Broad-scale geographic variation in the organization of rocky intertidal communities in the Gulf of Maine

Ecological Monographs, 84(4), 2014, pp. 579 597 Ó 2014 by the Ecological Society of America Broad-scale geographic variation in the organization of rocky intertidal communities in the Gulf of Maine ELIZABETH S. BRYSON, 1 GEOFFREY C. TRUSSELL, 1,3 AND PATRICK J. EWANCHUK 2 1 Marine Science Center and Department of Marine and Environmental Sciences, Northeastern University, 430 Nahant Road, Nahant, Massachusetts 01908 USA 2 Department of Biology, Providence College, Providence, Rhode Island 02912 USA Abstract. A major challenge facing ecology is to better understand how large-scale processes modify local-scale processes to shape the organization of ecological communities. Although the results of ecological experiments are repeatable on local scales, different results often emerge across broad scales, which can hinder the development of general predictions that apply across the geographical range of a community. Numerous studies in the southern Gulf of Maine have shaped our understanding of community organization and dynamics on New England rocky intertidal shores, where consumers strongly control recovery from disturbance on sheltered shores, and high invertebrate recruitment and competition for space dictate recovery on wave-exposed shores. It is unclear, however, whether the effects of consumers and recruitment variation on resulting community organization in this region apply more broadly to rocky intertidal habitats throughout the Gulf. We characterized variation in rocky intertidal community structure at 34 sites throughout the Gulf of Maine and experimentally examined the influence of consumers (present, absent) and wave energy (wave-exposed, sheltered) on community recovery from disturbance in the northern and southern Gulf. Our results reinforced previous work in the southern Gulf, because consumers dictated the recovery of fucoid algae and mussels on sheltered shores, whereas high barnacle and mussel recruitment and competition for space shaped recovery on wave-exposed shores. However, on sheltered shores in the northern Gulf, neither consumers nor barnacle and mussel recruitment impacted recovery, which was dominated by fucoid algae. Moreover, recovery on wave-exposed shores in the northern Gulf was quite distinct from that observed in the southern Gulf; barnacle and mussel recruitment was negligible and fucoid algae dominated recovery, including the long-term establishment of Ascophyllum nodosum, which is largely absent from wave-exposed shores in the southern Gulf. Thus, distinct community types emerged in the northern and southern Gulf despite their sharing of many of the same species. These patterns likely emerged because of regional differences in coastal oceanography that modulate the recruitment of barnacles and mussels. Hence, increased attention to regional factors should provide key insight into how rocky-shore communities are organized in the Gulf of Maine and elsewhere. Key words: coastal oceanography; community organization; competition; disturbance; Gulf of Maine; herbivory; predation; recruitment; rocky intertidal. INTRODUCTION A central goal of ecology is to understand how largescale processes modify local-level processes to shape the distribution and abundance of species, and the organization and dynamics of ecological communities (Wiens 1989, Levin 1992, Hastings 2010, McGill 2010). Because environmental gradients across larger scales can modify, for example, community assembly (Chase 2010, Hein and Gillooly 2011), the relative importance of bottomup and top-down processes (Menge 2000, Navarrete et al. 2005, Chase et al. 2010, Krenz et al. 2011), and the nature, intensity and scale of species interactions (Shurin Manuscript received 12 June 2013; revised 6 February 2014; accepted 25 February 2014. Corresponding Editor: S. A. Navarrete. 3 Corresponding author. E-mail: g.trussell@neu.edu 579 and Allen 2001, Chase 2003, Sanford and Worth 2010, Menge et al. 2011), it is difficult to derive overarching assembly rules for community ecology. Understanding how differences in biotic and abiotic context mediate changes in species interactions, and ultimately community organization has been identified as a major gap in ecology (Agrawal et al. 2007, Weiher et al. 2011). Rocky intertidal communities in the southern Gulf of Maine have long served as a model system to understand how abiotic and biotic factors influence succession after disturbance and resulting community organization (Menge 1976, 1978a, b, Lubchenco 1980, 1983, Petraitis 1987, Petraitis and Dudgeon 1999, Dudgeon and Petraitis 2001, Bertness et al. 2002, 2004a, b). A defining feature of these and other rocky shores is the amount of wave action they experience (i.e., wave-exposed vs. sheltered), which can influence larval and nutrient flux

580 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 rates (Leonard et al. 1998, Jenkins and Hawkins 2003, Bertness et al. 2004b), the availability of space via disturbance (Paine and Levin 1981, Denny et al. 1985), the extent of air exposure as a result of wave splash (Harley and Helmuth 2003), and the abundance and efficacy of mobile consumers (Kitching et al. 1959, Menge 1976, Menge and Sutherland 1976, Etter 1989). Hence, patterns of succession and resulting community organization often differ substantially between waveexposed and sheltered shores. On wave-exposed shores in the southern Gulf of Maine, barnacle recruitment (Semibalanus balanoides) during a narrow window between late February and April (Barnes 1957, Dudgeon and Petraitis 2001, Pineda et al. 2002, Kordas and Dudgeon 2009) often facilitates high mussel recruitment in the summer (Petraitis 1991, Bertness et al. 2004b). In the absence of consumer pressure, mussels eventually dominate these communities by overgrowing barnacles and outcompeting fucoid algae (Fucus vesiculosus, Ascophyllum nodosum) for space (Menge 1976). Of course, depending on the timing and scale that new bare space is made available by disturbance from waves and other factors, these habitats can also contain a mosaic of barnacles, mussels, and Fucus at any given time (Menge 1976, 1978a, b, Bertness et al. 1999, 2004b). In contrast, on sheltered shores in the southern Gulf, the supply of barnacle and mussel larvae is reduced (Bertness et al. 2004b), and resulting low recruitment, coupled with more intense predation by dogwhelks (Nucella lapillus) and green crabs (Carcinus maenas), further reduces mussel and barnacle abundance (Lubchenco and Menge 1978). As a result, competition for space is relaxed, allowing fucoid algae (initially Fucus vesiculosus