Climatic and Environmental Factors Influencing Occurrence and Distribution of Macroalgae — a Fjord Gradient Revisited

Vol. 532: 73–88, 2015 MARINE ECOLOGY PROGRESS SERIES Published July 21 doi: 10.3354/meps11341 Mar Ecol Prog Ser

OPENPEN ACCESSCCESS

Climatic and environmental factors influencing occurrence and distribution of macroalgae — a fjord gradient revisited

Kjersti Sjøtun1,*, Vivian Husa1,2, Lars Asplin2, Anne Dagrun Sandvik2

1Department of Biology, University of Bergen, PO Box 7803, 5020 Bergen, Norway 2Institute of Marine Research, PO Box 1870 Nordnes, 5817 Bergen, Norway

ABSTRACT: During the last decades, trends of increasing sea water temperatures and precipitation have been observed in the North Atlantic. Increasing sea water temperatures are expected to have strong effects on coastal benthic species. Here, the distributions of macroalgae were correlated to hydrographical indexes determined from measurements at sampling and hydrographical stations along the fjord during 2 investigation periods: 1955−1956 and 2008−2009. The following indexes were used: annual maximum sea temperature, minimum salinity, and salinity stress (calculated as the difference between maximum and minimum salinity). In addition, changes in macroalgal species abundance and distribution range in the fjord were calculated. The hydrographical measurements showed higher summer temperatures and reduced salinity stress due to lower winter salinity during 2008−2009. Results from constrained ordination analyses showed that the highest variation of the macroalgal distributions along the fjord was explained by hydrographical indexes from 5 m depth, and that there were strong response differences between the algal groups. The red algae were most strongly and positively correlated with the maximum temperature gradient, and also negatively correlated with increasing salinity stress. Many red algae species also increased in abundance and their distribution ranges shifted further into the fjord in 2008−2009. The brown algae showed the highest negative correlation with increasing salinity stress, and less change in abundance or range shifts along the fjord. Some brown algae species showed a strong correlation with temperature (positive or negative). These results demonstrate that both temperature and salinity changes will impact cold temperate macroalgal communities.

KEY WORDS: Macroalgal community · Hydrography · Climate change · Fjord gradient · Species composition

INTRODUCTION to anthropogenic impacts such as nutrient enrichment (e.g. Valiela et al. 1997, Middelboe & Sand- The coast is extensively used and densely inhab- Jensen 2000, Worm & Lotze 2006, Liu et al. 2013), ited in many regions, and under great pressure interactions between nutrient enrichment and graz- worldwide. Macroalgae dominate the vegetation in ers (Lotze & Worm 2000), and increased sedimenta- the intertidal and the euphotic zone, and conse- tion (Eriksson et al. 2002, Eriksson & Johansson quently, their occurrence and abundance may be 2005). More recently there has been a strong focus strongly affected by anthropogenic activity (Walker on effects of increasing sea temperatures in coastal & Kendrick 1998). Reports of conspicuous changes areas, and a number of cases with concurrent in macroalgal composition and abundances are due changes in macroalgae range shifts (e.g. Lima et al.

© The authors 2015. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 74 Mar Ecol Prog Ser 532: 73–88, 2015

2007, Dìez et al. 2012, Tanaka et al. 2012, Duarte et causes the formation of a pronounced brackish layer al. 2013) or community compositions (e.g. Husa et in the fjords during this period. Approximately 70% al. 2008, Dìez et al. 2012, Sangil et al. 2012) have of the large river systems in Norway have now been been reported. regulated for hydroelectric power plant production Sea temperature and salinity are usually the main (Myksvoll et al. 2014), with the main part being reg- physical factors which determine regional and local ulated after 1960 (Kaartvedt 1984). The regulation distributions of macroalgae in euphotic coastal waters. includes making basins for retaining water, and as a For most macroalgal species the seasonal tempera- result of this, the seasonal pattern with a pronounced ture extremes, sometimes in combination with day peak in freshwater discharge during spring and lengths, set biogeographical boundaries for survival, early summer has changed in many of the fjords growth or reproduction (van den Hoek 1982a,b, (Kaartvedt 1984). Breeman 1988, Lüning 1990). In addition to tempera- Large scale and mainly climate-driven changes ture tolerance limits, most macroalgae also have opti- have recently been observed in coastal ecosystems mum temperature ranges for photosynthesis and (Harley et al. 2006, Parmesan 2006, Aksnes et al. growth. For European cold-temperate algae the opti- 2009, Iles et al. 2012, Hernández-Fariñas et al. mum temperature for growth is often around 15°C, or 2014). The more long-lasting the fluctuations in the in the range between 10 and 15°C (Fortes & Lüning physical environment, the greater the ecosystem 1980). In addition to affecting survival and growth impacts (Sundby & Nakken 2008). The most rate, temperature may also influence the functional- marked ecological effects of such changes include ity of macroalgae in other ways such as influencing altered composition of trophic groups and food- fecundity and thereby local abundance. For example, webs. Thus, analyzing climate-driven changes in Krueger-Hadfield et al. (2013) observed that repro- the composition of different trophic levels is imper- ductive effort in the red alga Mastocarpus papillatus ative in understanding ecosystem effects, and this was positively correlated with temperature. Local can only be done by utilizing historical data. Here, variation in salinity will also set physiological toler- changes in macroalgal distributions between 2 ance limits for marine macroalgae, or affect growth investigation periods: 1955−1956 and 2008−2009, at and functionality in several ways (Kirst 1990). In a total of 20 stations in Hardangerfjord have been estuaries, where salinity of the surface waters varies analyzed in relation to hydrographical data corre- with precipitation and freshwater run-off from land, sponding to those time periods. The data of the macroalgal communities are likely to be dominated macroalgal distribution in 1955−1956 have previ- by euryhaline species with wide tolerance limits. ously been published in Jorde & Klavestad (1963) Variation in sea temperature and other marine and the stations were reinvestigated by Husa et al. physical factors is due to both natural variability and (2014), who observed an increase in number of spe- to anthropogenic activity. Inter-annual variability is cies per station and a higher occurrence of species typically the result of large scale weather patterns as, with a more southern distribution in 2008−2009 for example, described by the North Atlantic Oscilla- compared to the data from 1955−1956. Husa et al. tion index (NAO) (Lifland 2003). Anthropogenically (2014) suggested that the changes were caused by induced variability of physical factors is to a large ex- hydrographical changes, but did not provide any tent due to greenhouse gas induced climatic changes analyses of the macroalgal data in relation to resulting in increased temperatures and precipita- hydrographical data. Here, we have compiled data tion (Scavia et al. 2002). During the last decades in - on temperature and salinity along Hardangerfjord creased sea temperatures and precipitation have from 1955−1956 and 2008− 2009. The temperature been observed in the North Atlantic (Benestad & and salinity profiles were different between the 2 Melsom 2002, Lenderink et al. 2009). Elevated tem- periods, which enabled us to demonstrate signifi- peratures and increased freshwater run-off to the cant correlations between algal distributions and sea, causing lower salinity, may be especially pro- environmental gradients derived from the hydro- nounced in estuaries. While increased precipitation graphical datasets. Furthermore, we related these may have resulted in an overall increase in fresh- correlation patterns to changes in macroalgal spe- water run-off to estuaries, the establishment of cies abundances and distribution shifts along the hydroelectric power plants has caused a strong intra- fjord. Subsequently, we were able to show differ- annual change in freshwater run-off to many fjords in ences between algal groups with regard to envi- Norway. Snow melting during spring and early sum- ronmental responses, and to examine in detail mer results in high freshwater run-off to the sea and response differences between species. Sjøtun et al.: Macroalgae distributions along a fjord gradient 75

