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Long-term zooplankton responses to nutrient and consumer subsidies arising from migratory sockeye salmon Oncorhynchus nerka

Guangjie Chen , Daniel T. Selbie , Bruce P. Finney , Daniel E. Schindler , Lynda Bunting , Peter R. Leavitt and Irene Gregory-Eaves

G. Chen (guangjiechen@gmail.com) and I. Gregory-Eaves, Dept of Biology, McGill Univ., Montreal, Quebec, H3A 1B1, Canada. GC also at: Key Laboratory of Plateau Lake Ecology and Global Change, School of Tourism and Geography, Yunnan Normal Univ., Kunming, CH-650092 Yunnan, PR China. – D. T. Selbie, Fisheries and Oceans Canada, Science Branch, Salmon and Freshwater Ecosystems Division, Cultus Lake Salmon Research Laboratory, Cultus Lake, British Columbia V2R 5B6, Canada. – B. P. Finney, Dept of Biological Sciences, Idaho State Univ., Pocatello, ID 83209-8007, USA. – D. E. Schindler, School of Aquatic and Fishery Sciences, Univ. of Washington, Seattle, WA 98195, USA. – L. Bunting and P. R. Leavitt, Limnology Laboratory, Dept of Biology, Univ. of Regina, Regina, Saskatchewan, S4S 0A2, Canada.

Migratory animals, such as Pacifi c salmon, can signifi cantly shape communities in recipient habitats both by altering the fl ux of resources, and changing community composition and subsequent trophic interactions. Here we mainly used paleo-ecological records from natural sockeye salmon nursery lakes to quantify the response of plankton communities to the infl ux of salmon-derived nutrients and consumers (juvenile salmon). Our long-term data show that increases in the density of spawning salmon often elevated infl ux of nutrients, and, in turn, zooplankton production over the past few centuries. In contrast, signifi cant correlations were not detected in two lakes with extremely low or high average spawner densities (i.e. 1.5 and 34.7 � 10 3 spawners km �2 year �1 respectively). With increasing spawner densities across lakes, analysis of the size structure of subfossils in sediments revealed a strong decrease in body size of a main juvenile salmon prey item ( Eubosmina longispina ; r 2 � 0.36, p � 0.001, n � 67), consistent with an overriding eff ect of predation in lakes with high salmon den-sities. Th ese long-term data not only highlight the key role of salmon-derived nutrients in stimulating plankton communi-ties, but also suggest that the relative eff ect of nutrient and consumer subsidies varies along gradients of lake production, despite a single ultimate causal mechanism (migrating fi sh).

It has become increasingly recognized that ecosystems are not discrete entities, but rather are interconnected by fl ows of organisms, detritus and nutrients (Polis et al. 1997, Marc-zak et al. 2007). Th ese spatial subsidies can strongly alter the nutrient status and productivity of recipient ecosystems and profoundly impact biodiversity and food web patterns (Polis et al. 2004, Holt 2008). To date, spatial subsidy theory has focused primarily on the study of nutrient and detrital inputs to recipient ecosystems (Marczak et al. 2007). For example, we have seen large advances in the past decade in our understanding of how trophic interactions within recipi-ent food webs change with resource subsidies (e.g. strength of predation; Menge 2004, Leroux and Loreau 2008). How-ever, migrating organisms such as anadromous fi shes may not fi t well within existing spatial subsidy models because, in addition to being vectors of nutrient inputs, they are also parents to a new generation of off spring that are consum-ers in recipient food webs. To date little attention has been paid to the coupling of nutrient and consumer subsidies and their combined ecological impact on recipient communi-ties. Here, we defi ne the roles of Pacifi c salmon as nutrient and consumer subsidies across ecosystems, and explore the

combined eff ect of both subsidies on zooplankton popula-tions from lakes used as spawning and nursery systems.

Sockeye salmon nursery lakes are ideal systems for evaluating the ecological role of spatial subsidies of nutri-ents because the annual return of spawners from the North Pacifi c Ocean to freshwaters represents one of the most obvi-ous resource subsidies on the west coast of North America (Naiman et al. 2002). Salmon-derived nutrients (SDN), which are released primarily through the metabolism of spawning fi sh and death and decay of spawner carcasses, can strongly aff ect the primary production of recipient eco-systems (Schindler et al. 2005a). SDN may also enhance production of higher trophic levels (e.g. increased inverte-brate production) in natural nursery systems (Wipfl i et al. 1998, Schmidt et al. 1998). For example, a paleoecologi-cal study of two very productive salmon nursery systems (i.e. � 10 � 10 3 spawners km �2 year �1 ) documented a posi-tive relationship between spawner densities and zooplankton fl uxes (i.e. a paleolimnological estimate of past production; Sweetman and Finney 2003). However, previous food web studies have found that the eff ect of a fertilizer on secondary production can vary depending on lake nutrient status and

