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Ecol Evol
2019 Mar 01;95:2847-2862. doi: 10.1002/ece3.4963.
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Can multitrophic interactions and ocean warming influence large-scale kelp recovery?
Christie H
,
Gundersen H
,
Rinde E
,
Filbee-Dexter K
,
Norderhaug KM
,
Pedersen T
,
Bekkby T
,
Gitmark JK
,
Fagerli CW
.
Abstract
Ongoing changes along the northeastern Atlantic coastline provide an opportunity to explore the influence of climate change and multitrophic interactions on the recovery of kelp. Here, vast areas of sea urchin-dominated barren grounds have shifted back to kelp forests, in parallel with changes in sea temperature and predator abundances. We have compiled data from studies covering more than 1,500-km coastline in northern Norway. The dataset has been used to identify regional patterns in kelp recovery and sea urchin recruitment, and to relate these to abiotic and biotic factors, including structurally complex substrates functioning as refuge for sea urchins. The study area covers a latitudinal gradient of temperature and different levels of predator pressure from the edible crab (Cancer pagurus) and the red king crab (Paralithodes camtschaticus). The population development of these two sea urchin predators and a possible predator on crabs, the coastal cod (Gadus morhua), were analyzed. In the southernmost and warmest region, kelp forests recovery and sea urchin recruitment are mainly low, although sea urchins might also be locally abundant. Further north, sea urchin barrens still dominate, and juvenile sea urchin densities are high. In the northernmost and cold region, kelp forests are recovering, despite high recruitment and densities of sea urchins. Here, sea urchins were found only in refuge habitats, whereas kelp recovery occurred mainly on open bedrock. The ocean warming, the increase in the abundance of edible crab in the south, and the increase in invasive red king crab in the north may explain the observed changes in kelp recovery and sea urchin distribution. The expansion of both crab species coincided with a population decline in the top-predator coastal cod. The role of key species (sea urchins, kelp, cod, and crabs) and processes involved in structuring the community are hypothesized in a conceptual model, and the knowledge behind the suggested links and interactions is explored.
Figure 1. Photograph from Hammerfest in northern Norway, showing newly recovered Laminaria hyperborea where sea urchins Strongylocentrotus droebachiensis still are present (photograph: H. Christie)
Figure 2. A conceptual model of the main interactions between key components in the kelp/sea urchin ecosystem (cf Table 1 for a detailed description of each interaction) in the (a) southern and (b) northern part of the kelp recovery area. Positive effects are marked by â+â and negative effects by âââ. The outlined interactions are based on previous studies and existing literature. The degree of support for each interaction (cf Table 1) is indicated by arrow thicknesses from thick (strong) to thin (weak)
Figure 3. Map of northern Norway showing the distribution of the 11 sampling areas from Vega (~65.5oN, 12.5oE) to the Russian border in the northeast (and also north to ~71oN, 27oE) with relative abundance of sea urchins (Strongylocentrotus droebachiensis, green columns) and kelps (Laminaria hyperborea and Saccharina latissima, brown columns) based on a total of 1,249 stations. Presence of kelp and sea urchins is not mutually exclusive, and the total percentage might therefore exceed 100% in some areas. The number of stations in each sampling area is shown in brackets. The three climatic stations (Bud, Skrova, and Ingøy) are shown as light blue dots. Counties are shown as blue and violet sections along the coast. The borders between the barren ground area and the northern and southern kelp recovery area are indicated by dark red lines
Figure 4. Predicted curves from the GAM models showing the opposite probability of occurrence of kelp (left) and sea urchins along the coast at cobble and bedrock bottoms. Sea urchin and kelp presence was mutually exclusive on all sampled stations. See Appendix A for how the distance along the coast relates to latitude and sampling areas
Figure 5. Percentage of stations with presence of sea urchins (Strongylocentrotus droebachiensis) within sampling areas in the southern (Vega, n = 41, and Arctic Circle, n = 16) and northern (Kirkenes, n = 33) recovery zones, on the two substrate types, bedrock and cobblestone bottoms, the latter serve as a predator refuge
Figure 6. Average size (diameter ±2SE) of sea urchins (Strongylocentrotus droebachiensis) found on cobblestones (black) and bedrock (gray) along the coast. Neither maerl nor holdfast provided sufficient data to be included in the analyses. The dots show averages (±SE) at each sampling station. See Appendix A for how the distance along the coast relates to latitude and sampling areas
Figure 7. Average densities (predicted abundances per m2 ±2SE from GAM) of sea urchins (Strongylocentrotus droebachiensis) on three different substrate types (maerl beds, cobblestones, and bedrock) within the southern and northern recovery zones, and the barren zone (see map in Figure 3). The yâaxis is logâtransformed for illustrative purposes due to high sea urchin densities on maerl beds, particularly in the barren zone. The number of stations is shown at the column base
Figure 8. Landings of red king crabs (Paralithodes camtschaticus, upper panel) and edible crab (Cancer pagurus, lower panel) within different fisheries zones from the 1990s to 2011. The color codes of the curves match the fishery zones. Data are from the Norwegian Directorate of Fisheries. Yâaxis is logâtransformed to show temporal variation also at low catch levels
Figure 9. Temporal trends of coastal cod (Gadus morhua) stocks north of 62oN from 1984 to 2008 (Berg, 2012), and of king crab (Paralithodes camtschaticus) landings in eastern Finnmark, and edible crab (Cancer pagurus) landings in south Nordland. The color codes of the crab curves match the fishery zones in Figure 8 and coastal cod north of 62oN includes all fishery zones shown in Figure 8. Data are from the Norwegian Directorate of Fisheries
Figure 10. Detrended seasonal averages (a) and yearly maximum (b) sea surface temperatures (SST, measured at 1 m depth) from climatic stations at Bud (63°N), Skrova (68°N), and Ingøy (71°N; see map in Figure 3)
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