Species Interactions in a Successional Grassland. I. Seed Rain and Seedling RecruitmentAuthor(s): D. R. PeartSource: Journal of Ecology, Vol. 77, No. 1 (Mar., 1989), pp. 236-251Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/2260927Accessed: 20/08/2010 00:04

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Journal of Ecology (1989), 77, 236-251

SPECIES INTERACTIONS IN A SUCCESSIONAL GRASSLAND. I. SEED RAIN AND SEEDLING RECRUITMENT

D. R. PEART

Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, U.S.A.

SUMMARY (1) Seed rain and recruitment for the five most abundant species of grasses were

quantified in a California coastal grassland undergoing succession after release from sheep grazing.

(2) Species distributions were very patchy, and four patch types accounted for about 950/o of total cover. Three patch types ('perennial patches') were dominated, respectively, by one of three species of perennial grasses, Anthoxanthum odoratum, Holcus lanatus or Deschampsia holciformis. The fourth type ('annual patches') was dominated by annual grasses, including the most abundant annual Vulpia bromoides, the perennial grass Rytidosperma pilosum and forbs.

(3) Dispersal limited the seed rain to the species dominating the local vegetation. Species not present in patches contributed little to the seed rain and nothing to recruitment in the interiors of those patches.

(4) Species differed significantly in the densities of their seed rain in the patches they dominated, ranging from 2300 m-2 for R. pilosum to 82 300 m-2 for H. lanatus. The density of seed rain was patchy on all spatial scales examined (from cm to km), but was not significantly correlated with densities of recruits on any scale for the perennial species. However, V. bromoides recruitment correlated positively with the density of its seed rain on small spatial scales (up to 1 mi2) in annual patches. The poor relationship between seed rain and recruitment for the perennials probably reflects the over-riding importance of adult interference as an influence on seedling establishment in the perennial vegetation.

(5) A. odoratum had relatively high recruitment (30 m-2) in the patches it dominated. Other perennials had very low recruitment in their own stands (less than 5 m-2). V. bromoides had the highest recruitment (904 m-2) in annual patches.

(6) The seed bank contribution to recruitment was estimated using seed exclosures. Only those species abundant in the seed rain and in the local vegetation recruited inside the seed exclosures, i.e. there was no evidence of a persistent, functional seed bank of other species. The seed bank could account for no more than 30/o of V. bromoides recruitment in annual patches. However, establishment in the seed exclosures overestimated recruitment from the seed bank for A. odoratum and possibly for other perennial species

(7) The implications of the results for population dynamics and succession are discussed.

INTRODUCTION To understand the dynamics of change in plant communities, one must understand the population flux of the species in the community. The availability of propagules and the conditions affecting seedling establishment are crucial to our understanding of mecha- nisms controlling the abundances of adult plants (Harper 1977; Grubb 1977; Grubb, Kelly & Mitchley 1982). This is especially true for species that have low potential for vegetative expansion. To understand the dynamics of any single plant population it is, therefore, essential to quantify seed rain and recruitment as well as patterns in the

236

D. R. PEART 237

established vegetation. Further, because seeds and seedlings of most populations frequently encounter individuals of other species, a community-level study is needed to evaluate the importance of seed rain and recruitment for population dynamics and population interactions. The seed rain of a community has been documented in a few cases; in forest understorey (Wagner 1965; Falin'ska 1968), early glacial succession (Ryvarden 1971) and in grassland (Rabinowitz & Rapp 1980). Reader & Buck (1986) found that patchiness in the distribution of Hieracium in abandoned pasture could be explained partly by heterogeneity in the seed rain. However, there appears to be only one detailed community study that reports both seed rain and recruitment. Working in annual grassland, Hobbs & Mooney (1985) were able to explain the different abundances of species on gopher mounds and undisturbed vegetation in terms of seed input and seedling establishment. Their spatial comparisons of population flux were mainly between disturbed and undisturbed sites.

There are apparently no studies relating local seed-rain density to local abundance in the vegetative community, or evaluating the density response of natural recruitment to spatial variation in seed-rain density. In this paper, I examine the detailed spatial relations between abundances of species in the mature vegetation, in the seed rain, and in the ensuing cohort of seedling recruits in a grassland community dominated by five grass species. Unlike many perennial-dominated grasslands, where most grass reproduction is vegetative (Harberd 1961, 1967; Tamm 1948, 1956), the perennial grasses in this community rely on seeds for reproduction.

Of course, recruitment may also arise from the seed bank, whose distribution in space may differ from that of the seed rain (e.g. Thompson 1986), because the seed bank is formed from the seed rain in past years, and because the conditions affecting the germination and viability of seeds in the seed bank may differ from place to place. Spatial relations are even more complex when several species co-occur, and when the activities of seed predators, herbivores or physical disturbances have localized effects. It is not surprising that patchiness in distributions makes even a rudimentary theoretical treatment of population interactions difficult (Schaffer & Leigh 1976). This and related papers attempt to demonstrate (Peart 1989a, b) that patchiness can be used to advantage in field studies of species interactions. Spatial structure in the mature vegetation is a useful reference for examining the spatial relations between the vegetative dominants and the seeds and seedling recruits that they produce.

