BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-14-5069-2017Seagrass as major source of transparent exopolymer particles in the
oligotrophic Mediterranean coastIuculanoFrancescafiuculano@imedea.uib-csic.esDuarteCarlos MariaMarbàNúriahttps://orcid.org/0000-0002-8048-6789AgustíSusanahttps://orcid.org/0000-0003-0536-7293Department of Global Change Research, Instituto Mediterráneo de Estudios Avanzados (IMEDEA), CSIC-UIB, Esporles, 07190, Balearic Islands, SpainKing Abdullah University of Science and Technology (KAUST), Red Sea Research Center (RSRC), Thuwal, 23955-6900, Saudi ArabiaFrancesca Iuculano (fiuculano@imedea.uib-csic.es)15November201714225069507523December20169January20175September201724September2017This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/14/5069/2017/bg-14-5069-2017.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/14/5069/2017/bg-14-5069-2017.pdf
The role of seagrass, Posidonia oceanica, meadows as a source of
transparent exopolymer particles (TEPs) to Mediterranean coastal waters was
tested by comparing the TEP dynamics in two adjacent coastal waters in the
oligotrophic NW Mediterranean Sea, one characterized by oligotrophic open-sea
waters and the other accumulating seagrass leaf litter, together with an
experimental examination of TEP release by seagrass litter. TEP
concentrations ranged from 4.6 to 90.6 µg XG (xanthan
gum) Eq L-1, with mean (±SE) values of
38.7 (± 2.02) µg XG Eq L-1 in the site devoid of
seagrass litter, whereas the coastal beach site accumulating leaf litter had
> 10-fold mean TEP concentrations of
487.02 (± 72.8) µg XG Eq L-1. Experimental evaluation
confirmed high rates of TEP production by P. oceanica litter,
allowing calculations of the associated TEP yield. We demonstrated that
P. oceanica is an important source of TEPs to the Mediterranean Sea,
contributing an estimated 76 Gg C as TEPs annually. TEP release by
P. oceanica seagrass explains the elevated TEP concentration
relative to the low chlorophyll a concentration in the Mediterranean Sea.
Introduction
Transparent exopolymer particles (TEPs) are acidic and sulfated
polysaccharides enriched in deoxy sugars and galactose (Myklestad, 1995)
which are stainable with alcian blue (Alldredge et al., 1993). These organic
particles belong to the POC (particulate organic carbon) pool (Zhou et al.,
1998) and are ubiquitous in marine and limnetic ecosystems (Passow, 2002).
Their roles in several biogeochemical processes and their importance in
sedimentary carbon fluxes has been extensively documented (Engel and Passow,
2001) as, due to its sticky properties, the aggregation of these particles
may enhance the sinking flux and export of organic matter (Kiørboe and
Hansen, 1993; Simon et al., 2002) with important consequences for the
efficiency of the biological carbon pump (Mari et al., 2017, and references
therein). Phytoplanktonic cells, mainly diatoms, are believed to be the major
sources of TEPs in the marine environment (Passow and Alldredge, 1995a),
although benthic organisms, such as suspension feeders (Heinonen et al.,
2007) and macroalgal detritus (Thornton, 2004), have been also identified as
TEP sources. Indeed, marine macrophytes are important sources of dissolved
organic carbon (DOC) to coastal waters (Barrón et al., 2006) and may
therefore release precursors conducive to TEP formation, such as reported by
Thornton (2004) for macroalgae. However, seagrass meadows are also important
sources of DOC to the marine environment (Barrón et al., 2014), but their
role as a source of TEPs has not yet been assessed.