Fig. 1. Map of Hardangerfjord study area with macroalgal sampling (1−20) and hydrographical stations (H3−H7)

MATERIALS AND METHODS ings from 2008−2009 do not include measurements from Stn H6. Data from H6 were substituted by the Hydrography averages of measurements collected at 2 new hydrographical stations placed around 8 km further inside Data describing the variability in the Hardanger- the fjord from Stn H6 and 10 km seaward of Stn H6. fjord region sea temperature over the last 60 yr were The long-term trend in precipitation was derived obtained from the Utsira coastal monitoring station, from monthly recordings from a weather station situ- operated by the Institute of Marine Research, Nor- ated close to Stn 20 (Fig. 1), in the inner part of the way. The Utsira station (59° 18’ N, 04° 52’ E) is situ- Hardangerfjord area (data available from the Norwe- ated approximately 25 km southwest of the outside gian Meteorological Institute: http://eklima. met. no). mouth of Hardangerfjord, and the monthly mean In order to evaluate the effect of hydroelectric temperature values at 10 m depth are within the power plant constructions in Hardangerfjord, the same ranges as high frequency observations from freshwater run-off data from an unregulated river inside Hardangerfjord (Asplin et al. 2014). At Utsira and from a nearby hydroelectric power plant at the station, bi-weekly salinity and temperature profiles head of Hardangerfjord in the largest fjord branch date back to 1942 (Sætre et al. 2003). Sørfjord (Fig. 1) were compared (data available Salinity and temperature were measured in Har - from the Norwegian Water Resources and Energy dangerfjord monthly at 0, 5 and 10 m depths at 5 sta- Directorate: www.nve.no/vann-og-vassdrag/Data- tions (H3−H7) distributed along the fjord gradient databaser) (Petterson 2008). (Fig. 1) during 1955−1956 (Sælen 1962). These data were compared to recent data collected at irregular intervals (from every month to every 4 months) dur- Macroalgae communities ing 2008 and 2009, and supplemented with addi- tional measurements from 1992 and 1993 from loca- The macroalgal dataset used in the present study tions close to Stn H3 and H4 (data from 5 and 10 m consists of presence-absence recordings of species during the months November 1992 and June, August from 20 shore stations situated from the outer part of and September 1993). The hydrographical record- Hardangerfjord to the innermost fjord branches. Sta- 76 Mar Ecol Prog Ser 532: 73–88, 2015

tions 1−15 are placed in the Hardangerfjord proper, In order to test whether changes in macroalgal and Stns 16−20 in fjord branches (Fig. 1). Stations distributions between 1955−1956 and 2008−2009 were first investigated during the summers of 1955 could be related to hydrographical factors, the dis- and 1956 (Jorde & Klavestad 1963), and recently dur- tributions during the 2 periods were correlated to ing June−July in 2008 and 2009 (Husa et al. 2014). hydrographical indexes constructed from measure- Sampling during 2008−2009 was carried out using ments at the hydrographical Stns H3−H7 during the the methods and dredging depths as described in 2 investigation periods. The 2 successive years of Jorde & Klavestad (1963). The majority (19 of 20) of both periods did not differ much in their extreme stations sampled during 1955−1956 were sampled in values of temperature and salinity, and the meas- 1955, and in 2008−2009, 7 stations were sampled in urements during each period were compiled in 2008 and 13 in 2009. Macroalgae were collected from order to make the indexes. Macroalgae have been intertidal (at low tide by hand) and subtidal (dredg- shown to respond quickly to environmental changes ing from a boat at 5−21 m depths) areas at each sta- (Pedersen et al. 2008). Since extreme values for tion. Taxa were sampled and identified to species hydrographical variables over the year are most level when possible, according to Husa et al. (2014); likely to have an influence on survival or growth of very small species (<1 cm), crustose species and spe- macroalgae, seasonal maximum and minimum val- cies with uncertain taxonomic status were not in- ues of temperature and salinity were used in the cluded. Species recently introduced to Norway (since analyses. Temperature and salinity of the surface 1956) were also not included in the analyses. water may be prone to large short-term variations A pronounced gradient in macroalgal species rich- due to day-to-day variations in rainfall, air tempera- ness was found along the fjord during both the early ture or the horizontal advection of water masses, (1955−1956) and recent (2008−2009) investigations, therefore, the recordings from 5 and 10 m depth with a decrease in number of species with increasing were used to construct salinity and temperature distance to the mouth of the fjord (Jorde & Klavestad indexes. The following environmental indexes were

