Freshwater Biology (2014)
doi:10.1111/fwb.12415
Depth gradients in food-web processes linking habitats in large lakes: Lake Superior as an exemplar ecosystem MICHAEL E. SIERSZEN*, THOMAS R. HRABIK†, JASON D. STOCKWELL‡, ANNE M. COTTER*, JOEL C. HOFFMAN* AND DANIEL L. YULE§ *U.S. Environmental Protection Agency, Office of Research and Development, National Health and Ecological Effects Research Laboratory, Mid-Continent Ecology Division, Duluth, MN, U.S.A. † University of Minnesota – Duluth, Duluth, MN, U.S.A. ‡ University of Vermont, Burlington, VT, U.S.A. § U.S. Geological Survey, Lake Superior Biological Station, Ashland, WI, U.S.A
SUMMARY 1. In large lakes around the world, depth-based changes in the abundance and distribution of invertebrate and fish species suggest that there may be concomitant changes in patterns of resource allocation. Using Lake Superior of the Laurentian Great Lakes as an example, we explored this idea through stable isotope analyses of 13 major fish taxa. 2. Patterns in carbon and nitrogen isotope ratios revealed use of both littoral and profundal benthos among populations of most taxa analysed regardless of the depth of their habitat, providing evidence of nearshore–offshore trophic linkages in the largest freshwater lake by area in the world. 3. Isotope-mixing model results indicated that the overall importance of benthic food-web pathways to fish was highest in nearshore species, whereas the importance of planktonic pathways increased in offshore species. These characteristics, shared with the Great Lakes of Africa, Russia and Japan, appear to be governed by two key processes: high benthic production in nearshore waters and the prevalence of diel vertical migration (DVM) among offshore invertebrate and fish taxa. DVM facilitates use of pelagic food resources by deep-water biota and represents an important process of trophic linkage among habitats in large lakes. 4. Support of whole-lake food webs through trophic linkages among pelagic, profundal and littoral habitats appears to be integral to the functioning of large lakes. These linkages can be disrupted though ecosystem disturbance such as eutrophication or the effects of invasive species and should be considered in native species restoration efforts. Keywords: aquatic habitats, food web, Great Lakes, stable isotopes, trophic linkages
Introduction A growing body of work identifies water depth as an organising factor in the ecology of large, deep lakes. In Russia’s Lake Baikal, fish species are distributed according to depth; most notably, 29 species of sculpins have differentiated into shallow-water, benthic and pelagic species (Sideleva, 1996, 2000). Baikal’s remarkable assemblage of 240 species of amphipods and 207 species of oligochaetes is also organised according to depth (Kozhov, 1963; Snimschikova & Akinshina, 1994), with
benthos being food-limited and lower in abundance in abyssal zones compared to the nearshore (Martin, Martens & Goddeeris, 1999). In the Great Lakes of Africa, prolific species radiation has resulted in colonisation of a variety of habitats. Of the hundreds of species of cichlids in each of Lakes Tanganyika, Malawi and Victoria, strong depth associations may be found among shallow, offshore and benthic species (Fryer & Iles, 1972; Coulter, 1991; Konings, 2007). In the Laurentian Great Lakes of North America, cottid, coregonine and salmonine fish species are distributed across nearshore and deepwater
Correspondence: Michael E. Sierszen, U.S. Environmental Protection Agency, Mid-Continent Ecology Division, 6201 Congdon Blvd., Duluth, MN 55804, U.S.A. E-mail:
[email protected] Published 2014. This article is a U.S. Government work and is in the public domain in the USA.
