Blain C and Gagnon P (2014), Canopy-forming seaweeds in urchin-dominated sys...

ECB-ART-43423

PLoS One 2014 Jan 01;95:e98204. doi: 10.1371/journal.pone.0098204.

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Canopy-forming seaweeds in urchin-dominated systems in eastern Canada: structuring forces or simple prey for keystone grazers?

Blain C , Gagnon P .

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Models of benthic community dynamics for the extensively studied, shallow rocky ecosystems in eastern Canada emphasize kelp-urchin interactions. These models may bias the perception of factors and processes that structure communities, for they largely overlook the possible contribution of other seaweeds to ecosystem resilience. We examined the persistence of the annual, acidic (H2SO4), brown seaweed Desmarestia viridis in urchin barrens at two sites in Newfoundland (Canada) throughout an entire growth season (February to October). We also compared changes in epifaunal assemblages in D. viridis and other conspicuous canopy-forming seaweeds, the non-acidic conspecific Desmarestia aculeata and kelp Agarum clathratum. We show that D. viridis can form large canopies within the 2-to-8 m depth range that represent a transient community state termed "Desmarestia bed". The annual resurgence of Desmarestia beds and continuous occurrence of D. aculeata and A. clathratum, create biological structure for major recruitment pulses in invertebrate and fish assemblages (e.g. from quasi-absent gastropods to >150,000 recruits kg(-1) D. viridis). Many of these pulses phase with temperature-driven mass release of acid to the environment and die-off in D. viridis. We demonstrate experimentally that the chemical makeup of D. viridis and A. clathratum helps retard urchin grazing compared to D. aculeata and the highly consumed kelp Alaria esculenta. In light of our findings and related studies, we propose fundamental changes to the study of community shifts in shallow, rocky ecosystems in eastern Canada. In particular, we advocate the need to regard certain canopy-forming seaweeds as structuring forces interfering with top-down processes, rather than simple prey for keystone grazers. We also propose a novel, empirical model of ecological interactions for D. viridis. Overall, our study underscores the importance of studying organisms together with cross-scale environmental variability to better understand the factors and processes that shape marine communities.

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Genes referenced: LOC100887844 LOC100893907 LOC115925415

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	Figure 1. A thick canopy (∼70–90% cover) of sweeping Desmarestia viridis sporophytes at depths of 5 to 8 m on urchin (Strongylocentrotus droebachiensis) barrens in Bay Bulls (Newfoundland, eastern Canada) in June 2012 (A) and July 2013 (B).Maturing sporophytes of Desmarestia aculeata (foreground) and the kelp Alaria esculenta (background) intersperse with the D. viridis canopy. A sparse canopy (∼10–15% cover) of D. viridis below the lower edge of a shallow (0–2 m deep) A. esculenta bed in June 2011 (C). A cluster of A. esculenta amidst mixed canopy of D. viridis and D. aculeata at a depth of ∼3 m in July 2011 (D). Note that urchins are largely restricted to non-swept rocky surfaces (A, B, C, and D). (Photos: Patrick Gagnon)
	Figure 2. Mean (±SE) Desmarestia viridis cover and urchin (Strongylocentrotus droebachiensis) density at 2 (A, B), 3 (C, D), 4 (E, F), and 8 (G, H) m depths, and averaged across all depths (I and J) at Bread and Cheese Cove (BCC) and Keys Point (KP) from 8 March to 13 October, 2011.Each data point in panels A to H is the average cover of D. viridis or urchin density in 10 quadrats (0.8 m2 each) from two transects (20 to 25 m) at each depth. The seeming lack of standard error on some data points is due to low data variation. Solid and dashed horizontal lines are the average D. viridis cover and urchin density, respectively, from 8 April to 23 September (12 data points; see “Materials and methods” for the details of restriction of the statistical analyses to these points). The number in parentheses within each panel is the ratio of urchin density to D. viridis cover, also from 8 April to 23 September.

	Figure 4. Non-metric multidimensional scaling (nMDS) plots of Bray-Curtis similarities of Desmarestia viridis, Desmarestia aculeata, and Agarum clathratum based on associated epifauna (4th-root transformed density, individuals g−1 of seaweed) from 18 February to 9 October, 2011 at Keys Point.(A) Each data point is the average of samples for a given month [n = 7 to 10, except 3 for A. clathratum in February, for a total n = 221]. The trajectory of change for each seaweed is shown by solid lines connecting consecutive months. Numbers next to symbols indicate sampling month: February (2), March (3), April (4), May (5), June (6), July (7), August (8), September (9), and October (10). (B, C, D) Each data point is one sample within a given month (n = 80 [D. viridis], 77 [D. aculeata], and 64 [A. clathratum]). Group 1 and Group 2 designate clusters of months used in ANOSIM and SIMPER analyses (see Results).
	Figure 5. Mean (±SE) density (note the change in scale) of individuals in the six numerically dominant invertebrate taxa and gastropod (Lacuna vincta) and fish (unknown species) egg masses associated with Desmarestia viridis, Desmarestia aculeata, and Agarum clathratum from 18 February to 9 October, 2011 at Keys Point (n = 7 to 10 for each data point, except for A. clathratum in February where n = 3).Bivalvia: Hiatella arctica, Modiolus modiolus, and Mytilus sp.; Gastropoda: Dendronotus frondosus, Lacuna vincta, and Margarites helicinus; Copepoda: unidentified species in the Order Harpacticoida; Amphipoda: Ampithoe rubricata, Calliopius laeviusculus, Caprella linearis, Caprella septentrionalis, Gammarellus angulosus, Gammarus oceanicus, Gammarus setosus, Ischyrocerus anguipes, Leptocheirus pinguis, Pontogeneia inermis, and Stenothoe brevicornis; Polychaeta: Alitta virens, Autolytinae sp., Bylgides sarsi, Lepidonotus squamatus, Nereis pelagica, Phyllodoce mucosa, and Spirorbis borealis; Isopoda: Idotea baltica and Munna sp.
	Figure 6. Mean (±SE) Shannon diversity index, H' (A), Pielou's evenness index, J' (B), and species richness, S (C), of epifauna on Desmarestia viridis, Desmarestia aculeata, and Agarum clathratum from 18 February to 9 October, 2011 at Keys Point (n = 7 to 10 for each data point, except for A. clathratum in February where n = 3).

	Figure 8. Empirical model of ecological interactions in sporophytes of the annual, acidic (H2SO4), brown seaweed Desmarestia viridis in urchin (Strongylocentrotus droebachiensis) barrens in eastern Canada throughout an entire growth season (March to October).The dominant environmental controls (temperature and urchin grazing) are shown as open rectangles and dashed lines, D. viridis traits (cover/sweeping, specific growth rate [SGR], pH, and mortality) as gray ellipses and solid lines, and epifauna (fish eggs, bivalves [B], herbivorous gastropods [G], and predatory polychaetes [P] and isopods [I]) as solid rectangles and dotted lines. Numbers above rectangles and ellipses are the sources of information for temporal variation: 1 [present study]; 2 [28]; 3 [30]; 4 [35]; 5 [57]; 6 [36] (see “Discussion” for a detailed description of the model).

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