Marine shallow water areas are the parts of the Marine seabed systems M and Marine waterbody systems H that are in the euphotic zone, accordingly deep enough that sufficient light penetrates so that algae can grow. In 2018, fifteen ecosystem types were assessed, four of which are assessed as Endangered EN. The most significant impact factor for Northern kelp forest is sea urchin grazing. In the south of Norway, increased temperatures and increased runoff from land are the most significant factors.

The marine shallow waters are extremely varied and encompass habitats that range from brackish mudflats in the heart of a cove, to exposed reefs along the open coast. As a rule, these areas lie between 20 and 40 metres deep, depending on their position along the Norwegian coast. There are gradients in salinity, the amount of light, the degree of inclination (slope), waves, and currents; all of which influence the species composition. The major ecosystem types that are included in this assessment are described below.

Description of marine shallow water areas

Euphotic marine rock M1

Euphotic marine rock encompasses landscape features ranging from flat mountains, to sloping underwater crags, to almost vertical rock faces. In areas with seawater, that is with salinity between 18 and 34.8 psu (practical salinity unit), the underwater crags are dominated by algal communities that vary with the depth-related decrease in light intensity (i.e. depth) and the intensity of waves (i.e. wave action and currents). Examples of such communities are Green algae rock substrate, Red algae rock substrate, kelp forest, and strongly exposed rock substrate. In brackish areas (0.5 – 18 psu) the species composition is less familiar. Underwater crags in very exposed areas are subjected to such strong water movement energy that seaweed and kelp species fail to become established. Such ecosystem types are usually found on the outermost skerries. Those rock faces that have an extreme degree of exposure to tidal currents usually have special organism communities which are dominated by filter-feeding organisms such as dead man's fingers Alcyonium digitatum and various sea squirts (tunicates). In northern parts of Norway these communities can be affected by ice disturbance.

Of all the minor ecosystem types under M1 it is the kelp communities, as a whole, that are the most common. Kelp forest is a three-dimensional system with a large diversity of niches and therefore a large species diversity of both flora and fauna (Christie et al. 2003). They are among the most productive ecosystems on the planet (Abdullah and Fredriksen 2004) and cover large parts of the euphotic marine rock along the coast. The most common kelp species in Norway are sugar kelp Saccharina latissima, which is found in moderately exposed and sheltered areas, and tangle Laminaria hyperborea which grows in more exposed environments. Oarweed Laminaria digitata, which also grows in exposed conditions, is often found in a narrow belt, in somewhat shallower waters than tangle. The distribution of oarweed is less certain but it is probably also quite common.

Southern sugar kelp forest M1-3 has in the past 50 years had a decline in distribution, especially in Skagerrak. This is most likely due to increased temperatures and nutrients, as well as an increased level of particles and humus, that negatively influences the growth and recruitment of sugar kelp (Moy et al. 2008). These areas have been transformed into expanses dominated by filamentous algae. This situation is likely to deteriorate in the future, due to the expected continuation of global warming (including increased ocean temperatures), and increased runoff from land.

Littoral rock M3

Littoral rock has considerable variation in species composition, first and foremost related to the intensity of waves (e.g. wave exposure) and the duration of air exposure (i.e. vertical placement in the littoral zone), but also related to differences in salinity and terrain. The major type often covers small areas but occurs as a narrow band along most of Norway's long coastline. In communities in the upper part of the littoral zone barnacles, common periwinkle and blue mussels often form a characteristic narrow belt (minor types M3-6 M3-8 and M3-9), usually together with channelled wrack Pelvetia canaliculata. Further down, spiral wrack Fucus spiralis, represented by minor types M3-2 and M3-5, is common. In the most sheltered parts of the upper littoral zone it is usual to find rock substrates with green algae and barnacles (M3-3), while in the most exposed parts, the seabed is often dominated by filamentous algae. In the lower parts of the littoral rock, substrates with knotted wrack Ascophyllum nodosum (M3-1), bladder wrack Fucus vesiculosus (M3-4), and sea spaghetti Himanthalia elongata (M3-7) can be found along a wave exposure gradient.

