broad-scale geographic variation in the organization of rocky intertidal communities in the gulf of...
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Broad-scale geographic variation in the organization of rocky intertidal communities in the 6
Gulf of Maine 7
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Elizabeth S. Bryson1, Geoffrey C. Trussell1*, Patrick J. Ewanchuk2 9
1Marine Science Center and Department of Marine and Environmental Sciences, 430 Nahant 10
Road, Nahant, MA 01908 11
2Department of Biology, Providence College, Providence, RI 02912 12
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*Corresponding author 16
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Keywords: community organization, coastal oceanography, competition, disturbance, Gulf of 18
Maine, herbivory, predation, recruitment, rocky intertidal 19
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ABSTRACT 24
A major challenge facing ecology is to better understand how large-scale processes 25
modify local scale processes to shape the organization of ecological communities. Although the 26
results of ecological experiments are repeatable on local scales, different results often emerge 27
across broad scales, which can hinder the development of general predictions that apply across 28
the geographical range of a community. Numerous studies in the southern Gulf of Maine have 29
shaped our understanding of community organization and dynamics on New England rocky 30
intertidal shores, where consumers strongly control recovery from disturbance on sheltered 31
shores and high invertebrate recruitment and competition for space dictate recovery on wave-32
exposed shores. It is unclear, however, whether the effects of consumers and recruitment 33
variation on resulting community organization in this region apply more broadly to rocky 34
intertidal habitats throughout the Gulf. 35
We characterized variation in rocky intertidal community structure at 34 sites throughout 36
the Gulf of Maine and experimentally examined the influence of consumers (present, absent) and 37
wave energy (wave-exposed, sheltered) on community recovery from disturbance in the northern 38
and southern Gulf. Our results reinforced previous work in the southern Gulf because consumers 39
dictated the recovery of fucoid algae and mussels on sheltered shores, whereas high barnacle and 40
mussel recruitment and competition for space shaped recovery on wave-exposed shores. 41
However, on sheltered shores in the northern Gulf, neither consumers nor barnacle and mussel 42
recruitment impacted recovery, which was dominated by fucoid algae. Moreover, recovery on 43
wave-exposed shores in the northern Gulf was quite distinct from that observed in the southern 44
Gulf: barnacle and mussel recruitment was negligible and fucoid algae dominated recovery 45
including the long-term establishment of Ascophyllum nodosum, which is largely absent from 46
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wave-exposed shores in the southern Gulf. Thus, distinct community types emerged in the 47
northern and southern Gulf despite their sharing many of the same species. These patterns likely 48
emerged because of regional differences in coastal oceanography that modulate the recruitment 49
of barnacles and mussels. Hence, increased attention to regional factors should provide key 50
insight into how rocky shore communities are organized in the Gulf of Maine and elsewhere. 51
INTRODUCTION 52
A central goal of ecology is to understand how large-scale processes modify local level 53
processes to shape the distribution and abundance of species, and assembly, organization and 54
dynamics of ecological communities (Wiens 1989, Levin 1992, McGill 2010, Hastings 2010). 55
Because environmental gradients across larger scales can modify, for example, community 56
assembly (Chase 2010, Hein and Gillooly 2011), the relative importance of bottom-up and top-57
down processes (Menge 2000, Navarrete et al. 2005, Chase et al. 2010, Krenz et al. 2011), and 58
the nature, intensity and scale of species interactions (Shurin and Allen 2001, Chase 2003, 59
Sanford and Worth 2010, Menge et al. 2011), it is difficult to derive overarching assembly rules 60
for community ecology. Understanding how differences in biotic and abiotic context mediate 61
changes in species interactions and ultimately community assembly has been identified as a 62
major gap in ecology (Agrawal et al. 2007, Weiher et al. 2011). 63
Rocky intertidal communities in the southern Gulf of Maine have long served as a model 64
system to understand how abiotic and biotic factors influence succession after disturbance and 65
resulting community organization (Menge 1976, 1978a,b, Lubchenco, 1980, 1983, Petraitis 66
1987, Petraitis and Dudgeon 1999, Dudgeon and Petraitis 2001, Bertness et al. 2002, 2004a,b). 67
A defining feature of these and other rocky shores is the amount of wave action they experience 68
(i.e., wave-exposed versus sheltered), which can influence larval and nutrient flux rates (Leonard 69
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et al 1998, Jenkins and Hawkins 2003, Bertness et al. 2004a), the availability of space via 70
disturbance (Paine and Levin 1981, Denny et al. 1985), the extent of air exposure as a result of 71
wave splash (Harley and Helmuth 2003), and the abundance and efficacy of mobile consumers 72
(Kitching et al. 1959, Menge 1976, Menge and Sutherland 1976, Etter 1989). Hence, patterns of 73
succession and resulting community organization often differ substantially between wave-74
exposed and sheltered shores. 75
On wave-exposed shores in the southern Gulf of Maine, barnacle recruitment 76
(Semibalanus balanoides) during a narrow window between late February and April (Barnes 77
1957, Dudgeon and Petraitis 2001, Pineda et al. 2002, Kordas and Dudgeon 2009) often 78
facilitates high mussel recruitment in the summer (Petraitis 1991, Bertness et al. 2004a). In the 79
absence of consumer pressure, mussels eventually dominate these communities by overgrowing 80
barnacles and outcompeting fucoid algae (Fucus vesiculosus, Ascophyllum nodosum) for space 81
(Menge 1976). Of course, depending on the timing and scale that new bare space is made 82
available by disturbance from waves and other factors, these habitats can also contain a mosaic 83
of barnacles, mussels and Fucus at any given time (Menge 1976, 1978a,b, Bertness et al. 1999, 84
2004a). In contrast, on sheltered shores in the southern Gulf the supply of barnacle and mussel 85
larvae is reduced (Bertness et al. 2004a) and resulting low recruitment, coupled with more 86
intense predation by dogwhelks (Nucella lapillus) and green crabs (Carcinus maenas), further 87
reduces mussel and barnacle abundance (Lubchenco and Menge 1978). As a result, competition 88
for space is relaxed allowing fucoid algae (initially Fucus vesiculosus followed by the slower 89
growing Ascophyllum nodosum) to colonize, grow and form dense canopies that dominate the 90
shore (Dudgeon and Petraitis 2001). Although snail (Littorina littorea) grazing on young 91
recruits may slow fucoid algal recovery (Lubchenco 1983, Petraitis 1987), the eventually 92
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dominant Ascophyllum canopy typically covers a sparse understory of mussels and barnacles at 93
these sites (Bertness et al. 2004a), which contrasts with the dense mussel and barnacle 94
communities typical of wave-exposed shores (Menge 1976, 1978a,b) 95
The prevailing evidence indicates that these habitat-specific differences in succession and 96
community organization in the southern Gulf typically depend on the high recruitment potential 97
of dominant space occupying species and the impact of consumers on their abundance after 98
settlement. However, recent work on Gulf of Maine shores has revealed geographically based 99
differences in species interaction strength (Kordas and Dudgeon 2009, 2011) and community 100
organization following disturbance (Petraitis and Dudgeon 1999, 2004; Dudgeon and Petraitis 101
2001, Bertness et al. 2002, 2004a,b). Hence, there has been disagreement over whether 102
consumers drive the dynamics and organization of these communities or whether spatial and 103
temporal variation in recruitment levels of key species plays a more prominent role than 104
previously thought. For example, experiments at multiple locations in the southern Gulf found 105
that consumers prevented the recovery of fucoid algal canopies on sheltered shores (Bertness et 106
al. 2002, 2004a,b). In contrast, work in central Maine’s Penobscot Bay found that variability in 107
the timing and location of mussel, barnacle and fucoid algal recruitment and the size of patches 108
created by disturbance could result in mussel dominated or algal dominated community states 109
(Petraitis and Dudgeon 1999, Dudgeon and Petraitis 2001). These results also suggests that 110
