Exceptionally high organic nitrogen concentrations in a semi-arid South Texas estuary susceptible to brown tide blooms
Introduction
Estuaries provide critical habitat for important fish and shellfish species and play a vital role in the economy of coastal states, including Texas (Lacson and Lee, 1997, Jones and Tanyeri-Abur, 2001). Water quality is a major determinant of the health of estuaries, and consequently affects the ability of these systems to support healthy fisheries (Whitfield and Elliott, 2002, Eby et al., 2005). Texas has seven primary estuarine systems from its eastern border with Louisiana to its southern border with Mexico, along with numerous smaller bays within these systems. Texas’ coastal counties have experienced human population growth over the past two decades, with future growth expected to contribute to an additional 26–82% increase by 2050 (Texas State Data Center, http://txsdc.utsa.edu/Data/TPEPP/Projections/Index.aspx). Along with this growing urban footprint on coastal land use coverage, agriculture remains a significant land use in many Texas watersheds (NOAA Coastal Change Analysis Program). Worldwide, both urban and agricultural land uses have been shown to contribute to water quality degradation through pollutant (i.e., nutrients, bacteria) inputs to receiving waterbodies (Hopkinson and Vallino, 1995, Handler et al., 2006).
Despite the pronounced presence of urbanization and agriculture in Texas coastal watersheds, widespread negative effects on water quality have not been reported to date. Wetz et al. (2016) found localized negative effects of municipal wastewater discharge on a small secondary bay system (Oso Bay), but the ecosystem impacts were unclear. Thronson and Quigg (2008) summarized fish kill records for Texas estuaries from 1970 to 2006 and found that low dissolved oxygen during warmer months was believed to be an important cause of fish kills, yet the driver(s) of this low dissolved oxygen, whether natural or human-induced, were not determined. In the most recent National Estuarine Eutrophication Assessment, five of nine Texas estuaries assessed had moderate or moderate to low eutrophication condition, while four others lacked sufficient data for assessment (Bricker et al., 2007).
Although widespread water quality degradation is not apparent on the Texas coast, localized concerns have arisen over the past few decades. One area of concern is the Baffin Bay-Upper Laguna Madre complex. Since 1990, Baffin Bay and adjacent Upper Laguna Madre have experienced large, prolonged blooms of the “brown tide” phytoplankton species, Aureoumbra lagunensis (Buskey et al., 1998, Buskey et al., 2001). The first reported bloom began in early 1990 in tributaries of Baffin Bay, but eventually spread to both the Upper and Lower Laguna Madre (Stockwell et al., 1993), resulting in seagrass die-off (Onuf, 1996, Onuf, 2000). Remnants of this bloom persisted for nearly seven years in the Baffin Bay-Laguna Madre complex (Buskey et al., 2001). Since then, several additional brown tide blooms have occurred in the same area (unpubl. Texas Parks & Wildlife reports; Wetz et al. unpubl. data). Previous studies have attributed development of the 1990 brown tide bloom to both lack of top-down control and a concurrent pulse of nutrients that stimulated growth. Microzooplankton grazer abundances as well as benthic filter feeder abundances were very low during bloom development, coincident with a period of drought and hypersaline conditions (Montagna et al., 1993, Buskey et al., 1997). As for the nutrient pulse, it was speculated that this was derived from agricultural runoff and/or decay of dead fish (e.g., Stockwell et al., 1993, Whitledge, 1993), but the main source has never been identified. Likewise, virtually nothing is known about the nutrient source(s) that have allowed for brown tide bloom persistence and/or redevelopment in subsequent years. Experimental studies have determined that A. lagunensis is a mixotroph that relies on reduced nitrogen (ammonium, organic nitrogen) for growth, but it cannot utilize nitrate (DeYoe and Suttle, 1994, Muhlstein and Villareal, 2007, Agostoni and Erdner, 2011).
