The overall goal of this study was to investigate the effects of glacial influence on the diets of nearshore invertebrates, specifically the use of terrestrial subsidies, by assessing shifts in food resource use and trophic niche space over a range of watersheds with different glaciation levels and across seasonal discharge regimes. In contrast to a recent surge in the literature supporting the substantial use of terrestrial resources in marine invertebrate diets, the results of this study indicate that consumer diets were largely decoupled from terrestrial sources. Both Gr/De and Su/FF invertebrate taxa fed predominantly on marine sources across glacial influence and discharge regimes, although Gr/De relied more prominently on macroalgae and Su/FF on POM. While there were differences in resource space occupied by the two consumer groups, there were few patterns consistent with overall glacial influence or discharge period for either group. In contrast, drivers of consumer stable isotope composition were associated with unique watershed characteristics rather than linearly with glaciation. This combination of results suggests that terrestrial habitat characteristics may influence marine primary producers in the study system, but dietary augmentation with terrestrial resources may not be necessary for marine invertebrate consumers in a highly productive marine system like Kachemak Bay.
Stable Isotope Composition Of Consumers
The enrichment of the Gr/De group in 13C relative to the Su/FF group, indicating reliance on different food sources, is coherent with diet differences between the groups in other nearshore systems. For example, the typical δ13C values of grazing limpets of the genus Lottia are often 1–2‰ higher than the suspension-feeding genus Balanus when examined across the geographic spread from Puget Sound, Washington to the Lower Cook Inlet, Alaska (Ruesink et al., 2014; Siegert et al., 2022), consistent with feeding on an isotopically heavier food source. The taxa within the Gr/De group sampled in this study (Littorina spp. and Lottia spp.) are known to feed upon a mix of red, green, and brown algae (Kozloff, 1996). The range of macroalgal δ13C values was larger than any other diet source in this study, reflecting the wide range of macroalgal stable isotope values driven by environmental conditions, their thallus forms, growth rates, and carbon concentrating mechanisms (Wiencke & Fischer, 1990; France, 1995; Giordano et al., 2005). While δ13C isotope values of macroalgae within this study ranged from − 10‰ to -31‰, macroalgal isotopic variability may be even larger than demonstrated here, where we only considered four common intertidal macroalgae; the total diversity of macroalgae present in the system is considerable (Konar et al., 2010). Gr/De consumers were only positioned within the − 13‰ to -21‰ range, indicating their preferential feeding on macroalgae with higher δ13C values such as many brown algae (e.g., Siegert et al., 2022). While this study focused on intertidal macroalgae, the study system also contains abundant subtidal kelp forests (Spurkland & Iken, 2011), which could provide large amounts of brown algal biomass with heavier δ13C values from senescent or dislodged plants to the intertidal (Miller & Page, 2012); this is known to be a major food source for limpets elsewhere (Bustamante et al., 1995). An alternative, unsampled carbon source of high δ13C values could be microphytobenthos (MPB). MPB is an organic film in marine systems consisting of diverse microalgal assemblages and microorganisms such as cyanobacteria, diatoms, flagellates, and settled macroalgal spores as well as trapped detrital matter (MacIntyre et al., 1996). This biofilm covering rocky substrate is an accessible food source for grazing organisms. Although difficult to measure, previous studies in Alaska have reported mean MPB δ13C values of -16.9 ± 1.2‰ (McTigue & Dunton, 2017). This overlaps well with the Gr/De consumer values and is similar to the higher range of macroalgal δ13C values sampled in this study and, thus, poses as another viable endmember to explain the isotope range of the Gr/De group.
The taxa within the Su/FF group (Balanus spp. and Mytilus trossulus) generally feed on a mix of phytoplankton, small zooplankton, and POM. POM is a mixed source that combines non-living matter from the cellular components of plankton, bacteria, and protists with detrital components from plants, algae, and other marine organisms (Volkman & Tanoue, 2002). Especially the large portion of microalgae in POM leads to lower δ13C values compared to macroalgae (Lowe et al., 2014); the δ13C values of POMmix in this study were often 1–3‰ lower than macroalgae, despite the occasional overlap of the two sources in stable isotope space (Fig. 4). This greater ingestion of POM compared to macroalgae was reflected in the smaller δ13C values of the Su/FF than the Gr/De group. Still, macroalgal detritus has been shown to contribute to suspension-feeding bivalve diets (Duggins et al., 1989; Howe & Simenstad, 2015; Both et al., 2020), particularly during periods (Langdon & Newell, 1990) or locations (Siegert et al., 2022) of low phytoplankton abundance.
