Abstract
Resource subsidies in the form of allochthonous primary production drive secondary production in many ecosystems, often sustaining diversity and overall productivity. Despite their importance in structuring marine communities, there is little understanding of how subsidies move through juxtaposed habitats and into recipient communities. We investigated the transport of detritus from kelp forests to a deep Arctic fjord (northern Norway). We quantified the seasonal abundance and size structure of kelp detritus in shallow subtidal (0‒12 m), deep subtidal (12‒85 m), and deep fjord (400‒450 m) habitats using a combination of camera surveys, dive observations, and detritus collections over 1 year. Detritus formed dense accumulations in habitats adjacent to kelp forests, and the timing of depositions coincided with the discrete loss of whole kelp blades during spring. We tracked these blades through the deep subtidal and into the deep fjord, and showed they act as a short-term resource pulse transported over several weeks. In deep subtidal regions, detritus consisted mostly of fragments and its depth distribution was similar across seasons (50% of total observations). Tagged pieces of detritus moved slowly out of kelp forests (displaced 4‒50 m (mean 11.8 m ± 8.5 SD) in 11‒17 days, based on minimum estimates from recovered pieces), and most (75%) variability in the rate of export was related to wave exposure and substrate. Tight resource coupling between kelp forests and deep fjords indicate that changes in kelp abundance would propagate through to deep fjord ecosystems, with likely consequences for the ecosystem functioning and services they provide.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Armstrong JB, Bond MH (2013) Phenotype flexibility in wild fish: Dolly Varden regulate assimilative capacity to capitalize on annual pulsed subsidies. J Anim Ecol 82:966–975. https://doi.org/10.1111/1365-2656.12066
Barrón C, Apostolaki ET, Duarte CM (2014) Dissolved organic carbon fluxes by seagrass meadows and macroalgal beds. Front Mar Sci 1:42. https://doi.org/10.3389/fmars.2014.00042
Bernardino AF, Smith CR, Baco A et al (2010) Macrofaunal succession in sediments around kelp and wood falls in the deep NE Pacific and community overlap with other reducing habitats. Deep Sea Res Part I Oceanogr Res Pap 57:708–723. https://doi.org/10.1016/J.DSR.2010.03.004
Billett DSM, Lampitt RS, Rice AL, Mantoura RFC (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302:520–522. https://doi.org/10.1038/302520a0
Billett DS, Betta B, Rice A et al (2001) Long-term change in the megabenthos of the Porcupine Abyssal Plain (NE Atlantic). Prog Oceanogr 50:325–348. https://doi.org/10.1016/S0079-6611(01)00060-X
Bishop MJ, Coleman MA, Kelaher BP (2010) Cross-habitat impacts of species decline: response of estuarine sediment communities to changing detrital resources. Oecologia 163:517–525. https://doi.org/10.1007/s00442-009-1555-y
Bode A, Botas JA, Fernández E (1997) Nitrate storage by phytoplankton in a coastal upwelling environment. Mar Biol 129:399–406. https://doi.org/10.1007/s002270050180
Bologna PAX, Fetzer ML, McDonnell S, Moody EM (2005) Assessing the potential benthic–pelagic coupling in episodic blue mussel (Mytilus edulis) settlement events within eelgrass (Zostera marina) communities. J Exp Mar Biol Ecol 316:117–131. https://doi.org/10.1016/J.JEMBE.2004.10.009
Breiman L (2001) Random forests. Mach Learn 45:5–32. https://doi.org/10.1023/A:1010933404324
Breiman L, Cutler A (2015) Breiman and Cutler’s random forests for classification and regression based on a forest of trees using random inputs. https://www.stat.berkeley.edu/~breiman/RandomForests/. Accessed 22 Feb 2018
