Chlorophyll-a and derivatives in recent sediments as indicators of productivity and depositional conditions

Marine Chemistry 125 (2011) 39–48

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Marine Chemistry j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / m a r c h e m

Chlorophyll-a and derivatives in recent sediments as indicators of productivity and depositional conditions Małgorzata Szymczak-Żyła a, Grażyna Kowalewska a, J. William Louda b,⁎ a b

Marine Pollution Laboratory, Institute of Oceanology, Polish Academy of Sciences, ul. Powstańców Warszawy 55, 81-712 Sopot, Poland Organic Geochemistry Group, Department of Chemistry, Florida Atlantic University, Boca Raton, FL 33 431, United States

a r t i c l e

i n f o

Article history: Received 26 November 2010 Accepted 8 February 2011 Available online 15 February 2011 Keywords: Chloropigments-a Indicators Productivity Sediments Depositional environments Eutrophication

a b s t r a c t Chlorophyll-a and its derivatives in the recent sediments of nineteen sites from the southern coast of the Baltic, an eutrophic sea, were examined and compared to those of other regions of the world. This included the Venice Lagoon in Italy, Ardmucknish and Dunstaffnage Bays of Scotland and the southern coast of Florida (USA). High photoautotrophic production and high sedimentation rates were found to aid the development of hypoxic/anoxic conditions in sediments. Additionally, when physical mixing in water and/or sediments was slow or absent, anoxia resulted and enhanced the preservation of chloropigments-a. Alternately, low productivity, low sedimentation rates, and the turnover of water and/or mixing of sediments resulted in the maintenance of oxic conditions, and increased degradation of chloropigments-a and decomposition to colorless products. In this work, specific chlorophyll-a derivatives are becoming better identified as indicators for certain combinations of environmental processes, such as grazing by zooplankton and benthic biota, input of fresh microalgal material, oxygenation, anaerobic microbial activity and others. The distribution both of the sum of chloropigments-a (Σ Chlns-a, in nmoles/g-sediment, dry wt.) and the percentages specific derivatives in recent sediments are concluded as excellent, spatiotemporal averaged indicators of productivity and the physicochemical state/trends of various depositional environments. Conclusions drawn on the basis of past studies of Baltic Sea sediments, as well as those reported herein, appear extendable to other coastal areas. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Eutrophication (‘true feeding’) is a common problem in many coastal areas throughout the world. This characteristic applies not only for recent times but is also known to have occurred for millenia (Orive et al., 2002). Eutrophication results in high primary production and correspondingly high sedimentation rates. This sometimes natural phenomenon can also be enhanced by various anthropogenic activities (cultural eutrophication) connected with nutrient enrichment of the marine environment and often leads to negative environmental effects. The results of such enrichment are most visible in enclosed coastal marine basins, such as small lagoons and semi-enclosed seas like the Baltic. This cumulative nutrient enrichment, whether natural or man induced, is exacerbated by restricted water exchange (HELCOM, 2009). High primary production, followed by high sedimentation rates and a lack of mixing causing hypoxia/ anoxia in sediments and near-bottom water can be expressed by the formation of, often seasonal, laminar sediment layers (varves).

⁎ Corresponding author. Tel.: +1 561 297 3309; fax: +1 561 297 2759. E-mail addresses: [email protected] (M. Szymczak-Żyła), [email protected] (G. Kowalewska), [email protected] (J.W. Louda). 0304-4203/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.marchem.2011.02.002

Anoxia, obviously suppressing aerobic biota, is an important factor that lowers the intensity or even the existence of bioturbation in sediments. Physical factors such as light (photooxidation) and temperature (reaction rates) also play the important roles in the re-mineralization of organic matter undergoing sedimentation/burial. There are a variety of methods to estimate the extent and trends of nutrient-coupled productivity. In the Baltic, the most popular method (HELCOM, 2006) is based on chlorophyll-a monitoring of the water column. However, such method requires extensive monitoring data to estimate the averaged situation for any given area and time period. Chloropigments-a in sediments are well documented as indicating periods of high productivity/blooms and sediment anoxia/preservation in the past, both for fresh water (e.g. Leavitt, 1993; Hall et al.; 1997; Leavitt and Hodgson, 2001; Swain, 1985) and marine settings (e.g. Baker and Louda, 1986, 2002; Sun et al., 1999; Louda et al., 2000; Villanueva and Hastings, 2000). The contents of individual chloropigments-a in recent sediments, as with bulk organic matter, depend on primary production, grazing, sedimentation, accumulation rate, oxygen fugacity and hydrodynamics of water (Baker and Louda, 2002; Kowalewska, 2001; Reuss et al., 2005; Szymczak-Żyła and Kowalewska, 2009). Methods based on sedimentary chloropigment determination (cf. Baker and Louda, 1986, 2002; Harris et al., 1996; Kowalewska, 1997; Louda et al., 2000) give an averaged picture for an area.

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M. Szymczak-Żyła et al. / Marine Chemistry 125 (2011) 39–48