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habitats (Smith, 1964; Bronte et al., 2003; Eshenroder, 2008; Gamble et al., 2011a,b). The dominant macroinvertebrate taxa are also distributed according to depth, with the amphipod Diporeia historically concentrated in nearshore zones (Evans, Quigley & Wojcik, 1990; Lozano, Scharold & Nalepa, 2001), and the migratory malacostracan Mysis diluviana dominant in deeper (≥100 m) habitats (Johannsson, 1995; Pothoven, Fahnenstiel & Vanderploeg, 2004). These depth-specific patterns in consumers and their prey in large lakes suggest that there may also be depth structure in the major food-web pathways supplying energy to nearshore and offshore fishes. For example, the importance of benthic food-web pathways to fish nutrition may be higher in nearshore species than in those occupying deeper offshore habitats. Alternatively, benthic contributions to deepwater consumers may be unrelated to the abundance of benthic invertebrates. Although benthos abundance was low in deep Lake Superior habitats, the use of benthic resources by Mysis diluviana did not decline with depth, as increases in use of detritus offset declines in predation on benthic invertebrates (Sierszen et al., 2011). It remains to be resolved whether, and how, the nature of trophic linkages that support fish varies across habitats in large lakes. Stable isotope techniques are especially well suited for tracing food-web pathways. Isotopic differences among food sources make it possible to quantify their nutritional contributions (e.g. support from benthic versus planktonic sources; Hecky & Hesslein, 1995). In Lake Superior, stable isotope signatures of benthos and plankton diverge; d15N of Diporeia increased by approximately 4& from nearshore to deep (300 m) habitats, whereas d15N of zooplankton remained relatively constant. d13C of Diporeia declined sharply between 0 and 40 m, reflecting a gradient in their carbon source from periphyton-fixed C (d13C = 15&) to phytoplankton C (d13C = 28&; Sierszen, Peterson & Scharold, 2006). One implication of these patterns is that they may provide useful indicators of the sources of energy to higher consumers across depths. One would expect that benthivores and planktivores would have depth-isotope patterns similar to those of their primary foods and that consumers that rely on a mixture of benthic and pelagic prey would have an intermediate pattern. Consistent with this expectation, the d15N-depth relationship of Mysis diluviana had a slope between those of zooplankton and Diporeia, and Mysis was found to obtain approximately half of its nutrition from each source (Sierszen et al., 2011). In addition to revealing sources of nutrition, stable isotope techniques can be used to identify processes
influencing the ecology of consumers. Across depths in Lake Superior, the C and N stable isotope signatures of Diporeia revealed that periphyton production (at depths 150 m), sequentially supported benthic secondary production (Sierszen et al., 2006). Peak Diporeia abundance is found in the zone of highest deposition of fresh phytodetritus (Auer et al., 2013). Lake Superior has a food web considered the least disturbed among the Laurentian Great Lakes (Schmidt, Vander Zanden & Kitchell, 2009; Zimmerman & Krueger, 2009). By understanding its trophic structure and processes and comparing these features with other large lakes, we may use it as an exemplar to identify common properties of healthy large lake systems that are important to protect or re-establish in efforts to restore the functionality of disturbed systems. Here, we examine patterns in stable isotope ratios across depths to reveal sources of nutrition to fishes of different habitats. We also quantify the contributions of major food-web pathways to nearshore and deepwater fishes in Lake Superior and consider the ecological processes shaping the observed patterns. Finally, we examine the utility of isotope–depth relationships as indicators of the pathways supporting consumers.
Methods Site description Lake Superior of the Laurentian Great Lakes has a surface area of 82 100 km2 and is the largest freshwater lake in the world by area. Its maximum depth is 406 m, and average depth is 147 m. Nearshore habitats (Fig. 1) are occupied by pygmy whitefish (Prosopium coulteri), slimy sculpin (Cottus cognatus), lake whitefish (Coregonus clupeaformis) and lean lake trout (Salvelinus namaycush namaycush). Bloater (Coregonus hoyi), spoonhead sculpin (Cottus ricei) and burbot (Lota lota) range to offshore regions of intermediate depth, and profundal zones (150–400 m) contain deepwater sculpin (Myoxocephalus thompsonii), kiyi (Coregonus kiyi) and siscowet lake trout (Salvelinus namaycush siscowet). Humper lake trout (Salvelinus namaycush) is a morphotype that is principally distributed on large offshore reefs (Eshenroder, 2008). Cisco (Coregonus artedi) and rainbow smelt (Osmerus mordax) are pelagic planktivores, with rainbow smelt abundant in nearshore habitats and cisco occupying the offshore. The dominant macroinvertebrate taxa are also distrib-
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
Large lake habitat linkages
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Lean lake trout, burbot, bloater spoonhead sculpin, rainbow smelt Pygmy whitefish lake whitefish, slimy sculpin
10
10
Humper lake trout, Diporeia
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8
6
6
4
4
2
2
Mysis g m–2
12
Diporeia g m–2
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Siscowet lake trout, kiyi, cisco deepwater sculpin, Mysis diluviana
14
0
0 0
100
200
300
Depth, m
Fig. 1 Ranges of peak abundance of the major fish taxa in Lake Superior. Also illustrated are patterns in the depth distribution of biomass (wet mass m2) of the benthic amphipod Diporeia (filled circles) and the migratory malacostracan Mysis (triangles). Biomass data were adapted from Sierszen et al. (2011).
uted according to depth (Fig. 1). The abundance of benthos (principally Diporeia spp.) peaks in the nearshore, at depths of 40–60 m, and Mysis diluviana is dominant in depths of 100 m or more (Scharold, Lozano & Corry, 2004; Sierszen et al., 2006).
