The effects of changes in catchment nutrient loading and composition on the phytoplankton dynamics, development of hypoxia and internal nutrient dynamics in a stratified coastal lagoon system (the Gippsland Lakes) were investigated using a 3-D coupled hydrodynamic biogeochemical water quality model. The study showed that primary production was equally sensitive to changed dissolved inorganic and particulate organic nitrogen loads, highlighting the need for a better understanding of particulate organic matter bioavailability. Stratification and sediment carbon enrichment were the main drivers for the hypoxia and subsequent sediment phosphorus release in Lake King. High primary production stimulated by large nitrogen loading brought on by a winter flood contributed almost all the sediment carbon deposition (as opposed to catchment loads), which was ultimately responsible for summer bottom-water hypoxia. Interestingly, internal recycling of phosphorus was more sensitive to changed nitrogen loads than total phosphorus loads, highlighting the potential importance of nitrogen loads exerting a control over systems that become phosphorus limited (such as during summer nitrogen-fixing blooms of cyanobacteria). Therefore, the current study highlighted the need to reduce both total nitrogen and total phosphorus for water quality improvement in estuarine systems.
Excessive anthropogenic nutrient loading, particularly nitrogen, has led to widespread hypoxia and other ecological damages in estuarine and coastal areas (Howarth et al., 2011). About half of the known hypoxic events have been caused by eutrophication (Diaz and Rosenberg, 2008). High primary production as a result of eutrophication can lead to hypoxia or anoxia in poorly mixed bottom water and subsequently enhance the recycling of both nitrogen and phosphorus, which again can reinforce eutrophication (Correll, 1998). This has been found in many stratified estuarine systems around the world, including the Baltic Sea (Vahtera et al., 2007) and the Black Sea (Capet et al., 2016), the Neuse River Estuary (Paerl et al., 1995), and the Gippsland Lakes (Scicluna et al., 2015). The magnitude of sediment phosphorus release is related to severity of bottom-water dissolved oxygen (DO) depletion as well as the duration of hypoxia and/or anoxia. For example, Conley et al. (2002) found that the annual change in dissolved inorganic phosphorus (DIP) in the Baltic Sea was proportional to the area covered by hypoxic water rather than the catchment phosphorus load.
Although some researchers argued that a reduction in both nitrogen and
phosphorus were important to improve hypoxia in areas such as the Gulf of
Mexico (Rabalais et al., 2007) and the Baltic Sea (Vahtera et
al., 2007), others considered that nitrogen should be the primary factor
driving marine coastal eutrophication (Diaz, 2001; Hagy et al., 2004;
Howarth and Marino, 2006) and thus hypoxia. Regardless of this controversy,
the global river export of phosphorus to the coastal ocean has already
decreased significantly as a result of advances in wastewater treatment
technology since the start of the 21st century; however, nitrogen export
still remained high (Howarth et al., 2011). The form and composition
of nitrogen export, i.e. dissolved inorganic nitrogen (DIN) and particulate
organic nitrogen (PON), can also have a significant impact on receiving
coastal waters, as they have different residence times and bioavailability.
Seitzinger et al. (2002) showed that total global PON and DIN export
by rivers in 1990 were similar, but the DIN : PON ratios varied from region to
region. Generally speaking, the DIN : PON ratio was much higher in areas with
larger population, indicating that anthropogenic activities had a larger
influence on DIN export compared to PON export. The global DIN input to
coastal systems was predicted to increase by more than 120
Coupled hydrodynamic and biogeochemical models are now increasingly sophisticated and can capture complex biogeochemical feedbacks. There have been a number of successful applications of these models in studying the effects of changes in anthropogenic nutrient loading on the water quality dynamics in estuarine waters (Kiirikki et al., 2001; Webster et al., 2001; Neumann et al., 2002; Pitkänen et al., 2007; Skerratt et al., 2013). However, all these studies primarily focused on the effectiveness of alternative management scenarios for estuarine systems. None of these studies have addressed the sensitivity of hypoxia dynamics and internal nutrient cycling to different forms of nitrogen, phosphorus and organic carbon inputs, which has important scientific and management implications for estuarine water quality.