1963, Husa et al. 2014). In order to examine whether constructed: annual maximum temperature (Tmax), species exhibited changes in range distribution along annual minimum salinity (Smin), and salinity stress the fjord, data from the 2 investigations were utilized (Sstr). Salinity stress was calculated as the maximum for calculating range shifts between the 2 studies. The annual difference of the salinity measurements at distance along the fjord from the outermost to the in- each hydrographical station. Annual minimum tem- nermost station in the longest fjord branch was 126 km. perature was not included since it did not differ The distance was divided by number of stations (n = 18) much between the 2 investigation periods or be - along the fjord length resulting in 18 sectors, each 7 km tween the hydrographical stations. The calculated long, and when adding the sectors in the other fjord index values for each hydrographical station were branches this gave an average distribution of 1.1 sta- then assigned to the closest macroalgae stations. tions per sector. The sectors were numbered, and the Index values were interpolated for areas between difference in number of sectors between the innermost Stns H7 and H6, and Stns H6 and H5, and the sectors in which each of the species was recorded dur- resulting values were assigned to the macroalgae ing the 2 investigations was noted. In order to reduce stations between each hydrographical station. the effect of randomly occurring rare species, only spe- Correlations between species distributions and the cies recorded at more than 2 stations during one or temperature and salinity indexes during the early both of the investigations were included. (1955−1956) and recent (2008−2009) investigation In order to calculate concurrent changes in each periods were performed using a direct gradient species’ local abundance in the fjord between the 2 analysis with constrained ordination (linear Con- studies, the frequencies of each species within their strained Redundancy Analysis [RDA]) (Lepš & Šmi- distribution ranges were calculated. The abundance lauer 2003) and Monte Carlo permutation tests with of each species was calculated as the frequency of unrestricted permutations for significance; all analy- occurrence between the innermost station where a ses were performed in CANOCO Ver. 4.5. Results species was present and the outermost station (Stn 1). from Stns 19 and 20 were not included in the ordina- Only species recorded at more than 2 stations during tion analyses, since these were placed in separate one or both of the investigations were included. The fjord branches with no recent hydrographical meas- relative change in abundance for each species was urements nearby. Likewise, species recorded only calculated as difference in frequency from 1955− once during one or both investigations, and species 1956 to 2008−2009. with the same distribution during both studies or Sjøtun et al.: Macroalgae distributions along a fjord gradient 77

with only ~1 recording during one of the investiga- RESULTS tions, were omitted. A total of 78 macroalgae species were included in the ordination analyses: 5 Chloro- Hydrography phyta (green algae), 36 Phaeophyceae (brown algae) and 37 Rhodophyta (red algae) (Appendix 1). Analy- Temperature plots from the hydrographical sta- ses were carried out separately for the distributions tions in Hardangerfjord (H3−H7) during 1955−1956 of green, brown and red algae. and 2008−2009 are shown in Fig. 2. Whilst the mini-

1955–1956 2008–2009 20 20 0 m 18 18 16 16 14 14 12 12 10 10 8 8 H3 H4 6 6

Temperature (°C) H5 4 4 H6 2 2 H7 0 0

20 20 5 m 18 18 16 16 14 14 12 12 10 10 8 8 6 6 Temperature (°C) 4 4 2 2 0 0

20 20 10 m 18 18 16 16 14 14 12 12 10 10 8 8 6 6 Temperature (°C) 4 4 2 2 0 0 Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

Fig. 2. Temperature recordings at 0, 5 and 10 m depths at Stns H3−H7 during earlier (1955−1956) and recent (2008−2009) investigation periods. The data plots for H6 in 2008−2009 consist of measurement averages from 2 new hydrographical stations, placed 8 km further inside the fjord from Stn H6 and 10 km seaward of H6 78 Mar Ecol Prog Ser 532: 73–88, 2015

Table 1. Overview of environmental indexes based on measurements from 5 m depth at hydrographical Stns H3−H7, used in ordination and RDA analyses of macroalgal species distributions at shore Stns 1−18. Index values for the 2 periods are indi- cated by suffixes 1955−1956 and 2008−2009. Tmax = maximum temperature, Sstr = salinity stress, and Smin = salinity minimum; changes in environmental indexes between the 2008−2009 and 1955−1956 investigation periods are displayed in italics. Loca- tions of the hydrographical Stns H3−H7 are shown in relation to shore stations (numbered). Indexes are interpolated between Stns H7 to H6, and H6 to H5

Hydrographical stn: H7 H7 H6 H6 H5 H5 H4 H3 H3 H3 Station: 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Tmax 1955−1956 14 14 14 14 14.1 14.1 14.1 14.1 14.1 13.7 13.7 13.7 13.3 13.3 14.1 14.7 14.7 14.7 Tmax 2008−2009 16.8 16.8 16.9 17 17.1 17.2 17.3 17.4 17.4 17.6 17.6 17.6 17.8 17.8 16.4 15 15 15 ΔTmax 2.8 2.8 2.9 3 3 3.1 3.2 3.3 3.3 3.9 3.9 3.9 4.5 4.5 2.3 0.3 0.3 0.3

Sstr 1955−1956 3.6 3.6 5.1 6.6 8.1 9.6 11.1 12.6 12.6 13.3 13.3 13.3 14 14 17.9 17.1 17.1 17.1 Sstr 2008−2009 5.9 5.9 6.4 6.9 7.4 7.9 8.4 9 9 10.3 10.3 10.3 11.6 11.6 10.3 7.3 7.3 7.3 ΔS(str) 2.3 2.3 1.3 0.3 −0.7 −1.7 −2.7 −3.6 −3.6 −3 −3 −3 −2.4 −2.4 −7.6 −9.8 −9.8 −9.8

Smin 1955−1956 24.2 24.2 23.6 23 22.4 21.8 21.2 20.6 20.6 20 20 20 19.4 19.4 15 16 16 16 Smin 2008−2009 23.7 23.7 23.2 22.7 22.2 21.7 21.2 20.8 20.8 18.9 18.9 18.9 16.9 16.9 19 20.2 20.2 20.2 ΔSmin −0.5 −0.5 −0.4 −0.3 −0.2 −0.1 0 0.2 0.2 −1.1 −1.1 −1.1 −2.5 −2.5 4 4.2 4.2 4.2

18 18 1st quarter 2nd quarter 16 16

C) 14 14 o 12 12

10 10

8 8

Temperature ( 6 6

4 4

2 2 1950 1960 1970 1980 1990 2000 2010 1950 1960 1970 1980 1990 2000 2010 18 18 3rd quarter 4th quarter 16 16

C) 14 14 o 12 12

10 10

8 8

Temperature ( 6 6

4 4

2 2 1950 1960 1970 1980 1990 2000 2010 1950 1960 1970 1980 1990 2000 2010 Year Year Fig. 3. Time series of temperature (°C) at 10 m depth from the Utsira coastal monitoring station for annual quarters between 1955−2009: January−March (upper left), April−June (upper right), July−September (lower left) and October−December (lower right). Temperature exhibits a linear increase across all quarters Sjøtun et al.: Macroalgae distributions along a fjord gradient 79