Posidonia oceanica Delile (L.) is the dominant seagrass species of
the Mediterranean Sea (Duarte, 2004). P. oceanica meadows are highly
productive (Duarte and Chiscano, 1999) and release high amounts of dissolved
organic carbon (Barrón et al., 2014) as well as leaf litter (Cebrian and
Duarte, 2001; Gacia et al., 2002). The large production of DOC and detritus
by P. oceanica contrasts with the low planktonic primary production
in the oligotrophic Mediterranean littoral zone (Duarte et al., 1999), where
TEPs are nevertheless present (Mari et al., 2001; Beauvais et al., 2003;
Prieto et al., 2006; Ortega-Retuerta et al., 2010; Bar-Zeev et al., 2011) at
levels higher than expected, as indicated by high TEP / Chl a and
TEP / bacterial abundance ratios compared to other marine systems
(Ortega-Retuerta et al., 2010, 2017). Whereas TEPs are often assumed to be of
phytoplankton origin, the relatively high levels of TEPs (i.e. high
TEP / Chl a ratios) in oligotrophic Mediterranean waters suggest that
DOC release by Posidonia oceanica meadows could be a source of TEPs,
explaining the relative high TEP concentration reported for Mediterranean
waters (Ortega-Retuerta et al., 2010). Although macroalgae have been
identified as sources of TEPs, we are not yet aware of any study examining
the role of seagrass as source of TEPs. In this study, we monitored the
dynamics of TEP concentrations in two adjacent, but contrasting, oligotrophic
littoral sites of Majorca (NW Mediterranean Sea), an open coastline flushed
with open seawaters and an adjacent, 2 km, beach accumulated
Posidonia oceanica leaf litter. We tested the hypothesis that
seagrass leaf litter of P. oceanica represents an important source
of TEPs to this ecosystem, explaining the contrasting TEP concentrations and
dynamics observed in these coastal sites using a laboratory experiment.
Materials and methodsSampling sites and time-series observations
The study was carried out at two sites on the coast of the island of Majorca, Balearic Islands, NW Mediterranean Sea:
the Faro Cap Ses Salines experimental field
station (lat 39.264724∘ N, long 3.054446∘ E), where TEP concentrations were monitored fortnightly for 3 years
starting in January 2012. This is a pristine and oligotrophic rocky shore
ecosystem, with an extensive seagrass of P. oceanica meadow extended around 500 m
offshore (Álvarez et al., 2015) and flushed with open-sea water (Fig. 1a).
Es Caragol beach (lat 39.276784∘ N, long
3.043779∘ E), where TEP dynamics were monitored for 2
years starting in August 2012. This is a natural sandy beach at a site of
community importance (EU directive-red natura2000) where abundant seagrass
detritus accumulates on the shore (Fig. 1b), where it plays an important
geomorphological role (Simeone and De Falco, 2012).
Surface water samples at Faro Cap Ses Salines and Es Caragol were collected
fortnightly (monthly during winter months) in 2 L Nalgene bottles at noon
and 15:00, respectively. A total of 76 sampling events were completed at
Faro Cap Ses Salines between 9 January 2012 and 23 March 2015, while 45 sampling events were completed at Es Caragol
(from 9 August 2012 to 24 September 2014). Surface seawater samples of 250 mL from Faro Cap Ses
Salines for chlorophyll a determination were filtered through Whatman GF/F
filters and stored at -20 ∘C. Filters were extracted in 6 mL 90 % acetone for 24 h followed by fluorometric (Trilogy, Turner
design) Chl a determination, calibrated with pure Chl a, after Parsons et al. (1984).
Sea-surface temperature was measured in situ using a data logger (HOBO).
The two sites monitored at Cap Ses Salines (a) and at Es
Caragol beach (b), Majorca, NW Mediterranean Sea.
