The structuring role of fish in Greenland lakes: an overview based on contemporary and paleoecological studies of 87 lakes from the low and the high Arctic
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Lakes in Greenland are species-poor ecosystems and many are fishless. We studied the structuring role of fish in lakes in high- and low-Arctic Greenland. Major differences were observed in the trophic structure of the 87 lakes studied. Pelagic zooplankton biomass was on average 3–4-fold higher in the fishless lakes and dominated by large-bodied taxa such as Daphnia, the phyllopod Branchinecta and the tadpole shrimp Lepidurus. In contrast, small-bodied crustaceans dominated the lakes with fish. Analysis of microcrustacean remains in the surface sediment and contemporary benthic invertebrates also showed a marked influence of fish on community structure and the size of the taxa present. The cascading effect of fish on the microbial communities was modest, and no differences were observed for chlorophyll a. The cascading effect of fish on invertebrates depended, however, on the species present, being largest between fishless lakes and lakes hosting only sticklebacks (Gasterosteus aculeatus), while lakes with both Arctic charr (Salvelinus arcticus) and stickleback revealed a more modest response, indicating that presence of charr modulates the predation effect of sticklebacks. It is predicted that more lakes in Greenland will be colonised by fish in a future warmer climate, and this will substantially alter these vulnerable ecosystems.
KeywordsArctic lakes Trophic structure Fish Zooplankton Phytoplankton Ciliates Heterotrophic nanoflagellates Picoalgae Bacterioplankton
The relative importance of predator and resource control in the pelagial of lakes has been extensively debated. While some authors argue for higher importance of predator control in eutrophic lakes (Sarnelle, 1992; Leibold, 1989; Jeppesen et al., 1997a, b; Jürgens & Jeppesen, 2000), others suggest that its importance is even higher in oligotrophic lakes (McQueen et al., 1986; Brett & Goldman, 1996). Based on data from 466 lakes covering a 500-fold variation in total phosphorus, Jeppesen et al. (2003) concluded that fish predation on large-bodied zooplankton related unimodally to total phosphorus (TP) (low at intermediate TP and high in both oligotrophic and hypertrophic lakes) and that predation was higher in shallow lakes than in deep lakes at all TP levels. Their data also suggest that the high predation in oligotrophic lakes does not cascade to the pelagic phytoplankton level as observed in hypertrophic lakes. A unimodal relationship has also been suggested by others (Pace et al., 1999), with low zooplankton grazing in eutrophic lakes attributed to dominance of less palatable cyanobacteria.
Lakes and ponds in the Arctic are most often oligotrophic, poor in species and have simple pelagic food web structures (Rigler, 1978; Stross et al., 1980; Hobbie, 1984; Hobson & Welch, 1995). Among fishes, Arctic charr (charr) is often the only freshwater species found in high-Arctic lakes (Hammar, 1989; Riget et al., 2000; Wrona et al., 2005; Christiansen & Reist, 2013). Further south, three-spined stickleback (G. aculeatus L. 1958, nine-spined stickleback, Pungitius pungitius (L. 1758)) and a number of salmonids, grayling (Thymallus spp.) and whitefish (Coregonus spp.) and smelt (Osmerus spp.) appear (Hammar, 1989). The zooplankton community structure is also simple and highly influenced by the presence or absence of fish (O’Brien, 1975). In the presence of fish, large-bodied cladocerans such as Daphnia pulex Leydig (1860) and D. middendorffiana are substituted by smaller species like D. longiremis Fisher (1850) (if present in the area) and Bosmina spp., and the mean size of Holopedium gibberum Zaddoch (1855), Fisher (1850) declines (O’Brien, 1975).