In the present work, we sought to verify and extend conclusions drawn from previous Gulf of Gdańsk (Baltic Sea) to multi-annual studies of the Gulf and other Baltic sites. These past and present results were then compared to results obtained in the present study on samples from various other coastal zones in the world. That is, we ask the question; “are chloropigments-a good qualitative and quantitative indicators of the integration of productivity and depositional environmental conditions?” Areas studied included the European coastal zone: the Lagoon of Venice and the north-western coast of Scotland as well as sites in the USA coastal zone of the Atlantic Ocean: Florida Bay, Mrazek Pond (a saline lake in the southern Florida Everglades) and Little Lake Worth Florida. The sites were selected in such way to cover a large range of the environmental parameters (e.g. salinity, temperature, oxygen, depth, nutrient loading, etc.). 2. Materials and methods 2.1. Characteristics of the studied area 2.1.1. The southern Baltic Sea The sampling stations of the southern Baltic Sea were selected in such a way as to represent as many different environmental conditions as possible, including different water depths, sediment types and distances from the shore. Locations of the sampling stations are given in Fig. 1A and their characteristics in Table 1. Samples were collected from the Gdańsk Basin, Wisła Lagoon, open sea, Bornholm Deep, Pomeranian Bay and Szczecin Lagoon. Sites in the southern Baltic include the estuaries of the two largest Polish rivers — the Wisła and Odra. These two regions are very good model basins for studies on chlorophyll-a and its derivatives as indicators of nutrient loading and high productivity. There were previous studies on these areas (Kowalewska, 1997, 2005; Kowalewska et al., 2004; Szymczak-Żyła and Kowalewska, 2007) and certain data herein are drawn from those works. The Gulf of Gdańsk (area: 4940 km2, water volume: 291 km3: Majewski, 1994) is located in the south-eastern part of the Baltic and is a part of the Gdańsk Basin. The average depth is 59 m. The deepest part of the Gdańsk Basin is the Gdańsk Deep with depths reaching 110 m. Waters of the Gulf of Gdansk are characterized by complex oxygen, salinity and temperature structures due to large inflows of fresh water from the River Wisła (Vistula). Salinity in the surface waters of the Gulf of Gdańsk remains constrained within a range of 7 to 8 with an exception of area close to river mouth where salinity is low and variable (ca. 4.5).The waters in the deeper parts of the Gulf are stratified: the salinity of the surface waters is lower than that of the deeper waters (av. 12.5). The halocline formed in the deeper parts of the Gulf at depth 60–80 m (in the Gdańsk Deep up to 90 m) prevents the vertical mixing of water masses and leads to development of hypoxic/anoxic conditions in the bottom waters. Input of nutrients and organic matter with the Wisła waters causes high primary production (Witek et al., 1999). This area is characterized by intensive blooms of microalgae (diatoms and dinoflagelates), cyanobacteria and proliferation of macroalgae (green and brown algae). The Gdańsk Deep is the sink or depo-center for particulate matter both originating in the Gulf as a result of primary production (autochthonous) and transported (allochthonous) in by the Wisła River. The Gulf, as with the entire Baltic, has negligibly small tides (~ 1 cm) and the sea level changes mainly under the influence of wind. The Wisła (Vistula) Lagoon is the largest coastal reservoir (area: 838 km2, water volume: 2.3 km3) of the southern Baltic Sea, separated from the Gulf of Gdańsk by the Wisła Split. The Lagoon is a part of the Wisła Estuary with waters derived from the deltaic arms of the Wisła River. It is a shallow (av. depth: ~ 2.5 m) low salinity (from 1 to 5 at the Baltijsk Strait — the entrance to Baltic waters) ecosystem. The Lagoon has developed intense eutrophication with very high level of primary production in the water body (4–5 times higher than in the open

Baltic Sea) and a high accumulation of nutrients and organic matter in the sediments leading periodically to oxygen deficiency in near bottom waters despite of shallowness of the basin (Andrulewicz, 1997; HELCOM, 2003; IMGW, 2009). The Odra Estuary is located at the western end of the Polish seashore and includes the lower part of the Odra River, the Szczecin Lagoon which is connected to the open sea by three straits, and the Pomeranian Bay (Fig. 1A). The Szczecin Lagoon (area: 687 km2, water volume: 2.6 km3) is also a shallow (av. depth: ~4 m) low salinity (1–2) basin. Hydrologically, the Lagoon is most influenced by the very large inflow of freshwater from the River Odra and is a trap for particulate matter transported by this river. The Szczecin Lagoon is a heavily eutrophied water body, with high levels of primary production and oxygen depletion occurring despite the shallowness of the Lagoon (Andrulewicz, 1997, HELCOM, 2003; Łysiak-Pastuszak et al., 2009). The Pomeranian Bay (area: ~ 6000 km2, water volume: 73 km3) is located at the inflow of Odra to the Baltic and experiences strong local currents. Mean depth in this region is 13 m and the bottom of the bay is mostly covered with fine sand. The Bornholm Deep (P5) is the second deepest area in the southern Baltic (~95 m). Environmental conditions are similar to the Gdańsk Deep. This site is a sink for allochthonous organic matter transferred to the northern-east from the mouth of the Odra River. 2.1.2. Other marine coastal areas 2.1.2.1. The Venice Lagoon (Mediterranean). The Lagoon of Venice (Italy) is a large (area: 549 km2; 8–13 km wide) and shallow (av. depth: ~ 1 m) coastal basin of north-eastern Adriatic Sea (Fig. 1B). There is a tidal fluctuation of about 60 cm (Sfrizo et al., 1992). Strong tidal seawater inflows to the Lagoon are through three canals. Freshwater input is much lower than the seawater inflow during tides. Anthropogenic pressure in the Lagoon is very high but the environmental conditions there are different than those in the southern Baltic. Annual average salinity (~30) and temperatures (~16 °C) are much higher in this area, as is total solar irradiation, relative to the southern Baltic (Facca et al., 2002). The sediment sample was collected halfway between the Lido Port and Malamocco Port entrances (45°23.34′N × 12°20.52′E) near Lido (Fig. 1B) where sediments contain 80% of fine material and anoxia frequently occurs during the warm season (Sfrizo et al., 1992). 2.1.2.2. The north-western coast of Scotland (Atlantic Ocean coast). Samples were collected from Ardmucknish and Dunstaffnage Bays (Fig. 1C). Ardmucknish Bay is about 3 km wide and is situated at the mouth of Loch Etive. The salinity is much higher there (32–33) than the maximal salinity values in the southern Baltic. There is a tidal influence and the average annual solar irradiation is lower than the southern Baltic sites. The average annual temperatures are slightly lower or comparable to the southern Baltic. These bays are located in an unpolluted environment. 2.1.2.3. The southern coasts of Florida (Atlantic Ocean coast). Samples around the southern tip of Florida (USA) were collected in the Whipray Basin of Florida Bay, Mrazek Pond in the southern Florida Everglades and in Little Lake Worth, a marine lagoon near West Palm Beach, Florida (Fig. 1D). All three of these sites represent pigment accumulations derived from both phytoplankton and microphytobenthos as the sediment water interface is within the euphotic zone. Florida Bay is a large sub-tropical lagoon at the southern tip of mainland of Florida (area: ~ 2200 km2) with a mean depth about 1 m. Within the bay are a series of basins separated from each other by carbonate banks (~ 0–0.2 m) which leads to more or less restricted flows (Lee et al., 2002). The Whipray Basin site (20°03′23″N × 80°45′ 12″W) contains carbonate marl sediments and was ca. 0.5 m