In the ecosystem type Blue mussel beds (M3-6, M3-8, M3-9) the blue mussel Mytilus spp is usually found together with other species associated with saltwater such as the acorn barnacle Semibalanus balanoides and common periwinkle Littorina littorea just below the belt of the black lichen Verrucaria maura. There are three species of Mytilus along the Norwegian coast, these are M. edulis, M. trossulus, and M. galloprovincialis, along with individuals that are hybrids of these species (Brooks and Farmen 2013). In the past few years many reports have been received about reductions in the blue mussel stocks in Norway and other European countries (Hauge 2016). The reason is unknown but is presumed to be connected to changes in the marine environment, increased predation and occurrence of disease (Mortensen and Strohmeier, undated note).

Euphotic marine sediment M4

Euphotic marine sediment encompasses the variation from relatively sheltered areas dominated by silt and clay to comparatively exposed places dominated by gravel and small pebbles, from the littoral zone and down to the deepest part of the euphotic zone. The bottom material is unstable which implies that it can be altered by currents, wave action, and the burrowing activity of benthic fauna. The amount of organic matter varies from an almost complete absence of organic matter (sand, gravel and/or cobbles) to a seabed that is almost completely dominated by organic sediments, encompassing all grain sizes from the finest clay to cobbles. The fauna is dominated by species that live buried in the sediment (infauna) and species that live on the seabed (epifauna), while the flora consists of species that lie loosely on the seabed or are attached to pebbles and shell fragments. Unstable sediments cannot maintain communities of perennial sessile macro-algae as is the case with rock substrates.

Maerl beds (M4-11 and M4-20) are occurrences of coralline algae that grow loosely on the bottom. Maerl beds have not been systematically surveyed, but it is presumed that maerl beds are common in the north of Norway, and more unusual in the south. They are often found on sand, mud or gravel, and especially in areas with moderately strong water movement (e.g. tidal currents) that are sheltered from strong waves. Occurrences of detached coralline algae are formed by a number of species (Rinde et al. 2018), all of which can be affected to various degrees by acidification. Future scenarios indicate a complete loss of maerl beds in the Arctic in 2100, and a less severe loss in boreal regions (Brodie et al. 2014). However, field data for living maerl beds is lacking (e.g. AMAP 2013) and the temperatures and CO2, and pH levels which must be reached before negative effects can be expected for maerl beds are unclear, as well as whether this will take place in the next 50 years.

Seagrass beds M7

Seagrass beds comprise interconnected areas in shallow waters, and in the wet sand area of the littoral zone, that are dominated by plants in the Posidoniaceae, Zosteraceae, Hydrocharitaceae and Cymodoceaceae families (species with with long stems and floating leaves, usually attached to the seabed). First and foremost is eelgrass Zostera spp., although a number of other vascular plants may also dominate or have a presence. Eelgrass meadows comprise a large proportion of the seagrass beds in Norway. There is a documented reduction in a number of occurrences of eelgrass meadows in certain places in southern Norway, but there is insufficient available evidence to say whether the reduction is significant enough to warrant red-listing this major ecosystem type.

Tidal swamp M8

Halophytes are defined as plants that are adapted to a life in or closely connected to water (freshwater bottom, seabed, and/or littoral zone, and/or wetland) through the presence of air channels in the root, stems and/or leaves. The root or root stock can stand more or less permanently in water whilst the leaves and flowers rise above into the air. Macro-halophytes create a special habitat for both marine fouling organisms and benthic fauna, so that the halophyte belt as a whole has a species composition that differs significantly from communities without vascular plants, or those with more scattered vascular plants, or vascular plants with other life and growth forms. Single species stands of halophytes such as reeds Phragmites spp. are common.

Tidal rock pool seabed M9

Tidal rock pools are pools of water on bedrock in the littoral zone, that are physically separated from the ocean, that regularly, but not permanently, receive additions of seawater, and which do not have a permanent outlet to (or inlet from) the ocean. Tidal rock pools are characterised by considerable environmental variation, first and foremost in temperature and salinity, but the ecosystem type is also exposed to ice-scour. The less water the pool contains, and the more infrequently the pool receives fresh seawater, the greater the environmental variability.

The salinity decreases when large amounts of freshwater are added (e.g. with snowmelt or after heavy precipitation) and increases with extended dry periods in summer. The tendency to freeze over in winter is greater than in the ocean beyond, and in warm periods in summer the water in small rock pools can become very hot.

