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Feedbacks Between Nutrient Enrichment and Geomorphology Alter Bottom-Up Control on Food Webs

  • James A. Nelson
  • David Samuel Johnson
  • Linda A. Deegan
  • Amanda C. Spivak
  • Nathalie R. Sommer


Classic bottom-up theory predicts that increased resource availability (for example, nutrients) at the base of the food web will stimulate primary production and, in turn, secondary production. Recent studies, however, indicate that bottom-up controls on food web production can be modified by other factors, such as landscape configuration and continuity. As part of a 10-year ecosystem-scale experiment in a New England salt marsh, we investigated the response of secondary consumers, specifically a fish, the mummichog (Fundulus heteroclitus), to nutrient enrichment. In the first 6 years, we observed a classic bottom-up response of increased production of algae, invertebrate prey, and mummichogs. After the sixth year, however, mummichog biomass declined to below reference levels by the eighth year. This decline in mummichog biomass coincided with nutrient-induced collapse of the low-marsh habitat. Based on stable isotope analyses, field surveys, and small-scale experiments, we suggest that the geomorphic changes induced a trophic decoupling between creek and marsh habitats, thereby reducing mummichog access to prey in the intermittently flooded marsh. Thus, despite continued stimulation of algal and invertebrate prey production, fish abundances declined to below pre-enrichment levels. Our results demonstrate how geomorphic controls can override classic bottom-up control and emphasize the importance of long-term studies in detecting the response of slow-turnover phenomena (for example, changing landscapes).


food web theory nutrient enrichment landscape control saltmarsh estuary trophic subsidy spatially coupled geomorphology 



We thank the many, many undergraduates who contributed to data collection over the decade of this research; Allison Hall for her work conducting the mummichog diet experiment. Special thanks to Chris Stallings for his consultation on the statistical analysis. Thanks to David Behringer for creating the map of the field sites. We thank the two anonymous reviewers and the editor for their constructive comments. Support was provided by NSF (DEB-1354494, OCE-1238212, OCE-1233678), the Northeast Climate Science Center (DOI G12AC0000), the US Fish and Wildlife Service, and Woods Hole Oceanographic Institution. This paper is Contribution No. 3749 of the Virginia Institute of Marine Science, College of William & Mary.

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  1. Able K, Hagan S, Brown S. 2003. Mechanisms of marsh habitat alteration due to Phragmites: response of young-of-the-year mummichog (Fundulus heteroclitus) to treatment for Phragmites removal. Est Coasts 26:484–94.CrossRefGoogle Scholar
  2. Able KW, Hagan SM, Brown SA. 2006. Habitat use, movement, and growth of young-of-the-year Fundulus spp. in southern New Jersey salt marshes: comparisons based on tag/recapture. J Exper Mar Biol Ecol 335:177–87.CrossRefGoogle Scholar
  3. Baker R, Fry B, Rozas LP, Minello TJ. 2013. Hydrodynamic regulation of salt marsh contributions to aquatic food webs. Mar Ecol Prog Ser 490:37–52.CrossRefGoogle Scholar
  4. Baker HK, Nelson JA, Leslie HM. 2016. Quantifying striped bass (Morone saxatilis) dependence on saltmarsh-derived productivity using stable isotope analysis. Est Coasts 39:1537–42.CrossRefGoogle Scholar
  5. Banse K, Mosher S. 1980. Adult body mass and annual production/biomass relationships of field populations. Ecol Monogr 50:355–79.CrossRefGoogle Scholar
