native planting diversity and introduced plant litter ......6 2 dept of marine science and...
TRANSCRIPT
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Native planting diversity and introduced plant litter influence the development of an urban 1
coastal scrub ecosystem 2
Theresa Sinicrope Talley1,4 Kim Chi Nguyen1, Drew M. Talley2, Erick Ruiz3, Paul K. Dayton1 3
1Integrative Oceanography Division, Scripps Institution of Oceanography, La Jolla, CA 92093-4
0227 5
2 Dept of Marine Science and Environmental Studies, University of San Diego, San Diego, CA 6
92110 7
3Ocean Discovery Institute, 2211 Pacific Beach Dr., Suite A, San Diego, CA 92109 8
4 Current address: California Sea Grant Extension Program, Scripps Institution of Oceanography, 9
La Jolla, CA 92093-0232 10
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ABSTRACT 13
Invasive plants often alter the biotic and abiotic environments that they invade, making 14
conditions more conducive to further invasion and less so for native establishment. Restoration 15
in the presence of invaders, in particular after removal efforts, may therefore lead to alternative 16
and, often, undesirable states. Further inhibiting successful restoration are limited resources—17
while weed removal efforts gain momentum, the time, person-power and costs associated with 18
post-removal restoration are harder to come by. Needed are scientifically based yet simple and 19
inexpensive methods for encouraging post-removal ecosystem restoration. Using a field 20
experiment, we tested our hypothesis that the addition of organic litter and higher planting 21
diversity, characteristics of a mature system, would lead to faster development of most aspects of 22
the ecosystem (soils, communities of plants and animals) than no litter addition and a 23
2
monoculture. While we observed this general trend with the addition of plant litter, planting 24
diversity had relatively weak effects. The presence of live native plantings, regardless of 25
diversity level and often in association with litter presence, had associations with faster and/or 26
greater resemblance of experimental plots to the reference site. Resemblance occurred with 27
respect to environmental conditions, decomposition rates, plant abundance and community 28
composition, total abundance of fauna, and faunal diversity, and often within the first year. From 29
these results, we recommend 1) the use of a thick layer of organic litter as a gardening mulch and 30
carbon source for soil microbes, 2) the planting of often dispersal limited native perennials to 31
assuage harsh physical conditions and provide habitat and other functions, and 3) the planting of 32
a diversity of native species. While organic litter had the primary effect on early ecosystem 33
development, it is likely that the effects of plant diversity will increase as the restoration site 34
matures. These simple, inexpensive approaches should increase the rate of development of a 35
broadly functioning ecosystem, which will provide immediate benefits, and jump-start functions 36
that take longer to develop. 37
38
INTRODUCTION 39
Ecosystem development is complex and often unpredictable (Zedler and Callaway 1999). 40
Development trajectories are contingent upon the species present (or nearby) and their direct and 41
indirect interactions with each other and the abiotic environment. The presence of introduced 42
invasive species in particular may change the course of ecosystem development because they are 43
novel to the system, often altering the availability of resources (Zavaleta et al. 2001) and the 44
quantity, quality and form of productivity (Liao et al. 2008). Introduced invaders also often 45
engineer the abiotic environment to novel states that favor the invader and often disfavor natives 46
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(Zavaleta et al. 2001, Byers et al. 2007). The presence of these species, therefore, adds 47
uncertainty to restoration trajectories and end points. 48
49
In Southern California coastal ecosystems, plant species such as date palm (Phoenix 50
canariensis), tamarisk or salt cedar (Tamarix spp.) and ice plant (Carpobrotus spp. and 51
Mesembryanthemum spp.) alter abiotic and biotic properties of coastal transition ecosystems 52
through alterations of disturbance regimes, native plant architecture and biomass, sediment 53
and/or litter accretion rates, and substrate light attenuation, moisture and salinity, resulting in the 54
displacement of native perennials (palm: Talley et al. 2012, Holmquist et al. 2011; ice plant: 55
D’Antonio 1990, Bossard et al. 2000; tamarisk: Whitcraft et al. 2007). Restoration in the 56
presence of invaders such as these, in particular after removal efforts, may lead to alternative 57
and, often, undesirable states (e.g., Zavaleta et al. 2001, Byers et al. 2007). 58
59
Post-removal invasive plant debris. The goal of restoration is to reestablish processes and this 60
sometimes involves speeding up or bypassing processes. Organic soil amendments are often used 61
to add organic matter to otherwise depauperate soils (Levin and Talley 2001, Sutton-Grier et al. 62
2009). The amendments mimic plant litter accumulations by mitigating physically stressful 63
conditions (e.g., shading, moisture trapping) and by replenishing soil nutrients, such as nitrogen, 64
through decomposition. Plant litter also provides a carbon source for soil microbes, which are 65
efficient at decomposition and nitrogen uptake. The microbial community creates low-nitrogen 66
conditions that favor native plant species, which evolved with these conditions and that disfavor 67
nutrient hungry invaders (e.g., Alpert and Maron 2000). Litter may also encourage the 68
development of detritally-based food webs by offering food source and structural habitat 69
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(Gratton and Denno 2005, Kappes et al. 2007). Use of litter may be practical since off-site 70
disposal alternatives are often too expensive to pursue, on-site mulching and disposal leaves sites 71
carpeted with dead plant debris. Development may be inhibited, however, if the litter contains 72
seeds and encourages conditions favorable to the invaders. In this case, declines in grazer 73
diversity and abundance would be expected since grazers are likely more selective about food 74
plants than detritivores (Ernst and Cappuccino 2005, Gratton and Denno 2005). 75
76
Native plantings. Yet another barrier to desired developmental trajectories arises because most 77
native marsh and upland-transition plant species are recruitment limited, while several pervasive 78
invaders are not (Morzaria-Luna and Zedler 2007). The seeds of several particularly aggressive 79
invasive plants, including ice plant (Carpobrotus edulis, Mesymbryanthumum nodiflorum, M. 80
crystallinum) and sickle grasses (Parapholis incurva, P. pratensis), were virtually ubiquitous in 81
Tijuana Estuary-- found in the seed bank, rabbit pellets (ice plant only) and wrack carried into 82
newly created marshes by the tides (Morzaria-Luna and Zedler 2007). Native plant recruitment 83
limitation and prevalence of invader seeds may encourage both new and re-invasions and inhibit 84
native plant community recovery and the subsequent recovery of associated communities. 85
86
Planting diversity. Recovery of plant diversity is especially important in dispersal-limited 87
systems, such as these coastal systems, where newly created or open areas tend to be species-88