In this study, we utilised a 3-D coupled hydrodynamic–biogeochemical model to evaluate (1) the sensitivity of phytoplankton and hypoxia dynamics in the Gippsland Lakes to the change in composition of anthropogenic nutrient loading and (2) the consequent impact on internal nutrient dynamics.
The Gippsland Lakes, located in the southeast of Australia, are the largest
estuarine coastal lagoon system in Australia (Fig. 1). The system consists of three main lakes with a total surface area of
about 360
Gippsland Lakes, major tributaries and the location of Lake King North (LKN).
The Gippsland Lakes suffer recurring blooms of toxic nitrogen-fixing cyanobacteria in summers following floods in winter and spring. Together with stratification, high carbon delivery to the sediment in winter and spring following flood-induced diatom and dinoflagellate blooms caused depleted bottom-water oxygen in summer and a subsequent large release of phosphorus from the sediment in the central basins of Lake King and Victoria. Between July and August 2011, the Gippsland Lakes experienced two consecutive floods. In the following summer, a large toxic cyanobacteria bloom occurred in the lakes that persisted from mid-November 2011 to the end of January 2012. It was found that sediment phosphorus release as a result of depleted bottom DO rather than catchment load supplied most of the phosphorus to support the development of the bloom (Zhu et al., 2016).
The coupled model used in the current study was developed by Zhu
et al. (2016) using DHI's MIKE3 FM and ECO Lab. The model consists of two components, the hydrodynamic model and the
biogeochemical model. The hydrodynamic model simulated the
transport and turbulent mixing in the water column. The horizontal domain of
the hydrodynamic model was discretised as triangular and quadrilateral
elements with element areas ranging from 1500
The water quality model contains 41 state variables describing the chemical, biological and ecological processes occurring in the water
column and sediment compartments. The model included three groups of
phytoplankton, which were N-fixing cyanobacteria, vertically migrating
dinoflagellates and fast-growing diatoms. One group of grazers was included
and configured to avoid grazing on cyanobacteria. The mortality of
phytoplankton together with the catchment input was the major source of
organic matter. The organic matter was represented by particulate organic
carbon (POC), PON, and particulate organic phosphorus (POP) and was further
divided into labile and refractory fractions. To simplify, the dissolved
organic carbon and nutrients
and the hydrolysis process (conversion from
particulate to dissolved organic carbon and nutrients) have not been modelled
explicitly. Instead, the model has been configured in the way that
mineralisation of particulate organic carbon and nutrients took place without
going through hydrolysis first. An accumulation of organic matter layer in
the bottom water was formed due to settling. Some of the accumulated organic
matter would deposit in the sediment and some would return to the water column
by resuspension. The rates of deposition and resuspension were calculated
based on the modelled local shear stress and the critical shear stress
defined for deposition and resuspension. Burial was active when the total
thickness of sediment organic matter exceeded 20
It has previously been shown that internal phosphorus recycling is a key process within the Gippsland Lakes, requiring a refined implementation into water quality models (Webster et al., 2001). The present model overcame previous limitations by implementing sorption and desorption of sediment phosphate and bioirrigation into the model, enabling an accurate simulation of sediment phosphorus dynamics. The sorption and desorption of sediment phosphate were modelled explicitly based on the penetration depth of oxygen and nitrate and the sediment iron concentration, which was a spatially varying constant estimated by using the data collected from previous studies. The impact of bioirrigation was modelled by introducing a scaling factor that was used to adjust the diffusion rates of oxygen and inorganic nutrients at the sediment–water interface. The scaling factor was a function of temperature, DO and labile organic matter. In addition, the model also included a simple cohesive sediment transport module with two bed layers that took into account the salinity and shear stress due to wind–wave and current interactions.
The initial conditions, especially the sediment nutrient storage, could have a large impact on the model simulation. The initial condition of organic carbon, nitrogen, and phosphorus and inorganic nitrogen in the sediment was estimated by iteratively simulating the model for a year, and the concentration at the end of a simulation was used as the initial condition for successive simulations. This was repeated until the sediment nutrient inventory did not change substantially by the end of the simulation. A spatially varying sediment iron-bound phosphate distribution was estimated based on previous field studies.