The main questions addressed in this paper are: (i) Does the composition of the local seed rain closely reflect the composition of the local vegetative community, or does dispersal break down the patchiness evident in the reproductive adults? (ii) How are the species composition and abundance of recruits related to the seed rain and the vegetative community within patches? (iii) How is the seed bank contribution to recruitment related to the seed rain and the vegetative community within patches? Does the seed bank contribute substantially to recruitment? (iv) What are the implications of the spatial patterns of seed rain and recruitment for population interactions and successional change?

THE STUDY SITE

The study site is at Sea Ranch, Sonoma County (38?40'N, 123?24'W), on the coast 200 km north of San Francisco, CA, U.S.A. The vegetation of this area is coastal prairie (Heady et al. 1977; Hektner & Foin 1977a) and occupies the terraces between the coast ranges and

238 Seed rain in grassland

the ocean. The climate is mediterranean, with mean monthly temperatures ranging from 6 5 ?C to 15 ?C (Davidson 1975). Mean annual rainfall at Fort Ross, 31 km south of Sea Ranch, is 103 cm, 94% of which falls between October and April (U.S. Environmental Data and Information Service 1951-1975).

In 1968, sheep were removed from a section of the coastal terrace, 17 km long and 2 km wide, which is now undergoing post-grazing succession (Hektner & Foin 1977b; Foin & Hektner 1986). The study sites are located in the northern third of this area, where most land was protected from development. Grasses account for most of the cover, and there has been an increase in the absolute cover of both perennial and annual grasses since 1974. The percentage of bare ground has declined. Foin & Hektner (1986) found an increase in the relative cover of perennial bunchgrasses and a decline in relative cover of forbs and annual grasses. This paper examines the five species that now have highest cover: Anthoxanthum odoratum, Deschampsia holciformis Presl. (the only native), Rytidosperma pilosum (R. Br.) Connor et Edgar, Holcus lanatus and Vulpia bromoides S.F. Gray. Henceforth, these species will be referred to by their generic names only. All are perennial bunchgrasses except Vulpia, which is an annual grass. Nomenclature follows Munz (1973) throughout, except where authorities are cited.

Total absolute cover at most locations exceeds 100%. Typical canopy heights are 25 cm in annual patches and 60 cm in perennial-dominated areas. Maximum root penetration is 60 cm and varies little among patch types (Peart 1982). Germination begins after the first rains in autumn (usually October). The soil, a sandy loam underlain by sand at 60 cm, remains moist during the winter and begins to dry from the surface downwards in the spring. The grasses flower from April until June and produce seed from May until July. Perennials go dormant early in the summer and regenerate in the autumn. These general patterns in rainfall and phenology are very predictable from year to year.

Species distributions within the community are very patchy. Each of three patch types is dominated ( > 85% of total cover) by a single perennial (Anthoxanthum, Deschampsia or Holcus). Annual grasses are associated with forbs in a fourth distinct type of patch, referred to as an annual patch. Rytidosperma is found almost exclusively amongst the annuals in these annual patches. Patches are obvious in the field, the largest being up to 500 m2 in area. Smaller patches are common, the smallest 'patch' being a single bunchgrass, which can be up to 30 cm in foliage diameter; however, most individuals of Anthoxanthum, Holcus and Deschampsia have conspecific neighbours. In a representative 4-ha plot, 28% of the area consisted of patches between 9 m2 and 200 m2 in size, 48% consisted of patches between 200 m2 and 500 m2, and the remainder consisted of smaller patches and areas where individuals of different species were intermixed. The four perennial grasses all form discrete individual bunches, and no evidence was found from excavations of more extensive vegetative growth. Thus it is concluded that the patches are formed from seedling establishment. The species dominating local areas will be referred to as the 'resident' species; in annual patches both Rytidosperma and Vulpia are residents. Hektner & Foin (1977b) and Foin & Hektner (1986 and unpublished data) have sampled at several locations near the study sites. The five species studied account for 77% of total cover in this area, with Anthoxanthum contributing 43%, Holcus 7%, Deschampsia 5%, Rytidosperma 14% and Vulpia 8%. A further 18% is contributed by annual grasses (other than Vulpia) and forbs in the annual patches, and by forbs in perennial patches. The species comprising the four patch types, therefore, account for about 95% of total cover. The remaining 5% is mostly Rubus ursinus and Lupinus arboreus. Because perennials are apparently increasing in abundance during succession, and Vulpia is the most abundant

D. R. PEART 239

annual, it was possible to examine most of the spatial patterns that are important in the dynamics of the community by measuring seed rain and recruitment of the five most abundant species in each of the four patch types.

Although domestic animals had been removed, the area was accessible to native grazers, including black-tailed deer (Odocoileus hemionus), jackrabbits (Lepus californi- cus), meadow voles (Microtus californicus), pocket gophers (Thomomys bottae) and grasshoppers. Potential seed predators were meadow voles, birds and ants. All potential grazers and seed predators were much more abundant in annual- than in perennial- dominated patches (personal observation). Ants were not a conspicuous part of the soil fauna anywhere. There appeared to be no field evidence or other records of fires in the study area, although fires do occur frequently on the nearby ridges of the coast ranges.