poor (Talley and Levin 1999, Levin and Talley 2001, Morzaria-Luna and Zedler 2007). 89
Although the causes of relationships between diversity and ecosystem function are debated and 90
vary with system (e.g., Tilman et al. 1997, Huston 1997), there is general agreement that 91
ecosystems are more stable and ecologically valuable when diversity is maximized compared to 92
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minimized (e.g., Tilman et al. 1997). Recent studies (many performed in Tijuana Estuary) 93
revealed positive relationships between plant diversity and ecosystem properties and functions, 94
such as plant recruitment, canopy architecture, cover, biomass and quality (higher N) (Keer and 95
Zedler 2002, Lindig-Cisneros and Zedler 2002, Callaway et al. 2003, Sullivan et al. 2007). 96
Diversity has similar effects in other ecosystems, in addition to decreasing invasibility through 97
more efficient utilization of space and other resources (e.g., Tilman et al. 1997, Naeem 2006). 98
99
The effects of diversity on invasiveness may, however, vary with spatial scales or location. For 100
example, Levine (2000) found overlap of native riparian and introduced species over large scales 101
(100’s meters) where plant recruitment patterns (dispersal of floating propagules) and suitable 102
abiotic conditions were driven by river hydrology. Over small-scales (cm-meters), however, 103
higher diversity native assemblages monopolized space, fending off invaders (Levine 2000). 104
Similarly, relationships among species and environment may vary with location, especially 105
location along a physical gradient (e.g., Callaway 1995) where increased stress may change the 106
major relationship from competition to facilitation (Bertness and Hacker 1994). 107
108
Restoration goal. The restoration goal of this project is to convert an area recently cleared of 109
dominant invasive annuals to an ecosystem that resembles the remnant native patches of coastal 110
sage and high marsh transition. Assessing ecosystem development using ecosystem processes is 111
the ideal, but is also complex, relatively expensive, and often beyond the scope of time allowed 112
for site assessments. For these reasons, we assessed development using a comprehensive list of 113
physical, soil, plant and faunal variables that reflect ecosystem and community processes, that 114
were then compared between the experimental and reference areas. The experimental site was an 115
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encroached upon 1 acre parcel which had previously been a road waste dump site that was filled 116
and, in the year before this project, had been dominated by and cleared of standing 117
Chrysanthemum coronarium, Mesembryanthemum nodiflorum, and M. crystallanum. The soils 118
contained chunks of asphalt, concrete, and metal pipe; and an invasives-dominated seedbank (as 119
evidenced by regrowth of annuals outside of our experimental area). As with most restoration 120
sites, conversion of this site to a state that existed historically is not an option. The reference site 121
was an adjacent area of remnant but disturbed coastal sage and high salt marsh transition 122
ecotypes, dominated by perennial natives. The reference site had been bisected by a small paved 123
road that was later removed so contained some road debris and disturbed patches (cleared and /or 124
invaded) as in the experimental site. Despite the disturbance, the native dominated reference site 125
functions in desirable ways, such as supporting a diversity of wildlife and plants, including 126
species of concern such as the Federally endangered salt marsh bird’s beak (Cordylanthus 127
maritimus maritimus), the San Diego coastal horned lizard (Phrynosoma coronatum blainvillii), 128
the State of California endangered Belding’s savannah sparrow (Passerculus sandwichensis 129
beldingi), and the State and Federal Endangered light-footed clapper rail (Rallus longirostris 130
levipes). This disturbed but functional state makes the reference site an ideal development goal, 131
at least in the near term, for the experimental site. 132
133
GOAL AND SPECIFIC OBECTIVES 134
Our overarching research goal was to determine how the use of scientifically-based, yet 135
simple and inexpensive techniques-- varying planting diversity and adding introduced plant 136
litter-- influenced the early (first 2 yrs) development of an urban coastal scrub ecosystem. Our 137
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specific objectives were to assess the development of soil properties, native plant communities, 138
and ground-dwelling invertebrate communities compared to a nearby reference site. 139
We expected that plant litter presence and high planting diversity, characteristics of more 140
mature ecosystems, would expedite maturation of the restored ecosystem as reflected by 141
measured variables being most similar between the reference site and the litter and high diversity 142
treatments and most different from the lower diversity, unlittered treatments. We expected that 143
higher plant diversity and litter presence would reduce substrate physical stresses, increase 144
shading and limit germination of annuals, provide more organic material for decomposition and 145
soil amendment, provide a carbon source for microbes which would favor natives, and provide 146
greater abundance and diversity of food and habitat structure for invertebrates. 147
148
149
METHODS 150
This project was conducted at two elevations in a coastal scrub ecosystem at the north end of the 151
Tijuana River Estuary: coastal sage scrub (high elevation) and high salt marsh-upland transition 152
(low elevation) The study area consisted of a restored, experimental site and a reference site as 153
described above. 154
Ten replicate blocks containing treatment plots (80 cm diameter) were established in 155
January 2009 in the experimental site at each of the two elevations. Experimental treatments 156
were combinations of a litter treatment (introduced plant mulch was added or not added) and a 157
planting diversity treatment (0, 1, 3 or 6 species where 3-species was added in 2010). Plants 158
used in the planting diversity treatments were chosen based on common occurrence in the 159
reference site and surrounding area (Table plantlist). Extra plants from each species were kept in 160
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a nursery so that they were of similar size to those planted when used to replant mortalities. 161
Plants used to establish the 3-species plots were of larger size than the plants used in the previous 162
year in the 1- and 6-species plots in order minimize the time lag between plantings. The 163
experimental area was fenced in to avoid confounding effects of herbivores and plots were 164
watered as needed (at least two to three times per week during summer and fall, once per week 165
during the rest of the year when no rain fell). Reference site plots consisted of 18 replicate plots 166
(1m2) per elevation that captured the variability in plant diversity and composition used in the 167
experimental site. Due to the large size of the shrubs, the plot size used in the reference site was 168
larger than that used in the experimental site where plantings needed to be a bit more clustered to 169
improve survival. 170
Sampling and replanting of planting mortalities occurred biweekly throughout the first 171
season (from February through Septebember 2009). Replanting of dead plants continued 172