Sample collection and analyses Fish were collected from Lake Superior from nine nearshore ( number of isotope systems + 1). All possible combinations of each source are examined in small increments, and combinations that sum to the observed mixture within a small tolerance (ca. 0.1&) are considered feasible solutions. Each multivariate solution (i.e. each combination of source contributions that satisfies the model tolerance) is equally valid. However, each source has a univariate distribution of possible contributions, and the frequency of occurrence of a particular contribution in that distribution reflects the likelihood of that proportional contribution (Semmens et al., 2013). Correct reporting of model results requires that the distribution of feasible solutions be described (Phillips & Gregg, 2003). When a distribution of source contributions is well constrained (i.e. it has a relatively narrow range of possible contributions) and symmetrical, the mean (i.e. the most frequent contribution of that source) describes the most likely
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contribution, and the standard deviation may be used to express dispersion about the mean. Distribution characteristics determine whether the mean, median or mode reflects the most likely value, and whether standard deviations, confidence intervals and quartiles are best used to express dispersion. Because source distributions are often skewed, we used medians and quartiles to describe source (i.e. prey) contributions and in calculations of nutrition obtained through benthic food-web pathways (below). We used linear and nonlinear regression (SigmaPlot 9, Systat Software, Inc., San Jose, CA, U.S.A.) to test for significant changes in isotope signatures with depth of capture (median depth of trawl tow) of specimens. We used significant (P < 0.05) regressions to estimate d15N and d13C of fishes and invertebrates at 50 m intervals and used those values in the mixing model. For non-significant regressions, we used mean isotope ratios. For invertebrate prey, we used depth-isotope relationships established in Sierszen et al. (2011) that were based on 2005 and 2006 collections of Mysis diluviana, Diporeia spp., zooplankton of two size fractions (63–160 and >160 lm) and oligochaetes. Calculating isotope mixing across trophic levels requires knowledge of trophic fractionation of isotopes (i.e. the 15N and 13C enrichment of a consumer relative to its food). We used a nitrogen isotope fractionation factor of 3.4& (Cabana & Rasmussen, 1994) and carbon isotope fractionation of 1.0& (Vander Zanden & Rasmussen, 2001). Because d15N more clearly discriminated benthos and plankton than did d13C we generally used d15N in a single-isotope mixing approach, but included d13C for a dual-isotope approach when it improved the precision of our estimates. As recommended by Phillips & Gregg (2003), output values were restricted to those that conformed with known dietary information to provide well-constrained results. The dietary constraints were as follows: for slimy sculpin, pygmy whitefish and bloater, contributions from Diporeia exceed those from Mysis; for spoonhead sculpin, deepwater sculpin, lake whitefish and siscowet, contributions from Mysis exceed those from Diporeia (Becker, 1983; Gamble et al., 2011a,b). We did not identify appropriate dietary constraints for the other fish species, and none were applied. For each fish species, the prey included in the mixing model (Table 2) were those identified as major food items in an extensive diet study on Lake Superior (Gamble et al., 2011a,b), with additional support from Eschmeyer & Bailey (1955); Becker (1983); Selgeby (1988); Hoff, Link & Haskell (1997); Johnson et al.
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
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Table 2 Taxa analysed (abbreviations as in Fig. 2), range of total lengths of fish analysed, depths (at 50 m intervals) at which isotope-mixing model was run, and estimated nutritional contributions [median (1st–3rd quartile)] of diet items Taxon (abbreviation)
Total length (mm)
Depths (m)
Prey item proportions, median and range of 1st–3rd quartiles Mysis: 0.07 (0.03–0.11) Diporeia: 0.31 (0.25–0.36) Zooplankton: 0.04 (0.01–0.07) Oligochaetes: 0.57 (0.54–0.62) Mysis: 0.07 (0.03–0.13) Diporeia: 0.35 (0.28–0.42) Zooplankton: 0.04 (0.01–0.07) Oligochaetes: 0.49 (0.45–0.53) Mysis: 0.68 (0.57–0.78) Diporeia: 0.23 (0.11–0.34) Oligochaetes: 0.12 (0.10–0.14) Mysis: 0.46 (0.32–0.61) Diporeia: 0.11 (0.05–0.20) Zooplankton: 0.16 (0.10–0.24) Oligochaetes: 0.19 (0.09–0.31) Mysis: 0.84 (0.81–0.86) Diporeia: 0.17 (0.14–0.19) Mysis: 0.34 (0.20–0.33) Diporeia: 0.12 (0.06–0.17) Oligochaetes: 0.30 (0.15–0.45) Fish Eggs: 0.22 (0.10–0.48) Mysis: 0.78 (0.74–0.81) Zooplankton: 0.22 (0.20–0.24) Mysis: 0.43 (0.19–0.73) Diporeia: 0.09 (0.05–0.16) Zooplankton: 0.44 (0.29–0.56) Mysis: 0.39 (0.18–0.68) Zooplankton: 0.39 (0.18–0.66) YOY smelt: 0.22 (0.12–0.30) Mysis: 0.22 (0.14–0.29) Rainbow Smelt: 0.29 (0.24–0.34) Cisco: 0.24 (0.12–0.36) Lean Lake trout: 0.26 (0.17–0.35) Mysis: 0.41 (0.35–0.45) Diporeia: 0.13 (0.07–0.19) Kiyi: 0.28 (0.27–0.30) Deepwater sculpin: 0.20 (0.19–0.21) Mysis: 0.25 (0.10–0.43) Sculpin: 0.64 (0.60–0.67) Terrestrial insects: 0.08 (0.03–0.14) Mysis: 0.56 (0.35–0.82) Smelt: 0.15 (0.06–0.27) Kiyi: 0.10 (0.04–0.18) Lake Trout: 0.09 (0.04–0.16)
