Document Detail

Reciprocal subsidies and food web pathways leading to chum salmon fry in a temperate marine-terrestrial ecotone.
Jump to Full Text
MedLine Citation:
PMID:  20386705     Owner:  NLM     Status:  In-Process    
Stable isotope analysis was used to determine the relative proportions of terrestrial and marine subsidies of carbon to invertebrates along a tidal gradient (low-intertidal, mid-intertidal, high-intertidal, supralittoral) and to determine the relative importance of terrestrial carbon in food web pathways leading to chum salmon fry Oncorhynchus keta (Walbaum) in Howe Sound, British Columbia. We found a clear gradient in the proportion of terrestrially derived carbon along the tidal gradient ranging from 68% across all invertebrate taxa in the supralittoral to 25% in the high-intertidal, 20% in the mid-intertidal, and 12% in the low-intertidal. Stable isotope values of chum salmon fry indicated carbon contributions from both terrestrial and marine sources, with terrestrially derived carbon ranging from 12.8 to 61.5% in the muscle tissue of chum salmon fry (mean 30%). Our results provide evidence for reciprocal subsidies of marine and terrestrially derived carbon on beaches in the estuary and suggest that the vegetated supralittoral is an important trophic link in supplying terrestrial carbon to nearshore food webs.
Tamara N Romanuk; Colin D Levings
Related Documents :
25437235 - Risk, regulation and biotechnology: the case of gm crops.
14725885 - Nitrogen loading to pleasant bay, cape cod: application of models and stable isotopes t...
20386705 - Reciprocal subsidies and food web pathways leading to chum salmon fry in a temperate ma...
5929745 - Growth of desulfovibrio desulfuricans under heterotrophic and anaerobic conditions.
11275355 - Uridine uptake inhibition as a cytotoxicity test for a human hepatoma cell line (hepg2 ...
22039075 - Monitoring tobacco-specific n-nitrosamines and nicotine in novel marlboro and camel smo...
Publication Detail:
Type:  Journal Article; Research Support, Non-U.S. Gov't     Date:  2010-04-08
Journal Detail:
Title:  PloS one     Volume:  5     ISSN:  1932-6203     ISO Abbreviation:  PLoS ONE     Publication Date:  2010  
Date Detail:
Created Date:  2010-04-13     Completed Date:  -     Revised Date:  -    
Medline Journal Info:
Nlm Unique ID:  101285081     Medline TA:  PLoS One     Country:  United States    
Other Details:
Languages:  eng     Pagination:  e10073     Citation Subset:  IM    
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada.
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): PLoS One
Journal ID (publisher-id): plos
Journal ID (pmc): plosone
ISSN: 1932-6203
Publisher: Public Library of Science, San Francisco, USA
Article Information
Download PDF
Romanuk, Levings. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Received Day: 28 Month: 11 Year: 2009
Accepted Day: 17 Month: 3 Year: 2010
collection publication date: Year: 2010
Electronic publication date: Day: 8 Month: 4 Year: 2010
Volume: 5 Issue: 4
E-location ID: e10073
ID: 2851651
PubMed Id: 20386705
Publisher Id: 09-PONE-RA-14550R1
DOI: 10.1371/journal.pone.0010073

Reciprocal Subsidies and Food Web Pathways Leading to Chum Salmon Fry in a Temperate Marine-Terrestrial Ecotone Alternate Title:Intertidal Carbon Subsidies
Tamara N. Romanuk1*
Colin D. Levings2
Sharyn Jane Goldstienedit1 Role: Editor
1Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
2Centre for Aquaculture and Environmental Research, Department of Fisheries and Oceans, West Vancouver, British Columbia, Canada
University of Canterbury, New Zealand
Correspondence: * E-mail:
Contributed by footnote: Conceived and designed the experiments: TNR CDL. Performed the experiments: TNR CDL. Analyzed the data: TNR. Contributed reagents/materials/analysis tools: TNR CDL. Wrote the paper: TNR CDL.


Subsidies of prey and detritus across ecotones have been shown to affect food webs in both aquatic and terrestrial habitats [1]?[3]. In coastal areas, nearshore marine habitats commonly receive prey and detritus from adjacent terrestrial habitats [2]. This transfer of nutrients from terrestrial to marine habitats is also reciprocal, with nutrients derived from the marine environment entering terrestrial habitats in the form of beach wrack [2].

