In many coastal marine systems with low productivity, cross-habitat exchange of subsidies has been shown to have significant bottom-up effects. California rhodolith beds (Lithothamnion australe Foslie) support invertebrate communities whose biomass doesn’t appear to be supported by the limited productivity of rhodoliths. Detrital subsidies from the water column and adjacent giant kelp Macrocystis pyrifera forests may supplement the base of the food web in these beds. Stable isotope analyses were conducted using seawater organic matter, sediment organic matter, and macroalgae as endmembers to determine their relative importance to consumers and create trophic structure of a rhodolith bed off Santa Catalina Island. Using cluster analysis on carbon δ13C and nitrogen δ15N values of 13 invertebrate consumer taxa, five trophic groups were identified: planktivore, zooplanktivore, detritivore, herbivore, and carnivore. The isotope ratios of sediment organic matter from within rhodoliths were similar to benthic and drifting kelp M. pyrifera tissue, suggesting neighboring kelp habitats, or other unmeasured sources, may contribute to the organic matter within rhodoliths. Detritivores, herbivores, and carnivores appeared to consume particulate organic matter from the water column directly or indirectly through prey. Follow-up experiments indicated that increasing surface area of giant kelp pieces increased drift rates while smaller kelp material moved less and may have greater potential to be retained within rhodolith beds during periods of increased water motion. Overall, temporal fluctuations in the supply and export of suspended particulate organic matter from the water column and drift macroalgal subsidies from adjacent kelp forests may have considerable effects on secondary production and community structure of rhodolith beds.
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The datasets analyzed during the current study are summarized in Table 1.
Blazewicz-Paszkowycz M, Ligowski R (2002) Diatoms as food source indicator for some Antarctic Cumacea and Tanaidacea (Crustacea). Antarct Sci 14:11–15
Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Syst 42:411–440. https://doi.org/10.1146/annurev-ecolsys-102209-144726
Bond A, Diamond A (2011) Recent bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023
Bouillon S, Connolly RM, Lee SY (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. J Sea Res 59:44–58. https://doi.org/10.1016/j.seares.2007.05.001
Bracken M, Gonzalez-Dorantes C, Stachowicz J (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology 88:2211–2219
Brauns M, Brabender M, Gehre M, Rinke K, Weitere M (2019) Organic matter resources fuelling food webs in a human-modified lowland river: importance of habitat and season. Hydrobiologia 841:121–131. https://doi.org/10.1007/s10750-019-04011-4
Britton-Simmons KH, Rhoades AL, Pacunski RE, Galloway AWE, Lowe AT, Sosik EA, Dethier MN, Duggins DO (2012) Habitat and bathymetry influence the landscape-scale distribution and abundance of drift macrophytes and associated invertebrates. Limnol Oceanogr 57:176–184. https://doi.org/10.4319/lo.2012.57.1.0176
Cox TE, Murray SN (2005) Feeding preferences and the relationships between food choice and assimilation efficiency in the herbivorous marine snail Lithopoma undosum (Turbinidae). Mar Biol 148:1295–1306. https://doi.org/10.1007/s00227-005-0166-3
Davenport S, Bax N (2002) A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can J Fish Aquat Sci 59:514–530. https://doi.org/10.1139/F02-031
Dean TA, Thies K, Lagos SL (2009) Survival of Juvenile Giant kelp: the effects of demographic factors, competitors, and grazers. Ecology 70:483–495
Duggins DO, Simenstad C, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Sci New Ser 245:170–173
Filbee-Dexter K, Scheibling RE (2016) Spatial patterns and predictors of drift algal subsidy in deep subtidal environments. Estuaries Coasts 39:1724–1734. https://doi.org/10.1007/s12237-016-0101-5