variation in barnacle and mussel recruitment in the Gulf of Maine may not solely depend on 111
wave-exposure, but also local oceanographic processes that impact larval supply. Moreover, 112
consumer pressure was quite different in these studies, with Bertness et al. (2004a) observing 113
high predation rates within a single tidal cycle and Petraitis and Dudgeon (1999, 2004) observing 114
predation rates that were not apparent for several weeks. 115
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It is clear that there is the potential for substantial geographic variation in the factors 116
affecting community succession and organization in the Gulf of Maine. This is not surprising 117
because geographic variation in upwelling (Bustamante et al. 1995a, Menge et al. 1997, 2003, 118
2004), grazer impacts (Coleman et al. 2006), and the strength of positive and negative species 119
interactions (Bertness and Leonard 1997, Leonard 2000) can influence the succession and 120
organization of rocky shore communities. For example, large regional differences in community 121
organization have been documented in the eastern Atlantic (Coleman et al. 2006, Jenkins et al. 122
2008), which has many of the dominant species (Fucus, Ascophyllum, Semibalanus, Mytilus sp., 123
Carcinus and Nucella) found on Gulf of Maine shores. In the eastern Atlantic, latitudinal 124
differences in rocky shore community organization are likely driven by changes in the 125
abundance and impact of two patellid limpet species, Patella depressa and P. vulgata (Coleman 126
et al. 2006, Jenkins et al. 2008), which are absent from the western Atlantic and Gulf of Maine. 127
In general, herbivore control of fucoid algae appears to be more intense in the eastern Atlantic 128
than in the Gulf of Maine (Jenkins et al. 2008), whereas factors affecting barnacle and mussel 129
abundance may be more important on rocky shores in the western Atlantic (i.e. the Gulf of 130
Maine). 131
Over the last 20 years, many studies have shown that broad scale spatial variation in 132
rocky shore communities may reflect differences in oceanographic processes that impact larval 133
supply (e.g. Menge et al. 1994, 2003, Broitman et al. 2001, Navarrete et al. 2005, Blanchette et 134
al. 2008, Wieters et al. 2009). Because variation in barnacle and mussel recruitment can play a 135
key role in the succession and organization of Gulf of Maine rocky shores, identifying 136
geographic variation in coastal oceanography that influences larval supply may help reconcile 137
the disparate influence of consumer control and recruitment variation on community succession 138
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and organization throughout the Gulf of Maine. To examine whether distinct oceanographically 139
driven biogeographic provinces occur within the Gulf of Maine, we examined the influence of 140
physical stress (wave energy), recruitment, and consumers on community recovery after 141
disturbance in the northern and southern Gulf. To broaden the geographic scope of these 142
observations and experiments, we also examined between-site variation in community structure 143
on 34 shores across the Gulf of Maine basin. Our results suggest that the succession and 144
organization of rocky intertidal communities in the northern and southern Gulf are substantially 145
different despite sharing virtually the same species assemblages. Moreover, these differences 146
appear to be shaped by oceanographically driven recruitment variation that dictates subsequent 147
species interactions. 148
MATERIALS AND METHODS 149
Community Structure Across the Gulf of Maine 150
We characterized the structure of rocky intertidal communities with quadrat surveys at 34 151
sites spanning the Gulf of Maine (Fig. 1, Appendix A). We recorded the percent cover of all 152
visible, macroscopic, sessile species composing the canopy and understory in point-intercept 153
quadrats (25 points per 0.25 m2 quadrat) haphazardly placed (N = 10) in the mid-intertidal at 154
each site. This method provides reliable estimates of the abundance of common intertidal 155
species, but may be less so in estimating the abundance of rare species. Quadrats were randomly 156
tossed on horizontal emergent substratum within the fucoid algae zone. If a quadrat landed in a 157
tidepool, or rested vertically against a ledge, then the quadrat was moved to the nearest emergent, 158
horizontal surface. All algal or sessile invertebrate species located beneath an intercept were 159
recorded to yield percent cover data that regularly exceeded 100% because of the presence of 160
both the canopy and understory organisms. For any species that could not be conclusively 161
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identified in the field (rarely the case), a representative sample was collected for identification in 162
the laboratory. 163
Sites were assigned to 3 geographic regions based on documented oceanographic 164
circulation patterns (Pettigrew et al. 1998, 2005, see Fig. 1 for prevailing Gulf of Maine 165
circulation patterns). The Southern Gulf region ranged from Cape Cod, Massachusetts to 166
Penobscot Bay, Maine corresponding to the Western Maine Coastal Current (WMCC) that forms 167
from the outflow of the Penobscot River and the Eastern Maine Coastal Current (EMCC; 168
Churchill et al. 2005, Pettigrew et al. 2005, Manning et al. 2009). The Penobscot region ranged 169
from Penobscot Bay to Great Wass Island, Maine, where a portion of the EMCC moves offshore 170
to varying extents depending on seasonal and interannual variation. When offshore movement is 171
high, a freshwater plume from the Penobscot River replaces the surface waters in this region 172
(Pettigrew et al. 1998, 2005, Churchill et al. 2005, Hetland and Signell 2005, Pettigrew et al. 173
2005). The Northern Gulf region ranged from Great Wass Island to Cobscook Bay, Maine, 174
corresponding to the region where the Nova Scotia current and discharge from the St. John and 175
St. Croix rivers meet near the mouth of the Bay of Fundy to form the EMCC and southwestward 176
flow occurs (Hetland and Signell 2005, Pettigrew et al. 2005, Tilburg et al. 2012). The wave 177
exposure of each site (sheltered vs. exposed) was characterized based on personal observations 178
of coastal topography (e.g., headlands vs. bays) and wave action during calm and stormy periods, 179
and/or dissolution rates of plaster clod cards (Appendix A). 180
Variation in community structure was analyzed with multivariate analyses using the 181
Vegan package (Oksanen et al. 2013) for R version 3.0.0 (R Core Development Team 2013). A 182
Non-Metric Multidimensional Scaling (NMDS) plot was created to compare community 183
composition between sites using the ‘metaMDS’ function with untransformed percent cover data 184
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and a Bray-Curtis index. After the ordination plot was constructed from the metaMDS, the 185
function ‘ordiellipse’ was used to plot 95% confidence ellipses for the mean ordination of each 186
geographic region and wave exposure combination. We employed the ‘adonis’ function with a 187
Bray-Curtis index with 999 permutations to conduct a multivariate ANOVA (PERMANOVA), 188
with geographic region (Southern, Penobscot, Northern) and wave exposure (Exposed, 189
Sheltered) as orthogonally crossed factors to test for differences in community structure. 190
Subsequent Similarity Percentage (SIMPER) analyses using the ‘simper’ function determined the 191
contributions of dominant species and bare rock to the similarity between regions and wave 192
exposures. 193
Recovery from Disturbance Experiment: Study Sites 194
To examine patterns of recovery from disturbance, we chose two representative sites of 195
each wave exposure (sheltered, exposed) in each of two regions (Northern Gulf [Lubec, Maine], 196
Southern Gulf [Nahant, Massachusetts]). Due to the broad scale (distance between the two 197
regions was > 400 km) and labor-intensive nature of this experiment (144 experimental plots) 198
additional sites were not logistically feasible. Moreover, the results of the Gulf of Maine-wide 199
community structure survey confirmed that the study sites used in the recovery experiment were 200
representative of each geographic region. The exposed sites in the northern Gulf were on a 201
rocky headland between Julia Cove and Hamilton Cove in Lubec, Maine and the sheltered sites 202
were just north of Quoddy Head State Park in Lubec, Maine. In the southern Gulf, the two 203
exposed sites were on East Point in Nahant, Massachusetts and the two sheltered sites were in an 204
embayment northwest of East Point in Nahant, Massachusetts (see Appendix A for more 205
information). One of the wave-exposed sites in the southern Gulf was used in Menge’s early 206
studies (Menge 1976, 1978a,b) and the sheltered sites in the south were adjacent to those used by 207
