The biochemical composition of particulate organic matter (POM) produced through
phytoplankton photosynthesis is important in determining food quality for
planktonic consumers as well as the physiological conditions of phytoplankton.
Major environmental factors controlling the biochemical composition were
seasonally investigated in Gwangyang Bay, South Korea, which has only natural conditions
(e.g., no artificial dams). Water samples for the biochemical
compositions were obtained from three different light depths (100, 30, and
1 %) mainly at three sites in Gwangyang Bay from April 2012 to April 2013.
Different biochemical classes (carbohydrates, CHO; proteins, PRT; and
lipids, LIP) were extracted, and then the concentrations were determined by
the optical density measured with a spectrophotometer. The highest and lowest
PRT compositions among the three biochemical classes were found in April 2012
(58.0 %) and August 2012 (21.2 %), whereas the highest and lowest LIP
compositions were found in August 2012 (49.0 %) and April 2012 (24.8 %),
respectively. The CHO composition was recorded as high in January 2013 and
remained above 25 % during the study period. The calorific contents of
the
food material (FM) ranged from 1.0 to 6.1 Kcal m
Particulate organic matter (POM), mostly from phytoplankton photosynthesis in the euphotic layer, is an important food source for planktonic consumers in water columns (Cauwet, 1978). The biochemical contents reaching the benthic environments are largely utilized by benthic organisms (Nelson and Smith, 1986; Rice et al., 1994). Therefore, POM is an essential link between surface and benthic ecosystems (Graf, 1992). Previous studies showed that the biochemical composition of the POM, including protein (PRT), lipid (LIP), and carbohydrate (CHO) levels, could provide useful information on the nutritional value that is potentially available to consumers (Mayzaud et al, 1989; Navarro et al., 1993; Navarro and Thompson, 1995). However, previous studies mainly focused on the occurrence in the different patterns of the biochemical composition of POM. It is noteworthy to investigate how the biochemical composition of POM responds to changes in various environmental factors, such as nutrients, light, temperature, and salinity, and to assess food quantity for the higher trophic levels.
The sampling location in Gwangyang Bay, Korea. Maps of
Korea
The coastal areas represent one of the world's most vital aquatic resources,
supporting and providing food resources and habitats for large numbers of
fish and shellfish species (Kwak et al., 2012; Wetz and Yoskowitz, 2013;
references therein). In Gwangyang Bay on the southern coast of Korea (Fig. 1),
coastal shellfish farming and fisheries are prevalent. Over the past
decades, the bay has become industrialized with the construction of a steel
mill company, a power plant, and and industrial complex, and environmental
disturbances have been predicted. Also, estuaries have a high short-term
variability depending on many episodic events, such as freshwater inputs,
tidal cycles (neap and spring), and wind (storms) (Cloern and Nichols, 1985).
These anthropogenic forces and environmental changes drastically affect the
estuarine habitat properties, which can cause different biochemical
compositions in POM. Unfortunately, little information is available on
the biochemical composition of POM in the bay. Hence, this study
tested the main environmental factors determining the seasonal
variation and biochemical composition of POM and assessed the quantity of food
material (FM) in the bay. Physical (temperature, salinity, irradiance,
river input and rainfall data), chemical (nutrients), and biological
(chlorophyll
The study site was located in Gwangyang Bay (34.9
To obtain data for the seasonal variation in POM at the euphotic depth, the field
samplings were taken at three stations of the bay (St. 1 or St. 2A, St. 4,
and St. 5; see Fig. 1) on a seasonal basis in April, June, August, and October
in 2012 and January and April in 2013. St. 1 was changed to St. 2A after
April 2012 because of logistical problems. Both stations have similar
environmental conditions and are at a relatively close distance. Using a 5 L
Niskin (General Oceanics Inc., Miami, FL, USA)
water sampler, water samples were collected at different depths of three light
intensities (100, 30, and 1 % of surface irradiances; hereafter three light
depths) and transferred to brown sample bottles, which were previously washed
with a solution of 0.1 N HCl. The water samplings were conducted at high
tide periods before noon. The three different light depths were determined by
a Secchi disk using a vertical attenuation coefficient (
To obtain the in situ physical parameters, the water temperature and salinity were
measured with a YSI-30 (YSI Incorporated, Yellow Springs, OH, USA), and photosynthetically active
radiation (PAR) was measured onboard during the cruise. PAR was measured one
time per cruise every 30 s during the incubation hours for primary
productivity by a quantum sensor (LI-190SA; LI-COR Biosciences, Lincoln, NE, USA) with a data logger
(LI-1400; LI-COR) on deck. Since the main purpose of the PAR measurements was
to calculate the hourly primary productivity executed for 4–5 h during the day
at around noon local time, the irradiance values in this study might not be
representative for our sampling periods. Rainfall and river input data during
the study period were obtained from the Korea Meteorological Administration
(
In order to determine Chl
The water samples (300 mL) for POC, PON, and
The environmental factors and Chl
The water samples for the biochemical composition (carbohydrates, proteins,
and lipids) of POM were collected from three light depths. The water samples were
filtered through 47 mm GF/F (Whatman; 0.7
The protein (PRT) concentrations
were assessed according to a modified method of that used by Lowry et al. (1951). The
filters for the PRT analysis were transferred into 12 mL centrifuge tubes with
1 mL DH
The seasonal variation in biochemical composition in Gwangyang Bay.