Filbee-Dexter K, Wernberg T, Ramirez-Llodra E, Norderhaug KM, Pedersen MF (2018) Movement of pulsed resource subsidies from shallow kelp forests to deep fjords. Oecologia 187:291–304. https://doi.org/10.1007/s00442-018-4121-7
Foster MS (2001) Rhodoliths: between rocks and soft places. J Phycol 37:659–667
Foster MS, McConnico LM, Lundsten L, Wadsworth T, Kimbal T, Brooks LB, Medina-López M, Riosmena-Rodríguez R, Hernández-Carmona G, Vázquez-Elizondo RM, Johnson S, Steller DL (2007) Diversidad e historia natural de una comunidad de Lithothamnion muelleri-Sargassum horridum en el Golfo de California (Diversity and natural history of a Lithothamnion muelleri-Sargassum horridum community in the Gulf of California). Ciencias Mar 33:367–384
Foster MS, Amado Filho GM, Kamenos NA, Riosmena-Rodriguez R, Steller DL (2013) Rhodoliths and rhodolith beds. Smithson Contrib Mar Sci 39:143–155
Fry B (2006) Stable isotope ecology. Springer, New York
Gabara SS (2014) Community structure and energy flow within rhodolith habitats at Santa Catalina Island, CA. In: MSc thesis, San Jose State University, San Jose, CA
Gabara SS, Hamilton SL, Edwards MS, Steller DL (2018) Rhodolith structural loss decreases abundance, diversity, and stability of benthic communities at Santa Catalina Island, CA. Mar Ecol Prog Ser 595:71–88. https://doi.org/10.3354/meps12528
Gagnon P, Matheson K, Stapleton M (2012) Variation in rhodolith morphology and biogenic potential of newly discovered rhodolith beds in Newfoundland and Labrador (Canada). Bot Mar 55:85–99
Galloway AWE, Brett MT, Holtgrieve GW, Ward EJ, Ballantyne AP, Burns CW, Kainz MJ, Müller-Navarra DC, Persson J, Ravet JL, Strandberg U, Taipale SJ, Alhgren G (2015) A fatty acid based bayesian approach for inferring diet in aquatic consumers. PLoS One 10:e0129723. https://doi.org/10.1371/journal.pone.0129723
Gerard V (1976) Some aspects of material dynamics and energy flow in a kelp forest in Monterey Bay, California. Dissertation, University of California Santa Cruz
Gerard V, North W (1984) Measuring growth, production, and yield of the giant kelp Macrocystis pyrifera. Hydrobiologia 116(117):321–324
Graham MH (2004) Effects of local deforestation on the diversity and structure of Southern California giant kelp forest food webs. Ecosystems 7:341–357
Grall J, Leloch F, Guyonnet B, Riera P (2006) Community structure and food web based on stable isotopes (δ15N and δ13C) analysis of a North Eastern Atlantic maerl bed. J Exp Mar Bio Ecol 338:1–15. https://doi.org/10.1016/j.jembe.2006.06.013
Harrold C, Reed DC (1985) Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–1169
Hobson ES, Chess JR (1986) Relationships among fishes and their prey in a nearshore sand community off southern California. Environ Biol Fish 17:201–226. https://doi.org/10.1007/BF00698198
Hobson ES, Chess JR (2001) Influence of trophic relations on form and behavior among fishes and benthic invertebrates in some California marine communities. Environ Biol Fishes 60:411–457
Ince R, Hyndes GA, Lavery PS, Vanderklift MA (2007) Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuar Coast Shelf Sci 74:77–86. https://doi.org/10.1016/j.ecss.2007.03.029
Jaschinski S, Brepohl D, Sommer U (2011) Seasonal variation in carbon sources of mesograzers and small predators in an eelgrass community: stable isotope and fatty acid analyses. Mar Ecol Prog Ser 431:69–82. https://doi.org/10.3354/meps09143
Kaehler S, Pakhomov E, Kalin R, Davis S (2006) Trophic importance of kelp-derived suspended particulate matter in a through-flow sub-Antarctic system. Mar Ecol Prog Ser 316:17–22. https://doi.org/10.3354/meps316017
Kamenos NA, Moore P, Hall-spencer JM (2004) Small-scale distribution of juvenile gadoids in shallow inshore waters; what role does maerl play? ICES J. https://doi.org/10.1016/j.icesjms.2004.02.004