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Menge (1976, 1978a,b) and Lubchenco (1980, 1983) because their original sites are now subject 208
to high levels of human activity. 209
Consumer Density Surveys and Analysis 210
We monitored mobile consumer density at experimental study sites by recording the 211
number of mobile consumers in 10 randomly placed 0.25m2 quadrats in the mid-intertidal zone 212
at each replicate site in July 2005. Density data for the dominant mobile consumers (predators: 213
Nucella lapillus and Carcinus maenas and herbivores: Littorina littorea and Tectura testudinalis) 214
were analyzed with a 3-factor, nested design with geographic region and wave exposure as fixed 215
factors and site as a random factor nested within wave exposure and geographic region. Because 216
the high frequency of zero counts in the quadrats resulted in heteroscedasticity that could not be 217
corrected via transformation, we assessed the influence of geographic region and wave-exposure 218
on mobile consumer densities with Generalized Linear Mixed Models (GLMMs) that had a 219
negative binomial error distribution and a log link function (O’Hara and Kotze 2010, Linden and 220
Mantyniemi 2011, Warton and Hui 2011) using the glmmADMB package (Fornier et al. 2011, 221
Skaug et al. 2011) for R version 3.0.0 (R Core Development Team 2013). To determine the 222
influence of geographic region and wave-exposure and their interaction on the density of each 223
consumer, a model selection based approach to hypothesis testing using Akaike weights based 224
upon corrected Akaike Information Criterion (AICc) was employed to determine the best-fit 225
model (Burnham and Anderson 2002, 2004, Johnson and Omland 2004, Bolker et al. 2009). 226
Recovery from Disturbance Experiment: Approach & Analysis 227
This experiment was a 4-factor nested design with replicate sites (N = 2) as a random 228
factor nested within each wave-exposure (sheltered, exposed) and geographic region (northern, 229
southern). Hence in each region, there were two replicate wave-exposed and two replicate 230
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sheltered sites. At each replicate site (N = 8 in total), there were 6 independent replicates of each 231
caging treatment (cage, cage control, open), for a total of 144 experimental plots. 232
Each replicate plot was a 1 m x 1 m clearing (each clearing was separated by at least 2 m) 233
where all resident sessile algae and invertebrates were removed with paint scrapers and propane 234
torches in mid October 2003. The successful removal of all organisms in each plot was 235
confirmed in early March 2004 prior to the onset of barnacle recruitment. To maintain a 236
consistent sampling, the corners of a single 20 cm x 20 cm plot located in the center of each 1 m 237
x 1m clearing was marked with stainless steel lag screws installed into the substratum. In 238
addition, the fucoid algal canopy surrounding each clearing was trimmed to prevent it from 239
impacting the sampling area (e.g., whiplash, shading). All percent cover data were recorded in 240
these 20 cm x 20 cm plots. 241
Caging treatments (cage, cage control, or open) were applied to appropriate plots at each 242
site in each location. Consumer exclusion cages (25 x 25 x 5 cm; mesh opening = 0.5 cm) 243
constructed from stainless steel mesh were anchored into the rock to cover the 20 x 20 cm plot 244
located in the center of each 1 m x 1m clearing. The edges of cages were pressed flush to the 245
substratum and, if necessary, sealed with waterproof epoxy (Z-spar) to further ensure the 246
exclusion of consumers. Cage controls were constructed and installed in a similar manner except 247
that two sides of the cage were left open to allow access by consumers. Open plots were left 248
uncovered to allow full access by consumers. 249
We assessed recovery by photographing plots twice a year (spring and fall) over the 250
following 2 years. Mussels in the northern Gulf may include M. edulis, M. trossulus and hybrids 251
(Rawson et al. 2001), but field identification of these species is not feasible. Although the 252
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general rarity of mussels at sites in the northern Gulf makes it unlikely that this distinction 253
among species is important, all mussels are nevertheless referred to as Mytilus spp. 254
The percent cover of sessile species was determined from resulting photographs by 255
placing a layer of 36 random points over each photograph in Adobe Photoshop™ and recording 256
species identity underneath each point. If no species was present, the point was scored as bare 257
rock. If a point fell upon a mobile consumer, the sessile species to the immediate right of the 258
mobile species was recorded. As recovery progressed and a fucoid algal canopy developed, it 259
became necessary to collect percent cover data on understory species using a point-intercept 260
quadrat (with 36 points) in the field. 261
Percent cover data were analyzed with a 4-factor, nested ANOVA with replicate sites as a 262
random factor nested within each wave exposure (sheltered, exposed) and geographic region 263
(northern, southern) and caging treatment (cage, cage control, open) as a fixed factor. Although 264
we present the full pattern of recovery in our figures, we conducted our analyses on the percent 265
cover data collected during the last sampling date in Fall 2005 for the three dominant taxa (F. 266
vesiculosus, S. balanoides, and Mytilus spp.) in our plots because they were the primary drivers 267
of community recovery. Percent cover data were log10 (+1) transformed to meet the 268
homogeneity of variance assumption (Warton and Hui 2010). These analyses were performed 269
with JMP software for the Macintosh (version 10, SAS Institute, Cary, NC). 270
To further address importance of geographic region, wave exposure and consumer 271
exclusion to patterns of recovery, we determined the effect size (eta-squared, η2 = SSeffect/SStotal) 272
for each factor in our ANOVA model. Because of the large effect (Cohen 1988) of geographic 273
region (η2>0.22 for each species) and the significance of the region x wave exposure x caging 274
interaction, we examined the effect sizes (η2) for wave exposure, caging and their interaction for 275
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each geographic region. Separate 3-factor, nested ANOVAs with sites nested within wave 276
exposure and crossed with caging were performed for each species in each region and the 277
resulting sums of squares used to determine observed effect sizes. To examine relationships 278
between dominant species on wave-exposed shores in the southern Gulf where recruitment, and 279
likely competition for space, was highest, we used Pearson’s (r) correlations on percent cover 280
data obtained in the spring and fall of 2005. 281
Barnacle Recruitment 282
Annual barnacle (S. balanoides) recruitment was measured at each experimental study 283
site from 2004 to 2006 in 6 replicate ‘settlement’ plots (20 cm x 20 cm) that had been cleared of 284
all sessile organisms in early spring of each year. Each plot was photographed in late spring of 285
each year, after the completion of settlement. A grid of equally sized squares was then placed on 286
each photo in Adobe Photoshop™ before counting the number of barnacles present in 10 287
randomly chosen squares. Because barnacle settlement was quite high and uniform in southern 288
plots, total recruitment was determined by scaling up the average number of barnacles in these 289
subsamples to calculate barnacle density in each plot. Due to very low recruitment in the 290
northern Gulf, this approach was not necessary and all barnacle recruits within the 20 x 20 cm 291
plots were counted. Barnacle recruitment densities were analyzed with a four-factor nested 292
ANOVA with site as a random factor nested within region and wave exposure, and crossed with 293
year using JMP software for Macintosh (version 10, SAS Institute, Cary, NC). Although we 294
used the same physical areas each year, we reasoned that a repeated measures design was not 295
necessary because recruitment plots were re-cleared before each recruitment season and 296
therefore provided an independent assessment of recruitment variation for each year. Prior to 297
analysis, data were log transformed to meet the homogeneous variance assumption of ANOVA. 298
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Long-term Ascophyllum recovery 299
The long-term recovery of Ascophyllum in open plots at sheltered sites in both regions 300
was monitored from 2004-2011 by annually photographing each plot in the spring and fall. 301
Unfortunately, unanticipated changes in landowner restrictions in 2007 made such monitoring 302
impossible for the wave-exposed sites in the northern Gulf. However, beginning in 2005 we 303
were able to monitor long term Ascophyllum recovery in the open plots of another similar 304