Supralittoral vegetation in coastal areas may play similar roles in ecosystem functioning as riparian vegetation in freshwater systems [4]. In small watersheds with dense surrounding forests much of the stream organic matter originates in the surrounding forest [5] and in freshwater riparian and stream food webs terrestrial invertebrates can comprise more than 50% of energy intake by stream fishes and are often a preferred prey of salmonids [6]. Similarly, in marine coastal habitats, supralittoral vegetation may provide an important source of terrigenous input in the form of leaf litter to intertidal areas [7]?[8] and terrestrial and intertidal invertebrates have been shown to comprise a proportion of their diets of salmon fry caught in nearshore habitats [9]?[12], [14]?[15].

Marine sources of carbon and nitrogen have also been shown to subsidize terrestrial food webs [16]. Marine subsidies are particularly pronounced on islands, which often have extremely low terrestrial primary productivity [16]?[17] and for ecosystems with high throughputs of anadromous fishes such as salmonids, which subsidize terrestrial vegetation [18]?[19]. For example Hocking and Reimchen (2009) found that the ? 15N signatures of riparian vegetation in 27 watersheds in British Columbia was positively related to total the biomass of spawning chum and pink salmon [19].

On coastal beaches, beach wrack is an important food source and habitat that subsidizes both marine and terrestrial food webs. For example, Lewis et al. [20] have shown that beach wrack subsidizes marine shore crabs that ride the nightly tide to the wrack line to feed on talitrid amphipods which forage at night on the beach wrack. Wrack also provides food for terrestrial organisms, in particular terrestrial arthropods [17], [21]?[24]. Olabarria et al. [25] found that beach wrack arthropod communities were dominated by terrestrial consumers such as coleopteran tenebrionid and staphylinid species and dipteran flies.

Stable isotope analysis (SIA) has been used extensively to describe aquatic food webs [26] and has become increasingly popular method to quantify energy flow, especially in ecotones where the contributions of terrestrial and aquatic energy sources have distinct isotopic signatures [27]?[28]. The ratio of the stable isotopes of nitrogen 15N/14N is positively correlated with trophic level, and the ratio of carbon stable isotopes 13C/12C yields information about the production base of the food web [26]. Carbon fixed by terrestrial C3 plants in temperate regions has a characteristic 13C/12C ratio of approximately ?28? [29]. Aquatic plants exhibit a much wider range in ?13C (?50? to ?10?) relative to terrestrial plants, reflecting site-specific and species-specific factors [30]?[31]. Because terrestrial and aquatic primary producers often have distinct carbon sources, mixing models can be used to assess the relative proportions of these primary energy sources in consumer diets [32].

In this study we report the results of stable isotope analysis of carbon and nitrogen for a collection of marine, intertidal, and terrestrial organisms collected in the intertidal and supralittoral in Howe Sound, British Columbia, Canada. Our objective was to determine the proportion of terrestrially derived carbon (TC) and marine derived carbon (MC) along the intertidal to supralittoral gradient focusing specifically on the pathways of energy flow to chum salmon fry, Oncorhynchus keta (Walbaum), which reside in the estuary from March to June during their transition to the marine environment.


Howe Sound is a fjord located on the southeastern shore of the Strait of Georgia, British Columbia, Canada (Fig. 1). The Sound derives its estuarine characteristics from the Squamish River on the northern reaches and the Fraser River on the southern reaches, as well as smaller creeks along the shoreline. Between March and October 2002 we collected samples of supralittoral vegetation, macroalgae, invertebrates, and chum salmon fry on two beaches at Furry Creek, located on the east side of the Sound (Fig. 1). The creek is located between the North and South sites. Several species of salmon (chinook, coho, chum, pink) have been found in Furry Creek but because major runs of chum salmon occur in the Squamish and Fraser Rivers it is probable that most of the chum fry we sampled were from the latter two river systems. At Furry Creek South, where there is >50 m swath of intact supralittoral vegetation we collected supralittoral vegetation, macroalgae, invertebrates, and chum salmon fry (Fig. 2). At Furry Creek North, where the supralittoral vegetation was removed for a housing development, we only collected chum salmon fry. For additional details regarding the sites see Romanuk and Levings [12]?[13]. The beaches are within ?350 m of each other. Range of tidal heights during the sampling period was from 0.28 m to 4.85 m?1.29 SD.

Ten species of live terrestrial supralittoral plants and six species of live macroalgae were collected by hand at Furry Creek [12]. Samples of vegetation and algae were washed with distilled water and then frozen and stored. Invertebrates were collected in June and October in four distinct zones: supralittoral, high-intertidal (i.e. beach wrack zone), mid-intertidal, and low-intertidal zones. Sampling similar Orders across zones allowed us to compare how ?13C changed along the terrestrial to marine gradient. Three Orders were sampled in more than one zone: Diptera (primarily Chironomidae) were sampled in the supralittoral (adult), high-intertidal (adult), mid-intertidal (adult), and low-intertidal (larvae) zones; Acariformes were collected from the supralittoral, high- and mid-intertidal zone; Amphipoda (Talitridae) were collected from the high-, mid-, and low-intertidal zones. Gastropods and Mytilus sp. were collected in the mid-intertidal.