Oikos 120: 1317–1326, 2011 doi: 10.1111/j.1600-0706.2011.19042.x

© 2011 Th e Authors. Oikos © 2011 Nordic Society Oikos Subject Editor: James D. Roth. Accepted 17 January 2011

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food web composition (Jeppesen et al. 2003). Th erefore it remains unresolved whether the positive relationship found between SDN and zooplankton production is broadly appli-cable to the diversity of natural salmon lakes found along the west coast of North America (i.e. ranging from extremely low to high salmon spawner densities).

Migratory salmon are also a source of consumers to coastal nursery lakes (i.e. consumer subsidies). In general, the production of juvenile salmon increases as a function of the density of spawning anadromous adults (Shortreed et al. 2001), although depensatory and compensatory interactions can alter the precise form of the relationship between fry and adults (Ricker 1954, Essington et al. 2000). Hatching of salmon eggs can lead to the development of large pop-ulations of zooplanktivorous fi sh, which can regulate the trophic structure of local prey communities. In particular, numerous stocking experiments in sockeye salmon nursery systems reveal that zooplankton size structure and produc-tion are strongly aff ected by juvenile salmon (Koenings and Kyle 1997).

To date, few empirical studies have attempted to quantify the relative importance of nutrient and consumer subsidies in the same recipient habitat, yet the concomitant input of such subsidies is not uncommon in nature. Wherever there are large congregations of migrating animals (e.g. seabirds, wildebeest and anadromous salmon), there is the potential for signifi cant and concurrent inputs of nutrients and consumers. Th e net eff ect of nutrient and consumer subsidies on coastal salmon nursery lakes remains poorly understood. Sweetman and Finney (2003) suggested that SDN inputs had an over-riding infl uence on zooplankton abundances in comparison to predation pressure by juvenile salmon. However, their work focused on Bosmina longirostris , which is a less desirable prey item for sockeye salmon (Burgner 1991). By looking over a broader network of sites, we propose that consumer subsidies could interact with resource inputs and suppress the bottom – up eff ect of allochthonous nutrients in some ecosystems.

We conducted analyses of lake sediment records to defi ne community responses to changing salmon populations over a multi-centennial period. Our main objective was to deter-mine how zooplankton populations responded to the com-bined eff ects of SDN subsidies and predation regimes across lakes varying in salmon densities. Specifi cally, we anticipated

that secondary production would increase initially with SDN supply, but that at very high spawner densities, increases in vertebrate predation pressure by juvenile salmon could regu-late both prey abundances and their size structure, indepen-dent of nutrient fl uxes.

Material and methods

Study lakes

We defi ne our study area within southwest Alaska, where the landscape, climate and limnology of nursery systems are appro-priate for developing paleolimnological reconstructions of past salmon abundance (Selbie et al. 2009). Four salmon nursery lakes (Little Togiak, Nerka, Iliamna and Red) were selected and analyzed in this study (Appendix 1). We also compared the results of these sites to those from two lakes (Karluk and Frazer) previously analyzed by Sweetman and Finney (2003) to cover a broad gradient of modern sockeye escapement den-sities (means ranged from 0 to 34.7 � 10 3 spawners km �2 year �1 ; Table 1, Appendix 1). Th ese sites are all located at low elevation ( � 110 m a.s.l.) and have a relatively short distance from sea ( � 100 km). All of our study lakes are relatively deep (maximum depth of 45 – 301 m and mean depth of 29 – 49 m), with sparsely vegetated littoral zone.

Little Togiak (59 ° 35’N, 159 ° 10’W), Nerka (59 ° 35’N, 159 ° 05’W) and Iliamna (59 ° 30’N, 155 ° 00’W) lakes are located in the Bristol Bay area, which hosts the largest sock-eye salmon fi shery around the world. Th ese oligotrophic lakes currently have low to intermediate modern escapement densities (i.e. 1.5 – 2.4 � 10 3 spawners km -2 year -1 ). Lake Nerka is a large lake with relatively complex morphology and is connected to Little Togiak Lake by a short river. Iliamna Lake is part of the Kvichak River system and is the largest lake in Alaska. Red (57 ° 15’N, 154 ° 17’W), Karluk (57 ° 25’N, 154 ° 05’W) and Frazer (57 ° 15’N, 154 ° 08’W) lakes are all located on Kodiak Island. Red Lake is a small, meso-eutro-phic lake that currently has the highest modern escapement density in our lake set and one of the highest escapement densities within the Northeast Pacifi c. Karluk and Frazer lakes are larger, oligotrophic systems. Salmon were introduced to Frazer Lake in the 1950s following the installation of fi sh