experiment that had one wave-exposed site in the northern Gulf that was unaffected by 305
landowner restrictions and two wave-exposed sites in the southern Gulf. Because long-term 306
Ascophyllum recovery at each shore type was derived from two separate experiments with 307
different time spans and levels of site replication, recovery data for the wave-exposed sites were 308
analyzed with a one factor ANOVA that considered geographic region as a fixed effect. Because 309
unequal variances between sites could not be correct via transformation or modeled through 310
mixed model approaches, differences between these sites were assessed by adjusting the 311
significance level to that of the Brown-Forsythe test for unequal variances. Long-term 312
Ascophyllum recovery data at sheltered sites were analyzed with an ANOVA that considered 313
geographic region as a fixed effect and site as a random effect nested within geographic region. 314
Although figures present the full temporal pattern of recovery through time, we analyzed the 315
endpoint data collected in Fall 2011. 316
RESULTS 317
Community Structure Across the Gulf of Maine 318
Results of the metaMDS analysis indicated that sites in the northern and southern regions 319
of the Gulf of Maine clustered based upon wave exposure (Fig 2). Moreover, wave-exposed and 320
sheltered sites in the southern region clustered separately, whereas wave-exposed and sheltered 321
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sites clustered together in the northern region. Community structure was strikingly similar for 322
sites within the same wave exposure in the northern and southern regions. However, within the 323
Penobscot region, site-to-site similarity was reduced, as indicated by the large 95% confidence 324
ellipses (Fig. 2). One wave-exposed site (Milbridge, Maine) and one sheltered site (Grindstone 325
Neck, Maine) in the Penobscot region that did not cluster with sites of similar wave exposure 326
likely contributed to the reduced similarity in this region. 327
Results of the PERMANOVA indicated that community structure differed based upon 328
region and wave exposure, and that the effect of wave exposure differed between oceanographic 329
regions (PERMANOVA, Region x Exposure, F2,28 =4.5058, P=0.0008, Appendix B). Wave-330
exposure effects on community structure were far stronger in the southern Gulf than in the 331
northern Gulf (Figs. 2, 3, 4). In the Penobscot region, sites grouped based upon wave exposure 332
with most exposed sites and most sheltered sites clustering with their counterparts in the southern 333
Gulf. However, the overall similarity of sites within each wave exposure grouping was lower in 334
the Penobscot region, as evidenced by the larger ellipses (Fig. 2), than in other regions. The 335
similarity between wave-exposed and sheltered sites in the northern Gulf was likely driven by 336
the dominance of Ascophyllum at both wave exposures in this region, whereas this alga was only 337
dominant at sheltered sites in the southern Gulf and the Penobscot region (Figs. 3, 4, Table 1, 338
also see Appendix C). In contrast, Fucus dominated wave-exposed sites in the southern Gulf and 339
the Penobscot region. Hence, Ascophyllum and Fucus contributed to the lack of similarity 340
between wave-exposed and sheltered sites in the southern Gulf and the Penobscot region but 341
played a minor role in the lack of similarity among wave exposures in the northern Gulf. 342
Differences in the abundance of these fucoids also drove the dissimilarity between the wave-343
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exposed sites among the three regions, but lower barnacle and higher bare space percent cover 344
distinguished northern sheltered sites from those in the other regions. 345
Consumer Densities 346
Quadrat surveys indicated that predators and herbivores with strong effects on dominant 347
intertidal species were most abundant at sheltered sites in the southern Gulf. Green crabs (C. 348
maenas) were observed only at southern sheltered sites (Fig. 5a). The best fit model included 349
both region and wave exposure as fixed effects (GLMM, wi = 0.7451, Appendix D) and models 350
that lacked either of these effects were poor predictors of crab density (GLMM, wi = 0.0093, 351
Appendix D). Predatory (N. lapillus) and herbivorous (T. testudinalis) gastropods were most 352
abundant at southern wave-exposed sites and northern sheltered sites, respectively (Figs. 5b,c). 353
The greatest density of N. lapillus occurred at southern, wave-exposed sites (~150 snails m-2, 354
Fig. 3b) and models without either wave exposure or region received minimal support (GLMM, 355
wi = 0.0002 and < 0.0001 for wave exposure and region, respectively, Appendix D). T. 356
testudinalis density surpassed 10 limpets m-2 at the northern sheltered sites (Fig. 5c), and the best 357
model included both region and wave-exposure as fixed effects (GLMM, wi = 0.6390 Appendix 358
D). Finally, the herbivorous snail, L. littorea, reached densities of 25 snails m-2 at the southern 359
sheltered sites, and was comparatively absent from all other sites (Fig. 5d). The best fit model 360
includes both fixed effects and the interaction (GLMM, wi = 0.9978, Appendix D) and all other 361
models had minimal weight, indicating that although higher densities occurred at sheltered sites 362
in both regions, the magnitude of this effect was greater in the southern than in the northern Gulf. 363
Community Recovery at Wave-Exposed Sites 364
At northern wave-exposed sites, Fucus dominated community recovery and mussels and 365
barnacles were relatively unimportant (Fig. 6, Appendix E). In fact, we observed no mussel 366
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recruits in our plots at these sites and although barnacles recruited to our plots (Fig. 7a, Appendix 367
F), their abundance was relatively low and they never occupied more than 20% of the available 368
space. Surprisingly, the presence and absence of consumers had little impact on recovery (linear 369
contrast, P = 0.2045). In fact, Fucus recovery was strongest in uncaged, open plots reaching 370
100% cover after 2 years, whereas recovery was slower in caged and cage control plots, 371
presumably because of cage abrasion. When cages and cage controls were removed in Fall 372
2005 for photographic sampling, we frequently observed damaged fucoid fronds in our sampling 373
plots (E.S. Bryson, personal observation). 374
Recovery patterns at southern wave-exposed sites were dramatically different (Fig. 6, 375
Appendix E). At these sites, Fucus recruitment was quite low and recovery was dominated by 376
the recruitment and establishment dynamics of barnacle and mussels. In spring 2004, new 377
barnacle recruits dominated all plots regardless of consumer exclusion treatment but by the fall 378
mussels had replaced barnacles as the primary occupier of space. During the winter of 2004-379
2005, mussel density declined in open plots, but remained high in cage and cage control plots. It 380
is unlikely that consumer exclusion drove this pattern because consumers are inactive during 381
winter. Instead, winter disturbance likely caused mussel decline in open plots whereas the 382
physical structure provided by cages and cage controls prevented storm-induced mussel 383
dislodgement (Menge 1976). The following spring (2005) barnacle recruitment into bare patches 384
remained high (Fig. 5a), but was considerably lower in cage and cage control plots where mussel 385
abundance was high (Figs. 6a,c). By fall of 2005, mussel abundance had declined in all plots, 386
possibly because of heat waves during the summer. However, a mix of Fucus, barnacles, and 387
mussels were observed only in open plots where mussel cover had declined over winter and was 388
low in spring 2005 (Fig. 6). Pearson’s correlations indicate that mussel cover in the spring of 389
18
2005 explained over 50% of the variation in barnacle and Fucus cover in the fall of 2005 390
(Pearson’s r = -0.5262, -0.6734, and p < 0.0001, 0.0004 respectively, Table 2). Higher spring 391
mussel cover corresponded to lower barnacle and Fucus cover in the fall. However, mussel 392
cover in the fall of 2005 appeared independent of the barnacle, Fucus or mussel cover the 393
previous spring (Pearson’s r = 0.1391, -0.1399, 0.0575 respectively, p > 0.4157 for all, Table 2). 394
Moreover, the presence and absence of consumers appeared to be unimportant to recovery on 395
these shores. 396
Community Recovery at Sheltered Sites 397
Recovery on northern sheltered sites was remarkably similar to that found on their wave-398
exposed counterparts (Appendix E). Consumer pressure was unimportant to the recovery of 399
Fucus, which dominated all plots (linear contrast, P = 0.4071; Fig. 8). Mussel recruitment and 400
establishment did not occur and barnacle recruitment was low so that barnacles never occupied 401
more than 5% of the available space, regardless of consumer exclusion. 402
