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Estuaries and Coasts

, Volume 41, Issue 1, pp 193–205 | Cite as

Using Stable Isotopes to Assess the Contribution of Terrestrial and Riverine Organic Matter to Diets of Nearshore Marine Consumers in a Glacially Influenced Estuary

  • Emily J. WhitneyEmail author
  • Anne H. Beaudreau
  • Emily R. Howe
Article

Abstract

Terrestrial and marine ecosystems in Southeast Alaska are linked by the flow of freshwater from precipitation and glacial runoff, which transports nutrients and organic matter (OM) downstream to estuaries. We examined the contribution of terrestrial-riverine and marine OM to diets of fishes (N = 257, four species) and invertebrates (N = 90, six species) collected from glacially influenced estuaries in Southeast Alaska using multiple stable isotopes (δ13C, δ15N, and δ34S). Multivariate analysis of similarity (ANOSIM) was used to quantify variation in stable isotope composition of consumers across 6 months and three sites with watersheds that differed in their glacier and forest composition. Fishes showed weak differences (ANOSIM R = 0.141) in stable isotope composition among sampling months, moderate differences (ANOSIM R = 0.375) among sites, and strong differences (ANOSIM R = 0.583) among species. Invertebrates showed moderate differences (ANOSIM R = 0.352) in stable isotope composition among sampling months and strong differences among sites (ANOSIM R = 0.710) and species (ANOSIM R = 0.858). We found the greatest differences in stable isotope composition between the two estuary sites with watersheds containing the highest and lowest glacial coverage, indicating that the contribution of allochthonous OM to consumer diets varies across watershed types. Invertebrates collected from the site with the lowest glacial coverage in the watershed were more depleted in δ13C and δ34S, indicating higher use of terrestrial-riverine OM, than those at sites with higher watershed glacial coverage. High variation in stable isotope composition among species, months, and sites underscores the complexity of estuary food web responses to future glacier loss.

Keywords

Carbon source Southeast Alaska Allochthonous subsidy Estuary Terrestrial organic matter Glacier 

Introduction

Rivers deliver a substantial quantity of terrestrial organic matter (OM) to the marine environment (Hedges et al. 1997; Raymond and Bauer 2001), carrying approximately 0.4 Gt of total organic carbon to the global ocean each year (Schlesinger and Melack 1981). While allochthonous subsidies of nutrients and OM delivered from one habitat to another can greatly affect food web structure and dynamics in the recipient habitat (Polis et al. 1997), the importance of terrestrial-riverine OM (combined terrestrial and river material) to nearshore marine food webs may be highly variable across species and ecosystems (Darnaude et al. 2004; Martineau et al. 2004; Franca et al. 2011). For example, in arctic estuarine lagoons covered in sea ice for most of the year, food webs have been found to be heavily reliant on terrestrial carbon sources delivered by small rivers and streams (Dunton et al. 2006, 2012). In studies from other nearshore ecosystems, consumers did not rely heavily on terrestrially derived riverine OM, even in areas where it was most available (e.g., temperate saltmarsh in Massachusetts, USA, Deegan and Garritt 1997; mangrove ecosystem in Andhra Pradesh, India, Bouillon et al. 2000).

The variability and the magnitude of terrestrial-riverine OM delivered to estuaries, and its use by estuarine consumers, will vary as a function of river discharge and adjacent watershed characteristics. For instance, Hoffman et al. (2007) found that young-of-the-year shad in estuaries shifted from a reliance on autochthonous resources during years of low river discharge to primarily terrestrially derived OM during periods of high river flow in Mattaponi River, Virginia. Across the Atlantic, in the northwest Mediterranean, variation in sole fishery yields was linked to variable terrestrial particulate organic matter (POM) contributions to benthic food webs arising from fluctuating river flow (Darnaude et al. 2004). Abrantes et al. (2013) found that the importance of terrestrial OM to estuary consumers depends on watershed characteristics, with greater use in estuaries with adjacent watersheds dominated by C4 vegetation compared to those with predominantly C3 vegetation. Use of allochthonous OM can also vary among species based on their ontogeny, foraging behavior, habitat use, and the quality of the OM (Polis et al. 1997; Howe and Simenstad 2015). Collectively, these studies reveal that the relative importance of terrestrial and freshwater-derived OM varies among and within systems. Because estuarine consumers may show variable responses to allochthonous inputs and site characteristics, understanding how changes in terrestrial-riverine OM will affect estuarine food webs requires a place-based approach (Franca et al. 2011; Abrantes et al. 2013).

This study evaluated the contribution of terrestrial-riverine OM to consumers in estuaries of Southeast Alaska (SEAK), along the eastern Gulf of Alaska. Substantial annual freshwater flow (849 km 3 year−1; Hill et al. 2015), fed in part by runoff from glaciers (Larsen et al. 2015), transports high yields of OM to the Gulf of Alaska’s nearshore marine ecosystems. Of the estimated 0.13 ± 0.01 Tg of dissolved organic carbon contributed by glacial runoff, over 75% is likely to be bioavailable (Hood et al. 2009). Along the eastern Gulf of Alaska, the Pacific coastal temperate rainforest (PCTR) contributes substantial OM to downstream habitats (Fellman et al. 2010, 2015). Shallow soils and steep valley walls along the PCTR further facilitate transport of OM to local estuaries (Wipfli and Gregovich 2002). Given the permeable boundaries between the terrestrial and marine environments (Polis et al. 1997) and the landscape features that link these environments, terrestrial OM may provide an important subsidy to estuarine consumers along the PCTR. This hypothesis, however, has not been widely addressed in glacially influenced estuaries of SEAK (but see Arimitsu 2016 for examination of riverine OM use in a tidewater glacier system).