The total sediment DIN, iron-bound phosphate, and labile POC, PON, and POP in
the Gippsland Lakes were approximately 118
Catchment nutrient load data were obtained from the Water Measurement
Information System (previously was known as Victorian Water Resources Data
Warehouse), which is managed by the Department of Environment, Land, Water
and Planning (DELWP). The nutrient data consisted of various constituent
concentrations including total nitrogen (TN), nitrate, nitrite, ammonia,
total Kjeldahl nitrogen (TKN), total phosphorus (TP) and DIP. The
concentrations of the total inorganic and particulate organic nutrients were
first calculated using the raw data, and the particulate organic nutrients
were then further divided into labile and refractory fractions. There were no
measured data for the riverine carbon input; thus, the catchment organic carbon
load was estimated using the organic nitrogen load, assuming a
River flow rates and monthly catchment nutrient input.
On average, the western rivers (Latrobe, Thomson and Avon rivers)
and eastern rivers (Mitchell, Tambo and Nicholson rivers) each supplied
approximately 52 and 48
Nutrient loads between May 2010 and July 2012.
For the current study, we used the calibrated model as the base case and
simulated a number of nutrient load scenarios for the same period. There
were five sets of scenarios with adjusted loads for DIN, PON, TN (DIN
The annual total primary production (TPP) rate in Lake Wellington could
reach as high as 600
Modelled depth-integrated total annual primary production for the base case.
Modelled total primary production in Lake King between May 2010 and
July 2012: DIN, change in dissolved inorganic nitrogen load; PON
Modelled total area experiencing hypoxia in Lake King.
Occurrence of hypoxia as a percentage of time at LKN.
Median bottom-water DO concentration.
Annual sediment T
The total area in Lake King covered by hypoxic bottom water was about 40
The total
Annual sediment ammonia flux from Lake King.
Annual average denitrification efficiency in Lake King.
Annual sediment phosphate flux from Lake King.
Denitrification efficiency is a commonly used measure of the efficiency of nitrogen removal
from sediments. It has been defined as the percentage of
inorganic nitrogen released from the sediment as dinitrogen gas (
Through observations and modelling, we have previously documented the seasonal dynamics of phytoplankton and nutrient cycling in the Gippsland Lakes (Cook and Holland, 2012; Cook et al., 2010). High winter inflows carried nitrogen into the Gippsland Lakes, which stimulated phytoplankton production. Inputs of organic matter from internal production and the catchment led to hypoxia throughout spring and summer, which then caused phosphorus release from the sediment. We now discuss the sensitivity of this conceptual model to changes in external nutrient loading rates.
Outside the summer cyanobacterial blooms, the lakes are typically nitrogen
limited (Holland et al., 2012), and we therefore expected a
strong sensitivity of primary production to nitrogen loading rates.
Surprisingly, the model showed that primary production was equally sensitive
to inorganic and particulate nitrogen loading and that there were two
distinct mechanisms by which these two nitrogen forms were trapped within
the lakes. Particulate nitrogen can settle down to the sediment while only a
negligible portion of the inorganic nitrogen can be transported to the
sediment by diffusion unless converted to particulate form by
photosynthesis. To calculate how much PON or DIN could have been retained in
the lakes after the floods in July and August 2011, we used the model to
simulate the transport of PON and DIN, excluding all the biological and
chemical processes. The results from this simulation showed that 79
Conversely, without any biogeochemical processes such as
phytoplankton uptake, only 32
Sediment POC deposition rate at Lake King contributed by primary production and catchment input.
Seasonal hypoxia is controlled by both stratification and inputs of organic
carbon. The hypoxia observed in the Gippsland Lakes coincided with the
recent transition to higher flow following the Millennium drought, which
ended in 2010. Boesch et al. (2001) also reported the extended hypoxia
in the Chesapeake Bay in the 1970s, which coincided with a transition from
drought to wet years. Large freshwater inflows do not only enhance
stratification but also increase catchment carbon and nutrient loads.