In contrast, recovery on southern sheltered sites was strongly influenced by the presence 403
of consumers (Fig. 8, Appendix E). Initial barnacle recruitment in spring 2004 was high at these 404
sites (Fig. 7b), especially in cage and cage controls perhaps because these structures either 405
reduced thermal stress or water velocity, thereby enhancing larval settlement and survivorship. 406
By fall 2004, the effects of consumer exclusion began to emerge. Barnacle abundance declined 407
in open plots and cage controls and both mussels and Fucus began to dominate plots where 408
consumers were excluded. By spring 2005, the positive effects of consumer exclusion on Fucus 409
and mussels intensified. At the end of the experiment, consumer exclusion (caged plots) led to 410
communities dominated by Fucus (~60% canopy cover; linear contrast, caged vs. open, P = 411
0.0026) with an understory of mussels (~20% understory cover; linear contrast, caged vs. open, P 412
19
= 0.0018), barnacles (~35% understory cover; linear contrast, caged vs. open, P = 0.0003) and 413
bare space (~45%). By contrast, in open plots, Fucus still formed a canopy in the presence of 414
consumers despite its relatively lower abundance (~25-30%), and barnacles (~35%) and bare 415
space (~65%) dominated the understory while mussels were generally absent presumably 416
because of predation by green crabs and Nucella. 417
Long-term Ascophyllum Recovery 418
Recovery rates of Ascophyllum on wave-exposed shores differed between northern and 419
southern sites (ANOVA, P < 0.0004, Fig. 9, Appendix G). As expected, Ascophyllum remained 420
absent at southern wave-exposed sites whereas recovery at northern wave-exposed sites became 421
evident after 3 years, reaching ~15% cover after 7 years. On sheltered shores, Ascophyllum 422
recovery occurred at both northern and southern sites but was more substantial (ANOVA, P = 423
0.0224) at the northern sites reaching 40-50% cover after 8 years. 424
DISCUSSION 425
Our survey of 34 established rocky intertidal communities throughout the Gulf of Maine 426
revealed substantial differences in the distribution and abundance of key shared species that 427
likely influence how these communities are organized. In the northern Gulf, sites had a dense 428
canopy of Ascophyllum regardless of wave exposure and barnacles and mussels were either rare 429
or altogether absent. In the southern Gulf, extant community structure was consistent with 430
previous work (Menge 1976, Menge 1978a,b, Lubchenco 1980, Bertness et al. 2004a) showing 431
that barnacles, mussels and Fucus dominate wave-exposed shores and Ascophyllum dominates 432
sheltered shores. Communities in the Penobscot region of central Maine were generally aligned 433
with those on sheltered and wave-exposed shores in the southern Gulf. However, one wave-434
exposed site (Milbridge, Maine) with abundant Ascophyllum was more consistent with 435
20
communities typical of northern wave-exposed sites. In addition, a sheltered site in this region 436
(Grindstone Neck, Maine) was dominated by Fucus and barnacles rather than Ascophyllum and 437
was therefore more similar to wave-exposed sites in the southern region. Recovery patterns after 438
disturbance reinforced the notion that communities in the northern and southern Gulf are 439
organized differently. 440
Consumer Driven Dynamics in the Southern Gulf of Maine 441
Recovery in the southern Gulf indicates that the strong influence of recruitment, 442
competition for space, and consumer control on community organization depends on wave 443
exposure, which is consistent with previous research (Menge 1976, 1978a,b, Lubchenco and 444
Menge 1978, Bertness 2004a). On wave-exposed shores, barnacles recruited densely in the 445
spring of 2004, but were replaced by mussels in the fall. This transition may reflect barnacle 446
facilitation of mussel recruitment, which has been observed by others within the Gulf of Maine 447
(Menge 1976, Petraitis 1987). The subsequent impact of physical factors (e.g., thermal stress 448
and storm-induced dislodgement) likely drove cyclical patterns in mussel cover, which when 449
high, shaped subsequent recovery patterns by overgrowing barnacles and limiting the space 450
available for Fucus establishment. For example, barnacle recruitment in the year (2005) 451
following mussel establishment (Fig. 6) was much lower despite remarkably high and consistent 452
barnacle supply over the 3 years it was measured (Fig. 7a) and the abundance of Fucus remained 453
relatively low in cages and cage controls throughout the 2 year experiment. Only in open plots, 454
where mussel populations declined over winter because of dislodgement by storms (Menge 455
1976, Paine and Levin 1981, Denny et al. 1985, Hunt and Scheibling 2001, Carrington 2002), 456
did Fucus and barnacles establish larger populations. Thus, although open plots at wave-457
exposed sites included a mix of all three primary space occupying species, rather than mussel 458
21
dominance as observed by Menge (1976), the increase in both Fucus and barnacles after the 459
spring of 2005 appeared to largely hinge on mussel dynamics. These cyclical patterns of mussel 460
dominance are likely driven by variation in disturbance rather than by interactions with barnacles 461
and Fucus (Table 2). We suggest that this high recruitment-high turnover system creates 462
unstable biotic secondary substratum that may contribute to the lower recovery of Fucus and to 463
the absence of Ascophyllum from wave-exposed shores in this region. 464
Previous work has shown that Nucella can strongly control the abundance of barnacles 465
and mussels on wave-exposed shores in this region (Bertness et al. 2004a), but our experiment 466
provided no evidence of consumer control at these sites. Although high wave energies can limit 467
the effectiveness of Nucella (Burrows and Hughes 1989, Etter 1989, 1996), we were surprised to 468
find no evidence of consumer control because all aspects of our experimental cages, cage 469
controls and open plots were identical to those used by Bertness et al. (2004a) in southern Maine. 470
These disparate patterns of consumer effects on wave-exposed shores may reflect regional 471
differences within the southern Gulf of Maine similar to those observed by Kordas and Dudgeon 472
(2011) who found weaker consumer effects on Ascophyllum in Massachusetts than in southern 473
Maine. Thus, Nucella-barnacle and Nucella- mussel interactions may be stronger in southern 474
Maine than in Massachusetts where caging artifacts overrode any consumer effects. 475
Nevertheless, the resulting impacts of cages on mussels influenced subsequent recovery. For 476
example, mussel abundance after the first settlement season in fall 2004 was high, occupying 477
~60% of the available space in all treatments, but had declined only in open plots by the 478
following spring. Because cage controls maintained the same high mussel abundance as full 479
cages, we suggest that the physical structure provided by both cages and cage controls had a 480
positive effect on mussels by reducing the risk of dislodgement during winter storms. Indeed, 481
22
observations at our southern wave-exposed sites in the winter of 2004-2005 after storms revealed 482
substantial unoccupied space in our open plots, indicating that physical stress, rather than species 483
interactions, caused this decline. By fall 2005, cages and cage controls were full of empty 484
mussels, sand and shell hash, which negatively impacted mussel survival as well as the few 485
Fucus individuals present. Thus, the disparate patterns of consumer effects on mussels at wave-486
exposed sites between this study (i.e., reduced consumer pressure) and past work (Bertness et al. 487
2004a) may reflect either greater thermal stress, greater wave exposure, or both, at our sites in 488
Massachusetts. 489
On sheltered sites in the southern Gulf, the presence of consumers strongly influenced the 490
recovery of Fucus and mussels (Fig. 8). After 1 year of recovery, a Fucus canopy with a mix of 491
mussels and barnacles in its understory developed when consumers were excluded. When 492
consumers were present, however, bare space dominated plots with moderate cover of Fucus and 493
barnacles after 2 years. Although adult fucoids are relatively resistant to snail grazing, L. littorea 494
was abundant at these sites (Fig. 5d) and it can slow fucoid recovery by consuming germlings 495
and young recruits before they attain a size refuge and begin to produce chemical and structural 496
defenses (Lubchenco and Gaines 1981, Lubchenco 1983, Barker and Chapman 1990, Rhode et 497
al. 2004). Those Fucus that had escaped snail grazing, either via substratum or size-related 498
refugia (Lubchenco 1983), eventually led to this alga being more prevalent even in open plots 499
(~25% cover) after 2 years of recovery. 500