Estuaries in SEAK have limited anthropogenic development but subject to rapid change due to melting and retreating glaciers (Larsen et al. 2007). In SEAK, the proximity of glacial headwaters to the coast results in short transit times of freshwater and OM to estuaries. The average length of streams with glacial headwaters in SEAK is just 10 km, two orders of magnitude shorter than the average for the Western USA (O’Neel et al. 2015). This geographical compression increases the velocity of river effluent and alters the way in which sediment and other particulates are delivered to estuaries (Syvitski et al. 2005). These attributes set SEAK estuaries apart from other longer, non-glacially influenced systems. We focused on a nearshore marine ecosystem in SEAK that is fed by a variety of watershed types, from largely glaciated to predominantly precipitation-fed systems (Hood and Berner 2009; Fellman et al. 2010). Seasonal patterns of discharge, total annual discharge, and dissolved organic carbon concentrations in stream water vary as a function of watershed glacier coverage (Hood and Berner 2009); therefore, the delivery of terrestrial-riverine nutrients to estuaries in this region may vary across watershed types.

The objectives of this study were to (1) gain insight into the contribution of terrestrial-riverine and marine OM sources to the diets of estuary fishes and invertebrates using multiple stable isotopes (δ13C, δ15N, and δ34S) and (2) assess variation in stable isotope ratios of fish and invertebrate consumers across six sampling months and three sites that differed in watershed composition, from glaciated to forested. To address these objectives, we used a multiple stable isotope tracer approach to assess dietary sources for invertebrate and fish consumers and examined stomach contents of the fishes (e.g., Darnaude et al. 2004; Pasquaud et al. 2007). Given that terrestrial OM enters marine food webs through benthic pathways (Darnaude et al. 2004; Bell et al. 2016), we hypothesized that invertebrates would show greater use of terrestrial-riverine OM than higher trophic level fish. We further expected anadromous species to incorporate greater proportions of terrestrial-riverine OM than strictly marine species due to their use of both freshwater and marine habitats during their early life history. River flow into estuaries varies seasonally and is impacted by watershed characteristics, such as the extent of glacial and forest coverage (Hood and Berner 2009; Neal et al. 2010; Fellman et al. 2014). As such, we hypothesized that there would be higher contributions of terrestrial-riverine OM during the peak summer discharge period for glacier-fed watersheds (two sites) and during the peak late spring and early fall discharge period for a predominately rain-fed watershed (one site).

Methods

Study Sites

This study was conducted at three estuary sites near Juneau, Alaska, USA: Cowee Creek estuary (CC; 58.68° N, 134.95° W), Eagle River estuary (ER; 58.54° N, 134.85° W), and Mendenhall River estuary (MR; 58.33° N, 134.61° W; Fig. 1). These sites are located along Lynn Canal, a 140-km fjord in SEAK in the PCTR, which receives an average of 140 cm of precipitation annually at sea level (Fellman et al. 2015). Across sites, watershed composition ranges from 63% glaciated and 8% forested (MR) to 13% glaciated and 57% forested (CC; Table 1; Fellman et al. 2014). The confluence of the Herbert River and Eagle River flows into the ER estuary site. Together, the Herbert and Eagle River watersheds are intermediate to MR and CC in glacial and forest coverage (Table 1). CC has more extensive low gradient floodplain channels compared to either MR or ER (CBJ 2016). The delivery of freshwater helps determine the physical characteristics of these estuaries. Peak discharge during our sampling period occurred in mid-summer for each of the rivers, owing to higher contributions of glacial meltwater with warmer air temperatures (Whitney 2016). Additionally, the summer of 2014 (June, July, and August) was particularly wet in Juneau, receiving 62 cm out of the 175 cm of precipitation that fell in 2014 (National Weather Service 2015).
Fig. 1

Study site locations in Juneau, Alaska. Watershed boundaries are outlined in black

Table 1

Watershed characteristics for the Cowee Creek, Eagle River, and Mendenhall River watersheds

Site characteristics

Cowee Creek

Eagle Rivera

Mendenhall River

Watershed area (km2)b

110

276

222

River length (km)c

12.7

6.8–8.4

9.4

Glacier cover (%)b

13

48–49

63

Forest cover (%)b

57

23–25

8

Wetland coverage (%)b

5

2–5

1

Mean stream elevation (m)b

166

46–180

17

Mean stream slope (degrees)b

10

7–9

2.6

Mean estuary temperature (°C)d

10.56

10.66

9.8

Mean estuary salinity (‰)d

19.14

20.82

16.69

Mean estuary turbidity (NTU)d

13.57

13.49

17.73

aThe Herbert River joins the Eagle River approximately 1 km before the Eagle River estuary. The characteristics presented are for the combined Herbert and Eagle River watersheds

bFellman et al. (2014)

cUSDAFS (2014)

dWhitney (2016)

Sampling Protocol

Estuarine fishes were collected monthly during negative low tides from April to September 2014 by beach seine (15 m × 2.4 m net with 6.3 mm square mesh). Sampling occurred in the estuary adjacent to the river mouth along shallow, sloping, intertidal areas with fine sand and mud sediments and interspersed cobble. Based on the catch composition during pilot sampling in 2013, four abundant estuarine fish species representing different feeding guilds and life history types were selected for stable isotope and stomach content analysis: Pacific staghorn sculpin (Leptocottus armatus), starry flounder (Platichthys stellatus), Dolly Varden (Salvelinus malma), and juvenile coho salmon (Oncorhynchus kisutch). These taxa represent anadromous (coho salmon and Dolly Varden) and marine species (staghorn sculpin and starry flounder) that exhibit both opportunistic and generalist feeding behaviors. For stable isotope analysis, a target sample size of five individuals per sampling event was reached for starry flounder [mean length = 210 mm total length (TL) ± 43] and staghorn sculpin (mean length = 162 mm TL ± 39.8); however, fewer samples were retained for Dolly Varden (mean length = 183 mm fork length (FL) ± 52)]and juvenile coho salmon (mean length = 93.3 mm FL ± 11.84) due to their low abundance or absence in some sites or months (Table 2). Up to 25 individuals of each species were retained for stomach content analysis per sampling month (Table 3).
Table 2

