PAR and Turbidity
In situ data from the AWIPEV-COSYNA underwater observatory close to the
estuary of the Bayelva river were analyzed over time and used as a proxy
for the development of the underwater light conditions in Kongsfjorden.
Residual calculations used for the statistical analysis of changes over
time are shown in Figure 11 and associated absolute values are presented
in Appendix 8.
Turbidity significantly (p < 0.001) increased over time with
an average numerical increase of 0.104 FTU units per year (slope per
week = 0.002 FTU * average numbers of weeks per year = 52). Even more
prominent as the absolute average increase in turbidity per year,
however, was the change in the extreme values of turbidity. Starting in
2016, the positive residuals in turbidity significantly increased until
2020 with maximal values in 2019 of up to 70 FTU. In 2021, lower values,
similar to the pre-2016 phase were observed. Contrary to the turbidity,
the average PAR values per week significantly decreased over time (p
< 0.01) from 2017 to 2021 with a numerical value of - 0.29
µmol m-2 s-1 per year. Similar to
turbidity, not only the absolute numerical PAR values per week changed
but also the seasonal character of the phases with lower photon fluence
rates seemed to change. This became especially prominent in 2020 when
PAR values lower than the expected mean were measured over the entire
year.
4. Discussion
The present investigation indicates that Arctic kelp species are
differently affected by the strong changes in environmental conditions
that are prevailing along Svalbard’s coasts. Within the relatively short
time period of 25 years, a community which used to be dominated by
‘Digitate Kelps’ transformed to an Alaria esculenta dominated
kelp forest. This change was reflected in high biomasses, leaf area
indices and adult densities of A. esculenta at 5m and 10m, depth
levels from which the other two kelp species, Saccharina
latissima and ‘Digitate Kelps’, retreated over time. However, our time
series also showed that all investigated kelp and kelp-like species,
including A. esculenta , decreased their depth distribution and
abundance along the depth gradient throughout the years. Additionally,
the biomass maximum and the whole kelp forest progressively shifted
upwards to the uppermost depth level at 2.5m. This remained the only
habitat in which all three prevailing kelp species still had a balanced
age structure between juveniles and adults of different age classes
characterizing a mature kelp forest while this relationship decreased
with depth.
Svalbard experiences considerable impacts of global warming and
Kongsfjorden is an Arctic fjord with numerous glaciers in transition
(Bischof et al., 2019b). In July and August 1997 temperatures varied
around 4°C at Hansneset in the water column down to 20m (Hanelt et al.,
2001). In contrast, between 2016 and 2021 the monthly median ocean
temperature at 11m depth was 6.1°C in August at Ny Ålesund on the
southern coast of Kongsfjorden (Gattuso et al., 2023). At the same site
the average water temperature in the surface layer (upper 10m) even
reached a maximum of 8.4°C in summer 2020
(https://dashboard.awi.de/?dashboard=2847). Over the past decades
warming air and water temperatures led to a severe decline of the
seasonal sea ice extent and thickness so that in recent winters only the
northern part of the inner bay was covered by thin sea ice (Pavlova et
al., 2019; Payne & Roesler, 2019; Maturilli et al., 2019). This
elongation of the open water period leads to an extension of the
vegetation period which theoretically promotes kelp forest depth
extension as long as it is accompanied by improved water transparency
(Castro de la Guardia et al., 2023). However, our results indicate that
this potentially positive effect of less ice scouring and reduced sea
ice cover for kelp communities gets overshadowed by the counteracting
effects of sediment plumes occurring as a consequence of increasing
glacial melt (Niedzwiedz & Bischof, 2023; Payne & Roesler, 2019).
Geyman et al. (2022) showed that glaciers on Svalbard (including
Kongsfjorden area), retreated substantially over time as a response to
warming summer temperatures. The increasing subglacial meltwater
discharge of sea-terminating glaciers is suspected to be the main source
of the increasing sedimentation in Kongsfjorden (Svendsen et al., 2002).