mum temperatures during January−March did not between 1955 and 2009 (Fig. 5). The shift in the sea- differ strongly between 1955−1956 and 2008−2009, sonal cycle of freshwater run-off into Hardangerfjord the temperatures during summer and early autumn following the large river regulations is illustrated by were clearly higher throughout the fjord in 2008− data from the regulated river at the hydroelectric 2009 compared to the measurements in 1955−1956. plant Oksla in the inner part of Sørfjord and from the This was most evident at 0 and 5 m depth, where the largest nearby unregulated river system. In the maximum temperature was 4.7 °C and 4.5 °C higher, unregulated river the freshwater discharge displayed respectively, in 2008−2009 compared to measure- a typical pattern with low values during the winter, ments from 1955−1956. The difference in maximum and a spring flood and an autumn flood with peak summer temperatures between 1955−1956 and 2008− values of around 150 m3 s−1 (Fig. 6). The discharge 2009 was highest in the inner part of the fjord proper from the regulated river at the Oksla hydroelectric (Stns 10−14) and lowest at the innermost stations power plant had a more steady discharge of fresh (Stns 15−18) (Fig. 2, Table 1). Water temperatures water on around 50 m3 s−1 (Fig. 6) with highest dis- observed at 10 m depth at Utsira coastal monitoring charge in the cold season. station (outside Hardangerfjord) revealed an upward trend from 1955 to 2009 for all quarters of the year, and the highest temperature increase was observed Macroalgae communities during summer to autumn (2nd and 3rd quarter of the year) (Fig. 3). Relatively few green macroalgae were included in Salinity measured at Stns H3−H7 in the fjord varied the study; of these, Bryopsis hypnoides showed a between the 2 periods. During 1955−1956, the late au- clear increase in both distribution and abundance, tumn-to-winter maximum salinities at Stns H4−H7 while Codium fragile subsp. fragile showed a de- were between 33 and 34 at 0 and 5 m depth, whilst crease (Fig. 7A). While many brown algae showed ranging between 28 and 31 during 2008−2009 (Fig. 4). only minor changes in abundance and distribution At the innermost hydrographical station (H3), the between the 2 investigations, some displayed large maximum salinity during 1955−1956 was 30.7 and changes; Acrothrix gracilis, Dictyota dichotoma, Stic- 33.2 at 0 and 5 m depth, respectively, and ~27 (at both tyosiphon soriferus and Striaria attenuata showed a depths) during 2008−2009. At 10 m depth, the differ- pronounced increase in both abundance and distri- ences between the 2 periods were less pronounced. bution range, while Dictyosiphon foeniculaceus and Seasonal minimum salinity during summer to early Protohalopteris radicans showed a clear decrease autumn in the fjord was slightly lower at 0 m during (Fig. 7A). There were also several species with a 2008−2009 than during 1955−1956 (Fig. 4), and large negative shift in distribution ranges and little varied between 4.2 and 15.8 during 2008−2009, and difference in abundance, e.g. Halosiphon tomen - 7.6 and 21.6 during 1955−1956, at the inner- and tosus, Battersia racemosa and Battersia arctica. These outermost hydrographical stations, respectively. The occurred sparsely in the inner parts of the fjord in results also suggest more variability between monthly 1955−1956 but were not recorded in 2008−2009. Fi- recordings of salinity at 0 m in 2008−2009 than in nally a few large and dominating species showed 1955−1956. At 5 m depth on the other hand, the min- some increase in abundance without or with only a imum salinity recordings were much higher during minor extension in distribution (Desmarestia acu - 2008−2009 than during 1955−1956 in the innermost leata, D. viridis, Saccharina latissima, and Laminaria parts of the fjord (Fig. 4, Table 1). The minimum hyperborea) (Fig. 7A). While L. hyperborea was not salinities were 16 and 14.2 in 1955−1956, and 20.2 recorded in the fjord proper at all in 1955−1956 and 19 in 2008−2009, at stations H3 and H4 respec- (Jorde & Klavestad 1963), it was recorded at the 3 tively. Further out in the fjord there was a tendency outer stations in 2008−2009. Most of the red algae towards slightly lower minimum salinity values at showed an increase in both distribution range and 5 m depth during 2008−2009 when compared with abundance (Fig. 7B), while a few showed a decrease the results from 1955−1956. At 10 m depth only small (Aglaothamnion tenuissimum, Dumontia contorta and differences in recordings of minimum salinity Furcellaria lumbricalis). A few species also displayed between 1955−1956 and 2008−2009 were found a decrease in abundance without a concurrent shift in (Fig. 4). distribution range (Polyides rotunda, Corallina offici- Precipitation data from Eidfjord in the inner part of nalis and Ceramium virgatum) (Fig. 7B). Hardangerfjord showed that there has been a more Ordination analyses revealed strong correlations than 30% increase in the monthly mean values between species distributions and the environmental 80 Mar Ecol Prog Ser 532: 73–88, 2015

1955-1956 2008-2009 H3 36 0 m 36 H4 32 32 H5 H6 28 28 H7 24 24 20 20 16 16 Salinity 12 12 8 8 4 4 0 0

36 36 5 m 32 32 28 28 24 24 20 20

Salinity 16 16 12 12 8 8 4 4 0 0

36 10 m 36 32 32 28 28 24 24 20 20

Salinity 16 16

12 12

8 8

4 4

0 0 Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep

Fig. 4. Salinity recordings at 0, 5 and 10 m depth at Stns H3− H7 during earlier (1955−1956) and recent (2008−2009) investigation periods. The data plots for H6 in 2008−2009 consist of measurement averages from 2 new hydrographical stations, placed 8 km further inside the fiord from Stn H6 and 10 km seaward of Stn H6 indexes, where gradients of maximum temperature (1955−1956 and 2008−2009). However, a lower per- and salinity stress (difference between maximum and centage of the species’ distributions were explained minimum salinity during the year) were the strongest by environmental indexes at 10 m depth, and the F- predictors. Significant correlations (p = 0.002) were values of the analyses were considerably higher when identified between distributions of red, brown and using the environmental indexes from 5 m depth. green algae and the environmental indexes from both Therefore, the environmental indexes from 5 m depth 5 and 10 m depths during the 2 investigation periods were used in the subsequent analyses (Table 1). Sjøtun et al.: Macroalgae distributions along a fjord gradient 81