throughout the study but dramatically decreased after the first season so was not recorded. 173
Sampling of physical conditions, soils, plants and invertebrates in the plots occurred in May 174
2009, three months after the start of the experiment, and in April-May of 2010 and 2011. 175
Physical properties. Substrate temperature, humidity and light attenuation were measured 176
as relative to conditions above the canopy. Photosynthetic-light was measured using an Apogee 177
Quantum handheld light meter, and both humidity and temperature using an Extech 178
humidity/temperature pen. Measurements were made during mid-day (10 am- 2 pm) over two 179
consecutive days. Three measures were taken in each plot, averaged, and then standardized to 180
above canopy conditions (e.g., substrate light [µmol photons m-2 s-1] / full sunlight [µmol photons 181
m-2 s-1]). 182
183
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Soil and litter properties. Porewater salinity, soil moisture, soil organic matter content, texture, 184
and concentrations of nitrate and ammonium were made in each plot. Three soil cores (1.5 cm 185
diam X 10 cm depth) were collected from each plot and homogenized before analysis. A portion 186
of the soil was analyzed using the texture by feel method, and then the salinity of moistened soil 187
was taken by extracting water using a 10cc syringe with a filter paper inside, and reading the 188
salinity with a salinity refractometer (Zedler METHOD). Another portion of the soil was placed 189
in a pre-weighed crucible, weighed wet, dried at 55 degrees C until no weight loss, and then 190
weighed again to calculate percent moisture content. The soil was then combusted at 500 degrees 191
C overnight, and weighed again once cooled in a desiccator to calculate percent organic matter 192
content. A final portion of the soil was dried, ground and submitted to the U.C. Davis DANR 193
facility for nitrate and ammonium analysis. 194
The C:N content of litter, both added litter and what, if any, naturally accumulated, was 195
measured by collecting litter samples. Litter was rinsed in distilled water, dried, ground with a 196
coffee grinder and analyzed for C:N content at the DANR facility at U.C. Davis. 197
198
Decomposition rates were measured using litter bags containing known and similar weight 199
samples of clean, dry, chopped (2.5-5cm long segments) Chrysanthemum litter. One bag per plot 200
was deployed for 1 year, after which bags were brought to the lab and the contents were carefully 201
rinsed with distilled water, picked of living organisms, dried (45 degrees C until no weight loss) 202
and weighed. The loss in dry weight was divided by the initial weight to calculate proportion of 203
biomass lost through the year. The abundance and diversity living organisms within the bags 204
were not correlated with decomposition rates so are not presented further. 205
206
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Plant composition and biomass were assessed using non-destructive measures of plant maximum 207
height, longest diameter and perpendicular diameter for each individual of each species. Plant 208
volume was calculated from these measures (height X longest diameter X perpendicular 209
diameter) and used as a proxy for biomass. 210
211
Ground-dwelling invertebrate community. Invertebrates were sampled each spring using pitfall 212
traps, 250 ml plastic beakers set in the center of each plot at ground level, each with a funnel 213
sitting flush in the opening with a square piece of hardware cloth over the top. A few pieces of 214
litter were placed inside each trap to provide refuge to potential prey species. Plant litter was 215
placed over the top of trap (over the mesh) if in a litter treatment plot, or a small rock if in an 216
unlittered plot, to help camoflauge and secure the trap. Traps were left out for 5-6 days when 217
they were retrieved and the contents emptied into labeled zip top bags and returned in the lab 218
where they were frozen until processing. Animals were sorted from the debris in the sample 219
using a dissecting microscope and organisms were identified to the lowest taxonomic level 220
possible and enumerated. Unknowns were photographed and were brought or sent to specialists 221
for assistance. 222
223
Statistics. Edit with new analyses- restoration site only. 224
All data were log (x+1) transformed or arcsin square root transformed (proportion data) before 225
analyses (Zar 2009). Effects of treatment on first season planting mortality were tested with 2-226
way ANOVA using species level and litter/no litter treatments. No effects of date or block on 227
plant mortality were found so data were pooled. Differences in individual physical variables, soil 228
variables, as well as plant and invertebrate abundances and diversity (species richness and H’) 229
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between plot types (treatment and reference plots) were performed using ANOVA in JMP® 10 230
Statistical Software. Since the reference site did not have corresponding planting species and 231
litter addition treatment types, a two way ANOVA could not be used so treatment combinations 232
were used for the analyses (e.g., Litter-6 species, litter-1species vs. litter and 6 species). 233
Environmental drivers of treatment effects were explored by testing for relationships between the 234
response variable and environmental variables using forward, stepwise multiple regressions with 235
the criteria of p≤0.05 and r>0.04 for inclusion in the model. 236
Multivariate analyses were carried out on the suites of environmental conditions and 237
invertebrate assemblages using Primer Software (Clarke 1993). Environmental variables were 238
normalized, while the species lists with counts were log10 (x+1) transformed, with no other 239
abundance cut-offs, standardizations, relativizations or weighting used on the data. Euclidean 240
distance (environmental variables) and Bray-Curtis similarity indices (faunal data) of the log 241
(x+1) transformed data were calculated to compare the environment and fauna communities 242
between plots, and to relate the fauna to the environmental variables. Differences in the 243
environmental conditions and the invertebrate community between treatments were tested using 244
nonmetric multidimensional scaling (MDS) on the normalized environmental data and the Bray-245
Curtis similarity indices of log(x+1) transformed faunal data. Six different random starting points 246
with up to 1,000 steps were used. The stress values from the six runs were examined for stability 247
to determine whether a global solution had been found. Only analyses with stress values of <0.2 248
were used; stress is a measure of how well the solution (in this case the two-dimensional MDS 249
plots) represents the distances between the data. Clarke (1993) suggests values <0.1 are good and 250
<0.2 are useful. 251
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Significance testing for differences in environmental conditions and faunal composition 252
between plot types and between plant species found in each plot type was performed using an 253
analysis of similarity (ANOSIM) procedure on the Euclidean distance and Bray Curtis similarity 254
matrices. This is a randomized permutation test based on rank similarities of samples (Clark 255
1993). Analyses of dissimilarities in environmental conditions and faunal composition found 256