METHODS

Sampling design

Three patches of each type, all between 200 m2 and 500 m2 in size, were chosen within an 8 km x 1 km area for detailed monitoring. Patches of this size account for much of the study area, and are large enough to accommodate an adequate sampling scheme. Boundaries of patches were defined as perimeters beyond which the resident species contributed less than 85% relative cover. The three patches were deliberately chosen to differ from one another is size, slope, aspect and the relative abundances of species bordering the patches, so that conclusions from the study could be generalized to other patches of similar size. Within each vegetation type, aboveground biomass appeared quite uniform in most areas, but vegetation was visibly less dense in some sites, especially in some Deschampsia and annual patches. One of the three patches of each type was deliberately chosen to represent low biomass areas.

Seed-rain samples were organized into 'stations' and 'locations' within patches, so that seed rain could be examined on several spatial scales. For each patch type, one typical biomass patch was sampled most intensively, containing eleven sampling stations, while the remaining two patches were sampled at five stations. Stations were placed 3-6 m apart, approximately evenly over each patch, and at least 2 m inside the patch boundary. Stations consisted of a cluster of three locations at the apices of an equilateral triangle of side 60 cm. Locations were rejected if they included part of the basal area of a bunchgrass. In that case, the triangular sampling scheme was rotated (randomly clockwise or anti- clockwise) until locations were above bare soil. One 10 cm x 10 cm seed trap, to measure seed rain, and one 11 cm x 11 cm seed exclosure, to measure the contribution of the seed bank to recruitment, were placed at each location. In summary, there were three patches, containing twenty-one stations (five + five + eleven), with three locations per station, for a total of sixty-three sampling locations in each of the four patch types. The total number of sampling locations was, therefore, 63 x 4 = 252. The same locations were used to sample both Rytidosperma and Vulpia seeds in the annual patches.

All sampling was done in the interiors of patches, because (i) this allowed more control over vegetation type in the experimental design, (ii) the access of seeds to sites within patches could be evaluated, and (iii) the patterns of seed rain and recruitment in boundary

240 Seed rain in grassland

zones between patches were likely to be intermediate between those in the interiors of neighbouring patches.

Field methods

In each patch, the percentage cover of all species present was estimated in ten 0 25-m2 quadrats, with two quadrats adjacent to each of five stations. These stations were chosen at random in those patches with more than five stations. Cover was estimated visually at the end of the 1980 growing season, with the aid of a 50 cm x 50 cm quadrat frame divided by wires into nine equal parts. Aboveground biomass was estimated for each of the twelve patches by harvesting the vegetation at the end of the 1980 growing season in three randomly chosen 50 cm x 50 cm quadrats. The foliage was dried for twenty-four hours at 80 ?C in a forced-air oven and weighed.

Stations were permanently marked with metal stakes and flags. Seed traps were 10 cm x 10 cm stiff-cardboard squares covered with a paper grid and a layer of clear polyethylene. The polyethylene surfaces were coated with a sticky resinous substance (Tanglefoot Co., Grand Rapids, Michigan) to retain seeds, and the traps placed at the sampling locations before natural seed-fall in 1980. To test efficiency of seed capture, seed traps were placed in the field and seeds artificially dislodged from surrounding inflorescences. All seeds landing on seed traps were securely captured unless the cover of seeds on the traps approached 100%. Seeds captured on traps were marked with a fluorescent dye. After six weeks, no dyed seeds were found in the vicinity of the test traps, and seeds on the traps were still securely held. The condition of the traps used for sampling was checked frequently and, to ensure capture efficiency, traps were replaced every four weeks, or earlier if seed cover on them reached 75%. Seed-fall was sampled from 1 May until 30 September, except for Holcus, which was sampled until 30 October because of its longer seed retention.

The contribution of the seed bank to recruitment was estimated by excluding seeds from areas during the seed-fall period, and then recording the numbers of recruits in the exclosures. Exclosures were made from waxed cardboard milk cartons, sliced to form 11-cm square boxes open at the top and bottom and 2 cm tall. The tops were covered with 0 7-mm nylon mesh during the seed-fall period. One exclosure was secured at each location with metal stakes, and the surface of the soil scored with a thin blade at the base of the exclosure so that its base was 1 cm below the soil surface. This was done to ensure that weeds were not transported under the edges of exclosures during the heavy autumn rains. A seed trap was placed over each exclosure, so that recruitment from the seed bank was measured in the same locations as was the seed rain. The seed traps excluded light and direct precipitation as well as seeds, but the mesh and traps were removed after seed-fall, before any seedling emergence occurred. At the time of seedling emergence, soil appeared close to saturation, both inside and outside the exclosures.

Natural recruitment (i.e. where natural seed-fall was allowed to occur) was measured by counting all individuals that established and survived to the end of the growing season, i.e. to June 1981. Perennial recruits in the twelve patches were counted in three 50 cm x 50 cm quadrats, each adjacent to a randomly chosen station. Natural recruitment of Vulpia was measured at each location in the annual patches by counting individuals in perimeter strips (4 cm wide and 240 cm2 in area) that surrounded the exclosures and seed traps. Thus, natural recruitment for perennials was measured at the scale of a station, while seed rain and recruitment of Vulpia from the seed bank were measured at a finer

D. R. PEART 241

spatial scale, at the location level. Natural recruitment was not sampled at the location level for the perennials, because of their low recruitment rates per unit area. In the same 50 cm x 50 cm quadrats where recruitment of perennials were measured, seed production of the resident species was monitored in 1980 and 1981 by counting the number of seed heads produced.