With their long-term analysis of satellite images Konik et al. (2021)
revealed that Kongsfjorden experiences the phenomenon of “coastal
darkening” as water transparency considerably decreased between
1997-2019. We were able to confirm this trend with in situ measurements
from the AWIPEV-COSYNA underwater observatory and provide evidence that
the turbidity of the water column has increased over time at this
coastal site while light availability for macroalgal photosynthesis
decreased. The observed lower turbidity values in 2021 may have occurred
due to the comparatively colder spring and summer temperatures in the
marine Kongsfjorden ecosystem
(https://dashboard.awi.de/?dashboard=2847). However, the location of our
sensors at the outflow of the Bayelva river is not geographically close
to our study site Hansneset and can therefore only serve as a proxy for
the general trend of decreasing light levels with increasing glacial
melt throughout Kongsfjorden.
Experimental studies have shown that most kelp species present in
Kongsfjorden are capable of coping with increasing water temperatures if
they do not surpass 10°C (Diehl & Bischof, 2021; Franke et al., 2021;
Tom Dieck, 1993). Thus, the observed increase in summer seawater
temperatures (Payne & Roesler, 2019) seemingly do not directly account
for the observed changes in kelp structure. However, laboratory studies
with early life stages by Zacher et al. (2019) indicated a potential
competitive advantage of A. esculenta over L. digitataunder future Arctic warming. A. esculenta outcompeted L.
digitata due to higher growth rates when the two species were
co-cultivated at ambient (5°C) and elevated (9-10°C) summer temperatures
but not at 15°C where A. esculenta gets close to its upper
temperature limit (Zacher et al., 2019). The assumed North Pacific
origin of the brown algae order Laminariales together with their
relatively recent introduction to the Arctic after the last glaciation
might be the reason for the generally high temperature tolerances in
Arctic kelps (Lüning 1990; Tom Dieck 1993; Adey et al., 2008).
A decreasing annual light budget and the direct and indirect effects of
sedimentation are most likely the main abiotic factors causing the
observed changes in community dynamics and upwards shift of the kelp
forest (Fragkopoulou et al., 2022; Smith et al., 2022). Ecophysiological
studies showed that an increase in turbidity and sedimentation can have
negative effects on photosynthetic rates of adult kelps (Roleda et al.,
2008), germination capacity of spores as well as recruitment success of
juvenile kelps (Roleda, 2016; Zacher et al., 2016) and thus on the
overall productivity of Arctic kelps. A. esculenta spore
germination and sporophyte recruitment thereby were less susceptible to
sediment loading than L. digitata and S. latissima (Zacher
et al., 2016). Similarly, Niedzwiedz & Bischof (2023) reported that
under the current abiotic conditions in Kongsfjorden, with low
underwater light availability and enhanced temperatures, A.
esculenta is in advantage. In contrast to S. latissima , A.
esculenta exhibited low compensation irradiance together with low dark
respiration rates and a high carbon content independent of temperature
treatments (3°C and 7°C), which support our in situ data (Niedzwiedz &
Bischof, 2023). Even though experiments by Diehl & Bischof (2021)
suggested that S. latissima is especially able to acclimate to an
increase in temperature and nutrients as well as a decrease in salinity
caused by Arctic glacial melt water, this did not seem to be a
competitive factor shaping the current kelp forest at out study site.
Between 1996 and 1998, Hop et al. (2016) extensively investigated the
macroalgal distribution at five sites along the axis of Kongsfjorden by
combining quantitative destructive samplings with video transects. The
authors report that the gradient in abiotic environmental conditions was
reflected in highest macroalgal biomass at the outer fjord locations
Kapp Mitra and Kapp Guissez while deepest macroalgal coverage was
recorded in the inner fjord at Hansneset (Hop et al., 2016). Since than
other studies on macroalgal communities in Kongsfjorden were mostly
qualitative, except for Bartsch et al. (2016). According to the
hydroacoustic mapping study from 2007, Kruss et al. (2017) showed that
the coastline along the southern shore of Kongsfjorden was nearly
exclusively covered with large macroalgae until 15m water depth, while
further down to 30m macroalgal cover became much less. A video survey
performed in summer 2009 (Schimani et al., 2022) also indicated dense
kelp forests in the center of Kongsfjorden, including Hansneset, down to
30m. The latter authors assumed that kelp distribution along the fjord
axis is controlled by the exposure to glacial melt and available hard
substrata (Schimani et al., 2022).
Kelp forests were also investigated in other Svalbard fjords and
macroalgal communities showed to be individually shaped by site specific
physio-chemical conditions. A hydroacoustic investigation supported by
underwater videos compared Isfjorden on the warm west coast of Svalbard
and Storfjorden on the colder east coast (Wiktor et al., 2022).