TEP concentrations were determined following the colorimetric method of
Passow and Alldredge (1995b), where TEPs are detected after staining with
alcian blue (Sigma), a cationic copper phthalocyanine dye that complexes
carboxyl (-COO-) and half-ester sulfate (OSO3-) reactive groups
of acidic polysaccharides. Following each sampling event, triplicate
aliquots (Faro Cap Ses Salines: 300–700 mL; Es Caragol: 50–500 mL, depending
on the saturation of filters) were filtered through 0.4 µm pore size, 25 mm diameter polycarbonate filters under low and constant pressure
(150 mm Hg). Filters were subsequently stained with 1000 µL of a 0.02 %
working solution of alcian blue (pre-filtered through 0.2 µm) in 0.06 % acetic acid (pH = 2.5), allowed to stain for a few seconds, repeated
filtering and rinsed twice with Milli-Q water, to eliminate excess dye. Dyed
filters were stored at -80 ∘C until extraction at IMEDEA
laboratory. To perform the extraction, filters were placed in acid-cleaned 10 mL glass tubes, by adding 5 mL of 80 % sulfuric acid, for 2 to 3 h,
shaking two to three times to enhance extraction. Absorbance was read
spectrophotometrically (Shimadzu dual-beam spectrophotometer) at 787 nm in 1 cm disposable cuvettes. Triplicate blank filters were also analysed for
every batch of samples. Blank absorbance values at 787 nm were then
subtracted from the total absorbance values of samples, to account for the
capacity of alcian blue to stain filters. Four calibrations of the alcian
blue solutions were performed by using xanthan gum as standard (XG). The
calibration factor (F) was calculated as the mean of the eight estimates
obtained. TEP concentrations (TEP) were expressed in µg xanthan gum
(XG) equivalents per litre (µg XG Eq L-1) and calculated
following Eq. (1):
TEP=asample-ablankV-1×F,
where asample and ablank are absorbance values at 787 nm for
samples and blank filters, respectively; V is the sampled volume (in L) and
F is the calibration factor. The detection limit of the method was 2.2 µg XG Eq L-1, and the analytical
coefficient of variation was 13 %. TEP concentrations were transformed to carbon units (µg C L-1) by using the conversion factor of 0.75 proposed by Engel and
Passow (2001) in order to estimate the total TEP yield of P. oceanica leaf litter.
Experimental evaluation of TEP release by P. oceanica leaf
litter
P. oceanica leaf litter and surface seawater were sampled on 8 September 2014, the period
of leaf shedding for P. oceanica, from the seashore of Es Caragol and stored at 4 ∘C for transport to the laboratory. Six 5 L Pyrex glass
bottles were filled with seawater, pre-filtered by gravity through a 0.2 µm pore membrane size cartridge filter. Three replicated bottles
received 16.6 mg fresh weight L-1 of P. oceanica leaf litter, to obtain a final
concentration similar to that measured in the nearshore waters at Es
Caragol, and three replicated bottles, without P. oceanica leaf litter, were used as
control. The bottles were gently aerated with an air pump to provide mixing
and avoid the development of anoxic conditions. The bottles were incubated
at the in situ temperature at the time of sampling (26.3 ∘C) in a
temperature-controlled chamber, and water samples of TEP determinations
were collected at increasing time intervals: time 0 (11 September), 6,
12, 24, 48, and 264 h (22 September) after the start of
the experiment. The water volume and leaf biomass (fresh weight and dry
weight following desiccation at 60 ∘C for 24 h in a
drying oven) in the bottles were measured. Replicated 50 to 100 mL
volumes, pre-filtered through a 100 µm mesh to remove leaf litter,
were sampled using a 60 mL syringe and immediately filtered through 0.4 µm to collect, dye, and quantify TEP concentration following the procedure
described above (Passow and Alldredge, 1995b).
Time series of TEP concentrations
(µg XG Eq L-1± SE) and temperature (∘C) at
Cap Ses Salines (a) and Es Caragol beach (b).
Results
Surface seawater temperature ranged from 12.4 to 27.8 ∘C, registered in February 2012 and September 2014,
respectively, during the study (average ± SE = 19.4 ± 0.54 ∘C). Chlorophyll a concentration
ranged from 0.02 to 0.54 µg L-1 in July 2014 and March 2013, respectively, during the
study (average ± SE = 0.23 ± 0.01 µg L-1).
