Widespread kelp-derived carbon in pelagic and benthic nearshore fishes suggested by stable isotope analysis
Graphical abstract
Map of black rockfish (left) and kelp greenling (right) sampling locations in the northeast Pacific Ocean with pie charts representing the relative carbon contributions from kelp (brown) and phytoplankton (green) primary producers estimated using carbon (δ13C) and nitrogen (δ15N) stable isotope values of muscle tissue. Black rockfish feed pelagically in the nearshore water column and kelp greenling feed benthically in nearshore waters. Mixing models were used to estimate carbon contributions based on site-specific phytoplankton and kelp (Table 2) and trophic discrimination factors (mean ± SD) of 1.0 ± 1.0‰ for δ13C per trophic level. Image credits: kelp and phytoplankton Jane Thomas and Tracey Saxby, IAN Image Library (http://ian.umces.edu/imagelibrary) and fish pictures, Washington Department of Fish and Wildlife.
Introduction
Kelp forests are ubiquitous along temperate and sub-arctic coastlines (Dayton, 1985, Estes and Steinberg, 1988) where they provide habitat and prey for diverse and abundant fish assemblages (Bodkin, 1988, Efird and Konar, 2014, Leaman, 1980, Siddon et al., 2008). Kelp-derived energy may also provide a trophic benefit to fishes (Foster and Schiel, 1985, Koenigs et al., 2015), as is the case for several benthic invertebrates (Duggins et al., 1989, Eckman and Duggins, 1991, Fredriksen, 2003, Salomon et al., 2008, Tallis, 2009). Nearshore marine food webs are complex with energy derived from phytoplankton, macroalgae (e.g., kelp), and terrestrial primary production (Duggins et al., 1989, Dunton et al., 2012, Fredriksen, 2003, Tallis, 2009, von Biela et al., 2013) and changes in the availability of these energy sources appears to influence the growth and production of fishes (Robards et al., 2002, von Biela et al., 2011). Canopy-forming kelps are a conspicuous source of energy with a concentrated biomass of primary production available to food webs by grazers, detritivores, and filter feeders (Kaehler et al., 2006, Steneck et al., 2002). Understanding the extent to which kelp provides energy throughout the nearshore food web is a priority as warming temperatures, rising sea levels, and increased human development have the potential to disrupt the function of ecologically and economically important nearshore ecosystems (Agardy et al., 2005, Harley et al., 2006, Scavia et al., 2002). Critical knowledge gaps include understanding the extent to which kelp energy reaches higher trophic level predators, such as fishes, and whether kelp is a routine source of energy for pelagic-, as well as benthic-, feeding species.
Kelp forest fish assemblages include species that are associated with the seafloor and forage benthically and species that occur primarily in the water column and forage pelagically within and along the edge of kelp forests. We define kelp forest ecosystems in this study as subtidal rocky reefs characterized by canopy- and understory-forming kelp (brown algae of the order Laminariales) in the neritic zone and use the term pelagic to refer to water column feeding in nearshore habitats unless otherwise specified. Evidence of kelp-derived energy in nearshore food webs has most often focused on benthic invertebrates (Duggins et al., 1989, Fredriksen, 2003, Salomon et al., 2008, Tallis, 2009) and occasionally benthic fishes or other predators that consume benthic invertebrates (Duggins et al., 1989, McMeans et al., 2013). In these studies, kelp-derived energy enters food webs either through the direct grazing of live kelp by kelp herbivores (e.g., urchins) or more commonly as kelp detritus by filter and suspension feeders (e.g., clams and mussels) (Duggins et al., 1989, Fredriksen, 2003, Salomon et al., 2008, Tallis, 2009). Recently, the tissues of pelagic-feeding fishes in nearshore systems were shown to contain substantial amounts of benthically produced carbon (Kopp et al., 2015) and kelp carbon (Koenigs et al., 2015, Markel and Shurin, 2015).
If kelp-derived energy is an important reason why so many fishes are associated with kelp forests, kelp should be a routine and substantial source of primary production that supplies energy for species that have either benthic or pelagic feeding modes. Energy can be traced through food webs by analyzing carbon (δ13C) and nitrogen (δ15N) isotope values. Kelp generally have higher δ13C values than sympatric phytoplankton and these differences propagate up the food chain even when predators are separated from primary producers by several trophic levels (Duggins et al., 1989, Fredriksen, 2003, Michener and Kaufman, 2007, Page et al., 2008, Tallis, 2009). When the isotope values of both primary producers (e.g., kelp and phytoplankton) and focal consumers (e.g., fish) are measured, a stable isotope mixing model can estimate the relative carbon contribution of each primary producer (e.g., Parnell et al., 2010). Mixing models also require estimates of consumer trophic level that can be estimated from δ15N analysis and trophic discrimination factors, defined as the isotopic difference between consumer tissues and that of their prey (Δ13Ctissue-diet or Δ15Ntissue-diet). Ideally, isotope values of potential energy sources used in mixing models are well constrained, however, δ13C and δ15N values of phytoplankton and kelp can vary both spatially and seasonally (Bond and Diamond, 2011, Fox, 2013, Miller and Page, 2012, Page et al., 2008, Simenstad et al., 1993) and may require some considerations.