Sample sizes by fish species, site, and month for stable isotope analysis

2014

Species

Site

April

May

June

July

August

September

Total (n)

Pacific staghorn sculpin Leptocottus armatus

CC

5

5

5

5

5

5

30

ER

5

5

5

5

5

5

30

MR

5

5

5

5

5

5

30

Starry flounder Platichthys stellatus

CC

5

5

5

5

5

5

30

ER

5

5

5

5

5

5

30

MR

5

5

5

5

5

5

30

Dolly Varden Salvelinus malma

CC

0

0

5

5

4

5

19

ER

0

5

5

5

5

0

20

MR

4

0

2

1

1

0

8

Coho salmon Oncorhynchus kisutch

CC

0

2

6

0

0

0

8

ER

0

5

5

2

0

0

12

MR

0

5

4

1

0

0

10

Table 3

Diet composition of focal fish species presented as percent composition by weight (%W) and percent frequency of occurrence (%FO)

 

Coho salmon Oncorhynchus kisutch

Dolly Varden Salvelinus malma

Pacific staghorn sculpin Leptocottus armatus

Starry flounder Platichthys stellatus

(n = 94)

(n = 136)

(n = 402)

(n = 270)

%W

%FO

%W

%FO

%W

%FO

%W

%FO

Crustacean

59.6

75.5

50.4

81.6

5.0

53.0

6.9

22.2

Gammaridae

9.7

66.0

31.1

80.9

20.3

75.6

25.5

44.4

Insecta

26.9

91.5

2.8

66.2

4.0

18.2

0.2

6.3

Isopoda

0.9

11.7

0.3

24.3

19.2

44.8

48.2

8.5

Mollusca

0.3

7.4

0.2

23.5

3.0

36.1

14.6

54.4

Mysidae

0.3

18.1

12.0

48.5

34.4

64.9

0.7

7.8

Polychaeta

0.2

18.1

0.1

21.3

3.1

67.2

3.4

52.6

Teleostei

2.0

29.8

3.0

44.9

9.2

37.8

0.3

4.4

Other

0.2

19.1

0.2

19.9

1.7

20.1

0.1

4.1

Based on the results of the stomach content analysis, common prey of the four fishes were collected for stable isotope analysis. The majority of prey items across fish species were intertidal species that could be sampled during low tides. Intertidal invertebrates were collected by hand and dip net during low tides following beach seining in June and August. Primary consumers collected included blue mussels (Mytilus trossulus) and isopods (Gnorimosphaeroma oregonensis). Omnivores included gammarid amphipods (suborder Gammaridea) and invertebrate predators included Crangon shrimp (Crangon franciscorum franciscorum), hairy hermit crab (Pagurus hirsutiusculus), and nereid polychaete worms (family Nereididae).

To provide a baseline for comparison with fish and invertebrate consumer stable isotope composition, we collected terrestrial-riverine and marine OM sources for stable isotope analysis. Estuarine phytoplankton and POM samples were unsuccessfully collected due to high silt burdens in nearshore waters. Samples of the attached marine macroalgae, Fucus distichus evanescens, were collected by hand from intertidal rocks in June, July, and August. This species was selected as a representative marine macroalgae because it is a common and abundant intertidal species and the dominant marine vegetation observed at our sites; although eelgrass (Zostera marina) is present in the region, it was absent from our sites. Our sites also lack extensive marsh macrophytes with wetlands occupying less than 5% of the watershed for each site (Fellman et al. 2014; Table 1). This produces a distinct dichotomy between marine OM sources and terrestrial and riverine sources in our system.

Suspended terrestrial-riverine POM ≥250 μm, including leaf litter, was collected for stable isotope analysis approximately 1–2 km upstream of the river mouths adjacent to our study sites using a 250-μm mesh drift net. The net was anchored underwater close to the riverbed for 0.25–24 h, depending on the amount of material collected in the net (Wipfli and Gregovich 2002). Samples were collected opportunistically from CC in May, July, and September and from MR in September as a part of a larger project examining POM in streams. Samples collected upstream of the Herbert River/Eagle River confluence were primarily composed of sediment and low OM concentrations, precluding stable isotope analyses. Therefore, for ER, we used published stable isotope values for POM and leaf litter collected upstream from our ER site in the lower Herbert River in 2012 (Fellman et al. 2015; raw data provided by Jason Fellman, University of Alaska Southeast, March 2016).

Stable Isotope Measurements

Fish were rinsed in deionized water and muscle tissue was consistently excised from above the lateral line posterior to the head to reduce bias associated with biochemical heterogeneity, such as in lipid composition of different tissues (Michener and Kaufman 2007). Tissue samples were frozen until preparation for stable isotope analysis. Lipids were not extracted from tissue samples; however, the low lipid content of our samples (C/N < 3.5 for 99% of fish samples) limited potential impacts on our analyses (Post et al. 2007). We used muscle tissue from invertebrates, removing internal organs (Hill and McQuaid 2011) and hard structures to minimize carbonate contamination in samples (Goering et al. 1990). Multiple small invertebrates were combined to create a single sample as needed to attain the minimum weight for analysis. POM samples were rinsed and sorted to remove insects and excess sediment. Fucus sp. samples were rinsed in deionized water and epiphytes removed prior to drying. All samples were placed in a drying oven at 60 °C for 48–72 h and dried to a stable weight.