We used a variety of collection methods including epibenthic sleds in the low-intertidal zone and hand vacuums in the supralittoral, high-intertidal, and mid-intertidal zones. Taxa were identified to lowest taxonomic level possible while retaining enough material for stable isotope analysis. One species of amphipod, Hyale plumulosa, was identified to species. Invertebrates were washed, frozen, and stored and later combined into composite samples of at least 0.2 mg dry weight (i.e. many individuals comprised each sample). Pooling samples was necessary due to the small size/biomass of most of the invertebrates. When pooled samples were used, variance is reported as the variance across pooled samples.

Chum salmon fry typically migrate downstream to estuaries and nearshore marine habitats where they spend up to three weeks before making the transition to pelagic oceanic conditions [33]. Chum salmon fry are found in Howe Sound and the Strait of Georgia from March until late July and originate from the Squamish, Fraser, and other rivers discharging into the Strait [34]. Juvenile chum salmon were collected from March to June 2002 by beach seining at high tide using a 3 m?1 m beach seine with a mesh size of 6 mm set parallel to shore ?1?3 m from the beach depending on the slope. Seining was conducted when the tide was higher than 3.05 m.

Chum salmon fry were kept in plastic bags in a cooler in the field and immediately frozen in the laboratory at ?20?C. Fork length and wet weight were measured for 163 individual chum salmon fry and stomachs were removed from 28 fish for gut content analysis. Flank muscle tissue was then removed from 163 fish for stable isotope analysis. Fish samples for stable isotope analysis consisted of 1, 2 or 3 individuals. In total, stable isotope analysis was performed on 44 fish samples composed of 163 individual chum salmon fry. We have previously reported that there is no statistically significant difference in isotope values for fish samples composed of either individual fish or combined samples [12].

All samples were oven dried at 60?C until constant weight. Samples were then sent to the University of New Brunswick Stable Isotope Laboratory or to University of California at Davis Stable Isotope Laboratory where they were ground into powder. Samples of algae, supralittoral vegetation, invertebrates, and fish were oxidized, and the resulting CO2 and N2 were analyzed with a continuous flow-isotope ratio mass spectrometer. Ratios of carbon (13C/12C) and nitrogen (15N/14N) were expressed as the relative per mil (?) difference between the sample and conventional standards (Pee Dee Belemite carbonate and N2 in air) as follows: ?X?=?[Rsample/Rstandard?1]?1000(?), where X?=?13C or 15N, and R?=?13C:12C or 15N:14N.

Gut content analysis (GCA) was performed on 28 chum salmon fry. Gut contents were identified to lowest possible taxonomic level and results are shown for fraction of all individuals (numerical abundance summed over the 28 fish) and fraction occurrence (number of chum salmon fry with the prey item).

Data analysis

Carbon and nitrogen isotope ratios were averaged across all sampling dates and the two sites. Contributions of terrestrially derived carbon (TC) and marine derived carbon (MC) to the assimilated carbon in chum salmon fry were calculated using the procedures and programs outlined in [32]. The mixing model calculates the contribution of each primary source assuming that only two sources are contributing to the isotopic signatures of the consumers. Source A was calculated as the average ?13C of supralittoral vegetation and source B was calculated as the average ?13C of marine macroalgae. For each taxa we report the ?13C and ?15N, relative proportion of TC, the standard error (SE) associated with the proportion, and the lower and upper 95%ile confidence intervals when n is?=?or >3. When n?=?1 or 2 we only report ?13C and ?15N and relative proportion of TC. We were not able to use a three source mixing model using wrack detritus or POM because their isotopic signatures overlapped with either supralittoral vegetation or marine macroalgae (T. Romanuk, unpublished data; for a discussion of carbon sources in Howe Sound see [12]). The mixing model uses the same set of terrestrial and marine basal sources to calculate the relative proportions of terrestrial and marine carbon in the muscle tissue of chum salmon fry, thus the proportions of TC are qualitatively the same as those reported for ?13C.

This research was conducted according to relevant national guidelines of the Department of Fisheries and Oceans (Canada).

Stable isotope analysis of food web components
?13C and ?15N of primary producers and invertebrates

?13C and ?15N of macroalgae was enriched and isotopically distinct from terrestrial vegetation. The average ?13C value for terrestrial vegetation was ?28.34 (?2.43 SD; Table 1). The average ?13C value for marine macroalgae algae was ?16.0 (?3.02 SD; Table 1).