Consumer exclusion clearly enhanced mussel recovery presumably by preventing green 501
crabs, which were also abundant at these sites (Fig. 5a), from accessing them. Even after 2 502
years, mussels were not present in open plots, suggesting that the effects of consumer control by 503
green crabs on this species is stronger than that imposed by L. littorea on Fucus. This control of 504
23
mussel abundance, coupled with Fucus escapes from grazing, will presumably lead to even 505
greater Fucus abundance over the longer term (Menge 1976, 1978a, Lubchenco 1980, 1982, 506
1983, Bertness et al. 2004a). In contrast, we saw no strong evidence of consumer control on 507
barnacle abundance, perhaps because their primary predator, Nucella, was not abundant at these 508
sites (Fig. 5b). 509
Recruitment Limitation in the Northern Gulf of Maine 510
A striking feature of communities in the northern Gulf was that mussels and barnacles 511
were unimportant to community recovery on both wave-exposed and sheltered shores. Unlike 512
their southern counterparts, mussel recruitment and establishment was nonexistent and barnacle 513
recruitment and abundance was quite low at all sites in the northern Gulf (Figs. 6, 7, 8); these 514
recruitment patterns have continued in the years following this study (Bryson and Trussell, 515
unpublished). 516
In the northern Gulf, currents move southward along the Scotian shelf before flowing 517
northward to the mouth of the Bay of Fundy where intense tide-driven mixing occurs and the 518
southwestward movement of the Eastern Maine Coastal Current (EMCC) begins (Xue et al. 519
2000, Pettigrew et al. 2005). The proximity of the EMCC to the eastern Maine coastline can 520
vary seasonally and annually (Hetland and Signell 2005, Pettigrew et al. 2005) but analyses of 521
drifter data suggest high connectivity between Cutler, Maine (in the northern region) and sites in 522
western Nova Scotia (Manning et al. 2009). However, results of an experimental particle release 523
on the western coast of Nova Scotia suggest that planktonic larvae do not accumulate in eastern 524
Maine (Xue et al. 2008) because they either become entrained within the Bay of Fundy, 525
aggregate near Penobscot Bay, or are driven offshore. Moreover, it is unlikely that planktonic 526
larvae are transported northward from southern populations due to the strong southwestward 527
24
prevailing flow of the EMCC, which can exceed 0.15 m s-1 (Pettigrew et al. 2005, Manning et al. 528
2009, Tilburg et al. 2012). Finally, freshwater input from the St. Croix River into 529
Passamaquoddy Bay along the mouth of the Bay of Fundy (Pettigrew et al. 2005) may restrict 530
larval transport from either within the Bay of Fundy or from the Scotian shelf to this region. 531
Thus, the limited barnacle and mussel recruitment in the northern Gulf is likely derived from 532
either the sparse local populations or larvae from more northern populations that deviate from 533
prevailing flow patterns. This low recruitment may relax competition for space and may 534
promote algal dominance in these communities. 535
Although we suggest that local and meso-scale oceanographic conditions are responsible 536
for geographic variation in recruitment in the Gulf, more detailed studies of larval transport 537
along the Gulf of Maine coast will be essential to better address the role that oceanography plays 538
in shaping geographic variation in recruitment. Recent studies have improved the clarity and 539
detail of summer circulation patterns in the Gulf of Maine (Pettigrew et al. 1998, 2005, Churchill 540
et al. 2005, Hetland and Signell 2005, Manning et al. 2009), but winter circulation patterns are 541
less understood (but see Xue et al. 2000), which is unfortunate because barnacle larvae in the 542
Gulf are typically released during January and February. 543
The relative absence of consumers also may contribute to fucoid algal dominance on 544
northern Gulf shores (Figs. 6, 8), and we saw no evidence of consumer control on either Fucus 545
vesiculosus or Ascophyllum nodosum. For example, grazing by the herbivorous snail L. littorea 546
can slow fucoid algal recovery (Lubchenco and Gaines 1981, Lubchenco 1983, Barker and 547
Chapman 1990, Trussell et al. 2002, 2003), but this grazer was conspicuously absent from our 548
study sites and many others in the region perhaps due to either low recruitment or intense 549
harvesting (Bryson & Trussell, personal observations). Moreover, limpets (T. testudinalis) were 550
25
present at northern sites, particularly on sheltered shores, but previous work (Steneck 1982, 551
Steneck and Watling 1982, Watson and Norton 1987) and our results indicate that they do not 552
influence fucoid algal recovery. Our results suggest that both the relative absence of consumers 553
and low barnacle and mussel recruitment in the northern Gulf may contribute to fucoid algal 554
dominance in this region. This pattern is consistent with experimental work in the eastern 555
Atlantic where mussel recruitment is often patchy (Jenkins et al. 2008). In the eastern Atlantic, 556
fucoid algae recover quickly and dominate wave-exposed shores when either patellid limpets are 557
experimentally excluded (Hawkins 1981, Hawkins et al. 1992, Jenkins et al. 1999, 2005, 558
Coleman et al. 2006) or outside of their bioegeographic range (Cervin et al. 2004, Ingolfsson and 559
Hawkins 2008). Moreover, although competitive interactions between mussels and fucoid algae 560
have received little attention in Europe, there is evidence that suppression of mussels by crab 561
predators promotes the establishment of fucoid canopies (Janke 1990). 562
We should also note that increased nutrient availability in the northern Gulf of Maine 563
might contribute to the rapid recovery of fucoid algae in this region. High levels of inorganic 564
nutrients (nitrate, nitrite) occur within the EMCC (Pettigrew et al. 1998, Townsend et al. 2001) 565
due to upwelling caused by cyclonic circulation over Jordan basin and intense tidal flushing 566
(Townsend et al. 1987). Thus, the combined effects of weak top-down control and bottom-up 567
effects on nutrient availability and the recruitment of invertebrate competitors may ultimately 568
drive algal dominance in the northern Gulf. 569
Long-term Ascophyllum Recovery 570
Long-term monitoring of open plots revealed that Ascophyllum recovery is consistent 571
with previous work in the southern Gulf: Ascophyllum did not become established on wave-572
exposed shores (Fig. 9). In contrast, Ascophyllum began to recover on sheltered shores in the 573
26
southern Gulf, even in the presence of consumer pressure, achieving ~3-8% on sheltered shores 574
after 8 years. 575
Perhaps more interesting was the dominance of Ascophyllum in our community surveys 576
(Fig. 3a,b, Table 1) and its observed recovery (Fig. 9) at all of our northern wave-exposed sites. 577
In contrast to mussel and barnacle dominance on southern wave-exposed shores, dense 578
Ascophyllum canopies dominated these shores in the northern Gulf. Although it has long been 579
held that Ascophyllum is unable to achieve high abundance on wave-exposed shores in the Gulf 580
of Maine due to wave stress (Vadas et al 1990,) or competition from high densities of mussels 581
and barnacles (Dudgeon and Petraitis 2001), this species can become established on wave-582
exposed shores in the northeastern Atlantic (Jenkins et al. 2008). Ascophyllum recovery on 583
sheltered shores was more rapid in the north than the south, presumably because of the scarcity 584
of grazers like L. littorea, which can affect Ascophyllum recovery (Trussell et al. 2002). 585
Continued monitoring of these plots indicates that Ascophyllum may eventually replace Fucus as 586
the dominant canopy-forming alga on sheltered shores, which contradicts previously 587
hypothesized Fucus dominance once its becomes established (McCook and Chapman 1993, 588
1997, Dudgeon and Petraitis 2001). Ascophyllum recovery and dominance on wave exposed and 589
sheltered shores may occur because Ascophyllum is a more northern, boreal species than Fucus 590
(Vadas et al. 2004, Jenkins et al. 2008, Svensson et al. 2009), there is less competition from 591
mussels and barnacles (McCook and Chapman 1993, 1997, Dudgeon and Petraitis 2001), and the 592
EMCC may increase nutrient availability (Townsend et al. 1987, 2001, Pettigrew et al. 1998). 593
Regional Community Dynamics in the Gulf of Maine? 594
Views of how rocky intertidal communities are organized have long focused on the 595
dominant role of top-down, or consumer control (Paine 1966, Menge 1976, 1978a, b, Lubchenco 596
27
1983, Bertness et al. 2002, 2004a,b, Jenkins et al. 2005, 2008, Coleman et al. 2006, Davies et al. 597
2007). More recently, however, growing evidence suggests that coastal oceanography and 598
resulting bottom-up forcing can strongly influence these communities (Bustamante et al. 599
1995a,b, Menge et al. 1997, 2003, Menge 2000, Menge and Branch 2001, Leslie et al. 2005, 600