500 also strong positive correlations between the algal 450 distribution pattern and both maximum temperature and minimum salinity, but the significance of the first 400 canonical axis was much higher than for all the 350 canonical axes (F-value of the first canonical axis = 300 6.3 vs. 4.2 for all). The results of the RDA analysis showed that ~16.4% of the variation of the species 250 distribution could be explained by the gradient in 200 salinity stress, and ~28.2% by all 3 canonical axes Precipitation (mm) 150 together. The distribution of B. racemosa seemed to be positively correlated with increasing salinity 100 stress, while the distributions of Cutleria multifida, S. 50 latissima and Sphacelaria cirrosa were strongly neg- 0 atively correlated (Fig. 9). Of these, B. racemosa 1960 1970 1980 1990 2000 2010 showed a decrease in abundance and/or distribution Year in 2008−2009 when compared to the first study, while Fig. 5. Monthly precipitation (mm) and trend line from ob - S. latissima and C. multifida showed an increase servations at the weather station in Eidfjord, in the inner part of the Hardangerfjord region (Fig. 9). A high number of species showed a positive association with the gradient of minimum salinity (Fig. 9). These included large perennial algae such as Distributions of the 5 species of green algae in- Fucus serratus, F. spiralis, Halidrys siliquosa and cluded in the analyses were most strongly correlated Laminara digitata and L. hyperborea. However, except with the salinity gradients (Fig. 8). The results of the for the occurrence of L. hyperborea in the outer fjord RDA analysis showed that ~18% of the variation of in 2008−2009, none of these species showed large the species distribution could be explained by the changes between the 2 surveys. In addition, the dis- gradient of minimum salinity and ~24% of all the tributions of some species were associated with the canonical axes together (F-values = 7.1 for first gradient of maximum temperature (Fig. 9). H. tomen- canonical axes, and 3.8 for all). The distribution of C. tosus, B. arctica, P. radicans, D. foeniculaceus and fragile subsp. fragile and Cladophora rupestris Asperococcus fistulosus displayed a negative corre- showed some degree of positive correlation with the lation with maximum temperature, while S. attenu- gradient of minimum salinity (Fig. 8). How- ever, the negative axis of salinity stress was not independent of the axis of minimum salinity for the green algae, which makes the interpretation of the analysis difficult. In addition, C. rupestris is an intertidal species, and environmental gradients at 5 m may not be representative for the salinity at 0 m depth. However, the decrease in the abundance and range shift of C. fragile subsp. fragile and range shift of C. rupestris in 2008−2009 compared to 1955−1956 (Fig. 7A) may be caused by greater fluctuations in salinity of the surface waters, and also an overall slight decrease in minimum salinity of the surface waters in the fjord proper during 2008−2009 (Fig. 4, Table 1). Bryopsis hypnoides showed a positive correlation with the gradient of maximum temperature (Fig. 8). The brown algae distribution showed an Fig. 6. Daily river runoff (m3 s−1) during 2008 and 2009 from the unreg- overall strong negative correlation with an ulated river Sandvenvatn (black line) and from the hydroelectric power increasing salinity stress (Fig. 9). There was plant Oksla (blue line) in the inner part of Sørfjord 82 Mar Ecol Prog Ser 532: 73–88, 2015

18 Sti sor pared to 1955−1956, while those with a pos- A Bry hyp itive correlation showed an increase (Fig. 9). 14 The distribution of the red algae showed a strong positive correlation with the gradi- Acr gra 10 Cut mul ent of maximum temperature, and subse- Mes ver Cho fla Dic dic quently a significant negative correlation Ect fas Asp bul 6 Stri at with increasing salinity stress. The F-value of the first canonical axis was substantially Sac lat Lam hyp 2 Des vir Des acu higher (13.1) than for all the canonical axes (6.8). Around 29% of the variation in the –1 –0.8 –0.6 –0.4 –0.2–2 0 0.2 0.4 0.6 0.8 1 species distribution could be explained by Abundance shift the gradient in maximum temperature, –6 Cla rup while ~36% was explained by all 3 canoni- Cod fra Pun pla cal axes together. Among the red algae spe- –10 cies, Pterothamnion plumula, Bonnemaiso- Lit lam nia hamifera, Callithamnion corymbosun, Hal tom –14 Polysiphonia elongata and Scagelia pylai- displayed the strongest correlations Dic foe Pro rad Bat rac Bat arc shift Range saei –18 with the maximum temperature gradient (Fig. 10). Another group (Cystoclonium pur- 18 B Sca pyl Bon ham pureum, Lomentaria clavellosa, Polysipho- Bon asp Gri cor Pte plu nia fu coides, and Chylocladia verticillata) 14 Phyl cr Bro bys Eut cri showed a strong negative correlation with Cer pal Sei int Phy rub Chon cr increasing salinity stress. There was also a 10 Rhod co Cys pur Call cor large group which appeared to have both a Pol elo Rho div Cer dia strong positive association with maximum 6 Pol fuc Del san temperature and a negative association with the salinity stress gradient, e.g. Phy- Cer vir 2 Poly ro Coc tru codrys rubens, Brongniartella bys soides, Bonnemaisonia asparagoides, Chondrus –1 –0.8 –0.6 –0.4 –0.2–2 0 0.2 0.4 0.6 0.8 1 Cor off crispus, Rhodomela confervoides, and Sei - Abundance shift (Fig. 10). Most species Agl ten –6 ro spora interrupta Dum con Ahn pli with a clear positive association with maxi- –10 mum temperature or temperature in combination with a reduced salinity stress, Fur lum –14 showed a clear increase in abundance and/or range shift in the fjord in 2008−2009.

–18 shift Range Only a few of the red algae species that displayed a positive association with reduced Fig. 7. Changes in range distribution and relative abundance of (A) salinity stress alone showed such an in - brown and green algae and (B) red algae, between the early (1955−1956) and recent (2008−2009) investigation periods. Negative values represent crease (Fig. 10). The distribution of Phyllo - range shifts towards the mouth of Hardangerfjord, or a decrease in abun- phora pseudoceranoides showed some pos- dance within the range of distribution compared to the first study. Spe- itive correlation with the gradient of cies name definitions are given in Appendix 1, points not labelled are not minimum salinity, but did not differ in abun- referred to in the main text or the CANOCO analyses dance or distribution in 2008−2009 compared to 1955−1956. Finally, a group of red ata showed a strong positive correlation. In addition, algae (C. officinalis, C. virgatum and P. rotunda) were the distributions of S. soriferus, D. aculeata and D. correlated with each other but were not well corre- viridis also showed some degree of positive correla- lated with any of the environmental factors, except tion with the temperature maximum gradient. Most for a weak positive association with the gradient of brown algae that displayed a negative correlation minimum salinity (Fig. 10). These also showed a with maximum temperature also showed a decrease decrease in abundance in 2008−2009 when com- in abundance and/or distribution in 2008−2009 compared to 1955−1956, which may be associated with Sjøtun et al.: Macroalgae distributions along a fjord gradient 83

