Seaweed communities in four subtidal habitats within the Great Bay estuary, New Hampshire: Oyster farm gear, oyster reef, eelgrass bed, and mudflat

Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

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Seaweed communities in four subtidal habitats within the Great Bay estuary, New Hampshire: Oyster farm gear, oyster reef, eelgrass bed, and mudflat ⁎,1

Megan Glenn

T

, Arthur Mathieson, Raymond Grizzle, David Burdick

University of New Hampshire, Jackson Estuarine Laboratory, 85 Adams Point Rd, Durham, NH 03824, United States of America

ARTICLE INFO

ABSTRACT

Keywords: Aquaculture Ecosystem services Macroalgae Management

The seaweed communities that developed on oyster farm gear in the Great Bay Estuary in New Hampshire (NH) were compared to three adjacent natural subtidal habitats: an oyster reef, eelgrass bed, and a mudflat. Both farm gear and oyster reefs have received little attention with respect to associated seaweeds. Comparisons were based upon replicate quadrat samples taken during August, and October 2014, plus August 2015. Mean species richness (all dates combined, N = 12) was significantly and substantially lower on the mudflat (2.86 ± 0.56 SE taxa/0.25 m2), but not different among the other three habitats (range: 9.00 ± 0.97 to 11.00 ± 1.41 taxa/ 0.25 m2). Mean biomass was also statistically different across habitats (P < .0001), ranging from 5.6 ± 3.0 SE g/m2 on the mudflat to 409.9 ± 67.9 g/m2 on the farm gear. Multivariate (PRIMER) analysis showed each habitat pair had significantly different seaweed communities. Thirty-nine seaweed taxa were recorded from the four habitats over the three dates, plus June 2014 for all the habitats excluding Farm Gear: 22 red, 14 green, and 3 brown algae. Thirty-six of the 39 (92.3%) were native species, including several ulvoid green algae and the brown alga Pylaiella littoralis that has been associated with eutrophic habitats. Eight disjunct species that are more common south of Cape Cod were also collected. Three introduced Asiatic red algae were collected: Dasysiphonia japonica, Agarophyton vermiculophyllum and Melanothamnus harveyi. Non-native seaweeds represented 81% of the biomass on farm gear and 84% on mudflats, but lower fractions in other habitats. Overall, these data document the substantial value of the gear used on oyster farms in providing seaweed habitat in northern New England. Our findings for seaweeds are similar to previous research in the region and elsewhere, which documents the habitat value of oyster farm gear for fish and invertebrates. The artificial materials used for oyster farm gear can provide habitat for native as well as introduced species.

1. Introduction Oyster aquaculture is a rapidly growing industry in the northeastern US, where it typically involves deployment of various types of gear (Flimlin et al., 2008; Rice, 2006). Oyster farm gear in New Hampshire (NH) is deployed on the bottom and includes structures such as trays and racks, which contain bags that hold the oysters. The trays and racks extend up to ~1 m within the water column, resulting in increased vertical structure and availability of hard substrata compared to the ambient unvegetated soft-sediment bottom. Due in part to the increase in structure, oyster farm gear potentially has positive effects on habitat quality at farm sites (McCoy and Bell, 1991; NRC, 2010). For example, DeAlteris et al. (2004), Erbland and Ozbay (2008), and Glenn (2016) found increased motile and sessile macrofaunal populations on oyster

gear compared to adjacent natural habitats. Similar trends might be expected for seaweeds that colonize farm gear, but to our knowledge, no previous studies on macroalgal community development have been made on such gear nor comparisons with adjacent natural habitats. Seaweed communities within several natural estuarine habitats in northern New England have been well documented, including those within Great Bay, NH (Hardwick-Witman and Mathieson, 1983; Mathieson and Dawes, 2017; Mathieson and Hehre, 1986; Mathieson and Penniman, 1991). The seaweed flora of the Great Bay Estuary, including Great Bay proper, Little Bay and eight tidal rivers (Fig. 1), varies spatially due to physical diversity and patchiness of rocky substrata. Most species grow on hard surfaces but there are also substantial drift algal communities that occur on soft sediments, including both intertidal and subtidal mudflats, and in association with eelgrass beds.

Corresponding author. E-mail addresses: [email protected] (M. Glenn), [email protected] (A. Mathieson), [email protected] (R. Grizzle), [email protected] (D. Burdick). 1 Present address: UNH Manchester, 88 Commercial Street, Manchester NH 03101. ⁎

https://doi.org/10.1016/j.jembe.2019.151307 Received 20 June 2019; Received in revised form 19 December 2019; Accepted 20 December 2019 0022-0981/ © 2020 Elsevier B.V. All rights reserved.

Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

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Fig. 1. Study area in Great Bay, New Hampshire showing locations of three natural habitats and placement of experimental oyster farm gear (black box). Shapes show general areas where four replicate samples were taken in each of the natural habitats on a single date.

Although management policy typically focuses on potential negative impacts on the environment and conflicts with other uses, bivalve shellfish farms can provide important ecosystem services such as water filtration, nutrient removal, and habitat provision (Browdy and Hargreaves, 2009; Costa-Pierce, 2010; Rose et al., 2014; Forrest et al., 2009; Coen et al., 2011; Bricker and Parker, 2017). On the other hand, macroalgal communities can bloom and smother shellfish beds and eelgrass meadows (Short and Burdick, 1996); Harlin and Thorne-Miller, 1981; Valiela et al., 1992). There is a need to better understand the range of impacts, both positive and negative, that oyster farms can have on the environment in order to develop more comprehensive management policy. The present study compared subtidal seaweed communities that developed over 14 months on eastern oyster (Crassostrea virginica Gmelin) farm gear to seaweeds on three contiguous natural habitats: eelgrass bed, oyster reef, and mudflat. We interpreted our data in the context of provision of habitat and how such information might affect management of oyster farms.

Table 1 Ranges for water parameters measured by data sondes within 1 km of the study site arranged by the months preceding each of the four sampling periods (see below).

