Using stable isotopes to discern mechanisms of connectivity in estuarine detritus-based food webs

Marine Ecology Progress Series

Volumn 518, Issue , 2015, Pages 13-29

  Howe, Emily R ^a   Simenstad, Charles A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Estuarine ecology; Food web connectivity; Stable isotopes

Indexed keywords

ADVECTION; ASSIMILATION EFFICIENCY; BAYESIAN ANALYSIS; CONNECTIVITY; DEMERSAL FISH; DETRITUS; DISCHARGE; DOMINANCE; ECOTONE; ESTUARINE ECOSYSTEM; FOOD WEB; LANDSCAPE; LIFE HISTORY TRAIT; ORGANIC MATTER; STABLE ISOTOPE; TELEOST; TROPHIC INTERACTION;

PUGET SOUND; UNITED STATES; WASHINGTON [UNITED STATES];

PAROPHRYS VETULA; PISCES; SYNGNATHUS LEPTORHYNCHUS;

EID: 84920641241     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps11066     Document Type: Article

References (88)

1. Anderson M, Gorley R, Clarke K (2008) Permanova+ for Primer: guide to software and statistical methods. PRIMER-E Ltd, Plymouth
2. Asmus H, Asmus R (2000) Material exchange and food web of seagrass beds in the Sylt-Romo Bight: How significant are community changes at the ecosystem level? Helgol Mar Res 54:137-150
3. Babson AL, Kawase A, MacCready P (2006) Seasonal and interannual variability in the circulation of Puget Sound, Washington: a box model study. Atmos-Ocean 44:29-45
4. Barrows APW, Martin-Smith KM, Baine MSP (2009) Population variables and life-history characteristics of the alligator pipefish Syngnathoides biaculeatus, in Papua New Guinea. J Fish Biol 74:806-819
5. Bayer R (1980) Size, seasonality, and sex ratios of the bay pipefish (Syngnathus leptorhynchus) in Oregon. Northwest Sci 54:161-167
6. Brown T, Sibert J (1977) Food of some benthic harpacticoid copepods. J Fish Res Board Can 34:1028-1031
7. Buchheister A, Latour RJ (2010) Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445-461
8. Bulthuis D (1993) Review of water quality data in the Padilla Bay/Bayview watershed. Padilla Bay National Estuarine Research Reserve Technical Report No. 10, Washington State Department of Ecology, Mount Vernon, WA
9. Bulthuis D (1996) Coastal habitats in Padilla Bay, Washington: a review. Technical Report EL-96-15, US Army Engineer Waterways Experiment Station, Seattle, WA
10. Bulthuis D, Conrad A (1995) Guemes Channel and Padilla Bay: surface currents during flood tide. Padilla Bay National Estuarine Research Reserve Technical Report No. 15, Washington State Department of Ecology, Mount Vernon, WA
11. Bulthuis D, Shull S (2006) Monitoring the distribution of submerged aquatic vegetation in Padilla Bay, NERR-SWMP biomonitoring pilot site, 2004: final report. Padilla Bay National Estuarine Research Reserve, Washington State Department of Ecology, Mount Vernon, WA
12. Cadenasso ML, Pickett STA, Weathers KC (2004) Effect of landscape boundaries on the flux of nutrients, detritus, and organisms. In: Polis GA, Power ME, Huxel GR (eds) Food webs at the landscape level. University of Chicago Press, Chicago, IL, p 154-168
13. Chen SN, Sandford LP, Koch EW, Shi F, North EW (2007) A nearshore model to investigate the effects of seagrass bed geometry on wave attenuation and suspended sediment transport. Estuar Coast 30:296-310
14. Chittaro PM, Finley RJ, Levin PS (2009) Spatial and temporal patterns in the contribution of fish from their nursery habitats. Oecologia 160:49-61
15. Clarke KR, Gorley RN (2001) Primer v6: user manual/tutorial. PRIMER-E, Plymouth
16. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth
17. Cloern JE, Canuel EA, Harris D (2002) Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnol Oceanogr 47:713-729
18. Collins B, Sheikh A (2005) Historical reconstruction, classification, and change analysis of Puget Sound tidal marshes. Washington State Department of Natural Resources, Aquatic Resources Division, Olympia, WA