Pygmy whitefish (pygmy)
44–135
50–150
Slimy sculpin (slimy)
25–96
50–150
Spoonhead sculpin (spoon)
28–101
50–150
Bloater (bloat)
84–312
50–200
Lake whitefish (lwf)
88–462
50–57
Deepwater sculpin (dws)
26–132
50–300
Kiyi (kiyi)
42–264
50–300
Rainbow smelt (rbs)
34–179
50–300
Cisco (cisco)
52–416
50–300
Lean lake trout (lean)
28–748
50–200
Siscowet lake trout (siscowet)
92–725
50–300
Humper lake trout (humper)
214–548
41
Burbot (burbot)
140–436
50–200
(2004) and Sitar et al. (2008). Although those studies quantified diet proportions, we used the mixing model to estimate the proportions of each item. For humper lake trout, we used diet information provided by the Michigan Department of Natural Resources (Shawn Sitar, Marquette Fisheries Research Station, Marquette, MI, U.S.A.). Terrestrial insects were identified as a frequent food item for humper lake trout, for which we used mean values of d15N = 0.36& and d13C = 28.8& obtained from analyses of forest tent caterpillars
(Malacosoma disstria) which we collected near the Duluth EPA Mid-Continent Ecology Division. The proportional contributions of each food item (overall median, first and third quartiles) are reported across all depths analysed per species. The identification of benthic and planktonic food-web pathways and their contributions to fish were based on the primary consumers at the origin of each pathway (i.e. benthic and planktonic invertebrates). This avoided logical inconsistencies that could arise from defining the
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
Large lake habitat linkages pathways according to primary producers. For example, although profundal benthic invertebrates feed on detrital phytoplankton (Fitzgerald & Gardner, 1993), it is logical to consider deepwater sculpin feeding on Diporeia as a benthic trophic interaction. It also clarifies the analysis in nearshore zones, where benthic invertebrates are supported by a combination of periphyton and phytodetritus (e.g. Sierszen et al., 2006). We quantified the amount of each consumer’s nutrition that had originated from benthic food-web pathways starting with invertebrate prey (Diporeia and oligochaetes, 100% benthos; adult Mysis, 50% benthos; juvenile Mysis, 100% plankton (Sierszen et al., 2011); zooplankton, 100% plankton). When piscivory was indicated and prey fish had a length-isotope relationship, we used appropriate prey isotopic signatures by calculating the maximum length of prey fish according to Damsgard (1995). Total benthic contributions to each fish taxon were quantified at each depth as the sum of the benthic proportions of their prey. To summarise benthic inputs to each taxon, we generated box-and-whisker plots in which the box shows the range of median benthic contributions across all depths analysed, and the whiskers show the median first and third quartiles among depths. Finally, to test whether benthic support of fish nutrition was indicated by increasing d15N with depth and, conversely, planktonic support of fish nutrition was indicated by constant d15N with depth, we compared depth-isotope patterns with mixing model results. Lake whitefish, which were collected at only two depths (37 and 58 m; Table 1), and humper lake trout, which were only collected at one depth (41 m), were not included in this analysis.
Results Patterns in isotope ratios Within taxa, d15N varied by as much as 6.8& among individuals (Table 1), or the equivalent of two trophic levels (e.g. Hobson & Welch, 1995). For seven of the 12 taxa analysed, 9–31% of the variability could be explained by depth of capture of the individual fish. We found statistically significant increases in d15N with depth for pygmy whitefish, slimy sculpin, spoonhead sculpin, bloater, deepwater sculpin, lean lake trout and siscowet lake trout. Kiyi, rainbow smelt, cisco and burbot did not have significant changes in d15N with depth. The wide range of isotope values for kiyi was influenced by three small (c. 43 mm) kiyi with d15N of 3.2–3.3&; larger kiyi (81–264 mm) had d15N ranging from 5.8 to
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8.0&. Total length explained 7–27% of the variability in d15N for pygmy whitefish, deepwater sculpin, rainbow smelt, cisco and burbot (Table 1). For deepwater sculpin (but no other taxa), there was a positive relationship between total length and depth. However, diet information (T.R. Hrabik, unpubl.) revealed no significant ontogenetic change in diet with length, and depth of capture probably explained the trend in d15N for deepwater sculpin. For rainbow smelt, there was a weak but significant negative relationship between depth and total length, which was also found by Yule et al. (2007). d13C varied as much as 13& within taxa, indicating support from multiple production sources. d13C did not change systematically with depth for any taxon (Table 1).