  6. Baxter CV, Fausch KD, Murakami M, Chapman PL. 2004. Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85:2656–63.CrossRefGoogle Scholar
  7. Bohannan BJ, Lenski RE. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3:362–77.CrossRefGoogle Scholar
  8. Carpenter SR, Cole ML, Pace M, Van de Bogert M, Bade DL, Bastviken D, Gille JR, Hodgson JF, Kritzberg ES. 2005. Ecosystem subsidies: terrestrial support of aquatic food web from 13C addition to contrasting lakes. Ecology 86:2737–50.CrossRefGoogle Scholar
  9. Christian RR, Allen DM. 2014. Linking hydrogeomorphology and food webs in intertidal creeks. Est Coasts 37:74–90.CrossRefGoogle Scholar
  10. Clavero M, Pou-Rovira Q, Zamora L. 2009. Biology and habitat use of three-spined stickleback (Gasterosteus aculeatus) in intermittent Mediterranean streams. Ecol Freshw Fish 18:550–9.CrossRefGoogle Scholar
  11. Currin C, Wainright S, Able K, Weinstein M, Fuller C. 2003. Determination of food web support and trophic position of the mummichog, Fundulus heteroclitus, in New Jersey smooth cordgrass (Spartina alterniflora), common reed (Phragmites australis), and restored salt marshes. Est Coasts 26:495–510.CrossRefGoogle Scholar
  12. Davis JM, Rosemond AD, Eggert SL, Cross WF, Wallace JB. 2010. Long-term nutrient enrichment decouples predator and prey production. Proc Natl Acad Sci 107:121–6.CrossRefPubMedGoogle Scholar
  13. De Boeck P, Bakker M, Zwitser R, Nivard M, Hofman A, Tuerlinckx F, Partchev I. 2011. The estimation of item response models with the lmer function from the lme4 package in R. J Stat Softw 39:1–28.CrossRefGoogle Scholar
  14. Deegan LA. 2002. Lessons learned: the effects of nutrient enrichment on the support of nekton by seagrass and saltmarsh ecosystems. Estuaries 25:585–600.CrossRefGoogle Scholar
  15. Deegan LA, Bowen JL, Drake D, Fleeger JW, Friedrichs CT, Galvan K, Hobbie JE, Hopkinson CS, Johnson DS, Johnson JM, Lemay LE, Miller E, Peterson B, Picard C, Sheldon S, Vallino JJ, Warren RS. 2007. Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecol Appl 17:S42–63.CrossRefGoogle Scholar
  16. Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–92.CrossRefPubMedGoogle Scholar
  17. Drake DC, Peterson BJ, Galvan KA, Deegan LA, Hopkinson CS, Johnson JM, Koop-Jakobsen K, Lemay LE, Picard C. 2009. Salt marsh ecosystem biogeochemical responses to nutrient enrichment: a paired 15N tracer study. Ecology 90:2535–46.CrossRefPubMedGoogle Scholar
  18. Ferry KH, Mather ME. 2012. Spatial and temporal diet patterns of subadult and small adult striped bass in massachusetts estuaries: data, a synthesis, and trends across scales. Mar Coast Fish 4:30–45.CrossRefGoogle Scholar
  19. Fleeger JW, Johnson DS, Galvan KA, Deegan LA, Galván KA, Deegan LA. 2008. Top-down and bottom-up control of infauna varies across the saltmarsh landscape. J Exper Mar Biol Ecol 357:20–34.CrossRefGoogle Scholar
  20. Folch J, Lees M, Sloane-Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509.PubMedGoogle Scholar
  21. Haas HL, Freeman CJ, Logan JM, Deegan L, Gaines EF. 2009. Examining mummichog growth and movement: are some individuals making intra-season migrations to optimize growth? J Exper Mar Biol Ecol 369:8–16.CrossRefGoogle Scholar
  22. Halpin PM. 2000. Habitat use by an intertidal salt-marsh fish: trade-offs between predation and growth. Mar Ecol Prog Ser 198:203–14.CrossRefGoogle Scholar
  23. Hansen RA. 2000. Effects of habitat complexity and composition on a diverse litter microarthropod assemblage. Ecology 81:1120–32.CrossRefGoogle Scholar