followed by the slower-growing Ascophyllum nodosum) to colonize, grow, and form dense canopies that dominate the shore (Dudgeon and Petraitis 2001). Although snail (Littorina littorea) grazing on young recruits may slow fucoid algal recovery (Lubchenco 1983, Petraitis 1987), the eventually dominant Ascophyllum canopy typically covers a sparse understory of mussels and barnacles at these sites (Bertness et al. 2004b), which contrasts with the dense mussel and barnacle communities typical of waveexposed shores (Menge 1976, 1978a, b) The prevailing evidence indicates that these habitatspecific differences in succession and community organization in the southern Gulf typically depend on the high recruitment potential of dominant space-occupying species and the impact of consumers on their abundance after settlement. However, recent work on Gulf of Maine shores has revealed geographically based differences in species interaction strength (Kordas and Dudgeon 2009, 2011) and community organization following disturbance (Petraitis and Dudgeon 1999, 2004, Dudgeon and Petraitis 2001, Bertness et al. 2002, 2004a, b). Hence, there has been disagreement over whether consumers drive the dynamics and organization of these communities, or whether spatial and temporal variation in recruitment levels of key species plays a more prominent role than previously thought. For example, experiments at multiple locations in the southern Gulf found that consumers prevented the recovery of fucoid algal canopies on sheltered shores (Bertness et al. 2002, 2004a, b). In contrast, work in central Maine s Penobscot Bay found that variability in the timing and location of mussel, barnacle, and fucoid algal recruitment and the size of patches created by disturbance could result in mussel-dominated or algaldominated community states (Petraitis and Dudgeon 1999, Dudgeon and Petraitis 2001). These results also suggest that variation in barnacle and mussel recruitment in the Gulf of Maine may not solely depend on wave exposure, but also local oceanographic processes that impact larval supply. Moreover, consumer pressure was quite different in these studies, with Bertness et al. (2004b) observing high predation rates within a single tidal cycle, and Petraitis and Dudgeon (1999, 2004) observing predation rates that were not apparent for several weeks. It is clear that there is the potential for substantial geographic variation in the factors affecting community succession and organization in the Gulf of Maine. This is not surprising, because geographic variation in upwelling (Bustamante et al. 1995b, Menge et al. 1997, 2003, 2004), grazer impacts (Coleman et al. 2006), and the strength of positive and negative species interactions (Bertness and Leonard 1997, Leonard 2000) can influence the succession and organization of rocky-shore communities. For example, large regional differences in community organization have been documented in the eastern Atlantic (Coleman et al. 2006, Jenkins et al. 2008), which has many of the dominant species (Fucus, Ascophyllum, Semibalanus, Mytilus sp., Carcinus, and Nucella) found on Gulf of Maine shores. In the eastern Atlantic, latitudinal differences in rocky-shore community organization are likely driven by changes in the abundance and impact of two patellid limpet species, Patella depressa and P. vulgata (Coleman et al. 2006, Jenkins et al. 2008), which are absent from the western Atlantic and Gulf of Maine. In general, herbivore control of fucoid algae appears to be more intense in the eastern Atlantic than in the Gulf of Maine (Jenkins et al. 2008), whereas factors affecting barnacle and mussel abundance may be more important on rocky shores in the western Atlantic (i.e., the Gulf of Maine). Over the last 20 years, many studies have shown that broad-scale spatial variation in rocky shore communities may reflect differences in oceanographic processes that impact larval supply (e.g., Menge et al. 1994, 2003, Broitman et al. 2001, Navarrete et al. 2005, Blanchette et al. 2008, Wieters et al. 2009). Because variation in barnacle and mussel recruitment can play a key role in the succession and organization of Gulf of Maine rocky shores, identifying geographic variation in coastal oceanography that influences larval supply may help reconcile the disparate influence of consumer control

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 581 FIG. 1. Map of the Gulf of Maine with prevailing oceanographic currents. The Eastern Maine Coastal Current (EMCC, blue) flows southwesterly along the coast from the mouth of the Bay of Fundy until the Penobscot Bay region, at which point water either moves offshore or continues southwesterly to form the Western Maine Coastal Current (WMCC, red). Also shown are the Nova Scotia Current (black) and cyclonic circulation around Jordan Basin (yellow). Points along the coastline indicate sites where community structure surveys were conducted. Due to the proximity of some sites, some points may overlap. Blue triangles indicate sites in the Northern region, black circles indicate sites in the Penobscot region, and red squares indicate sites in the Southern region. Solid points indicate wave-exposed sites and open points indicate sheltered sites. and recruitment variation on community succession and organization throughout the Gulf of Maine. To examine whether distinct oceanographically driven biogeographic provinces occur within the Gulf of Maine, we examined the influence of physical stress (wave energy), recruitment, and consumers on community recovery after disturbance in the northern and southern Gulf. To broaden the geographic scope of these observations and experiments, we also examined between-site variation in community structure on 34 shores across the Gulf of Maine basin. Our results suggest that the succession and organization of rocky intertidal communities in the northern and southern Gulf are substantially different despite sharing virtually the same species assemblages. Moreover, these differences appear to be shaped by oceanographically driven recruitment variation that dictates subsequent species interactions. MATERIALS AND METHODS Community structure across the Gulf of Maine We characterized the structure of rocky intertidal communities with quadrat surveys at 34 sites spanning the Gulf of Maine (Fig. 1; Appendix A). We recorded the percent cover of all visible, macroscopic, sessile species composing the canopy and understory in pointintercept quadrats (25 points per 0.25-m 2 quadrat) haphazardly placed (N ¼ 10) in the mid-intertidal at each site. This method provides reliable estimates of the abundance of common intertidal species, but may be less so in estimating the abundance of rare species. Quadrats were randomly tossed on horizontal emergent substratum within the fucoid algae zone. If a quadrat landed in a tide pool, or rested vertically against a ledge, then the quadrat was moved to the nearest emergent, horizontal surface. All algal or sessile invertebrate species located beneath an intercept were recorded to yield percent cover data, which regularly exceeded 100% because of the presence of both the canopy and understory organisms. For any species that could not be conclusively identified in the field (rarely the case), a representative sample was collected for identification in the laboratory. Sites were assigned to three geographic regions based on documented oceanographic circulation patterns (Pettigrew et al. 1998, 2005; see Fig. 1 for prevailing Gulf of Maine circulation patterns). The southern Gulf region ranged from Cape Cod, Massachusetts to Penobscot Bay, Maine, corresponding to the Western