Both Gr/De and Su/FF groups showed similar decreasing trends of δ13C values with increasing percent watershed glaciation during all discharge periods. These patterns could be explained by either a change in diet or a glacially-driven decrease in the δ13C value of a diet source across watersheds. There is no indication of diet change with watershed glaciation in our mixing model estimates of diets. In contrast, the δ13C values of autotrophs (e.g., phytoplankton, macroalgae) are determined by uptake fractionation during photosynthesis (Keller & Morel, 1999), which is influenced by cell physiology (Popp et al., 1998), ambient environmental conditions (Burkhardt et al., 1999), and the availability of dissolved inorganic carbon (DIC) (Sharkey & Berry, 1985; Lammers et al., 2017). The mobilization of geogenic DIC is especially high in high-latitude, watersheds with glacial coverage due to physical weathering associated with glacial movement (Tranter & Wadham, 2013), and the DIC yield is often greater in watersheds of higher glacial coverage relative to those of lower or no coverage (Jenckes et al., 2022). This pattern is consistent with the positive relationship between the flux of DIC and glacial coverage of watersheds in this study (Appendix I, Table A1). As a result, the greater flux of DIC from watersheds with glacial coverage is likely to decrease the δ13C values of marine phytoplankton, because carbon stable isotope discrimination in most marine algae is inversely related to the concentration of DIC in the aqueous pool (Sharkey & Berry, 1985). Because the proportion of sources contributing to POMestu were rather consistent across sites and seasons, including only very small contributions from terrestrial material, these results suggest that the slight decrease in POMestu δ13C values may stem from differences in the δ13C of local, estuarine phytoplankton that were unaccounted for in our offshore, marine phytoplankton samples.
Estimated Source Contributions To Invertebrate Consumers And Pom
The highly similar diet contributions of POMmix, macroalgae, and terrestrial plants across sites to both feeding groups suggests that these diet sources are consumed in similar proportions irrespective of glacial coverage of the watershed. Though our mixing model of POMestu showed greater terrestrial contributions at some sites of higher glacial coverage, there was no linear increase, and the overwhelmingly dominant (~ 90%) marine component strongly indicates that seasonal or site-specific differences in the composition of POMmix have minimal impact on consumer diets. Therefore, differences in consumer stable isotope composition among sites were not explained by clear changes in the proportion of sources, especially terrestrial sources, contributing to their diets (Fig. 5, Table 4). We had hypothesized that the terrestrial source contribution to consumer diets would vary among sites and discharge periods, considering that discharge volume and composition were expected to have higher terrestrial exports in watersheds with higher glacial cover and during peak discharge, which would influence the available resource pool. However, contrary to that expectation, the proportion of terrestrial contribution to both feeding groups’ diets was minor (7–10%) and consistent across discharge periods. These results suggest that the temporal uncertainty associated with tissue turnover and informative prior choice is minimal. Additionally, the inclusion of small amounts of terrestrial components in consumer diets could at least in part be an artifact of the model, because all sources included in the model will be attributed by default some level of contribution (Parnell et al., 2013; Phillips et al., 2014). It is also possible that the prevalence of terrestrial OM was underestimated in these models because we used live land plants as endmembers, rather than riverine POM, which ultimately is the degraded plant material transported in rivers to the coastal system. During this transport, the fractionation associated with degradation and mixing with soil organic matter can result in a ~ 2‰ increase in the δ13C values of riverine POM by the time it is discharged into the ocean (Fiers et al., 2019). δ13C values of riverine POM in glacially-influenced systems in Southeast Alaska were − 28‰ (Whitney et al. 2018), a value that overlaps with those of the upland plants in our study. While we do not have riverine POM carbon isotope data, the potential increase in δ13C would still position the riverine POM outside the trophic niche space of the consumers in this study (Fig. 4), although the calculated proportion of terrestrial matter in the consumer diet may have been slightly higher. Lastly, by including POMestu as part of our POMmix endmember, with POMestu including a small terrestrial component, we likely accounted for a small intake of OMterr in the diets of consumers.