Navarrete et al. 2005, Barth et al. 2007, Blanchette & Gaines 2007, Blanchette et al. 2008, 601
Broitman et al. 2008, Witman et al. 2010, Benedetti-Cecchi and Trussell 2013, Menge and 602
Menge 2013). For example, shifts from persistent upwelling in central and northern California to 603
intermittent upwelling along the coast of Oregon are associated with marked increases in 604
barnacle recruitment (Connolly and Roughgarden 1998, Connolly et al. 2001, Broitman et al. 605
2008, Krenz et al. 2011, Menge et al. 2011) and similar relationships between upwelling, 606
recruitment patterns and onshore community structure have been documented in New Zealand 607
(Menge et al. 1999), Chile (Lagos et al. 2005, Navarrete et al. 2005) and the Galapagos Islands 608
(Witman et al. 2010) 609
Compared to rocky shore communities on many western coastlines (e.g., US Pacific 610
coast, Chilean coast), coastal upwelling is relatively unimportant in the Gulf of Maine. Although 611
the influence of oceanographic processes on onshore community organization have been less 612
intensively studied in the Gulf of Maine, coastal downwelling may contribute to the patterns we 613
observed. The rapid southward movement of surface waters of the EMCC in the northern Gulf 614
and the slower, southward flow of the WMCC in the southern Gulf may create conditions of 615
strong and weak coastal downwelling in the north and south, respectively. Recent studies 616
indicate that strong downwelling can reduce ecological subsidies, larval recruitment, and growth 617
as well as weaken species interactions in New Zealand (Menge et al. 2002, 2003, Menge and 618
Menge 2013), and we observed similar patterns in the northern Gulf. However, the importance 619
28
of downwelling in this system remains unclear because the prevailing flow of the EMCC 620
opposes the prevailing northwestward wind direction in the GOM. Thus, more research is 621
necessary to address the strength and potential impacts of downwelling in the Gulf of Maine. 622
Although the precise mechanism remains unclear, it appears that regional variation in 623
coastal oceanography, which is characterized by distinct cyclonic circulation and along-shore 624
currents (Brooks 1985, Pettigrew et al. 1998, 2005, Xue et al. 2008), strongly drives barnacle and 625
mussel recruitment that is consistently low and high in the northern and southern Gulf, 626
respectively. Coastal oceanography, in addition to intense human harvesting in the north, may 627
also drive the north-south increase in the abundance of L. littorea, which, like barnacles and 628
mussels, has a planktonic larval phase. Thus, we suggest that the deterministic recruitment 629
variation between the northern and southern Gulf is a primary driver of disparate community 630
organization in these two regions, particularly on wave-exposed shores. In the north, consumers 631
were rare and thus unimportant to recovery, and low barnacle and mussel recruitment may allow 632
fucoid algae, particularly Ascophyllum, to dominate both sheltered and wave-exposed shores. In 633
the south, high barnacle and mussel recruitment and ensuing disturbance and competitive 634
dynamics appeared to be most important on wave-exposed shores. Moreover, we observed 635
strong consumer control only at southern sheltered sites, which suggests that consumer control 636
may not be a pervasive feature of Gulf of Maine rocky shores. 637
Our study cannot directly address the possibility of alternative stable community states 638
driven by recruitment variation because our clearings were below the size threshold (12m2) 639
thought necessary (Dudgeon and Petraitis 2001, Petraitis and Dudgeon 2004) for the 640
development of alternative community states. However, indirect evidence suggests that the 641
Penobscot Region, the location of studies by Petraitis and Dudgeon, may have the conditions 642
29
necessary for the emergence of alternative (barnacle and mussel versus Ascophyllum) dominated 643
community states. Unlike the southern Gulf, consumer pressure is relaxed in this region and 644
unlike the northern Gulf there is the potential for high barnacle and mussel recruitment that 645
varies in space and time (Dudgeon and Petraitis 2001). For example, this region has many small 646
bays that may retain barnacle and mussel larvae either because of differences in flushing rates 647
(e.g., Gaines and Bertness 1992) or because of onshore-offshore movement of the thermal 648
boundary established by the EMCC that may strongly dictate larval transport (Hayhurst and 649
Rawson 2009, Owen and Rawson 2013). Finally, our community surveys revealed high affinity 650
between sites in the Penobscot Region and those in the southern Gulf, but two Penobscot sites 651
diverged from this pattern. One sheltered site in the Penobscot Region had high Fucus and 652
barnacle abundance and one wave-exposed site had high Ascophyllum abundance. Although 653
more work is clearly needed, these patterns are certainly consistent with the outcome expected 654
from substantial recruitment variation and relaxed consumer pressure rather than that produced 655
by deterministic consumer control. 656
In summary, our study reveals that despite largely sharing the same suite of species, the 657
factors dictating rocky shore community organization differ substantially across the Gulf of 658
Maine. Long-standing views of community organization that were primarily shaped by classic 659
work in the south do not apply in the northern Gulf and may be unreliable in the Penobscot 660
region. Although these conclusions emerged because of the broad scale nature of this study, it is 661
clear that attention to both local and regional factors is also needed to more fully understand 662
pattern and process. 663
664
665
30
ACKOWLEDGMENTS 666
We thank G. Bernatchez, M. Doellman, T. Dwyer, and C. Matassa for their assistance in 667
the field, C. Matassa for her assistance in photograph analysis, and P. Petraitis, M. Bertness, M. 668
Bracken, S. Vollmer and three anonymous reviewers for their valuable input of this manuscript. 669
We are also grateful to S. Navarrete for his considerable and constructive advice and T. Gouhier 670
for helping generate the map for the Gulf of Maine. This work was submitted in partial 671
fulfillment of the requirements for the PhD in Ecology, Evolution and Marine Biology from 672
Northeastern University and was supported by grants from the US National Science Foundation 673
to G.C.T. (OCE-0240265, OCE-0727628) and Sigma Xi to E.S.B. This is contribution no. 303 674
from the Marine Science Center and the Department of Marine and Environmental Sciences. 675
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SUPPLEMENTAL MATERIAL 995
Appendix A: Study sites, listed from south to north, used to assess natural community structure. 996
Sites are categorized based upon oceanographic region (Southern, Penobscot or Northern) and 997
wave energy (Sheltered, Wave-exposed). 998
999
Appendix B: Results of a 2-factor multivariate ANOVA assessing variance in community 1000
structure with geographic region and wave exposure as fixed factors using a Bray-Curtis index 1001
and 999 permutations. 1002
45
Appendix C: Average percent similarity between geographic region or both high and low wave 1003
energy regimes based upon SIMPER analyses of Bray Curtis similarities, and the contributions 1004
of dominant space-occupiers (Ascophyllum nodosum, Fucus vesiculosus, Mytilus spp., 1005
Semibalanus balanoides) and Bare Rock to the dissimilarity between sites. 1006
1007
Appendix D: Akaike weights of full and reduced Generalized Linear Mixed Models with 1008
Negative Binomial Error Distribution to examine differences in consumer density due to region 1009
and wave exposure. 1010
1011
Appendix E: Results of a 4-factor nested ANOVA on the percent cover of sessile species and 1012
effect sizes (η2). 1013
1014
Appendix F: Results of a 4-factor nested ANOVA on Semibalanus balanoides recruitment 1015
density. 1016
1017
Appendix G: Analyses of Ascophyllum nodosum percent cover in the Fall of 2011. 1018
1019
1020
1021
1022
1023
1024
46
Table 1: Average percent similarity between wave-exposed and sheltered sites in each 1025
geographic region based upon SIMPER analyses of Bray Curtis similarities, and the 1026
contributions of dominant space-occupiers (Ascophyllum nodosum, Fucus vesiculosus, Mytilus 1027
spp., Semibalanus balanoides) and Bare Space to the dissimilarity between sites. 1028
1029
Region Species Exposed
Abundance
Sheltered
Abundance
Contribution to
Dissimilarity (%)
Southern
A. nodosum
4.18 86.20 34.98
F. vesiculosus 71.56 12.60 24.87
Mytilus sp. 16.58 1.27 6.36
S. balanoides 44.74 44.53 5.11
Bare Rock 17.70 27.93 6.68
Penobscot
A. nodosum
30.00 73.00 28.49
F. vesiculosus 66.65 24.87 27.41
Mytilus sp. 4.40 0.00 2.44
S. balanoides 37.90 34.40 10.85
Bare Rock 21.10 22.00 4.64
Northern
A. nodosum
95.90 98.60 4.49