Water Temp (°C) Salinity Dissolved Oxygen (mg/L) pH

Jun – 2014

Jul- Aug 2014

Sep – Oct 2014

Nov 2014 – Aug 2015

12.3–22.7 22.5–28.6 6.6–13.2

18.2–30.0 13.8–28.9 1.7–10.3

10.8–24.3 24.8–32 6.1–11

1.5–25.7 11.9–31.8 6.1–12.3

7.4–8.0

7.9–8.1

7.4–8.2

7.2–8.3

outcrops. The predominant subtidal habitats include eelgrass beds, oyster reefs, and unvegetated muddy sediments. The study site was chosen because all three natural habitats (eelgrass bed, oyster reef, and mudflat) occur in close proximity. Farm gear habitat was simulated at the site by deploying twelve replicate ¼-scale cubical oyster racks on mudflat, each holding three 35-mm mesh plastic oyster bags containing ~190 oysters averaging 52 mm in shell height at the beginning of the experiment (Fig. 2). The four habitats were sampled with a custom-made sampling device (0.5 m × 0.5 m × 0.5 m; =0.25 m2 bottom area sampled and 0.125 m3 water column volume sampled) constructed of plastic-coated steel wire lined with plastic screening material with 4-mm openings (Fig. 3). During each sampling occasion, four identical samplers were tossed haphazardly into each of the natural habitats, landing 5 to 10 m apart and sinking to the bottom with their open end downward. A knife with a 30-cm long blade was then inserted under each sampler just below the sediment surface and worked around each sampler's perimeter to cut a pathway for inserting the closure device constructed of thin sheet metal; this was particularly needed in the eelgrass and oyster reef habitats. After sliding the bottom closure through the sediment and closing the bottom opening, the sampler was inverted, trapping all seaweeds (and other organisms) inside. The trapped material was sieved within the sampling device (lined with 4 mm mesh) and returned to the laboratory where the algae were sorted, identified, and weighed

2. Methods 2.1. Study area, field and laboratory methods The study was conducted in Great Bay at a site southeast of Woodman Point, in the Town of Newington, NH (Fig. 1). The Great Bay Estuary is a mesohaline, macrotidal (~2.7 m tidal range) system that receives the freshwater discharges from seven major tidal rivers and is connected to the Atlantic Ocean at Portsmouth Harbor (Short, 1992; NHEP, 2000). On an annual basis, water temperature ranges from near zero in winter to over 25 °C in late summer when the Bay's shallow waters are warmed substantially above adjacent coastal waters (Table 1). Salinity typically is > 25, but can be reduced to < 5 during extreme rain events. Dissolved oxygen is typically near saturation levels (but can briefly fall to lower levels in summer), and pH varies narrowly around 7.8. Great Bay proper is ~44 km2 in area and is bounded by intertidal mudflats with fringing salt marshes and rockweed-covered bedrock 2

Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

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2.2. Data analysis The sampling device used for all four habitats yielded quantitative sampling units that can be expressed by surface area or volume; only area units are used herein. All statistical tests were based on the null hypothesis that there were no differences among the four habitat types in the dependent variable being analyzed. Due to the distribution of naturally occurring habitats in Great Bay, habitat is confounded by site. A repeated measures was employed in the analysis, with four main habitats sampled on three dates and four replicates sampled within each habitat. Data from June 2014 were not included in the analysis because this was when the farm gear was initially deployed (and not sampled). Biomass data were log transformed in order to satisfy Shapiro-Wilks test for normality and Levene's test for homogeneity. Habitat comparisons were made using Tukey's HSD Test following a significant habitat effect in ANOVAs for total community biomass, biomass of native and exotic species, and species richness across seasons (JMP, 2015). Multivariate statistics assessed among-habitat variations resulting from differences in species composition using ANOSIM and SIMPER (PRIMER, 2016). The data from the incomplete sampling in June (no farm gear) were excluded. Two mudflat samples had no algae whatsoever, so analysis was performed following the addition of 0.05 g (one half the minimum biomass) of a common taxa (Ulva); this allowed all samples to be included and improved stability, but did not affect the outcome of the tests. Species biomass was square-root transformed and a resemblance matrix was constructed using Multi-Dimensional Scaling to cluster observations and compare habitats in ANOSIM. Finally, the percentage contribution of specific species to pair-wise habitat differences were examined using SIMPER (PRIMER, 2016).

Fig. 2. Oyster rack (“farm gear”) used to hold oyster bags. Racks in this photo are all empty, bags would be located on each of the three levels.

3. Results 3.1. Among-habitat comparisons A total of 39 seaweed taxa were collected over the course of the study, 35 in eelgrass, 28 from the oyster reef, 25 from farm gear, and 12 from the mudflat (Table 2). All four subtidal habitats were dominated by red algae, followed by greens; only three species of browns were collected and only in June 2014, hence no brown algae were included in the ANOVAs or multivariate analyses. An ANOVA using repeated measures with replicates nested within habitats showed species richness varied by habitat, month and their interaction (Table 3). Averaged across all three sampling occasions, the number of species per plot differed significantly among the four habitats (P < .0001, Fig. 4a). Species richness was greatest for farm gear, lower for oyster reef and lowest on the mudflat, with the average number of algal species in eelgrass between and similar to both farm gear and oyster reef. Species richness varied by month (P < .0001) and was generally lowest for the October sampling. Seaweed biomass also differed significantly among the four habitats (P < .0001), with farm gear supporting the greatest biomass, followed by eelgrass and oyster reef, and significantly less biomass found on the mudflat (Fig. 4b). The same pattern and statistical differences were found for the biomass of exotic algae found in the four habitats (Table 3). Native algae exhibited a slightly different pattern, and when graphed together with exotics showed that farm gear supported more exotic algal biomass than natural habitats of eelgrass beds, oyster reefs and mudflats but the proportion of exotics was high in both mudflats (84%) and farm gear (81%, Fig. 5). Based on percent occurrence and total biomass collected on a per taxon basis, the mudflat was dominated by red algae whereas the other three habitats were dominated by similar numbers of red and green taxa (Tables 2 and 4). Focusing on biomass, the same three taxa (i.e. Gracilaria tikvahiae, A. vermiculophyllum, and Ulva lactuca) represented > 90% of the total seaweed biomass collected from each

Fig. 3. Sampling device used to extract samples from all four study habitats (see text for details).

(wet weight to the nearest 0.1 g). The same general process was followed for sampling the farm gear, except four of the twelve replicate rack and bag units were haphazardly chosen on each occasion and sampled destructively. The sampler was quickly dropped over each unit pushing it to the bottom and trapping all organisms inside. In all four habitats and on each sampling date, this procedure resulted in four replicates with complete removal of organisms occupying 0.25 m2 of seafloor area and 0.125 m3 of the water column directly above the sampled area. Seaweed identification was based on Mathieson and Dawes (2017), Villalard-Bohnsack (1995), and Taylor (1962), plus other references cited by Mathieson (2016). The nomenclature primarily follows Guiry and Guiry (2015) and Silva et al. (1996), except for some recent changes resulting from molecular studies (e.g. Diaz-Tapia et al., 2017; Gurgel et al., 2018; Hayden et al., 2003; Kucera and Saunders, 2008; Lane et al., 2006; Wynne et al., 2019). Savoie and Saunders (2013, 2015, 2019) recently discussed taxonomic confusion between two morphological similar red algae Melanothamnus harveyi and M. japonica, which are difficult to differentiate without molecular tools. In the present text we have designated this complex as “M. harveyi.” 3

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Table 2 Seaweed taxa collected from four major habitats associated with an oyster aquaculture site at Nannie Island, at Woodman Point area of Great Bay, New Hampshire expressed as mean % occurrence and biomass (g damp dried weight/m2) N = 15 for all habitats except FG where N = 12; EG = Eelgrass; FG = Farm gear; MF = Mud flat; OR = Oyster Reef.