Mean ?13C and TC in invertebrates increased with elevation along the tidal gradient ranging from ?17.28 (TC?=?12%) in the low-intertidal to ?18.43 (TC?=?20%) in the mid-intertidal, ?19.1(TC?=?25%) in the high-intertidal, and ?24.38 (TC?=?68%) in the supralittoral. TC ranged from 0% (for low-intertidal chironomids and mid-intertidal gastropods) to 87.2% for supralittoral Homoptera (Table 2). No taxa had ?13C indicative of a 100% terrestrial carbon source and for some consumers enrichment increased toward the lower elevations. Of the three taxa present in more than three tidal zones, Dipteran and Acariformes showed a clear gradient of enrichment in ?13C and TC from the supralittoral zone to the low-intertidal zone (Fig. 3). In contrast, there was no clear pattern of enrichment in ?13C for Amphipoda from the high- to low-intertidal zones.

Mean ?15N was lowest in the supralittoral (2.45) and highest in the mid-intertidal (7.9) with low-intertidal (5.53) and high-intertidal (6.4) displaying intermediate values. ?15N for secondary consumers ranged from 0.59 to 9.45 (mean 6.18?2.67 SD; Table 2). Intertidal Diptera had the highest ?15N (9.45) followed by barnacles (9.14) and Collembola (8.85). Supralittoral Homoptera (0.59) and supralittoral Acariformes (0.83) had the lowest ?15N. The only taxa to show a trend in ?15N along the tidal gradient was Acariformes, with ?15N lowest in the supralittoral (0.83) and highest in the mid-intertidal (6.55; Fig. 3).

?13C and ?15N of chum salmon fry

Chum salmon fry had an average fork length of 37 mm (range 29 to 52 mm) and an average wet weight of 0.48 g (range 0.2 to 1.35 g). ?13C for chum salmon fry averaged ?19.71 (n?=?44) ranging from ?23.59 to ?17.58 (?1.21 SD; Table 2 and Fig. 4) and ?15N averaged 13.94 ranging from 10.4 to 15.99 (?1.34 SD). TC ranged from 12.8 to 61.5% (mean 30%) with lower and upper confidence intervals of 12 and 48% (? SE 0.07).

Gut contents

Twenty-six prey taxa were identified in the gut content analysis of 28 individual chum salmon fry (Table 3). The five most abundant prey taxa by fraction of individual prey items were adult Chironomidae (60%), Harpacticoidea (8.9%), pupal Chironomidae (7.7%) gammarid Amphipoda (6.2), and larval Chironomidae (5%). Adult Chironomidae were present in 68% of individual chum followed by larval Chironomidae (50%), pupal Chironomidae (43%), gammarid Amphipoda (25%), Corophium sp. (Amphipoda; 21%), and Harpacticoidea (21%).


Our results suggest the importance of reciprocal subsidies in the terrestrial-marine ecotone in the Howe Sound estuary. Not only was marine derived carbon present in consumers present in the supralittoral zone, no supralittoral consumers were characterized by 100% terrestrially derived carbon. Likewise, terrestrially derived carbon was present even in the low-intertidal zone, particularly in amphipods. We found a clear gradient in terrestrially derived carbon down the tidal zone ranging from 68% across all taxa in the supralittoral to 25% in the high-intertidal, 20% in the mid-intertidal, and 12% in the low intertidal. This gradient was particularly clear for Diptera and Acariformes, two of the three taxa that were present in four or three zones respectively. In contrast to our results for carbon, there was no general spatial trend for ?15N suggesting that trophic position does not change systematically along the tidal gradient.

Stable isotope values of chum salmon fry and their prey indicated carbon contributions from both terrestrial and marine sources, with terrestrially derived carbon ranging from 12.8 to 61.5% in the muscle tissue of chum salmon fry (mean 30%). Adult chironomids were the dominant prey item of juvenile chum as has been previously reported at beaches in Howe Sound for juvenile chum salmon [15]. Stable isotope analysis of carbon in the intertidal Dipterans showed that between 9 and 53% of the carbon was terrestrially derived. Together, these results suggest that Dipterans are a major food web pathway for terrestrial carbon in chum salmon fry.

McCutchan et al. [35] has shown that enrichment of ?13C averages +0.4?0.12? (mean ? SE) from diet to consumer and ?15N averages +2.0?0.20? (mean ? SE) from diet to consumer. [35]. Our results suggest that: 1) adult Dipteran collected in the low and mid-intertidal, 2) Collembola and Amphipoda collected in the mid-intertidal, and 3) the amphipod H. plumulosa collected in the high-intertidal are the only groups of prey taxa that fall within potential ?13C and ?15N ranges for being a primary prey source (Fig. 4).