Britton-Simmons KH, Rhoades AL, Pacunski RE et al (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
Bustamante RH, Branch GM, Eekhout S (1995) Maintenance of an exceptional intertidal grazer biomass in South Africa: subsidy by subtidal kelps. Ecology 76:2314–2329. https://doi.org/10.2307/1941704
Costanza R, Fisher B, Mulder K et al (2006) Biodiversity and ecosystem services: a multi-scale empirical study of the relationship between species richness and net primary production. Ecol Econ 61:478–491. https://doi.org/10.1016/j.ecolecon.2006.03.021
de Bettignies T, Wernberg T, Lavery PS et al (2013) Contrasting mechanisms of dislodgement and erosion contribute to production of kelp detritus. Limnol Oceanogr 58:1680–1688. https://doi.org/10.4319/lo.2013.58.5.1680
Dethier MN, Brown AS, Burgess S et al (2014) Degrading detritus: changes in food quality of aging kelp tissue varies with species. J Exp Mar Biol Ecol 460:72–79. https://doi.org/10.1016/j.jembe.2014.06.010
Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283
Enríquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N: P content. Oecologia 94:457–471. https://doi.org/10.1007/BF00566960
Evans SN, Abdo DA (2010) A cost-effective technique for measuring relative water movement for studies of benthic organisms. Mar Freshw Res 61:1327. https://doi.org/10.1071/MF10007
Fagerli CW, Norderhaug KM, Christie HC (2013) Lack of sea urchin settlement may explain kelp forest recovery in overgrazed areas in Norway. Mar Ecol Prog Ser 488:119–132
Fagerli CW, Norderhaug KM, Christie H, Pedersen MF, Fredriksen S (2014) Predators of the destructive sea urchin Strongylocentrotus droebachiensis on the Norwegian coast. Mar Ecol Prog Ser 502:207–218
Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281:200–207. https://doi.org/10.1126/SCIENCE.281.5374.200
Figurski JD, Malone D, Lacy JR, Denny M (2011) An inexpensive instrument for measuring wave exposure and water velocity. Limnol Oceanogr Methods 9:204–214. https://doi.org/10.4319/lom.2011.9.204
Filbee-Dexter K, Scheibling RE (2012) Hurricane-mediated defoliation of kelp beds and pulsed delivery of kelp detritus to offshore sedimentary habitats. Mar Ecol Prog Ser 455:51–64. https://doi.org/10.3354/meps09667
Filbee-Dexter K, Scheibling RE (2014) Detrital kelp subsidy supports high reproductive condition of deep-living sea urchins in a sedimentary basin. Aquat Biol 23:71–86. https://doi.org/10.3354/ab00607
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, Scheibling RE (2017) The present is the key to the past: linking regime shifts in kelp beds to the distribution of deep-living sea urchins. Ecology 98:253–264. https://doi.org/10.1002/ecy.1638
Gage JD (2003) Food inputs, utilization, carbon flow and energetics. In: Tyler PA (ed) Ecosystems of the deep oceans. Elsevier, Oxford, p 313
Gattuso J-P, Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst 29:405–434. https://doi.org/10.1146/annurev.ecolsys.29.1.405
Gattuso J-P, Gentili B, Duarte CM et al (2006) Light availability in the coastal ocean: impact on the distribution of benthic photosynthetic organisms and contribution to primary production. Biogeosciences 3:489–513. https://doi.org/10.5194/bg-3-489-2006
Harrold C, Light K, Lisin S (1998) Organic enrichment of submarine-canyon and continental-shelf benthic communities by macroalgal drift imported from nearshore kelp forests. Limnol Oceanogr 43:669–678. https://doi.org/10.4319/lo.1998.43.4.0669
Heck KL, Carruthers TJB, Duarte CM et al (2008) Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11:1198–1210. https://doi.org/10.1007/s10021-008-9155-y