In preparation for stable isotope analysis, each sample was ground into a homogeneous powder using a mortar and pestle. Samples were weighed to the nearest 0.01 mg using a micro-analytical balance and packaged in tin capsules. Isotopic ratios of samples were analyzed for carbon (δ13C), nitrogen (δ15N), sulfur (δ34S) using a Delta V Advantage continuous flow Isotope Ratio Mass Spectrometer (Thermo Fisher) coupled with a NC2100 elemental analyzer (Carlo Erba) at the Colorado Plateau Stable Isotope Laboratory, Northern Arizona University, Flagstaff, Arizona, USA (http://www.isotope.nau.edu/index.html). Weight based carbon to nitrogen ratios were also calculated.

Isotope ratios are reported using the δ notation, which indicates the ratio of the heavy isotope to the light isotope relative to an international standard. It is defined by the formula:
$$ \delta X(\mathit{{\mbox{\fontencoding{U}\fontfamily{wasy}\selectfont\char104}}})=[({R}_{sample}/{R}_{standard})- 1]\cdot 1000 $$

where X is the heavy isotope and R is the ratio of 13C/12C, 15N/14N, or 34S/32S. The standards for 13C and 15N were Vienna-PeeDee Belemnite (V-PDB) and air, respectively, while Vienna Canyon Diablo Troilite (V-CDT) was the standard for 34S. The analytical precision was found to be ±0.07‰ for δ13C and ±0.08‰ for δ15N (N = 115) based upon replicate measurements of an internal peach tree leaf standard obtained from the National Institute of Technology. For δ34S, replicate measurements of bovine liver standard had an analytical error of ±0.14‰ (N = 150). Paired aliquots of tissue samples were submitted to the external laboratory to measure analytical error. The median difference between paired aliquots was 0.14‰ for δ34S (N = 40), 0.07‰ for δ13C (N = 41), and 0.06‰ for δ15N (N = 41), which are consistent with the error levels reported for other estuarine consumers (Howe and Simenstad 2011).

Stomach Content Analysis of Fishes

We analyzed stomach contents of the four fish species to supplement stable isotope analysis and gain insight into the specific prey items fish were consuming. In the laboratory, stomachs were removed from fish specimens and preserved in 80% ethanol. We performed stomach content analysis following standard methods in fish feeding ecology (e.g., Chipps and Garvey 2007). The total weight (blotted wet weight, to the nearest 0.01 g) of stomach contents was recorded and individual prey items were sorted and identified to the lowest taxonomic level possible. For each prey item, we recorded blotted wet weight (to the nearest 0.01 g) and length (to the nearest 0.1 mm) for intact items. We characterized the diet composition of the four fish species using the standard metrics frequency of prey occurrence and percent composition by weight (Chipps and Garvey 2007). Frequency of occurrence (FO) was calculated as the number of sampled stomachs containing a given prey taxon, divided by the total number of sampled stomachs by species. The proportion by weight (%W) was calculated as the weight of a given prey taxon divided by the total weight of all prey consumed by the predator species.

Statistical Analyses

Stable isotope composition reflects food habits of organisms in the preceding weeks to months (Buchheister and Latour 2010; Heady and Moore 2013). Variation in stable isotope composition among consumer species, sites, and sampling months can be interpreted relative to basal sources (i.e., primary producers). Marine sources tend to be enriched in 13C, 34S, and 15N compared to terrestrial or freshwater sources (Connolly et al. 2004; Montoya 2007), thereby creating a terrestrial to marine continuum in stable isotope composition. Species with a stable isotope composition along this continuum rely on varying proportions of the marine and terrestrial sources.

We used multivariate analyses to compare consumer isotope composition (δ13C, δ15N, and δ34S) by site, month, and species. Principal component analysis (PCA) was used to explore species and site relationships. Analysis of similarity (ANOSIM) was used to test for differences in the stable isotope composition of consumers among sites and months. We performed a three-way ANOSIM on a similarity matrix constructed using a Euclidean distance measure (Clarke et al. 2014) to examine overall species, site, and month differences for fishes and invertebrates separately. Differences across sites and months were examined individually by fish and invertebrate species using a two-way ANOSIM with site and month as factors. ANOSIM produces an R statistic, which indicates the degree of separation between groups; R values range from 0 to +1. The greater the distance from zero, the more different groups are from one another. Weak differences were indicated by R values ≤0.25, R values 0.26 to 0.50 indicated moderate differences, and strong differences between groups were indicated by R values ≥0.51 (Creque and Czesny 2012). P values are also generated by ANOSIM; however, we did not rely on them for inference as these values are permutation-based and, therefore, strongly affected by sample size (Clarke et al. 2014). Multivariate analyses were conducted in PRIMER v.7.0 (Plymouth Marine Laboratories; UK, Clarke and Gorley 2015).