Marine cave and overhang M10

Marine caves receive less light compared with marine seabeds at a corresponding depth, and have a more stable environment (e.g. less wave intensity) than normal rock seabeds. Caves therefore offer good shelter for fish, larvae etc. As is the case with terrestrial caves, marine caves are known to contain specialised organisms e.g. crustaceans without pigment. Little research has been conducted into the species composition of marine caves in Norway.

Anoxic marine sediment M13

Marine sediment substrates characterised by a lack of oxygen comprise seabed systems in fjords and estuarine inlets where insufficient water circulation leads to permanently anoxic bottom conditions. As anoxic conditions require insufficient water circulation, anoxic marine seabeds are first and foremost associated with low water circulation and are therefore dominated by sediment substrates. However, the combination of anoxic conditions and rock substrates also occur.

Circulating fjord, estuary, lagoon and rock pool waterbody H2

This is a major type at the natural system level and is therefore a separate assessment entity. Circulating water masses in saline waterbodies physically separated from the ocean include ecosystems that continuously, or periodically, receive seawater and therefore satisfy the definition of brackish water or saltwater. As ecosystems, these waterbodies are partially closed systems. Discharges from land of freshwater with dissolved and particulate organic matter result in reduced salinity that often varies considerably throughout the year. In very isolated fjord arms and estuarine inlets where large rivers empty, the waters can be very brackish for parts of the year.

In fjords and estuarine inlets with shallow sills, a more or less permanent thermocline is formed between the overlying water masses with reduced salinity, and underlying hypersaline deep waters from the Atlantic Ocean (which are classified as Oceanic waterbody H1 or Anoxic marine waterbody H3). The H2 major type is characterised by water circulating for periods of the year but with large local variations driven by temperature conditions and the addition of fresh water. In some systems there is circulation in spring and autumn, corresponding to that which occurs in freshwater. Marine water bodies include ecosystems of floating, drifting, and swimming organisms in the open waters in saltwater and brackish water (salinity > 0.5 psu). With an increasing degree of isolation from the ocean and decreasing size, species that are typical for oceanic waterbodies are gradually replaced; in part with species adapted to freshwater, as well as with species with a high tolerance for variations in temperature and salinity, similar to the conditions found in rock pools.

Assessed ecosystem types

In total, nine major ecosystem types in NiN have been assessed. Under Marine seabed systems M this applies to the major types discussed above: Euphotic marine rock M1, Littoral rock M3, Euphotic marine sediment M4, Seagrass bed M7, Tidal swamp M8, Tidal rock pool seabed M9, Marine cave and overhang M10, and Anoxic marine sediment M13. Under Marine waterbody systems H, only Circulating fjord, estuary, lagoon and rock pool waterbody H2 is assessed.

In addition to the major types the expert committee has selected some minor types, or combinations of minor types under M1, M3 and M4, as assessment entities. This is due to their having a qualitatively different impact factor than those which impact on the major type; and a factor which can result in allocation to a higher Red List category.

Southern sugar kelp forest M1-3 has in the past 50 years had a reduction in distribution, especially in Skagerrak. Southern sugar kelp forest was selected as an assessment entity as it is exposed to a regional impact which is qualitatively different than that which impacts the major type. These impact factors provide a basis for a higher Red List category than that which is allocated to the major type.

From mid-Norway and northwards large areas dominated by kelp forest have in the past 40-50 years been overgrazed by sea urchins (Norderhaug and Christie 2009). Even though large expanses of kelp forest have now recovered, sea urchins still dominate enormous areas (Rinde et al. 2014). The three minor types Northern sugar kelp forest M1-3, Northern kelp forest M1-5 and Northern sublittoral rock with oarweed M1-6 are therefore selected as separate assessment entities for the north of Norway (selection criterion Type 1.3), as sea urchin grazing is considered to be an impact factor with a qualitatively different impact in the north than elsewhere in the country.