While the phytoplankton community often is diverse with many genera of cyanobacteria, diatoms, dinoflagellates, chrysophytes and chlorophytes, the nutrient-poor conditions often leave the Arctic lakes with less than one microgram of chlorophyll per litre and dominance of chrysophytes (Christoffersen et al., 2008a, b). The microbial loop (heterotrophic bacteria, heterotrophic nanoflagellates, HNF and ciliates) forms an important link between the primary producers and higher trophic levels in Arctic lakes based on dissolved organic carbon released from algae via grazing by zooplankton and not least the external loading of dissolved organic carbon (DOC) (Rautio et al., 2011a, b).
Greenland lakes are species-poor ecosystems and many of them are fishless. With a few exceptions, the existing fish community consists of charr, which is found in lakes and rivers all over Greenland, while in the south-western to mid regions three-spined stickleback also occurs, either as the only species or together with charr. This provides the possibility of investigating both the effects of fish on tropic structure in general and the specific effects of the three fish communities present. While it is recognised that both charr and three-spined stickleback can exert strong predation on zooplankton and zoobenthos (Dahl-Hansen, 1995), it is an open question how the two species in combination affect lake trophic structure. Evidence of interspecific competition between sticklebacks and other young salmonids (e.g. sockeye salmon, Oncorhynchus nerka (Walbaum 1752)) is unequivocal (Wotton, 1984), but knowledge of interactions with Arctic charr is scarce. While large-sized charr predate on three-spined sticklebacks (L’Abée-Lund et al., 1992; Klemetsen et al., 2002), young charr have a clear preference for small insect larvae or crustaceans and may thus have overlapping resource requirements with three-spined sticklebacks (Jørgensen & Klemetsen, 1995). Such interguild predation is common in nature and widespread across communities and ecosystems (Polis & Holt, 1992), here with charr as the top predator and sticklebacks as the intermediate predator. The ecological effects of intraguild predation include direct effects on the survival and distribution of the competing predators as well as indirect effects on the abundance and distribution of prey species and other species within the community. Intraguild predation may be beneficial for the shared prey species by lowering the overall predation pressure, particularly if the intermediate predator consumes more of the shared prey (Polis & Holt, 1992). This may be further strengthened if the intermediate predators avoid otherwise optimal habitats because of the presence of the top predator (Polis & Holt, 1992). Numerous studies have shown that three-spined sticklebacks when abundant in brackish lakes can have strong effects on both zooplankton and small benthic macroinvertebrates (Williams & Delbeek, 1989; Pont et al., 1991; Jakobsen et al., 2003, 2004), and it is therefore reasonable to assume that it may be a potential strong competitor to young and small-sized charr. Accordingly, in a series of Greenland lakes, Ignasi et al. (unpublished results) found that the condition of charr was significantly lower in lakes with sticklebacks than in lakes without, indicating competition for food. Moreover, habitat displacement was found, also suggesting competition. Whether the net effect of competition, predation and habitat displacement benefits the zooplankton is, however, not clear, although it may be assumed that predation on sticklebacks would release predation on zooplankton compared with the stickleback-only lakes, while the charr-only lakes would exhibit the weakest effect on zooplankton, given that charr also show a cannibalistic behaviour (Klemetsen et al., 2002).
We studied 87 lakes and ponds in high-Arctic North East Greenland and low-Arctic West Greenland of which 39 lakes and ponds were naturally fishless and the remaining lakes had charr and/or stickleback. In this paper, we present an overview of the effects of fish on lake trophic structure. Our hypothesis was that fish exert strong top-down effects on zooplankton and zoobenthos, whereas the effects on phytoplankton and microbes are comparatively weak due to nutrient limitation (bottom-up control). We also expected that the magnitude of the predation risk on zooplankton and small macrobenthos would decrease from stickleback-only to charr-only lakes, being lowest in charr-stickleback lakes, the latter due to charr predation on sticklebacks and habitat displacement. Our study is the most comprehensive study of Greenland lakes so far by including multitrophic quantitative levels of fish, zooplankton, surface remains of cladocerans, phytoplankton (chlorophyll a), protists, bacterioplankton and benthic invertebrates.