To evaluate the potential importance of post-dispersal seed removal by animals, a seed removal experiment was done in the annual-patch vegetation, where potential seed predators (mainly meadow voles) were most abundant. For each of the five species, five plastic Petri dishes, each containing 100 seeds, were placed randomly in an annual patch during the late summer when naturally dispersed seeds were abundant on the soil. The dishes were set into the surface litter so that their upper rims were flush with the litter surface. After two weeks, the dishes were removed and the number of seeds remaining in each was recorded. There was no rain during this period and field tests showed that even the strongest winds could not disturb the seeds in the dishes. Seeds were much more visible in the dishes than in the litter, because naturally dispersed seeds fall between fragments of litter. Further, mechanical disturbance by animals would tend to add litter to the dishes, but reduce the numbers of seeds in them. Therefore, actual seed removal rates by predators should be less than or equal to those estimated in this experiment.

The SAS statistical programs (Statistical Analysis Institute 1986) were used for all analyses.

RESULTS

Vegetative cover In the patches sampled, Anthoxanthum, Holcus and Deschampsia dominated their

respective patch types with 92%, 91 % and 86% relative cover, respectively (Table 1). In annual patches, Rytidosperma and Vulpia contributed 35% and 20%, respectively, with annual grasses other than Vulpia making up 24% relative cover. Aira caryophyllea (17%) was the second most abundant annual grass. Perennial forbs accounted for 17% relative cover in the annual patches, mostly Plantago lanceolata (11%). Relative cover of species was similar among patches of different biomass in each perennial patch type. However, the lowest biomass annual patch had the lowest mean relative cover of Vulpia (14% compared with 24% for typical biomas patches) and of Rytidosperma (29% compared with 38%).

Biomass of vegetation Mean aboveground biomass was not significantly different between the two typical

biomass patches in any patch type (t-tests), so data for the two typical biomass patches were pooled. In all four patch types, the patch selected for low biomass had significantly lower biomass than the other two (Table 2). The ratio of mean aboveground biomass in low compared to typical biomass patches was 0 38 in Deschampsia patches, 0 50 in annual patches, 0 71 in Holcus patches and 0-86 in Anthoxanthum patches. Bare ground contributed a higher proportion of total area in low than in typical biomass patches of the same type. This difference was significant in all except Anthoxanthum patches (Table 2).

Seed rain A total of 127 523 seeds of the five species studied were collected from the 252 seed-trap

locations and identified. Seeds of other species were not counted, but those falling in

242 Seed rain in grassland

TABLE 1. Mean relative cover (%) of species in four patch types in a grassland at Sea Ranch, California. Data are pooled from two typical biomass patches and one low biomass patch in each patch type. n = nine quadrats, each 0-25 m2, in each patch

type.

Patch type Species Anthoxanthum Holcus Deschampsia Annual Anthoxanthumodoratum 92 4 1 8 5 2 Holcus lanatus 90 8 4.6 Deschampsia holiformis 86 0 Rytidosperma pilosum 1.5 2 3 35 3 Vulpia bromoides 1.2 20 3 Aira caryophyllea 16 9 Plantago lanceolata 0 8 0 7 11 0 Iris douglasiana 1 4 Bromus mollis 3.8 Linum bienne 22 Cynosurus echinatus 2.0 Carex sp. 0 5 Rumex acetosa 0 3 1 3 1 8 Hypochaeris radicata 1 5 Lolium perenne 0 7 Rubus ursinus 4 9 1 8 0 8 0 6 Pteridium aquilinum 0 9 0 8 0 6 Bromus diandrus 0 5 Leguris sp. 0 5 Other species* 2 3 Total 100 0 100 0 100 0 100 0

* Each contributed less than 0 50/o relative cover.

perennial patches were almost exclusively Rumex acetosa, and these contributed less than 5 % of the total (estimate from a random subsample). In annual patches, Vulpia seeds were the most abundant, but many species of forbs and grasses were represented, principally Aira caryophyllea, R. acetosa, Plantago lanceolata and Bromus mollis. Thus almost all seeds falling in perennial-dominated patches were counted, but a substantial part of the seed rain in annual patches was not quantified. Nevertheless, the contributions to the seed rain by the five species sampled can be compared to their relative abundances in the vegetation of annual patches.

TABLE 2. Aboveground biomass of vegetation and percentage bare ground in four patch types in a grassland at Sea Ranch, California (means + 1 S.E.). For aboveground biomass, n = three in low biomass patches, and n = six in typical biomass patches. For bare ground, n = ten quadrats in low biomass patches and n = twenty quadrats in typical biomass patches; all quadrats were 0-25 m2.

Percentage cover data were arcsin transformed for analyses.

