A new perspective on the importance of marine-derived nutrients to threatened stocks of Pacific salmon (Oncorhynchus spp.)

A new perspective on the importance of marine-derived nutrients to threatened stocks of Pacific salmon (Oncorhynchus spp.)
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  See discussions, stats, and author profiles for this publication at: A new perspective on the importance of marine-derived nutrients to threatened stocks of Pacificsalmon (Oncorhynchus...  Article   in  Canadian Journal of Fisheries and Aquatic Sciences · April 2011 DOI: 10.1139/f05-113 CITATIONS 47 READS 128 5 authors , including: Some of the authors of this publication are also working on these related projects: Estimating Common Growth Patterns in Juvenile Chinook Salmon (Oncorhynchus tshawytscha) fromDiverse Genetic Stocks and a Large Spatial Extent   View projectEvaluating Indicators of Human Wellbeing for Ecosystem-Based Management   View projectMark D ScheuerellNational Oceanic and Atmospheric Administrat… 75   PUBLICATIONS   2,340   CITATIONS   SEE PROFILE Phillip LevinNorthwest Fisheries Science Center 176   PUBLICATIONS   4,333   CITATIONS   SEE PROFILE Beth L. SandersonNational Oceanic and Atmospheric Administrat… 27   PUBLICATIONS   811   CITATIONS   SEE PROFILE All content following this page was uploaded by Beth L. Sanderson on 04 January 2017. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the srcinal documentand are linked to publications on ResearchGate, letting you access and read them immediately.  RAPID COMMUNICATION / COMMUNICATION RAPIDE  A new perspective on the importance of marine-derived nutrients to threatened stocks of Pacificsalmon (  Oncorhynchus  spp.) Mark D. Scheuerell, Phillip S. Levin, Richard W. Zabel, John G. Williams, andBeth L. Sanderson Abstract:  Considerable research has highlighted the important role of anadromous salmon in importing marine-derivednutrients to freshwater and riparian ecosystems. These subsidies are thought to support diverse food webs and increasethe growth and survival of juvenile salmon during their freshwater residency. Quite recently, however, salmon smoltshave been identified as important exporters of nutrients from freshwater ecosystems. Using a mass-balance approach,we examined the phosphorus-transport dynamics by spring/summer Chinook salmon ( Oncorhynchus tshawytscha ) in theSnake River basin and estimated that net phosphorus transport into the basin over the past 40 years was <2% of histor-ical levels. Furthermore, a nonlinear relationship existed between nutrient import by adults and subsequent export bysmolts, such that smolts exported proportionally more phosphorus as spawner abundance decreased. In 12% of years,smolts exported more than adults imported, resulting in a net loss of phosphorus from the ecosystem. This loss of marine subsidies may have caused a state shift in the productivity of the freshwater ecosystem, resulting in strongdensity-dependent survival observed in juvenile salmon. These results suggest that conserving this threatened stock of salmon requires the need to explicitly address the important role of marine-derived nutrients and energy in sustainingsalmon populations. Résumé :  De nombreux travaux ont démontré le rôle significatif des saumons anadromes dans le transport des nutri-ments d’srcine marine vers les écosystèmes d’eau douce et les écosystèmes de rivage. On croit que ces apports ali-mentent divers réseaux trophiques et favorisent la croissance et la survie des jeunes saumons durant leur séjour en eaudouce. Tout à fait récemment, cependant, il a été démontré que les saumoneaux exportent d’importantes quantités denutriments hors des écosystèmes d’eau douce. L’établissement de bilans massiques nous a permis d’étudier la dyna-mique du transport du phosphore par les saumons quinnat ( Oncorhynchus tshawytscha ) de printemps et d’été dans lebassin versant de la rivière Snake; le transport net de phosphore vers le bassin au cours des 40 dernières années est<2 % des quantités du passé. De plus, il existe une relation non linéaire entre l’importation des nutriments par lesadultes et l’exportation subséquente par les saumoneaux : les saumoneaux exportent en proportion plus de phosphore àmesure que l’abondance des reproducteurs diminue. Dans 12 % des années, les saumoneaux exportent plus que lesadultes n’importent, ce qui entraîne une perte nette de phosphore dans l’écosystème. Cette perte des apports marinspeut avoir causé une modification du niveau de productivité de l’écosystème d’eau douce, ce qui explique que la survieobservée chez les jeunes saumons est fortement reliée à la densité. Nos résultats indiquent qu’il faut tenir compte defaçon particulière du rôle significatif des nutriments et de l’énergie d’srcine marine dans le maintien des populationsde saumons, si l’on veut conserver ce stock menacé de saumons.