Materials and methods
Contemporary water samples
Composite samples were collected with a 5 l Schindler sampler at 0.5–3 m intervals (depending on the depth of the lakes) from the surface to 1 m above the bottom in the deepest part of each lake and mixed. For zooplankton analyses, 12–20 l subsamples were filtered onto a 20 μm filter and fixed in acid Lugol’s solution. For chemical analyses, a subsample of 250 ml was frozen, and for chlorophyll a a duplicate 1 l sample was filtered on a GF/C filter (Whatman) and frozen until analysis.
Lake water total phosphorus was determined as molybdate reactive phosphorus (Murphy & Riley, 1972) following persulphate digestion (Koroleff, 1970) and total nitrogen as nitrite + nitrate after potassium persulphate digestion (Solórzano & Sharp, 1980). Chlorophyll a was determined spectrophotometrically after ethanol extraction (Jespersen & Christoffersen, 1987).
Zooplankton was identified to genus/species level and counted at ×40–100 magnification (Olympus). Rotifer biomass was calculated using standard dry weights (Dumont et al., 1975; Bottrell et al., 1976), while cladoceran and copepod biomasses were calculated based on length–weight relationships (Dumont et al., 1975; Bottrell et al., 1976) based on measurements of 25 individuals of each species (when possible). The zooplankton:phytoplankton biomass ratio was calculated after converting Chla to biomass by multiplying with 66 (Jeppesen et al., 2003). This is a crude conversion factor. We therefore calculated the ratio for the lakes for which both phytoplankton biomass and chla are available. The ratio varied largely among lakes, but in both lakes with and without fish the mean conversion factor did not differ significantly from the 66. The median value was, however, 40% lower in both lakes with and without fish (unpublished data). Thus, we found no systematic difference among the lakes with and without fish that could influence the differences in the zooplankton:phytoplankton ratios.
Ciliates, HNF, bacterioplankton, picoplankton
Ciliate abundances were obtained from Lugol-preserved (3%) unfiltered water samples examined using an inverted light microscope (Olympus) at 200–400 magnification. Abundances of bacteria and heterotrophic nanoflagellates (HNF) were obtained from glutaraldehyde-preserved (2%) samples that were filtered onto 0.2 and 0.8 µm black polycarbonate filters (Osmonics), respectively, after being stained with 4,6-diamidino-2-phenylindole (DAPI) at a final concentration of 0.5 µg ml and subsequently counted in an epifluorescence microscope (Olympus BH2) at ×1250 magnification. The microscope was equipped with an ultra-violet and blue filter set with excitation and emission wavelengths of 365 and 390 nm. The counting procedure for HNF included 10 random tracks and for bacteria 10 random grids. After counting, the cell radius of minimum 25 randomly selected HNF or 100 randomly selected bacteria was measured. Biomasses were obtained by multiplying cell volumes by abundances.
Picoalgae (PA) abundance was determined by direct counting of cells from 5–10 tracks using epifluorescence microscopy (Olympus, BH-2, mounted with an HBO 103 W/2 DC OSRAM light bulb) in 5 ml aliquots of sample filtered onto a 0.2 μm white polycarbonate filter. The microscope was equipped with a blue (emission wavelength 515 nm) and a green filter (590 nm) to observe the autofluorescence. Following the counting, the cell radius of minimum 10 and up to 20 randomly selected PA was measured. Biomasses were obtained by multiplying cell volumes by abundances.
Quantitative information on fish was obtained from overnight catches using multiple mesh-sized (height 1.5 m) gill nets with 14 randomly distributed sections of 3 m (mesh size: 6.25–75 mm). Depending on lake/pond size, 4–10 nets were used in each lake. The nets were set parallel to the shore at approx. 2 m depth and in the larger lakes also at a mid-lake station. In lakes deeper than 10 m (16 lakes), both benthic (placed at the bottom) and pelagic nets (positioned at half the max depth) were used at the mid-lake station. For each net section, all fish were identified to species level, counted and weighed, and fork length was measured. Catch per unit effort in terms of number of fish net−1 night−1 (approx. 18 h) (CPUEn) was calculated for each lake based on the mean catch of all nets.