M. Szymczak-Żyła et al. / Marine Chemistry 125 (2011) 39–48

Fig. 1. Location of the sampled areas: A) southern Baltic Sea; B) Venice Lagoon; C) north-western coast of Scotland; and D) southern coasts of Florida. 41

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Table 1 Characteristics of the sampling stations of the southern Baltic Sea. Station

Gdańsk Basin

Wisła Lagoon

Szczecin Lagoon

Pomeranian Bay open sea

Date of collection

G2 P116 P110 ZN2 P110d PGd NP Zw19 Zw21 Zw23 L 15 18 38 35 32 37 P5 P3

1995–2007 (n = 10) 1995–2007 (n = 7) 2003–2007 (n = 4) 1995–2006 (n = 6) 1996–2006 (n = 4) 1996–2007 (n = 5) 2003–2007 (n = 3) 2008 (n = 1) 2008 (n = 1) 2008 (n = 1) 1996–2000 (n = 5) 1999–2000 (n = 2) 1999–2000 (n = 2) 1997–2000 (n = 7) 2001 (n = 1) 1997–2001 (n = 2) 2001 (n = 1) 1996–2000 (n = 4) 1995–2001 (n = 3)

Water depth [m]

~ 110 ~ 90 ~ 70 ~ 20 ~ 32 ~ 30 ~ 13 ~3 ~ 2.5 ~ 2.5 ~ 10 ~5 ~6 ~ 10 ~ 10 ~ 40 ~9 ~ 95 ~ 90

Near-bottom water parameter salinity

temperature [°C]

oxygen [mg/l]

12.3–14.0 11.7–12.4 10.3–10.5 7.0–7.4 7.3–7.5 7.3–7.6 7.0–7.6 0.5 0.9 1.8 1.8–1.9 1.0–1.6 1.3–3.7 7.1–7.8 6.9 6.8–7.2 7.1 11.5 10.2

4.1–8.3 4.5–7.8 4.6–6.1 4.0–13.7 3.2–10.0 4.4–9.4 7.7–15.3 21.4 22.0 21.2 12.7–14.4 11.1–14.0 14.5–14.6 12.5–13.5 13.2 11.8–13.6 12.2 8.1 8.6

~ 0–6.7 0.8–5.7 2.7–7.7 8.2–11.5 7.7–11.3 7.5–11.3 5.4–10.9 – – – 3.4–6.6 4.4–4.6 4.9–9.9 8.0–10.3 – 9.4 – 1.2–4.8 2.2–5.0

Sediment type

Corg⁎ [%]

Clay Silty clay Clayey silt Fine-grained sand Medium-grained sand Fine-grained sand Medium-grained sand Sandy silt Silty sand Sandy silt Clayey silt Sandy silt Silty sand Sandy silt Course-grained sand Fine-grained sand Vari-grained sand Silty clay Sand-silt-clay

5.8–7.8 6.6–8.2 5.4–6.1 0.2–0.3 0.1–0.3 0.9–3.4 0.1–0.2 3.3 4.3 3.9 6.1–7.7 3.1–4.2 5.5–5.6 0.2–1.8 0.1 0.1–0.2 0.2 4.8–5.4 0.2–1.0

⁎ In 0–1 cm sediment layer.

(±0.2 m) deep at mid-tide. This site experiences salinities on an annual basis of 15–45 due to wet/dry season differences in fresh water flow from the southern Everglades and temperatures of 15–35 °C. Sampling of Florida Bay and certain results from those samples have been reported previously (Site WR2 in Louda et al., 2000). Mrazek Pond is a small (ca. 0.5 km2) saline lake surrounded by a red mangrove (Rhizophora mangle) forest. Sampling site (25°11′12″ N × 80°53′38″W) was in ~0.1–0.2 m of water. Mrazek Pond is in the southern transition region between the fresh water Everglades and the estuarine/marine nature of northern Florida Bay. Temperatures range a bit higher and lower than the Whipray Basin site due to the lower volume and depth of the water. Salinities are rather low (5–15) due to fresh water seepage flow from the southern Everglades and direct rain inputs. The sediment consisted of a dark brown sapropel with both decaying red mangrove leaves and microalgae. Previous pigment-based chemotaxonomic work at this site, revealed a mixed microalgal community dominated by diatoms, cryptophytes and cyanobacteria, in that order (Louda unpubl. 2002). Lake Worth is a marine lagoon running from Atlantic Ocean along the south-eastern Florida coasts near West Palm Beach and separated from the Atlantic Ocean by a substantial barrier island. Water exchange with the ocean occurs on a semidiurnal basis about 5 km south through the Lake Worth Inlet. Fresh water input occurs in the Summer/Fall wet season via drainage from the surrounding lands and direct rain input. Salinities typically range from near open ocean (~ 36) to mildly estuarine (~ 20–25) conditions. The depth of Lake Worth is 0.1 to 2 m with a channel (Intracoastal Waterway) of about 3–4 m depth. The bottom is mainly well compacted and oxygenated at the surface sandy sediment. There are also several small separated basins, such as Little Lake Worth (sampled site LLW — 26°49′46″ N × 80°02′59″W: z = ~9 m: Fig. 1C), with limited exchange of water where anthropogenic eutrophication has led to oxygen deficiency. Green-S bacteria (Phaeobacteroides sp.) occur in bottom water and sediments. LLW has black highly sulfidic organic bottom sediments (Prize-Bolter, 2010). 2.2. Sampling of sediments Samples of recent sediments of southern Baltic Sea were collected at 19 sites in different seasons between the years 1995 and 2008. Collection of recent sediments (up to 10 cm deep) employed one of the following methods; a core sampler of Niemistö type, a box-corer (for sandy sediments) or a van Veen grab sampler (for sediments of