between plot types and plant species, and the particular variables or taxa contributing to the 257
dissimilarity, were carried out using SIMPER (Clarke 1993). The SIMPER results specify which 258
variables are responsible for the ANOSIM results by comparing the average environmental value 259
or abundances of each taxon between each plot type. The average dissimilarity between samples 260
from within and between each treatment (litter X species level, reference) is computed and then 261
broken down into contributions from each variable/species. Those variables or species with high 262
average terms relative to the standard deviation are important in the differentiation of 263
environmental conditions and faunal assemblages within each plot type. 264
Tests of the environmental variables that best explain faunal community differences were 265
conducted using the Bray-Curtis similarity indices with the BEST Analysis in Primer Software 266
using the BVSTEP method (criteria: rho > 0.95, delta rho < 0.001) with fixed starting variables 267
and a Euclidean distance resemblance measure. BVSTEP sequentially adds environmental 268
variables, keeping those that best explain faunal community patterns and eliminating those that 269
explain least. Several iterations of the test are run with a random selection of variables to ensure 270
that the best match is found (Clarke 1993, Clarke and Warwick 2001). 271
272
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RESULTS Add in new restoration only results- sub for whole system analyses, simplfy results 273
(restoration only: diversity and litter effets on soil, plants, faunal ab/div). rest and ref-274
multivariate analyses – enviro (soil, plant, faunal comp), compare faunal div/ab in rest and ref. 275
Environmental state of reference and treatment plots. (was Litter and diversity effects on 276
environmental state ) 277
Throughout the two years of the study, environmental conditions remained generally more 278
similar within treatments than between treatments (Table. Anosim enviro) due to similar 279
volumes of native and/or introduced plants, plant diversity and density, and similar light 280
attenuation and substrate moisture (humidity and/or soil %water) within treatments (SIMPER 281
variables). In general during the first year (2009-2010), treatments with litter and/or with 282
plantings (regardless of diversity level) had environmental conditions that were more similar to 283
the reference site than plots without litter and/or without plantings (Table ANOSIM enviro). It 284
took two years for any of the treatments to resemble the reference site or each other (Table 285
ANOsim enviro). In particular, environmental conditions in the high marsh treatments planted in 286
the first season most resembled the reference site by the 3rd season (2011). The 3-species plots, 287
which were planted in season 2, and all unplanted treatments remained the most different from 288
the reference site due to higher volumes of introduced plants and lower volumes of native plants, 289
less shading, warmer temperatures, and denser but shorter plants than in the reference site 290
(SIMPER, variables responsible for ~75% of differences; Table ANOSIM enviro). In the coastal 291
sage scrub, all treatments resembled the reference site by the 3rd season except for the unplanted, 292
no litter treatment (Table ANOsim enviro), which also had higher volumes of introduced and 293
lower volumes of native plants, denser but shorter plants (weed seedlings) and less shading than 294
the reference site (SIMPER, variables responsible for ~75% of differences). 295
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At both elevations during all three dates, plots with litter compared with no litter (within 296
the same diversity level) had lower density and volume of introduced plants, higher substrate 297
surface humidity, soil moisture, and shading; and cooler temperatures, less soil salinity, and 298
lower nitrate concentrations (i.e., more microbial activity, REF) (SIMPER variables explaining 299
~75% of differences between litter treatments). Unplanted plots with and without litter differed 300
the most each year, while the 6-species planted plots with and without litter differed the least 301
from each other and had no significant environmental differences by the 3rd season (Table 302
ANOSIM enviro). In general, the degree of differences between the litter and no litter plots 303
decreased for all diversity levels over these two years (Table ANOSim enviro). 304
Higher planting diversity (comparisons within litter and no-litter treatments) was 305
associated with more plant species, higher native plant volume, lower introduced plant volume, 306
more shading, higher substrate humidity and moister soil throughout the two years of the project 307
(SIMPER variables explaining ~75% of differences between litter treatments). Bigger 308
environmental differences occurred, however, between planted, regardless of planting diversity, 309
and unplanted plots. Only in the coastal sage during the 3rd season did an unplanted treatment 310
(with litter) resemble planted treatments. These results illustrate that plants, especially diverse 311
plantings, and litter additions may reduce environmental stress, invasion, and variability in 312
young sites. 313
314
Litter and planting diversity effects on soil development 315
Decomposition rates in the coastal sage from the 1st year were highest in plots with both litter 316
and plantings, 2nd highest in plots with litter and no planting, and lowest in plots with no litter 317
(regardless of planting presence). Rates in the reference site were intermediate and similar to the 318
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littered, planted plots and littered unplanted plots (Table ANOVA soil). Higher decomposition 319
rates in this first year were associated with greater relative substrate humidity (Table REG 320
decomp-env), an effect of additions of litter and plantings (Table ANOVA soil). By the end of 321
the 2nd year, there were no differences in rates between and among the experimental and 322
reference plots (Table ANOVA soil), reflected by the lack of strong relationships between 323
decomposition and environmental variables (Table REG decomp-env). Soil organic matter 324
content was similar between the experimental plots but lower than in the reference site for the 325
first two seasons. By the 3rd season, there was no difference in organic matter content between 326
any of the plots (Table ANOVA soil) illustrating that decomposition of added litter and newly 327
produced plant leaf litter may have begun contributing to soil organic matter content. 328
Similar patterns were found in the high marsh, with higher decomposition rates occurring 329
in littered plots, especially with 1-species plantings, than unlittered plots. These highest rates 330
were comparable to the rates within the reference site (Table ANOVA soil). Decomposition rates 331
in the first year were associated with both lower volumes of introduced plants and more soil 332
moisture in the high marsh (Table REG decomp-env)—conditions favored by experimental 333
additions of litter and plantings (Table ANOVA soil). By the end of the 2nd year, rates were also 334
similar among all plot types. Decomposition in the 2nd year was associated with increased 335
moisture and substrate humidity, and less introduced plant volume, but these conditions began to 336