CHLOROPHYCEAE Bryopsis plumosa (Hudson) C. Agardh Chaetomorpha linum (O. F. Müller) Kützing Chaetomorpha picquotiana Montagne ex Kützing Cladophora sericea (Hudson) Kützing Prasiola stipitata Suhr in Jessen Ulva compressa C. Linnaeus Ulva flexuosa subsp. flexuosa Wulfen Ulva flexuosa subsp. paradoxa (C. Agardh) M. J. Wynne Ulva intestinalis C. Linnaeus Ulva lactuca C. Linnaeus Ulva linza C. Linnaeus Ulva prolifera O. F. Müller Ulva rigida C. Agardh Ulva sp.

EG

FG

6.7% (< 0.01 g) 13.3% (0.01 g) 6.7% (0.03 g) 13.3% (0.01 g) 13.3% (0.01 g) 8.3% (0.10 g) 26.7% (0.02 g) 33.3% (0.06 g) 6.7% (< 0.01 g) 86.7% (125.1 g) 6.7% (< 0.01 g)

8.3% (0.13 g)

20% (33.64 g) 26.7% (0.02 g)

PHAEOPHYCEAE Ascophyllum nodosum (C. Linnaeus) Le Jolis Hincksia granulosa (J. E. Smith) P. Silva ex Silva, Meñez et Moe Pylaiella littoralis (C. Linnaeus) Kjellman

MF

OR

13.3% (0.01)

41.7% (0.03 g) 16.7% (0.01 g) 33.3% (0.03 g) 58.3% (2.16 g) 33.3% (0.15 g) 100% (196.1 g) 33.3% (0.03 g) 6.7% (0.13 g) 41.7% (4.30 g)

13.3% (0.011 g) 13.3% (0.01 g) 6.7% (< 0.01 g) 53.3% (3.52 g) 13.3% (0.54 g)

habitat (Table 4). The habitats that were most similar to one another based on the level of shared species were farm gear compared to oyster reef (20 taxa, 83.3%), eelgrass compared to oyster reef (25 taxa, 79.4%), and eelgrass compared to farm gear (23 taxa, 76.7%; Table 5). By contrast, the low number of species found on the mudflat resulted in reduced affinities, ranging from 11 taxa (59.5%) in common with farm gear to 12 taxa (51.1 & 60%) compared to eelgrass and oyster reef, respectively.

100% (129.0 g) 6.7% (< 0.01 g) 6.7% (< 0.01 g) 6.7% (< 0.01 g) 20% (0.51 g) 60% (0.188 g) 86.7% (2.06 g) 60% (0.42 g) 6.7% (6.03 g) 6.7% (< 0.01 g) 20% (0.21 g) 26.7% (0.18 g) 73.3% (18.4 g) 73.3% (357.3 g) 40% (0.11 g) 66.7% (0.50 g) 20% (1.07 g) 6.7% (< 0.01 g) 100% (6.08 g) 13.3% (0.11 g)

13.3% (5.17 g) 20% (0.02 g) 13.3% (2.43 g)

6.7% (0.27 g) 6.7% (< 0.01 g)

RHODOPHYCEAE Agarophyton vermiculophyllum (Ohmi) Gurgel, J. N. Norris and S. Fredericq Aglaothamnion halliae (F. S. Collins) N. E. Aponte, D. L. Ballantine et J. Norris Aglaothamnion roseum (Roth) Maggs et L'Hardy-Halos Antithamnion cruciatum (C. Agardh) Nӓgeli Callithamnion corymbosum (J. E. Smith) Lyngbye Callithamnion tetragonum (Withering) S. F. Gray Ceramium deslongchampsii Chauvin in Duby Ceramium virgatum Roth Chondria baileyana (Montagne in Bailey) Harvey Chondrus crispus Stackhouse Coccotylus truncatus (Pallas) M. J. Wynne et J. N. Heine Cystoclonium purpureum (Hudson) Batters Dasya baillouviana (S. G. Gmelin) Montagne Dasysiphonia japonica (Yendo) H.-S. Kim Gracilaria tikvahiae McLachlan Hooperia divaricata (Durannt) M. J.Wynne, M.J. Wynne, C.W. Schneider and G. W. Saunders Kapraunia schneideri (Stuercke and Freshwater) Savoie and G. W. Saunders Melanothamnus harveyi (J. W. Bailey) M.-S. Kim, H.-G. Choi, Guiry et G.W. Saunders in Choi et al. Phyllophora pseudoceranoides (S. G. Gmelin) Newroth et A. R. Taylor Polysiphonia elongata (Hudson) Sprengel Polysiphonia fucoides (Hudson) Greville Polysiphonia stricta (Dillwyn) Greville

20% (0.02 g) 26.7% (0.03 g) 6.7% (< 0.01 g) 86.7% (60.0 g) 8.3% (< 0.01 g)

100% (1307.5 g) 8.3% (0.01 g) 33.3% (0.02 g) 16.7% (0.01 g)

66.7% (44.20 g)

58.3% (0.19 g) 66.7% (1.54 g) 66.7% (12.5 g)

20% (0.02 g) 13.3% (0.01 g) 13.3% (0.01 g)

13.3% (0.14 g) 100% (8.43 g) 100% (97.3 g) 41.7% (0.09 g) 66.7% (9.51 g)

6.7% (< 0.01 g) 20% (0.21 g) 33.3% (0.62 g) 6.7% (0.05 g) 20% (0.04 g)

8.3% (1.00 g) 83.3% (1.57 g) 83.3% (1.57 g)

100% (111.40 g) 6.7% (< 0.01 g) 46.7% (0.06 g) 6.7 (< 0.01 g) 13.3% (0.01 g) 46.7% (0.27 g) 40% (0.65 g) 60% (2.62 g) 6.7% (0.01 g) 26.7% (0.21 g) 53.3% (0.96 g) 100% (131.70 g) 66.7% (1.32 g) 6.7% (0.03 g) 53.3% (0.19 g) 40% (0.08 g) 6.7% (< 0.01 g)