To evaluate the effect of fish on benthic invertebrates in the littoral zone, we sampled six lakes situated on the same stream system in West Greenland, of which three hosted three-spined sticklebacks, while the other three upstream lakes were fishless due to a physical barrier (steep slope). For invertebrate sampling, we used a Kajak core sampler (5.2 cm in diameter) at six randomly selected sites in the littoral zone at a depth of 0.5 m. The upper 10 cm sediment samples were filtered on a 210 μm sieve, and the retained benthic invertebrates were counted.
We further sampled surface sediment for subsequent counting of cladoceran and phyllopod remains. Three to five cores were taken with a Kajak sampler in the deepest part of the lakes or in uniform shallow lakes at a mid-lake station. From each core, the upper 0–1 cm was sampled and pooled. Wet weight and ash-free dry weight were determined on a 5 ml aliquot. Approximately 5 ml sediment was used for quantifying the zooplankton remains. The samples were weighed and boiled in 25 ml 10% KOH for 20 min to remove easily degradable organic matter and subsequently kept cold (4°C) for no longer than two weeks until taxonomical analysis was performed. To facilitate the counting, the remains were divided into two size fractions: >140 µm and 80–140 µm by filtering. Remains of cladocerans and foraminifers >80 µm were identified using a stereomicroscope (100×, Leica MZ12) and an inverted light microscope (320×, Leitz Labovert FS). Remains >140 µm were all counted except for Chydorus sphaericus (O.F. Müller 1776), which was subsampled due to high abundance. Remains in the 80–140 µm size fraction were all subsampled and about 300 remains were identified and counted. For identification, the keys of Frey (1959), Margaritora (1985), Loeblich & Tappan (1988), Hann (1990) and Røen (1995) were used. As the different fragments within the Cladocera suborder are unequally preserved, only the most abundant and the most representative fragment of a species was used for data analysis.
We used t test (accounting for equal/non-equal variance) for differences in physico-chemical variables and chlorophyll a in lakes with and without fish. Except for pH and water temperature, data were log-transformed to stabilise variance.
Due to high variability, and in some cases of presence of zeroes, we used Wilcox-non-parametric two sample tests (two-sided) for biological variables (NPAR1WAY procedure, normal approximation, SAS Institute, 1989) such as the macroinvertebrates and cladocerans in the surface sediment.
We finally performed linear regression on various biological variables against total phosphorus using region (EG, WG) as class variable. As no effect of region was found for any of the relationships during this exercise, we combined the data from the two regions.
Morphometry and nutrient state
Selected physico-chemical variables for the different regions. Zoo:phyt is the ratio between zooplankton and phytoplankton biomass (in dry weight, DW)
Surface area (ha)
Max depth (m)
Total phosphorus (μg l−l)
Total nitrogen (μg l−l)
Chlorophyll a (μg l−l)
Total zooplankton (μg DW l−l)
North East Greenland (EG)
12.3, 1.9 (0.2–213)
4.1, 1.8 (0.2–27.7)
13.7, 9 (2–81)
267, 200 (191–830)
1.2, 0.8 (0.2–4.9)
0.5, 0.2 (0–4.2)
18, 7 (7–28)
West Greenland (WG)
30.9, 21.3 (1.3–184)
15.8, 11.4 (0.9–67)