Wisła Lagoon). In all, sixty-nine cores of recent sediments from the southern Baltic Sea were collected, at some stations up to ten times (Table 1). The sediment cores, except from Wisła Lagoon where only 0–5 cm long samples were collected, were divided into layers: 0–1 cm, 1–5 cm, 5–10 cm,. Samples were transferred to polyethylene bags and kept at −20 °C until further analysis. Chloropigments-a were determined in all 174 sediment samples of southern Baltic Sea. Samples of recent sediment of other coastal areas were collected: (i) from Venice Lagoon in October 2007 (core sampler); (ii) from coast of Scotland in August 2007 (Ardmucknish Bay - core sampler, Dunstaffnage Bay — manual corer from intertidal zone during low-tide period); (iii) from coasts of Florida in June 2004 (stations LLW and MP- Wildco hand core sampler) and in Florida Bay (station WR2: 10 cm × 1 m acrylic piston corer: Louda et al., 2000). Except for samples from station LLW (Florida) where only surface sediment (0–1 cm) was collected, sediment cores were divided into layers as follows; (i) Venice Lagoon: 0–1 cm, 1–5 cm, 5–20 cm; (ii) coast of Scotland: Ardmucknish Bay: 0–1 cm, 1–5 cm, 5–10 cm; Dunstaffnage Bay: 0–1 cm, 1–5 cm (iii) coasts of Florida: station MP: 0–1 cm, 1–3 cm, 3–5 cm, 5–7 cm; station WR2: into 2 cm long layers. Samples were transferred to polyethylene bags and kept at −20 to −30 °C until being analyzed. 2.3. Analysis 2.3.1. Pigment analysis Pigment analyses involved organic solvent extraction of the sediment followed by separation and identification using highperformance liquid chromatography (HPLC) coupled to full spectrum diode array detectors (DAD, aka PDA for PhotoDiodeArray). Pigment analyses, except for the Whipray Basin sites (see below), were carried out according to procedures described in Kowalewska (1997, 2005) and Szymczak-Żyła et al. (2008a). Frozen sediment samples were placed into the glass centrifuge tube, left to thaw, centrifuged to remove water, flushed with acetone, sonicated and re-centrifuged. Extractions were repeated until color disappeared from the supernatant (~ 2–3 times). The combined acetone fractions were subjected to liquid:liquid separation in the system:acetone extract:benzene:water. The benzene layer was transferred to a glass vial and evaporated to dryness in a stream of argon. Separations were carried out using a chromatograph system (Knauer, Germany) equipped with a diode-array detector (DAD). The mobile phase was an acetone: water gradient system, at an elution rate of 1 mL min−1.

M. Szymczak-Żyła et al. / Marine Chemistry 125 (2011) 39–48

The solvents used were filtered and degassed with helium. During analysis the detector registered spectrum in the range 360–700 nm. The particular pigments were identified using their retention times and the spectrum characteristic for each compound. The pigment content was determined on the basis of both the HPLC chromatogram and absorption spectrophotometric measurements using equations described previously (Kowalewska 1997, 2005; Szymczak-Żyła et al. 2008a). Extraction and subsequent HPLC analysis of pigments from the Whipray Basin sample (WR2) were performed as detailed in Louda et al. (2000). A sediment sample was thawed, mixed, centrifuged, decanted to remove excess water, mixed with tetrahydrofuran (THF), sonicated and placed in a refrigerator for 1 h. THF is an unusual solvent for sediment extractions but it was shown to be the best for these carbonate marls through a thorough series of solvent comparison tests. Tests with fresh phytoplankton revealed no pigment alterations due to THF extraction. The sample was centrifuged, decanted, the supernatant was passed through a 0.45 mm filter, and the solvent was removed in a stream of dry nitrogen. Separations were carried out using a chromatograph system equipped with a Waters photodiode array (PDA) detector (Waters990, Millepore, Massachusetts, USA). Gradient elution involved solvents: A — 0.5 M solution of ammonium acetate in methanol/water (85/15 v/v), B — acetonitrile/water (90/10 v/v), and C — ethyl acetate. Electronic absorption spectra were recorded through the range of 330–800 nm. The pigments were identified based on retention time and spectral properties of particular compound. Quantitative analysis relied on molar extinction and E-1%/1 cm coefficients taken from the literature for each pigment (cf. Louda et al., 1998, 2000). Comparison of the two analytical methods employed herein was previously shown to give similar data (cf. Szymczak-Żyła et al., 2008a). The following chloropigments-a were analyzed for in all samples: chlorophyll-a, chlorophyll-a-allomers, chlorophyll-a-epimer, pheophytin-a, pheophytin-a-epimer, pheophorbides-a (aka pheophorbides I), pyropheophorbide-a (aka pheophorbides II), pyropheophytina, and steryl chlorin esters. In the literature (cf. Baker and Louda, 1986, 2002), all these derivatives are covered by the term ‘early diagenesis products’ to distinguish them from mid- to late diagenesis products. 2.3.2. Additional analyses 2.3.2.1. Determination of organic carbon in sediments. Organic carbon concentration in sediments was determined using the wet chromic acid titration method (Gaudette et al., 1974). 2.3.2.2. Granulometric analysis of sediments. The granulometric characteristics of sediments were determined using the wet sieve analysis according to Folk and Ward (1957). 2.4. Environmental parameters During sediment sampling of the southern Baltic, the following parameters were measured: depth, temperature, salinity and oxygen concentration in seawater. The measurements were carried out using: — a CTD sonde (SBE 911+, Sea-Bird Electronics, INC., USA), — multiparametric sonde for water quality control (YSI 6000 UPG, USA) and a portable multiparametric instrument (Multi 197i, WTW, Germany). 2.5. Statistical analysis The results were statistically processed using STATISTICA 6.0 software. The following statistical methods have been used: correlation analysis, analysis of variation (ANOVA) and cluster analysis. In cases when data were not normally distributed (tested using the Shapiro–Wilk test), non-parametric methods were used. Correlation