3.2. General floristic patterns Thirty-six of the 39 seaweed taxa (92.3%) from the four habitats were native species, while Dasysiphonia japonica, Agarophyton vermiculophyllum and Melanothamnus harveyi were introduced species that probably originated from Japan or the Northwest Pacific (Mathieson and Dawes, 2017; Mathieson et al., 2008a,b), and all three species occurred in all four habitats (Table 2). Exotic species made up most of the total biomass on the farm gear (Fig. 5), but this was largely due to

Table 3 Statistical model to compare seaweed biomass and species richness among the four habitat types. Overall Model

R2 = 0.86

48 Observations

Species (#/0.25m2)

F = 6.52

P = .0001

R2 = 0.91

F = 10.74

P = .0001

Ln Biomass (0.25m2)

R2 = 0.91

F = 10.24

P = .0001

R2 = 0.92

F = 10.97

P = .0001

Ln Exotic Biomass (0.25m2)

Ln Native Biomass (0.25m2)

Variable

DF

MS

F

P

MS

F

P

MS

F

P

MS

F

P

Habitat Month Habitat*Month Rep[Habitat] Random Error

3 2 6 12

168 106 26.40 4.40

38.3 17.2 4.26 0.71

0.0001 0.0001 0.0046 0.7271

54.1 0.1 1.19 0.62

87 0.14 1.66 0.86

0.0001 0.8778 0.1748 0.591

48.4 2.27 1.01 0.7

68.7 3.25 1.46 1.01

0.0001 0.0562 0.2355 0.4706

39.8 0.6 2.41 0.41

97.5 1.11 4.43 0.75

0.0001 0.3463 0.004 0.7019

24

6.19

0.72

0.7

4

0.54

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Fig. 4. Habitat means +/− SE of algae for species richness (A) and biomass (B) with all sampling dates averaged (N = 12). Red algae (hashed bars) and green algae (solid bars) are shown separately for each habitat but were analyzed together and both analyses showed significant differences among habitats. Habitats with the same letter are not significantly different according to Tukeys post-hoc test (alpha = 0.05).

every habitat comparison, the three or four dominant nuisance algae in the Bay (Agarophyton vermiculophyllum, Gracilaria tikvahiae, Ulva lactuca and sometimes Dasysiphonia japonica) accounted for most of the differences between algal communities. Two of the four are exotics: Dasysiphonia japonica and A. vermiculophyllum; the complete SIMPER tables may be found in the online resources. 4. Discussion 4.1. Among habitat comparisons There is a substantial literature on the seaweeds of the GBE, mainly focusing on species occurring on natural hard substrates or as drift (unattached) algae (Hardwick-Witman and Mathieson, 1983; Mathieson and Hehre, 1986; Mathieson and Penniman, 1986, 1991). The present study documented high biomass of seaweeds on oyster farm gear, showing substantial habitat. To our knowledge these data are unique in the literature for oyster farm gear, though they are similar to previous research on clam farms (Powers et al., 2007). Moreover, these findings for macroalgae are similar to previous research in Great Bay (Glenn, 2016) as well as studies in other areas that described the same general trend for invertebrates and fish (DeAlteris et al., 2004; Erbland and Ozbay, 2008): oyster farm gear provides habitat for a wide range of organisms, and its value as measured by a variety of metrics is substantial. The present study indicated that the seaweed community that developed on the farm gear was somewhat similar in taxonomic richness and other metrics to seaweed communities on persistent eelgrass and oyster reef habitats but was significantly different in multivariate analyses and consisted of 81% exotic species biomass in comparison to eelgrass (22%) and oyster reef (37%). Although our study was not focused on successional patterns, relevant literature should be considered in interpreting the data, particularly for the farm gear. Previous research on successional patterns for seaweeds in New England colonizing hard substrata reveals a complex process involving competition, predation, and physical disturbances, which interact to determine the overall trajectory and community characteristics (reviewed by Mathieson et al., 1991). For example, Lubchenco (1983) and Chapman and Johnson (1990) described differences between annual and perennial taxa in competitive and other interactions in early successional stages for algal communities in New England, with some taxa attaining density dominance within several months. McCook and Chapman (1997) also found rapid early colonization by many seaweed taxa within 1 year at several study sites from Massachusetts to Nova Scotia, but wide differences among sites over the 3-year study period. Thus, it seems reasonable to conclude that our 16 month study likely characterized much of the algal community development that would normally occur on oyster farm gear, but did not characterize the full extent possible because maintenance practices that

Fig. 5. Biomass means +/− standard error for native algae (hashed bars) and exotic algae (solid bars) in the four habitats. Native and exotic biomasses were analyzed separately; values with the same letter (Native: Capital letters, Exotic lowercase letters) are not statistically different according to Tukeys post hoc tests (Table 3).

one species, A. vermiculophyllum (Table 3). In contrast, the biomass of native seaweeds was higher in eelgrass compared to exotics. Several native species that were commonly collected are characteristic of eutrophic habitats (Mathieson and Dawes, 2017; Wilkinson, 1980). Nine were ulvoid green algae, Ulva compressa, U. flexuosa subsp. flexuosa. U. f. subsp. paradoxa, U. intestinalis, U. lactuca, U. linza, U. prolifera, U. rigida, and U. species. Two of these ulvoid species (U. flexuosa subsp. paradoxa and U. lactuca) occurred at all four habitats, while U. compressa and U. prolifera were both restricted to single habitats. The guanotrophic green alga Prasiola stipitata, which can form extensive green coatings in areas of sea bird excrement and eutrophic estuarine habitats (Guiry and Guiry, 2015; Mathieson and Dawes, 2017), was recorded from three habitats. The brown alga Pylaiella littoralis, which is often referred to as “mung” because of its extensive growth in eutrophic habitats (Gross and Cheney, 1993, 1994; Lyons et al., 2007, 2009), was restricted to only one date in eelgrass habitats. When seaweed species composition (based on biomass) in each habitat was examined using Analysis of Similarity (ANOSIM), significant differences between all of the habitats were found (Global R = 0.513; Table 6). Oyster reefs and eelgrass beds supported most similar algal communities, although they were still significantly different (P < .005). A 3-dimensional graph of each sample based on a non-metric MDS of a Bray-Curtis similarity matrix following square root transformation showed that the mudflat samples had fewer species in disparate algal communities compared to the tighter but distinct communities sampled in the farm gear, eelgrass beds and oyster reefs (Fig. 6). The species that accounted for most of the differences between habitat types were found using the SIMPER analysis (PRIMER, 2016). In 5