  24. Heck KL, Valentine JF, Pennock JR, Chaplin G, Spitzer PM. 2006. Effects of nutrient enrichment and grazing on shoalgrass Halodule wrightii and its epiphytes: results of a field experiment. Mar Ecol Prog Ser 326:145–56.CrossRefGoogle Scholar
  25. Hedges LV, Gurevitch J, Curtis PS. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–6.CrossRefGoogle Scholar
  26. Hershey AE, Gettel GM, McDonald ME, Miller MC, Mooers H, O’Brien WJ, Pastor J, Richards C, Schuldt JA. 1999. A geomorphic–trophic model for landscape control of Arctic lake food webs. Bioscience 49:887–97.CrossRefGoogle Scholar
  27. Hillebrand H, Kahlert M. 2001. Effect of grazing and nutrient supply on periphyton biomass and nutrient stoichiometry in habitats of different productivity. Limnol Oceanogr 46:1881–98.CrossRefGoogle Scholar
  28. Howe ER, Simenstad CA, Toft JD, Cordell JR, Bollens SM. 2014. Macroinvertebrate prey availability and fish diet selectivity in relation to environmental variables in natural and restoring north San Francisco bay tidal marsh channels. San Franc Est Watershed Sci 12:1.Google Scholar
  29. Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT. 2014. Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–50.CrossRefPubMedGoogle Scholar
  30. Javonillo R, Deegan L, Chiravalle K, Hughes J. 1997. The importance of access to salt-marsh surface to short-term growth of Fundulus heteroclitus in a New England salt marsh. Biol Bull 193:288.CrossRefPubMedGoogle Scholar
  31. Jennings S, Warr KJ, Mackinson S. 2002. Use of size-based production and stable isotope analyses to predict trophic transfer efficiencies and predator-prey body mass ratios in food webs. Mar Ecol Prog Ser 240:11–20.CrossRefGoogle Scholar
  32. Johnson DS. 2011. High-marsh invertebrates are susceptible to eutrophication. Mar Ecol Prog Ser 438:143–52.CrossRefGoogle Scholar
  33. Johnson DS. 2014. Fiddler on the roof: a northern range extension for the marsh fiddler crab Uca pugnax. J Crustac Biol 34:671–3.CrossRefGoogle Scholar
  34. Johnson DS. 2015. The savory swimmer swims north: a northern range extension of the blue crab Callinectes sapidus? J Crustac Biol 35:105–10.CrossRefGoogle Scholar
  35. Johnson DS, Fleeger JW. 2009. Weak response of saltmarsh infauna to ecosystem-wide nutrient enrichment and fish predator reduction: a four-year study. J Exper Mar Biol Ecol 373:35–44.CrossRefGoogle Scholar
  36. Johnson D, Jessen B. 2008. Do spur-throated grasshoppers, Melanoplus spp. (Orthoptera: Acrididae), exert top-down control on smooth cordgrass Spartina alterniflora in Northern New England? Est Coasts 31:912–19.CrossRefGoogle Scholar
  37. Johnson DS, Short MI. 2013. Chronic nutrient enrichment increases the density and biomass of the mudsnail, Nassarius obsoletus. Est Coasts 36:28–35.CrossRefGoogle Scholar
  38. Johnson D, Fleeger J, Galván K, Moser EB. 2007. Worm holes and their space-time continuum: spatial and temporal variability of macroinfaunal annelids in a Northern New England salt marsh. Est Coasts 30:226–37.CrossRefGoogle Scholar
  39. Johnson DS, Scott WR, Deegan LA, Mozdzer TJ. 2016. Saltmarsh plant responses to eutrophication. Ecol Appl 26:2649–61.CrossRefGoogle Scholar
  40. Kearns PJ, Angell JH, Howard EM, Deegan LA, Stanley RH, Bowen JL. 2016. Nutrient enrichment induces dormancy and decreases diversity of active bacteria in salt marsh sediments. Nat Commun 7:12881.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kennedy C. 2013. Habitat heterogeneity concentrates predators in the seascape: linking intermediate-scale estuarine habitat to striped bass distribution. Masters Thesis.