TEP concentrations ranged from 4.6 to 90.6 µg XG Eq L-1 in Faro
Cap Ses Salines and from 26.8 to 1878.4 µg XG Eq L-1 in Es
Caragol, with significantly (paired t test, p < 0.05) higher mean TEP
concentrations at Es Caragol (38.7 ± 2.02 µg XG Eq L-1)
compared to Faro Cap Ses Salines (487.02 ± 72.8 µg XG Eq L-1). TEP concentrations changed greatly seasonally, with maximum TEP
values in waters sampled at the Faro Cap Ses Salines observed in February,
likely associated with the phytoplankton bloom occurring at that time, and
June (Fig. 2a). In contrast, TEP dynamics showed a more erratic temporal
pattern at Es Caragol, with no clear seasonal patterns (Fig. 2b). Mean
(±SE) TEP / Chl a ratios were also > 10-fold greater at Es
Caragol (3109.9 ± 468.9) than at the Faro Cap Ses Salines (286.3 ± 55.7), with a clear seasonal cycle
characterized by maximum TEP / Chl a ratios in June and July at the Faro Cap Ses Salines, whereas at Es Caragol
they remained elevated throughout the year, except between January and March
when values were relatively low (Fig. 3a, b).
During the experimental evaluation initial TEP concentrations (30.4 µg XG Eq L-1) increased slightly after 6 h incubation, to remain uniform
throughout the rest of the experiment in the absence of P. oceanica leaf litter (Fig. 4). In contrast, TEP concentrations increased greatly throughout the
experiment in the presence of P. oceanica litter, reaching values of 1551 µg XG Eq L-1, comparable to maximum values observed at Es
Caragol, after 264 h (Fig. 4). The corresponding TEP yield of P. oceanica corresponded to 14.128 ± 11.294 µg XG Eq L-1 or
2344 ± 357.26 µg C g DW-1. The yield of TEPs in the presence of P. oceanica litter was 9.77 times
greater than that in control bottles (1.384 ± 1.582 µg XG Eq L-1).
Monthly TEP / Chl a ratios means ± SE at Cap Ses
Salines (a) and Es Caragol beach (b).
Discussion
The results presented provide, to the best of our knowledge, the first
evidence that seagrass leaf litter is a source of TEPs to coastal waters.
Thornton (2004) demonstrated the formation of TEPs from the acidic
polysaccharides released by macroalgal detritus of different species, but the
role of seagrass litter as a source of TEPs has not been reported to date. The
role of P. oceanica leaf litter as a source of TEPs is demonstrated
here through the > 10-fold difference in concentration and
TEP / Chl a ratios between the two adjacent coastal areas studied, one
containing rapidly flushed open-sea water and the other representing an
accumulation site for P. oceanica leaf litter. The experimental
evidence reported further confirms the role of TEPs formed by precursors
released by P. oceanica leaf litter, together with the associated
microbial heterotrophic community (Peduzzi and Herndl, 1991), in explaining the differences between the two sites, as the
TEP concentration reached, using a concentration of leaf litter similar to
that observed in Es Caragol, is comparable to the maximum values observed in
situ.
TEP accumulation (mean ± SE) in the presence (blue line) and
absence (dark line) of P. oceanica litter. The solid lines show the
fitted second-order polynomial equations (R2=0.77 and 0.53,
respectively).
P. oceanica, as well as seagrasses in general, exports a large
fraction of its net primary production as leaf litter, on average about
24 % of net primary production (Duarte and Cebrián, 1996). A fraction of this leaf
litter is exported to the shoreline following leaf shedding by P. oceanica in the late summer and early autumn (Mateo et al., 2003). Leaf
litter is then deposited on the beach and re-entrained in the water during
storms, resulting in the pulses of TEPs observed at Es Caragol.