582 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 Maine Coastal Current (WMCC) that forms from the outflow of the Penobscot River and the Eastern Maine Coastal Current (EMCC; Churchill et al. 2005, Pettigrew et al. 2005, Manning et al. 2009). The Penobscot region ranged from Penobscot Bay to Great Wass Island, Maine, where a portion of the EMCC moves offshore to varying extents depending on seasonal and interannual variation. When offshore movement is high, a freshwater plume from the Penobscot River replaces the surface waters in this region (Pettigrew et al. 1998, 2005, Churchill et al. 2005, Hetland and Signell 2005). The Northern Gulf region ranged from Great Wass Island to Cobscook Bay, Maine, corresponding to the region where the Nova Scotia current and discharge from the St. John and St. Croix rivers meet near the mouth of the Bay of Fundy to form the EMCC, and southwestward flow occurs (Hetland and Signell 2005, Pettigrew et al. 2005, Tilburg et al. 2012). The wave exposure of each site (sheltered vs. wave-exposed) was characterized based on personal observations of coastal topography (e.g., headlands vs. bays) and wave action during calm and stormy periods, and/or dissolution rates of plaster clod cards (Appendix A). Variation in community structure was analyzed with multivariate analyses using the Vegan package (Oksanen et al. 2013) for R version 3.0.0 (R Development Core Team 2013). A Non-Metric Multidimensional Scaling (NMDS) plot was created to compare community composition between sites using the metamds function with untransformed percentage cover data and a Bray-Curtis index. After the ordination plot was constructed from the metamds, the function ordiellipse was used to plot 95% confidence ellipses for the mean ordination of each geographic region and wave exposure combination. We employed the adonis function with a Bray-Curtis index with 999 permutations to conduct a multivariate ANOVA (PERMANOVA), with geographic region (southern, Penobscot, northern) and wave exposure (wave-exposed, sheltered) as orthogonally crossed factors to test for differences in community structure. Subsequent Similarity Percentage (SIMPER) analyses using the simper function determined the contributions of dominant species and bare rock to the similarity between regions and wave exposures. Recovery from disturbance experiment: study sites To examine patterns of recovery from disturbance, we chose two representative sites of each wave exposure (sheltered, wave-exposed) in each of two regions (northern Gulf [Lubec, Maine]; southern Gulf [Nahant, Massachusetts]). Due to the broad scale (the distance between the two regions was.400 km) and laborintensive nature of this experiment (144 experimental plots), additional sites were not logistically feasible. Moreover, the results of the Gulf of Maine-wide community structure survey confirmed that the study sites used in the recovery experiment were representative of each geographic region. The wave-exposed sites in the northern Gulf were on a rocky headland between Julia Cove and Hamilton Cove in Lubec, Maine, and the sheltered sites were just north of Quoddy Head State Park in Lubec, Maine. In the southern Gulf, the two wave-exposed sites were on East Point in Nahant, Massachusetts, and the two sheltered sites were in an embayment northwest of East Point in Nahant, Massachusetts (see Appendix A for more information). One of the wave-exposed sites in the southern Gulf was used in Menge s early studies (Menge 1976, 1978a, b), and the sheltered sites in the south were adjacent to those used by Menge (1976, 1978a, b) and Lubchenco (1980, 1983), because their original sites are now subject to high levels of human activity. Consumer density surveys and analysis We monitored mobile consumer density at experimental study sites by recording the number of mobile consumers in 10 randomly placed 0.25-m 2 quadrats in the mid-intertidal zone at each replicate site in July 2005. Density data for the dominant mobile consumers (predators, Nucella lapillus and Carcinus maenas, and herbivores, Littorina littorea and Tectura testudinalis) were analyzed with a three-factor, nested design, with geographic region and wave exposure as fixed factors and site as a random factor nested within wave exposure and geographic region. Because the high frequency of zero counts in the quadrats resulted in heteroscedasticity that could not be corrected via transformation, we assessed the influence of geographic region and wave exposure on mobile consumer densities with Generalized Linear Mixed Models (GLMMs) that had a negative binomial error distribution and a log-link function (O Hara and Kotze 2010, Linden and Mantyniemi 2011, Warton and Hui 2011) using the glmmadmb package (Skaug et al. 2011, Fournier et al. 2012) for R version 3.0.0 (R Development Core Team 2013). To determine the influence of geographic region and wave exposure and their interaction on the density of each consumer, a model-selection-based approach to hypothesis testing using Akaike weights based upon corrected Akaike Information Criterion (AIC c ) was employed to determine the best-fit model (Burnham and Anderson 2002, 2004, Johnson and Omland 2004, Bolker et al. 2009). Recovery from disturbance experiment: approach and analysis This experiment was a four-factor nested design with replicate sites (N ¼ 2) as a random factor nested within each wave exposure (sheltered, wave-exposed) and geographic region (northern, southern). Hence in each region, there were two replicate wave-exposed and two replicate sheltered sites. At each replicate site (N ¼ 8in total), there were six independent replicates of each caging treatment (cage, cage control, open), for a total of 144 experimental plots.