Table 1. Limnological summary of the six Alaskan study lakes. Annual average values are used for spawner density, total phosphorus and zooplankton data. Two bosminid species are identifi ed in this study: Eubosmina longispina (E) and Bosmina longirostris (B). p-levels at � 0.001 and � 0.01 are indicated by ∗ ∗ ∗ and ∗ ∗ respectively, and unavailable data are marked with a dash (−). We have used Frazer Lake as a paleolim-nological reference system because no salmon spawners were present prior to 1951 AD. However, because there are no limnological data for Frazer Lake during this time period, we have presented recent water chemistry and zooplankton data. All data were collated from Schrof et al. (2000), Brock et al. (2006) and Schindler (unpubl.).

Lake Frazer Little Togiak Nerka Iliamna Karluk Red

Spawner density ( � 10 3 km �2 ) 0.0 1.5 2.4 2.2 18.7 34.7Surface area (km 2 ) 16.6 6.0 201.0 2622.0 39.5 8.4Mean depth (m) 33 30 39 44 49 29Total phosphorus ( μ g l �1 ) 5.4 6.7 6.5 3.9 8.0 34.0

Total zooplankton (no. m �3 ) 5686 1153 2314 7548 12 008 15 154No. of years 14 29 38 19 25 8Bosminid:zooplankton ratio 0.57 0.28 0.42 0.30 0.09 0.19r 2 (Bosminid – zooplankton) 0.81 ∗ ∗ ∗ 0.46 ∗ ∗ ∗ 0.74 ∗ ∗ ∗ 0.73 ∗ ∗ ∗ 0.63 ∗ ∗ ∗ 0.71 ∗ ∗ Bosminid species B only E only B � E E only B only B � EMean Bosminid size (mm) 0.37 – – 0.51 0.43 0.44

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ladders and thus we have used sedimentary data that pre-date this time to represent a reference system for this study.

Juvenile sockeye salmon are the numerically dominant planktivorous fi sh in our study lakes (i.e. � 50%; Schrof et al. 2000, Scheuerell and Schindler 2003), feeding on pelagic crustacean zooplankton. Although other plankti-vores (e.g. three-spine stickleback and kokanee salmon) are present in these lakes, juvenile sockeye salmon tend to out-perform these competitors for forage and habitats (Burgner 1991, Quinn 2004). Estimates of juvenile salmon density are not available for many of our sites, but previous studies have demonstrated that juvenile densities of sockeye salmon increase signifi cantly with spawner densities (Appendix 2), with density-dependent compensation and depensation mechanisms altering the precise relationship at very low and high adult densities respectively (Achord et al. 2003). Con-sequently, the previous year’s spawner density can be used to approximate the following season ’ s density of juvenile salmon (Schindler et al. 2005b, Rich et al. 2009). Under these con-ditions, elevated density of juvenile salmon can be expected to increase predation pressure on planktonic prey items, as has been shown for salmonid-rearing lakes along western North America (Beauchamp et al. 2004, Quinn 2004).

Our study largely focused on the remains of bosminid taxa because they are an important group of prey for juve-nile salmon, a dominant component of the zooplankton community by abundances and preserve well in lake sedi-ments. For example, Eubosmina encompass 30 – 60% of the total number of prey items in the diet of sockeye fry within the limnetic zones of Nerka, Little Togiak and Iliamna lakes (Hoag 1972). It has been shown that Eubosmina adapt to increased fi sh predation by reducing their body sizes at the population level (e.g. antennules and carapaces; Amundsen et al. 2009). Across all of our lakes, bosminids are numeri-cally the most dominant herbivores and make up an average of 31% of the total zooplankton abundance estimated by net tow samples (range across lakes � 9 – 57%; Table 1). Bos-minids are also signifi cantly and positively correlated with total zooplankton abundances (r 2 � 0.46 – 0.81, p � 0.01; Table 1) and thus serve as a reliable indicator for second-ary production. Past trends in zooplankton dynamics can be inferred from the paleolimnological record because bosminid remains preserve well in lake sediments (Kerfoot 1981). Fur-thermore, the density of bosminid remains has been shown to accurately track changes in water column production (Hann et al. 1994). In contrast, copepods, such as Cyclops , do not preserve well in lake sediments (Korhola and Rautio 2001). Taken together, we conclude that the densities of bosminid remains in lake sediments are robust estimates of the long-term dynamics in zooplankton grazer production.