13.1, 10 (4–32)
734, 500 (120–2240)
1.3, 1.0 (0.3–5.4)
1.9, 0.7 (0.04–22)
60, 23 (28–92)
EG with fish
25.3, 5.9 (0.2–213)
7.3, 4.4 (0.6–27.7)
18.3, 9.0 (2–81)
165, 180 (40–380)
1.1, 0.8 (0.4–3.1)
0.2, 0.15 (0.0–0.9)
11, 7 (0.01–32)
EG without fish
1.5, 0.8 (0.2–8.1)
1.7, 1.5 (0.3–6.3)
9.9, 9.5 (2–29)
347, 280 (90–830)
1.3, 0.9 (0.2–4.9)
0.7, 0.5 (0.0–4.2)
48, 28 (0–167)
WG with fish
14.9, 7.3 (1.3–40.9)
18, 10.5 (1.2–67)
10.5, 9.0 (4–27)
415, 350 (120–1280)
1.3, 0.9 (0.4–3.5)
33, 28 (5–84)
WG without fish
40.2, 26 (1.5–184)
13.7, 11.5 (0.9–34)
15.4, 12.0 (5–32)
1.013, 630 (170–3240)
3.0, 1.5 (0.04–22)
143, 92 (13–538)
While no significant difference was found in depth and lake area among the water bodies with and without fish in WG (P > 0.30), the lakes with fish were deeper and larger than those without fish in EG (P < 0.001). In both areas, TN (P < 0.003 (WG) and TP (P < 0.004 (EG)) were significantly higher in lakes without fish, while no significant difference was found for TEMP (P > 0.19 and P > 0.06), pH (P > 0.09 and P > 0.10), CHLA (P > 0.94 and P > 0.87) or TP (P > 0.08 and P > 0.17) among water bodies with and without fish within each region.
When lakes in WG were divided into charr-only, stickleback-only and charr-stickleback lakes, we found no significant differences in TP (P > 0.64), TN (P > 0.42), CHLA (P > 0.29) or depth (P > 0.46) between the charr-only and stickleback-only lakes. However, TN differed (P < 0.03) between the charr-only and the charr-stickleback lakes, while both TN (P < 0.01) and CHLA (P < 0.02) were higher in the stickleback-only lakes than in the stickleback-charr lakes (Fig. 2).
Biological communities in the pelagic
Charr was the only fish species recorded in the lakes in EG. Here, charr individuals were caught in 18 of the 42 lakes. In lakes with charr, mean depth always exceeded 3 m, except in one lake in Lille Sødal (Daneborg) connected to the sea by a low-gradient stream. In WG, fish were present in 15 of the 39 water bodies. Most of the water bodies in the Kangerlussuaq area near the ice cap were devoid of fish. Only lakes connected to coastal waters via streams hosted three-spined sticklebacks, and one connected to the Kangerlussuaq Fjord had charr in low abundance (0.45 fish net−1). Physical barriers, largely steep slopes, hinder migration of fish to some lakes. In lakes with charr, their abundance was significantly (P < 0.02) higher in WG than in EG, and given the absence of sticklebacks in EG, total fish abundance was also higher (P < 0.01).
When further dividing the water bodies in WG into four categories: fishless, charr-only, both charr and sticklebacks and stickleback-only, a more diverse pattern emerged. The largest difference was found among waterbodies without fish and lakes with only sticklebacks (Fig. 2). Lakes with only sticklebacks had a significantly lower biomass of total zooplankton (P < 0.02), cladocerans (P < 0.04) and calanoid copepods (P < 0.011) and a marginally lower zooplankton:phytoplankton biomass ratio (P < 0.07), while the biomasses of small cladocerans (P < 0.05), rotifers (P < 0.0001), ciliates (P < 0.002) and HNF(P < 0.04) were all higher. Moreover, the body masses of cladocerans (P < 0.0001) and cyclopoid copepods (P < 0.01) were significantly lower than in the fishless water bodies, but significantly larger for ciliates (P < 0.007) (Fig. 2).