Kelly J, Krumhansl KA, Scheibling R (2012) Drift algal subsidies to sea urchins in low-productivity habitats. Mar Ecol Prog Ser 452:145–157. https://doi.org/10.3354/meps09628
Krumhansl KA, Scheibling R (2012a) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302. https://doi.org/10.3354/meps09940
Krumhansl KA, Scheibling RE (2012b) Detrital subsidy from subtidal kelp beds is altered by the invasive green alga Codium fragile ssp. fragile. Mar Ecol Prog Ser 456:73–85. https://doi.org/10.3354/meps09671
Kurle CM, McWhorter JK (2017) Spatial and temporal variability within marine isoscapes: implications for interpreting stable isotope data from marine systems. Mar Ecol Prog Ser 568:31–45. https://doi.org/10.3354/meps12045
Leclerc J-C, Riera P, Leroux C, Lévêque L, Laurans M, Schaal G, Davoult D (2013) Trophic significance of kelps in kelp communities in Brittany (France) inferred from isotopic comparisons. Mar Biol 160:3249–3258. https://doi.org/10.1007/s00227-013-2306-5
Madigan DJ, Carlisle AB, Dewar H, Snodgrass OE, Litvin SY, Micheli F, Block BA (2012) Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem. Sci Rep 2:654
Mann KH (1988) Production and use of detritus in various freshwater, estuarine and coastal marine ecosystems. Limnol Oceanogr 33:910–930
Martin A (1966) Feeding and digestion in two intertidal gammarids: Marinogammarus obtusatus and M. pirloti. J Zool 148:515–525
Mehner T, Rapp T, Monk CT, Beck ME, Trudeau A, Kiljunen M, Hilt S, Arlinghaus R (2019) Feeding aquatic ecosystems: whole-lake experimentaladdition of angler’s ground bait strongly affects omnivorous fish despite low contribution to lake carbon budget. Ecosystems 22:346–362. https://doi.org/10.1007/s10021-018-0273-x
Millar KR, Gagnon P (2018) Mechanisms of stability of rhodolith beds: sedimentological aspects. Mar Ecol Prog Ser 594:65–83
Miller RJ, Page HM (2012) Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence. Mar Biol 159:1391–1402. https://doi.org/10.1007/s00227-012-1929-2
Miller RJ, Page HM, Brzezinski M (2013) δ13C and δ15N of particulate organic matter in the Santa Barbara channel: drivers and implications for trophic inference. Mar Ecol Prog Ser 474:53–66. https://doi.org/10.3354/meps10098
Moncreiff C, Sullivan M (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 215:93–106. https://doi.org/10.3354/meps215093
Mouillot D, Villéger S, Scherer-Lorenzen M, Mason NWH (2011) Functional structure of biological communities predicts ecosystem multifunctionality. PLoS One 6(3):e17476. https://doi.org/10.1371/journal.pone.0017476
Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotope ecology. Front Ecol Environ 5:429–436. https://doi.org/10.1890/060150.1
Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974
Ouisse V, Riera P, Migné A, Leroux C, Davoult D (2012) Food web analysis in intertidal Zostera marina and Zostera noltii communities in winter and summer. Mar Biol 159:165–175. https://doi.org/10.1007/s00227-011-1796-2
Page HM, Reed D, Brzezinski M, Melack J, Dugan J (2008) Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Mar Ecol Prog Ser 360:47–62. https://doi.org/10.3354/meps07382
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672. https://doi.org/10.1371/journal.pone.0009672
Phillips D (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125. https://doi.org/10.1007/s004420100786
Polis GA, Holt RD, Menge BA, Winemiller KO (1996) Time, space and life history: influences on food webs. In: Food webs: integration of patterns and dynamics, pp 435–460
Polis G, Anderson W, Holt R (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316
Raven JA, Johnston AM, Kubler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378
Rodríguez SR (2003) Consumption of drift kelp by intertidal populations of the sea urchin Tetrapygus niger on the central Chilean coast: possible consequences at different ecological levels. Mar Ecol Prog Ser 251:141–151