Sediment collection and analyses

Sediment cores (ranging from 37 to 53 cm long) were retrieved from a deep, depositional basin in each lake using a gravity corer. Th e cores were sectioned at fi ne intervals ( � 0.5 cm) and freeze-dried for further analyses. We ana-lyzed samples from cores of Nerka and Red lakes that were previously studied by Schindler et al. (2005a) and Finney et al. (2000), respectively, where more details on the sampling and geochemistry can be found.

Th e chronology for each of the cores is based on 210 Pb dating, where the constant rate of supply model was applied to calculate dates from 210 Pb activities. Beyond the range of unsupported 210 Pb activity (i.e. samples older than ∼ 120 – 150 years old), we estimated sediment age by assuming constant sedimentation rates to the core bottom or to an independent age marker (ie. tephra or 14 C date).

Sedimentary δ 15 N analysis followed standard methods (Talbot 2001). Briefl y, homogenized sediment subsamples were measured using a continuous fl ow isotope ratio mass spectrometer. All measurements were conducted at Univ. of Alaska Fairbanks, Univ. of Regina or Univ. of Washington with a measurement precision of 0.2 ‰ . Th e δ 15 N values are expressed in standard δ notation relative to standard atmospheric nitrogen. As both salmon nutrient input and non-salmon sources (e.g. the watershed load) can contribute to the total nutrient loading in lakes, we calculated the per-centage nitrogen (% N) derived from spawning salmon using a two-source mixing model (Schindler et al. 2005a). Th e estimation error (i.e. 95% CI) was generated by conducting 10 000 Monte Carlo permutations where the value for each constituent of the two-source mixing model was drawn from its Gaussian distribution. Th is mixing model incorporates sedimentary δ 15 N data from reference lakes as an estimate for the background δ 15 N. Th is model assumes that any process-ing of sedimentary δ 15 N is independent of the amount of nutrients derived from spawning salmon and the N isotope ratio of sockeye salmon (i.e. 11.2 0.45 ‰ , mean SD) was constant through time. Only subtle variation in sedimen-tary δ 15 N was observed in the reference lakes in this study during the past several centuries (i.e. the average value with 1 SD was 3.32 0.16 ‰ for Frazer (reference lake for Karluk and Red), 2.97 0.18 ‰ for Grant (reference lake for Nerka and Little Togiak) and 3.02 0.28 ‰ for Tazimina (reference lake for Iliamna)) (Finney et al. 2000). All lake records had low atomic C:N ratios with limited range of variation (i.e. the averaged values with 1 SD varying from 7.4 0.6 in Iliamna to 10.1 0.5 in Nerka), suggesting very limited input of catchment-derived organic matter into our study lakes (Selbie et al. 2009). As identifi ed in Kr ü mmel et al. (2009), Red Lake may have experienced incomplete diagenesis (e.g. elevated N content and lower than expected δ 15 N values in the top 8 cm of sediment core). In this study, we found little change to the results of correlation analyses after excluding the samples of the top 8 cm and therefore the data from the whole core is included in the subsequent data analysis.

To reconstruct past changes in total phosphorus (TP) concentrations, we enumerated and identifi ed sedimentary diatom assemblages following standard methods (Chen et al. 2011). Estimates of historical lake-water phosphorus con-centration were generated by applying British Columbia or Alaskan transfer functions following the protocol described in Gregory-Eaves et al. (2003).

Zooplankton analyses

To prepare sedimentary cladoceran samples, we followed the standard methods outlined by Korhola and Rautio (2001). Briefl y, approximately 0.1 g of freeze-dried sediment was treated with 50 ml 10% KOH to defl occulate the sample. We then added 5 ml of 10% HCl to remove the carbonates

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three- to fi ve-fold both among lakes, and through the past centuries in sites with abundant adult salmon (Fig. 1). For example, SDN account for 10 – 40% of all nitrogen infl uxes in Little Togiak and Nerka lakes, 30 – 70% in Illiamna and Karluk lakes, and up to 88% in highly productive Red Lake. Similarly, diatom-inferred concentrations of total phospho-rus (TP) increased as a function of % SDN in the three lakes in which salmon accounted for at least 20% of total N infl ux (r 2 � 0.31 – 0.61, p � 0.01), but not in reference Frazer Lake, or in Little Togiak Lake (Fig. 2).