Lakes with both charr and sticklebacks also differed markedly from the stickleback-only lakes (Figs. 2, 3). The biomass of all cladocerans pooled (P < 0.007) as well as the biomass of small cladocerans (P < 0.001), Holopedium (P < 0.03) and calanoid copepods (P < 0.0006) was higher and so was the zooplankton:phytoplankton ratio. The higher values occurred despite a lower TN (P < 0.03) and no differences in TP or CHLA. By contrast, HNF biomass was lower than in the stickleback-only lakes. Moreover, the body masses of cladocerans (P < 0.01), cyclopoid copepods (P < 0.04) and total zooplankton (P < 0.001) were significantly larger than in the stickleback-only lakes.
Less significant differences were found between the other lake types (Figs. 2, 3). Lakes with charr only exhibited a higher ciliate biomass (P < 0.02), a higher ciliate body mass (P < 0.0001) and a higher HNF biomass (P < 0.02) than the fishless water bodies, but a lower body size of cladocerans (P < 0.05). Lakes with both charr and sticklebacks had a higher biomass of ciliates (P < 0.002) and larger body masses of ciliates (P < 0.001) and HNF (P < 0.06), but a lower body mass of cladocerans (P < 0.004), than the fishless water bodies. Finally, charr lakes with sticklebacks had a higher biomass (P < 0.04) and a larger body mass (P < 0.009) of calanoid copepods but a smaller body mass of total zooplankton than the charr-only lakes. Weaker differences between charr-only lakes and the other lake types may in part reflect the low number of these lakes (4) compared with the other categories. In none of the comparisons did we reveal any differences in biomass of PA, bacterioplankton or CHLA.
Microcrustacean remains in the surface sediment
We found major differences in zooplankton and benthic invertebrate communities among water bodies with and without fish, while the impacts of fish were less pronounced for protists and no difference was found for phytoplankton biomass expressed as CHLA.
The contemporary summer samples clearly demonstrated the effect of fish predation pressure on zooplankton community structure and body mass. It may be claimed that the snapshot approach provides a somewhat uncertain picture. Nevertheless, the results are supported by the results obtained from remains of cladocerans in the surface sediment of lakes and ponds, integrating all seasons and several years. The absence of daphnids in all but one lake with fish concurs with results from previous investigations in high-Arctic lakes where large-bodied Daphnia species were found to be restricted to shallow lakes and ponds in which fish are absent, the latter because the lakes freeze solid during winter (O’Brien 1975; Halvorsen & Gullestad, 1976; Husmann et al., 1978; Stross et al., 1980) or because of lack of contact to the sea in the past or at present. Our results showed that large-bodied Daphnia were even absent in deep lakes (> 65 m) when fish were present, even when fish occurred in low abundances. In continental Arctic lakes and in sub-Arctic lakes, smaller-sized species like D. longiremis in Canada and D. longispina (O.F. Müller 1776) in Iceland and northern Norway have been shown to co-exist with charr and occasionally also with sticklebacks if fish density is low (Dahl-Hansen, 1995). The apparently stronger effect of fish on Daphnia in the Greenland lakes may reflect that only large-bodied forms of the D. pulex complex are present. Also Alpine lakes show a strong response of fish presence on Daphnia (Anderson, 1971; Carlisle & Hawkins, 1998; Gliwicz et al., 2001; Knapp et al., 2001). By comparing oligotrophic lakes in North East Greenland and eutrophic Danish lakes, Jeppesen et al. (2003) concluded that the predation risk for large-bodied zooplankton is higher per capita fish in oligotrophic Arctic lakes than in morphometrically comparable eutrophic temperate lakes for a number of reasons: zooplankton is exposed to fish predation for a longer period before reproduction than in eutrophic temperate lakes, and higher water clarity improves the foraging success of visually hunting fish. In addition, due to a higher contribution of the benthic community to lake production, benthic–pelagic feeding fish may maintain a potentially high predation pressure on the pelagic zooplankton, even in periods when zooplankton is scarce. Finally, only large but predation-vulnerable Daphnia occurs in Greenland and often shows higher pigmentation in Arctic lakes, making them more vulnerable to predation by fish (Haney & Buchanan, 1987; Sægrov et al., 1996). High vulnerability of large-bodied zooplankton to predation in oligotrophic lakes is not restricted to the Arctic but is also found in high mountain lakes (Anderson, 1971, 1982; Paul et al., 1995).