The lipid (LIP) concentrations were extracted according to a column method
modified from Bligh and Dyer (1959) and Marsh and Weinstein (1966). The
filters for LIP analysis were transferred into 16 mL glass tubes with 3 mL
of chloroform–methanol (1 : 2,
Carbohydrate (CHO) concentrations were measured according to Dubois et
al. (1956). The POM samples for carbohydrate analysis were transferred
individually into 15 mL polypropylene (PP) tubes. After 1 mL of DH
Statistical tests were carried out using the statistic software SPSS
(
The observed nutrient limitations during the study period (nd: not detected).
The values of the environmental factors were summarized in Table 1. The
temperature ranged from 5.5 to 26.1
The highest nutrient concentrations were measured in April 2012 when the
concentrations of NO
The surface irradiance averaged from each measurement for 4–5 h ranged from
167.9
The monthly rainfall and river input at the study location ranged from 15.6 to
559.0 mm (annual
average
The monthly patterns of rainfall and river input.
The
The contents of CHO, PRT, and LIP of POM in the water column were
14.2–412.3
In order to estimate the biochemical composition as food quality, we
obtained the relative contributions of each biochemical concentration of POM to FM based
on percentage. The biochemical compositions of each class (CHO, PRT, and
LIP) were 8.3–59.1, 6.8–74.9, and 9.4–68.3 %, respectively (annual
average
The
The biochemical concentrations, composition, calorific values, and contents in Gwangyang Bay (“–” indicates no data).
The calorific values and contents of FM were 5.4–7.9 Kcal g
The relationships between the biochemical pools and environmental conditions were determined by using a Pearson's correlation matrix (Table 6). Based on the results,
we found significant positive relationships between PRT composition and
river input (
The positive relationship between river input and protein composition. River inputs were integrated from 20 days prior to our sampling dates.
The significant correlation coefficient (
The annual average Chl
The inverse relationship between lipid compositions and protein compositions.
Despite this dissimilarity in environmental factors with high Chl
In general, POM consists of a mixture of living as well as detritus materials
(phytoplankton, bacteria, zooplankton, fecal pellets, terrestrial matter,
etc.) originating from freshwater and estuarine and marine environments. POM
samples can be characterized or determined for the source of the major
contributor(s). The C : N ratio generally ranges between 6 and 10 for
phytoplankton, whereas the ratios are between 3 and 6 for zooplankton and
bacteria (Savoye et al., 2003; references therein). For terrestrial organic
matter, the C : N ratios are normally over 12 (Savoye et al., 2003;
references therein). Therefore, it is useful to classify phytoplankton from
heterotrophs and terrestrial materials (Lobbes et al., 2000; Savoye et al.,
2003; Lee and Whitledge, 2005). In this study, the average C : N ratio of
POM was 7.0 (SD
The biochemical pools of POM originating from phytoplankton are influenced by various environmental factors, such as temperature, salinity, nutrients, and light conditions (Morris et al., 1974; Smith and Morris, 1980; Rivkin and Voytek, 1987; Boëchat and Giani, 2008; Cuhel and Lean, 1987; Mock and Kroon, 2002; Khotimchenko and Yakoleva, 2005; Ventura et al., 2008; Sterner et al., 1997). In this study, significant relationships were found between environmental conditions and biochemical pools, especially PRT and LIP (Table 5). Temperature was positively and negatively correlated with LIP and PRT. Previous studies reported that higher temperature stress mainly affects nitrogen metabolism (Kakinuma et al., 2006), which is related to a significant decrease in PRT with increases in LIP and CHO content (Tomaselli et al., 1988; Oliveira et al., 1999). In phytoplankton under high temperature-stressed conditions, the decrease in PRT content is related to the breakdown of the protein structure and interference with enzyme regulators (Pirt, 1975). LIP is predominant because LIP is more closely associated with the cell structure, particularly thickened cell walls (Smith et al., 1989; Kakinuma et al., 2001, 2006). Our results are in agreement with other work, as described above.