Zooplankton community composition

Across all lakes, bosminid taxa dominated the sedimentary zooplankton assemblages (Fig. 1). Eubosmina longispina was the most abundant cladoceran across the sedimentary records of four study lakes. Both Bosmina longirostris and E. longispina co-occurred in sediments of Nerka and Red lakes, but generally B. longirostris was either less abundant or absent in sediment samples from both lakes (Fig. 1B, D). Th ese community compositions diff er from the previously-studied Karluk and Frazer lakes, where B. longirostris was the only bosminid species preserved in lake sediments (Sweet-man and Finney 2003).

Daphnia remains were present in extremely low abun-dances in all sediment cores. Th is result is consistent with the net tow data where Daphnia constituted only a minor part of zooplankton communities ( � 10%; Schrof et al. 2000). Daphnia remains (belonging to D. longispina group) were most prevalent in Little Togiak lake sediments, but rarely amounted to more than 10% of the bosminid fl ux (Fig. 1A). As a result, we have focused our data analyses on bosminid size structure and fl ux.

Effects of salmon on zooplankton size structure

Sedimentary bosminid remains from the four Eubosmina -dominated lakes showed strong size variation in antennules, carapaces and mucros (Appendix 3). In particular, we found that the lengths of bosminid antennules, carapaces and mucros all tended to be smaller when salmon densities were high. Over-all, we suggest that these body size patterns are largely driven by variation in the size structure of individual Eubosmina as this taxon comprised 90 – 100% of all antennules in each lake.

Analysis of antennules attached to headshields, used to distinguish among individual bosminid species, revealed that the response of E. longispina and B. longirostris varied across lakes of diff ering SDN (Fig. 3). Specifi cally, we detected a strong negative correlation between the antennule length (AL) of E. longispina and % N derived from salmon, even after accounting for diff erence in zooplankton size that were lake-specifi c (r 2 � 0.36, p � 0.001, n 1 (number of lakes) � 4, n 2 (total number of samples) � 67; Fig. 3A, Table 2). In con-trast, we did not detect any trend in the AL of B. longirostris across the SDN gradient (r 2 � 0.01, p � 0.356, n 1 � 4, n 2 � 57; Fig. 3B, Table 2).

Effects of salmon on zooplankton production

Bosminid fl uxes were correlated positively with % N derivedfrom salmon in three lakes with intermediate spawner

and fi nally the slurry was fi ltered through a 36 μ m sieve to retain cladoceran fragments (including very small fragments like postabdominal claws of Daphnia ). Permanent slides were then prepared by transferring a 0.05 ml aliquot of the well-mixed concentrate to a glass slide through a precision pipette. Glycerin – safranin jelly was then added and a pin was used to mix the jelly and the sample residue gently.

We followed standard protocols for identifying, measuring and enumerating subfossil cladocerans (Korhola and Rautio 2001). Briefl y, the slides were scanned and counted using a compound microscope under 200 � and 400 � magnifi -cations. At least 100 cladoceran remains were enumerated for each sample, and counts were adjusted to refl ect the number of remains that an individual would produce; one individual cladoceran has two carapaces, one headshield and one postabdominal claw. To take into account diff erential sedimentation rates, the count was then recalculated as fl ux rate (individuals cm -2 year -1 ) to approximate the secondary production in this study. We mainly used Frey (1958) as the taxonomic guides for our identifi cations. For the Bosmini-dae group, we used headshield features (mainly head pore position) to distinguish diff erent species (Goulden and Frey 1963), whereas the carapace and mucro parts were identi-fi able only at group level. Daphnia were identifi ed to spe-cies groups, as postabdominal claws were the only remains found in sediment. Th e lengths of antennules, carapaces and mucros were used to represent the body size of bosminids. All the size data were collected under 400 � magnifi cation following the standard metrics as used in Kerfoot (1981).

To evaluate the generality of the results derived from analy-ses of the sedimentary records, we conducted complementary analyses of contemporary zooplankton data. Zooplankton net tow data were compiled for 11 lakes from Schrof et al. (2000) and from sources that had records for at least 20 years from lakes in Bristol Bay (D. Schindler unpubl.). Our analy-ses are based on annually averaged zooplankton densities (individuals m –2 ), as net tow samples were typically collected at least four times per year between 1981 – 2005 (using a coni-cal net with a diameterof 0.2 m and 153 μ m mesh). A more detailed description of zooplankton sampling and counting is reported in Schrof et al. (2000). We focused our analyses on zooplankton grazers, which included bosminids, Daphnia and Diaptomus as they represent a group that has previously been shown to be sensitive to both nutrient dynamics and predation from sockeye fry (Schmidt et al. 1998).