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Table 4 Rank mean percent occurrence and biomass (damp dried/m2) patterns for the top 10–12 seaweed taxa from an oyster aquaculture site near Woodman Point, Newington, Great Bay, New Hampshire. % Occurrence Eelgrass Bed

Farm Gear

P. fucoides A. vermiculophyllum U. lactuca C. virgatum D. japonica G. tikvahiae M. harveyi C. virgatum C. baileyana U. flexuosa ssp. paradoxa

Mudflat

Oyster Reef

100% 100% 86.70% 86.70% 73.30% 73.30% 66.70% 60% 60% 33.50%

U. lactuca D. japonica G. tikvahiae A. vermiculophyllum P. fucoides P. stricta C. virgatum M. harveyi C. baileyana C. deslongchampsii

100% 100% 100% 100% 83.30% 83.30% 66.70% 66.70% 66.70% 58.10%

A. vermiculophyllum U. intestinalis G. tikvahiae C. deslongchampsii D. japonica M. harveyi U. rigida C. virgatum C. baileyana U. flexuosa ssp. paradoxa C. purpureum H. divaricata

66.70% 53.30% 33.30% 20% 20% 20% 13.30% 13.30% 13.30%

G. tikvahiae A. vermiculophyllum U. lactuca H. divaricata C. baileyana D. japonica M. harveyi A. roseum C. deslongchampsii C. virgatum P. fucoides

100% 100% 86.70% 66.70% 60% 53.30% 53.30% 46.70% 46.70% 40% 40%

6.70% 6.70% 6.70%

G. tikvahiae

357.3 g

A. vermiculophyllum

1307.5 g

A. vermiculophyllum

44.2 g

G. tikvahiae

131.7 g

A. vermiculophyllum U. lactuca U. rigida D. japonica K. schneideri C. crispus C. virgatum C. tetragonum M. harveyi

129.0 g 125.1 g 33.6 g 18.4 g 6.1 g 6.03 g 2.06 g 0.51 g 0.50 g

U. lactuca G. tikvahiae C. baileyana M. harveyi D. japonica Ulva sp. U. flexuosa ssp. paradoxa P. fucoides P. stricta

196.1 g 97.3 g 12.5 g 9.5 g 8.4 g 4.3 g

Ulva lactuca G. tikvahiae U. rigida D. japonica H. divaricata C. virgatum C. baileyana U. flexuosa ssp. flexuosa M. harveyi

3.5 g 0.62 g 0.54 g 0.213 g 0.053 g 0.011 g 0.011 g

A. vermiculophyllum U. lactuca U. rigida C. baileyana A. nodosum L. divaricta D. japonica C. deslongchampsii D. baillouviana

114.0 g 6.0 g 5.15 g 2.62 g 2.4 g 1.32 g 0.96 g 0.272 g 0.213 g

Biomass

2.2 g 1.6 g 1.6 g

marine ecosystems (Coen et al., 1999; Newell, 2004; McKindsey et al., 2006; reviewed in Coen and Grizzle, 2007; Forrest et al., 2009) including studies of shellfish farm gear (D'Amours et al., 2008; DeAlteris et al., 2004; Erbland and Ozbay, 2008; Tallman and Forrester, 2007). McCoy and Bell (1991) defined three axes to describe the relationships encompassed by “habitat structure”: heterogeneity, complexity, and scale. We did not assess our data using this level of characterization of the four habitats. However, we recognize that they could be arranged along a gradient from the mudflat with least structural heterogeneity and complexity to the farm gear with the most. In addition to these three structural characteristics, the farm gear provided hard as well as rigid substrata extending about ~0.5 m above the bottom overall and consisting of three levels (bags) of oysters. Thus, differences among the habitats would be expected and our metrics on seaweed communities reflect this overall gradient. Future studies might be designed to assess habitat provision with respect to more detailed characterization of structural differences in different types of farm gear.

Table 5 Affinities of seaweed populations from the four habitats expressed as number and percentage of shared taxa.

EG FG MF OR MEAN # MEAN %

EG

FG

MF

OR

35 (100%) 23 (76.7%) 12 (51.1%) 25 (79.4%) 23.8 76.80%

25 (100%) 11 (59.5%) 20 (83.3%) 19.8 79.90%

12 (100%) 12 (60%) 11.8 67.70%

28 (100%) 21.3 80.70%

EG = eelgrass; FG = farm gear; MF = mudflat; OR = oyster reef. Table 6 Results of Pairwise Tests using ANOSIM. Groups

R statistic

Significance level %

Actual permutations

Number ≥ Observed

M, EG M, OR M, FG EG, OR EG, FG OR, FG

0.553 0.493 0.586 0.279 0.668 0.779

0.1 0.1 0.1 0.5 0.1 0.1

999 999 999 999 999 999

0 0 0 4 0 0

0.005 g 0.038 g

4.2. General floristic trends Farm gear supported significantly greater biomass of exotic species than native species (Fig. 5). Conversely, native seaweed biomass was greater on the natural sites (eelgrass beds and oyster reefs). A similar trend was reported by Geraldi et al. (2014) who found that oyster reefs in their study area were dominated by the native seaweed Codium decorticatum but bulkheads and revetments were dominated by the nonnative Codium fragile. Tyrrell and Byers (2007) similarly reported a dominance of exotic fouling organisms (tunicates) on artificial hard substrate compared to natural. Three non-native seaweeds were particularly common in the present study: D. japonica, A. vermiculophyllum, and M. harveyi. These introduced species have proliferated in the North Eastern United States (Abreu, 2011; Abreu et al., 2011; Dijkstra et al., 2017; Mathieson and Dawes, 2017; Nyberg, 2007; Nyberg and Wallentinu, 2009; Rueness, 2005) and they have the potential of

remove seaweeds from gear vary from farm to farm. Our (Grizzle) personal observations over several years of seaweed communities that developed on farm gear in the GBE compare well with the present findings, but also suggest that more diverse and dense communities might be expected under some conditions and in some areas. Differences in bottom roughness and vertical structure of the farm gear relative to the three natural habitats also warrant discussion. There is a substantial literature describing increases in organism abundance and biomass on shellfish habitats that provide vertical structure in 6

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M. Glenn, et al.

