Trends in Estuarine Phytoplankton Ecology

7.02

Trends in Estuarine Phytoplankton Ecology

C Lancelot, Université Libre de Bruxelles, Brussels, Belgium K Muylaert, K.U. Leuven Campus Kortrijk, Kortrijk, Belgium © 2011 Elsevier Inc. All rights reserved.

7.02.1 7.02.2 7.02.2.1 7.02.2.2 7.02.2.3 7.02.2.4 7.02.2.5 7.02.3 7.02.4 References

Introduction Multi-Stressors behind Phytoplankton Development in Estuaries Hydrodynamics Hydro-Sedimentary Processes as Drivers of Light Availability Nutrients Salinity Gradient Top-Down Control Trends Conclusions and Perspectives

5 6 6 7 8 9 9 10 11 12

Abstract A review of the multi-stressors behind phytoplankton development in estuaries shows that differences in salinity tolerances and in physical processes (freshwater and particle transport, tidal amplitude, mixing processes, and in upward/downward boundaries) feature in the phytoplankton successions and magnitudes that are specific to each estuary. Nutrient loads play generally only a small role except in subtropical and tropical estuaries during periods of low discharge. The high variability of estuaries worldwide makes their monitoring difficult and the global assessment of their functioning in response to changes in climate and anthropogenic pressures stresses the need to develop online fully coupled river–estuary–coastal ocean physical– biological models at regional scales.

7.02.1 Introduction Estuaries are shallow open systems strongly influenced by river inflows, mixing with the coastal ocean and exchanges across the sediment– and atmosphere–water interfaces. They have distinct salinity gradients in their lower part and a tidal influ ence in the upper freshwater part providing specific hydrological properties when compared to rivers. Estuaries form transitional zones between freshwater and marine envi ronments and are characterized by a large variability in physical, chemical, and biological properties under the dual influence of climate and anthropogenic changes (e.g., Paerl et al., 2010). Aquatic phototrophs (phytoplankton, periphy ton, and macrophytes) compete for light, nutrients and inorganic carbon, and the balance among phototrophs changes with size, depth, and nutrient status of their habitat. In the often nutrient-rich and turbid shallow waters such as estuaries, phytoplankton usually dominates over macrophytes and benthic microalgae (Sand-Jensen and Borum, 1991). The question of an actual estuarine phytoplankton assem blage has been debated lively. Recent statistical analysis of ecological boundaries in estuaries shows no evidence of true estuarine biological communities but rather the existence of a continuum of biological assemblages along the salinity gradient, defining estuaries as ecoclines rather than ecotones (Attrill and Rundle, 2002; Quinlan and Philips, 2007; Muylaert et al., 2009). While marine phytoplankton are adapted to high salinity and freshwater species to low salinity, some of them have evolved at an intermediate salinity (e.g., Jackson et al., 1987; Devassy and Goes, 1988; Roubeix and Lancelot, 2008; Muylaert et al., 2009)

or are resistant to salinity fluctuations and thus can survive in brackish waters (Figure 1). Understanding how freshwater and marine phytoplankton organisms respond to the varying and contrasted physico-chemical conditions encountered when transported downstream and upstream along the estuary is a prerequisite for describing the estuarine succession of phyto plankton assemblages and for assessing the ecological and biogeochemical role of estuaries, in terms of, for example, reten tion of anthropogenic nutrients and direction of water– atmosphere CO2 exchange. Providing a connection with the hinterland through the river, water quality and biological communities of estuaries are strongly influenced by freshwater inputs that deliver sus pended sediments, biogenic elements (nutrients) like nitrogen (N), phosphorus (P) and silicon (Si), and contaminants from land runoff and wastewater discharge (see Chapter 5.10). Nutrient inputs in particular reflect the ways that humans produce and consume food and how they manage water courses and wastewaters in the watersheds. Nutrient inputs to the tidal freshwater estuary and the response of the freshwater phytoplankton community are, however, modulated by cli mate change acting on runoff and rainfall and also on temperature and clouds. At the ocean boundary, changes in atmospherically driven currents by modifying phytoplankton composition and growth conditions in nearshore waters also influence phytoplankton species dominance in the estuary through the tidal flushing which transports coastal phytoplank ton cells into the estuary. Phytoplankton development and species dominance in the estuaries are clearly driven by a complex interplay between

5

6


Probability

1.0

(a)

0.8

Tetrastrum staurogeniaeforme Scenedesmus spp.