To defi ne relationships among variables we conducted correlation (Pearson product-moment) or regression analyses and analyses of covariance (ANCOVA) using the R program (R Development Core Team 2008). Where we pooled data across lakes, we conducted ANCOVA to avoid infl ating our degrees of freedom due to within-lake pseudoreplication. In our ANCO-VAs, we included study lake as a covariate and % N derived from salmon or salmon spawner density as a random factor.

Results

Effects of salmon on nutrients in nursery lakes

Application of a two-box mixing model suggests that the rel-ative importance of SDN (% N derived from salmon) varied

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Discussion

Migratory animals can alter recipient ecosystems by changing the infl ux of resources (Anderson and Polis 2004) and con-sumers (Knight et al. 2005), although little is known of how the combined eff ect of individual subsidies may vary along gradients of donor intensity. Here we demonstrate that subsi-dies of nutrients, which were derived from spawning salmon (Fig. 2), regulate the production of zooplankton in salmon nursery lakes at intermediary densities of spawning salmon (Fig. 4), but that concomitant increases in predation inten-sity (Fig. 3, Appendix 2) modulate the relationship between nutrient input and production of the main zooplankton spe-cies in high salmon density lakes (i.e. � 20 � 10 3 spawners km –2 year –1 ; Fig. 4F, 5). Similarly, low densities of spawning salmon ( � 2 � 10 3 spawners km -2 year -1 ) appeared insuffi -cient to regulate changes in zooplankton abundance through either nutrient or consumer mechanism (Fig. 3, 4). Overall, we suggest that interaction between resource and consumer subsidies has important implications for developing predic-tions regarding food web responses to spatial subsidies.

densities (Fig. 4). For example, bosminid fl ux varied as a function of % SDN in Nerka, Iliamna and Karluk lakes (r � 0.82 – 0.92, p � 0.001; Fig. 4C – E), but not in Frazer (% N replaced with δ 15 N) or Little Togiak (r � 0.10, p � 0.3; Fig. 4A – B) where sockeye salmon population was either absent or in low density ( � 2 � 10 3 spawners km -2 year -1 ). Secondary production was also uncorrelated to the relative level of N derived from salmon in Red Lake (r � 0.00, p � 0.987, n � 16; Fig. 4F), the most productive of the nursery systems in this study.

Similar to our paleolimnological analyses, we found that modern zooplankton densities showed a signifi cant non-linear relationship with sockeye salmon spawner density (Fig. 5). Specifi cally, we observed a signifi cant second-order polynomial relationship between spawner density and annually-averaged estimates of zooplankton grazer abundance (r 2 � 0.33, p � 0.001, n 1 � 11 (num-ber of lakes), n 2 � 82 (total number of samples, where lake grouping was included as a covariate)), with grazer production highest at intermediate spawner densities (Fig. 5).

Figure 1. Sedimentary profi les of Little Togiak Lake (A), Nerka Lake (B), Lake Iliamna (C) and Red Lake (D) showing the age model, % N derived from salmon, the fl ux and body size of three zooplankton ( Eubosmina longispina , Bosmina longirostris and Daphnia spp.). A reference line (dashed line) at 200 μ m is shown in each plot of antennule length.

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(Brock et al. 2006) and earlier studies have demonstrated that SDN are readily assimilated into food webs of nursery systems (Finney et al. 2000, Gregory-Eaves et al. 2007). Th e stimu-latory eff ect of SDN has also been documented in modern surveys (Schmidt et al. 1998) and forms the theoretical basis for the lake fertilization treatments of sockeye nursery lakes (Stockner and MacIssac 1996, Hyatt et al. 2004). However, when SDN inputs are consistently low, paleolimnological records of diatoms and zooplankton from large sockeye nurs-ery lakes have shown minimal changes (Selbie et al. 2007).

Comparison of our results with other salmon studies suggests that there is a minimum level of marine nutrient inputs needed for there to be a detectable transfer of salmon-derived nutrients to secondary production. For example, in Little Togiak Lake where SDN input was modest ( � 30%; Fig. 1A), bosminid production was not correlated to marine nutrient input (Fig. 4B), despite the fact these nutrients were signifi cant driver of algal production and community com-position (Chen et al. 2011). Similarly, non-linear responses are apparent in resident fi sh in response to carcass addition treatments in streams (Janetski et al. 2009). Consistent with these fi ndings, a large meta-analysis of a wide array of ecosys-tems noted that lower trophic levels were, on average, twice as responsive to resource subsidies as consumers (Marczak et al. 2007). Muted or threshold eff ects in higher trophic levels are likely due to the longer generation times of these organisms as well as the ‘ source omnivory ’ nature of their diet (Anderson and Polis 2004, Marczak et al. 2007). In the absence or at modest levels of salmon-derived nutrients, other environmental factors such as changes in temperature and catchment-derived nutrient loadings could infl uence zooplankton production (Schindler et al. 2005b). How-ever, we found that the zooplankton production before the introduction of salmon was signifi cantly lower than after the introduction of salmon in Frazer Lake (p � 0.005; Student ’ s t-test), suggesting an overriding eff ect of sizable salmon nutrients over other confounding factors.