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analysis was used to evaluate the relationships between the chloropigment-a content in the sediment and the environmental parameters. The calculated correlation coefficient is a measure of the strength of the linear relationship between variables. A correlation with p b 0.05 was regarded as significant. The differences between the mean chloropigment-a content in samples from different regions were determined from the results of the variance analysis. Cluster analysis was used to create a classification of the sampling stations taking into account chloropigments-a and organic carbon content in sediments, and percentage of particular pigments in sum of chloropigments-a. 3. Results and discussion The long-term average concentrations of sum of chloropigments-a (Σ Chlns-a) in sediments from the southern Baltic Sea are presented in Fig. 2. The highest values of pigments were found in sediments collected at the station P116, where the average concentration of Σ Chlns-a in surface (0–1 cm) layer of sediments was ~ 450 nmol g−1 d.w. (range: ~330 nmol g−1 d.w in March 1995 to ~900 nmol g−1 d.w in May 2003). Sediments at stations G2 and P110 also contained high concentrations of chloropigments-a. All these stations are within the Gdańsk Deep. As described earlier, the Gdańsk Deep is a sink (depo-center) for particulate matter which originates both in the Gulf as a result of primary production and that is transported by Wisła River (Jankowski and Staśkiewicz, 1994). Sediments at these stations contained the highest percentage of the fine-grained fraction and organic carbon (Table 1). The average organic carbon content in the surface sediments collected at the station P116 was ~7.5% and the average percentage of finest (b0.063 mm) sediment fraction was ~99%. Even though environmental conditions in the Bornholm Deep were somewhat similar to the Gdańsk Deep, concentrations of chloropigments-a in Bornholm Deep sediments were much lower (av. ~ 95 nmol g−1 d.w.). The Bornholm Deep receives allochthonous organic matter from the Odra River, has less anthropogenic nutrients and experiences highly variable oxic/anoxic fluctuations. That is, inflows (Feistel et al., 2006) to the Baltic across Danish Straits can be intense and reach the central Baltic Basins. This leads to flushing and sporadic alternating episodes of elevated bottom water oxygenation or anoxia with hydrogen sulfide generation (Nehring, 1987). Thus, the preservation conditions in the Gdansk Deep, which is less prone to thermohaline flushing, appears linked directly to more permanent bottom water oxygen depletion (Bralewska and Witek, 1995; IMGW, 2009) relative to the episodic fluctuating conditions in the Bornholm Deep (Nehring, 1987). Large amounts of chloropigments-a and organic carbon were also recorded in sediments from the Szczecin Lagoon which is a trap for organic matter carried by Odra River (Lampe, 1999; Osadczuk et al., 1996). The input of nutrients and organic matter with the Odra waters causes a high level of primary production (Andrén, 1999; WIOŚ, 2001). At station L, the mean concentration of Σ Chlns-a in surface sediments was ~325 nmol g−1 d.w. (ranging from ~150 nmol g−1 d.w in October 1996 to ~530 nmol g−1 d.w in August 1996) and the mean organic carbon content was ~7.0%. In the Wisła Lagoon, primary productivity is about 4–5 times higher than the open Baltic Sea (HELCOM, 2003; IMGW, 2009). However, concentrations of sedimentary pigments were lower than in the Gdańsk Deep and similar to values (av. ~90 nmol g−1 d.w.) determined for the Bornholm Deep sediments. This reservoir is very shallow and generally well oxygenated but, during periods of elevated primary production, organic matter flux can lead to oxygen depletion in the near bottom water (aka benthic boundary layer, BBL) and surficial sediments. Relative to muddy areas, the sandy sediments from the southern Baltic Sea contained much lower amounts of organic carbon (from 0.1% at stations P110d, NP, 35, and 32 to 3.5% at station PGd, Table 1)

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M. Szymczak-Żyła et al. / Marine Chemistry 125 (2011) 39–48

Fig. 2. Average contents of the sum of chloropigments-a in the surface layer (0–1 cm) of sediments collected in the southern Baltic Sea (1995–2008) [nmol g−1 d.w.].

and chloropigments-a (Fig. 2). The water in these parts of the southern Baltic is shallow and consequently well oxygenated. High light and water column mixing, together with local offshore currents, do not favor accumulation of pigments in sediments. Additionally, the larger grained (sand size) sediments of the southern Baltic Sea allow for better water column-sediment diffusive gas exchange (aeration). Taking into account chloropigment-a and organic carbon content in sediments, cluster analysis of the sampling stations in the southern Baltic Sea showed that sediments located in the Deeps (Gdańsk and Bornholm) and Lagoons (Szczecin and Wisła) differ from other stations of the southern Baltic Sea (Fig. 3) and the analysis of variance (Kruskal–Wallis ANOVA) indicated that these differences are statistically significant (p b 0.01). Analysis of correlation (Spearman R, Table 2) revealed a statistically significant positive correlation between Σ Chlns-a and both organic carbon content (r = 0.95, p b 0.05) and finest fraction (r = 0.92, p b 0.05), as well as a negative correlation with oxygen content in near bottom waters (r = −0.65, p b 0.05). Also, individual chloropigments-a, with the exception of pheophorbides-a, displayed such relationships. This observation is in agreement with previous

Fig. 3. Result of cluster analysis including total chloropigment and organic carbon contents: Hierarchical dendrogram of the southern Baltic Sea sampling stations (Ward's method, Euclidean distance).