The surface sediment data also show strong predation effects of fish on cladocerans as the abundances of resting eggs of large-bodied cladocerans (e.g. Daphnia, Simocephalus and Eurycercus) and mandibles of the phyllopod Branchinecta were almost exclusively confined to lakes and ponds without fish, whereas small-bodied forms (e.g. B. longirostris and Alona) dominated in lakes with fish. A similar pattern has earlier been detected in the more species-poor lakes and ponds in EG, where remains of Daphnia and Lepidurus only occurred in fishless lakes and ponds, while Chydorus and Alona dominated in lakes with fish only (Jeppesen et al., 2003).
The effect of predation was further evidenced by the relationships between various biotic variables and TP. While the biomass of zooplankton was not related to TP in lakes with fish (likely due to fish predation), it increased significantly with TP when fish were absent. Conversely, CHLA, bacterioplankton, HNF and PA were all related to TP in lakes with fish (Fig. 4), suggesting bottom-up regulation on phytoplankton and the microbial community. In Arctic lakes the microbial community (heterotrophic bacteria and HNF as well as ciliates) is strongly dependent on the amount and composition of dissolved organic carbon, which is partly governed by primary production and the release from soil and permafrost (e.g. Rautio & Vincent, 2006; Rautio et al., 2011b).
Our results suggest that the major effect of fish on zooplankton community structure cascades to a rather limited extent to the biomass of phytoplankton and bacterioplankton. A similar pattern was found by Jeppesen et al. (2000) in a study of 25 mainly oligotrophic to slightly eutrophic shallow lakes in the south island of New Zealand using a similar snapshot sampling approach as in the present study, while strong cascading effects on both phytoplankton and microorganisms have been found in several eutrophic and hypertrophic temperate lakes (Pace et al., 1999; Jürgens & Jeppesen, 2000). We cannot, however, fully exclude the possibility that the lack of a negative relationship between the biomasses of zooplankton versus phytoplankton and microorganisms is an artefact related to the selected snapshot sampling strategy. Thus, risk of mismatches exists, especially when dealing with fast-growing organisms such as phytoplankton and protists. While cascading effect of fish was weak for phytoplankton, our unpublished results indicate a stronger effect on benthic algae being higher in lakes with fish in lakes in Greenland.
When dividing the lakes in WG further into categories based on fish species present, a more diverse pattern emerged. Lakes with only three-spined sticklebacks showed, as hypothesised, the largest top-down effect on zooplankton. When compared with the fishless lakes and ponds, these stickleback lakes had a substantially lower biomass of total zooplankton, cladocerans and calanoid copepods, lower body masses of cladocerans and cyclopoid copepods and a lower zooplankton:phytoplankton biomass ratio, while the biomasses of small cladocerans, rotifers, ciliates and HNF as well as ciliate body mass were higher.
When sticklebacks and charr occurred together, the effect on zooplankton was somewhat lower, likely reflecting that charr predation on sticklebacks and/or foraging limitation by the sticklebacks enhanced the risk of predation. Compared with the stickleback-only lakes, these lakes exhibited higher biomasses of small cladocerans, Holopedium and calanoid copepods, higher body masses of cladocerans and cyclopoid copepods and a higher zooplankton:phytoplankton ratio, while the biomass of HNF was lower. In accordance with our results, Popadin (2002) found the size of Holopedium in three Russian lakes to differ between lakes depending on the fish stock present. They were small sized in a lake with permanent presence of nine-spined sticklebacks, intermediate sized in a lake with recent invasion of nine-spined sticklebacks and large sized in a lake with a mixed population of fish including also piscivores. Size at maturity followed the same pattern, indicating adaptation to the different fish communities (Popadin, 2002).