[Traduit par la Rédaction]  Scheuerell et al. 964 Introduction The century-long decline of Pacific salmon in the Colum-bia River Basin is well documented, and because of theenormous economic, social, and ecological value that soci-ety places on salmon, the “salmon problem” now representsone of the United States’ most contentious environmental is-sues (Ruckelshaus et al. 2002). In the Snake River, the larg- Can. J. Fish. Aquat. Sci.  62 : 961–964 (2005) doi: 10.1139/F05-113 © 2005 NRC Canada 961 Received 15 April 2005. Accepted 20 April 2005. Published on the NRC Research Press Web site at on13 May 2005.J18655 M.D. Scheuerell, 1 P.S. Levin, R.W. Zabel, J.G. Williams, and B.L. Sanderson.  National Marine Fisheries Service,Northwest Fisheries Science Center, 2725 Montlake Boulevard East, Seattle, WA 98112, USA. 1 Corresponding author (e-mail:  est tributary to the Columbia River, wild populations of spring/summer Chinook salmon ( Oncorhynchus tshawytscha )fell dramatically from the 1960s through the 1990s, resultingin their listing under the US Endangered Species Act. Habi-tat degradation, overharvest, hydroelectric dams, hatcheryproduction, interactions with exotic species, and shifts inocean-climate conditions have all contributed to their demise(Ruckelshaus et al. 2002). No matter what the ultimate causeof their downfall, another more subtle problem emerges fromthis large drop in salmon abundance: freshwater spawningand rearing habitat has experienced a massive decrease inmarine-derived nutrients (Gresh et al. 2000).Anadromous salmon play an integral role on their returnto freshwater ecosystems because they accumulate >95% of their biomass in the ocean, which results in the import of substantial marine-derived nutrients into the relativelynutrient-poor streams and lakes (Schindler et al. 2003). Nu-trient enrichment from decomposing carcasses leads to in-creased production of benthic algae and macroinvertebrates,which indirectly enhances salmon food resources (Wipfli etal. 2003). Salmon eggs and carcasses also serve as a directfood source for macroinvertebrates and fishes, and juvenilesalmonids show increased growth in streams with additionalsalmon resources (Bilby et al. 1998; Wipfli et al. 2003). This implies a positive feedback loop, such that increasing num-bers of returning adult salmon contribute more marine-derived nutrients to freshwater systems, thereby leading tobetter juvenile growth and survival and subsequently largerpopulation sizes (Wipfli et al. 2003).Recent investigations aimed at understanding the causesand consequences of juvenile mortality in wild Snake Riverspring/summer Chinook salmon suggest that the large de-cline in marine-derived nutrients over the past century limitsthe survival of juveniles (Achord et al. 2003; Zabel et al.2005). While the import of nutrients by adult salmon has po-tentially large value to freshwater ecosystems, recent work by Moore and Schindler (2004) on Alaska sockeye salmon( O. nerka ) stocks highlighted the importance of nutrient ex-port by salmon smolts as they migrate to sea. They hypothe-sized that depending on the strength of density dependence,at low spawning densities smolts could theoretically exportmore nutrients than their parents import to freshwater eco-systems. Here we estimated changes in net transport of marine-derived nutrients into the Snake River basin over thelast 40 years compared with historical periods to determinehow they might have influenced the threatened wild stock of Snake River spring/summer Chinook salmon. We hypothe-sized that a large reduction in marine-derived nutrients couldhave caused the strong density-dependent survival observedamong juveniles and resulted in a state shift in the produc-tivity of the freshwater ecosystem. Methods Following Moore and Schindler (2004), the annual import(  I  ) of phosphorus by adult salmon into freshwater in year  t   is  I A m p t t  = ⋅ ⋅ A A while the annual export (  E  ) of phosphorus by salmon smoltsto the ocean in year  t   is  E S m p t t  = ⋅ ⋅ S S where  A t   is the total number of adult spawners