F. vesiculosus 2.80 1.20 3.63
47
Mytilus sp. 0.00 0.00 0.00
S. balanoides 0.20 1.90 2.32
Bare Rock 32.80 45.30 24.88
1030
1031
1032
1033
1034
1035
1036
1037
1038
1039
1040
1041
1042
1043
1044
1045
1046
1047
1048
48
Table 2. Matrix of Pearson’s r correlations between the percent cover of dominant space 1049
occupying species (Semibalanus balanoides, Mytilus sp. and Fucus vesiculosus) in the spring and 1050
fall of 2005. N=36 for all correlations and asterisks indicate corresponding p-values <0.01. 1051
1052
S. balanoides cover Spring 2005
Fucus cover Spring 2005
Mytilus sp. cover Spring 2005
S. balanoides cover Fall 2005
0.7861* -0.1083 -0.5262*
Fucus cover Fall 2005
0.1256 0.4915* -0.6734*
Mytilus sp. cover Fall 2005
0.1391 -0.1399 0.0575
1053
1054
1055
1056
1057
1058
1059
1060
1061
1062
1063
1064
1065
49
FIGURE LEGENDS 1066
Figure 1. Map of the Gulf of Maine with prevailing oceanographic currents. The Eastern Maine 1067
Coastal Current (EMCC, blue) flows southwesterly along the coast from the mouth of the Bay of 1068
Fundy until the Penobscot Bay region, at which point water either moves offshore or continues 1069
southwesterly to form the Western Maine Coastal Current (WMCC, red). Also shown are the 1070
Nova Scotia Current (black) and cyclonic circulation around Jordan Basin (yellow). Points along 1071
the coastline indicate sites where community structure surveys were conducted. Due to the 1072
proximity of some sites, some points may overlap. Blue triangles indicate sites in the Northern 1073
region, black circles indicate sites in the Penobscot region, and red squares indicate sites in the 1074
Southern region. Solid points indicate wave-exposed sites and open points indicate sheltered 1075
sites; the symbols for some site overlap. 1076
1077
Figure 2. Two-dimensional Non-metric Multidimensional Scaling (NMDS) plot constructed 1078
using the ‘metaMDS’ function with a Bray-Curtis distance index of untransformed community 1079
structure data (Stress = 0.07876). Each point represents a single site and ellipses represent 95% 1080
confidence intervals of the mean ordination for each region and exposure combination. Blue 1081
triangles indicate northern sites, black circles indicate Penobscot sites and red squares indicate 1082
southern sites. Solid points and lines indicate wave-exposed sites and open points and dashed 1083
lines indicate sheltered sites. 1084
1085
Figure 3. Average percent cover of dominant space-occupying species and bare rock in 1086
established communities on wave-exposed shores: (A) Fucus, (B) Ascophyllum, (C) 1087
50
Semibalanus, (D) Mytilus sp. and (E) Bare Rock. On the x-axis, sites are ordered by latitude 1088
from southernmost (left) to northernmost (right). 1089
1090
Figure 4. Average percent cover of dominant space-occupying species and bare rock in 1091
established communities on sheltered shores: (A) Fucus, (B) Ascophyllum, (C) Semibalanus, (D) 1092
Mytilus sp. and (E) Bare Rock. On the x-axis, sites are ordered by latitude from southernmost 1093
(left) to northernmost (right). 1094
1095
Figure 5. Average density of mobile consumers on wave-exposed (black bars) and sheltered 1096
(stippled bars) shores in the southern and northern Gulf of Maine. (A) Carcinus maenas and (B) 1097
Nucella lapillus are important consumers of barnacles (Semibalanus balanoides) and mussels 1098
(Mytilus spp.) and the herbivorous gastropods (C) Tectura testudinalis and (D) Littorina littorea 1099
consume algae. Error bars indicate 1 standard error of the mean and n = 20 at each location and 1100
wave exposure. Note: y-axis scale varies for each consumer. 1101
1102
Figure 6. Mean (±SE) percent cover of the dominant space-occupying organisms (A) 1103
Semibalanus balanoides, (B) Fucus vesiculosus, and (C) Mytilus spp. over 2 years on wave-1104
exposed shores in the southern (red lines) and northern (blue lines) Gulf of Maine. Effects of the 1105
presence (open plots, circles) and absence (cage, squares) of consumers and cage controls 1106
(triangles) are also shown. Although recovery through time is shown, only end point data were 1107
analyzed. 1108
1109
51
Figure 7. Mean (± SE) recruitment density (no. m-2) of Semibalanus balanoides into 1110
experimental recruitment clearings in the spring of 2004-2006 on (A) wave-exposed and (B) 1111
sheltered shores in the southern (red bars) and northern (blue bars) Gulf of Maine. 1112
1113
Figure 8. Mean (±SE) percent cover of the dominant space-occupying organisms (A) 1114
Semibalanus balanoides, (B) Fucus vesiculosus, and (C) Mytilus spp. over 2 years on sheltered 1115
shores in the southern (red lines) and northern (blue lines) Gulf of Maine. Effects of the 1116
presence (open plots, circles) and absence (cage, squares) of consumers and cage controls 1117
(triangles) are also shown. Although recovery through time is shown, only end point data were 1118
analyzed. 1119
1120
Figure 9. Mean (± SE) percent cover of Ascophyllum nodosum in open plots on (A) wave-1121
exposed and (B) sheltered shores in the southern (red lines) and northern (blue lines) Gulf of 1122
Maine. We monitored the recovery of open plots from the original manipulative recovery 1123
experiment on sheltered shores for 8 years beginning in 2004. Because of unanticipated changes 1124
in site accessibility, we were only able to monitor recovery at one wave-exposed site in the 1125
northern Gulf and two wave-exposed sites in the southern Gulf for 7 years beginning in early 1126
2005. Note that for the southern wave-exposed sites there was no recovery so data points for 1127
each site overlap. Although recovery through time is shown, only end point data were analyzed 1128
and data points and error bars reflect standard errors of the mean. 1129
1130
52
Figure 1. 1132
1133
1134
1135
1136
1137
1138
1139
1140
1141
1142
1143
1144
1145
1146
1147
1148
1149
1150
1151
1152
1153
1154
−71 −70 −69 −68 −67 −66 −65 −64
4041
4243
4445
4647
Longitude (°W)
Latit
ude
(°N
)
Maine
MA
NH
Nova Scotia
New Brunswick
Bay of Fundy
−1.0 −0.5 0.0 0.5 1.0
−0.5
0.0
0.5
NMDS1
NM
DS2
North ExposedNorth ShelteredPenob. ExposedPenob. ShelteredSouth ExposedSouth Sheltered
54
Figure 3. 1168
A B 1169
1170
C D 1171
1172
E 1173
1176
1177
1178
1179
1180
0
20
40
60
80
100
Fucu
s Pe
rcen
t Co
ver
0
20
40
60
80
100
Asco
phyl
lum
Per
cent
Cov
er
0
20
40
60
80
100
Sem
ibal
anus
Per
cent
Cov
er
0
20
40
60
80
100
Myt
ilus
sp. P
erce
nt C
over
0
20
40
60
80
100
Turr
ett
Cunn
er L
edge
East
Poi
ntPi
geon
Cov
eCa
pe N
eddi
ckCa
pe E
lizab
eth
Gian
t St
eps
Pem
equi
d Pt
.Ch
ambe
rlain
Pt.
Cham
berla
in E
ast
Bass
Har
bor
Otte
r Pt
.Sc
hood
ic P
t.M
cLel
lan
Park
Wes
tern
Hea
dHa
milt
on C
ove
Quod
dy H
ead
Quod
dy L
ight
Bare
Roc
k Per
cent
Cov
er
55
Figure 4. 1181
A B 1182
1183
C D 1184
1185
E 1186
1187
1188
1189
1190
1191
1192
0
20
40
60
80
100
Fucu
s Pe
rcen
t Co
ver
0
20
40
60
80
100
Asco
phyl
lum
Per
cent
Cov
er
0
20
40
60
80
100
Sem
ibal
anus
Per
cent
Cov
er
0
20
40
60
80
100
Myt
ilus
sp. P
erce
nt C
over
0
20
40
60
80
100
Cano
e Be
ach
Fort
y St
eps
Past
For
tyLo
bste
r Co
ve
Cham
berla
in B
ayPo
rt C
lyde
New
port
Cov
e
Bar
Harb
orGr
inde
ston
e Ne
ck
Fraz
er P
oint
So.
Addi
son
Roqu
e Bl
uffs
Stea
mbo
at W
harf
Carr
ying
Cov
e
Nort
h Qu
oddy
Coas
t Gu
ard
Bare
Roc
k Per
cent
Cov
er
56
Figure 5. 1193
A B 1194
1195
1196
1197
1198
1199
1200
1201
C D 1202
1203
1204
1205
1206
1207
1208
1209
1210
1211
1212
1213
1214
0
5
10
15
20
Tect
ura
test
udin
alis
dens
ity (
no. m
-2)
South North0
10
20
30
40
50
LItt
orin
a lit
tore
a den
sity
(no.
m-2
)
South North
0
1
2
3
4
5ExposedSheltered
Carc
inus
mae
nas d
ensit
y (n
o. m
-2)
South North0
50
100
150
200
Nuce
lla la
pillu
s den
sity
(no.
m-2
)
South North
57
Figure 6. 1215
A 1216
1217 1218
1219
1220
1221
1222
B 1223
1224
1225
1226
1227
1228
1229
C 1230
1231
1232
1233
1234
1235
1236
0
20
40
60
80
100
S F S F
Barn
acle
Per
cent
Cov
er
2004 2005
O
C O C CC
CC
0
20
40
60
80
100
S F S F
Fucu
s Pe
rcen
t Co
ver
2004 2005
O
O
C
C
CC
CC
0
20
40
60
80
100
S F S F
Mus
sel P
erce
nt C
over
2004 2005
O
O C CC
CCC
58
Figure 7. 1237
A 1238
1239
1240
1241
1242
1243
1244
B 1245
1246
1247
1248
1249
1250
1251
1252
1253
1254
1255
1256
1257
1258
10
102
103
104
105
106
2004 2005 2006
Barn
acle
Rec
ruitm
ent
Dens
ity (
no. m
-2) Wave Exposed
10
102
103
104
105
106
2004 2005 2006
Barn
acle
Rec
ruitm
ent
Dens
ity (
no. m
-2) Sheltered
59
Figure 8. 1259
A 1260
1261
1262
1263
1264
1265
1266
B 1267
1268
1269
1270
1271
1272
1273
C 1274
1275
1276
1277
1278
1279
1280
0
20
40
60
80
100
S F S F
Barn
acle
Per
cent
Cov
er
2004 2005
O
C CC
C CC O
0
20
40
60
80
100
S F S F
Fucu
s Pe
rcen
t Co
ver
2004 2005
O
CCO
CC
CC
0
20
40
60
80
100
S F S F
Mus
sel P
erce
nt C
over
2004 2005
C
CC OC CC O
60
Figure 9. 1281
A 1282
1283 1284
1285
1286
1287
1288
1289
1290
B 1291
1292
1293
1294
1295
1296
1297
1298
1299
1300
1301
1302
0
10
20
30
40
50
60As
coph
yllu
m P
erce
nt C
over
05 06 07 08 09 10 11
Wave Exposed
0
10
20
30
40
50
60
Asco
phyl
lum
Per
cent
Cov
er
Sheltered
04 05 06 07 08 09 10 11