Fig. 10. Ordination of red algae distributions (R), and the environmental factors: Tmax = maximum summer tempera- Fig. 8. Ordination of green algae distributions (G), and the ture, Smin = minimum salinity recordings, and Sstr = maximum environmental factors: Tmax = maximum summer tempera- variation in salinity, at the hydrographical Stns H3−H7 in ture, Smin = minimum salinity recordings, and Sstr = maximum Hardangerfjord during the 2 investigation periods. Species variation in salinity, at the hydrographical Stns H3−H7 in with increase in abundance (≥30%) and/or distribution Hardangerfjord during the 2 investigation periods. Species range (≥6 sectors) between 1955−1956 and 2008−2009 are with increases in abundance (≥30%) and/or distribution underlined; species with the same amounts of decrease in range (≥6 sectors) between 1955−1956 and 2008−2009 are abundances and/or distribution ranges are framed. Species underlined; species with the same amounts of decrease in name definitions are given in Appendix 1 abundances and/or distribution ranges are framed. Species name definitions are given in Appendix 1 DISCUSSION

The strong correlations between the distributions of macroalgae and environmental indexes at 5 m depth indicate that temperature and salinity gradients in the shallow parts are most important in determining the horizontal macroalgal distribution in Hardanger- fjord. High densities of sea urchins (Echinus acutus) and relatively little algal vegetation at many places below 2−8 m depth in Hardangerfjord has been documented in a recent (2009–2010; Husa et al. 2014) and earlier investigation (1955−1956; Jorde & Klaves- tad 1963); thus this situation seems to have persisted over the last decades. However, during summer, when salinity is at its lowest in the surface layer, Husa et al. (2014) observed no sea urchins above 8 m in Fig. 9. Ordination of brown algae distributions (B), and the Hardanger fjord. This suggests that the brackish sur- environmental factors: Tmax = maximum summer tempera- face layer during summer keeps the sea urchin den- ture, Smin = minimum salinity recordings and Sstr = maximum sity low in the shallow subtidal, and that sea urchin variation in salinity, at the hydrographical Stns H3−H7 in grazing mainly takes place below 5 m depth. Conse- Hardangerfjord during the 2 investigation periods. Species with increases in abundance (≥30%) and/or distribution quently, the vegetation will be undisturbed in the up- ranges (≥6 sectors) between 1955−1956 and 2008−2009 are per depth range where it is most exposed to seasonal underlined, species with the same amounts of decrease in temperature and salinity variations. abundances and/or distribution ranges are framed. Species One of the most conspicuous hydrographical name definitions are given in Appendix 1 changes in Hardangerfjord in 2008−2009 compared to 1955−1956 was the higher surface temperatures dur- slightly lower values of minimum salinity at 5 m in ing summer. Temperatures at 10 m depth outside the inner parts of the fjord proper in 2008−2009 com- Hardangerfjord are representative of those in Hardan- pared to 1955−1956 (Table 1). gerfjord at this depth (Asplin et al. 2014). Conse- 84 Mar Ecol Prog Ser 532: 73–88, 2015

quently the long-term trend of increasing sea temper- high degree of association with the maximum tem- atures observed at the monitoring station outside perature gradient, demonstrating a positive effect of Hardangerfjord, especially during summer, also ap- high 2008−2009 summer temperatures on many red plies to the fjord water. The temperature variations of algae. The study involved very few green algae, the upper and most brackish layer are more variable since only taxa identified to species were included in and prone to year-to-year variation in surface fluxes. the analyses. With the exception of Bryopsis hyp- However, the higher summer temperature found at all noides, the distribution of the green algae was not examined depths in Hardangerfjord during 2008− affected by high summer temperatures in 2008−2009. 2009 is in accordance with a relatively warm period The brown algae showed some positive response to (last 20 years) shown by meteorological observations the higher temperatures in the fjord during 2008− (http://folk. uib. no/ ngfhd/ Climate/climate-t-utsira. html). 2009, but less than the red algae. This is in accor- Differences in other environmental variables be - dance with red algae generally having a higher affin- tween 1955−1956 and 2008−2009 were also evident, ity to warm water compared to brown algae (Price et such as lower winter salinity of the upper layers of al. 2006, Santelices et al. 2009). A likely consequence the fjord waters and a less pronounced seasonal of higher sea temperatures in cold temperate zones is brackish layer in the fjord branch in 2008−2009. A therefore that a number of red algal species may long-term trend of decreasing salinity in the upper become more locally abundant. However, the results layers of Norwegian fjord water has also been of the present study show that the reduced salinity reported by Aksnes et al. (2009). The salinity varia- stress during summer in 2008−2009 also had a strong tions of the fjord water are due to both variations in positive effect on the occurrence of many red algae. freshwater run-off to the fjord and to variable salinity In estuaries such as Hardangerfjord, salinity may of the inflowing water from the coast. Furthermore, be more important than temperature in influencing the changes in salinity are caused by both increased the macroalgal composition, and salinity is known to precipitation in coastal areas in south Norway, and influence the ratio between red and brown algae by the fact that a large fraction of the spring and (Munda 1978, Middelboe et al. 1997, Schubert et al. autumn flood has been redistributed mainly to the 2011). Generally, red algae seem to be more sensitive winter season due to hydroelectric power production. to salinity than brown algae (Kain & Norton 1990), Around 93% of the hydroelectrical power production and hypoosmotic treatment has, for example, been made from rivers to Hardangerfjord is due to river shown to more negatively affect photosynthesis in regulations made after 1955, and 72% of this produc- red algae than in brown algae (Kirst 1990). Based on tion has come from regulations of 2 large river sys- compilations of field data collected along salinity gra- tems ending in 2 inner fjord branches (Johnsen et al. dients, Kain & Norton (1990) suggested that a salinity 2007). The data of the present study show that the around or slightly below 20 was a critically lower tol- hydroelectrical power production has resulted in erance limit for many red algae. In the present study lower fresh water run-off to Hardangerfjord during the salinity stress was the second most important spring and summer and higher run-off during winter, environmental index explaining the distribution of when compared to the natural hydrological pattern. red algae, but relatively few red algae showed a pos- The less pronounced seasonal brackish layer in the itive response to the reduced salinity stress alone. fjord branch, where salinity values at 5 m depth were The combination of high summer temperature and higher in 2008−2009 compared to 1955−1956, is thus reduced salinity stress seemed to have a more pro- most likely due to the shift in freshwater run-off to nounced positive effect on red algae. The combined the fjord. This, in combination with lower winter effects of salinities and temperatures on macroalgal salinity, is the most likely cause for the reduced salin- growth have seldom been tested, however Hanisak ity stress (i.e. difference between maximum and min- (1979) found that the green alga Codium fragile imum salinity during the year) in most parts of the subsp. fragile had a wider salinity tolerance when fjord in 2008−2009, when compared to 1955−1956. growing under optimum temperatures. Clear differences in the responses of 3 macroalgal The brown algae showed less change in abun- species groups to the environmental factors were dances and range shifts than the red algae, and were observed in the present study. The red algal species also less responsive to the increase in temperature showed a high degree of correlation with the maxi- from 1955−1956 to 2008−2009, even though some mum temperature gradient. Many species with species showed a strong correlation with the maxi- higher abundances and increased range distribu- mum temperature gradient. The strong positive corre- tions in 2008−2009 compared to 1955−1956 showed a lation between the temperature gradient and distri- Sjøtun et al.: Macroalgae distributions along a fjord gradient 85