results obtained by Szymczak-Żyła and Kowalewska (2007) who studied chloropigment-a contents in sediments of Gulf of Gdańsk and with other authors who also reported the strong influence of oxygen and/or sediment grain-size and water depth on pigment concentration in sediments (Bianchi et al., 2000; Rabalais et al., 2004; Reuss et al., 2005; Shankle et al., 2001; Villanueva and Hastings, 2000). Based on the present study, and previous investigations of Gulf of Gdańsk, we conclude that the sediments richest in chloropigments-a are from the southern Baltic regions having local hydrodynamic conditions that promote rapid sedimentation and hypoxia/anoxia. These sediments also have the highest organic carbon contents and the highest percentage of the finest grain size fraction. This includes the Deep of Gdańsk and the Szczecin Lagoon, in that order (Fig. 4A). From the other areas, only sediments of the southern coast of Florida were similarly rich in chloropigments-a where at station MP concentration of Σ Chlns-a in surface sediment layer amounted to ~280 nmol g−1 d.w (Fig. 4A). Slightly lower content of chloropigment-a was determined at station LLW (Florida) (~150 nmol g−1 d.w). At station WR2 chloropigments concentration was distinctly lower (~20 nmol g−1 d.w). Sediment samples from the southern coast of Florida were characterized by high contents of organic carbon (~13% at MP, ~8% at LW and ~6% at WR2), even higher than the Gdańsk Deep samples (Fig. 5). Lower chloropigment per organic carbon content at these sites likely derives from the extremely short water columns with concurrent high rates of photooxidation and aeration with wind driven mixing events. This appears to be so even though most of the chloropigments would derive from the microphytobenthos at the sediment-water interface. Sediments of the Lagoon of Venice (~30 nmol g−1 d.w at station VL) and from Scotland (~40 nmol g−1 d.w at station AB2) exhibited the lowest concentrations of chloropigments-a. Organic carbon contents in sediments from these areas were also low (b 2%). Sediments differed not only with the total contents of chloropigments-a but also in percentage of particular derivatives (Fig. 4B). The processes of chlorophyll-a decomposition in the sea can depend on several factors. This includes, first of all the environmental conditions (e.g. light, oxygen, pH, etc.), including hydrodynamic conditions and also the characteristics of the organisms from which the parent molecule originates (species specificity), grazing and the stability of the particular derivatives. One can conclude from the studies of the Gulf of Gdańsk sediments, determined before and after the vegetative growing season in 2003–2004 (Szymczak-Żyła and Kowalewska,

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Table 2 Correlation coefficient (Spearman R) of chloropigment-a concentration in the surface layer of sediments and the percentage of particular chloropigments-a in the sum of chloropigments-a with environmental parameters: seawater depth, salinity (S), oxygen concentration (O2) in and temperature (t) of near-bottom water, content of organic carbon (Corg) and sediment fraction (samples collected from the southern Baltic Sea, 1995–2008). Parameter

Chl-a-allom⁎⁎) Chl-a Chl-a′ Phytin-a Phytin-a′ Phide-a Pyrophide-a Pyrophytin-a SCEs Σ Chlns-a %Chl-a-allom %Chl-a %Chl-a′ %Phytin-a %Phytin-a′ %Phide-a %Pyrophide-a %Pyrophytin-a %SCEs

Seawater depth [m]

S

O2 [mg l− 1]

t [°C]

Corg [%]

Sediment fraction [%] 2 mm

1 mm

0.5 mm

0.25 mm

0.125 mm

0.063 mm

− 0.36⁎ − 0.21 − 0.11 − 0.29 − 0.15 − 0.34 − 0.33 − 0.19 − 0.15 − 0.29 − 0.27 0.02 0.35 − 0.21 − 0.11 − 0.39⁎ −0.16 0.37⁎

0.80⁎ 0.93⁎ 0.93⁎ 0.95⁎ 0.86⁎ 0.40⁎ 0.90⁎ 0.96⁎ 0.91⁎ 0.95⁎ − 0.60⁎

− 0.60⁎ − 0.56⁎ − 0.65⁎ − 0.63⁎ − 0.51⁎

− 0.65⁎ − 0.61⁎ − 0.72⁎ − 0.70⁎ − 0.57⁎

− 0.59⁎ − 0.49⁎ − 0.61⁎ − 0.69⁎ − 0.47⁎

− 0.60⁎ − 0.57⁎ − 0.65⁎ − 0.77⁎ − 0.51⁎

− 0.57⁎ − 0.52⁎ − 0.55⁎ − 0.68⁎ − 0.47⁎

− 0.22 − 0.53⁎ − 0.63⁎ − 0.57⁎ − 0.63⁎

− 0.20 − 0.64⁎ − 0.72⁎ − 0.69⁎ − 0.70⁎ 0.52⁎

− 0.15 − 0.59⁎ − 0.70⁎ − 0.68⁎ − 0.68⁎ 0.53⁎

− 0.24 − 0.58⁎ − 0.75⁎ − 0.74⁎ − 0.75⁎ 0.50⁎

− 0.04 − 0.62⁎ − 0.65⁎ − 0.59⁎ − 0.68⁎

− 0.22 − 0.30 − 0.09 − 0.10 0.39 0.50⁎ − 0.36 − 0.55⁎

0.01 − 0.21 − 0.14 0.07 0.36 0.44 − 0.39 − 0.56⁎

− 0.06 − 0.18 − 0.26 0.04 0.25 0.48⁎ − 0.40 − 0.54⁎

− 0.35 − 0.35 − 0.29 − 0.45 − 0.18 − 0.32 − 0.34 − 0.39 − 0.38 − 0.45 0.11 0.09 0.18 − 0.33 0.11 − 0.41 0.01 0.34 0.15

0.33 0.36⁎ 0.45⁎ 0.52⁎ 0.44⁎

0.49⁎ 0.43⁎ 0.52⁎ 0.57⁎ 0.45⁎

− 0.62⁎ − 0.55⁎ − 0.73⁎ − 0.65⁎ − 0.63⁎

0.25 0.49⁎ 0.51⁎ 0.54⁎ 0.49⁎

0.28 0.56⁎ 0.59⁎ 0.58⁎ 0.57⁎

− 0.06 − 0.61⁎ − 0.76⁎ − 0.73⁎ − 0.65⁎ 0.67⁎

− 0.27 − 0.20 0.13 0.36⁎ 0.21 0.02 − 0.02 0.28 0.27

− 0.18 0.00 0.16 0.13 − 0.07 − 0.11 − 0.03 0.25 0.29

− 0.09 − 0.58⁎ − 0.16 − 0.14 0.60⁎ 0.53⁎ − 0.69⁎ − 0.65⁎

0.14

0.08 0.43⁎ 0.20 0.22 − 0.25 − 0.53⁎ 0.55⁎ 0.50⁎

0.41 − 0.26 − 0.36 − 0.06 − 0.06 0.30 0.46 − 0.42 − 0.42

0.18 − 0.04 0.02 − 0.35 − 0.16 0.12 0.14 − 0.02 − 0.13

N 0.063 mm 0.81⁎ 0.83⁎ 0.79⁎ 0.92⁎ 0.63⁎ 0.36 0.82⁎ 0.88⁎ 0.79⁎ 0.92⁎ − 0.42 0.38 0.03 0.22 − 0.02 − 0.11 − 0.34 0.14 0.31