Hobday AJ (2000) Persistence and transport of fauna on drifting kelp (Macrocystis pyrifera (L.) C. Agardh) rafts in the Southern California Bight. J Exp Mar Biol Ecol 253:75–96. https://doi.org/10.1016/S0022-0981(00)00250-1
Hoover RS, Hoover D, Miller M et al (2006) Zooplankton response to storm runoff in a tropical estuary: bottom-up and top-down controls. Mar Ecol Prog Ser 318:187–201
Kim S (1992) The role of drift kelp in the population ecology of a Diopatra ornata Moore (Polychaeta: Onuphidae) ecotone. J Exp Mar Biol Ecol 156:253–272. https://doi.org/10.1016/0022-0981(92)90250-E
Krause-Jensen D, Duarte CM (2016) Substantial role of macroalgae in marine carbon sequestration. Nat Geosci 9:737–742. https://doi.org/10.1038/ngeo2790
Krumhansl K, Scheibling R (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302. https://doi.org/10.3354/meps09940
Krumhansl KA, Okamoto DK, Rassweiler A et al (2016) Global patterns of kelp forest change over the past half-century. Proc Natl Acad Sci 113:13785–13790. https://doi.org/10.1073/pnas.1606102113
Mann K (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981. https://doi.org/10.1126/science.155.3758.81
Marczak LB, Thompson RM, Richardson JS (2007) Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–148. https://doi.org/10.1890/0012-9658(2007)88[140:MTLHAP]2.0.CO;2
Matthews JBL, Heimdal BR (1980) Pelagic productivity and food chains in fjord systems. In: Farmer DM, Levings CD (eds) Fjord Oceanography. Springer, Boston
Mcleod E, Chmura GL, Bouillon S et al (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO 2. Front Ecol Environ 9:552–560. https://doi.org/10.1890/110004
Moy FE, Christie H (2012) Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar Biol Res 8:309–321. https://doi.org/10.1080/17451000.2011.637561
Nielsen SL, Banta GT, Pedersen MF (2004) Decomposition of marine primary producers: Consequences for nutrient recycling and retention in coastal ecosystems. In: Banta G, Pedersen M, Nielsen S (eds) Estuarine nutrient cycling: the influence of primary producers. Springer, Dordrecht, pp 187–216
Norderhaug KM, Christie H (2011) Secondary production in a Laminaria hyperborea kelp forest and variation according to wave exposure. Estuar Coast Shelf Sci 95:135–144. https://doi.org/10.1016/J.ECSS.2011.08.028
Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237. https://doi.org/10.1016/S0169-5347(00)01862-0
Pauly D, Christensen V (1995) Primary production required to sustain global fisheries. Nature 374:255–257
Platt T, Harrison WG, Lewis MR et al (1989) Biological production of the oceans: the case for a consensus. Mar Ecol Prog Ser 52:77–88
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology. Annu Rev Ecol Syst 28:289–316. https://doi.org/10.1146/annurev.ecolsys.28.1.289
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Ramirez-Llodra E, Brandt A, Danovaro R et al (2010) Deep, diverse and definitely different: unique attributes of the world’s largest ecosystem. Biogeosciences 7:2851–2899. https://doi.org/10.5194/bg-7-2851-2010
Ramirez-Llodra E, Rinde E, Gundersen H et al (2016) A snap shot of the short-term response of crustaceans to macrophyte detritus in the deep Oslofjord. Sci Rep 6:23800. https://doi.org/10.1038/srep23800
Renaud PE, Løkken TS, Jørgensen LL et al (2015) Macroalgal detritus and food-web subsidies along an Arctic fjord depth-gradient. Front Mar Sci 2:31. https://doi.org/10.3389/fmars.2015.00031
Rowe L, Richardson JS (2001) Community responses to experimental food depletion: resource tracking by stream invertebrates. Oecologia 129:473–480. https://doi.org/10.1007/s004420100748
Sato T, El-Sabaawi RW, Campbell K et al (2016) A test of the effects of timing of a pulsed resource subsidy on stream ecosystems. J Anim Ecol 85:1136–1146. https://doi.org/10.1111/1365-2656.12516