Differences in the stable isotope composition of estuarine consumers can be interpreted relative to the composition of the source material (DeNiro and Epstein 1978; Peterson et al. 1985). Differences in carbon and sulfur isotope ratios indicate assimilation of different OM sources by consumers, while nitrogen isotope ratios reflect the trophic level of the organism as well as OM sources (DeNiro and Epstein 1978; Peterson and Fry 1987). Sulfur isotopes are less commonly used but can help distinguish between coastal sources when carbon isotope composition is similar (Connolly et al. 2004). In our case, the sulfur isotope ratio supported the separation of primary sources indicated by the carbon and nitrogen isotope ratios. To visualize the position of estuarine consumers in relation to source isotope polygons (Fig. 2), we assigned trophic enrichment (fractionation) factors (TEF, mean ± SD) based on McCutchan et al. (2003) for non-lipid extracted muscle tissue (1.1 ± 1.3 ‰ for δ13C and 2.8 ± 1.4 ‰ for δ15N). The TEFs were then adjusted for consumers based on trophic position. To capture two trophic level shifts, we followed the methods of Vander Zanden and Rasmussen (2001) to sum the TEF and variances. The final TEF values used for fish were 1.5 ± 1.7 ‰ for δ13C and 5.1 ± 2.1 ‰ for δ15N.
Fig. 2

Stable isotope biplots by fish species adjusted for trophic enrichment factors. Mean source values adjusted for trophic enrichment factors are shown by black points. Error bars indicate ±1 SD of the combined source and trophic enrichment factor SD. Staghorn sculpins (a), starry flounders (b), Dolly Varden (c), and coho salmon (d)

Results

Isotopic Separation of Allochthonous and Autochthonous Primary Sources

The isotope composition for the marine macroalgae, Fucus sp., showed a distinct marine signature (Table 4). The δ13C values for Fucus sp. (−16.9 ± 1.1‰) were slightly enriched compared to values for phytoplankton (−19.8 ± 1.4‰) collected in April and May 1986, in Auke Bay, in close proximity to our MR site (Goering et al. 1990). Further, the δ34S in Fucus sp. (−22.7 ± 0.2‰) aligns with values for seawater sulfate; generally, δ34S is between 20 and 22‰, with an ocean average of 21.75 ± 0.02‰ (Szabo et al. 1950). In contrast to Fucus sp., the POM samples reflect a mixture of terrestrial and riverine sources (Finlay 2001). The C/N ratios of the POM, ranging from 22.6 to 34.1, are consistent with the range of values reported for terrestrial C3 plants and freshwater macrophytes (Finlay and Kendall 2007). The POM samples, though variable, were substantially depleted in δ13C values (−28.0 ± 1.0‰) and δ15N values (0.5 ± 1.4‰) relative to Fucus sp. (Table 4).
Table 4

Stable isotope signatures of organic matter sources

Source

Marine OM (Fucus sp.)

Mean ± SD

Terrestrial-riverine OM (POM)

Mean ± SD

δ13C

−16.9 ± 1.1 (n = 18)

−28.0 ± 1.0 (n = 5)

δ15N

5.8 ± 0.5 (n = 18)

0.5 ± 1.4 (n = 5)

δ34S

22.7 ± 0.2 (n = 18)

−1.2 ± 4.6 (n = 3)

Differences in Diet among Consumers

We analyzed δ13C, δ15N, and δ34S values in muscle tissue samples of fishes (n = 257, four species) and invertebrates (n = 99, six species; Table 5). The intertidal invertebrates sampled were enriched in δ13C relative to the POM samples and generally grouped closely to Fucus sp. values (Table 5 and Fig. 3). Invertebrate species were strongly different from one another (three-way ANOSIM; R = 0.858, p < 0.001) with differences in δ13C and δ34S contributing the most to the observed differences. The stable isotope composition of invertebrates showed lower variation across samples of the same species compared to fish, likely due to combining multiple individuals in a single sample. Marine fishes, staghorn sculpins (δ13C = −16.0 ± 1.5‰), and starry flounders (δ13C = −15.6 ± 1.3‰), were enriched in δ13C relative to anadromous Dolly Varden (δ13C = −20.4 ± 3.3‰) and juvenile coho salmon (δ13C = −26.5 ± 5.6‰); all four fish species were enriched in δ13C relative to POM (−28.0 ± 1.0‰; Fig. 2). Coho salmon carbon isotope composition was highly variable; however, there was no significant relationship with fish length (R 2 = 0.05, p = 0.21). The mean sulfur isotope composition of the fish species ranged from 9.5 ± 5.2‰ for coho salmon to 17.0 ± 1.2‰ for staghorn sculpin and followed a similar pattern as carbon (Table 5 and Fig. 3). The smallest fish we analyzed, coho salmon, had the lowest δ15N value (δ15N = 10.1 ± 1.9‰) and staghorn sculpins had the highest (δ15N = 13.1 ± 0.7‰). Dolly Varden (δ15N = 12.5 ± 1.2‰) and starry flounders (δ15N = 11.9 ± 0.6‰) were intermediate in nitrogen isotope composition. Fish and invertebrate species were enriched by 7–13‰ relative to the δ15N of POM (0.5 ± 1.4‰).
Table 5

Mean stable isotope values (‰) by species and site

Species

n

δ13C

δ15N

δ34S

Fig. 3 label

CC

ER

MR

CC

ER

MR

CC

ER

MR

Leptocottus armatus

90

−17.0 (1.8)

−15.4 (0.8)

−16.0 (1.2)

12.9 (0.7)

12.8 (0.5)

13.5 (0.7)

18.0 (0.7)

16.6 (1.1)

16.3 (1.0)

1

Platichthys stellatus

90

−16.1 (1.1)

−15.7 (0.9)

−15.1 (1.5)

11.6 (0.4)

11.8 (0.4)

12.3 (0.6)

17.6 (0.4)

16.2 (1.1)

15.0 (1.1)

2

Salvelinus malma

47

−19.1 (0.7)

−20.6 (1.9)

−22.7 (7.0)

13.0 (0.8)

12.4 (1.1)

11.6 (1.6)

17.1 (1.1)

15.6 (2.3)

13.6 (2.9)

3

Oncorhynchus kisutch

30

−24.1 (2.5)

−25.2 (3.9)

−30.0 (7.6)

10.7 (2.2)

9.9 (1.7)

9.5 (1.8)

13.0 (2.2)

9.2 (4.6)

6.9 (6.2)

4

Mytilus trossulus

18

−19.0 (0.5)