Macroalgal communities in both fjords were similar but macroalgal bottom
coverage in water depths above 6m was considerably less in Storfjorden
than in Isfjorden, assumingly due to higher ice scouring pressure in the
colder Arctic fjord (Wiktor Jr et al., 2022). The observed pattern in
Storfjorden may be similar to the Hansneset kelp forest from 1996/98
(Hop et al., 2012), whereas the current state (this study) might
correspond more to reports from the warmer Isfjorden, also opening to
the west coast, with highest macroalgal coverage at shallow water
depths. In 2021 the variation between the single collected replicates
from 5m and below was small, indicating a homogenous and undisturbed
macroalgal community. In contrast, at 2.5m the samples were largely
different, as one replicate was dominated by A. esculenta , one by
‘Digitate Kelps’ and the third was mixed but contained fewer adult
kelps. This heterogeneity of replicates in the shallow subtidal
indicates a heterogenous community exposed to ice scouring. Overall, the
observed increase in macroalgal biomass at 0m and 2.5m between 1996/98
and 2012/13 as well as the present investigation provides additional
evidence that the reduction of ice scouring pressure continued in 2021
(Bartsch et al., 2016; Hop et al., 2012).
In Hornsund, at the southern tip of Svalbard, kelp forest communities
along the fjord axis reflect a strong gradient in abiotic conditions
with varying distance to the glacier front (Ronowicz et al., 2020).
Compared to Hansneset, total kelp biomass at the Hornsund sites were
much lower at 5m and similar at 10m, except for the glacier free site
where kelp biomass interestingly increased with depth (Ronowicz et al.,
2020). In contrast to our study, ‘Digitate Kelps’ and S.
latissima were prominent in the glacially exposed kelp forests of
Hornsund whereas A. esculenta was only present at a site
characterized by high water transparency (Ronowicz et al., 2020). Along
the coastline of the Eastern Canadian Arctic Filbee-Dexter et al. (2022)
reported a positive correlation between the elongation of the open water
period and kelp biomass. In contrast to the biomass distribution along
the depth transect at Hansneset the latter authors observed an increase
in kelp biomass with depth from 5m to 15m across their 55 sites
indicating that the influence of ice scouring at lower depths was much
more pronounced than in Kongsfjorden. However, our findings of
decreasing kelp biomass along the depth gradient were congruent to Smith
et al. (2022) who reported a similar pattern for Laminaria
hyperborea kelp forests in the U.K. which was strongly shaped by
decreasing underwater light availability.
The Arctic kelps investigated in our study possess a differential
strategy in biomass accretion and thereby carbon allocation to perennial
structures of holdfast and stipe and annual formation of blades. While
adult ‘Digitate Kelps’ invested most biomass in their holdfast and
blades, S. latissima and A. esculenta individuals
expressed highest stipe biomasses. These ecological differences between
the three prevailing kelp species have diverse consequences. When
abundance and dominance relationships of macroalgal species at Hansneset
change over time, the 3D structure of the kelp forest and therefore the
habitat conditions for associated species shift accordingly. Epifaunal
biodiversity is highest in kelp holdfasts compared to blades and lowest
on stipes, but even though species richness is consistent between
‘Digitate Kelps’, S. latissima and A. esculenta the most
commonly associated species vary in a kelp specific manner
(Włodarska-Kowalczuk et al., 2009). Consequently, the continuous
alteration in biotic and abiotic factors at our study site has indeed
already influenced the fauna inhabiting the kelp forest as species
abundances, taxonomic composition as well as biomass distribution varied
over time (Paar et al., 2016; Niklass, 2022). Paar et al. (2016) showed
that the biomass and secondary production of associated macrozoobenthos
is strongly associated with macroalgal depth distribution as both
parameters were highest in the upper most sublittoral in 2012/13, which
represented an inverted pattern compared to 1996/98. At greater depths,
where dominant kelps are absent, other macroalgae species likeDesmarestia aculeata , Ptilota spp. and Phycodrys
rubens also strongly promote epifaunal communities (Lippert et al.,
2001; Włodarska-Kowalczuk et al., 2009), indicating their often
overlooked important role for Arctic benthic ecosystems. Furthermore,
higher trophic levels like fish are influenced by the structure and
bottom coverage of habitat forming macroalgae (Brand & Fischer, 2016).