Regulation of zooplankton communities by consumer subsidies

Based on our analyses of both paleolimnological and net tow data, we suggest that consumer subsidies of planktivorous

Regulation of zooplankton communities by nutrient subsidies

Our paleolimnological analyses revealed that historical pro-duction of zooplankton often increased as a linear function of the magnitude of salmon-derived nutrient fl uxes. For exam-ple, an increase in both nutrient loading (measured as DI-TP; Fig. 2) and bosminid fl ux (Fig. 4C – E) were associated with more spawning salmon in lakes with intermediate density of spawning salmon (i.e. 2 – 20 � 10 3 spawners km -2 year -1 ). Th ese results were expected because carcass-derived nutrients have been shown to be integrated quickly into the open waters

Figure 2. Relationships between diatom-inferred total phosphorus (DI-TP; μ g l �1 ) and % N derived from salmon for each of our study lakes. TP values were reconstructed using the diatom-TP transfer functions as detailed in Gregory-Eaves et al. (2003). Regres-sion lines are added for Nerka, Karluk and Red lakes, where there are signifi cant correlations (r 2 � 0.49, 0.61 and 0.31, respectively; p � 0.01). We did not detect a signifi cant relationship in Little Togiak, but this is likely because of weak signal relative to noise. Specifi cally, we found that the range of estimated TP values (i.e. 2.9 μ g l� 1 ) was within the prediction errors ( 2.1 μ g l �1 ) of the DI-TP transfer function applied. Data for Iliamna Lake are not shown as the diatom assemblage was characterized by taxa that refl ect its unique physical characteristics (i.e. this site is the largest lake in Alaska with cool epilimnetic waters and deep thermocline; Chen et al. 2011).

Figure 3. Scatterplots showing the relationship of the average antennule lengths of both Eubosmina longispina (plot A) and Bosmina longi-rostris (plot B) with % N derived from salmon for each sediment interval examined across lakes. Th ese data were collected from paleolim-nological records from Little Togiak, Nerka, Iliamna and Red lakes in plot A, and Frazer, Nerka, Karluk and Red lakes in plot B. Note the diff erence in scale on the y-axis between plots.

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(Koenings and Kyle 1997) and other larger zooplankton (e.g. Daphnia ; Scheuerell et al. 2005). Our evidence of intensive fi sh predation on large-bodied zooplankton also agrees well with fi eld observations from other anadromous fi sh systems (Post et al. 2008).

In contrast, the smaller and more cryptic Bosmina lon-girostris is considerably less vulnerable to visually orienting juvenile salmon fry. Consistent with this fact, we note that antennule length of B. longirostris did not vary signifi cantly as a function of % SDN in our study lakes (Fig. 3B). Preda-tion by invertebrates like Cyclops , however, can be an impor-tant driver of B. longirostris morphology (e.g. antennules and mucros) when juvenile fi sh densities are relatively low (Kerfoot 1981).

Advancing spatial subsidy theory

Most theoretical and empirical studies of spatial subsidies to date have focused on the movement of either resources or consumers separately (reviewed in Polis et al. 1997, Polis et al. 2004). Our study is novel in that we have shown that nutrient and consumer subsidies can interact and have signif-icant eff ects on the recipient community. Specifi cally, Pacifi c salmon can directly cause changes in resource pools within recipient ecosystems and these consumers can also aff ect pro-cess rates indirectly through feeding (i.e. material and process subsidies; Flecker et al. 2010). Furthermore, we showed that the strength of both nutrient and consumer subsidies can also vary as a function of the density of the migrating popu-lation. Th is latter result is consistent with earlier studies that found that the strength of trophic interaction facilitated by

juvenile salmon can outweigh the infl uence of nutrient sub-sidies arising from spawner carcasses on zooplankton densi-ties in the highest salmon spawner density lakes (i.e. � 20 000 spawners km −2 ). Although lake nutrient concentrations can increase as a function of salmon spawner densities (Fig. 2), it is also true that higher densities of sockeye salmon spawners can give rise to high densities of planktivorous progeny (Rich et al. 2009; Appendix 2). Th e strength of the predation pressure exerted by planktivores along the salmon spawner gradient is clearly evident in our analysis of zooplankton size structure.