19. Connolly RM, Gorman D, Guest MA (2005) Movement of carbon among estuarine habitats and its assimilation by invertebrates. Oecologia 144:684-691
20. Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31-47
21. Fry B (2006) Stable isotope ecology. Springer, New York, NY
22. Garcia EA, Bertness MD, Alberti J, Silliman BR (2011) Crab regulation of cross-ecosystem resource transfer by marine foraging fire ants. Oecologia 166:1111-1119
23. Gordon DC, Prouse NJ, Cranford PJ (1985) Occurrence of Spartina macrodetritus in Bay of Fundy waters. Estuaries 8:290-295
24. Greenwood MJ, McIntosh AR (2008) Flooding impacts on responses of a riparian consumer to cross-ecosystem subsidies. Ecology 89:1489-1496
25. Grossman EE, George DA, Lam A (2011) Shallow stratigraphy of the Skagit River Delta, Washington, USA, derived from sediment cores. USGS Open File Report 2011-1194. http://pubs.usgs.gov/2011/1194
26. Guest MA, Connolly RM (2004) Fine-scale movement and assimilation of carbon in saltmarsh and mangrove habitat by resident animals. Aquat Ecol 38:599-609
27. Guest MA, Connolly RM, Lonergan NR (2004) Carbon movement and assimilation by invertebrates in estuarine habitat at the scale of meters. Mar Ecol Prog Ser 278:27-34
28. Gunderson DR, Armstrong DA, Shi YB, McConnaughey RA (1990) Patterns of estuarine use by juvenile English sole (Parophrys vetulus) and Dungeness crab (Cancer magister). Estuaries 13:59-71
29. Gustafson R, Lenarz W, McCain W, Builder T, Method R (2000) Status review of Pacific hake, Pacific cod, and walleye pollock from Puget Sound, WA. US Department of Commerce, Seattle, WA
30. Hart J (1973) Pacific fishes of Canada. Fisheries Research Board of Canada, Ottawa
31. Holland M, Whigham DF, Gopal B (1990) The characteristics of wetland ecotones. In: Naiman RJ, Decamps H (eds) The ecology and management of aquatic-terrestrial ecotones. The Parthenon Publishing Group, Paris
32. Hood W (2010) Tidal channel meander formation by depositional rather than erosional processes: examples from the prograding Skagit River Delta (Washington, USA). Earth Surf Process Landf 35:319-330
33. Hurst TP, Ryer CH, Ramsey JM, Haines SA (2007) Divergent foraging strategies of three co-occurring north Pacific flatfishes. Mar Biol 151:1087-1098
34. Huxel GR, McCann K (1998) Food web stability: the influence of trophic flows across habitats. Am Nat 152:460-469
35. Johnson SW, Thedinga JF, Neff AD, Harris PM, Lindeberg MR, Maselko JM, Rice SD (2010) Fish assemblages in nearshore habitats of Prince William Sound, Alaska. Northwest Sci 84:266-280
36. Kneib RT (2000) Saltmarsh ecoscapes and production transfers by estuarine nekton in the southeastern United States. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic Publishers, Dordrecht, p 267-291
37. Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM and others (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev Camb Philos Soc 87:545-562
38. Lazzari M, Able K (1990) Northern pipefish, Syngnathus fuscus, occurrences over the Mid-Atlantic Bight continental shelf: evidence of seasonal migration. Environ Biol Fishes 27:177-185
39. Leysen H, Christiaens J, De Kegel B, Boone MN, Van Hoorebeke L, Adriaens D (2011) Musculoskeletal structure of the feeding system and implications of snout elongation in Hippocampus reidi and Dunckerocampus dactyliophorus. J Fish Biol 78:1799-1823
40. Lubetkin SC, Simenstad CA (2004) Multi-source mixing models to quantify food web sources and pathways. J Appl Ecol 41:996-1008
41. Maier G, Simenstad C (2009) The role of marsh-derived macrodetritus to the food webs of juvenile chinook salmon in a large altered estuary. Estuar Coast 32:984-998