Marine or predominantly-marine sources (macroalgae, POMmix,) contributed substantially (~ 90% combined sources) to the diets of both feeding groups across space and time. The consistently high proportion of marine sources in consumer diets may represent a preference for higher-quality food derived from marine environments. Marine algae (macroalgae and phytoplankton) are more nutritious relative to terrestrial plant litter, in part due to a higher content of polyunsaturated fatty acids (Guo et al., 2016) and the absence of lignocellulosic structural compounds found in terrestrial plants (Wells et al., 2017). Lignins are aromatic polyphenols present in vascular plant cells that are only made bioavailable through extracellular enzyme hydrolysis by microbes (Weiss et al., 1991), a process considered a rate-limiting step in the remineralization of organic carbon in the marine environment (Arnosti, 2011). The absence of lignin in most marine algae promotes proportionately greater amounts of directly bioavailable organic matter for marine consumers. As a result, phytoplankton and macroalgae are evidently a major source of nutrition for these organisms. Similarly, the major contribution of these marine sources instead of terrestrial components to POMmix presents it as high-quality food as well. The use of a diverse source array of macroalgae, phytoplankton, and POM by consumers aids in their resilience to the loss of, or variability in, a particular food source and contributes to ecosystem stability (Rooney & McCann, 2012; Siegert et al., 2022). Sufficient availability of these sources may reduce the need for consumers to supplement their diets with lower-quality terrestrial resources. This idea is in line with optimal foraging theory, where the quality of a subsidy is important to the foraging strategies of animals, because they seek to optimize their digestible intake (forage quality), while minimizing the energetic cost of finding and handling food (Pyke 1984). Also, consumer life history traits (e.g., breeding success) are directly related to the availability of preferred food resources (Österblom et al., 2008) and, thus, could be negatively impacted by the reduced nutritional value of critical diet items. Kachemak Bay is a highly productive embayment (Chester & Larrance, 1981), characterized by high macroalgal diversity and abundance (Konar et al., 2010), high macroalgal growth rates (Spurkland & Iken, 2012) and high phytoplankton production (Griffith et al., 1982). Given that these resources seem plentiful relative to OMterr, it is plausible that they are sufficient to be the primary food resources for these consumers.
Trophic niche space, quantified in this study as SEV (Table 5), represents the range of resources used by an organism and is a metric of resilience to disturbance and resource use among groups (e.g., competition among taxa) (Layman et al., 2007). The Gr/De group’s SEV were consistently greater than those of the Su/FF group. This evidenced the dietary flexibility of the Gr/De group to include both macroalgae and POMmix in their diets. The Gr/De group feeds on macroalgae when POMmix is seasonally limited and then increases POMmix, when it becomes available, while the Su/FF group nearly exclusively feeds on POMmix. The higher trophic plasticity of the Gr/De group may render them more resilient than the Su/FF group to changes in basal resources. It is advantageous for the Gr/De group to be able to move to obtain desired resources, whereas truly sessile organisms, such as barnacles, are subject to the transport of food within reach. On the global scale, motile taxa tend to outperform range-restricted taxa in response to glacial retreat (Cauvy-Franié & Dangles, 2019). It has been suggested that increased precipitation with advanced climate change will weaken phytoplankton and even macroalgal-based trophic pathways in intertidal food webs in favor of a more pronounced detrital pathway (Vinagre et al., 2018). A similar pattern could be expected in this high-latitude environment, where both precipitation as well as glacial melt are predicted to increase for the foreseeable future (O’Neel et al., 2015). It seems that the Gr/De group may be more resilient and better pre-adapted to such changes. A possible decline in the more specialized Su/FF group could lead to a loss of food web complexity, functionality, and stability of coastal food webs, leading to functional homogenization and a loss of productivity in coastal systems (Hawkins et al., 2008; Clavel et al., 2011). Conversely, it has been proposed that climate-related warming trends in polar and cold-temperate systems could also increase biodiversity in intertidal food webs through migrating species (Gauzens et al., 2020), although it remains to be seen if that applies to glacially-influenced systems, such as our study region, and how this might influence energy transfer to higher trophic levels.
Watershed Drivers Of Consumer Stable Isotope Composition
For estuarine consumers, the supply of marine sources is largely driven by dynamic processes, including light availability, nutrients, currents (Sommer, 1989), and static attributes, such as substrate and wave exposure (Konar et al., 2016). Supply of OMterr to the coastal environment is governed by the composition of terrestrial characteristics, including vegetation, soils, lithology (Tiwari et al., 2017), and the watershed attributes that contribute to their mobilization and transport, such as hydrologic processes and catchment structure (Godsey et al., 2009). Once discharged, the distribution of allochthonous OMterr to coastal consumers primarily depends on local hydrodynamics and the sinking rate of materials (Howe et al., 2017; Lehmann et al., 2002). As a result, the OMterr available to different invertebrate feeding types uniquely varies relative to the contributing watershed’s source and transport attributes. The dbRDA model results indicated that the two feeding groups associate with overall similar watershed drivers in this study system, yet, with different responses to these drivers. Specifically, the Gr/De group’s stable isotope composition was regulated primarily by factors associated with transport (ruggedness) and sourcing (river length), while the Su/FF group was regulated primarily by factors associated with sourcing (TSS, percent vegetation).