become more similar among the treatments toward the end of the project (Tables ANOVA soil, 337
plant). Soil organic matter was initially greater in the reference site than experimental plots, 338
between which there were no differences (Table ANOVA soil). Organic matter content was 339
similar across all plots in the 2nd season, and was generally greater in the experimental site than 340
16
reference site in the 3rd season (Table ANOVA soil), again likely revealing contributions of the 341
decomposition of added litter and developing plant litter to soil organic matter content. 342
343
Litter and planting diversity effects on early planting mortality 344
There was no effect of date on planting mortality so data from the first season (8 months) were 345
pooled. Total planting mortality of high marsh plants was not affected by the treatments (Talbe 346
ANOVA morts-hm). Both Salicornia subterminalis and Frankenia salina, however, had 5-12 347
times higher mortality rates when grown in monoculture with relatively little effect of litter 348
presence (Table ANOVA morts-hm). Total planting mortality was highest in unlittered coastal 349
sage scrub plots and/or in mixed (6) species plantings (Table ANOVA morts-cs). Mortality of 350
Artemisia californica, had no strong associations with the treatments, while mortality of 351
Eriogonum fasciculatum was highest in plots without litter and, as with the common high marsh 352
species, when planted alone (Table ANOVA morts-cs). 353
354
Litter and planting diversity effects on plant community development 355
At both elevations in the first season, the plant communities within all but the planted, litter 356
treatments differed from the reference site (Table ANOSIM PLT) because there were greater 357
volumes of natives in the reference site (in particular, the dominant natives such as Frankenia 358
and Salicornia in the high marsh, and Artemisia and Eriogonmum in the coastal sage; SIMPER 359
variables explaining ~90% of differences between sites). The planted plots with litter did not 360
initially differ from the reference site because introduced species growth was minimal and 361
plantings grew well (SIMPER variables accounting for <1% of differences). By the second and 362
into the third season, the plant communities of all treatments differed from the reference site 363
17
although plots with plantings (regardless of litter presence) were less different from the reference 364
communities (coastal sage: 64-86% dissimilarity, high marsh: 82-98%) than those that did not 365
receive plantings (both coastal sage and high marsh: 99-100% dissimilarity) (Table ANOSIM 366
PLT). In these 2nd and 3rd seasons, the planted treatments had greater volumes of native plants 367
(especially the less dominant species such as Malacothamnus, Lotus, Atriplex in the coastal sage 368
and Isocoma and Distichlis in the high marsh), while the unplanted treatments had smaller 369
volumes of natives and greater volumes of introduced plants, in particular Bassia, 370
Chrysanthemum, Mesymbryanthemum nodiflorum, than in the reference site (SIMPER variables 371
explaining ~ 75% of differences between treatments). 372
By the 2nd season for the coastal sage and the 3rd season for the high marsh, litter presence 373
did not influence plant communities, which were similar between treatments that received 374
similar plantings (same diversity levels of litter vs no litter) (Table ANOSIMplant). The plant 375
communities among the diversity levels remained different (Table ANOSIMplant), however, 376
because of the survival and predominance of the species originally planted. The plant 377
communities in the unplanted plots remained significantly different than the planted treatments 378
throughout the study (Table ANSOMplant) due to dominance by introduced species and a lack of 379
recruitment of native plants in the unplanted plots (SIMPER variables explaining ~90% of 380
differences between treatments). Further, by the 3rd season in both elevations, the plant 381
communities within the unplanted treatments were about as dissimilar to each other (90-97% 382
dissimilarity within treatments) as they were to the planted plots (92-100% dissimilarity between 383
treatments; Table ANOSIM plant) due to the different compositions of common weeds (SIMPER 384
variables explaining ~75% of dissimilarity within unplanted treatments). 385
386
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The ground-dwelling invertebrate community 387
Composition. In the first season, 46 species were found across the whole study area, consisting of 388
predominantly coleopterans (43%), hymenopterans (21%), collembolans (21%), thysanurans 389
(18%) and arachnids (5%). The reference plots hosted 17 species unique to the reference site, 390
including carabid and tenebrionid beetles, tussock moth larvae, a millipede, collembolans, a 391
native ant, wasps, hemipterans, psycosids, pseudoscorpion and spiders. The experimental site 392
hosted 5 species, all of which were spiders. By the 2nd season, there were 61 species found across 393
the study area including 41% coleopterans, 15% dermapterans, 13% hymenoptera, 10% 394
collembolans, and 7% arachnids. There were 15 species unique to the reference site, similar to 395
the list from the 1st season, and 14 species unique to the experimental site. In this year, the 396
unique species included carabid beetles, hemipterans, a lepidopteran, a dermapteran, 397
orthopterans, Theba paisana (Italian garden snail), and a lycosid spider. In the 3rd season there 398
were 56 species found, with 41% isopods, 25% collemolans, 8% coleopterans, 7% dermapterans, 399
7% arachnids and 4% hymenopterans. Each site had about 12 species that were unique, both 400
comprised of different representatives of coleopterans, hemipterans, lepidopterans, arachnids, 401
hymentopteras. Native ants, tussock moth, and pseudoscorpions were still only found in the 402
reference site. 403
404
Litter and planting diversity effects on faunal diversity and total abundance. 405
Total abundances of both high marsh and coastal sage faunas in the first season were similar in 406
the experimental litter plots and reference sites, and tended to be lower in the unlittered plots 407
(Table ANOVA invert). In the high marsh, abundance was negatively associated with the 408
volume of introduced plants (Table invert-env reg), which was lowest in the littered and 409
19
reference plots (Table ANOVA plant). In the coastal sage, abundance was positively associated 410
with soil moisture (Table invert-env reg), which was highest in the littered plots (Table ANOVA 411
soil). 412
In the high marsh during the 2nd season, abundance was similar within and between the 413
sites (Table ANOVA invert) and was not correlated with any of the environmental variables 414
(Table invert-env reg). Abundance, however, differed again in the 3rd season with no clear trend 415
across the treatments (Table ANOVA invert). The lowest abundance was in the littered 6-416
species plots, the highest was in the unlittered, unplanted plots, and intermediate abundances 417
occurred in the other treatments and reference site (Table ANOVA invert). In this last year, 418
abundance was weakly but negatively associated with soil moisture (Table invert-env reg), 419
which tended to be highest in the presence of litter and/or 6-species plantings and lower in the 420
unlittered and reference plots (Table ANOVA soil). 421
In the 2nd and 3rd season within the coastal sage, the differences in fauna had no clear 422
