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Biological Correlates of Sea Urchin Recruitment in Kelp Forest and Urchin Barren Habitats

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Biological Correlates of Sea Urchin Recruitment in Kelp Forest and Urchin Barren Habitats Vol. 663: 115–125, 2021 MARINE ECOLOGY PROGRESS SERIES Published March 31 https://doi.org/10.3354/meps13621 Mar Ecol Prog Ser OPEN ACCESS Biological correlates of sea urchin recruitment in kelp forest and urchin barren habitats B. Weitzman1,2,3,*, B. Konar2 1US Geological Survey, Alaska Science Center, Anchorage, AK 99508, USA 2University of Alaska Fairbanks, College of Fisheries and Ocean Sciences, Fairbanks, AK 99709, USA 3Present address: NOAA, National Ocean Service, National Centers for Coastal Ocean Science, Homer, AK 99603, USA ABSTRACT: Shifts between the alternate stable states of sea urchin barren grounds and kelp forests correspond to sea urchin density. In the Aleutian Archipelago, green sea urchins Strongy- locentrotus polyacanthus are the dominant herbivores that graze kelp forests. Sea urchin recruit- ment is an important driver that influences sea urchin density, particularly in the absence of top- down control from a keystone predator such as the sea otter Enhydra lutris. To understand how the biological community may influence patterns of sea urchin recruitment, we compared sea urchin recruit (size ≤20 mm) densities with biomass of other benthic organisms in both barren ground and kelp forest habitats at 9 islands across the Aleutian Archipelago. Patterns of biological community structure between the 2 habitats did not explain patterns of sea urchin recruits; how- ever, the same 10 specific taxa were found to correlate with sea urchin recruits in each habitat. Taxa that showed strong positive correlations included Codium, Constantinea, Schizymenia, and hydrozoans, while strong negative correlations were observed with Pachyarthron and Pugettia. Weak positive correlations were observed with Alcyonidium and ascidiaceans in both habitats, while weak variable relationships were detected with Polysiphonia and Corallina between habi- tats. The observed species-specific relationships may be due to small sea urchin displacement by larger conspecifics, larval responses to settlement cues, post-settlement survival via biogenic refu- gia, or potentially predation. These potential species-specific interactions were apparent, regard- less of habitat, and it can be inferred that they would be preserved in the presence or absence of keystone predation. KEY WORDS: Kelp forest · Nearshore habitats · Recruitment · Species interaction · Urchin barrens 1. INTRODUCTION urchins can have important effects on marine habi- tats, as they heavily graze fleshy macroalgae and Sea urchins are often the key herbivore causing cause bioerosion of biogenic reef habitats (Steneck et the transition between the alternate stable states of al. 2017, Rasher et al. 2020). They also provide a key kelp forest (high fleshy macroalgal cover and low food source for upper trophic levels, such as the sea urchin density) to barren ground (low fleshy macro- otter Enhydra lutris in the north Pacific (Watt et al. algal cover and high urchin density) habitats on tem- 2000, Larson et al. 2015). Urchin demographics influ- perate rocky reefs (Estes & Duggins 1995, Gagnon et ence the role that urchins play in an ecosystem as a al. 2004, Filbee-Dexter & Scheibling 2014). Habitat herbivore or as prey. Demographic factors such as shifts towards sea urchin barrens have been reported size, fecundity, and recruitment will affect popula- across temperate latitudes globally (Johnson et al. tion density, grazing rates, and movement (Himmel- 2011, Ling et al. 2015, Krumhansl et al. 2016). Sea man 1986, Dumont et al. 2006). While effects that © The authors 2021. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 116 Mar Ecol Prog Ser 663: 115–125, 2021 urchins can have on habitat and ecosystem structure and high urchin density) and kelp forests (high fleshy and the role that they play in food webs are well macroalgal cover and low urchin density), there known, the drivers of sea urchin demographics are would likely be different biological correlates of sea complex. Sea urchin demographics may be influ- urchin recruitment. However, if there were similar enced by environmental gradients (Ebert 2010, Ling species associated with sea urchin recruitment in et al. 2015) and can vary greatly across regions due both habitats, this would suggest overarching spe- to environmental forcing on sea urchins through cies interactions that are key drivers to sea urchin ontogeny (Estes & Duggins 1995). Recruitment and recruitment, regardless of habitat state. post-settlement survival is a fundamental process in sea urchin demographics. Biological drivers can have