Despite the mixing model results showing that terrestrial sources were virtually absent from POMestu samples and only constituted a small portion of consumer diets, the flux of terrestrial materials can still be important for coastal food webs. OMterr influx can stimulate coastal productivity through pathways other than direct ingestion by primary consumers. For example, the Gr/De groups’ stable isotope composition was driven most by river length and ruggedness. Gr/De at sites with shorter streams (JAK, GRW) were distinct (higher δ13C values) from those at sites with longer streams (HAL, WOS; lower δ13C values). This may reflect the available carbon stocks stored in river floodplains, which contain the majority of carbon found in most river corridors (Dunne et al., 1998; Sutfin et al., 2016). Rivers with lower gradients and longer reaches tend to have larger floodplains than rivers with higher gradients and shorter reaches. The distribution of organic carbon in floodplains varies based on local vegetation, upstream inputs, and river-basin morphology (Sutfin et al., 2016), and deposits of inorganic materials to the lower reaches are often dominated by smaller sediment size classes (e.g., glacial silt; Wolman & Leopold, 1957). These organic and inorganic materials are mobilized downstream during high-flow events and, when washed into the estuary, the organic carbon fraction can stimulate the growth of heterotrophic bacteria in the nearshore estuary (Sutfin et al., 2016; Xu et al., 2018). Incidentally, the Gr/De group may consume heterotrophic bacteria assimilated within periphytic algae (Haglund & Hillebrand, 2005). Furthermore, inorganic materials from the riverine pulse may act as ballast to organic marine aggregates (e.g., marine snow) suspended in the coastal water column and deposit them into intertidal regions for consumption (Ross et al., 2022). Suspended marine aggregates of biogenic origin also host pronounced microbial communities (Alldredge & Silver, 1988), which, like the consumption of heterotrophic bacteria, would influence consumer δ13C values when consumed based on the carbon source used in microbial respiration (Jennings et al., 2017).
The Su/FF group was more prominently affected by the factors related to sourcing (TSS and percent vegetation). TSS is the chief export of mountainous watersheds and represents the amalgamation of the rugged land surface, topographically limited vegetation, short fluid transit times, and glacial erosion (Anderson, 2005; Lafrenière & Sharp 2005, Wheatcroft et al., 2010). TSS is an expression of glacial influence because it generally increased with the glacial coverage of the sites in this study. This relationship between Su/FF stable isotope composition and the TSS flux most likely represents intermediate pathways, such as marine phytoplankton responding to the input of nutrients and other trace minerals (Arrigo et al., 2017). TSS concentration is a strong driver in the adsorption capacity of soluble reactive nutrients, such as iron and phosphorous, which desorb during the mixing of fresh and saline waters (Nguyen et al., 2019). Desorbed soluble reactive nutrients can then stimulate strong phytoplankton production (Arrigo et al., 2017), serving as food for the Su/FF group. This glacial input of nutrients can lead to depleted 13C values in organic matter (Calleja et al., 2017), which could explain the lower δ13C values we observed in consumers in watersheds with higher glacial cover.
Interpretation of the percent vegetation vector for both feeding groups is less straightforward. In theory, it may represent a variety of processes, such as the direct subsidy of vegetal detritus to consumer diets, the enhancement of intermediate production of heterotrophic bacteria, or the control of vegetation on the transport of particulates in watercourses. Firstly, vegetal detritus as a subsidy to diets was unsupported in the mixing model analysis. Second, if heterotrophic bacteria were a major part of both groups’ diets, one would expect to see an increase in δ15N of consumers, because of the added trophic step the remineralization of recalcitrant OM by heterotrophic bacteria introduces (Bell et al., 2016). There were no apparent differences in the δ15N of either group among sites (Fig. 4, Table 2) and thus, no clear evidence of a lengthened food chain by heterotrophic bacteria. However, a lengthened food chain would rely on heterotrophic bacteria as a relatively consistent food resource for the consumers; the fact that we did not see an increase in δ15N does not rule out intermittent microbe consumption or a lag effect in consumer δ15N values based on consumer tissue turnover times that we may not have captured with our sampling strategy. Lastly, the site-specific confidence ellipses for Su/FF were generally ordered by glaciation, except for the HAL site, which supports the opposing influence of TSS in stream water, and the effect of percent vegetation in reducing the delivery of solids to streams.