  42. Kneib RT. 1986. Size-specific patterns in the reproductive cycle of the killifish, Fundulus heteroclitus, (Pisces: Fundulidae) from Sapelo Island, Georgia. Copeia 1986:342–51.CrossRefGoogle Scholar
  43. Kneib RT. 1997. The role of tidal marshes in the ecology of estuarine nekton. Oceanogr Mar Biol Ann Rev 35:163–220.Google Scholar
  44. Kuznetsova A, Brockhoff PB, Christensen RH. 2017. lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26.CrossRefGoogle Scholar
  45. Laundré JW, Hernández L, Ripple WJ. 2010. The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7.CrossRefGoogle Scholar
  46. Lima SL. 2002. Putting predators back into behavioral predator–prey interactions. Trends Ecol Evol 17:70–5.CrossRefGoogle Scholar
  47. Lockfield KC, Fleeger JW, Deegan LA. 2013. Population-level responses by the mummichog, Fundulus heteroclitus, to chronic nutrient enrichment in a New England Salt Marsh. Mar Ecol Prog Ser 492:211–22.CrossRefGoogle Scholar
  48. McCann KS, Rasmussen JB, Umbanhowar J. 2005. The dynamics of spatially coupled food webs. Ecol Lett 8:513–23.CrossRefPubMedGoogle Scholar
  49. McGlathery KJ. 1995. Nutrient and grazing influences on a subtropical seagrass community. Mar Ecol Prog Ser 1:239–52.CrossRefGoogle Scholar
  50. McIvor CC, Odum WE. 1988. Food, predation risk, and microhabitat selection in a marsh fish assemblage. Ecology 69:1341–51.CrossRefGoogle Scholar
  51. McQueen DJ, Johannes MRS, Post JR, Stewart TJ, Lean DRS. 1989. Bottom-up and top-down impacts on freshwater pelagic community structure. Ecol Monogr 59:289–309.CrossRefGoogle Scholar
  52. Menge BA, Lubchenco J, Bracken MES, Chan F, Foley MM, Freidenburg TL, Gaines SD, Hudson G, Krenz C, Leslie H. 2003. Coastal oceanography sets the pace of rocky intertidal community dynamics. Proc Natl Acad Sci 100:12229–34.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Neckles HA, Wetzel RL, Orth RJ. 1993. Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia 93:285–95.CrossRefPubMedGoogle Scholar
  54. Nelson JA, Deegan L, Garritt R. 2015. Drivers of spatial and temporal variability in estuarine food webs. Mar Ecol Prog Ser 533:67–77.CrossRefGoogle Scholar
  55. Neutel A-M, Heesterbeek JAP, van de Koppel J, Hoenderboom G, Vos A, Kaldeway C, Berendse F, de Ruiter PC. 2007. Reconciling complexity with stability in naturally assembling food webs. Nature 449:599–602.CrossRefPubMedGoogle Scholar
  56. Pauly D, Christensen V. 1995. Primary production required to sustain global fisheries. Nature 374:255–7.CrossRefGoogle Scholar
  57. Pautzke SM, Mather ME, Finn JT, Deegan LA, Muth RM. 2010. Seasonal use of a New England estuary by foraging contingents of migratory striped bass. Trans Am Fish Soc 139:257–69.CrossRefGoogle Scholar
  58. Power ME, Dietrich WE, Finlay JC. 1996. Dams and downstream aquatic biodiversity: potential food web consequences of hydrologic and geomorphic change. Environ Manag 20:887–95.CrossRefGoogle Scholar
  59. Pringle RM, Fox-Dobbs K. 2008. Coupling of canopy and understory food webs by ground-dwelling predators. Ecol Lett 11:1328–37.CrossRefPubMedGoogle Scholar
  60. Rooney N, McCann KS. 2012. Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–6.CrossRefPubMedGoogle Scholar
  61. Rooney N, McCann KS, Moore JC. 2008. A landscape theory for food web architecture. Ecol Lett 11:867–81.CrossRefPubMedGoogle Scholar
  62. Rosenzweig ML. 1971. Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–7.CrossRefPubMedGoogle Scholar
  63. Rozas LP, Minello TJ. 1997. Estimating densities of small fishes and decapod crustaceans in shallow estuarine habitats: a review of sampling design with focus on gear selection. Estuaries 20:199–213.CrossRefGoogle Scholar
  64. Sabo JL, Power ME. 2002. River-watershed exchange: effects of riverine subsidies on riparian lizards and their terrestrial prey. Ecology 83:1860–9.Google Scholar