in year  t  ,  S  t   isthe total number of smolts going to sea in year  t  ,  m  repre-sents the mean mass of an individual adult ( m A ) or smolt( m S ), and  p  represents the proportion of phosphorus in thebody of adults (  p A ) or smolts (  p S ). Our spawner data from1962–1999 came from Petrosky et al. (2001) and includedan average 9.2% of hatchery adults that were released tospawn in the wild. For 2000–2004 we used spawner esti-mates from Scheuerell and Williams (2005), which did notinclude any additional hatchery adults. We used the numberof wild smolts recorded at the uppermost dam on the SnakeRiver from brood years 1962–1984 and 1990–2002 (for de-tails see Scheuerell and Williams 2005). We did not includeany hatchery smolts in our calculations because their foodcomes from outside the basin, making their nutrient exportirrelevant for our purposes. We used 5.5 kg as the meanmass of adult Chinook salmon from the Snake River basin(Peery et al. 2003) and 12 g for the mean mass of smolts(Doug Marsh, Northwest Fisheries Science Center, NationalMarine Fisheries Service, 2725 Montlake Boulevard East,Seattle, WA 98112, USA, unpublished data). Following Mooreand Schindler (2004), we assumed that the mass-specificconcentrations of phosphorus were 0.38% and 0.43% foradults and smolts, respectively. These concentrations mayvary somewhat but are assumed to be broadly applicable(Moore and Schindler 2004) and would only influence ourresults slightly. We concentrated on phosphorus because of its importance in limiting primary productivity in freshwaterecosystems, but similar results could be shown for nitrogenby applying the respective nitrogen-to-phosphorus ratios fromthe literature (sensu Moore and Schindler 2004).We fit a Beverton-Holt stock–recruit relationship to thephosphorus imported by the adults (stock) in year  t   andthose exported by their smolts (recruits) 2 years later. Thisrelationship takes the form  E  a I b I  t t t  +  =⋅+ 2 where the export (  E  ) of phosphorus by smolts is a nonlinearfunction of the nutrients imported (  I  ) by their parents. We fitthe parameters by minimizing the negative log-likelihood of the model and assuming log-normally distributed errors. Wealso calculated the percentage of imported adult phosphorusthat smolts export for the same brood years (  E  t  +2  /   I  t  ).The mass-balance approach that we used to estimate netimports of marine-derived nutrients delivered to the SnakeRiver basin was based on calendar years. We used this basisrather than brood years because of the strong seasonal dy-namics in biogeochemical cycles driven by abiotic factorssuch as temperature, precipitation, and irradiance. The an-nual net flow ( F  ) of phosphorus into freshwater in year  t  simply becomes F I E  t t t  = − where  I  t   and  E  t   are the import and export of phosphorus, re-spectively, as described above. When  F  t   is positive, there is anet import of nutrients into the freshwater ecosystem in agiven year, but when  F  t   is negative, smolts actually export © 2005 NRC Canada 962 Can. J. Fish. Aquat. Sci. Vol. 62, 2005  more nutrients than adults bring back. For these calculations,we also included adult return data from 2003 and 2004. Results and discussion We found a strong relationship between the amount of phosphorus imported by adult Chinook salmon and that ex-ported by their offspring (  R 2 = 0.74,  a  = 207,  b  = 537;Fig. 1 a ). Across the entire data set examined, adult Chinook salmon imported 456 ± 322 kg phosphorus·year –1 (mean ± 1standard deviation, SD), whereas smolts exported 86 ± 49 kgphosphorus·year –1 . Using a historical estimate of 1.1 × 10 6 spawners (Peery et al. 2003) at an average weight of 8 kg(Gresh et al. 2000), adult Chinook would have imported33 440 kg phosphorus·year –1 into the Snake River basin,more than 70 times the current estimate. In addition, if weassume a historical smolt-to-adult survival rate of 4.6% (themaximum over the past 40 years) and a individual mass of 18 g (1.5 times the current mass), smolts would have ex-ported 1851 kg phosphorus·year –1 , more than 20 times theamount of phosphorous currently exported by smolts.As the number of spawners decreased, smolts subsequentlyexported a greater percentage of the phosphorus that theirparents imported into basin (Fig. 1 b ). On average, smolts ex-ported 24 ± 10% of the phosphorus imported by adults sincethe early 1960s. This was significantly higher than our his-torical estimate of 5.5% based