−18.2 (0.6)

−17.4 (0.5)

7.5 (0.5)

7.7 (0.2)

7.7 (0.3)

19.3 (0.5)

19.3 (0.4)

17.9 (0.6)

10

Gnorimosphaeroma oregonensis

18

−17.4 (0.2)

−18.4 (1.4)

−16.7 (0.7)

9.3 (0.6)

9.7 (0.6)

9.6 (0.1)

20.2 (0.2)

20.1 (0.4)

19.2 (0.6)

9

Gammaridea

18

−18.0 (0.7)

−17.7 (0.3)

−16.5 (0.2)

8.4 (0.2)

9.1 (0.4)

9.6 (0.2)

18.8 (0.5)

19.1 (0.6)

18.0 (0.6)

8

Crangon franciscorum

17

−14.8 (0.5)

−14.2 (0.9)

−15.0 (0.9)

11.1 (0.4)

11.0 (0.7)

11.2 (0.5)

18.0 (0.5)

16.4 (2.2)

16.3 (0.6)

5

Pagurus hirsutiusculus

14

−16.1 (0.4)

−16.3 (0.1)

−15.0 (0.5)

11.1 (0.1)

11.0 (0.5)

10.9 (0.3)

20.3 (0.4)

19.7 (0.5)

18.0 (0.7)

6

Nereididae

14

−17.8 (1.1)

−17.0 (0.6)

−13.4 (0.4)

9.0 (0.6)

10.8 (0.6)

10.9 (0.9)

20.1 (0.3)

18.4 (1.0)

14.6 (1.0)

7

CC Cowee Creek estuary, ER Eagle River estuary, MR Mendenhall River estuary

Fig. 3

Stable isotope biplots with source materials (dark gray), invertebrates (light gray), and fishes (black). Numbers identity specific species listed in Table 5. Raw values (not adjusted for trophic enrichment) were averaged across month and site. Error bars show the standard error for each isotope

There were strong differences in stable isotope composition among fish species (three-way ANOSIM; R = 0.583, p < 0.001), indicating variation in their use of allochthonous and autochthonous resources. The greatest differences among the four fishes were between starry flounders and juvenile coho salmon (three-way ANOSIM pairwise; R = 0.838, p < 0.001). The PCA plot, based on stable isotope composition of fish, showed a separation of marine species (staghorn sculpin and starry flounder) from anadromous species (Dolly Varden and coho salmon). This pattern is supported by ANOSIM pairwise tests, which indicated greater species differences between marine and anadromous groups (R = 0.750 to 0.838, p < 0.001) than within each group (R = 0.401 to 0.406, p < 0.001). Stomach content data reflect the stable isotope results, showing a greater contribution of aquatic and terrestrial insects to the diets of anadromous species compared to marine species. Of the four species, juvenile coho salmon showed the highest contribution of insects to the diet by weight (24.5–45.4%, depending on site; Table 3). Depending on the site, 83.3–95.5% of the sampled coho salmon and 12.5–71.4% of the sampled Dolly Varden contained insects in their stomachs (Table 3). The proportion of sampled staghorn sculpin and starry flounder containing insects was 11.2–25.2 and 4.5–9.4%, respectively, depending on the site (Table 3). Neomysis mercedis, a mysid species found in fresh and brackish waters, were consumed by all four species but in particular by staghorn sculpins with 64.9% of the sampled stomachs containing mysids.

Seasonal and Spatial Variation in δ13C and δ34S

When we examined all fish species together for evidence of seasonal variation in the relative importance of terrestrial-riverine OM, we found a weak difference among sampling months (three-way ANOSIM; R = 0.141, p < 0.001). Individually, starry flounders showed weak differences among months (two-way ANOSIM; R = 0.203, p < 0.001). There was monthly variation in the δ13C and δ34S values of starry flounder samples of up to 3.2 and 4‰, respectively, but with no clear seasonal trend. Staghorn sculpins showed weaker differences across months (two-way ANOSIM; R = 0.094, p = 0.005) without a discernable temporal trend. Dolly Varden (two-way ANOSIM; R = 0.085, p = 0.079) and coho salmon (two-way ANOSIM; R = 0.172, p = 0.074) showed no significant temporal variation between April to September. Invertebrates showed moderate differences in stable isotope composition between sampling months (three-way ANOSIM; R = 0.352, p < 0.001). These differences were driven by isopods and nereids that were depleted in δ13C (0.9–1.3‰ depletion) and δ15N (0.6–0.7‰ depletion) in June relative to their counterparts sampled in August.

There were moderate differences among sites in fish consumers’ use of OM (three-way ANOSIM; R = 0.375, p < 0.001). We found the strongest differences between fish from MR and CC (three-way ANOSIM, CC/MR pairwise; R = 0.551, p < 0.001). The site-specific patterns of OM use differed between marine and anadromous species. For both staghorn sculpins and starry flounders, ER fish more closely resembled fish from CC than fish from MR. For Dolly Varden and coho salmon, ER fish more closely resembled fish from MR than fish from CC. Marine fish from MR were enriched in δ13C and δ15N relative to those from CC (Table 5). Conversely, anadromous fishes from MR were depleted in δ13C and δ15N relative to those from CC (Table 5). Invertebrate stable isotope composition showed strong site differences (three-way ANOSIM, R = 0.710, p < 0.001). As with fish, the samples from CC and MR were the most distinct (three-way ANOSIM; CC/MR pairwise test; R = 0.866, p < 0.001). Overall, invertebrates were generally enriched in δ13C and δ15N at MR compared to CC.