Fig. 6. Three-dimensional plot of non-metric multi-dimensional scaling based on biomass data sorted by habitat with all sampling dates combined.

regulatory framework for permitting oyster farms in most states, including New Hampshire, has focused on minimizing potential negative impacts and user conflicts (Duff et al., 2003; Rice, 2006, 2008). But there is a growing trend towards more comprehensive management. For example, the National Research Council published a comprehensive assessment that focused on identifying best practices that could enhance the benefits and minimize the negative effects of bivalve aquaculture (NRC, 2010). In 2018, the National Oceanic and Atmospheric Administration (NOAA) rolled out its National Shellfish Initiative which aims “…to increase populations of bivalve shellfish in our nation's coastal waters—including oysters, clams, and mussels—through commercial production and conservation activities.” (https://www. fisheries.noaa.gov/content/national-shellfish-initiative). And several states have followed NOAA's lead, including Rhode Island (http:// www.shellfishri.com/ri-shellfish-initiative/). The present study adds habitat provision for seaweeds to the literature on the potential effects of oyster farming. Oyster farming in the GBE at present is restricted to the shallow subtidal waters in Little Bay, with about 30 ha (75 acres) licensed for oyster farming in 2018. During 2018, it was estimated that a total of 800 full scale rack-and-bag units were deployed on the farms (pers. comm., Robert Atwood, NH Fish and Game Department; Robert.Atwood@wildlife). The surface area of the top of each unit is ~1.0 m2, and it can be considered “new” hard substrate available for colonization by algae (and other organisms) because all farms are located on mudflat. Thus, although rack-and-bag gear in 2018 represented only a small portion (800 m2; =0.08 ha) of the 30 ha licensed for oyster farming, it is expected that the amount of farm gear in the water will increase as the industry develops. Management of wild populations of oysters has in recent decades become twofold, including the long-term historical focus on oysters as a fishery, and more recently on the ecological roles they play (Brumbaugh and Coen, 2009; Brown et al., 2014; Baggett et al., 2015). The latter focus has led to a rapidly growing literature on restoring oyster populations, and most coastal states in the US have some kind of “restoration” program. Programs that are aimed at the ecological roles of oysters typically include consideration of the various ecosystem services (e.g. habitat provision) oyster reefs provide, and the relevant literature focuses nearly entirely on invertebrates and fish (Coen and Humphries, 2017). Data from the present study on the wild reef adds habitat for seaweeds to the literature on the ecosystem services provided by oyster reefs.

altering native biodiversity and ecosystem functioning of subtidal communities (Keller et al., 2019; Ramsey-Newton et al., 2017). An ongoing ecological debate (e.g., Sotka and Byers, 2019) surrounds valuing ecosystem functions of exotic species. Melanothamnus hareyi has become a major nuisance alga on Cape Cod Beaches (Lyons et al., 2007, 2009) where it impacts tourist usage and beach access. In high densities it can adversely affect the growth of host plants through shading and nutrient competition (Anon, 2005). There are similar negative effects by drift populations of Agarophyton and Ulva (Mathieson, 2016: Mathieson et al., 2008a,b) which have also proliferated in Great Bay, likely due to increased nutrient concentrations (PREP, 2013, 2018). A. vermiculophyllum has also been linked to increases in Vibrio bacteria (Gonzalez et al., 2014) which poses unique circumstances on oyster farms in particular. Drift algae have been known to proliferate and become a nuisance, as respiration can lead to hypoxic events, faunal die-offs, and loss of highly valued habitat provided by seagrass (Harlin and Thorne-Miller, 1981; Short et al. 2002; Short and Burdick, 1996; Valiela et al., 1992). Non-natives and drift algae populations can also provide important ecological functions. Drift populations of Agarophyton and Ulva may enhance benthic species richness (Norkko et al., 2000) and increase habitat heterogeneity and complexity, providing refuge and forage for other species. Similarly, Dijkstra et al. (2017) found that D. japonica, which had recently covered up to 90% of some kelp beds (Dayton, 1985; Steneck et al., 2002), also supported two to three times more invertebrates at the base of the food chain than comparable kelp beds. A. vermiculophyllum may also enhance multiple ecosystem processes and functions. For example, it generates biological productivity and diversity, attenuates and/or dissipates tidal currents and waves, and results in nutrient and pollution uptake (Nyberg et al., 2009; Ramus et al., 2017). 5. Conclusion and management implications The present study provides new knowledge on a neglected component (seaweed communities) in the broader literature on oysters, including natural reefs and farms. For farms, there is a growing literature on both their negative and positive effects on the ecosystem (see references in Shumway, 2011 and Smaal et al., 2019). Consideration of the full range of impacts, including social dimensions, in a management context has been termed “ecosystem approaches to aquaculture” (CostaPierce, 2010), “integrative management” (Cranford et al., 2012), or similar. Although the potential ecological benefits of oyster farming have long been recognized by government regulators, the history of the 7

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Funding

interests or personal relationships that could have appeared to influence the work reported in this paper.

Partial funding was provided by the New Hampshire Agricultural Experiment Station via the USDA National Institute of Food and Agriculture Hatch Projects 1007230 and 100387. This is Scientific Contribution Series #569 Jackson Estuarine Laboratory and the Center of Marine Biology.

Acknowledgments We received help in field work, data analysis, and other respects from: Dave Shay; Krystin Ward; Chris Peter, Research Coordinator at the Great Bay National Estuarine Research Reserve; Courtney Brooks; Anna Bruning; Caroline Doherty; Liz Folz; Lesley Gardner; Anya George; Matthew Glenn; Jane Harrington; Jordan Hillyard; Debra Kam; Bill and Julie Kath; Peg O'Neil; Jillian Robillard; and Elizabeth Werner.

Declaration of Competing Interest The authors declare that they have no known competing financial Appendix A. Table showing SIMPER results Mudflat vs. Eelgrass Habitats Average dissimilarity = 87.14 Mudflat

Eelgrass

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Coccotylus truncatus Chaetomorpha linum Aglaothmnion roseum Ulva flexuosa ssp. paradoxa Cladophora sericae Ulva linza Ulva intestinalis Prasiola stipitata Cystoclonium purpureum Ulva flexuosa spp. flexuosa Ulva spp. Lomintaria divaricata Ulva spp.(filamentous) Dasya baillouviana Ulva rigida Phyllophora pseaudoceranoides Ceramium deslongchampsii Chondria baileyana Neosiphonia harveyi Chondus crispus Ceramium virgatum Polysiphoniaum fucoides Dasysiphonia japonica Agarophyton vermiculophyllum Ulva lactuca Gracilaria tikvahiae

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.17 0 0 0.04 0 0 0 0 0.07 4.32 0.61 0.04