Aboveground biomass (g dry wt 0 25 m-2) Bare ground ('o) Patch type Low Typical Significance Low Typical Significance

Anthoxanthum 258+ 162 299+82 t=2-5,d.f.=7,P<005 27+ 13 20+ 1-7 t=08,d.f.=28,P>04 Deschampsia 153 +235 398+ 188 t=77,d.f.=7,P<0001 11-5+30 0-2+01 t=41,d.f.=28,P<0001 Holcus 205+76 290+87 t=62,d.f.=7,P<0001 84+ 19 1 6+ 15 t=3 3d f.=28,P<001 Annual 71+52 142+60 t=76,d.f.=7,P<0001 21 5+4-1 7-1+2-1 t=38,d.f.=28,P<0001

D. R. PEART 243

100 _ (a) 80000 75 ^ - 60000 50 - _ 40 000 25 - _ 20 000

100 ( (b) -100000 75 - - 75 000 50 - - 50000 X, 25 _ - 25 000

c0

IO10 (C) -40000 ? 75 6 30 00? 50 - - 20 000 Z'

25 _* _ _10 000

1 00 ( d) -8000

75 - - 6000

50 - - _:4000

FIG. 1. Percentage relative cover (solid bars) and density of seed rain (open bars) for five dominant grass species, in vegetation patches in a grassland at Sea Ranch, California. (a) Anthoxanthum patches; (b) Holcus patches; (c) annual patches; (d) Deschampsia patches. Relative cover based on

total cover of all species present.

The seed rain was very different among perennial patch types. The relative abundances of species in the seed rain closely matched their abundance in the local vegetative community in both Anthoxanthum and Holcus patches. Where Anthoxanthum dominated the vegetation (92% relative cover), it also dominated the seed rain (Fig. la). Similarly, in Holcus patches, Holcus accounted for 91 % relative cover and dominated the seed rain (Fig. Ib). In annual patches, the seed rain of the five species sampled was dominated by the two that were the main resident species in annual patches. However, the seed rain of these species was not in proportion to their cover. Although Vulpia had only 20% relative cover, compared with 35% for Rytidosperma, the density of Vulpia seeds was 13 times that of Rytidosperma (Fig. Ic).

In contrast to the other perennial-dominated patches, there were marked differences between species' abundances in the seed and vegetative communities in Deschampsia patches (Fig. Id). Deschampsia dominated the vegetation (86% relative cover), but not the seed rain. In spite of their low cover, the seed rain of Anthoxanthum and Holcus in Deschampsia patches were each about equal to that of Deschampsia.

244 Seed rain in grassland

TABLE 3. Spatial heterogeneity in the seed rain of five dominant grass species, in vegetation patches in a grassland at Sea Ranch, California. Values are percentages of variation in seed-rain density attributable to differences among patches, stations within patches, and locations within stations. Separate nested ANOVA for each

species, d.f. = 62.

Species Patch type Patch Station Location Total Anthoxanthum Anthoxanthum 39 2 31 6 29 2 100 Deschampsia Deschampsia 56.7 19 5 23 8 100 Holcus Holcus 62-9 27-3 9 8 100 Rytidosperma Annual 43-8 24-0 32-2 100 Vulpia Annual 38.8 22-0 39-2 100

Mean 48-2 24 9 26 9 100

The maximum seed rain densities produced by each secies (i.e. within the patch types where they were the vegetative dominants) differed significantly (one-way ANOVA with log transformed data, F4,62 = 242, P < 0-00 1). The rankings were Holcus > Anthoxanthum > Vulpia> Deschampsia> Rytidosperma (all comparisons denoted > were significant by Tukey's multiple-comparison test, P < 0 05). There was more than one order of magnitude difference between Holcus, with a mean of 64 285 seeds m-2 in Holcus- dominated patches, and Rytidosperma, with a mean of 2 263 m-2 in annual patches.

Spatial variation in the density of the seed rain was examined separately for each resident species, using nested ANOVA (Table 3). Over all species, differences among patches contributed an average of 48% of the total variance in seed-rain density. Differences among stations contributed 25%, and differences among locations 27% of the total variance. Some of the differences among patches were associated with differences in biomass: the seed-rain density of resident species was significantly less in the low than in the typical biomass patches for Deschampsia, Holcus, Rytidosperma and Vulpia (t = 2 6- 34, d.f.=61, P<005). Anthoxanthum seed-rain density did not differ significantly between low and typical biomass patches (t = 1 2, d.f. = 61, P > 0 2) but, as noted above, the difference in biomass between low and typical biomass patches of Anthoxanthum was less than for other patch types.

Seed removal There were no significant differences among species in the proportions of seeds

removed from Petri dishes in annual patches (one-way ANOVA with arcsin transformation, F4,20 = 1 1, P> 0 1). The mean percentages of seeds remaining in Petri dishes after three weeks were Anthoxanthum 89%, Deschampsia 95%, Holcus 94%, Rytidosperma 93% and Vulpia 93%. Thus, post-dispersal seed predators apparently remove only a small proportion of seeds of any species.

Recruitment In all patch types, the recruits (Table 4) were the same species that dominated the seed

rain (Fig. la-d). In Anthoxanthum-dominated and Holcus-dominated patches, only the dominant species were recruited. Similarly, in annual patches, the only perennial grass recruits were Rytidosperma, the dominant bunchgrass in those patches. In Deschampsia patches Deschampsia, Anthoxanthum and Holcus recruited; each of these species was well represented in the seed rain (Fig. Id), and present in the local vegetation (Table 1).