bution of Striaria attenuata, and its increase in distri- mum salinity in the main fjord was slightly lower in bution range and abundance during 2008−2009, can 2008−2009 than in 1955−1956, and is, therefore, be attributed to the relatively high summer tempera- unlikely to be the underlying cause of the recent tures since it has a high upper temperature limit of arrival of L. hyperborea in the fjord. The occurrence survival (Peters & Breeman 1992). Some brown algae of L. hyperborea is on the other hand usually associ- exhibited a clear decrease in occurrence in 2008−2009 ated with high wave-exposure (Kain 1971), and the compared to 1955−1956, and for some species, this appearance of L. hyperborea in the outer part of the decrease can be related to the higher temperature in fjord in 2008−2009 may, therefore, be due to recent 2008−2009. Battersia arctica has a clear northern dis- changes in wind patterns causing more waves in the tribution (Prud’homme van Reine 1982, Guiry & Guiry outer area. Another example is Battersia racemosa, 2014) and could be expected to decline with an in- which appeared to have a clear positive association crease in summer temperature, and the sporophytic with increasing salinity stress and was not found in stage of Halosiphon tomentosus has been shown not 2008−2009. This species normally occurs in sandy lit- to grow at a temperature above 15°C (Sundene 1963). toral pools (Prud’homme van Reine 1982) where The apparent complete disappearance of the brown salinity can vary much over short time spans. In the algae Dictyosiphon foeniculaceus and P. radicans earlier study of the algal vegetation in Hardanger- from the area is on the other hand strange, since both fjord, Battersia racemosa was found on a few locali- species have been recorded much further south in Eu- ties in the infralittoral fringe of the innermost parts of rope than the location of the present study area the fjord proper and the fjord branches (Jorde & (Prud’homme van Reine 1982, Peters & Breeman Klavestad 1963). The decrease of this species in 1992) and they should thus be expected to tolerate Hardangerfjord may be due to low competitive abili- summer temperatures above 15°C. The abundance of ties in a presently less stressful habitat. Saccharina latissima was slightly higher in 2008−2009 When comparing the results of the present study compared to 1955−1956, and was associated with with those from the coastal area north of Hardanger- lower salinity stress. Consequently, the results of the fjord (Husa et al. 2008), some species appear to have present study suggest that summer temperatures up recently increased in abundance according to both to 18−19°C do not seem to affect S. latissima nega- studies (Table 2). However, the increase in the abun- tively, while Sogn Andersen et al. (2013) showed that dances of species in Hardangerfjord is mostly associ- temperatures above 20°C are detrimental. ated with a reduction in salinity stress in 2008−2009 The members of the Order Fucales were more compared to 1955−1956, with the exception of 2 spe- closely related to the salinity gradients than the tem- cies (Phycodrys rubens and Pterothamnion plumula), perature gradient, but their abundance and distribu- whose increase can be fully or partly attributed to tion range were relatively unaltered in 2008−2009 high summer temperatures. One of the reasons why compared to 1955−1956. This can be attributed to the the species related to decreased salinity stress have fact that species belonging to the Order Fucales are become more common in Hardangerfjord may be adapted to the littoral zone habitat which has that there has been an increase in propagule pres- extremely short time variations in salinity. The distri- sure of these species, coming from the coastal area butions of most brown algae with a pronounced outside the fjord; for example, Dictyota dichotoma increase in abundance or distribution range during 2008−2009 were associated Table 2. Macroalgae species that increased in abundance both in Hardan- with a decrease in salinity stress, either gerfjord (this study) and the coastal area outside Hardangerfjord (Husa et alone or in combination with increased al. 2008). The environmental index with the strongest association with summer temperature or an increase in each species distribution is given. Sstr = salinity stress, Tmax = maximum summer temperature, R = red algae, B = brown algae the minimum salinity. However, we can- not rule out that other environmental factors, not included in the analyses here, Species Environmental index can also be responsible for the observed Acrothrix gracilis (B) Sstr (negatively correlated) changes in the vegetation. For example, Cystoclonium purpureum (R) Sstr (negatively correlated) Laminaria hyperborea occurred in the Delesseria sanguinea (R) Sstr (negatively correlated) outer part of the fjord in 2008−2009, and Dictyota dichotoma (B) Sstr (negatively correlated) Phycodrys rubens (R) T (positively)/S (negatively) its distribution showed some positive cor- max str Pterothamnion plumula (R) Tmax (positively correlated) relation with the gradient of minimum Rhodophyllis divaricata (R) Sstr (negatively correlated) salinity in the study. However, the mini- 86 Mar Ecol Prog Ser 532: 73–88, 2015

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World-wide elec- tronic publication, National University of Ireland, bring about a further increase in precipitation and Galway. www.algaebase.org (accessed on: 24 March sea temperatures, the combined effects of sea tem- 2014) perature and salinity changes on the macroalgae Hanisak MD (1979) Growth patterns of Codium fragile ssp. vegetation in estuaries could be more important than tomentosoides in response to temperature. Mar Biol 50: 319−332 effects of temperature changes alone. Harley CDG, Hughes AR, Hultgren KM, Miner BG and others (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9: 228−241 Acknowledgements. We are grateful to Hildur Pétursdóttir Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas (Hafrannsoknanstofnunin, Iceland) for help with the RL, Coyle TA, Graham MH (2012) Effects of climate CANOCO program and interpretation of the analyses; to Anders Ruus (NIVA, Norway) for information and permis- change on global seaweed communities. 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Appendix 1. Species from 20 stations in Hardangerfjord, with name abbreviations. Nomenclature follows Guiry & Guiry (2014). *Species not included in CANOCO analyses

Taxon Abbrev. Taxon Abbrev.