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 583 Each replicate plot was a 1 3 1 m clearing (each clearing was separated by at least 2 m) where all resident algae and sessile invertebrates were removed with paint scrapers and propane torches in mid-october 2003. The successful removal of all organisms in each plot was confirmed in early March 2004 prior to the onset of barnacle recruitment. To maintain a consistent sampling, the corners of a single 20 3 20 cm plot located in the center of each 1 3 1 m clearing were marked with stainless steel lag screws installed into the substratum. In addition, the fucoid algal canopy surrounding each clearing was trimmed to prevent it from impacting the sampling area (e.g., whiplash, shading). All percent cover data were recorded in these 20 3 20 cm plots. Caging treatments (cage, cage control, or open) were applied to appropriate plots at each site in each location. Consumer exclusion cages (25 3 25 3 5 cm; mesh opening was 0.5 cm) constructed from stainless steel mesh were anchored into the rock to cover the 20 3 20 cm plot located in the center of each 1 3 1 m clearing. The edges of cages were pressed flush to the substratum, and if necessary, sealed with waterproof epoxy (Z-spar; Pettit Marine Paint, Rockaway, New Jersey, USA) to further ensure the exclusion of consumers. Cage controls were constructed and installed in a similar manner, except that two sides of the cage were left open to allow access by consumers. Open plots were left uncovered to allow full access by consumers. We assessed recovery by photographing plots twice a year (spring and fall) over the following two years. Mussels in the northern Gulf may include M. edulis, M. trossulus, and hybrids (Rawson et al. 2001), but field identification of these species is not feasible. Although the general rarity of mussels at sites in the northern Gulf makes it unlikely that this distinction among species is important, all mussels are nevertheless referred to as Mytilus spp. The percent cover of sessile species was determined from resulting photographs by placing a layer of 36 random points over each photograph in Adobe Photoshop and recording species identity underneath each point. If no species was present, the point was scored as bare rock. If a point fell upon a mobile consumer, the sessile species to the immediate right of the mobile species was recorded. As recovery progressed and a fucoid algal canopy developed, it became necessary to collect percent cover data on understory species using a point-intercept quadrat (with 36 points) in the field. Percent cover data were analyzed with a four-factor, nested ANOVA with replicate sites as a random factor nested within each wave exposure (sheltered, exposed) and geographic region (northern, southern) and caging treatment (cage, cage control, open) as fixed factors. Although we present the full pattern of recovery in our figures, we conducted our analyses on the percent cover data collected during the last sampling date in Fall 2005 for the three dominant taxa (F. vesiculosus, S. balanoides, and Mytilus spp.) in our plots because they were the primary drivers of community recovery. Percent cover data were log 10 (x þ 1) transformed to meet the homogeneity of variance assumption (Warton and Hui 2011). These analyses were performed with JMP software for the Macintosh (version 10, SAS Institute 2014). To further address importance of geographic region, wave exposure, and consumer exclusion to patterns of recovery, we determined the effect size (eta-squared, g 2 ¼ SS effect /SS total ) for each factor in our ANOVA model. Because of the large effect (Cohen 1988) of geographic region (g 2. 0.22 for each species) and the significance of the region 3 wave exposure 3 caging interaction, we examined the effect sizes (g 2 ) for wave exposure, caging, and their interaction for each geographic region. Separate three-factor, nested ANOVAs with sites nested within wave exposure and crossed with caging were performed for each species in each region, and the resulting sums of squares were used to determine observed effect sizes. To examine relationships between dominant species on wave-exposed shores in the southern Gulf, where recruitment, and likely competition for space, was highest, we used Pearson s (r) correlations on percentage cover data obtained in the spring and fall of 2005. Barnacle recruitment Annual barnacle (S. balanoides) recruitment was measured at each experimental study site from 2004 to 2006 in six replicate settlement plots (20 3 20 cm) that had been cleared of all sessile organisms in early spring of each year. Each plot was photographed in late spring of each year, after the completion of settlement. A grid of equal-sized squares was then placed on each photo in Adobe Photoshop before counting the number of barnacles present in 10 randomly chosen squares. Because barnacle settlement was quite high and uniform in southern plots, total recruitment was determined by scaling up the average number of barnacles in these subsamples to calculate barnacle density in each plot. Due to very low recruitment in the northern Gulf, this approach was not necessary and all barnacle recruits within the 20 3 20 cm plots were counted. Barnacle recruitment densities were analyzed with a four-factor nested ANOVA with site as a random factor nested within region and wave exposure, and crossed with year using JMP software for Macintosh (version 10, SAS Institute 2014). Although we used the same physical areas each year, we reasoned that a repeated-measures design was not necessary because recruitment plots were re-cleared before each recruitment season, and therefore provided an independent assessment of recruitment variation for each year. Prior to analysis, data were log transformed to meet the homogeneous variance assumption of ANOVA. Long-term Ascophyllum recovery The long-term recovery of Ascophyllum in open plots at sheltered sites in both regions was monitored from