Similar to many other estuary systems, such as the Baltic Sea
(Conley et al., 2002) and the Black Sea (Capet et al., 2013),
the suppressed oxygen replenishment due to stratification and high oxygen
consumption from the mineralisation of deposited organic carbon were the
main causes of the hypoxia in Lake King. Stratification in Lake King could
last up to several months before the water column became well-mixed again.
Lake King also had a higher deposition rate compared to the other parts of
the lakes and the majority of the POC deposition was found to be in the
deeper basin in northern Lake King. This was because a semi-closed
circulation pattern was formed in this area as a result of the interaction
between the outgoing river flow and the incoming tidal flow from the ocean,
resulting in a lot of POC being trapped in the area unless there was a large
flood or storm surge. Another important reason for POC retention in the Lake
King basin was that the bottom shear stress in this area was generally low
and the 90th percentile shear velocity was only 0.34
There has been controversy as to whether internal primary production
stimulated directly by anthropogenic nutrients or external catchment organic
carbon inputs caused hypoxia in estuaries such as the Gulf of Mexico
(Boesch et al., 2009). Previous studies have suggested that carbon
either derived from algal blooms or the catchment could result in estuarine
hypoxia depending on the hydrological and meteorological conditions
(Paerl et al., 1998). To compare the relative importance of the
catchment carbon and primary production to the development of hypoxia in
Lake King and sediment phosphorus flux, a mass balance calculation was
undertaken to calculate the amount of labile POC deposited in the sediment
of Lake King. The mass balance calculation was carried out for the period
between July 2011 and January 2012 and this was when severe hypoxia and high
sediment
The 2011 winter flood brought approximately 4500
Internal nutrient recycling can be a critical supply of nutrients to algal
growth and it is therefore important to consider the sensitivity of these
processes to changes in external loading. Consistent with previous studies
(Mulholland et al., 2008; Gardner and McCarthy, 2009), denitrification
efficiency increased with reduced nitrogen loading rates, which reduced
sediment hypoxia and sediment organic carbon mineralisation rates.
Interestingly, at high reductions in phosphorus loading, there was also a
large increase in denitrification efficiency, which resulted from the
already noted transition to
We have previously shown that the primary source of phosphorus fuelling
summer blooms of
Compared to DIN, PON had a slightly larger impact on the bottom DO
concentration in Lake King most likely because POC load was related to PON
load. The results showed that LKN was more susceptible to TN loading to a
certain extent when compared to TP. However, initial input of catchment
phosphorus was essential to stimulate primary production, which contributed
the majority of the carbon enrichment in the sediment. To eliminate hypoxia in
the Gippsland Lakes within the timescale (
For the Gippsland Lakes, the majority of the catchment nutrient flux was
non-point source introduced by the flood, making it difficult to manage. The
reduction in dissolved inorganic nutrients in flood waters would be
particularly more challenging. However, the current study has shown that the
water quality in the lakes was also largely influenced by particulate
nitrogen and phosphorus, each of which comprised about 60 and 80
Hypoxia and associated sediment phosphorus release in Lake King were predominantly driven by stratification and sediment carbon enrichment. Primary production stimulated by nitrogen loads rather than catchment organic carbon input contributed the majority of the carbon enrichment and was therefore responsible for the depletion of bottom-water DO in summer. Although a significant amount of phosphorus was stored in the sediment, it would only be released under low bottom-water DO conditions in which a large quantity of POC settled in the sediment, which was ultimately driven by nitrogen loading. In addition, the residence time of flood-introduced DIN could be largely influenced by a number of factors including the availability of phosphorus in flood water. It was found that DIN introduced by floods could be converted to PON by photosynthesis quickly enough to prevent being flushed out of the lakes. The current study demonstrated that it is important to reduce both TN and TP in hypoxia mitigation in estuarine systems.
The model data are available upon request to the corresponding author (Yafei Zhu, yafei.zhu@monash.edu).
The authors declare that they have no conflict of interest.
This work was supported by the Australian research council grant LP140100087 to PLMC and the Victorian Department of Environment, Land, Water and Planning. The authors also thank DHI for provision of licenses for MIKE21 SW, MIKE3 FM and ECO Lab. Edited by: Caroline P. Slomp Reviewed by: two anonymous referees