Discussion

Stable Isotope Composition of Estuarine Consumers

Variation in OM use among marine and anadromous fishes as well as invertebrates indicated that a multispecies approach is needed to understand OM use in estuaries. Stable isotope composition was strongly different between marine and anadromous fishes. Anadromous fishes showed greater individual variation compared to marine fishes, reflecting differences in foraging, with some individuals’ carbon isotope ratios more closely resembling those of terrestrial-riverine OM than others. Stable isotope composition of staghorn sculpins and starry flounders aligned more closely with Fucus values, suggesting a greater use of marine OM sources compared to Dolly Varden and coho salmon. Anadromous fish move between habitats based on life stage (e.g., out-migrating coho salmon) or to take advantage of feeding opportunities, such as Dolly Varden making feeding forays into freshwater in pursuit of salmon eggs (Jaecks and Quinn 2014). This movement likely contributed to the observed variability and at times high allochthonous OM use. In contrast, starry flounders and staghorn sculpins showed less variability in stable isotope composition and were more enriched in δ13C than anadromous species (Fig. 2), suggesting similar feeding behaviors among individuals with a focus on marine prey. The separation between marine and anadromous species shows that there are variable patterns of terrestrial-riverine and marine OM use among fish species residing in estuaries. This result aligns with research in other parts of Alaska, which indicates that allochthonous OM use by estuarine consumers, such as sea birds, can vary substantially by species (e.g., Dunton et al. 2006; Arimitsu 2016).

For juvenile coho salmon that likely recently left the freshwater, the timing of their outmigration and estuarine residence time are confounding factors in interpreting their variable stable isotope composition. As juvenile coho salmon transition from freshwater to the marine environment, their diet shifts (e.g., Duffy et al. 2010), and as muscle tissue turnover occurs with growth, the stable isotope composition of muscle tissue follows this shift. Thus, the stable isotope composition of juvenile coho salmon in estuaries may vary depending on whether the composition has stabilized to the new environment or whether the transition is still occurring. Additionally, the presence of hatchery released juvenile coho salmon near ER may contribute to variability in stable isotope composition. Only about 7% of the locally produced hatchery coho salmon are marked (DIPAC 2015), making it challenging to distinguish between hatchery and wild fish in the estuary. Moreover, strong negative carbon isotope composition of coho salmon were well below measured values of riverine POM, likely reflecting feeding on a source not sampled in this project. Literature values suggest freshwater periphyton or phytoplankton as δ13C depleted sources to coho salmon (Marty and Planas 2008). Additionally, the δ15N values for coho and other species were slightly enriched relative to the marine source even after adjustment for trophic enrichment (Fig. 2), suggesting additional marine sources with a higher δ15N value than we measured.

Marine invertebrate use of allochthonous OM was also highly variable. Some species (gammarids and blue mussels) were more enriched in δ13C compared to other species (isopods, Crangon shrimp, hermit crab, and nereids). Terrestrial OM may be incorporated to a greater extent by benthic and epibenthic species at the base of food webs, as suggested by more depleted δ13C in marine invertebrates compared to marine fish. This finding is supported by research indicating that dissolved OM is readily incorporated by primary consumers (Franca et al. 2011; Bell et al. 2016). Epibenthic and benthic prey make up a large proportion of the diets of staghorn sculpins and starry flounders from these sites; however, they also consume a variety of juvenile fishes (Table 3), which may dilute the allochthonous OM signature. We recognize that the life history, body size, and species examined may alter our understanding of the role of terrestrial-riverine OM sources in estuaries.

Seasonal Patterns in Stable Isotope Composition

Given the fluctuation in river discharge at each of our three sites over the course of the sampling period (Whitney 2016), we expected that there would be temporal shifts observed in the stable isotope data. Invertebrates were more depleted in δ13C in June (below peak discharge) compared to August (near peak discharge; Whitney 2016) based on stable isotope composition. This result contrasted with our hypothesis that allochthonous OM use would be highest following peak flows but is supported by research indicating that benthic algae in glacial rivers and macroinvertebrate productivity has been found to be highest in spring and fall, outside the window of peak glacial runoff (Milner and Petts 1994; Brittain and Milner 2001). This suggests that riverine OM may be more available to estuarine consumers outside of summer months and could explain δ13C depletion in invertebrates from June compared to August.

Temporal shifts in fish stable isotope ratios were less pronounced and did not show a decrease in δ13C and δ34S, which would indicate greater allochthonous OM use, following peak flow periods. While there were slight shifts in the stable isotope ratios of staghorn sculpins and starry flounders over the sampling period, no directional trend was detected. No significant shifts were identified for Dolly Varden or coho salmon. The lack of trends may be a result of the high in situ productivity of the estuary. Given the abundance of food resources available, allochthonous OM appears to be incorporated in fish diets at a consistent level rather than following predicted seasonal trends in availability. Complete tissue turnover in fish muscle can take weeks to months (e.g., Heady and Moore 2013). However, isotopic turnover due to dietary changes can be detected before the isotopic composition of muscle tissue is equilibrated with the diet (Buchheister and Latour 2010). Given the extended period of higher freshwater discharge in the study estuaries between July and September (Whitney 2016) relative to earlier sampling months, we expected there would be sufficient time under the higher flow regime for any associated diet shifts to be detectable in muscle tissue; however, no defined seasonal pattern was detected. For coho salmon, although the combined carbon, nitrogen, and sulfur composition did not show a significant temporal trend, δ13C isotope values increase as summer progressed [May (mean ± SD) −28.88 ± 6.41; June −26.02 ± 4.15; July −19.42 ± 1.46]. This increase reflects dietary shifts that occur with smolting and increased estuarine residence time and, in turn, higher consumption of marine prey.