D. R. PEART 245

TABLE 4. Natural recruitment of seedlings m-2 (mean+ 1 S.E.) of five dominant grass species, in vegetation patches in a grassland at Sea Ranch, California. n = nine quadrats (each 0 25 M2) in each patch type, except for Vulpia in annual patches,

where n = sixty-three perimeter strips (each 240 cm2, see text).

Patch type Species Anthoxanthum Holcus Deschampsia Annual

Anthoxanthum 302 +15 20 409 +19 9 0 Holcus 0 1 8+1 8 120+59 0 Deschampsia 0 0 31 ?+22 0 Rytidosperma 0 0 0 4 9+?16 Vulpia 0 0 0 904 1+74.8

However, Anthoxanthum and Holcus outnumbered Deschampsia among the recruits in Deschampsia patches. The annual Vulpia had the highest density of recruits, with a mean of 904 m-2 in annual patches. No Vulpia recruits were found under Rytidosperma canopies in any of the quadrats. Species other than the five studied did not recruit in any of the perennial-dominated patches. However, other common species in the annual patches, principally Aira caryophyllea, Rumex acetosa and Plantago lanceolata, did recruit both inside and outside the seed exclosures.

Among species, there was no significant correlation between the density of recruits and the density of the seed rain. The result was similar within species for the perennials; seed- rain density was not significantly correlated with the density of recruits for any perennial species on any spatial scale measured, i.e. among stations or among patches. For Anthoxanthum, the non-significant r values were negative in each of the three Anthoxanthum patches. In contrast, recruitment of the annual Vulpia was significantly and positively correlated with seed-rain density, both at the location level (r=0 31,

3000 -(a) r2 ,=o-os p< 0-05

2000 -

1000 --8

N 0 5x0 O?Ix0 E

0 5 x 104 105 16 5 x 105 a)

- 2000- (b)

z1 500 -

1000 - o as 0 r2 0-22

500 ooP<0 05

0 2 X104 4 x104 6 x104 8 x104

Number of seeds (m2)

FIG. 2. Relation between seed-rain density and the density of recruits for Vulpia bromoides, (a) at the location level, (b) at the station level. r2 and P values are for linear correlations.

246 Seed rain in grassland

TABLE 5. Seedling recruitment (m-2) inside seed exclosures for five dominant grass species, in vegetation patches in a grassland at Sea Ranch, California. Values are

means+ 1 S.E, n = sixty-three exclosures (each 121 cm2) in each patch type.

Patch type Species Anthoxanthum Holcus Deschampsia Annual

Anthoxanthum 194+293 1.1+1.1 46-0+?81 0 Holcus 0 2-6 + 2-6 3-9? 1*8 0 Deschampsia 0 0 7.6+3 2 0 Rytidosperma 0 0 0 1 3+1 3 Vulpia 0 0 0 27 5 + 1-8

P < 005; Fig. 2a) and at the station level (r = 047, P < 05; Fig. 2b), although the percentage of total variation in the density of recruits that was explained by seed-rain density was only 9% at the scale of locations and 22% at the scale of stations. On the scale of whole patches, the rankings of Vulpia seed-rain density and recruitment did not correspond.

The species composition of recruits was the same in the seed exclosures as in the quadrat samples of natural recruitment. In each patch, recruitment from the seed bank was limited to those species present in the local vegetative community and the previous year's seed rain. Recruitment of Vulpia in the annual patches was much less in the exclosures (mean=28 m-2; Table 5) than natural recruitment (mean=904 m-2; Table 4, t=3 5, d.f. = 124, P < 0-001). However, recruitment of Anthoxanthum in Anthoxanthum patches was higher in the exclosures than in the quadrats (t = 2-6, d.f. = 70, P < 005), so the density of recruits in the exclosures obviously overestimated the seed bank contribution to natural recruitment for this species. Mean recruitment in exclosures was also higher than natural recruitment for Anthoxanthum and Deschampsia in Deschampsia patches, but not significantly so.

As noted above, seed-rain density was greater in the typical than in the low biomass patches for all resident species except Anthoxanthum. Nevertheless, only Vulpia had significantly more recruits in typical compared to low biomass patches (t = 3 2, d.f. = 61, P < 0-05). There were actually fewer recruits in the typical than in the low biomass patches for both Deschampsia and Holcus, although the differences were not significant.

Variation in seed production between years Seed-head production in 1980 was not significantly different from that in 1981 for any

resident species (t = 0-4-0-9, d.f. = 16, P > 0 2). The mean numbers of seed heads 0-25 m-2 in 1980 and 1981, respectively, were Anthoxanthum, 367 and 333; Holcus, 152 and 203; Deschampsia, 29 and 22, and Rytidosperma, 26 and 27.

DISCUSSION

Local areas of the grassland were heavily dominated by one or a few species. The species composition of the seed rain was also very heterogeneous in space and reflected the species composition of the locally dominant vegetation in patches. That seed rain within patches

D. R. PEART 247

included only patch-resident species indicates that limited dispersal prevents species outside patches from gaining access to the interiors of those patches. Dwire (1983), working in the same grassland, demonstrated that the invasion of annual patches by Anthoxanthum was limited by the dispersal of Anthoxanthum seeds. Dispersal limitation in the seed rain was reflected in recruitment: inside all patches except those dominated by Deschampsia, only the locally dominant species recruited. Even in Deschampsia patches, all species of recruits were present in the patches as reproductive adults.