on the calculations above ( t   =10.4, df = 33,  P  < 0.0001) or the overall average 16% forBristol Bay sockeye salmon ( t   = 4.52, df = 33,  P  < 0.0001)reported by Moore and Schindler (2004). Furthermore, if weadjust their estimates to account for the 67% average harvestrate on adults, average phosphorus export by Bristol Baysmolts would also drop to near 5%.We found a sharp decline in net transport of phosphorusfrom the early 1960s to the early 1980s (Fig. 2) correspond-ing to the large reduction in the size of adult salmon runsduring that time. This downturn in phosphorous transportwas followed by low and relatively constant transport throughthe 1990s, until an upswing began around 2000. Importantly,our calculations reveal that in 1980, 1994, 1995, and 1999,Chinook smolts actually exported more phosphorus thanadults imported in those years (Fig. 2), resulting in a net ex-port of nutrients from the system. Earlier research indicatedthat a major reduction in marine-derived nutrients deliveredto the freshwater and surrounding riparian ecosystems co-incided with dramatic declines in returns of adult salmon tothe Columbia River basin over the last century (Gresh et al.2000), but our findings based on the mass-balance approachof  Moore and Schindler (2004) suggest that the situation isworse than previously thought for the Snake River basin —in some years, the input of nutrients was reduced to thepoint that nutrient exports actually exceeded imports.Two lines of evidence suggest that marine-derived nutri-ents are important for supporting productive freshwater eco-systems in this region. First, Achord et al. (2003) foundcompensatory mortality in Chinook juveniles even thoughpopulations were far below historic levels, and they hypothe-sized that the large loss of marine-derived nutrients in theSnake River basin had lowered carrying capacity. As the © 2005 NRC Canada Scheuerell et al. 963 Fig. 1.  ( a ) Nutrient import–export (stock–recruit) relationship of phosphorus transport by spring/summer Chinook salmon ( Onco-rhynchus tshawytscha ) based on brood years 1962–1982 and1990–2002 and ( b ) the percent of the adult nutrients that smoltsexport for the same brood years. Similar relationships exist fornitrogen but vary by a factor of 7.9 for adults and 5.7 forsmolts, their respective N:P ratios (for details see Moore andSchindler 2004). Fig. 2.  Net phosphorus transport by spring/summer Chinook salmon ( Oncorhynchus tshawytscha ) over time. In years whennet transport is negative, smolts export more phosphorus to theocean than adults import to the freshwater ecosystem.  number of returning adults declined during the 1980s and1990s, the percent of marine-derived nutrients exported bysmolts increased (Fig. 1), with a subsequent decrease in theoverall transport of phosphorus to fresh waters (Fig. 2), pos-sibly creating the negative feedback loop postulated by Achordet al. (2003). Second, following a shift toward improvedocean conditions in 1999, the number of spawning adultsdestined for the Snake River basin increased (Scheuerell andWilliams 2005), with a subsequent increase in the net trans-port of marine-derived nutrients (Fig. 2). However, the num-ber of smolts per spawner produced in the 2001 and 2002brood years was 33 and 55, respectively (John G. Williams,unpublished data), significantly lower than the average 69 ±24 smolts per spawner produced during the previous period(1962–1977) of good ocean conditions and relatively highnutrient transport (2001,  t   = 6.05, df = 15,  P  < 0.0001; 2002, t   = 2.32, df = 15,  P  < 0.05). This raises the possibility thatthe freshwater ecosystem has shifted to a less productivestate (sensu Scheffer and Carpenter 2003).Our results clearly have important implications for the re-covery of threatened Snake River Chinook salmon. Recentpopulation viability analyses of Snake River spring/summerChinook salmon found that increasing juvenile productivitycould lead to large increases in overall population size andthat overall declines in marine-derived nutrients almost cer-tainly contributed to the currently low productivity (Zabel etal. 2005). While the direct impacts of habitat degradation,harvest, hydroelectric dams, and hatchery production allcontributed to the observed declines in salmon populationsthroughout this region, their indirect effects on the amountof marine-derived nutrients and energy delivered to theseecosystems also exacerbated the problem (Ruckelshaus et al.2002). Can the