584 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 FIG. 2. Two-dimensional Non-metric Multidimensional Scaling (NMDS) plot constructed using the metamds function with a Bray-Curtis distance index of untransformed community structure data (stress ¼ 0.07876). Each data point represents a single site, and ellipses represent 95% confidence intervals of the mean ordination for each region and exposure combination. Light gray triangles indicate northern sites, black circles indicate Penobscot sites, and dark gray squares indicate southern sites. Solid points and lines indicate wave-exposed sites; open points and dashed lines indicate sheltered sites. 2004 to 2011 by annually photographing each plot in the spring and fall. Unfortunately, unanticipated changes in landowner restrictions in 2007 made such monitoring impossible for the wave-exposed sites in the northern Gulf. However, beginning in 2005 we were able to monitor long-term Ascophyllum recovery in the open plots of another similar experiment that had one waveexposed site in the northern Gulf that was unaffected by landowner restrictions, and two wave-exposed sites in the southern Gulf. Because long-term Ascophyllum recovery at each shore type was derived from two separate experiments with different time spans and levels of site replication, recovery data for the wave-exposed sites were analyzed with a one-factor ANOVA that considered geographic region as a fixed effect. Because unequal variances between sites could not be corrected via transformation or modeled through mixed-model approaches, differences between these sites were assessed by adjusting the significance level to that of the Brown- Forsythe test for unequal variances. Long-term Ascophyllum recovery data at sheltered sites were analyzed with an ANOVA that considered geographic region as a fixed effect and site as a random effect nested within geographic region. Although figures present the full temporal pattern of recovery through time, we analyzed the endpoint data collected in Fall 2011. RESULTS Community structure across the Gulf of Maine Results of the metamds analysis indicated that sites in the northern and southern regions of the Gulf of Maine clustered based upon wave exposure (Fig. 2). Moreover, wave-exposed and sheltered sites in the southern region clustered separately, whereas waveexposed and sheltered sites clustered together in the northern region. Community structure was strikingly similar for sites within the same wave exposure in the northern and southern regions. However, within the Penobscot region, site-to-site similarity was reduced, as indicated by the large 95% confidence ellipses (Fig. 2). One wave-exposed site (Milbridge, Maine) and one sheltered site (Grindstone Neck, Maine) in the Penobscot region that did not cluster with sites of similar wave exposure likely contributed to the reduced similarity in this region. Results of the PERMANOVA indicated that community structure differed based upon region and wave exposure, and that the effect of wave exposure differed between oceanographic regions (PERMANOVA, Region 3 Exposure, F 2,28 ¼ 4.5058, P ¼ 0.0008; Appendix B). Wave-exposure effects on community structure were far stronger in the southern Gulf than in the northern Gulf (Figs. 2 4). In the Penobscot region, sites grouped based upon wave exposure with most wave-exposed sites and most sheltered sites clustering with their counterparts in the southern Gulf. However, the overall similarity of sites within each wave exposure grouping was lower in the Penobscot region, as evidenced by the larger ellipses (Fig. 2), than in other regions. The similarity between wave-exposed and sheltered sites in the northern Gulf was likely driven by the dominance of Ascophyllum at both wave exposures in this region, whereas this alga was only dominant at sheltered sites in the southern Gulf and the Penobscot region (Figs. 3 and

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 585 FIG. 3. Average percent cover of dominant space-occupying species and bare rock in established communities on wave-exposed shores: (A) Fucus,(B) Ascophyllum,(C) Semibalanus,(D) Mytilus sp., and (E) bare rock. On the x-axis, sites are ordered by latitude from southernmost (left) to northernmost (right). Data represent mean þ SE. 4, Table 1; also see Appendix C). In contrast, Fucus dominated wave-exposed sites in the southern Gulf and the Penobscot region. Hence, Ascophyllum and Fucus contributed to the lack of similarity between waveexposed and sheltered sites in the southern Gulf and the Penobscot region, but played a minor role in the lack of similarity among wave exposures in the northern Gulf. Differences in the abundance of these fucoids also drove the dissimilarity between the wave-exposed sites among the three regions, but lower barnacle and higher bare space percent cover distinguished northern sheltered sites from those in the other regions. Consumer densities Quadrat surveys indicated that predators and herbivores with strong effects on dominant intertidal species were most abundant at sheltered sites in the southern Gulf. Green crabs (C. maenas) were observed only at southern sheltered sites (Fig. 5A). The best fit model included both region and wave exposure as fixed effects (GLMM, w i ¼ 0.7451; Appendix D) and models that lacked either of these effects were poor predictors of crab density (GLMM, w i ¼ 0.0093; Appendix D). Predatory (N. lapillus) and herbivorous (T. testudinalis) gastropods were most abundant at southern waveexposed sites and northern sheltered sites, respectively (Fig. 5B, C). The greatest density of N. lapillus occurred at southern, wave-exposed sites (;150 snails/m 2 ; Fig. 3B) and models without either wave exposure or region received minimal support (GLMM, w i ¼ 0.0002 and,0.0001 for wave exposure and region, respectively; Appendix D). T. testudinalis density surpassed 10