For each of the main species, the relationships between dominance in the mature vegetative commnity, dominance in the seed rain and dominance in recruitment were examined. Because of limited dispersal, dominance in these three life-history stages tends to be concentrated in the same species within patches. In Deschampsia patches, unlike the other patch types, the relative contributions of species depended strongly on the life- history stage considered. The minority species in the vegetation, Anthoxanthum and Holcus, contributed equally with Deschampsia to the seed rain (Fig. ld), and outnum- bered the vegetative dominant Deschampsia among the recruits (Table 4). This pattern suggests that Anthoxanthum and Holcus may be invading Deschampsia patches as succession proceeds, although it does not provide direct (i.e. dynamic) evidence of an invasion process.

The seed rain for all species was variable even within patches (Table 3). For the annual, Vulpia, some of this variation in seed-rain density was associated with variation in recruitment (Fig. 2a, b), but this was not so for the perennials. The absence of a relationship between the densities of seeds and recruits for the perennials may, in part, be due to the small sample sizes resulting from their low rates of seedling recruitment. However, it is also likely that, because higher biomass vegetation was associated with higher seed-rain density, the inhibitory effect of vegetation on seedling recruitment tended to compensate for high seed inputs. New recruits should experience more interference from the established vegetation in perennial than in annual patches, because of the higher cover, biomass and height of perennial vegetation, especially early in the growing season before the annuals attain their maximum size. Other workers have noted the lack of a strong relationship between recruitment and density of seed input in closed swards. Symonides (1979) found a poor relation between seed producton and seedling establishment in the tussock grass Corynephorus canescens. Putwain, Machin & Harper (1968) and Gross (1980) found no effect of increased seed input on the recruitment of Rumex acetosella or Verbascum thapsus, respectively.

In contrast to the perennial-dominated vegetation, 45% of the vegetative cover in annual patches was due to annuals (Table 1), representing space unoccupied by living vegetation at the beginning of the growing season when potential recruits germinate. Compared to recruitment of perennials in perennial-dominated vegetation, Vulpia recruitment in annual patches should be more influenced by seed-rain density and less influenced by biomass of vegetation. Vulpia recruitment was, in fact, highest in the annual patches of highest biomass, where the highest seed-rain density of Vulpia occurred, and a significant positive correlation between seed-rain density and density of recruits was found for Vulpia (Fig. 2).

Interference among the recruits themselves would be expected to follow the reverse pattern. Such interference should be greater in annual than in perennial patches, because of the higher density of recruits in the annual patches. The recruitment data indicate that intraspecific interference among Vulpia recruits was likely. Vulpia recruits dominated the annuals in annual patches, and were found at a mean density (averaged over locations) of

248 Seed rain in grassland

904 m-2, thirty times denser than recruitment of any of the perennial species. Further, the mean local density of conspecifics experienced by individual Vulpia recruits was 1248 m-2, 38% higher than the overall spatial average. The mean experienced density was calculated by weighting the density recorded in each 240-cm2 sampling location by the number of individuals found there (Lloyd 1967). The disparity between these means reflects aggregation in the distribution of Vulpia within the annual patches, and clearly this aggregation increases the potential for intraspecific interference. However, the relationships between density of recruits and density of seed rain for Vulpia (Fig. 2) do not clearly indicate density-dependent mortality. Much of the scatter in Fig. 2 may be attributable to interactions between Vulpia and other, less abundant annuals, whose density varies in space. Inhibition by Rytidosperma also contributed to spatial variability in the relationship between seed rain and recruitment, because no Vulpia recruits established under Rytidosperma individuals in the annual patches. Density-dependent effects in Vulpia may well be absorbed in individual seed production, without extensive mortality. Watkinson & Harper (1978) found that at densities of Vulpiafasiculata above 100 m-2, the number of spikelets per plant, but not survivorship, was inversely related to plant density. Such plastic responses may be quite common in plant populations (Watkinson 1985). The low rate of seed removal from Petri dishes in the field suggests that seed predation or seed caching by animals probably do not substantially influence the relationships between local seed-rain density and local recruitment that were examined in this study.

Because only those species abundant in the local seed rain were found as seedlings in the seedling exclosures, there was no evidence of a functional seed bank of species that formerly occupied sites, as found, for example, by Rabinowitz (1981) and Major & Pyott (1966). In this community, the species composition of the seed rain was a good predictor of the species composition of natural recruitment, at least in the absence of major disturbance. The usual method of examining the seed bank is by counting viable seeds in the soil or the seedlings emerging from soil samples (Harper 1977; Thompson & Grime 1979; Thompson 1986). This method is appropriate for characterizing the seed bank community and its potential contribution to the vegetative community (Major & Pyott 1966). However, the actual contribution of the seed bank to recruitment in any one year will be much less than the total number of viable seeds in the soil, because recruitment from the seed bank depends on a complex of environmental factors and the requirements of species for germination and early survival (Silvertown 1980; Thompson & Grime 1983; Gorski, Gorska & Norwicki 1977; Slade & Causton 1979).