0 0 0 0 0 0 0 0 0.03 0.01 0.01 0.01 0.02 0.06 0 0.33 0.04 0.13 0.16 1.88 0.45 1.32 5.75 35.97 31.46 115.28

0.03 0.03 0.04 0.05 0.05 0.07 0.07 0.12 0.14 0.16 0.19 0.24 0.32 0.4 0.45 0.56 0.59 1.1 1.28 1.42 2.3 3.25 6.06 17.17 18.78 32.29

Mudflat

Oyster Reef

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Ulva linza Ulva intestinalis Cystoclonium purpureum Ulva flexuosa ssp. paradoxa Cladophora sericae Callithamnion tetroagonum Prasiola stipitata Ulva spp. Ulva flexuosa spp. flexuosa Dasya baillouviana Ulva spp.(filamentous) Aglaothmnion roseum Polysiphoniaum fucoides Ceramium deslongchampsii Ulva rigida Neosiphonia harveyi Ceramium virgatum Lomintaria divaricata Dasysiphonia japonica

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.17 0 0 0 0.07

0 0 0 0 0 0 0 0.01 0.01 0.01 0.01 0.01 0.01 0.05 0 0.06 0.18 0.05 0.3

0.03 0.03 0.05 0.07 0.07 0.07 0.1 0.17 0.17 0.23 0.3 0.33 0.34 0.54 0.57 0.72 0.76 0.91 2.41

Percentage

Cumulative

Diss/SD

Contribution

Percentage

0.3 0.3 0.3 0.27 0.27 0.3 0.3 0.43 0.39 0.55 0.65 0.8 0.62 0.47 0.32 0.43 0.9 0.95 1.07 0.3 1.23 1.6 1.69 1.93 1.78 3.96

0.03 0.03 0.05 0.06 0.06 0.08 0.08 0.13 0.16 0.19 0.22 0.28 0.36 0.46 0.51 0.64 0.68 1.27 1.47 1.62 2.64 3.73 6.96 19.7 21.55 37.05

100 99.97 99.94 99.89 99.83 99.77 99.69 99.61 99.48 99.32 99.14 98.92 98.64 98.28 97.82 97.31 96.67 95.99 94.72 93.25 91.63 88.99 85.26 78.3 58.6 37.05

Percentage

Cumulative

Diss/SD

Contribution

Percentage

0.3 0.3 0.3 0.29 0.29 0.3 0.41 0.54 0.54 0.67 0.64 0.69 0.78 0.87 0.34 1 0.54 0.72 0.84

0.04 0.04 0.06 0.09 0.09 0.09 0.13 0.21 0.21 0.28 0.37 0.41 0.42 0.67 0.7 0.88 0.93 1.11 2.94

100 99.96 99.92 99.85 99.77 99.68 99.6 99.47 99.26 99.05 98.77 98.4 97.99 97.58 96.91 96.21 95.33 94.4 93.29

Mudflat vs. Oyster Reef Habitats Average dissimilarity = 81.83

8

Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

M. Glenn, et al. Chondria baileyana Ulva lactuca Gracilaria tikvahiae Agarophyton vermiculophyllum

0.04 0.61 0.04 4.32

0.8 17.9 34.43 31.56

2.93 18.52 24.24 28.24

Eelgrass

Oyster Reef

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Coccotylus truncatus Chaetomorpha linum Callithamnion tetroagonum Ulva linza Ulva intestinalis Cystoclonium purpureum Prasiola stipitata Ulva flexuosa spp. flexuosa Aglaothmnion roseum Ulva spp. Ulva spp.(filamentous) Dasya baillouviana Lomintaria divaricata Phyllophora pseaudoceranoides Ceramium deslongchampsii Neosiphonia harveyi Chondus crispus Chondria baileyana Ceramium virgatum Polysiphoniaum fucoides Dasysiphonia japonica Agarophyton vermiculophyllum Ulva lactuca Gracilaria tikvahiae

0 0 0 0 0 0.03 0 0.01 0 0.01 0.02 0.06 0.01 0.33 0.04 0.16 1.88 0.13 0.45 1.32 5.75 35.97 31.46 115.28

0 0 0 0 0 0 0 0.01 0.01 0.01 0.01 0.01 0.05 0 0.05 0.06 0 0.8 0.18 0.01 0.3 31.56 17.9 34.43

0.02 0.02 0.03 0.06 0.06 0.08 0.1 0.14 0.15 0.15 0.24 0.3 0.37 0.4 0.41 0.73 0.96 1.37 1.43 2.03 3.73 7.25 7.55 13.69

0.98 1.65 2.39 2.28

3.58 22.63 29.63 34.51

90.35 86.77 64.14 34.51

Percentage

Cumulative

Diss/SD

Contribution

Percentage

0.3 0.3 0.29 0.4 0.4 0.3 0.59 0.73 0.7 0.79 0.78 0.57 0.74 0.42 1.01 1.13 0.3 1 1.32 1.38 1.45 1.41 1.48 1.54

0.05 0.05 0.08 0.14 0.14 0.19 0.25 0.34 0.35 0.37 0.59 0.72 0.89 0.98 0.99 1.76 2.33 3.31 3.47 4.92 9.05 17.57 18.29 33.17

100 99.95 99.9 99.82 99.69 99.55 99.36 99.11 98.77 98.42 98.05 97.46 96.74 95.85 94.87 93.87 92.11 89.78 86.47 83 78.09 69.04 51.46 33.17

Percentage

Cumulative

Eelgrass vs. Oyster Reef Habitats Average dissimilarity = 41.26

Mudflat vs. Farm Gear Habitats Average dissimilarity = 89.24 Mudflat

Farm Gear

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Diss/SD

Contribution

Percentage

Aglaethmnion halliae Cystoclonium purpureum Prasiola stipitata Callithamnion corymbosum Ulva compressa Bryopsis plumosa Ulva prolifera Ulva linza Aglaothmnion roseum Cladophora sericae Ulva flexuosa ssp. paradoxa Dasya baillouviana Lomintaria divaricata Ulva intestinalis Polysiphonia elongata Ulva rigida Ceramium deslongchampsii Ulva flexuosa spp. flexuosa Ulva spp. Ceramium virgatum Polysiphoniaum fucoides Ulva spp.(filamentous) Neosiphonia harveyi Chondria baileyana Dasysiphonia japonica Gracilaria tikvahiae Ulva lactuca Agarophyton vermiculophyllum

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.17 0 0 0 0 0 0 0 0.04 0.07 0.04 0.61 4.32

0 0 0 0 0.03 0.03 0.03 0.01 0.01 0.01 0.08 0.04 0.02 0.04 0.25 0 0.05 0.14 0.23 0.39 0.39 0.54 2.38 3.13 2.11 24.34 49.03 326.63