This interpretation is supported by the chum salmon fry gut content analysis, which found the highest number of individuals and highest occurrence of prey taxa in stomachs were adult, larval, and pupal Chironomidae. Collembola and Amphipoda were also abundant and common as food items. While the results from the stable isotope analysis also suggest that Cirripedia may be a primary prey source for chum salmon fry, the Cirripedia collected for stable isotope analysis were adults which may differ in their isotope ratios from free-living juveniles which are potential chum fry food. Six percent of fish had juvenile barnacles in the stomach contents, although the abundance of this prey item in the stomach contents was low (?1%).

Taxa that fall outside of the above range of ?15N values may still be an important link [36] through either another consumer or because their basal source was significantly different from the basal source for chum (Fig. 4). These taxa include: 1) Acariformes collected from both the high- and mid-intertidal, 2) supralittoral Diptera, 3) Amphipoda collected from the high- and mid-intertidal, and 4) Mytilus sp. and Isopoda collected from the mid-intertidal (Fig. 4). All of these taxa except for Mytilus sp. larvae, the only life stage of Mytilus sp. that can be eaten by juvenile salmonids, were found in the gut contents (Table 3).

While the remaining groups fall outside the potential ranges for ?13C fractionation from diet to consumer [35]?[36], these taxa may still make up a portion of the diet of chum; however, their contribution to the isotopic values of chum is either marginal, or alternatively, opportunistic feeding on taxa with both strong terrestrial signatures such as Homoptera as well as taxa with strong marine signatures such as larval Chironomidae may have resulted in isotopic signatures that reflect a wide range of prey sources. For example, across all chum salmon fry analyzed we found that Homoptera made up 0.3% and larval Chironomidae made up 8.8% of the gut contents by number of individuals (Table 3).

In conclusion, our results show a clear gradient in the proportion of terrestrially derived carbon in invertebrate taxa that decreases down the tidal zone from 68% in the supralittoral to 25% in the high-intertidal, 20% in the mid-intertidal, and 12% in the low intertidal. Stable isotope values and gut content analysis of chum salmon fry indicated carbon contributions from both terrestrial and marine derived sources. Our results suggest that the vegetated supralittoral is an important trophic link in supplying terrestrial carbon to nearshore food webs.


Competing Interests: The authors have declared that no competing interests exist.

Funding: NSERC PDF and Discovery Grant to TNR. Department of Fisheries and Oceans (Canada) provided funding for the data collection, stable isotope analysis, and gut content analysis. The funders had no role in the analysis, decision to publish, or preparation of the manuscript.

Beth Piercey, Shirley Fuchs, and Perry Poon assisted in either the field or the lab.