As sea urchins do not thrive in very exposed areas, it is the Northern sugar kelp forest M1-3 that has been most vulnerable to sea urchin grazing. Gundersen et al. estimated in 2011 that the affected area of sugar kelp forest in the Norwegian Sea and Barents Sea was 6500 km2, considerably less than 50 years ago. The part of the Northern kelp forest (M1-5) which grows in moderately exposed areas in the north has also been impacted by sea urchin grazing. Gundersen et al. estimated in 2011 that the affected area of kelp forest in the Norwegian Sea and Barents Sea was 2000 km2. As is the case for Northern sugar kelp forest, the Northern kelp forest ecosystem type has also partially recovered (Rinde et al. 2014), but the current total area of kelp forest is still presumed to be considerably smaller than it was 50 years ago. Northern sublittoral rock with oarweed M1-6 is usually found in a narrow area between the algal belt (seaweed) and kelp forest in wave-exposed areas. The distribution of Northern sublittoral rock with oarweed has barely been surveyed and neither has it been modelled. Therefore very little is known about the extent of the area it comprises. In the meantime it is likely that this type of ecosystem type has been exposed to the same regional effects as kelp Laminaria hyperborea during the same 50 year period; in other words, sea urchin grazing.

In addition maerl beds (M4-11 and M4-20) has also been selected as an assessment entity. Maerl beds have not been systematically surveyed, but it is thought that maerl beds are common in the north of the country and more unusual in the south.

In the past few years many reports have been received from Norway and other European countries about the reduction in blue mussel stocks (Hauge 2016). The reason is unknown but it is presumed to be associated with changes in the marine environment, increased predation, and occurrence of disease (Mortensen and Strohmeier, undated note). Blue mussel beds (M3-6, M3-8, M3-9) is therefore selected as a separate assessment entity.

Ecosystem types on the Red List

At the major type level all assessment entities under marine shallow waters are assessed as being of Least Concern LC. Four assessment entities are singled out on the basis of their having impact factors that are qualitatively different than those which impact on the major type, and where the ecosystem type has been allocated to a higher Red List category than the major type. These are Northern sugar kelp forest, Southern sugar kelp forest, Northern kelp forest and Northern sublittoral rock with oarweed. In the north of Norway, the sea urchin situation has been the determining factor for the Red List classification, and although large areas with kelp forest have now regenerated, kelp forest areas are still considerably smaller than they were 50 years ago. As sea urchins prefer less exposed areas, sugar kelp forest is most impacted, and therefore assessed as Endangered EN, while kelp forest is assessed as near threatened NT. Due to the lack of field data or other knowledge about Northern sublittoral rock with oarweed, experts have relied upon assessments of northern sugar kelp forest, and kelp forest, and agreed upon a Red List category for Northern sublittoral rock with oarweed that falls between them i.e. Vulnerable VU. For the south, the assumption of future increased temperatures and increased amounts of nutrients and particles in the sea have resulted in a Red List category of Endangered EN.

The assessments for the north of Norway are justified on the basis of a reduction in the past 50 years (criterion A) and disruption of biotic processes and interactions (criterion D). The assessment for the south is justified on the basis of a reduction in the past 50 years (criterion A) and environmental degradation (criterion C).

Also assessed were Blue mussel beds which consists of three minor types that include blue mussels, and Maerl beds which consists of two minor types which include maerl beds. Blue mussel beds are assessed as vulnerable VU. The assessments of Blue mussel beds is justified by a reduction in the past 50 years (criterion A) and environmental degradation (criterion C). For Maerl beds ocean acidification is a potential threat. However, it is not known how Maerl beds have developed in the past 50 years. Neither is it possible to predict the degree of degradation that can be expected in the next 50 years (C criterion). The potential threat that ocean acidification poses to coralline algae has therefore ensured that the ecosystem type Maerl beds is assessed as Data Deficient DD.

Impact factors

In the north, the sea urchin situation has been the determining factor for the Red List classification, and even though large areas with kelp forest have now grown back, the kelp forest areas are still much smaller than they were 50 years ago. For Southern sugar kelp forest the assumption of future increased temperatures and increased amounts of nutrients and particles in the sea, as a result of increased runoff from land, have been the determining factors. Reductions in the populations of blue mussels have been reported in many places in Norway. The reason for the decrease is unknown, but possible explanations are changes in the ocean environment, increased predation, and occurrence of disease. For Maerl beds ocean acidification is a possible future threat, but there is considerable uncertainty associated with the future scenarios for this factor.