trend across treatments except that plots with litter and either no plantings or 3-species plantings 423
maintained higher abundances than in the reference site (Table ANOVA invert). Abundances 424
increased with both increased soil moisture and decreased plant heights in the 2nd season, and 425
increased with plant density in the 3rd season (Table reg invert-env), both indications of a 426
dominance of annual weeds, such as iceplant. 427
Diversity (H’ and ricnhness) in the high marsh during the first season was highest in the 428
reference site, and did not differ from the experimental 1-species littered plots. Diversity tended 429
to be lowest in plots with no litter (Table ANOVA invert). Both measures of diversity were 430
negatively associated with volume of introduced plants (Table REG invert-env), which was 431
highest in the unlittered plots (Table ANOVA plant). By the 2nd season, high marsh diversity was 432
20
similar or higher in the experimental sites than reference site with no clear trend across 433
treatments. Species richness in this 2nd season was negatively associated with soil salinity, which 434
did not differ between plots, and positively associated with soil nitrate concentration, which 435
tended to be higher in the unlittered and/or unplanted plots than in littered, planted or reference 436
plots (Table ANOVA soil). Diversity represented by H’ did not differ in the 2nd season, and no 437
high marsh faunal diversity differences were found in the last season (Table ANOVA invert). 438
Similarly, these diversity variables were not correlated with any of the environmental variables 439
for these dates (Table REG invert-env). 440
In the coastal sage during the 1st season, faunal diversity was similar across all plots and 441
between the experimental and reference sites. There were, however, positive correlations 442
between diversity (both richness and H’) and soil organic matter content (Table REG invert-env), 443
which was highest in the reference site and similar across all experimental treatments (Table 444
ANOVA soil). In the 2nd season, species richness was highest in the planted and littered plots (1-, 445
3- and 6-species), intermediate in the unplanted plots (litter and no litter) and the 3-species, 446
unlittered plots, and lowest in the other planted, unlittered plots (1- and 6-species) and the 447
reference site (Table ANOVA invert). H’ did not differ among plots. Both species richness and 448
H’ were positively associated with soil moisture, which did not differ among plots, and richness 449
was also positively associated with soil organic matter content (Table REG inv-env), which was 450
highest in the reference site and similar among all treatments (Table ANOVA soil). By the 3rd 451
season, diversity tended to be highest in plots with litter regardless of planting diversity level, 452
and similar or lower in the no litter and reference plots (Table ANOVA invert). In this last 453
season, diversity was positively associated with relative substrate temperature, which did not 454
differ among plots (Table ANOVA soil). 455
21
456
Faunal responses to litter and planting diversity treatments. 457
In the first season within the high marsh and coastal sage, the faunal communities generally 458
differed between the litter and no litter treatments, with no clear trends in similarity or 459
differences with planting diversity treatment (Table ANOSIM pitfall). In general, plots with 460
litter supported more of the Argentine ant, bristletails, silverfish and sometimes more of the 461
beetles, Harpalus herbivagus and Metoponium abnorme, while unlittered plots had higher 462
abundances of the beetle Blapstinus sp (SIMPER taxa contributing ~75% of differences between 463
treatments). Most of the factors influencing fauna at both elevations (BEST high marsh R=0.27, 464
coastal sage R=0.17) in this first season differed across these treatments, with soil nitrate 465
concentration, soil salinity, and volume of introduced plants lowest in high marsh litter compared 466
with unlittered plots (Tables ANOVA soil, plant); and soil moisture and light attenuation highest 467
in coastal sage litter compared with unlittered plots (Tables ANOVA soil, plant). 468
In the high marsh, this trend continued into the 2nd season except that the litter and no-469
litter 6-species plantings developed similar communities (Table ANOSIM pitfall hmt) with 470
dominance by Harpalus herbivagus, Forficula auricularia (European earwigs), Metoponium 471
abnorme, and Armadillid isopods in both treatments (Table taxa). The 6-species treatments did 472
not differ in many of the environmental factors that were important for fauna (based on BEST 473
R=0.23), including similar soil moisture, salinity, ammonium, and volume of plants (Table 474
ANOVA soil, plant). By the 3rd season, there was community similarity between all the litter and 475
no-litter plots within each planting diversity (ANOSIM Table pitfall hmt). Most of the remaining 476
community differences in this last season were between the unplanted plots and/or the plots 477
planted in the 2nd season (3-species plantings), and the plots planted in the first year (1- and 6-478
22
species planted plots). The unplanted and recently planted plots had higher abundances of 479
earwigs, bristletails, and the Argentine ant, while the 1- and 6-species planted plots had generally 480
higher abundances of Harpalus herbivagus and occasionally higher abundances of Metoponium 481
abnorme (SIMPER taxa explaining ~75% of differences between treatments). In the final two 482
seasons, faunal communities were responding mostly to soil salinity, soil nitrate (2010 only), 483
plant diversity (weeds and plantings), native plant volume and light attenuation (BEST R=0.23 in 484
2010, R=0.12 in 2011), which were greatest (except for soil salinity and nitrate) in the more 485
diversely planted and/or littered plots (Table ANOVA plant). 486
In the 2nd season in the coastal sage, many of the experimental communities resembled 487
each other except for no litter, planted plots (1- and 6-species) which were similar to each other, 488
but differed from most of the littered plots (ANOSIM Table pitfall css) due to generally higher 489
abundances of European earwig, Argentine ant, Metoponium abnormae and Harpalus herbivagus 490
in the unlittered plots and more Armadillid isopods, spiders and collembolan in the litter plots, 491
(SIMPER taxa contributing ~75% of differences between treatments). Faunal communities were 492
driven by the density and total area of plants (BEST R=0.15), with density greatest in these 493
planted, unlittered treatments (i.e., weed presence increased plant density). By the 3rd season, 494
none of the treatments differed significantly from each other (ANOSIM Global P=0.72) due to 495
similar occurrences of collembola, armadillid isopods, and dictynid spiders (Table taxa). Taxa 496
were responding to number and volume of plants, as well as light attenuation, variables which 497
did not vary too much among treatments in the coastal sage during this 3rd season (Tables 498
ANOVA plant, soil). 499
500
Faunal community development. 501
23
Invertebrate communities in all treatments differed from those in the reference site until 502
the 3rd season when the communities in the experimental and reference coastal sage scrub 503
became fairly similar (ANOSIM Global P=0.72); and one high marsh community (one-species, 504
litter treatment) resembled the reference site (ANOSIM pairwise p=0.135) in this 3rd season. The 505