42. 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
43. McBride A, Wolf K, Beamer E (2006) Skagit Bay nearshore habitat mapping. Skagit River System Cooperative, La Conner, WA, www.skagitcoop.org/documents/EB2180-McBride%20et%20al-2006.pdf
44. McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378-390
45. Moore JW, Schindler DE, Ruff CP (2008) Habitat saturation drives thresholds in stream subsidies. Ecology 89:306-312
46. 15N) signatures of particulate organic matter in the lower Amazon River: seasonal contrasts and connectivity between floodplain lakes and the mainstem. Org Geochem 42:1159-1168
47. Murphy M, Johnson S, Csepp D (2000) A comparison of fish assemblages in eelgrass and adjacent subtidal habitats near Craig, Alaska. Alsk Fish Res Bull 7:11-21
48. Nakano S, Masashi M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166-170
49. Nelson J, Chanton J, Coleman F, Koenig C (2011) Patterns of stable carbon isotope turnover in gag, Mycteroperca microlepis, an economically important marine piscivore determined with a non-lethal surgical biopsy procedure. Environ Biol Fishes 90:243-252
50. Nelson R (1989) Padilla Bay hydrologic study. Prepared for Western Washington University by Entranco Engineers, Kirkland, WA. Padilla Bay National Estuarine Research Reserve Reprint Series No. 12, Washington State Department of Ecology, Mount Vernon, WA
51. Odum EP (1980) The status of three ecosystem-level hypotheses regarding salt marsh estuaries: tidal subsidy, outwelling, and detritus based food chains. In: Kennedy VS (ed) Estuarine perspectives. Academic Press, New York, NY, p 485-495
52. Pennak R (1953) Freshwater invertebrates of the United States. The Ronald Press Company, New York, NY
53. Pittman SJ, McAlpine CA, Pittman KM (2004) Linking fish and prawns to their environment: a hierarchical landscape approach. Mar Ecol Prog Ser 283:233-254
54. Plummer M (2003) JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling. In: Hornik K, Leisch F, Zeileis A (eds) Proc 3rd Int Workshop on Distributed Statistical Computing (DSC 2003), Mar 20-22, 2003, Vienna, p 20-22
55. Plummer M, Best N, Cowles M, Vines S (2006) CODA: Convergence diagnosis and output analysis for MCMC. R News 6:7-11
56. Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 18:293-320
57. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718
58. Rooper CN, Gunderson DR, Armstrong DA (2003) Patterns in use of estuarine habitat by juvenile English sole (Pleuronectes vetulus) in four Eastern North Pacific estuaries. Estuaries 26:1142-1154
59. Ryer CH, Orth RJ (1987) Feeding ecology of the northern pipefish, Syngnathus fuscus, in a seagrass communitiy of the lower Chesapeake Bay. Estuaries 10:330-336
60. Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ (2003) Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31-37
61. Schmid-Araya J, Schmid P (2000) Trophic relationships: integrating meiofauna into a realistic benthic food web. Freshw Biol 44:149-163
62. Semmens BX, Ward EJ, Moore JW, Darimont CT (2009) Quantifying inter- and intra-population niche variability using hierarchical Bayesian stable isotope mixing models. PLoS ONE 4:e6187
63. Sheaves M (2009) Consequences of ecological connectivity: the coastal ecosystem mosaic. Mar Ecol Prog Ser 391:107-115
64. Shokri MR, Gladstone W, Jelbart J (2009) The effectiveness of seahorses and pipefish (Pisces: Syngnathidae) as a flagship group to evaluate the conservation value of estuarine seagrass beds. Aquat Conserv: Mar Freshw Ecosyst 19:588-595
65. Silver J (2009) Effects of a non-native eelgrass (Zostera japonica) on sediment nitrogen cycling microbial communities and processes. MS Thesis, University of Washington, Seattle, WA