The approach taken here differs in that the current year's seed rain was excluded, and recruitment measured in situ inside the exclosures. This method seems more appropriate than seed counts or greenhouse germination studies for estimating the actual seed-bank contribution to natural recruitment. However, the seed-bank contribution to recruitment in perennial patches was clearly overestimated by the seed-exclosure method, because Anthoxanthum recruits were more numerous inside the exclosures than outside. Although care was taken to minimize disturbance to the canopy, the manipulations inevitably increased light penetration and changed its spectral quality for a short time (about 30 min) and this may have stimulated germination. Another possible experimental artefact was the slight disturbance of the soil surface where the exclosures were placed. Both soil disturbance and placement of objects can influence emergence (e.g. Harper, Williams & Sagar 1965). However, recruits inside and outside the exclosures were not concentrated at or near the edges, for any of the species examined (personal observation).

D. R. PEART 249

Anthoxanthum recruitment in the exclosures was 40-50 times higher than that of the other perennials (Table 5). The results indicate that a persistent, functional seed bank for Anthoxanthum exists, and suggests that recruitment of this species is sensitive to minor canopy disturbance. The contribution of the seed bank to Vulpia recruitment in annual patches was estimated to be about 3% from the seed exclosure experiment. Three percent may be an overestimate, because interference was probably reduced inside the exclosures, due to lower seedling densities there. Based on a very detailed study of spatial heterogeneity in the seed bank, Thompson (1986) suggested that most studies involve too few samples, and recommended a minimum of fifty soil samples for the greenhouse- emergence method of evaluating seed banks. For the in situ method used in this study, 263 samples were obtained, stratified by vegetation type. However, because of the relatively low recruitment rates expected in the field compared with rates of emergence from soil samples in the greenhouse, and because of the substantial variability evident in the results of Table 5, it is suggested here that sampling for in situ evaluations of seed bank contributions to recruitment should probably be even more extensive than for the greenhouse-germination method.

An obvious limitation of a short-term, intensive study of seed rain and recruitment is that patterns may vary from year to year. While such variation undoubtedly occurs in this community, it is probably much less than in many other plant communities. The seasonality in rainfall is very predictable. Although rainfall in 1980 was near average for the area, and 1981 was an unusually wet year, seed production by the five species studied did not change significantly from 1980 to 1981. Finally, successional change over the period 1974-78 was directional and fairly regular (Foin & Hektner 1986), although this period included two of the driest years in recent decades, 1976 and 1977. Unlike the perennials, annuals in grassland may fluctuate widely in abundance from year to year (Pitt & Heady 1978). Vulpia may not be representative of the other annuals in this study, and no data other than vegetative cover were collected for the less common species, mostly annuals and forbs, so no conclusions can be drawn regarding their patterns of seed rain and recruitment in the annual patches. However, the community is now dominated by perennials, which are increasing in abundance (Foin & Hektner 1986). Consequently, much of the dynamics of succession involves the establishment of the dominant perennials.

The species examined depend on seedling recruitment for the establishment of adult plants. Patchiness in the distribution of mature plants strongly influenced the placement of seeds, the establishment of recruits and, therefore, the potential locations of the next generation of mature plants. These important and reciprocal spatial relationships, between seed distributions and the distributions of adult plants, must be common in plant communities. Most populations are clumped (Kershaw 1973), and because seed dispersal is usually concentrated around parent plants (Levin & Kerster 1974; Harper 1977; Levin 1981; Howe & Smallwood 1982), aggregation in mature plants should usually lead to patchiness in the seed rain. But, although seed rain may be highest near adult plants, studies in old field and grassland communities indicate that adults usually inhibit recruitment under and near themselves by reducing the suitability of microsites for germination and establishment (e.g. Tripathi & Harper 1973; Gross & Werner 1982; Fenner 1985; Shaw & Antonovics 1986; Peart 1989a, b).

To analyse further the spatial dynamics of populations in this community, more information on the potential of each species to invade the vegetation in each patch type is needed. This potential depends on its dispersal ability, the density of its seed rain and the

250 Seed rain in grassland

colonization ability of its seeds (i.e. their ability to establish, grow and survive at a site). The seed rain produced within patches ranged over more than an order of magnitude in the order Holcus > Anthoxanthum > Vulpia > Deschampsia > Rytidosperma. Few seeds of any of these species are dispersed beyond 4 m (Peart 1982). The data reported here on natural recruitment within patches are mainly limited, because of the natural pattern, to the estabishment of species in vegetation dominated by conspecifics. An experimental approach, with seeds introduced at controlled densities, can evaluate the pair-wise interactions involved in the colonization of vegetation dominated by one species, by seeds of a second species. The results of a series of such experiments are reported in Peart (1 989a, b).

ACKNOWLEDGMENTS

I thank T. C. Foin for stimulating discussion and encouragement, C. L. Folt and J. White for comments on the manuscript, and J. D. Nichols for assistance with data analysis. The Sea Ranch Association generously provided field accommodation and access to field sites.

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(Received 2 September 1987; revision received 2 May 1988)