other high marsh treatments were an average (±1SD) of 72±0.07% dissimilar from the reference 506
site in 2011, down from 90±0.01% dissimilar in 2010 and 77±0.01% dissimilarity in 2009. 507
The high marsh experimental plots started out with higher abundances of the Argentine 508
ant, bristletails, and silverfish, while the reference plots had more native ants, Armadillidae 509
isopods, spiders, and several beetles (Harpalus herbivagus, Harpalus sp., Metoponium abnorme, 510
unknown Tenebrionid). The exception was that the unplanted, unlittered plots contained fewer of 511
the Argentine ant than the reference site. Differences in high marsh faunal communities in 2009 512
were associated with volume of introduced plants, litter C:N ratios, soil nitrate concentration, and 513
soil salinity (BEST R=0.27), all of which except salinity were lower in the reference site than 514
experimental site (Table ANOVA soil). In the following two seasons, compositions in the 515
experimental site remained similar except that in 2010, the Argentine ant declined and there were 516
increases in European earwigs, the beetles Harpalus herbivagus and Metoponium abnorme, and, 517
in 2011, there were additionally increases in springtails relative to the reference site (SIMPER 518
taxa contributing ~75% of the differences between sites each year). The environmental variables 519
explaining faunal differences were soil moisture, ammonia concentrations, soil salinity, and total 520
plant density and species richness (BEST R=0.23) with soil moisture and ammonium 521
concentrations being greatest in the reference site, and plant density and richness intermediate 522
(Tables ANOVA soil, plant). The community similarity between the littered, one species 523
treatment and the reference plots was due to the occurrences of isopods and collembola in both 524
24
areas (Table taxa), which also experienced similar soil moisture and ammonium concentrations 525
(Table ANOVA soil). 526
The taxa and trends in the coastal sage were similar to those of the high marsh. During 527
the first season in the coastal sage scrub, the experimental site housed higher abundances of the 528
Argentine ant, bristletails, silverfish, European earwig and the ground beetle Harpalus 529
herbivagus than the reference site, which had more native ants, spiders, earthworms and the 530
tenebrionid beetle, Metoponium abnorme (SIMPER species accounting for ~75% of dissimilarity 531
between sites). The only exception was that the unplanted, unlittered experimental plots 532
contained few Argentine ant and silverfish. These coastal sage fauna were associated with soil 533
moisture, light attenuation and litter C:N ratios (BEST R= 0.17), where soil moisture and light 534
attenuation (litter plots only) were highest in the experimental site (Table ANOVA SOIL). These 535
faunal trends extended into the 2nd season (SIMPER species accounting for ~75% of dissimilarity 536
between sites) except that in the experimental site, abundances of the Argentine ant decreased, 537
while springtails and Metoponium abnorme abundances increased. Litter C:N was the strongest 538
correlate of faunal communities in 2010 (BEST R=0.20) and was highest in the reference site 539
(Table ANOVA SOIL). In the third season, communities in all the experimental and the 540
reference plots were somewhat similar. While the trends of the first two seasons could still be 541
observed, there were ubiquitous occurrences of isopods (Armadillidae), Lycosid spiders, 542
earthworms, and Harpalus herbivagus throughout both sites. Fauna communities were associated 543
with decomposition rate, plant density, total plant volume and light attenuation (BEST R=0.20), 544
none of which differed in 2011 between the reference and experimental sites (Table ANOVA 545
soil). 546
547
25
DISCUSSION 548
We hypothesized that the addition of organic litter and higher planting diversity, characteristics 549
of a mature system (e.g., Odum 1969) would lead to faster development of most aspects of the 550
ecosystem (soils, communities of plants and animals) than no litter addition and a monoculture 551
(e.g., O’Brien and Zedler 2006, Sutton-Grier et al. 2009, Isbell et al. 2012). While we observed 552
this general trend with the addition of plant litter, planting diversity had relatively weak effects. 553
The presence of live native plantings, regardless of diversity level and often in association with 554
litter presence, had associations with faster and/or greater resemblance of experimental plots to 555
the reference site. Resemblance occurred with respect to environmental conditions, 556
decomposition rates, plant abundance and community composition, total abundance of fauna, 557
and faunal diversity, and often within the first year. This is not to say that the experimental site 558
was functionally similar to the reference site within the time frame of this study- many of the 559
measured variables still differed by the 2nd year, and the longer-term trajectories of those 560
variables that did resemble the reference site are uncertain (Zedler and Callaway 1999). Further, 561
many more variables reflecting potentially important ecosystem functions, such as direct 562
measure of microbial communities (van der Heijden et al. 2008) and vertebrate community 563
members, were not measured in this study so are also uncertain. Finally, our focus was within 564
our plots. The site as a whole (including areas between plots) was still visibly different and will 565
take time to fill in and continue to develop, as with any restoration site (REF-restoration is an 566
ongoing process). The early trajectory of increasing resemblance between the littered and/or 567
planted treatments and the reference site, however, indicates that these treatments establish 568
environments conducive to our restoration goals (Klotzi and Gootjans 2001). In particular, litter 569
26
and live plants ameliorate physical stresses, and likely enhance trophic and non-trophic resources 570
for plants, invertebrates and microbes. 571
572
The presence of plant litter contributed to development likely through both physical and 573
trophic pathways. Litter presence, especially within the first year, mitigated harsh physical 574
substrate conditions (trapped moisture, increased shade), supported the highest decomposition 575
rates (similar to the reference site) and reduced coastal sage planting mortality. Litter also 576
reduced introduced plant invasion through physical effects of shading, and encouraging 577
microbial communities and, therefore, lower nitrate levels (Alpert and Maron 2000), which can 578
favor native plants (Lowe et al. 2003). Litter, at least initially, influenced faunal abundance, 579
diversity, and community composition through its effects on physical conditions and plant 580
community characteristics. Litter hosted more invertebrate pests, such as silverfish, the European 581
earwig and the Argentine ant, than in the reference site. Since these species favor moist 582
conditions and use plant litter for nesting (Flint 1998, Johnson and Triplehorn 2004, Menke and 583
Holway 2006), it follows that higher abundances were found in plots with litter and plantings. 584
Litter hosted higher abundances of detritivores and/or microbivores such as collembolan and 585
isopods, likely due to both provision of food and moist habitat conditions (e.g., Johnson and 586
Triplehorn 2004). Spiders were also associated with litter, which could have been due to the litter 587