1. Hasler AD. Year: 1975Coupling of Land and Water SystemsNew YorkSpringer-Verlag
2. Polis GA,Anderson WB,Holt RD. Year: 1997Toward and integration of landscape and food web ecology: the dynamics of spatially subsidized food webs.Ann Rev Ecol Sys28289316
3. Wipfli MS. Year: 1997Terrestrial invertebrates as salmonid prey and nitrogen sources in streams: contrasting old-growth and young-growth riparian forests in southeastern Alaska, U.S.A.Can J Fish Aquat Sci5412591269
4. Levings CD,Romanuk TN. Year: 2004Overview of research and thoughts on the marine riparian as fish habitat in British Columbia.Lemieux JP,Brennan JS,Farrell M,Levings CD,Myers D37 Proceedings of the DFO/PSAT sponsored marine riparian experts workshop, Tsawwassen, B.C., February 17?18, 2004. Can Man Rep Fish Aquat Sci. 2680.
5. Gregory SV,Swanson FJ,McKee WA,Cummins KW. Year: 1991An ecosystem perspective of riparian zones.Bioscience41540551
6. Hunt RL. Year: 1975Use of terrestrial invertebrates as food for salmonids.Hasler ADCoupling of land and water systemsNew YorkSpringer-Verlag137152
7. Barnes RSK,Hughes RN. Year: 1988An Introduction to Marine EcologyLondonBlackwell
8. Mann KH,Lazier JRN. Year: 1991Dynamics of Marine EcosystemsLondonBlackwell
9. Healey MC. Year: 1980The ecology of juvenile salmon in Georgia Strait, Britsh Columbia.McNeil WJ,Himsworth DCSalmonid ecosystems of the North PacificCorvallisOregon State University Press203229
10. Toft JD,Cordell JR,Simenstad CA,Stamatiou LA. Year: 2007Fish distribution, abundance, and behavior along city shoreline types in Puget Sound.N Amer J Fish Manag27465480
11. Sobocinski KL. Year: 2003The impact of shoreline armoring on supratidal beach fauna of central Puget Sound. Master of Science thesis, University of Washington, School of Aquatic and Fishery Sciences, Seattle, WA.
12. Romanuk TN,Levings CD. Year: 2005Stable isotope analysis of trophic position and terrestrial vs marine carbon sources for juvenile Pacific salmonids in nearshore marine habitats.Fish Manag Ecol12113121
13. Romanuk TN,Levings CD. Year: 2003Associations between arthropods and supralittoral vegetation: dependence of terrestrial and aquatic taxa on vegetation.Envir Ent3213431353
14. Maier GO,Simenstad CA. Year: 2009The Role of Marsh-Derived Macrodetritus to the Food Webs of Juvenile Chinook Salmon in a Large Altered Estuary.Estuaries and Coasts32984998
15. Levings CD,Barry KL,Grout JA,Piercey GE,Marsden AD,et al. Year: 2004Effects of acid mine drainage on the estuarine food web, Britannia Beach, Howe Sound, British Columbia, Canada.Hydrobiologia525185202
16. Anderson WB,Polis GA. Year: 1998Marine subsidies of island communities in the Gulf of California: evidence from stable carbon and nitrogen isotopes.Oikos817580
17. Polis GA,Hurd SD. Year: 1996Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities.Am Nat147396423
18. Helfield JM,Naiman RJ. Year: 2001Effects of salmon-derived nitrogen on riparian forest growth and implications for stream productivity.Ecology8224032409
19. Hocking MD,Reimchen TE. Year: 2009Salmon species, density and watershed size predict magnitude of marine enrichment in riparian food webs.Oikos11813071318
20. Lewis TL,Mews M,Jelinski DE,Zimmer M. Year: 2007Detrital subsidy to the supratidal zone provides feeding habitat for intertidal crabs.Estuaries and Coasts30451458
21. Inglis G. Year: 1989The colonisation and degradation of stranded Macrocystis pyrifera (L.) C. Ag. by the macrofauna of a New Zealand sandy beach.J Exp Mar Biol Ecol125203217
22. Dugan JE,Hubbard DM,McCrary MD,Pierson MO. Year: 2003The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California.Est Coast Shelf Sci58S2540
23. Colombini I,Aloia A,Fallaci M,Pezzoli G,Chelazzi L. Year: 2000Temporal and spatial use of stranded wrack by the macrofauna of a tropical sandy beach.Mar Biol136531541
24. Jedrzejczak MF. Year: 2002Stranded Zostera marina L. vs wrack fauna community interactions on a Baltic sandy beach (Hel, Poland): a short-term pilot study. Part II. Driftline effects of succession changes and colonization by beach fauna.Oceanologia44367387
25. Olabarria C,Lastra M,Garrido J. Year: 2007Succession of macrofauna on macroalgal wrack of an exposed sandy beach: Effects of patch size and site.Mar Env Res63194016890281
26. Peterson BJ,Fry B. Year: 1987Stable isotopes in ecosystem studies.Ann Rev EcolSys18293320
27. Rau GH. Year: 1980Carbon-13/Carbon-12 variation in subalpine lake aquatic insects: food source implications.Can J Fish Aquat Sci37742746
28. Rounick JS,Winterbourn MJ. Year: 1986Stable carbon isotopes and carbon flow in ecosystems.Bioscience36171177
29. O'Leary MH. Year: 1988Carbon isotopes in photosynthesis. Fractionation techniques may reveal new aspects of carbon dynamic in plants.Bioscience38328329
30. Osmond CB,Valaane N,Haslam SM,Uotila P,Roksandic Z. Year: 1981Comparisons of ?13C values in leaves of aquatic macrophytes from different habitats in Britain and Finland; some implications for photosynthetic processes in aquatic plants.Oecologia50117124
31. Farquhar GD. Year: 1989Models of integrated photosynthesis of cells and leaves.Phil Trans Roy Soc Lond Series B323357367
32. Phillips DL,Gregg JW. Year: 2001Uncertainty in source partitioning using stable isotopes.Oceologica127171179
33. Healey MC. Year: 1982Juvenile Pacific salmon in estuaries: the life support system.Kennedy VSEstuarine comparisonsNew YorkAcademic Press315341
34. Syvitski JPM,Macdonald RD. Year: 1982Sediment character and provenance in a complex fjord: Howe Sound, British Columbia.Can J Earth Sci1910251044
35. McCutchan JH Jr,Lewis WM,Kendall C,McGrath CC. Year: 2003Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur.Oikos102378390
36. Vander Zanden MJ,Rasmussen JB. Year: 1999Primary consumer d13C and d15N and the trophic position of aquatic consumers.Ecology8013951404


[Figure ID: pone-0010073-g001]
doi: 10.1371/journal.pone.0010073.g001.
Figure 1  Map of the British Columbia, the Strait of Georgia, and Howe Sound showing the two beaches (Furry Creek, North and South: FCN, FCS).