The relationships between nutrients and biochemical pools could be explained
by nutrient limitation and the characteristics of each biochemical compound.
A combination of nutrient concentrations and ratios can be used to assess
nutrient limitation (Dortch and Whitledge, 1992; Justić et al., 1995).
Dortch and Whitledge (1992) suggested that nutrient limitations exist
in the Mississippi river plume and the Gulf of Mexico. This is based on the assumption that if the dissolved inorganic
phosphorus (DIP), dissolved inorganic nitrogen (DIN), and dissolved silicon
(DSi) concentrations in the water column are less than 0.2, 1.0, and
2.0
Although irradiance is also known to be an important governing factor for
biochemical composition, irradiance was not statistically correlated with
biochemical pools in this study (Table 6). We measured PAR during our short
incubation time (4–5 h) for phytoplankton productivity as a parallel study.
Since this short time of measured irradiance can be largely variable by
local weather, it might not be enough to reflect and detect the change in the
biochemical composition of phytoplankton with irradiance. The irradiance
between April 2012 and April 2013 was largely various (approximately
10 times lower in April 2012 than in April 2013; Table 1). The increasing
synthesis of proteins is found as light intensity decreases because a
relatively lower irradiance saturation level is required for protein
synthesis compared to that required for other biochemical components (Lee et al., 2009;
Suárez and Marañón, 2003; Morris and Skea, 1978; Morris et al., 1974).
Consistently, the protein compositions were significantly higher in
April 2012 than in April 2013 (
The structure and composition of phytoplankton assemblages and species could
have a significant influence on the seasonal variation in biochemical
composition. Although we did not conduct a study of the phytoplankton community
structure, there is a seasonal succession in the phytoplankton community structure
in the bay. Previous studies showed that the dominant phytoplankton community
was made up of diatoms with the dominant species
A comparison of the biochemical quantity of POM, FM, and the calorific contents.
However, other studies in different regions reported that environmental conditions, such as temperature, nutrients, and irradiance, are more important controlling factors in biochemical composition than variation in the phytoplankton community and species composition (Lindqvist and Lignell, 1997; Suárez and Marañón, 2003). In this study, we also concluded that DIN from river input was a primary governing factor for the seasonal variation in the biochemical composition of phytoplankton in Gwangyang Bay as discussed above.
Since there were no comparable data available in South Korea, we compared our results with other regions (Table 7), although they were conducted in different seasons and at different sampling depths. The PRT contents in this study were as high as in the Ross Sea (Fabiano and Pusceddu, 1998; Fabiano et al., 1999a), the Amundsen Sea (Kim et al., 2016), and the Humboldt Current System (Isla et al., 2010). A similar range of LIP contents was observed in Bedford Basin (Mayzaud et al., 1989), Yaldad Bay (Navarro et al., 1993), and the Humboldt Current System (Isla et al., 2010). The CHO contents were comparatively higher in this study than in other studies, except Bedford Basin (Mayzaud et al., 1989) and Yaldad Bay (Navarro et al., 1993). One of the highlights is that the calorific contents of FM in this study were generally higher than those in other areas, except in several regions. The FM values were comparatively higher than in other regions, such as the northern Chukchi Sea (Kim et al., 2015; Yun et al., 2015), the Ross Sea (Fabiano et al., 1996, 1999a; Fabiano and Pusceddu, 1998; Pusceddu et al., 1999), the Amundsen Sea (Kim et al., 2016), and the northern part of the East Sea (J. J. Kang et al., unpublished). They were similar to the Humboldt Current System, which is known as an important spawning site for pelagic fish and the highest abundance of anchovy eggs (Isla et al., 2010). Actually, the southern coastal sea (including our study area) in Korea represents calm seas, an indented coastline, and numerous bays, which have high habitat diversities for fish and shellfish (Kwak et al., 2012) with favorable conditions for mariculture (Kwon et al., 2004). The high quantity of FM and the calorific contents of POM found in this study reflected the good nutritive conditions of the primary food materials, mainly provided by phytoplankton, for the maintenance of productive shellfish and fish populations in Gwangyang Bay.
Data are available and can be requested from the corresponding author (sanglee@pusan.ac.kr).
The authors declare that they have no conflict of interest.
We thank the anonymous reviewers who greatly improved an earlier version of the manuscript. This research was supported by the project “Long-term change of structure and function in marine ecosystems of Korea” funded by the Korean Ministry of Oceans and Fisheries. Edited by: G. Herndl Reviewed by: two anonymous referees