586 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 FIG. 4. Average percent cover of dominant space-occupying species and bare rock in established communities on sheltered shores: (A) Fucus,(B) Ascophyllum,(C) Semibalanus,(D) Mytilus sp., and (E) bare rock. On the x-axis, sites are ordered by latitude from southernmost (left) to northernmost (right). Data represent mean þ SE. limpets/m 2 at the northern sheltered sites (Fig. 5C), and the best model included both region and wave exposure as fixed effects (GLMM, w i ¼ 0.6390 Appendix D). Finally, the herbivorous snail, L. littorea, reached densities of 25 snails/m 2 at the southern sheltered sites, and was comparatively absent from all other sites (Fig. 5D). The best fit model includes both fixed effects and the interaction (GLMM, w i ¼ 0.9978; Appendix D) and all other models had minimal weight, indicating that although higher densities occurred at sheltered sites in both regions, the magnitude of this effect was greater in the southern than in the northern Gulf. Community recovery at wave-exposed sites At northern wave-exposed sites, Fucus dominated community recovery and mussels and barnacles were relatively unimportant (Fig. 6; Appendix E). In fact, we observed no mussel recruits in our plots at these sites, and although barnacles recruited to our plots (Fig. 7A; Appendix F), their abundance was relatively low and they never occupied.20% of the available space. Surprisingly, the presence and absence of consumers had little impact on recovery (linear contrast, P ¼ 0.2045). In fact, Fucus recovery was strongest in uncaged, open plots reaching 100% cover after two years, whereas recovery was slower in caged and cage control plots, presumably because of cage abrasion. When cages and cage controls were removed in Fall 2005 for photographic sampling, we frequently observed damaged fucoid fronds in our sampling plots (E. S. Bryson, personal observation).

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 587 TABLE 1. Average percentage similarity between wave-exposed and sheltered sites in each geographic region based upon SIMPER analyses of Bray-Curtis similarities, and the contributions of dominant space-occupiers (Ascophyllum nodosum, Fucus vesiculosus, Mytilus spp., Semibalanus balanoides) and bare rock to the dissimilarity between sites. Region and 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 Mytilus sp. 0.00 0.00 0.00 S. balanoides 0.20 1.90 2.32 Bare rock 32.80 45.30 24.88 Recovery patterns at southern wave-exposed sites were dramatically different (Fig. 6; Appendix E). At these sites, Fucus recruitment was quite low and recovery was dominated by the recruitment and establishment dynamics of barnacles and mussels. In spring 2004, new barnacle recruits dominated all plots regardless of consumer exclusion treatment, but by the fall mussels had replaced barnacles as the primary occupier of space. During the winter of 2004 2005, mussel density declined in open plots, but remained high in cage and cage control plots. It is unlikely that consumer exclusion drove this pattern because consumers are inactive during FIG. 5. Average density of mobile consumers on wave-exposed (black bars) and sheltered (stippled bars) shores in the southern and northern Gulf of Maine. (A) Carcinus maenas and (B) Nucella lapillus are important consumers of barnacles (Semibalanus balanoides) and mussels (Mytilus spp.), and the herbivorous gastropods (C) Tectura testudinalis and (D) Littorina littorea consume algae. Data represent mean 6 SE; n ¼ 20 at each location and wave exposure. Note that the y-axis scale varies for each consumer.

588 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 winter. Instead, winter disturbance likely caused mussel decline in open plots, whereas the physical structure provided by cages and cage controls prevented storminduced mussel dislodgement (Menge 1976). The following spring (2005) barnacle recruitment into bare patches remained high (Fig. 5A), but was considerably lower in cage and cage control plots where mussel abundance was high (Fig. 6A, C). By fall of 2005, mussel abundance had declined in all plots, possibly because of heat waves during the summer. However, a mix of Fucus, barnacles, and mussels were observed only in open plots where mussel cover had declined over winter and was low in spring 2005 (Fig. 6). Pearson s correlations indicate that mussel cover in the spring of 2005 explained.50% of the variation in barnacle and Fucus cover in the fall of 2005 (Pearson s r ¼ 0.5262, 0.6734, and P, 0.0001, 0.0004, respectively; Table 2). Higher spring mussel cover corresponded to lower barnacle and Fucus cover in the fall. However, mussel cover in the fall of 2005 appeared independent of the barnacle, Fucus, or mussel cover the previous spring (Pearson s r ¼ 0.1391, 0.1399, 0.0575, respectively, P. 0.4157 for all; Table 2). Moreover, the presence and FIG. 6. Mean (6SE) percent cover of the dominant spaceoccupying organisms (A) Semibalanus balanoides, (B) Fucus vesiculosus, and (C) Mytilus spp. over two years on waveexposed shores in the southern (dark gray lines) and northern (light gray lines) Gulf of Maine. Effects of the presence (open plots [O], circles) and absence (cage [C], squares) of consumers and cage controls ([CC] triangles) are also shown. Although recovery through time is shown, only end point data were analyzed. FIG. 7. Mean (6SE) recruitment density of Semibalanus balanoides into experimental recruitment clearings in the spring of 2004 2006 on (A) wave-exposed and (B) sheltered shores in the southern (dark gray bars) and northern (light gray bars) Gulf of Maine.