Mixing model results Mysis was an important constituent in the nutrition of all taxa examined (Table 2). Use of Mysis was lowest for two of the nearshore taxa, pygmy whitefish (Mysis median proportion 0.07; 1st to 3rd quartiles 0.03–0.11) and slimy sculpin (0.07; 0.03–0.13) and highest for kiyi (0.78; 0.74–0.81) and burbot (0.56; 0.35–0.82). The nutritional importance of Diporeia was highest in nearshore taxa. Among piscivores, lean lake trout obtained equivalent contributions from rainbow smelt and cisco. Cannibalism by lean lake trout was substantial and was a necessary scenario to balance the model. In contrast, siscowet and humper lake trout relied more upon invertebrate prey than did lean lake trout. Piscivory by burbot was distributed among smelt, coregonines and lake trout (Table 2). Overall inputs from benthic food-web pathways were highest in demersal forage fishes and ranged from about 40 to 100% (Fig. 3a). Benthic contributions were near or above 40% for all species but rainbow smelt, cisco and burbot (Fig. 3b and c), which relied strongly on zooplankton and Mysis prey (Table 2). Estimates of benthic contributions overlapped among species, which was expected from their overlap in depth ranges and food habits. There was a gradient in the use of benthic resources that coincided with the depth distributions of the species, with nearshore taxa (slimy and spoonhead sculpin, pygmy whitefish) obtaining the greatest contributions; bloater, which is an intermediate-depth species in Lake Superior, obtaining intermediate amounts of benthic support, and the deepest taxa (deepwater sculpin and kiyi) obtaining the least (Fig. 3a). Although lake whitefish were collected at shallow depths, their benthic inputs were lower than those of other nearshore fishes,
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
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M. E. Sierszen et al. d15N and benthivory
(a) pygmy
Among forage fish species, those with high contributions from benthic resources had significant regressions between d15N and depth. The three nearshore demersal species (slimy and spoonhead sculpin, pygmy whitefish) and the intermediate-depth bloater all had significant increases in d15N with depth (Table 1). The majority of the estimates of benthic nutrition for these taxa were greater than 60% (Fig. 3a). Deepwater sculpin also had a significant d15N-depth regression (Table 1), and estimates of benthic nutrition were centred at 45% but with large error estimates (Fig. 3a). d15N of kiyi, rainbow smelt and cisco were invariant with depth (Table 1), and these three species all had benthic contributions below 50% (Fig. 3a,b). Among piscivores, burbot had benthic contributions less than 40% and a non-significant relationship between d15N and depth, and siscowet lake trout had higher benthic inputs and a significant d15N-depth regression. Lean lake trout, however, had benthic inputs lower than 40% (Fig. 3c) and a significant trend with depth (Table 1).
slimy spoon bloat lwf dws kiyi
(b) rbs cisco
(c) siscowet humper lean burbot
Discussion 0.0
0.2
0.4
0.6
0.8
1.0
Depth patterns in food-web pathways
Proportion benthic nutrition
Fig. 3 Proportion of nutrition that is benthic for (a) benthic forage fishes, (b) pelagic planktivores and (c) predatory fishes. Abbreviations for taxa are listed in Table 2. Boxes represent the range of medians across depths of analysis; whiskers show the median first and third quartiles among depths.
due to high use of Mysis (Table 2). For spoonhead sculpin, bloater, kiyi and rainbow smelt, median benthic contributions decreased with depth at each 50 m interval, resulting in a greater range of median contributions for those species in Figure 3. Relatively high support from Mysis and zooplankton for planktivorous cisco and rainbow smelt (Table 2) resulted in low proportions of benthic nutrition, ranging from about 5 to 35% (Fig. 3b). Benthic contributions to siscowet lake trout were near 50%, and benthic support of humper lake trout was somewhat higher than those for siscowets (Fig. 3c). Lean lake trout used benthic resources less than the deepwater morphotypes, with estimates of benthic contributions at or below 40% due to high feeding on planktivorous rainbow smelt and cisco. Neither lean nor siscowet lake trout estimates changed appreciably with depth. Burbot relied somewhat less on benthic resources than the other piscivores, due to high use of Mysis and rainbow smelt.