We found that Eubosmina longispina, a taxon known to be an important diet item of age-0 salmon (Burgner 1991), showed a 26% decrease in mean antennule size as a function of %SDN among lakes (Fig. 3A). Th is fi nding is consistent with earlier studies, which have reported that juvenile sock-eye salmon exhibit size-selective predation on Eubosmina

Table 2. Summary of analysis of covariance (ANCOVA) results test-ing the infl uence of % N derived from salmon (% N) on the anten-nule length (AL) of both bosminid species after correcting for the impact of lake grouping. The number of lakes (n 1 ) and the total num-ber of samples analyzed (n 2 ) are shown together with the coeffi cient of determination (r 2 ) of the regression with % N data. Also included are p-values for the random factor % N, the covariate lake group-ing (Lake), and the interaction of % N and Lake.

Response variable n1

p-value

n2 r2 Model % N % N

× Lake Lake

AL of E. longispina 4 67 0.36 linear <0.001 0.464 <0.001AL of B. longirostris 4 57 0.01 linear 0.356 0.336 <0.001

Figure 4. Relationships between total bosminid fl ux (open circles) or fl ux of Eubosmina longispina (closed circles) and % N derived from salmon (N isotope used in Frazer Lake) in each of the six paleolimnological records examined. Signifi cant relationships (p � 0.001) between total bosmind fl ux and % N derived from salmon were detected in three of the study lakes: Nerka (r � 0.83, n � 19; plot C), Iliamna (r � 0.92, n � 14; plot D) and Karluk (r � 0.82, n � 30; plot E). Eubosmina fl ux was signifi cantly correlated with % N derived from salmon in Nerka and Iliamna lakes (p � 0.001, r � 0.82 and 0.92, respectively; best fi t line not shown). Data for Karluk and Frazer lakes were collated from Sweetman and Finney (2003).

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the spatial subsidies is dependent on nature and magnitude of the subsidies (Knight et al. 2005, Janetski et al. 2009).

In a review of the literature, Polis et al. (1997) concluded that consumer subsidies often result in declines of in situ food resources. However, our study shows that this relation-ship is not always applicable. Specifi cally, we found SDN subsidies signifi cantly enhanced secondary production up until a very high density of juvenile salmon was attained (Fig. 4, 5). Our work also suggests that it is appropriate to revisit some resource-subsidized systems to examine whether consumer subsidies are also present. For example, migrating birds like cormorants ( Phalacrocorax sp.) can serve as impor-tant nutrient vectors for recipient ecosystems through feces (Ellis et al. 2006). However, a few other studies have revealed that these piscivorous birds can adversely aff ect resident fi sh population (Rudstam et al. 2004). Th erefore habitats used by migrating animals, which represent both nutrient and consumer subsidies, are ideal for examining the interaction among diff erent spatial subsidies in diverse ecosystems.

Acknowledgements – Th is work was supported by the Gordon and Betty Moore Foundation, Canadian Foundation for Innovation, Natural Sciences and Engineering Research Council, and National Science Foundation. We thank Bjoern Wissel for conducting part of the stable isotope analyses.

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Appendix 1

Appendix 1. Map of the six Alaskan lakes included in the paleolim-nological analyses. Appendix 2. Scatterplot showing the correlation between age-0

sockeye salmon density and previous year ’ s spawner density in 31 salmon nursery lakes from British Columbia. Th is signifi cant and positive relationship shows that higher juvenile populations are generally associated with more sockeye salmon spawners in salmon nursery lakes. Both variables are square rooted transformed (SQRT) and data are collected from Shortreed et al. (2001).

Appendix 3. Scatterplots showing the antennule length (A), carapace length (B) and mucro length (C) of all bosminids along the gradient of % N derived from salmon from the four Eubosmina-type salmon lakes (Little Togiak, Nerka, Iliamna and Red Lake). All the antennule, carapace and mucro data show a reduced body size with increased % N derived from salmon across lakes (p � 0.001, n � 67, r 2 � 0.35, 0.22 and 0.18 respectively), with the smallest bosminid remains found in Red Lake. In the ANCOVA analysis, we found that both % N derived from salmon (random factor) and lake grouping (our covariate, n � 3) were signifi cant factors (p � 0.001).