Site Characteristics Contributing to Allochthonous OM use

Differences in stable isotope ratios of consumers across sites suggest that watershed characteristics may affect diets of consumers in adjacent estuarine habitats. The stable isotope ratios of invertebrates and fishes separated samples from MR and CC. CC invertebrates were depleted in δ13C relative to invertebrate samples from MR, indicating invertebrates used more terrestrial-riverine OM at CC. Site differences among fish were variable by species. The results of this study augment other research showing that estuarine OM use is affected not only by river length and flow (Deegan and Garritt 1997; Darnaude et al. 2004; Hoffman et al. 2007) but also by watershed characteristics, such as glacial and forest coverage. The CC and MR watersheds differ in glacial and forest coverage as well as watershed area (Table 1). Higher forest coverage at CC may lead to greater export of terrestrial OM and, in turn, greater incorporation of this OM source into the diets of estuarine invertebrates; however, the site differences likely reflect the combined effect of multiple watershed features. Watershed features such as forest coverage, slope, and elevation change can all impact the type of material moving downstream at each site (Wipfli and Gregovich 2002; Lisi et al. 2013). Research has shown that certain types of OM may be more beneficial to consumers and that consumers can preferentially take up specific OM sources when multiple sources are present (Martineau et al. 2004).

Despite site differences, the contribution of allochthonous OM to marine fish diets was relatively low across sites. Low incorporation of allochthonous OM by consumers near river mouths, where the contribution of terrestrial OM is expected to be the highest (Deegan and Garritt 1997; Vinagre et al. 2008), may be in part related to discharge and circulation patterns that affect retention of OM in these estuaries. During higher flow periods, such as those occurring during summer months (Weingartner et al. 2009), river flow can efficiently export OM out of the immediate vicinity of estuarine consumers (Peterson et al. 1994; Eyre 1998). The rapid export of OM and particulates offshore has also been seen in river systems with few distributary channels (Syvitski et al. 2005; Howe 2012). For example, the north channel of the Skagit River in Puget Sound, Washington, is highly channelized and research has shown that marsh OM contributes <10% to the diet of bivalves (Macoma spp.) in the estuary (Howe 2012). The short distance from headwaters to the estuary in our study systems may cause terrestrial-riverine OM to be transported in a manner resembling more developed, channelized systems.

The type and quality of the OM that is exported into the study estuaries may also have affected the observed OM use by estuarine consumers. While glacial rivers have been shown to transport large quantities of bioavailable dissolved organic carbon (Hood et al. 2009; Fellman et al. 2010), the export of macroinvertebrates and detritus can be highly variable among stream systems (Wipfli and Gregovich 2002). The high C/N ratio measured for POM samples collected from CC and MR suggest that river POM is predominately detrital and refractory material (Martineau et al. 2004) and may be of lower quality to consumers (Finlay and Kendall 2007). The quality of the OM exported to the marine environment is linked to the detrital conditioning of terrestrial material. As decaying leaf litter and detritus pass through wetlands, microbes colonize on the surface of the litter and break down cellulose making this material available to higher trophic levels (Boon et al. 2006; Spencer et al. 2007). The rapid transit times of these short systems and cold stream temperatures may limit the level of microbial conditioning of OM and in turn limit the use of allochthonous OM by estuarine consumers.

In addition to short river lengths, the lack of expansive wetlands (≤5% watershed coverage) at each of the sites influences the strength of food web linkages. In systems with large wetlands and salt marshes, vascular plants, such as Spartina, can be a dominant carbon source for estuarine consumers (Peterson and Howarth 1987; Hoffman et al. 2007). The limited wetlands at our study sites greatly reduce the potential OM contribution of this source. In this sense, our system resembles mangrove and sea grass dominated systems where OM sources can be broken into two clear categories (Vaslet et al. 2012). Furthermore, the limited wetland habitat available to these sites and in turn the reduced contribution of a wetland OM source intermediate to terrestrial-riverine OM and marine OM may explain why sulfur stable isotopes were not required to separate our sources. Without wetland plants as a strong intermediate source, our terrestrial-riverine OM and marine OM sources could be separated by carbon and nitrogen alone.

Conclusions

In coastal SEAK, there is abundant terrestrial OM input to streams, with the potential for this material to be transported downstream into estuaries. Yet, our results indicate that estuarine consumers’ use of terrestrial and riverine material was variable across species, with anadromous fishes being more depleted in δ13C and δ34S and consuming a higher proportion of aquatic and terrestrial insects than marine fishes. Differences among species, months, and sites underscore the reality that estuarine food web responses to allochthonous subsidies can be complex and dynamic. As glaciers in SEAK continue to thin and retreat (Larsen et al. 2007), the watershed characteristics of these study sites, such as glacial and forest coverage and river flow, will change. Over longer time scales, reduced glacial coverage and increased forested areas may result in greater incorporation of terrestrial-riverine OM in the diet of estuarine consumers. This study provides the opportunity to contrast current terrestrial-riverine OM use by estuarine consumers with food web connectivity under future conditions.

Notes

Acknowledgements

We thank Asia Beder, Doug Duncan, Ragnhildur Fridriksdottir, Melissa Rhodes-Reese, and many field volunteers for their assistance in collecting fish and invertebrate samples. Thanks to Carolyn Bergstrom, Franz Mueter, and two anonymous reviewers for their insightful comments on earlier drafts of this manuscript. This study was funded by the Alaska Experimental Program to Stimulate Competitive Research (EPSCoR) NSF award no. OIA-1208927, Alaska Sea Grant (award no. RR/14-01), and the University of Alaska Fairbanks.

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Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Emily J. Whitney
    • 1
    Email author
  • Anne H. Beaudreau
    • 1
  • Emily R. Howe
    • 2
  1. 1.College of Fisheries and Ocean SciencesUniversity of Alaska FairbanksJuneauUSA
  2. 2.The Nature ConservancySeattleUSA

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