We found that the distribution of invertebrate, forage fish and piscivorous fish species in Lake Superior underlies depth-dependent patterns in trophic linkages within the whole-lake food web. Carbon and nitrogen stable isotope ratios revealed use of both littoral and profundal benthos among populations of most taxa analysed regardless of the depth of their habitat, providing evidence of nearshore–offshore trophic linkages in the largest freshwater lake by area in the world. Overall use of benthos was strongest among nearshore demersal species and weakest among planktivores. Contributions of benthic pathways to fish taxa declined with the depth of their habitat, corresponding with the declining abundance of benthic invertebrates and increasing abundance of Mysis offshore. We were able to discern these trends because of the patterns in planktonic and benthic isotope ratios with depth (Sierszen et al., 2006). The use of stable isotope techniques to discern nearshore and offshore habitats, and therefore our ability to trace coupling between those habitats, may be influenced by lake trophy. Although neither d13C nor d15N of plankton in oligotrophic Lake Superior varied systematically with depth, work in eutrophic Lake Victoria revealed factors that can structure planktonic isotope
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
Large lake habitat linkages values in large lakes. Nitrogen fixation by nearshore cyanobacteria and light limitation of offshore N fixation resulted in an offshore 15N-enrichment gradient (Hecky et al., 2010). In turn, the great biomass of cyanobacteria inshore sustained high rates of primary productivity that reduced C isotope fractionation, thereby 13C-enriching nearshore plankton and setting up a 13C enrichment gradient inverse to that of 15N (Hecky et al., 2010). As in Lake Superior, in oligotrophic Lake Baikal planktonic d13C was not structured by depth (Yoshii et al., 1999). Using fish tissue d13C to reflect the amount of littoral versus pelagic nutrition, we found that d13C varied as much as 13& within taxa, indicating multihabitat support of populations. Sierszen et al. (2006) found that d13C of Diporeia decreased through the photic zone from 15& inshore to 28& at 40 m depth. The nearshore decline in Diporeia d13C reflected a shift from a periphyton diet (d13C = 15 to 7&; Strand, 2005) to a diet of sedimented phytoplankton (d13C = 27&; Keough, Sierszen & Hagley, 1996). In contrast, zooplankton d13C did not change systematically across depths but varied between 26 and 31& (Sierszen et al., 2006). For all fish taxa except cisco and bloater, d13C values indicated inputs from littoral periphyton (indicated by d13C > 24&) as well as from pelagic production (d13C from 26 to 32&). Relationships between d13C and depth of capture were lacking, possibly because the Lake Superior littoral zone occupies a depth interval (0–40 m) that is small relative to our range of analysis or to foraging ranges of fishes. We used mean d13C values in the mixing model to provide a population-level perspective, while recognising variability in diet habits among individuals. Stable isotope analyses in other large lakes also revealed strong linkages to littoral production among fishes and multiple-habitat support of individual fish taxa. Among Lake Malawi cichlid species, mean d13C ranged from about 4 to 24&, indicating a wide range of feeding niches (Bootsma et al., 1996; Kidd et al., 2001). d13C of fish tissues has been used to estimate amount of benthic feeding in Lake Malawi cichlids (Kidd et al., 2001) and in lake trout (Guildford et al., 2008). The range in d13C that Guildford et al. (2008) found across 23 lakes (21.2 to 29.4&) was similar to the range we found for lean lake trout within Lake Superior (20.7 to 28.9&). d13C of Lake Baikal fishes also revealed variation in habitat use among and within species. Pelagic sculpins and amur held clearly pelagic signals (d13C from 26 to 33&), whereas benthic sculpin species were 13C-enriched (means ranged from 12 to 24&
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among species) but varied by as much as 10& within species (Kiyashko et al., 1998), again indicating multihabitat support of populations. Benthic nutrition was also indicated by nitrogen isotope signatures with a strong depth dependency. Progressive 15N-enrichment of benthos with depth occurs through a combination of processes; as detritus sinks, decomposition causes release of light isotopes, and the residual detritus becomes progressively 15N-enriched as it sinks (Saino & Hattori, 1985; Ostrom et al., 1998). Colonisation by bacteria, which effectively adds higher isotope ratios to the detrital particles, contributes to isotope enrichment. Zoobenthos that feed upon sedimented detritus also become 15N-enriched with depth (Sierszen et al., 2006), and we found that benthivorous fishes similarly exhibit 15N enrichment with depth. Fish species that obtained much of their nutrition from benthic resources had d15N values that increased with depth, reflecting the pattern exhibited by benthic primary consumers. Therefore, fishes collected from deep habitats may appear to occupy a higher trophic position than in reality, or higher than that of fishes collected shallow, if their d15N is not compared to the foodweb baseline at depth. For example, using Diporeia to describe the baseline and the depth – d15N regressions for lean and siscowet lake trout to predict their mean d15N at several depths, we can calculate trophic position according to the formula TPc = [(d15Nc d15ND)/3.4] + 2, where TPc is the trophic position of the consumer, d15Nc and d15ND are the d15N at each depth for the consumer and Diporeia, respectively, 3.4& is the trophic enrichment factor, and 2 is the correction applied because a primary consumer is being used as the baseline (Vander Zanden et al., 2000). At 100 m, the estimated mean trophic positions of lean and siscowet lake trout are 3.5 and 3.6, respectively; at 150 m, they are 3.7 and 3.6, and at 200 m, they are 3.4 and 3.1. Therefore, although their trophic niches may differ because of differences in diet or use of benthic resources, their trophic positions are similar across depths where they co-occur. One would not reach the same conclusion if the 100 m lean lake trout mean d15N of 8.5& were simply compared with the 200 m mean siscowet d15N of 9.5&, the mean 300 m siscowet d15N of 10.0& or the maximum siscowet d15N we obtained of 10.8&. Although this phenomenon and potential solutions have previously been described (e.g. Vander Zanden & Rasmussen, 1999), we feel that the heightened potential for large errors due to 15 N-enrichment in very deep lakes warrants our emphasis that primary consumer baselines must be characterised across depths.