0.03 0.03 0.05 0.06 0.1 0.11 0.11 0.12 0.13 0.16 0.17 0.19 0.19 0.21 0.3 0.34 0.36 0.48 0.7 1.01 1.09 1.25 2.16 2.97 3 12.76 14.34 46.84

0.3 0.29 0.44 0.44 0.3 0.3 0.3 0.69 0.68 0.8 0.37 0.37 0.78 0.53 0.3 0.32 1.04 0.63 0.74 0.92 0.95 1.1 0.93 0.82 0.93 2.36 1.76 3.83

0.03 0.03 0.06 0.06 0.11 0.12 0.13 0.13 0.14 0.18 0.19 0.21 0.21 0.23 0.34 0.38 0.41 0.54 0.78 1.13 1.22 1.41 2.42 3.33 3.36 14.3 16.07 52.49

100 99.97 99.93 99.87 99.81 99.7 99.57 99.45 99.32 99.17 98.99 98.81 98.6 98.39 98.16 97.82 97.44 97.04 96.5 95.71 94.59 93.36 91.96 89.54 86.21 82.85 68.56 52.49

9

Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

M. Glenn, et al. Eelgrass vs. Farm Gear Habitats Average dissimilarity = 49.79 Eelgrass

Farm Gear

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Coccotylus truncatus Chaetomorpha linum Aglaethmnion halliae Callithamnion corymbosum Cystoclonium purpureum Ulva compressa Prasiola stipitata Bryopsis plumosa Ulva prolifera Ulva linza Cladophora sericae Aglaothmnion roseum Ulva flexuosa ssp. paradoxa Ulva intestinalis Lomintaria divaricata Polysiphonia elongata Dasya baillouviana Ceramium deslongchampsii Phyllophora pseaudoceranoides Ulva flexuosa spp. flexuosa Ulva spp. Chondus crispus Ulva spp.(filamentous) Ceramium virgatum Polysiphoniaum fucoides Neosiphonia harveyi Chondria baileyana Dasysiphonia japonica Ulva lactuca Gracilaria tikvahiae Agarophyton vermiculophyllum

0 0 0 0 0.03 0 0 0 0 0 0 0 0 0 0.01 0 0.06 0.04 0.33 0.01 0.01 1.88 0.02 0.45 1.32 0.16 0.13 5.75 31.46 115.28 35.97

0 0 0 0 0 0.03 0 0.03 0.03 0.01 0.01 0.01 0.08 0.04 0.02 0.25 0.04 0.05 0 0.14 0.23 0 0.54 0.39 0.39 2.38 3.13 2.11 49.03 24.34 326.63

0.02 0.02 0.02 0.04 0.06 0.07 0.07 0.08 0.08 0.09 0.1 0.1 0.1 0.15 0.16 0.21 0.26 0.29 0.3 0.34 0.48 0.68 0.83 0.93 1.3 1.45 1.86 2.51 6.84 8.98 21.39

Oyster Reef

Farm Gear

Average

Species

Av.Abund

Av.Abund

Dissimilarity

Aglaethmnion halliae Callithamnion tetroagonum Callithamnion corymbosum Prasiola stipitata Ulva compressa Bryopsis plumosa Ulva prolifera Ulva linza Ulva flexuosa ssp. paradoxa Cladophora sericae Aglaothmnion roseum Ulva intestinalis Dasya baillouviana Polysiphonia elongata Lomintaria divaricata Ceramium deslongchampsii Ulva flexuosa spp. flexuosa Ulva spp. Polysiphoniaum fucoides Ceramium virgatum Ulva spp.(filamentous) Neosiphonia harveyi Dasysiphonia japonica Chondria baileyana Gracilaria tikvahiae Ulva lactuca Agarophyton vermiculophyllum

0 0 0 0 0 0 0 0 0 0 0.01 0 0.01 0 0.05 0.05 0.01 0.01 0.01 0.18 0.01 0.06 0.3 0.8 34.43 17.9 31.56

0 0 0 0 0.03 0.03 0.03 0.01 0.08 0.01 0.01 0.04 0.04 0.25 0.02 0.05 0.14 0.23 0.39 0.39 0.54 2.38 2.11 3.13 24.34 49.03 326.63

0.02 0.03 0.04 0.07 0.08 0.09 0.09 0.09 0.11 0.11 0.15 0.16 0.2 0.23 0.32 0.33 0.39 0.54 0.74 0.86 0.95 1.65 1.91 2.3 5.47 7.55 23.64

Percentage

Cumulative

Diss/SD

Contribution

Percentage

0.3 0.3 0.3 0.44 0.3 0.3 0.59 0.3 0.3 0.71 0.8 0.71 0.3 0.56 1.01 0.3 0.57 1.08 0.41 0.72 0.82 0.29 1.17 1.19 1.23 1.03 0.85 1.29 1.45 1.27 2.1

0.03 0.03 0.04 0.08 0.12 0.14 0.14 0.15 0.16 0.18 0.19 0.2 0.2 0.3 0.33 0.42 0.52 0.58 0.61 0.69 0.96 1.38 1.68 1.86 2.61 2.91 3.75 5.05 13.73 18.03 42.96

100 99.97 99.94 99.9 99.82 99.7 99.57 99.42 99.27 99.11 98.94 98.75 98.55 98.35 98.06 97.73 97.31 96.79 96.2 95.6 94.91 93.95 92.57 90.9 89.04 86.43 83.52 79.77 74.73 60.99 42.96

Percentage

Cumulative

Diss/SD

Contribution

Percentage

0.3 0.29 0.44 0.6 0.3 0.3 0.3 0.74 0.3 0.81 0.88 0.55 0.57 0.3 0.83 1.09 0.72 0.8 0.88 1.01 1.15 0.97 1.01 0.96 1.16 1.4 3.13

0.05 0.05 0.09 0.15 0.16 0.18 0.18 0.2 0.23 0.23 0.32 0.34 0.42 0.49 0.67 0.69 0.8 1.12 1.55 1.78 1.97 3.42 3.97 4.78 11.38 15.68 49.12

100 99.95 99.9 99.81 99.66 99.5 99.32 99.14 98.94 98.71 98.49 98.17 97.83 97.41 96.92 96.25 95.56 94.76 93.63 92.09 90.31 88.34 84.91 80.95 76.17 64.79 49.12

Oyster Reef vs. Farm Gear Habitats Average dissimilarity = 48.13

10

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Journal of Experimental Marine Biology and Ecology 524 (2020) 151307

References

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