Sauchyn L, Scheibling R (2009) Degradation of sea urchin feces in a rocky subtidal ecosystem: implications for nutrient cycling and energy flow. Aquat Biol 6:99–108. https://doi.org/10.3354/ab00171
Silver P, Wooster D, Palmer MA (2004) Chironomid responses to spatially structured, dynamic, streambed landscapes. J North Am Benthol Soc 23:69–77. https://doi.org/10.1899/0887-3593(2004)023<0069:CRTSSD>2.0.CO;2
Smith BD, Foreman RE (1984) An assessment of seaweed decomposition within a southern Strait of Georgia seaweed community. Mar Biol 84:197–205. https://doi.org/10.1007/BF00393005
Smith KL, Kaufmann RS, Baldwin RJ (1994) Coupling of near-bottom pelagic and benthic processes at abyssal depths in the eastern North Pacific Ocean. Limnol Oceanogr 39:1101–1118. https://doi.org/10.4319/lo.1994.39.5.1101
Smith KLJ, Baldwin RJ, Ruhl HA et al (2006) Climate effect on food supply to depths greater than 4000 meters in the northeast Pacific. Limnol Oceanogr 51:166–176. https://doi.org/10.4319/lo.2006.51.1.0166
Smith CR, De Leo FC, Bernardino AF et al (2008) Abyssal food limitation, ecosystem structure and climate change. Trends Ecol Evol 23:518–528. https://doi.org/10.1016/J.TREE.2008.05.002
Sweetman AK, Chapman A (2011) First observations of jelly-falls at the seafloor in a deep-sea fjord. Deep Sea Res Part I Oceanogr Res Pap 58:1206–1211. https://doi.org/10.1016/J.DSR.2011.08.006
Vanderklift MA, Wernberg T (2008) Detached kelps from distant sources are a food subsidy for sea urchins. Oecologia 157:327–335. https://doi.org/10.1007/s00442-008-1061-7
Vetter EW (1995) Detritus-based patches of high secondary production in the nearshore benthos. Mar Ecol Prog Ser 120:251–262
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
Wallace JB, Eggert SL, Meyer JL, Webster JR (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 102(80):102–104. https://doi.org/10.1126/science.277.5322.102
Wernberg T, Vanderklift MA, How J, Lavery PS (2006) Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 147:692–701. https://doi.org/10.1007/s00442-005-0318-7
Wilmers CC, Estes JA, Edwards M et al (2012) Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests. Front Ecol Environ 10:409–415. https://doi.org/10.1890/110176
Wolff T (1979) Magrofaunal utilization of plant remains in the deep sea. Sarsia 64:117–143. https://doi.org/10.1080/00364827.1979.10411373
Yang LH, Bastow JL, Spence KO, Wright AN (2008) What can we learn from resource pulses. Ecology 89:621–634. https://doi.org/10.1890/07-0175.1
Yang LH, Edwards KF, Byrnes JE et al (2010) A meta-analysis of resource pulse–consumer interactions. Ecol Monogr 80:125–151
Yeager CLJ, Harding LW, Mallonee ME (2005) Phytoplankton production, biomass and community structure following a summer nutrient pulse in Chesapeake Bay. Aquat Ecol 39:135–149. https://doi.org/10.1007/s10452-004-4767-6
Acknowledgements
This work was funded by the Norwegian Research Council through the KELPEX project (NRC Grant no. 255085/E40). In addition, TW received funding from The Australian Research Council (DP170100023). We are grateful for assistance in the field from Stein Fredriksen, Camilla With Fagerli, Nicolai Lond Frisk, Malte Jarlgaard Hansen, and Sabine Popp. The comments of the editor and two reviewers greatly help improve the original manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Robert O. Hall.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Filbee-Dexter, K., Wernberg, T., Norderhaug, K.M. et al. Movement of pulsed resource subsidies from kelp forests to deep fjords. Oecologia 187, 291–304 (2018). https://doi.org/10.1007/s00442-018-4121-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4121-7