0.6

Coelastrum sp. Planktothrix aghardii

0.4 Gymnodinium sp. Monoraphidium centortum

0.2

Pediastrum spp.

0 1.0 (b)

Stephanodiscus hantzschii

ocean–estuary–river physical–biogeochemical models that describe nutrient/contaminant transformations and phyto plankton development along the land–ocean continuum in response to regional changes in climate and human pres sures. As a first step in this direction, we review here the multistressors which are behind phytoplankton development in estuaries in order to help to understand trends in estuarine phytoplankton and to define the needed physical and trophic resolution of the coupled models which are to be used for assessing their future in response to changing climate and for the implementation of environmental policies.

Probability

0.8

Rhodomonas sp. Cyclotella scaldensis Thalassiosira proschkinae 0.6 Actinocyclus normannii Melosira varians Oocystis spp. 0.4 Melosira nummuloides 0.2

0 1.0

Probability

0.8

Actinastrum hantzschii

(c) Guinardia delicatula

Raphoneis amphiceros

0.6

Lithodesmium undulatum

Chaetoceros Rhizosolenia pungens

0.4 0.2

Mixing depth-to photic depth ratio

Triceratuim alternans Rhizosolenia sp. 0 16 14 12 10 8 6 4 2 0 30

(d)

(e)

Salinity

25 20 15 10 5 0 0

20

40

60

80

100 120 140 160 180

Distance from estuary mouth (km) Figure 1 Modeled responses of selected phytoplankton taxa along the longitudinal axis of the Scheldt estuary. Taxa with population maximum in river (a), within the estuary (b), and in coastal waters (c) as adapted from Muylaert et al. (2009) in relationship with the annual mean mixing-to-photic depth (d) and salinity distribution (e) as adapted from Lionard, M., Muylaert, K., Van Gansbeke, D., Vyverman, W., 2005b. Influence of changes in salinity and light intensity on growth of phytoplankton communities from the Schelde river and estuary (Belgium/The Netherlands). Hydrobiologia 540, 105–115. With kind permission from Springer Science + Business Media.

processes occurring over the regional ocean basins and within the watersheds. Such a complexity could be resolved by devel oping and implementing at regional scale coupled

7.02.2 Multi-Stressors behind Phytoplankton Development in Estuaries Considering the interplay between the stressors that are specific for each estuary, each of them is discussed below as a necessary but not exclusive condition for allowing phytoplankton to develop in the estuary. When relevant, interacting factors are pointed out and specific examples are given.

7.02.2.1

Hydrodynamics

Freshwater inputs in estuaries result in a net downstream trans port of water within the estuary. Together with freshwater inputs, the exchange of water with the coastal zone determines the residence time of the water within the estuary. Yet for several of the world’s largest rivers, discharge often exceeds the tidal prism and mixing of freshwater and seawater occurs in coastal waters (e.g., Amazon (Demaster et al., 1996), Changjiang (Edmond et al., 1985), Zaire/Congo (van Bennekom et al., 1978), and Danube (Humborg et al., 1997)). Conversely in the arid and subtropical regions, evapo ration exceeds precipitation during the dry season giving rise to higher salinity in the estuary compared to the adjacent coastal waters. This process typifies inverse estuaries such as the Fitzroy estuary (Radke et al., 2010), the Spencer Gulf (Smith and Veeh, 1989), and the San Quintin Bay (Camacho-Ibar et al., 2003). Because phytoplankton is passively transported along with the water currents, it can only increase within the estuary when net specific growth rates (i.e., the balance between phytoplank ton growth and losses by lysis, grazing, and/or sedimentation) exceed the residence time of the water (Lucas et al., 2009). In many estuaries, the residence time is primarily influenced by river discharge (see Chapter 5.11). Hence, the development of phytoplankton blooms is often, but not always, inversely cor related with river discharge (e.g., Strayer et al., 2008). River discharge varies strongly over different timescales and latitudes and this variability affects phytoplankton dynamics. As a gen eral trend, the timing and magnitude of hydrological factors is more contrasted, episodic, and intense in subtropical and trop ical estuaries due to the seasonal monsoons and the occurrence of droughts, tropical storms, and hurricanes (e.g., Devassy and Goes, 1988; Eyre and Balls, 1999; Briceño and Boyer, 2010). Discharge differences between dry and wet seasons are gener ally two orders of magnitude higher than those observed in temperate estuaries (Eyre and Balls, 1999). In temperate regions, river discharge tends to be higher during winter and lower in summer. In such estuaries, the onset of the phytoplankton bloom in spring often coincides