⁎ Statistically significant p b 0.05. ⁎⁎ Chl-a-allom — chlorophyll-a allomers; Chl-a — chlorophyll-a; Chl-a′ — chlorophyll-a epimer; Phytin-a — pheophytin-a; Phytin-a′ — pheophytin-a epimer; Phide-a — pheophorbides-a; Pyrophide-a — pyropheophorbides-a; Pyrophytin-a — pyropheophytin-a; SCEs — sum of steryl chlorine esters; and Σ Chlns-a — sum of chloropigments-a.

2007), that the particular chlorophyll-a derivatives which occur in recent sediments can be good indicators of environmental conditions and processes. Chlorophyll-a allomers are markers of fresh photoautotrophic organic matter originating from the coastal zone where the

oxygen conditions are good. Pheophytin-a occurs in seawater and is marker of senescent/slightly decomposed phototrophic matter in sediments. Chlorophyll-a epimer (Chl-a′) is apparently a thermodynamically more favored pigment formed during initial senescence/

Fig. 4. A) Average contents [nmol g−1 d.w.] of the sum of sedimentary chloropigments-a. B) Average percentages of specific pigments in the sum of chloropigments-a.

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Fig. 5. Relationship between the concentrations of the sum of sedimentary chloropigments-a and organic carbon contents.

diagenesis (Louda et al., 1998, 2002) and its percentage in sediments is higher than that in seawater as a result. Pheophorbides-a are relatively less stable derivatives and indicate the presence of comparatively fresh material. Pyropheophorbide-a is not only a marker of grazing of zooplankton and zoobenthos (references in Baker and Louda 2002; Bianchi et al., 1998, 2002; Head and Harris, 1996) but is also produced during the senescent of certain phytoplankton (Louda et al., 1998, 2002). Pyropheophytin-a and steryl chloropigments are found most often in sediments rather than in seawater (Szymczak-Żyła and Kowalewska, 2007; Szymczak-Żyła et al., 2008b). However, both were also found in sediment trap samples containing a high percentage of zooplankton fecal pellets (Baker and Louda, 2002; King and Wakeham, 1996; Talbot et al., 1999) and have been shown to rapidly form under the influence of sedimentary microbes and preserved under anoxia (Szymczak-Żyła et al., 2008b). Results of other regions of the southern Baltic Sea are in agreement with conclusions of the Gulf of Gdańsk studies. Fig. 4B presents the average percentage of particular pigments in the sum of chloropigments-a for sediment samples collected from different studied regions and additionally two extreme situations — composition of chloropigments-a in phytoplankton from the Gulf of Gdańsk and deep sediment samples from Gotland Deep (Kowalewska et al., 1999). Environmental factors, such as oxygen or light (Kowalewska and Szymczak, 2001; Louda et al., 1998, 2002; Cuny et al., 2002) cause deterioration of the tetrapyrrole macrocycle and decomposition of chloropigments-a to the colorless products, sometimes with formation of small quantities of chlorophyll-a allomers and the epimer, pheophytin-a and pheophorbides-a. As one can see, these derivatives were dominant in freshly derived microalgal material. The average content of sum of these chlorophyll-a derivatives in seawater collected from Gulf of Gdańsk was ~ 90% (Fig. 4B). In turn, in the deep layers of the Gotland Deep sediments content of sum of these derivatives was 40% at the 70 cm depth in sediment and 23% at 360 cm (Kowalewska et al., 1999). Chlorophyll-a allomers occur in highest percentage in the coastal sediments of southern Baltic Sea, samples from coast of Scotland and from station MP (coast of Florida), but lower than found in phytoplankton from the Gulf of Gdańsk (3–7%, Fig. 4B). Despite low concentrations, these derivatives are good indicators of sediments originating from the well oxygenated coastal zone. Such a conclusion is supported by a positive statistically significant correlation with the

oxygen concentration in the near-bottom water and a positive correlation with the sediment fraction of coarser grain-size (0.25– 1 mm) (Table 2). Higher percentages of pheophorbides-a were only found in sediments from coastal areas of southern Baltic Sea (open sea — coastal). From the other areas studied, the highest percentages of pheophorbides-a were found for the Ardmucknish Bay (coast of Scotland) sediments (Fig. 4B). These derivatives are relatively unstable and, as we know from previous studies, pheophorbides-a most often occur in the water column or in freshly formed sediments. The contents of pheophorbides-a can also be dependent on the time of sampling and were found to be much higher in the May 2003 samples than in those from October 2004 (Szymczak-Żyła and Kowalewska, 2007). Cyanobacteria, chlorophytes and diatoms aged in vitro in either anoxic or oxic conditions have been reported as producing large percentages of pheophorbide-a (Louda et al., 1998, 2002). Both low total chloropigments-a content in sediments of Ardmucknish Bay and occurrence of chlorophyll-a allomers and pheophorbides-a suggest good oxygen conditions and an apparent lack of nutrient enrichment in Ardmucknish Bay of Scotland. Pyropheophorbide-a percentages were slightly higher at coastal stations of the southern Baltic Sea, especially in Pomeranian Bay, which correlates well with the known intensive grazing activity in that area (Chojnacki, 1991; Piesik and Wawrzyniak-Wydrowska, 1997). The percentages of these derivatives are positively correlated with oxygen contents in near-bottom water and the sediment fractions of grain-size 0.25 and 1.0 mm and negatively with organic carbon contents. Heterotrophic organisms transform chlorophyll-a mostly to pyropheophorbide-a (Abele-Oeschger and Theede, 1991; Bianchi et al., 1988; Cartaxana et al., 2003, Szymczak-Żyła et al., 2006). In those studies, organisms were found to excrete non-decomposed chlorophyll-a and pyropheophorbide-a in feces and pseudofeces pigments and therefore contribute to their enrichment within sediments. High percentages of pyropheophorbide-a were also determined in sediment samples of Florida Bay (WR2, Fig. 4B) and likely represents both the senescence/death alterations (Louda et al. 1998, 2002) of chlorophyll-a in the large diatom component of these sediments (Louda et al. 2000) as well as the grazer (copepod, molluscs, etc.) induced changes given above. Pyropheophytin-a and steryl chlorin esters (SCEs) made up a considerable percentage in older Gotland Deep sediments (up to 74%