The seasonal variability in TEP / Chl a ratios at Faro Cap Ses Salines, where
leaf litter accumulation is precluded by strong currents, shows a maximum in
the summer (June and July), likely resulting from TEP precursors released by
the nearby seagrass meadow. Ortega-Retuerta et al. (2010) already reported
elevated TEP / Chl a ratios during early summer in the Mediterranean Sea, with
values comparable to those we observe at the Faro Cap Ses Salines.
These observations suggest that P. oceanica meadows, the dominant ecosystem in
Mediterranean coastal waters, are an important source of TEP precursors in
the Mediterranean Sea (Ortega-Retuerta et al., 2010). Considering the
average leaf production of P. oceanica of 876 g DW m-2 y-1 (Duarte and
Chiscano, 1999), the estimated 37 000 km2 covered by P. oceanica in the
Mediterranean Sea (range 31 040 to 43 550 km2, Marbà et al., 2014)
and the average TEP yield from leaf litter experimentally derived here (2344 µg C g DW-1), we calculated that P. oceanica releases about 76 Gg C as
TEPs annually to the Mediterranean Sea. However, this estimate should be
considered a first-order estimate, as it involves considerable uncertainty,
compounding that derived from the substantial variability in primary
production of P. oceanica (Duarte and Chiscano, 1999), that in the area covered by P. oceanica
meadows in the Mediterranean Sea, and variability in TEP yield across
meadows and over time, as the estimate used was derived from a single meadow
in the autumn. Improving this estimate will require narrowing down these
sources of uncertainty as well as the capacity to compare it with estimates
of other sources of TEPs, such as phytoplankton, which are not yet available
at the basin scale. The contribution of P. oceanica meadows to TEP release may
contribute to explain, along with other processes, the elevated TEP / Chl a
ratios characteristic of the Mediterranean Sea (Ortega-Retuerta et al.,
2010). The role of P. oceanica as a relevant source of TEP precursors is enhanced by
the contrast between the high production of P. oceanica meadows (Duarte and Chiscano,
1999), resulting in a high production of detritus (e.g. Mateo and Romero,
1997; Cebrián and Duarte, 2001) releasing TEP precursors, and the
oligotrophic nature of the Mediterranean Sea, leading to low production in
the pelagic compartment. In fact, both P. oceanica (e.g. Alcoverro et al., 1997) and
phytoplankton (e.g. Krom et al. 1991) are likely to be strongly
nutrient-limited in the Mediterranean Sea, which has been shown to enhance
the release of TEP precursors through carbon overflow during nutrient
limiting conditions (Mari et al., 2001; Radić et al., 2005). Despite the
limitations acknowledged above, estimates highlight the important role of P. oceanica
litter as source of TEPs in the Mediterranean and suggest that seagrass
meadows may play a similarly important role in other regions supporting
extensive seagrass meadows, such as the Caribbean, Australia, and South East
Asia.
Seagrass meadows have been recently shown to be globally relevant sources of
DOC to the marine ecosystem (Barrón et al., 2014), and Mari et al. (2017)
have recently assessed that the global TEP production could represent 2.5 to
5 Pg C yr-1. Here we provide the first evidence that seagrass meadows
can also play a relevant, even locally dominant, role as sources of TEPs and,
therefore, for the particle dynamics in the ocean. This finding has
important biogeochemical implications and provides a new pathway to be
accounted for when considering the fate and fluxes of organic matter in the
continuum of DOM–POM bridge.
All relevant data are presented within the
paper.
The authors declare that they have no conflict of
interest.
Acknowledgements
This work is a contribution to the StressX project, funded by the Spanish
Ministry of Economy and Innovation (CTM2012-32603). Francesca Iuculano was supported by
JAE predoctoral fellowship from the Consejo Superior de Investigaciones
Científicas (CSIC). We thank Juan de la Cruz Martinez Ayala for help with sampling and
Chl a measurements.
Edited by: Gerhard Herndl
Reviewed by: two anonymous referees
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