a strong influence on 2. MATERIALS AND METHODS sea urchin recruitment through multiple pathways that influence post-settlement distribution, growth, At 9 islands in the Aleutian Archipelago, from and survival. Sea urchin growth and age structure Chuginadak in the east to Attu in the west (Fig. 1), a can be influenced by the algal cover on which they total of 360 benthic community quadrats were exam- are feeding (Ling et al. 2019). Additionally, the whip- ined from both habitats, barren ground or kelp forest, ping action of kelps, particularly Desmarestia viridis in August 2016 and 2017. At each island, 4 sites were and Eualaria fistulosa, can physically prevent sea established, 2 within each habitat type that best rep- urchins from overgrazing (Konar et al. 2014). Globally, resented these habitats based on the presence or top-down control of sea urchin demographics via pre- absence of consistently dense subcanopy kelps dation has long been recognized (Pederson & Johnson across the entire area to be sampled (see Metzger et 2006, Fagerli et al. 2014, Sheppard-Brennand et al. al. 2019 for details on community structure within 2017). In the Aleutian Archipelago of Alaska, the pre- both types of habitats). While some limited fleshy cipitous decline of sea otters in the late 1990s and macroalgae were found in barrens, there was an early 2000s, likely due to killer whale predation (Estes obvious lack of kelp species (primarily Eualaria, Tha- et al. 1998), has allowed us to examine how benthic lassiophyllum, and Saccharina) and an abundance of ecosystems function in the absence of keystone pred- sea urchins. All sites were in approximately 6 to 8 m ators. Here, the presence of both barren ground and water depth, on rocky benches along exposed shore- kelp forest habitats across the Aleutian Archipelago lines. At each site, divers using SCUBA scraped all offers an ideal opportunity to investigate how biologi- mobile and sessile epibiota from each of 10 haphaz- cal features influence sea urchin recruitment within ardly placed 0.25 m2 quadrats into a fine mesh pillow these 2 habitats. Kelp forests are believed to be more case. All invertebrates and macroalgae were re tur - biodiverse and productive than barren grounds, with ned to the shipboard laboratory for species identifi- a large amount of food available to sea urchins that cation and quantification of total wet biomass (g). All can survive. The obvious differences in community organisms were visually identified to the finest taxo- structure between kelp forest and barren ground nomic resolution possible with the aid of light micro- habitats are likely to drive differences in sea urchin recruitment, which may differ between kelp forest and barren grounds (Himmelman 1986) due to dif- ferences in pre- and post-settlement processes that regulate growth and survival of newly recruited sea urchins (Rowley 1989). Here, we ask how the surrounding biological community influences pat- terns of sea urchin recruitment and whether taxa that are correlated with recruits differ between kelp forest and barren ground habitats. We hypo - thesized that given the different com- munity structures between barren Fig. 1. The Aleutian Archipelago with study islands. (f) Benthic community grounds (low fleshy macroalgal cover sampling sites Weitzman & Konar: Biological correlates of sea urchin recruitment 117 scopes and species keys. Test diameters of all sea (PERMANOVA; McArdle & Anderson 2001) with Ha - urchins were measured to the nearest mm using bitat treated as a fixed factor and Island treated as a calipers to determine size frequencies within each random factor. A similarity percentage analysis (SIM- quadrat. PER) was used to determine the community taxa most Data used in this study were initially analyzed for important in explaining the dissimilarity in community overall community structure differences between structure between habitats. A distance based linear habitats (Metzger et al. 2019) and then archived with regression (DistLM; Anderson et al. 2008) analysis the Biological & Chemical Oceanography Data Man- was used to statistically determine the community agement Office as epibenthic community abundance taxa that were significantly correlated with sea urchin (Edwards & Konar 2018a) and biomass (Edwards & recruit densities, using the fourth-root transformed Konar 2018b). Our analyses used PRIMER v7 and community biomass by quadrat as the predictor vari- PERMANOVA+ (PRIMER-e, Quest Research; Ander- able worksheet. DistLM and nMDS were constructed son et al. 2008, Clarke et al. 2014, Clarke & Gorley for barren ground and remnant kelp forest habitats 2015). Individual sea urchin sizes were assigned a independently, to determine taxa that were signifi- size class (Recruit: ≤20 mm, Small: 21−35 mm,
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