with a decrease in river discharge. In the San Francisco Bay estuary, phytoplankton blooms are restricted to periods of low river discharge in summer (Cloern et al., 1983). In the turbid freshwater zone of macrotidal estuaries, phytoplankton blooms are also restricted to sustained periods of low river discharge in summer (Filardo and Dunstan, 1985; Jackson et al., 1987; Sin et al., 1999; Muylaert et al., 2005; Arndt et al., 2007). River discharge is sensitive to meteorological conditions showing contrasted inter-annual variability that is often reflected in phytoplankton biomass. In the lower reaches of the Hudson River estuary, phytoplankton blooms are limited by a short residence time of the water. In years when discharge of the Hudson River is low however, residence time in the estuary increases and phytoplankton blooms can develop (Howarth et al., 2000). In the turbid freshwater zone of temperate macrotidal estuaries, phytoplankton biomass also tends to be higher during dry than wet summers (e.g., Lionard et al., 2008). In tropical estuaries the monsoon-driven seasonal discharge patterns and the episodic pulses of freshwater inputs caused by tropical storms or hurricanes constrain phytoplankton biomass building for short periods immediately following floods, that is, when the turbidity caused by the transported suspended particles is decreased (e.g., Devassy and Goes, 1988; Sarma et al., 2009). The occurrence of drought/flood events strongly influences the bloom pattern, that is, the position and species dominance of the phytoplankton biomass maxima along the estuary (e.g., Valdes-Weaver et al., 2006; Costa et al., 2009). Such a positive correlation between phytoplankton increase and transport time is still not found in some estuaries (see references in Lucas et al., 2009). This is explained by a negative balance of phytoplankton growth versus loss processes due to either elevated grazing (Alpine and Cloern, 1992; Strayer et al., 2008), lysis, or sedimentation rates and suggests that the phy toplankton growth-loss balance is modulating the relationship between phytoplankton development and hydrology (Cloern, 1996). Hence, the different response of phytoplankton taxa such as cyanobacteria and diatoms to changing transport times reported by Paerl et al. (2006) might be explained by differences in species growth physiology and susceptibilities to grazing and sinking (Lucas et al., 2009).

7.02.2.2 Hydro-Sedimentary Processes as Drivers of Light Availability Light is a necessary condition for phytoplankton growth. Light availability in the water column is determined by incident sur face light and the vertical light extinction coefficient KPAR which determines the depth of the euphotic zone. The ratio between the euphotic depth and the upper mixing depth then deter mines the light available to phytoplankton cells when transported up and down in the mixed layer. When the euphotic depth is shallow compared to the mixing depth, photosynthesis is insufficient to compensate for dark respira tion and phytoplankton cells lyse or enter a dormancy phase. Several studies have illustrated the importance of evaluating the mixing-to-euphotic depth ratio for understanding light limitation of phytoplankton development in estuaries (Kromkamp and Peene, 1995; Irigoien and Castel, 1997; Desmit et al., 2005). In estuaries, KPAR is mainly determined by the elevated turbidity that distinguishes many estuaries from

7

freshwater and ocean ecosystems where light attenuation is primarily governed by phytoplankton cells. Turbidity has long been considered as the main factor controlling light availability and hence phytoplankton development in estuaries, irrespec tive of nutrient concentrations (Cloern, 1987; Fichez et al., 1992; Heip et al., 1995). This elevated turbidity is due to high concentrations of suspended sediments driven by essentially three mechanisms acting at different locations along the estu ary: (1) tidal currents or wind or wave action resulting in resuspension of bottom sediments in shallow estuaries; (2) local accumulation of suspended matter at the so-called turbidity maxima; and (3) river inputs of large quantities of suspended sediments of terrestrial origin into the estuary. Tidal currents are particularly strong in estuaries that are situated relatively far from amphidromic points such as those near the English Channel or along the East coast of Canada. By causing resuspension of bottom sediments, the tidal currents have a strong influence on turbidity and hence on light avail able for phytoplankton photosynthesis. Monbet (1992) showed that turbidity is higher and phytoplankton biomass is significantly lower in macrotidal estuaries (>2 m tidal range) compared to microtidal estuaries (