66. Simenstad CA, Cordell JR, Fresh KL, Carr M (1995) Trophic linkages from epibenthic crustaceans in littoral flat habitats: seasonal and regional comparisons. Padilla Bay National Estuarine Research Reserve Reprint Series No. 35, Washington State Department of Ecology, Mount Vernon, WA
67. Stribling JM, Cornwell JC, Currin C (1998) Variability of stable sulfur isotopic ratios in Spartina alterniflora. Mar Ecol Prog Ser 166 73-81
68. Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595-601
69. 15N fractionation in fishes. J Exp Mar Biol Ecol 340:1-10
70. Takahashi E, Connolly RM, Lee SY (2003) Growth and reproduction of double-ended pipefish, Syngnathoides biaculeatus, in Moreton Bay, Queensland, Australia. Environ Biol Fishes 67:23-33
71. Terry C (1977) Stomach contents methodology: still lots of questions. In: Sirnenstad CA, Lipovsky SJ (eds), Fish food habits studies. Proc 1st Pacific Northwest Tech Workshop, Oct 13-15, 1976, p 87-92
72. Thayer G, Stuart H, Kenworthy W, Ustach J, Hall A (eds) (1978) Habitat values of salt marshes, mangroves, and seagrasses for aquatic organisms. American Water Resources Association, Minneapolis, MN
73. Toole CL (1980) Intertidal recruitment and feeding in relation to optimal utilization of nursery areas by juvenile English sole (Parophrys vetulus: Pleuronectidae). Environ Biol Fishes 5:383-390
74. USGS (US Geological Survey) (2011) USGS real-time water data for Washington State, http://waterdata.usgs.gov/wa/nwis/rt
75. Van Wassenbergh S, Roos G, Aerts P, Herrel A, Adriaens D (2011) Why the long face? A comparative study of feeding kinematics of two pipefishes with different snout lengths. J Fish Biol 78:1786-1798
76. 13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061-2066
77. Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) River continuum concept. Can J Fish Aquat Sci 37:130-137
78. Vinagre C, Fonseca V, Cabral H, Costa MJ (2006) Habitat suitability index models for the juvenile soles, Solea solea and Solea senegalensis, in the Tagus estuary: de fining variables for species management. Fish Res 82:140-149
79. Vinagre C, Salgado J, Cabral HN, Costa MJ (2011) Food web structure and habitat connectivity in fish estuarine nurseries-impact of river flow. Estuar Coast 34:663-674
80. Vizzini S, Mazzola A (2004) The trophic structure of the pipefish community (Pisces: Sygnathidae) from a western Mediterranean seagrass meadow based on stable isotope analysis. Estuaries 27:325-333
81. Vizzini S, Mazzola A (2006) Sources and transfer of organic matter in food webs of a Mediterranean coastal environment: evidence for spatial variability. Estuar Coast Shelf Sci 66:459-467
82. Ward EJ, Semmens BX, Schindler DE (2010) Including source uncertainty and priori in the analysis of stable isotope mixing models. Environ Sci Technol 44:4645-4650
83. Webster K, Ogston A, Nittrouer C (2012) Delivery, reworking and export of fine-grained sediment across the sandy Skagit River tidal flats. Cont Shelf Res 60 (Suppl):S58-S70
84. Wiens JA (2002) Riverine landscapes: taking landscape ecology into the water. Freshw Biol 47:501-515
85. Wiggins W, Ruppert G, Smith R, Reed L, Courts M (1997) Water resources data, Washington, Water Year 1997. Water Data Report WA-97-1, US Geological Survey, Tacoma, WA
86. Wilson AB (2006) Genetic signature of recent glaciation on populations of a near-shore marine fish species (Syngnathus leptorhynchus). Mol Ecol 15:1857-1871
87. Yang ZQ, Khangaonkar T (2009) Modeling tidal circulation and stratification in Skagit River estuary using an unstructured grid ocean model. Ocean Model 28:34-49
88. Young HS, McCauley DJ, Dunbar RB, Dirzo R (2010) Plants cause ecosystem nutrient depletion via the interruption of bird-derived spatial subsidies. Proc Natl Acad Sci USA 107:2072-2077