Lakes with only charr showed intermediate effects, with smaller cladocerans and higher abundances of ciliates and HNF than in the fishless lakes. In addition, there was a lower biomass and body mass of cladocerans but a larger body mass of total zooplankton than in charr-stickleback lakes. This suggests that sticklebacks moderate the charr predation on zooplankton. Selective predation by charr on cladocerans over copepods is a well-reported phenomenon and has in some cases affected zooplankton community composition and size structure (Nilsson & Pejler, 1973; Langeland, 1982; Dahl-Hansen et al., 1994; Eloranta et al., 2013).
The benthic communities that we studied in six lakes also suggest strong top-down control of fish (here exclusively sticklebacks) on benthic invertebrates and the effects were similar in nature and magnitude to those found in Alpine lakes (Bradford et al., 1998; Carlisle & Hawkins, 1998; Knapp et al., 2001). Large-bodied “exposed” forms were reduced or not found in lakes with fish, while the abundances of small-bodied chironomids belonging to Orthocladiinae as well as Pisidium were higher in the lakes with fish. In contrast to the study by Carlisle & Hawkins (1998) and Knapp et al. (2001), however, we did not find high abundance of oligochaetes in lakes with fish. However, the oligochaete:chironomid ratio was substantially higher than in the fishless lakes. Though such high ratios are usually attributed to eutrophication (Wiederholm, 1980), our data suggest a strong impact of fish, as has been observed in oligotrophic lakes on the Faroese Islands (Jeppesen et al., 2002) and in Danish Lake Ring (Berg et al., 1994). These effects may well cascade to the benthic algae, changing composition and biomass, though evidence of this is lacking. Given that the majority of the production in Arctic lakes is benthic (Vadeboncoeur et al., 2003; Rautio et al., 2011b), it is likely that the fish effects are even greater than demonstrated in the present study.
Major changes are expected to occur in the lakes of Greenland as a result of global warming. Lakes that are currently isolated and fishless may become colonised by fish due to increased runoff mediated by a shift from precipitation as snow to a higher proportion of rain. Lakes that today have landlocked populations of charr and sticklebacks may in a warmer future be connected to the sea, either permanently or temporarily. Our results show that appearance of fish in lakes will have drastic effects on invertebrate community structure. Analyses of remains in the sediment in a lake in North East Greenland provide further evidence of this. In this lake, a sudden shift occurred during the mid-Holocene warming period, 5000 years ago, with a pronounced reduction in the abundance of Daphnia and chironomids (Bennike et al., 2008), which is indicative of appearance of fish in the lake (Davidson et al., 2011). Today, this lake has a landlocked population of dwarf charr (Bennike et al., 2008). Recent discoveries have shown that sticklebacks are moving northwards to North East Greenland and Svalbard (Nielsen et al., 2011; Svenning et al., 2015). It is far too early, though, to evaluate the effect of sticklebacks on other trophic levels, but if the warming of the northern lakes continues it seems likely that immigration will continue to take place.
We are grateful to Henrik Skovgaard, Rie Stoor and Iben Hansen for assistance in the field. We thank Anne Mette Poulsen, Kathe Møgelvang and Tinna Christensen for manuscript assistance and layout and the technical staff at Aarhus University and University of Copenhagen for valuable support. We wish to thank the Danish Polar Centre for valuable logistic support during our stay at Zackenberg. The work was supported by the “Global Climate Change Programme” (No. 9700195), the Commission for Scientific Research in Greenland, The North Atlantic Research Programme 1998–2000, the Arctic Programme, 1998–2002, the Nordic Council of Ministers and the Danish National Science Research Council (Research Project “Consequences of weather and climate changes for marine and freshwater ecosystems. Conceptual and operational forecasting of the aquatic environment”), the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378 (http://www.mars-project.eu) and CRES, and during the writing phase by the The North Water Project (NOW) funded by the Velux Foundations and the Carlsberg Foundation.
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