recent high returns of adults to the basin re-store the century-long depletion of marine-derived nutrientsand increase overall productivity of the freshwater ecosys-tem? Certainly shifts in ocean-climate conditions and theirsubsequent impacts on salmon survival occur over time, andwe cannot predict how long the currently favorable oceanconditions will last (Scheuerell and Williams (2005) and ref-erences therein). Therefore, it remains to be seen how theecosystem will respond before the Northeast Pacific switchesonce again to a less productive regime for Columbia Riversalmon.Much of the discussion related to habitat restoration forthreatened and endangered salmon concentrates on thesmall-scale physical aspects of habitat (e.g., adequate stream-flow, spawning gravel, large woody debris) or the large-scaleprocesses (e.g., agricultural land use, road density) that alterthose habitat features (Ruckelshaus et al. 2002). Neverthe-less, carrying capacity for Pacific salmon depends funda-mentally on properly functioning biogeochemical cycles anddiverse food webs that are strongly influenced by marine-derived nutrients and energy (Schindler et al. 2003). Thus,while the amount and quality of habitat may limit populationsize, our results indicate that levels and dynamics of nutri-ents may also be crucial. This means that an ecosystemapproach to management requires “ecologically defensiblerecovery goals” (sensu Peery et al. 2003) that take into con-sideration the important role of anadromous salmon in main-taining healthy freshwater and riparian ecosystems.  Acknowledgements Comments by Jon Moore, Daniel Schindler, Jim Helfield,and an anonymous reviewer helped to improve the manu-script. We also thank the numerous personnel who assistedwith data collection over the past 43 years. The views ex-pressed herein are those of the authors and do not necessar-ily reflect those of the National Oceanic and AtmosphericAdministration or its agencies. References Achord, S., Levin, P.S., and Zabel, R.W. 2003. Density-dependentmortality in Pacific salmon: the ghost of impacts past? Ecol.Lett.  6 : 335–342.Bilby, R.E., Fransen, B.R., Bisson, P.A., and Walter, J.K. 1998. Re-sponse of juvenile coho salmon ( Oncorhynchus kisutch ) andsteelhead ( Oncorhynchus mykiss ) to the addition of salmon car-casses to two streams in southwestern Washington, U.S.A. Can.J. Fish. Aquat. Sci.  55 : 1909–1918.Gresh, T., Lichatowich, J., and Schoonmaker, P. 2000. An estimationof historic and current levels of salmon production in the North-east Pacific ecosystem: evidence of a nutrient deficit in the fresh-water systems of the Pacific Northwest. Fisheries,  25 : 15–21.Moore, J.W., and Schindler, D.E. 2004. Nutrient export from fresh-water ecosystems by anadromous sockeye salmon ( Oncorhynchusnerka ). Can. J. Fish. Aquat. Sci.  61 : 1582–1589.Peery, C.A., Kavanagh, K.L., and Scott, J.M. 2003. Pacific salmon:setting ecologically defensible recovery goals. BioScience,  53 :622–623.Petrosky, C.E., Schaller, H.A., and Budy, P. 2001. Productivity andsurvival rate trends in the freshwater spawning and rearing stageof Snake River chinook salmon ( Oncorhynchus tshawytscha ).Can. J. Fish. Aquat. Sci.  58 : 1196–1207.Ruckelshaus, M.H., Levin, P., Johnson, J.B., and Kareiva, P.M. 2002.The Pacific salmon wars: what science brings to the challenge of recovering species. Annu. Rev. Ecol. Syst.  33 : 665–706.Scheffer, M., and Carpenter, S.R. 2003. Catastrophic regime shiftsin ecosystems: linking theory to observation. Trends Ecol. Evol. 18 : 648–656.Scheuerell, M.D., and Williams, J.G. 2005. Forecasting climate-induced changes in the survival of Snake River spring/summerChinook salmon. Fish. Oceanogr.  14 . In press.Schindler, D.E., Scheuerell, M.D., Moore, J.W., Gende, S.M., Fran-cis, T.B., and Palen, W.J. 2003. Pacific salmon and the ecology of coastal ecosystems. Front. Ecol. Environ.  1 : 31–37.Wipfli, M.S., Hudson, J.P., Caouette, J.P., and Chaloner, D.T. 2003.Marine subsidies in freshwater ecosystems: salmon carcasses in-crease the growth rates of stream-resident salmonids. Trans. Am.Fish. Soc.  132 : 371–381.Zabel, R.W., Scheuerell, M.D., McClure, M.M., and Williams, J.G.2005. The interplay between climate variability and density de-pendence in the population viability of Chinook salmon. Conserv.Biol.  19 . In press. © 2005 NRC Canada 964 Can. J. Fish. Aquat. Sci. Vol. 62, 2005 View publication statsView publication stats
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