Black rockfish (Sebastes melanops) and kelp greenling (Hexagrammos decagrammus) are ideal focal predators for examining the use of both kelp and phytoplankton energy pathways in the northeast Pacific Ocean. Both fishes are widely distributed in nearshore habitats with small individual home ranges (∼1 km2; Love, 2011, Parker et al., 2007), assuring that capture locations reflect foraging grounds. Each species represents one of the two principal feeding modes in aquatic marine ecosystems, pelagic and benthic. Black rockfish are water-column (e.g., pelagic) generalists that consume forage fish, euphausiids, and zooplankton, and often aggregate near steep rocky reefs in relatively shallow water <55 m deep (Brodeur et al., 1987, Love, 2011, Love et al., 2002, Pirtle et al., 2012, Rosenthal, 1983). Kelp greenling are benthic generalists that consume sea cucumbers, brittle stars, crabs, amphipods, shrimp, worms, and snails on or near the seafloor (Love, 2011, Moulton, 1977, Rosenthal, 1983). Based on these feeding modes, we anticipated that each species would acquire carbon contributions from both kelp and phytoplankton pathways, but that kelp greenling would derive substantially larger carbon contributions from kelp than black rockfish. Ontogenetic dietary shifts may occur in either species, thus we considered individual fish size. To determine whether pelagic- and benthic-feeding predators consistently use both kelp and phytoplankton pathways, black rockfish and kelp greenling were collected from eight nearshore sites in the northeast Pacific Ocean from California to Alaska, spanning 25 degrees of latitude (∼35 to 60°N) and two large marine ecosystems, the California Current and Gulf of Alaska. The former is a seasonal coastal upwelling system, whereas the latter is predominantly a year-round downwelling system.
Section snippets
Sample collection and stable isotope analysis
A total of 308 black rockfish and 336 kelp greenling were captured at eight subtidal rocky reef sites in the northeast Pacific Ocean: Katmai National Park and Preserve, AK (KATM); western Prince William Sound, AK (WPWS); Elfin Cove, AK (ELFI); Whale Bay, AK (WHAL); Clayoquot Sound, BC (CLAY); Neah Bay, WA (WASH); Monterey Bay, CA (MONT); and Big Sur, CA (BIGS) (Fig. 1; Table 1). Sea otters were present at all sites; predation by otters increases kelp production and species diversity via
Results
The average length of black rockfish (one-way ANOVA, F = 35.7, P < 0.001) and kelp greenling (one-way ANOVA, F = 13.8, P < 0.001) differed among sites (Table 1). Rockfish from BIGS and MONT were the smallest (P < 0.05 for pairwise comparisons with all other sites) and those from ELFI and WPWS were largest (P < 0.05 for all pairwise comparisons except fish from ELFI were not significantly larger than those from KATM or CLAY), while rockfish from other sites were intermediate in mean length.
Discussion
This collection of nearshore fish isotope values provides the first evidence of routine kelp-derived carbon contributions to benthic- and pelagic-feeding nearshore fishes across a wide latitudinal gradient. Kelp forests have been known to benefit fish by providing habitat (Bodkin, 1986, Efird and Konar, 2014, Holbrook et al., 1990, Reisewitz et al., 2006, Siddon et al., 2008), and our data suggests that kelp also provides an important source of primary production for the food webs used by
Conclusions
Overall, the high muscle δ13C values and isotope mixing model results of both kelp greenling and black rockfish strongly suggest that a 13C-enriched carbon source, likely dominated by canopy kelp, contributes substantially to the benthic and pelagic food webs that these species utilize across both coastal upwelling and downwelling systems in the northeast Pacific Ocean. If kelp contributes substantial energy to fishes, it follows that shifts in kelp production could influence fish production in
Acknowledgements
This work is part of the Pacific Nearshore Project supported by the U.S. Geological Survey, Ecosystems Mission Area and the Department of the Interior on the Landscape Initiative to investigate biotic response to environmental variation in nearshore habitats of the northeast Pacific Ocean. We thank the USGS Pacific Nearshore Team for project support, H. Coletti and the National Park Service, M. Murray and the Monterey Bay Aquarium, S. Larson at the Seattle Aquarium, S. Hoobler and the
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