CHLOROPHYTA RHODOPHYTA Blidingia minima (Nägeli ex Kützing) Kylin Bli min Aglaothamnion tenuissimum (Bonnemaison) Agl ten Bryopsis hypnoides J.V. Lamouroux Bry hyp Feldmann-Mazoyer Bryopsis plumosa (Hudson) C. Agardh Bry plu* Ahnfeltia plicata (Hudson) Fries Ahn pli Cladophora rupestris (Linnaeus) Kützing Cla rup Bonnemaisonia asparagoides (Woodward) Bon asp Codium fragile subsp. fragile (Suringar) Hariot Cod fra C. Agardh Prasiola stipitata Suhr ex Jessen Pra sti Bonnemaisonia hamifera Hariot Bon ham Ulva lactuca Linnaeus Ulv lac* Brongniartella byssoides Bro bys (Goodenough & Woodward) Schmitz PHAEOPHYCEAE Callithamnion corymbosum (Smith) Lyngbye Call cor Acrothrix gracilis Kylin Acr gra Ceramium diaphanum (Lightfoot) Roth Cer dia Ascophyllum nodosum (L.) Le Jolis Asc nod* Ceramium virgatum Roth Cer vir Asperococcus bullosus J.V. Lamouroux Asp bul Ceramium tenuicorne (Kützing) Wærn Cer ten Asperococcus fistulosus (Hudson) Hooker Asp fis Ceramium pallidum (Nägeli ex Kützing) Cer pal Battersia arctica (Harvey) Draisma, Bat arc Maggs & Hommersand Prud’homme & H.Kawai Chondrus crispus Stackhouse Chon cr Battersia racemosa (Greville) Draisma, Bat rac Chylocladia verticillata (Lightfoot) Bliding Chy ver Prud’homme & H.Kawai Coccotylus truncatus (Pallas) Wynne & Heine Coc tru (Lyngbye) Kützing Cha plu Chaetopteris plumosa Compsothamnion thuyoides (J.E.Smith) Nägeli Com thy* (L.) Stackhouse Chor fi Chorda filum Corallina officinalis Linnaeus Cor off (Müller) C.Agardh Cho fla Chordaria flagelliformis Cystoclonium purpureum (Hudson) Batters Cys pur (Hudson) C.Agardh Cla spo* Cladostephus spongiosus Delesseria sanguinea (Hudson) Lamouroux Del san (J.E. Smith) Greville, Cut mul Cutleria multifida Dilsea carnosa (Schmidel) Kuntze Dil car* (Turner) Greville) Dumontia contorta (Gmelin) Ruprecht Dum con Desmarestia aculeata (L.) Lamouroux Des acu Euthora cristata (C. Agardh) Kützing Eut cri Desmarestia viridis (Müller) Lamouroux Des vir Furcellaria lumbricalis (Hudson) Lamouroux Fur lum Dictyosiphon foeniculaceus (Hudson) Greville Dic foe Gelidium spinosum (Gmelin) Silva Gel spi* Dictyota dichotoma (Hudson) Lamouroux Dic dic Griffithsia corallinoides (L.) Trevisan Gri cor Ectocarpus siliculosus (Dillwyn) Lyngbye Ect sil Hildenbrandia rubra (Sommerfelt) Meneghini Hil rub* Ectocarpus fasciculatus Harvey Ect fas Lomentaria clavellosa (Turner) Gaillon Lom cla Elachista fucicola (Velley) Areschoug Ela fuc Lomentaria orcadensis (Harvey) Lom orc* Fucus serratus Linnaeus Fuc ser Collins ex Taylor Linnaeus Fuc spi Fucus spiralis Mastocarpus stellatus (Stackhouse) Guiry Mas ste* Linnaeus Fuc ves* Fucus vesiculosus Monosporus pedicellatus (Smith) Solier Mon ped (L.) Lyngbye Hal sil Halidrys siliquosa Palmaria palmata (L.) Kuntze Pal pal* (Lyngbye) Jaasund Hal tom Halosiphon tomentosus Phycodrys rubens (L.) Batters Phy rub Kjellman Hap glo* Haplospora globosa Phyllophora pseudoceranoides (Gmelin) Phyl ps Hinkcsia sandrina (Zanardini) Silva Hin san* Newroth & Taylor Laminaria digitata (Hudson) Lamouroux Lam dig Phyllophora crispa (Hudson) Dixon Phyl cr Laminaria hyperborea (Gunnerus) Foslie Lam hyp Plumaria plumosa (Hudson) Kuntze Plu plu* Litosiphon laminariae (Lyngbye) Harvey Lit lam Polyides rotunda (Hudson) Gaillon Poly ro Mesogloia vermiculata (Smith) Gray Mes ver Polysiphonia elongata (Hudson) Sprengel Pol elo Pelvetia canaliculata (L.) Decaisne & Thuret Pel can* Polysiphonia fibrillosa (Dillwyn) Sprengel Pol fib Protohalopteris radicans (Dillwyn) Draisma, Pro rad Polysiphonia fucoides (Hudson) Greville Pol fuc Prud’homme & H.Kawai Polysiphonia stricta (Dillwyn) Greville Pol str (Roth) Greville Pun pla Punctaria plantaginea Porphyropsis coccinea (J. Agardh Por coc* Pylaiella littoralis (L.) Kjellman Pyl lit* ex J.E. Areschoug) Rosenvinge Saccharina latissima (L.) C.E. Lane, C. Mayes, Sac lat Ptilota gunneri Silva, Maggs & Irvine Pti gun Druehl & G.W. Saunders Pterothamnion plumula (Ellis) Nägeli Pte plu (Lyngbye) Link Scy lom Scytosiphon lomentaria Pterosiphonia parasitica (Hudson) Falkenberg Pte par* (Roth) Kützing Spe par Spermatochnus paradoxus Rhodomela confervoides (Hudson) Silva Rhod co (Roth) C.Agardh Sph cir Sphacelaria cirrosa Rhodomela lycopodioides (L.) C. Agardh Rhod ly* Nägeli ex Kützing Sph nan* Sphacelaria nana Rhodophyllis divaricata (Stackhouse) Papenfuss Rho div Zanardini Sph plu* Sphacelaria plumula Scagelia pylaisaei (Montagne) M.J. Wynne Sca pyl (Lyngbye) Sph cae Sphaceloderma caespitulum Seirospora interrupta (Smith) Schmitz Sei int Draisma, Prud’homme & H.Kawai Schmitzia hiscockiana Maggs & Guiry Sch his* Spongonema tomentosum (Hudson) Kützing Spo tom Spermothamnion repens (Dillwyn) Rosenvinge Spe rep* Stictyosiphon soriferus (Reinke) Rosenvinge Sti sor Vertebrata lanosa (L.) T.A. Christensen Ver lan* Stictyosiphon tortilis (Ruprecht) Reinke Sti tor Striaria attenuata (C. Agardh) Greville, Stri at (Greville) Greville Tilopteris mertensii (Turner) Kützing Til mer

Editorial responsibility: Morten Pedersen, Submitted: August 19, 2014; Accepted: May 11, 2015 Roskilde, Denmark Proofs received from author(s): July 6, 2015