itself and/or the higher proportions of native plants acting as a cover for hunting predators, or 588
increasing associated prey species (Bultman and Uetz 1984, Talley et al. 2012). 589
590
The presence relative to absence of plantings generally had a stronger effect than planting 591
diversity level. Often in combination with litter addition, planting presence contributed to more 592
27
environmental similarity among littered plots, and greater soil moisture, shading, native plant 593
community development, and initially higher decomposition rates than unlittered plots. More of 594
the herbivorous beetles, Metaponium abnorme and Harpalus herbivagus, were observed in 595
planted plots, especially with litter present. The presence of native plants may have served as a 596
food source while the enhancement of the proportional abundance of natives offered by litter 597
may have also contributed to support of herbivores (Wolkavich 2010). 598
599
When planting diversity did have effects, different planting diversity levels conferred different 600
benefits. The higher diversity treatment compared with the lower diversity treatments was 601
associated with lower mortality rates of common-species plantings, higher overall plant 602
diversity, higher native plant volume, lower introduced plant volume, and lower variability of 603
environmental conditions and faunal communities within treatments. It may be that the higher 604
diversity mixes resulted in complementarity effects, where mixes of different species more 605
efficiently used limiting resources (e.g., light, nutrients) and resulted in less environmental and 606
faunal variability (more stability) than monocultures (e.g., Tilman and Downing 1994, Worm et 607
al. 1996). Mixes may also have resulted in sampling effects, where multiple species increase the 608
chance of inclusion of a species that is a better competitor and/or stabilizer (e.g., Naeem et al. 609
1996, Loreau 2000, Dukes 2002). 610
The monoculture plantings (1-species) were often associated with lower total planting 611
mortality rates, comparatively high substrate humidity and, in combination with litter in the high 612
marsh, high initial decomposition rates and the first resemblance to reference site faunal 613
community. This was likely due to the selection of particular species that contributed to these 614
processes and not a monoculture per se (e.g., Dukes 2002). Monoculture plantings consisted of 615
28
plants that were among the most abundant in the reference site, often forming large monocultural 616
stands. Their abundance indicated that these species are were suited for the local environment 617
with respect to their physiological tolerances and/or intra-specific facilitation (Padilla and 618
Pugnaire 2006, McIntire and Fajardo 2011). In particular in the experimental high marsh, 619
Frankenia salina formed dense patches that were uniformly low to the ground relative to the 620
varying heights of mixed plots. The dense patches were able to trap humidity, a strong correlate 621
with decomposition rates, and ameliorate harsh physical conditions such as soil salinity. In harsh 622
physical environment such as this, plant taxa that grow quickly with dense, low cover might have 623
a large effect on development. 624
The 3-species plantings did not differ from the other diversity levels for most variables. 625
When differences did occur, the differences were consistent with the younger age of these plots 626
and not intermediate diversity effects (e.g., smaller native shrubs, higher introduced plant 627
volumes, faunal abundance overshoots in the 3-species compared with reference plots.) 628
629
Recommendations 630
The biotic and abiotic differences among the experimental treatments and the reference site 631
began to decrease with the timeframe of this study, especially in the plots that received organic 632
litter and live native plants. Methods that encourage the rapid establishment of a broadly 633
functioning ecosystem provide immediate benefits, and may jump-start functions that take longer 634
to develop. 635
Organic litter. The use of a thick layer (5-8 cm) of plant litter as a gardening mulch 636
shades the soil surface limiting germination of the seedbank, which consists mostly of introduced 637
annuals. Litter also retains moisture, encouraging growth of plantings. The downside of litter, 638
29
especially in combination with irrigation is encouragement of pests like Argentine ant, earwigs 639
and silverfish. It is best to use litter from the site, so as not to spread these species, or from a 640
clean litter source. After native plants establish, allow the natural precipitation regime with 641
desiccation throughout the dry season to curb the growth of pest populations. 642
Plant native perennials after invasive annual removal. Natives in this ecosystem are 643
dispersal limited and would be slow to recruit naturally, if at all (Lindig-Cisneros and Zedler 644
2002, Morzaria-Luna and Zedler 2007). Without plantings, the introduced annuals will germinate 645
from the seedbank (Morzaria-Luna and Zedler 2007) and re-dominate after the first rains. 646
Limiting reinvasion of annuals is crucial because a shift from a perennial shrub to an annual herb 647
dominated plant community would dramatically change the physical, chemical and trophic 648
characteristics of an ecosystem, with bottom–up effects on the greater community (Cook and 649
Talley in revision). Perennial shrubs, compared with annual herbs, tend to be larger (more 650
volume), provide live woody biomass throughout the year, and live much longer allowing the 651
provision of more of the functions that are desirable for this area such as mitigating harsh 652
physical conditions and providing habitat for invertebrates (this study), providing habitat for a 653
diversity of vertebrates (e.g., Chase et al. 2002), enhanced carbon storage (Zan et al. 2001, 654
Koteen et al. 2011), upland runoff filtration, erosion control and storm surge buffering (e.g., 655
Mitsch and Gosselink 2007). The inclusion of fast growing, generally larger native shrubs such 656
as Frankenia salina, Iscoma, menziesii, Artemisia californica, Eriogonum fasciculatum and 657
Artriplex canescens, would quickly add needed biomass to immediately provide physical 658
modifications, habitat and to start accumulating litter biomass. 659
Include a diversity of native species in the plantings. While organic litter had the primary 660
effect on early ecosystem development, it is likely that the effects of plant diversity will increase 661
30
as the restoration site matures. With time, plants will fill in and come into direct contact with 662
each other leading to stronger interactions. Time also allows for the colonization of species, in 663
particular, those species that are rare or slow to colonize resulting in higher numbers of and more 664
intense interspecific interactions (Thompson 1994). Further, recent studies reveal mechanistic 665
links between diversity and function across an array of ecosystems (Isbell et al. 2011) and the 666
need for diversity to sustain multiple ecosystem functions (Zavaleta et al. 2010). For this estuary 667
in particular, plant diversity was linked with higher primary productivity (Zedler et al. 2001, 668
Callaway et al. 2003), canopy complexity (Keer and Zedler 2002), and reduced invasion (Lindig-669
Cisneros and Zeder 2002). 670
671
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