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Examination of d15N-depth relationships suggests that they may be useful indicators of overall food-web pathway support for forage fish. Taxa with increasing d15N values with depth (e.g. slimy sculpin, pygmy whitefish) primarily obtained nutrition from benthic pathways, and those with level (zero slope) relationships (e.g. cisco, kiyi) were largely supported by planktonic pathways. d15N-depth relationships were less consistent indicators for piscivores, probably because the highly mobile predators obtained resources from a variety of habitats and depths. There was a broad range, from near 0% to near 100%, among taxa in the overall use of benthic resources, and our prediction of declining importance of benthic food-web pathways with depth was largely supported. Among forage fishes, the importance of benthos declined offshore in apparent response to declining abundance of benthic invertebrates with depth. Fishes occupying profundal and pelagic habitats obtained greater amounts of their nutrition from planktonic foodweb pathways, through zooplankton and Mysis. Compared to forage fishes, piscivores had a centralised, moderate span in their amounts of benthic nutrition. d13C values indicated that most taxa used both littoral and pelagic resources, even though they obtained varying overall amounts of benthic support; predators integrated resources at a higher level across benthic and pelagic habitats, as also found by Vander Zanden & Vadeboncoeur (2002). A prominent feature of this system is that linkages among multiple habitats support the whole-lake food web. This is accomplished through several processes. In nearshore zones, periphyton production and sedimentation of fresh phytodetritus combine to support benthos and demersal fishes. Offshore, planktonic production supports demersal consumers through two processes: sedimentation of phytodetritus and diel vertical migration (DVM). DVM is a dynamic foraging process prominent among deepwater biota, including Mysis, kiyi and siscowet and humper lake trout in large lakes including Lake Superior, Great Bear, Great Slave and Mistassini (Eshenroder, 2008, Ahrenstorff et al., 2011). The siscowet and humper morphotypes represent physiological adaptations to vertical migration (Henderson & Anderson, 2002; Hrabik et al., 2006; Zimmerman, Krueger & Eshenroder, 2006). Through DVM, deepwater consumers are able to obtain planktonic nutrition and thus occupy a habitat with few benthic food resources. Deepwater sculpin, which have not been reported to migrate as adults, obtain planktonic nutrition through consumption of Mysis and the eggs of migratory fishes. Planktonic path-
ways support pelagic planktivores, and predation by lean lake trout on planktivorous ciscoes and rainbow smelt represents a nearshore–offshore linkage between pelagic and nearshore habitats. Connections between offshore pelagic and nearshore benthic habitats are also apparent as cisco eggs, produced by planktonic pathways, support lake whitefish and other nearshore benthic fishes as the eggs incubate during the winter (Stockwell et al., 2014).
Functional convergence of diverse taxa Similarities among a variety of systems suggest that these depth-organised food-web processes are important properties of large lakes. As in Lake Superior, the stable isotope signatures of benthic amphipods in Lake Baikal indicated reliance on benthic primary production in nearshore habitats and increasing contributions of phytoplanktonic carbon in deep zones (Yoshii, 1999). Eshenroder, Sideleva & Todd (1999) noted the striking functional convergence among the pelagic sculpins of Lake Baikal and the deepwater ciscoes of the Great Lakes, which have developed adaptations to facilitate vertical migration. Baikal also has an ecological analogue of Mysis, the pelagic amphipod Macrohectopus branichii, which migrates from daytime depths of 100–200 m to night-time depths of 50–70 m to feed on zooplankton (Rudstam et al., 1992). The migratory ciscoes of the Laurentian Great Lakes and migratory sculpins of Lake Baikal appear to have evolved specifically to feed on the respective migratory macroinvertebrates, Mysis and Macrohectopus (Eshenroder et al., 1999). As in Lake Superior, attached algae in coastal zones and planktonic algae offshore fuel the food web of Lake Biwa, Japan (Yamada et al., 1998). Biwa also has an analogue to Mysis in its endemic profundal amphipod Jesogammarus annandaleii, which undergoes DVM from deep habitats to access pelagic zooplankton (Ishikawa & Urabe, 2005). The endemic isaza fish (Chaenogobius isaza) also migrates to feed on Jesogammarus and zooplankton (Ogawa et al., 2001). In Lake Malawi, nearshore zones are characterised by high benthivory (Abdallah & Barton, 2003; Duponchelle et al., 2005). In contrast, over 80% of the support of deepwater fish species is by pelagic production (Darwall et al., 2010), through feeding on zooplankton and the midge Chaoborus edulis, which is a zooplanktivore (Allison, Irvine & Thompson, 1996). Lake Malawi demersal fish directly use a planktonic food-web pathway through migratory Chaoborus edulis (Irvine, 1997; Duponchelle et al., 2005) and fish DVM, notably by the catfish
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
Large lake habitat linkages Synodontis njassae (Thompson et al., 1995). In Lake Tanganyika, the pelagic clupeid Stolothrissa tanganicae performs nocturnal DVM to feed on zooplankton and apparently does not feed during daylight hours. During seasonal clupeid abundance maxima, adult demersal Nile perch (Late mariae) migrate to feed on Stolothrissa (Coulter, 1991). In deep temperate lakes, profundal benthos, and therefore benthivory, are limited by the decreasing food quality of detritus that has decomposed while sinking through deep-water columns (Mozley & Howmiller, 1977; Evans et al., 1990). In the African lakes, the abundance of benthos at depth is limited by anoxia (Muli, 2005). In both cases, the solution for deep fishes is to access planktonic food-web pathways through DVM.