Aerial image of Furry Creek showing the location of the two beaches on either side of the creek (? 2009. Google. Map Data. 2004 Tele Atlas).

[Figure ID: pone-0010073-g002]
doi: 10.1371/journal.pone.0010073.g002.
Figure 2  Beach at Furry Creek (South), Howe Sound, British Columbia at high tide showing wrack line and supralittoral vegetation.

[Figure ID: pone-0010073-g003]
doi: 10.1371/journal.pone.0010073.g003.
Figure 3  Carbon (?13C) and nitrogen (?15N) values of prey taxa in supralittoral, beach wrack, mid-intertidal and low-intertidal zones.

Lines show taxa collected in more than two zones: Acariformes (hatched line), Diptera (dotted line), and Amphipoda (solid line). Values in brackets represent the fraction of terrestrially derived carbon (TC).

[Figure ID: pone-0010073-g004]
doi: 10.1371/journal.pone.0010073.g004.
Figure 4  Carbon (?13C) and nitrogen (?15N) values for chum salmon fry and all prey taxa samples collected in the study.

Habitat associations for the potential prey taxa are denoted by shaded circles or triangles: 1) white circles?=?supralittoral, 2) grey circles?=?high-intertidal/beach wrack, 3) black circles?=?mid-intertidal and 4) black triangles?=?low-intertidal. Chum salmon fry?=?open squares.

[TableWrap ID: pone-0010073-t001] doi: 10.1371/journal.pone.0010073.t001.
Table 1  Stable isotope values of carbon (?13C) and nitrogen (?15N) for primary producers.
Habitat Trophic Group Common Name Species n ?13C ?15N
Supralittoral vegetation Red Alder Alnus rubra 1 ?28.78 ?0.72
Supralittoral vegetation Salmonberry Rubus spectabilis 1 ?30.44 ?0.5
Supralittoral vegetation Nootka Rose Rosa nutkana 1 ?27.77 ?0.09
Supralittoral vegetation Grass Poaceae 1 ?30.04 0.64
Supralittoral vegetation Beach Pea Lathyrus japonicus 1 ?28.23 ?0.44
Supralittoral vegetation Bracket Fungus 1 ?22.71 ?4.2
Supralittoral vegetation Western Red Cedar Thuja plicata 1 ?26.28 ?3.53
Supralittoral vegetation Salal Gaultheria shallon 1 ?28.46 ?3.16
Supralittoral vegetation Sitka Spruce Picea sitchensis 1 ?28.21 ?1.81
Supralittoral vegetation Hairy Cat's Ear Hypochaeris radicata 1 ?31.69 ?0.97
Supralittoral vegetation Black Twinberry Lonicera involucrata 1 ?27.37 ?2.84
Supralittoral vegetation Blueberry Vaccinium spp. 1 ?31.81 ?4.27
Supralittoral vegetation Moss Bryophyta 1 ?26.62 ?0.34
Intertidal macroalgae Japanese Weed Sargassum muticum 1 ?14.64 2.83
Intertidal macroalgae Bleach Weed Prionitis lanceolatus 1 ?16.88 6.39
Intertidal macroalgae Black Tassel Pterosiphonia bipinnata 1 ?19.49 4.67
Intertidal macroalgae Tangle Laminaria spp. 1 ?10.83 6.84
Intertidal macroalgae Green Tuft Cladophora microcladioides 1 ?18.05 5.06
Intertidal macroalgae Rock Weed Fucus gardneri 1 ?16.12 4.47

Terrestrial vegetation was collected in the supralittoral and macroalgae was collected in the intertidal. Shown are common names and species names, number of samples (n), and sample ?13C and ?15N.