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 589 Matrix of Pearson s r correlations between the percentage cover of dominant spaceoccupying species (Semibalanus balanoides, Mytilus sp., and Fucus vesiculosus) in the spring and fall of 2005. TABLE 2. Cover 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 Note: N ¼ 36 for all correlations. ** P, 0.01. absence of consumers appeared to be unimportant to recovery on these shores. Community recovery at sheltered sites Recovery on northern sheltered sites was remarkably similar to that found on their wave-exposed counterparts (Appendix E). Consumer pressure was unimportant to the recovery of Fucus, which dominated all plots (linear contrast, P ¼ 0.4071; Fig. 8). Mussel recruitment and establishment did not occur and barnacle recruitment was low so that barnacles never occupied.5% of the available space, regardless of consumer exclusion. In contrast, recovery on southern sheltered sites was strongly influenced by the presence of consumers (Fig. 8; Appendix E). Initial barnacle recruitment in spring 2004 was high at these sites (Fig. 7B), especially in cage and cage controls, perhaps because these structures either reduced thermal stress or water velocity, thereby enhancing larval settlement and survivorship. By fall 2004, the effects of consumer exclusion began to emerge. Barnacle abundance declined in open plots and cage controls, and both mussels and Fucus began to dominate plots where consumers were excluded. By spring 2005, the positive effects of consumer exclusion on Fucus and mussels intensified. At the end of the experiment, consumer exclusion (caged plots) led to communities dominated by Fucus (;60% canopy cover; linear contrast, caged vs. open, P ¼ 0.0026) with an understory of mussels (;20% understory cover; linear contrast, caged vs. open, P ¼ 0.0018), barnacles (;35% understory cover; linear contrast, caged vs. open, P ¼ 0.0003), and bare space (;45%). By contrast, in open plots, Fucus still formed a canopy in the presence of consumers despite its relatively lower abundance (;25 30%), and barnacles (;35%) and bare space (;65%) dominated the understory, while mussels were generally absent, presumably because of predation by green crabs and Nucella. Long-term Ascophyllum recovery Recovery rates of Ascophyllum on wave-exposed shores differed between northern and southern sites (ANOVA, P, 0.0004, Fig. 9; Appendix G). As expected, Ascophyllum remained absent at southern wave-exposed sites, whereas recovery at northern wave-exposed sites became evident after three years, reaching ;15% cover after seven years. On sheltered shores, Ascophyllum recovery occurred at both northern and southern sites but was more substantial (ANOVA, P ¼ 0.0224) at the northern sites, reaching 40 50% cover after eight years. DISCUSSION Our survey of 34 established rocky intertidal communities throughout the Gulf of Maine revealed substantial differences in the distribution and abundance of key shared species that likely influence how these communities are organized. In the northern Gulf, sites had a dense canopy of Ascophyllum regardless of wave exposure, and barnacles and mussels were either rare or altogether absent. In the southern Gulf, extant community structure was consistent with previous work (Menge 1976, 1978a, b, Lubchenco 1980, Bertness et al. 2004b), showing that barnacles, mussels, and Fucus dominate wave-exposed shores and Ascophyllum dominates sheltered shores. Communities in the Penobscot region of central Maine were generally aligned with those on sheltered and wave-exposed shores in the southern Gulf. However, one wave-exposed site (Milbridge, Maine) with abundant Ascophyllum was more consistent with communities typical of northern waveexposed sites. In addition, a sheltered site in this region (Grindstone Neck, Maine) was dominated by Fucus and barnacles rather than Ascophyllum, and was therefore more similar to wave-exposed sites in the southern region. Recovery patterns after disturbance reinforced the notion that communities in the northern and southern Gulf are organized differently. Consumer-driven dynamics in the southern Gulf of Maine Recovery in the southern Gulf indicates that the strong influence of recruitment, competition for space, and consumer control on community organization depends on wave exposure, which is consistent with previous research (Menge 1976, 1978a, b, Lubchenco and Menge 1978, Bertness et al. 2004b). On waveexposed shores, barnacles recruited densely in the spring of 2004, but were replaced by mussels in the fall. This transition may reflect barnacle facilitation of mussel recruitment, which has been observed by others within the Gulf of Maine (Menge 1976, Petraitis 1987). The subsequent impact of physical factors (e.g., thermal

590 ELIZABETH S. BRYSON ET AL. Ecological Monographs Vol. 84, No. 4 stress and storm-induced dislodgement) likely drove cyclical patterns in mussel cover, which when high, shaped subsequent recovery patterns by overgrowing barnacles and limiting the space available for Fucus establishment. For example, barnacle recruitment in the year (2005) following mussel establishment (Fig. 6) was much lower despite remarkably high and consistent barnacle supply over the three years it was measured (Fig. 7A), and the abundance of Fucus remained relatively low in cages and cage controls throughout the two-year experiment. Only in open plots, where mussel populations declined over winter because of FIG. 8. Mean (6SE) percent cover of the dominant spaceoccupying organisms (A) Semibalanus balanoides, (B) Fucus vesiculosus, and (C) Mytilus spp. over two years on sheltered shores in the southern (dark gray lines) and northern (light gray lines) Gulf of Maine. Effects of the presence (open plots [O], circles) and absence (cage [C], squares) of consumers and cage controls [CC] (triangles) are also shown. Although recovery through time is shown, only end point data were analyzed. FIG. 9. Mean (6SE) percent cover of Ascophyllum nodosum in open plots on (A) wave-exposed and (B) sheltered shores in the southern (dark gray lines) and northern (light gray lines) Gulf of Maine. We monitored the recovery of open plots from the original manipulative recovery experiment on sheltered shores for eight years beginning in 2004. Because of unanticipated changes in site accessibility, we were only able to monitor recovery at one wave-exposed site in the northern Gulf and two wave-exposed sites in the southern Gulf for seven years beginning in early 2005. Note that for the southern waveexposed sites there was no recovery, so data points for each site overlap. Although recovery through time is shown, only end point data were analyzed. Data points and error bars represent mean 6 SE.