Habitat linkages in large lake food webs It is clear that although connectedness among habitats has been emphasised for small systems (e.g. Schindler & Scheuerell, 2002), multihabitat interactions are integral to even the world’s largest lakes. The processes linking habitats in small and large lakes are generally similar and include sedimentation of pelagic production to benthic habitats and movements of organisms among habitats. Of particular importance in large lakes is the role of migratory macroinvertebrates, which greatly enhance benthic–pelagic coupling (e.g. Linden & Kuosa, 2004; Patwa et al., 2007) and appear to have provided the evolutionary stimulus for the development of vertically migrating pelagic fishes of diverse taxonomies (Eshenroder et al., 1999). Whereas evidence regarding terrestrial subsidies to small lake food webs has been provided (Cole et al., 2011), large lake food webs appear to obtain little support from terrigenous carbon (Zigah et al., 2012; Wilkinson et al., 2013). Ecosystem disturbance can disrupt the processes that link aquatic habitats. Eutrophication alters the functional organisation of lakes; although planktonic primary production increases with eutrophication, the loss of benthic algal production through shading by phytoplankton causes a net decline in whole-lake primary production and concomitant losses of benthic food-web pathways (Vadeboncoeur, Lodge & Carpenter, 2001; Vadeboncoeur et al., 2003; Chandra et al., 2005). Loss of native fishes and replacement by non-native species with different foraging and spawning habits can also result in the loss of habitat coupling supporting whole food webs (Stockwell et al., 2014). In the lower Laurentian Great Lakes and other systems, invasions by Ponto-Caspian dreissenid mussels have caused system-wide food-web shifts from
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dominance by pelagic-profundal linkages to benthic-littoral pathways (Higgins & Vander Zanden, 2010). Subsequent declines in planktonic biomass and catastrophic losses of Diporeia and other benthos led to lower growth and condition of commercially valuable whitefish (Rennie, Sprules & Johnson, 2009). The reliance of Mysis on both planktonic and benthic foods (Sierszen et al., 2011) and increased predation on Mysis following the loss of Diporeia (Owens & Dittman, 2003; Pothoven & Madenjian, 2008) may put it at risk, and Mysis declines in Lake Michigan have been documented (Pothoven, Fahnenstiel & Vanderploeg, 2010). Any risk to Mysis, or its counterparts in other large lakes of the world, would also put at risk the essential functional linkages they provide. Nile perch (Lates niloticus) were introduced to Lake Victoria in the 1950s but did not become dominant until nearly 30 years later (Hecky et al., 2010). Multiple stressors, especially nutrient loading and a warming trend, led to a new stable state characterised by eutrophication that facilitated dominance by Nile perch, catastrophic declines in native haplochromine cichlids (which had comprised 80% of the demersal fish biomass) and rapid increases in fishery yields. Together, environmental stressors and introduced species changed the Lake Victoria food web from one with diverse benthic and pelagic functionalities to a simplified pelagic-dominated system (Hecky et al., 2010). This examination illustrates that depth-organised food webs are common features in large, deep lakes. Further, ecosystem-level support of large lake food webs relies on processes that link diverse habitats within them, and those linkages are often performed by native macroinvertebrate and fish species that have evolved in the systems. The functional role of native fishes has been highlighted as an important benefit of re-establishing native fishes (Zimmerman & Krueger, 2009; Stockwell et al., 2014). Our analysis suggests that intact cross-habitat trophic linkages are diagnostic of well-functioning large-lake food webs, and that preservation of those functional attributes be a priority in efforts to protect and restore large lakes.
Acknowledgments We wish to thank Aisha Beaty, Andrew Just and Corlis West for preparing fish samples for analysis; the Captain and crew of the R/V Kiyi for collecting fish samples; and Shawn Sitar for providing humper lake trout samples and diet information. Sample collection was partially supported by Minnesota Sea Grant R/F-15 to TRH and JDS. The manuscript was greatly improved through
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
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constructive comments by Robert Hecky, Donald Phillips and Daniel Schindler. The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the US Environmental Protection Agency. This is also contribution number 1866 of the USGS Great Lakes Science Center. Any use of trade, product or firm names is for descriptive purposes only and does not imply endorsement by the US Government.
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(Manuscript accepted 19 June 2014)
Published 2014. This article is a U.S. Government work and is in the public domain in the USA., Freshwater Biology, doi: 10.1111/fwb.12415