Existing knowledge

For assessment entities without any known area of distribution (criterion B1), but where there is reason to believe they exist along the entire Norwegian coast, the minimum convex polygon (MCP) is calculated based on the coastline of the Norwegian mainland. This area is approximately 700 000 km2. Corresponding calculations are made for southern Norway and northern Norway with distribution areas of 115 000 km2 and 350 000 km2 respectively.

For natural reasons marine ecosystem types are complicated to survey. Direct observation techniques such as aerial photos and satellite imagery can only be used to a small extent to identify marine ecosystem types below the littoral zone. To a significant degree surveying has therefore been carried out using indirect methods. For example, for survey work which is part of the 'National programme to survey and monitor marine biological diversity – coastal areas' (DN handbook 19), distribution models have been developed based on point observations from the field, modelled against bottom topography and physical factors in GIS (Bekkby et al. 2011). For kelp forest and shell sand substrates there are distribution models in Naturbase (managed by the Norwegian Environment Agency) which use polygons to denote presumed presence. For the distribution (total area) of Euphotic marine sediment, as well as sugar kelp forest, the rule-based models developed by Gundersen et al. (2011) have been used. These are estimated using the environmental variables, depth, wave exposure, and degree of inclination (slope). The area of Euphotic marine sediment is estimated using the Norwegian Mapping Authority Hydrographic Services's digital bathymetric model together with a degree of inclination (a slope of < 7 degrees is presumed to be marine sediment). Shallow areas extend down to 40 metres. This is roughly the lowest point at which red algae grows along the coast, and it represents the lower depth limit for the euphotic zone on a country-wide basis. The minor types under Euphotic marine sediment can be located using sediment mapping data from the Geological Survey of Norway (NGU). However, this mapping is at present quite basic for coastal areas (< 40 m) and provides no basis for determining areas at a national level. The largest and most significant eelgrass meadows have been surveyed on a national basis and the areas have been extracted from Naturbase. These are multiplied with a proxy figure of 1.5 to provide for the inclusion of smaller meadows, as well as for those composed of species other than eelgrass. For other ecosystem types there is no available information about the total area (distribution).

None of the assessed ecosystem types under marine shallow waters are sufficiently rare that there are grounds to use the B2 criterion where occurrences are estimated in ≤ 55 10 x 10 km grid cells – not even where ecosystem types have been delimited along regional lines according to the selection criterion Type 1.3. Therefore, all assessment entities are classified as being of Least Concern LC for this criterion.

There is very little knowledge regarding the distribution of brackish ecosystem types. Neither have these been prioritised as part of the 'National programme to survey and monitor biological diversity – coastal areas'. Brackish minor types are found under the major types M1, M3, M4, M7 and M8. In order to delineate and calculate the areas of brackish ecosystem types, high resolution marine base maps (models) are required. These can capture the small-scale variation found, for example, close to the shore in bays, coves and inlets. With few exceptions the current models of salinity in Norway are inadequate. The only complete model is Norkyst800, which only has a resolution of 800 m. This means it is unsuitable for the delineation of saline, fairly brackish (5-18 psu) and brackish (0.5-5 psu) waters.

Bathymetric models are currently available for the entire Norwegian coast in 50 x 50 metre resolution. This is nevertheless too coarse to capture the fine-scale environmental variation that contributes to creating the mosaic of ecosystem types that exist in a narrow belt along the Norwegian coast. With more high-resolution bathymetric models, such as those that exist for certain areas where the seabed data has been released, there would be an entirely different basis for fine-scale modelling of ecosystem types along the coast. For areas shallower than 5-10 metres, as well as the shoreline, the solution may lie in the use of drones.

Expert Committee

The members of the expert committee for Marine shallow waters were Hege Gundersen (chair), Trine Bekkby, Kjell Magnus Norderhaug, Eivind Oug, Bjørn Gulliksen and Eli Rinde.

Acknowledgements

Many individuals and institutions have contributed to this work. The following deserve particular thanks: Hartvig Christie (NIVA) for his contribution regarding kelp forests, Marit Mjelde (NIVA) – occurrences of brackish water and tidal swamps; Mats G. Walday (NIVA) – euphotic marine rock; Pål Buhl-Mortensen (HI) – ocean acidification; and Reidulv Bøe from the Geological Survey of Norway (NGU) for contributions regarding maerl beds and ocean acidification.

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