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4. Conclusions

Fig. 6. Relationship between the percentages of total surficial sedimentary chlorophyll derivatives formed by the sum of pyrophaeophytin-a and steryl chlorine esters, and the oxygen concentrations of near-bottom water.

in 368–362 cm layer) (Fig. 4B). Within recent sediments, the highest percentages of these derivatives were in samples collected from deep stations, namely the Gdańsk and Bornholm Deeps. Also the Wisła Lagoon and Szczecin Lagoon samples contain considerable amount of these derivatives. From our other study areas, the highest percentages of pyropheophytin-a and steryl chlorin esters were in sediments from Little Lake Worth, where percentage of these two derivatives amounted to ~44%. (Fig. 4B). Pyropheophytin-a and steryl chlorins were characterized by a positive correlation with organic carbon and a negative correlation with the oxygen concentration in the nearbottom water (Table 2, Fig. 6). These observed correlations indicate that pyropheophytin-a and steryl derivatives of phorbides are retained mainly in anoxic sediments rich in organic carbon, such as the Gdańsk and Bornholm Deeps. Despite their shallowness, both the Lagoons of the southern Baltic Sea and Little Lake Worth were characterized by low oxygen concentration in near-bottom waters. Others have also reported substantial amounts of these derivatives in anoxic sediments (Chen et al., 2001; Louda et al., 2000; Shankle et al., 2001; Villanueva and Hastings, 2000). Cluster analysis of the areas studied (Fig. 7), taking into account percentage of specific pigments in the sum of chloropigments-a, showed that composition of chloropigment-a in sediments of Gdańsk and Bornholm Deep, Szczecin and Wiała Lagoon and Little Lake Worth were similar. According to our previous laboratory investigation, a highly important factor in the decomposition of chlorophyll-a, is the presence of oxygen and aerobic microorganisms. In anoxic conditions, chlorophyll-a is preferentially degraded to pyropheophytin-a and steryl phorbide derivatives (Szymczak-Żyła et al., 2008b). This could explain the highest relative occurrence of these derivatives in anoxic sediments, such as the Deeps and Lagoons of the southern Baltic or in Little Lake Worth in Florida.

Both the sum of chloropigments-a and specific chlorophyll-a derivatives in recent sediments are good markers for the spatiotemporal integrated state of various depositional environments. Nevertheless, both the concentration and the percentage of each pigment in the sum of chloropigments-a is taken as reflecting the interaction of primary production, grazing, sedimentation rate, water mixing, solar radiation, water depth, turbidity, average temperature, bottom water oxygen fugacity and the abundance of benthic and micro-organisms. Despite different environmental conditions between the sediments of the southern Baltic and certain other coastal areas of the world, no differences were discovered in the sort of particular chloropigment-a, in recent sediments of the studied regions but in their percentages in the sum. These studies indicate that particular sedimentary chlorophyll-a derivatives may be taken as markers of the syn- and postdepositional integrated environmental conditions. Chlorophyll-a allomers are characteristic for sediments originating from the oxygenated coastal zone. Chlorophyll-a and pheophorbides-a indicate the presence of comparatively fresh material. Pyropheophorbide-a are mainly a marker for grazing, by zooplankton and/or zoobenthos. Finally, pyropheophytin-a and the steryl derivatives occur mainly in anoxic sediments. High percentage of these last derivatives in sediments is caused by the processes, in which microorganisms are involved.

Acknowledgements This work has been done in the Statutory Research Programme of the Institute of Oceanology PAS and partly in the framework of the grant no. N00014-4 04-1-404 from the Department of the U.S. Navy: Naval Research International Field Office. We express our gratitude to Dr. Brygida Wawrzyniak-Wydrowska of the Paleooceanology Department, Szczecin University, for collecting of sediment samples from Szczecin Lagoon and Pomeranian Bay and for performing the granulometric analysis, and also to Dr. Jan Warzocha of Sea Fisheries Institute in Gdynia for collecting samples from Wisła Lagoon. Dr. Ludwik Lubecki of IOPAS is acknowledged for performing organic carbon content analysis. The authors would like to thank Prof. Bruno Pavoni of University of Venice and Dr. Frithjof Küpper of The Scottish Association for Marine Science, for the opportunity to obtain sediment samples from Venice Lagoon and from coast of Scotland in the framework of cooperation: Polish-Italian joint research project for years 2007–2009 (project no. 11) and agreement between Royal Society of Edinburg and Polish Academy of Sciences. Drs. W.H. Orem and E. Shinn of the United States Geological Survey are thanked for their guidance and assistance in obtaining the Whipray Basin cores in Florida Bay. Previous funding to JWmL for the Florida Bay study derived from the United States National Oceanic and Atmospheric Administration and the Lake Worth studies were partly covered with funds from the South Florida Water Management District and Florida Atlantic University. JWmL and MS-Z thank the Visitor Support Program (VSP) of the United States Office of Naval Research, International Field Office for travel and living expenses for Malgorzata Szymczak-Zyla.(VSP# 4047 and Grant # N00014-04-1-4047. 2004).

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