[TableWrap ID: pone-0010073-t002] doi: 10.1371/journal.pone.0010073.t002.
Table 2  Stable isotope values of carbon (?13C) and nitrogen (?15N) and proportion of terrestrially derived carbon (TC) for consumers (invertebrates, fish).
Habitat Common Name/Taxa n Mean ?13C Mean ?15N SD ?13C SD ?15N % TC SE TC L 95%CI TC U 95%CI TC
Low-intertidal Amphipoda 6 ?18.94 4.8 2 0.22 23.99 8.39 4.1 43.8
Mid-intertidal Chironomidae 2 ?15.63 6.26 0.51 0.58 0
Mid-intertidal Talitridae 3 ?17 7.89 0.56 0.26 8.1 9.58 0 32.74
Mid-intertidal Amphipoda (Hyale plumulosa) 3 ?16.73 8.25 0.04 0.2 5.92 9.44 0 30.2
Mid-intertidal Diptera 3 ?19.96 9.45 3.04 2.63 32.09 15.82 0 82.5
Mid-intertidal Mussels (Mytilus sp.) 1 ?21.86 6.13 47.46
Mid-intertidal Gastropoda 1 ?15.68 7.24 0
Mid-intertidal Barnacles 1 ?18.17 9.14 17.59
Mid-intertidal Collembola 3 ?18.15 8.85 0.19 0.21 17.42 8.38 0 39
Mid-intertidal Acariformes 1 ?21.29 6.55 42.79
High-intertidal Isopoda 1 ?16.99 7.72 7.94
High-intertidal Talitridae 3 ?17.4 7.24 0.48 0.58 11.35 9.18 0 34.9
High-intertidal Diptera 3 ?17.14 8.29 0.52 0.25 9.24 9.43 0 33.5
Supralittoral Acariformes 1 ?22.71 3.69 54.29
Supralittoral Diptera 3 ?22.56 5.22 0.15 1.49 53.16 5.56 40.6 65.7
Supralittoral Homoptera 3 ?26.76 0.59 0.4 1.32 87.2 5.27 76 98.4
Supralittoral Hymenoptera 3 ?24.44 3.17 0.76 0.57 68.4 6.06 55 81.7
Supralittoral Acariformes 1 ?23.78 0.83 62.97
Marine Chum salmon fry n?=?44 ?19.71 13.94 1.21 1.34 30.03 0.07 0.12 0.48
(Oncorhynchus keta) min ?23.59 10.4 12.78
max ?17.58 15.99 61.5

Shown are values for taxa by habitat (supralittoral, high-intertidal, mid-intertidal, low-intertidal) and common name/taxa and species name. Shown are the number of samples(n), the mean and standard deviation (SD) for ?13C and ?15N, the proportion of TC (%) including the mean, standard error (SE), and upper (U) and lower (L) 95 percentile confidence limits of TC calculated using the mixing model (Phillips and Gregg 2001). For chum salmon fry the minimum and maximum values of ?13C, ?15N, and TC are also shown.

[TableWrap ID: pone-0010073-t003] doi: 10.1371/journal.pone.0010073.t003.
Table 3  Gut contents by fraction of total individuals and fraction of occurrence for 28 chum salmon fry.
Taxa Life stage Fraction of Individuals Fraction of occurrence
Diptera Chironomidae adult 68.04% 17.46%
Diptera Chironomidae pupa 7.48% 7.94%
Oligochaeta adult 5.61% 4.76%
Amphipoda Gammaridae adult 4.30% 7.94%
Amphipoda Corophiidae adult 2.24% 7.94%
Teleost 1.87% 3.17%
Copepoda Harpacticoida adult 1.68% 4.76%
Cirripedia larva 1.50% 6.35%
Diptera Chironomidae larva 1.50% 9.52%
Homoptera Aphididae adult 1.12% 6.35%
Amphipoda Talitridae adult 0.93% 1.59%
Cumacea adult 0.75% 3.17%
Diptera Ceratopogonidae adult 0.56% 1.59%
Diptera Ephydridae adult 0.37% 1.59%
Diptera Heleomyzidae adult 0.37% 1.59%
Chelifera Tanaidacea adult 0.19% 1.59%
Plecoptera Capniidae adult 0.19% 1.59%
Coleoptera Staphylinidae larva 0.19% 1.59%
Diptera Unidentified larva 0.19% 1.59%
Diptera Unidentified adult 0.19% 1.59%
Diptera Empididae adult 0.19% 1.59%
Diptera Sciaridae adult 0.19% 1.59%
Hymenoptera Eulophidae adult 0.19% 1.59%
Arachnida Araneae adult 0.19% 1.59%
n 728 prey items 28 fish

Shown is the taxa and life stage.

Article Categories:
  • Research Article
Article Categories:
  • Ecology
  • Ecology/Ecosystem Ecology
  • Ecology/Marine and Freshwater Ecology
  • Ecology/Plant-Environment Interactions
  • Ecology/Spatial and Landscape Ecology

Previous Document:  Editorial peer reviewers' recommendations at a general medical journal: are they reliable and do edi...
Next Document:  Type-specific cervico-vaginal human papillomavirus infection increases risk of HIV acquisition indep...