November 2014 BROAD-SCALE VARIATION ON ROCKY SHORES 591 dislodgement by storms (Menge 1976, Paine and Levin 1981, Denny et al. 1985, Hunt and Scheibling 2001, Carrington 2002), did Fucus and barnacles establish larger populations. Thus, although open plots at waveexposed sites included a mix of all three primary spaceoccupying species, rather than mussel dominance as observed by Menge (1976), the increase in both Fucus and barnacles after the spring of 2005 appeared to largely hinge on mussel dynamics. These cyclical patterns of mussel dominance are likely driven by variation in disturbance rather than by interactions with barnacles and Fucus (Table 2). We suggest that this high recruitment high turnover system creates unstable biotic secondary substratum that may contribute to the lower recovery of Fucus and to the absence of Ascophyllum from wave-exposed shores in this region. Previous work has shown that Nucella can strongly control the abundance of barnacles and mussels on wave-exposed shores in this region (Bertness et al. 2004b), but our experiment provided no evidence of consumer control at these sites. Although high wave energies can limit the effectiveness of Nucella (Burrows and Hughes 1989, Etter 1989, 1996), we were surprised to find no evidence of consumer control because all aspects of our experimental cages, cage controls, and open plots were identical to those used by Bertness et al. (2004b) in southern Maine. These disparate patterns of consumer effects on wave-exposed shores may reflect regional differences within the southern Gulf of Maine similar to those observed by Kordas and Dudgeon (2011), who found weaker consumer effects on Ascophyllum in Massachusetts than in southern Maine. Thus, Nucella barnacle and Nucella mussel interactions may be stronger in southern Maine than in Massachusetts, where caging artifacts overrode any consumer effects. Nevertheless, the resulting impacts of cages on mussels influenced subsequent recovery. For example, mussel abundance after the first settlement season in fall 2004 was high, occupying ;60% of the available space in all treatments, but had declined only in open plots by the following spring. Because cage controls maintained the same high mussel abundance as full cages, we suggest that the physical structure provided by both cages and cage controls had a positive effect on mussels by reducing the risk of dislodgement during winter storms. Indeed, observations at our southern wave-exposed sites in the winter of 2004 2005, after storms, revealed substantial unoccupied space in our open plots, indicating that physical stress, rather than species interactions, caused this decline. By fall 2005, cages and cage controls were full of empty mussels, sand, and shell hash, which negatively impacted mussel survival as well as the few Fucus individuals present. Thus, the disparate patterns of consumer effects on mussels at wave-exposed sites between this study (i.e., reduced consumer pressure) and past work (Bertness et al. 2004b) may reflect either greater thermal stress, greater wave exposure, or both, at our sites in Massachusetts. On sheltered sites in the southern Gulf, the presence of consumers strongly influenced the recovery of Fucus and mussels (Fig. 8). After one year of recovery, a Fucus canopy with a mix of mussels and barnacles in its understory developed when consumers were excluded. When consumers were present, however, bare space dominated plots with moderate cover of Fucus and barnacles after two years. Although adult fucoids are relatively resistant to snail grazing, L. littorea was abundant at these sites (Fig. 5D), and it can slow fucoid recovery by consuming germlings and young recruits before they attain a size refuge and begin to produce chemical and structural defenses (Lubchenco and Gaines 1981, Lubchenco 1983, Barker and Chapman 1990, Rhode et al. 2004). Those Fucus that had escaped snail grazing, either via substratum or size-related refugia (Lubchenco 1983), eventually led to this alga being more prevalent even in open plots (;25% cover) after two years of recovery. Consumer exclusion clearly enhanced mussel recovery, presumably by preventing green crabs, which were also abundant at these sites (Fig. 5A), from accessing them. Even after two years, mussels were not present in open plots, suggesting that the effects of consumer control by green crabs on this species is stronger than that imposed by L. littorea on Fucus. This control of mussel abundance, coupled with Fucus escapes from grazing, will presumably lead to even greater Fucus abundance over the longer term (Menge 1976, 1978a, Lubchenco 1980, 1982, 1983, Bertness et al. 2004b). In contrast, we saw no strong evidence of consumer control on barnacle abundance, perhaps because their primary predator, Nucella, was not abundant at these sites (Fig. 5B). Recruitment limitation in the northern Gulf of Maine A striking feature of communities in the northern Gulf was that mussels and barnacles were unimportant to community recovery on both wave-exposed and sheltered shores. Unlike their southern counterparts, mussel recruitment and establishment were nonexistent and barnacle recruitment and abundance were quite low at all sites in the northern Gulf (Figs. 6 8); these recruitment patterns have continued in the years following this study (E. S. Bryson and G. C. Trussell, unpublished data). In the northern Gulf, currents move southward along the Scotian shelf before flowing northward to the mouth of the Bay of Fundy, where intense tide-driven mixing occurs and the southwestward movement of the Eastern Maine Coastal Current (EMCC) begins (Xue et al. 2000, Pettigrew et al. 2005). The proximity of the EMCC to the eastern Maine coastline can vary seasonally and annually (Hetland and Signell 2005, Pettigrew et al. 2005), but analyses of drifter data suggest high connectivity between Cutler, Maine (in the northern region) and sites in western Nova Scotia (Manning et al. 2009). However, results of an experimental particle