ0.255 Nematoda (litter) 0.120 0.042 0.190 0.004 Gastropoda 0.167 0.369* 0.250 0.185 Ϫ0.052 Diplopoda Ϫ0.061 Ϫ0.071 Ϫ0.574*** 0.279 Ϫ0.120 0.087 Staphylinidae Ϫ0.127 0.028 Ϫ0.088 0.187 0.127 0.169 0.183 Coleoptera 0.050 Ϫ0.100 Ϫ0.033 0.079 0.205 Ϫ0.162 Ϫ0.129 0.511** Notes: For each taxonomic group the data are expressed as ([diversity index inside exclosure] Ϫ [diversity index outside exclosure])/[diversity index inside exclosure]. Diversity indices were calculated using families for Nematoda, Diplopoda, and Coleoptera; subfamilies for Staphylinidae; and species for Gastropoda. *, **, *** Correlation coef®cient is signi®cantly different from 0 at P ϭ 0.05, 0.01, and 0.001, respectively. ² Not determined on the basis of representing a spurious correlation. November 2001 BROWSING MAMMALS AND DECOMPOSERS 611

Finally, our study enabled us to evaluate the effects The effects of agricultural practices on the soil biota of of an introduced functional group of organisms on the some upland grasslands. Agriculture, Ecosystems and En- vironment 45:25±45. structure and function of indigenous communities in Bardgett, R. D., S. Keiller, R. Cook, and A. Gilburn. 1998a. which that group was previously absent. Only a handful Dynamic interactions between soil animals and microor- of studies have considered how alien organisms affect ganisms in upland grassland soils amended with sheep key properties of indigenous communities and ecosys- dung: a microcosm experiment. Soil Biology and Bio- tems (i.e., invasive plants, Vitousek and Walker 1989; chemistry 30:531±539. Bardgett, R. D., and D. L. Leemans. 1995. The effects of invasive invertebrates, Beggs and Rees 1999, Carroll cessation of fertilizer application, liming and grazing on and Hoffmann 2000). As a result of its very recent microbial biomass in a reseeded upland pasture. Biology colonization by humans, New Zealand presents an op- and Fertility of Soils 19:148±154. portunity, unparalleled in most parts of the world, for Bardgett, R. D., D. A. Wardle, and G. W. Yeates. 1998b. investigating ecological consequences of introduced Linking above-ground and below-ground interactions: how plant responses to foliar herbivory in¯uence soil organisms. alien organisms. Our results demonstrate that the in- Soil Biology and Biochemistry 30:1867±1878. troduction of deer and goats to New Zealand forests Beggs, J. R., and J. S. Rees. 1999. Restructuring of Lepi- has caused far-ranging but often unpredictable effects doptera communities by introduced Vespula wasps in a at both the community- and ecosystem-level of reso- New Zealand beech forest. Oecologia 119:565±571. lution, with particularly adverse effects for indigenous Bengtsson, J., H. SetaÈlaÈ, and D. W. Zheng. 1996. Food webs and nutrient cycling in soil: interactions and positive feed- plant communities and populations of most groups of backs. Pages 30±38 in G. A. Polis and K. O. Winemiller, litter-dwelling mesofauna and macrofauna. editors. Food websÐintegration of patterns and dynamics. ACKNOWLEDGMENTS Chapman and Hall, New York, New York, USA. Binkley, D., and C. Giardina. 1998. Why do tree species We thank the following people for information enabling us affect soils? The warp and woof of tree-soil interactions. to relocate exclosure plots, for accompanying us on some of Biogeochemistry 42:89±106. our ®eld trips, or for help in sampling and backpacking soil Brookes, P. C., A. Landman, G. Pruden, and D. S. Jenkinson. and litter from the ®eld: Peter Abbott, Phil Alley, Nils Anthes, Bruce Burns, Larry Burrows, David Byers, Alison Evans, 1985. Chloroform fumigation and the release of soil ni- John Gow, Sean Husheer, Merilyn Merrett, Juha Mikola, trogen: a rapid direct extraction method for measuring mi- Claire Newell, Marcy and Rory Rowe, Bianca Ryburn, Karl crobial biomass nitrogen in soils. Soil Biology and Bio- Schasching, Mark Smale, Cam Speedy, and John von Tun- chemistry 17:837±842. zelman. John Leathwick provided the macroclimate data for Burke, I. C., W. K. Lauenroth, R. Riggle, P. Brannen, B. the thirty locations and Bianca Ryburn, Moira Dexter, and Madigan, and S. Beard. 1999. Spatial variability of soil Kate Orwin provided laboratory assistance. Anouk Wanrooy properties in the shortgrass steppe: the relative importance prepared the illustrations and Peter Bellingham, Bruce Burns, of topography, microsite and plant species in controlling and Claire Newell assisted with plant identi®cations. The spatial patterns. Ecosystems 2:422±428. New Zealand Department of Conservation is acknowledged Carreiro, M. M., and R. E. 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