Schaal G, Riera P, Leroux CC (2012) Food web structure within kelp holdfasts (Laminaria): a stable isotope study. Mar Ecol 33:370–376. https://doi.org/10.1111/j.1439-0485.2011.00487.x
Semmens BX, Moore JW, Ward EJ (2009) Improving Bayesian isotope mixing models: a response to Jackson et al. (2009). Ecol Lett 12:E6–8. https://doi.org/10.1111/j.1461-0248.2009.01283.x
Steller DL, Riosmena-Rodriguez R, Foster MSM, Roberts CA (2003) Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of disturbance. Aquat Conserv Mar Freshw Ecosyst 13:S5–S20. https://doi.org/10.1002/aqc.564
Stock BC, Jacoson AL, Ward EJ, Parnell AC, Phillips DL, Semmens BX (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ Preprints 6:e26884v1. https://doi.org/10.7287/peerj.preprints.26884v1
Timko PL (1976) Sand dollars as suspension feeders: a new description of feeding in Dendraster excentricus. Biol Bull Mar Biol Lab Woods Hole 151:247–259
Tompkins PA (2011) Distribution, growth, and disturbance of Catalina Island rhodoliths. In: Masters Thesis. Moss Landing Marine Laboratories, San Jose State University
Tompkins PA, Steller DL (2016) Living carbonate habitats in temperate California (USA) waters: distribution, growth, and disturbance of Santa Catalina Island rhodoliths. Mar Ecol Prog Ser 560:135–145. https://doi.org/10.3354/meps11919
Vafeiadou A-M, Materatski P, Adão H, De Troch M, Moens T, Troch M, Moens T (2013) Food sources of macrobenthos in an estuarine seagrass habitat (Zostera noltii) as revealed by dual stable isotope signatures. Mar Biol 160:2517–2523. https://doi.org/10.1007/s00227-013-2238-0
Vanderklift MA, Ponsard S (2003) Sources of variation in a consumer-diet d15N enrichment: a meta-analysis. Oecologia 136:169–182
Vetter EW (1995) Detritus-based patches of high secondary production in the nearshore benthos. Mar Ecol Prog Ser 120:251–262. https://doi.org/10.3354/meps120251
Vetter EW, Dayton PK (1998) Macrofaunal communities within and adjacent to a detritus-rich submarine canyon system. Deep Sea Res Part II Top Stud Oceanogr 45:25–54. https://doi.org/10.1016/S0967-0645(97)00048-9
Vetter EW, Dayton PK (1999) Organic enrichment by macrophyte detritus, and abundance patterns of megafaunal populations in submarine canyons. Mar Ecol Prog Ser 186:137–148. https://doi.org/10.3354/meps186137
Wakefield RL, Murray SN (1998) Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar Biol 130:631–642. https://doi.org/10.1007/s002270050285
Yingst JY (1982) Factors influencing rates of sediment ingestion by Parastichopus parvimensis (Clark), an epibenthic deposit-feeding holothurian. Estuar Coast Shelf Sci 14:119–134
I would like to thank D. Steller, P. Tompkins, S. Hamilton, R. Mehta, J. Redwine, M. Marraffini, M. Fox, A. Muth, K. Meagher Robinson, E. Robinson, B. Higgins, D. van Hees, K. van Hees, I. Moffit, K. Kopecky, S. Sampson, A. Macleod, and A. Olson for field help. I also thank M. Graham, S. Hamilton, and D. Steller for advice and comments during the development and completion of this work. I would also like to thank T. Oudin, L. Oudin, and K. Spafford at the USC Wrigley Institute for Environmental Studies. I thank Dr. Patrick Gagnon and four anonymous reviewers for their time and constructive feedback that improved this manuscript.
This work was funded by The American Academy of Underwater Sciences (AAUS) Kevin Gurr Scholarship Award, Moss Landing Marine Laboratories (MLML) Signe Lundstrom Memorial Scholarship, MLML Wave Award, Council on Ocean Affairs, Science & Technology (COAST) Student Award for Marine Science Research, David and Lucile Packard Foundation Award, and the Dr. Earl H. Myers and Ethel M. Myers Oceanographic and Marine Biology Trust.
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Gabara, S.S. Trophic structure and potential carbon and nitrogen flow of a rhodolith bed at Santa Catalina Island inferred from stable isotopes. Mar Biol 167, 30 (2020). https://doi.org/10.1007/s00227-019-3635-9