  65. Sanders D, Platner C. 2007. Intraguild interactions between spiders and ants and top-down control in a grassland food web. Oecologia 150:611–24.CrossRefPubMedGoogle Scholar
  66. Semmens BX, Stock BC, Ward E, Moore JW, Parnell A, Jackson AL, Phillips DL, Bearhop S, Inger R. 2014. MixSIAR: A Bayesian stable isotope mixing model for characterizing intrapopulation niche variation.Google Scholar
  67. Sheaves M. 2009. Consequences of ecological connectivity: the coastal ecosystem mosaic. Mar Ecol Prog Ser 391:107–15.CrossRefGoogle Scholar
  68. Spivak AC. 2015. Benthic biogeochemical responses to changing estuary trophic state and nutrient availability: a paired field and mesocosm experiment approach. Limnol Oceanogr 60:3–21.CrossRefGoogle Scholar
  69. Spivak AC, Ossolinski J. 2016. Limited effects of nutrient enrichment on bacterial carbon sources in salt marsh tidal creek sediments. Mar Ecol Prog Ser 544:107–30.CrossRefGoogle Scholar
  70. Spivak A, Reeve J. 2015. Rapid cycling of recently fixed carbon in a Spartina alterniflora system: a stable isotope tracer experiment. Biogeochemistry 125:97–114.CrossRefGoogle Scholar
  71. Spivak AC, Canuel EA, Je Duffy, Jp Richardson. 2007. Top-down and bottom-up controls on sediment organic matter composition in an experimental seagrass ecosystem. Limnol Oceanogr 52:2595–607.CrossRefGoogle Scholar
  72. Spivak AC, Canuel EA, Duffy JE, Richardson JP. 2009. Nutrient enrichment and food web composition affect ecosystem metabolism in an experimental seagrass habitat. PLoS ONE 4:e7473.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Stevens MHH, Steiner CE. 2006. Effects of predation and nutrient enrichment on a food web with edible and inedible prey. Freshw Biol 51:666–71.CrossRefGoogle Scholar
  74. Taylor MH, Leach GJ, DiMichele L, Levitan WM, Jacob WF. 1979. Lunar spawning cycle in the mummichog, Fundulus heteroclitus (Pisces: Cyprinodontidae). Copeia 1:291–7.CrossRefGoogle Scholar
  75. Thomson RL, Forsman JT, Mönkkönen M, Hukkanen M, Koivula K, Rytkönen S, Orell M. 2006. Predation risk effects on fitness related measures in a resident bird. Oikos 113:325–33.CrossRefGoogle Scholar
  76. Tumbiolo ML, Downing JA. 1994. An empirical model for the prediction of secondary production in marine benthic invertebrate populations. Mar Ecol Prog Ser 114:165–7.CrossRefGoogle Scholar
  77. Ward J, Tockner K, Schiemer F. 1999. Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regul Rivers Res Manag 15:125–39.CrossRefGoogle Scholar
  78. Ware DM, Thomson RE. 2005. Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science 308:1280–4.CrossRefPubMedGoogle Scholar
  79. Warren RS, Niering WA. 1993. Vegetation change on a northeast tidal marsh: interaction of sea-level rise and marsh accretion. Ecology 74:96–103.CrossRefGoogle Scholar
  80. Wenner CA, Musick JA. 1975. Food habits and seasonal abundance of the American eel, Anguilla rostrata, from the lower Chesapeake Bay. Chesap Sci 16:62–6.CrossRefGoogle Scholar
  81. Wilson RM, Chanton J, Lewis G, Nowacek D. 2009. Combining organic matter source and relative trophic position determinations to explore trophic structure. Est Coasts 32:999–1010.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • James A. Nelson
    • 1
    • 2
  • David Samuel Johnson
    • 3
  • Linda A. Deegan
    • 2
    • 4
  • Amanda C. Spivak
    • 5
  • Nathalie R. Sommer
    • 2
  1. 1.Department of BiologyUniversity of Louisiana at LafayetteLafayetteUSA
  2. 2.Ecosystem CenterMarine Biological LaboratoryWoods HoleUSA
  3. 3.Virginia Institute of Marine Science, College of William & MaryGloucester PointUSA
  4. 4.Woods Hole Research CenterFalmouthUSA
  5. 5.Marine Chemistry and Geochemistry DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA

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