The Arctic flora is characterized by only a small amount of endemic
Arctic species compared to those with a wider cold-temperate to Arctic
distribution. Wilce (2016) identified only 21 of 161 macroalgal species
to be Arctic endemics. In Kongsfjorden, this relation is even smaller as
has been outlined by Hop et al. (2012) who noticed that one half of the
macroalgal species encountered were truly Arctic to cold-temperate while
the other half had even wider distribution ranges and there were only
four Arctic endemic species including the kelp Laminaria
solidungula . Especially this kelp may be negatively impacted by warming
waters (Tom Dieck, 1992; Roleda, 2016). We observed that this rare
species which had only been present with very small individuals at
Hansneset (Bartsch et al., 2016; Hop et al., 2012) was not encountered
anymore in our quantitative 2021 samples. However, in other Svalbard
fjords L. solidungula is still present (Ronowicz et al., 2020;
Wiktor Jr et al., 2022). In future, macroalgal species distribution
ranges are predicted to shift northwards with an increasing number of
Atlantic species potentially spreading into the warming Arctic while
Arctic species retreat (Fredriksen et al., 2019; Krause-Jensen &
Duarte, 2014; Kortsch et al., 2012; Weslawski et al., 2010).
Kelp forests contribute
strongly to the net primary production and the coastal carbon cycle as
carbon is fixed in their biomass through photosynthesis (Krause-Jensen
& Duarte, 2016; Pessarrodona et al., 2022; Smale et al., 2022).
Pessarrodona et al. (2022) highlighted their ecological importance by
stating that the global net primary production of subtidal seaweed
forests even exceeds coastal phytoplankton productivity. Smale et al.
(2016) reported a wide average carbon standing stock of 721 g C
m-2 at 5m for Laminaria hyperborea kelp forests
along the coast of the U.K. Their conversion of biomass to carbon stock
was based on the assumption that carbon content makes up
~30% of kelp DW which included also the holdfast and
stipe DW (Smale et al., 2016). In contrast, we investigated blade carbon
content (Figure 10) and showed that the carbon content differs in a kelp
species specific manner (A. esculenta 34%, ‘Digitate Kelps’
27%, S. latissima 32%). When applying the same calculation as
Smale et al. (2016) to the overall kelp DW collected at Hansneset
(Appendix 4) we estimated 489.6 g C m-2 at 2.5m and
190.2 g C m-2 at 5m. Both values are lower compared to
the average of the U.K. kelp forests (Smale et al., 2016). But most
importantly our study showed that carbon and nitrogen allocation
strategies significantly vary between kelp species as has already
recently been shown for Alaria marginata and S. latissimafrom Alaska (Umanzor & Stephens, 2022) and cold-temperate kelp species
(Gilson et al., 2021). Consequently, the contributions of each kelp
species to the overall carbon standing stock in kelp forests can vary
according to the relative carbon content in biomass. In this respect the
observed change from a ‘Digitate Kelps’ forest into an A.
esculenta kelp forest reveals a higher potential for carbon allocation
in A. esculenta blades compared to ‘Digitate Kelps’ blades. This
may have even wider consequences for the whole carbon budget of the
surrounding waters as there is a continuous release of dissolved organic
carbon (DOC) from kelps into the surroundings (Weigel & Pfister, 2021)
which may thereby have changed the DOC budget of Kongsfjorden within the
last decade.
In Arctic fjords detached macroalgal detritus is transported to deeper
locations where they may support secondary production or biological
carbon sequestration (Cui et al., 2022; Schimani et al., 2022). Even
though not significantly different, mean blade biomass of ‘Digitate
Kelps’ (21.4 g DW) from Hansneset was nearly double compared to A.
esculenta (12 g DW) in 2021 (Figure 8). Considering that kelp blades
decay over the seasons and storm waves fragment or even detach the
thalli (Krumhansl & Scheibling, 2012) it is likely that the change in
species dominance leads to less carbon being exported for local carbon
sequestration. Together with the kelp forest retreat at our study site,
this might resemble the predicted decline in kelp forest contribution to
marine carbon cycles under the negative impacts of increasing water
turbidity (Blain et al., 2021). However, the potential contribution of
kelp forests in general to natural carbon sequestration remains a
controversially discussed topic in current research (Hurd et al., 2022;
Krause-Jensen et al., 2022; Smale et al., 2022; Pedersen et al., 2020).