Brown tide is not the only issue of concern in terms of water quality in Baffin Bay. For example, hypoxia has been documented, including on several occasions that coincided with large fish kills over the past decade (unpubl. Texas Parks & Wildlife reports). In addition, a large fish kill occurred in late 2010 coincident with hypoxia as well as a bloom of the dinoflagellate Pyrodinium bahamense (unpubl. Texas Parks & Wildlife reports). P. bahamense is known to produce toxins under certain conditions (Phlips et al., 2015), and has been implicated in low dissolved oxygen events that led to fish kills elsewhere (e.g., Morrison and Greening, 2011). Recent studies suggest that P. bahamense is typically most competitive under relatively high nutrient input conditions (Phlips et al., 2015). As with the prevalence of brown tide blooms, it is unclear as to whether the hypoxic events as well as P. bahamense bloom represent symptoms of larger-scale water quality degradation or simply natural variability.
Here we report results from an assessment of water quality conditions in Baffin Bay, Texas. The primary focus is on the spatial extent of, and long-term changes in, select water quality indicators. Differences are also highlighted between Baffin Bay and other estuarine systems along the Texas coast that have not experienced brown tide blooms, offering new insight into potential drivers of brown tide bloom formation and persistence.
Section snippets
Baffin Bay characteristics
Baffin Bay is a shallow (<2–3 m) subtropical estuary located in a semi-arid region (Fig. 1). Land use in the Baffin Bay watershed is dominated by agriculture (44%), with urban contribution limited to small cities such as Kingsville (pop. 26,213) and Alice (pop. 19,576) (NOAA Coastal Change Assessment Program). The semi-arid climate coupled with high evaporation rates in the region can lead to hypersaline conditions in Baffin Bay. Winds can be relatively strong in the region and are thought to
Spatial patterns
Broad spatial patterns in water quality variables along the Texas coast were determined by calculating the 10-year average (from 2003 to 2013) of each relevant variable from all available SWQM estuarine sites. There is a strong salinity gradient on the Texas coast, with lower salinities in the northern estuaries and much higher salinities to the south (Fig. 2). This coincides with well-documented precipitation and freshwater inflow gradients (Montagna et al., 2013). Chlorophyll a concentrations
Discussion
For the central-south Texas coast as a whole, symptoms of water quality degradation were generally limited to a few small systems (e.g., Carancahua Bay and Oso Bay) and a site adjacent to the Arroyo Colorado outflow in the Lower Laguna Madre. In fact, most of the estuarine systems examined in this analysis displayed low nutrient and chlorophyll concentrations. Baffin Bay was a notable exception, as it is displaying multiple symptoms of eutrophication including very high organic carbon and
Acknowledgements
We thank the dedicated citizen scientist volunteers who were integral in the Baffin Bay data collections, including: Jim Atkins, Frank Baumann, Jerry Bjork, Jan Cannamore, Al Gordon, Michael Henry, Carl Hooker, Thomas Mullenix, Scott Murray, David Rowsey, Ron Ryon, Jim Scoggins, Charles Sellers, Diane Sellers, John Sutton and Paul Wimberly. We also thank the following individuals for assistance with sample processing: Victor Batres, Kalman Bugica, Kelsey Fisher, Anne-Marie Gavlas, Cory Staryk,
References (59)
- et al.
Analysis of ammonium transporter and urease gene expression in Aureoumbra lagunensis
Harmful Algae
(2011) - et al.
Distributions and seasonal variability of dissolved organic nitrogen in two estuaries in SW England
Mar. Chem.
(2008) - et al.
Seasonal dynamics of dissolved Ra isotopes in the semi-arid bays of south Texas
Mar. Chem.
(2010) - et al.
Effects of nutrient enrichment in the nation's estuaries: a decade of change
Harmful Algae
(2008) - et al.
Nutrient, sulfur and carbon dynamics in a hypersaline lagoon
Estuar. Coast Shelf Sci.
(2004) - et al.
Ecosystem disruptive algal blooms of the brown tide species, Aureococcus anophagefferens and Aureoumbra lagunensis
Harmful Algae
(2012) - et al.
Expansion of harmful brown tides caused by the pelagophyte, Aureoumbra lagunensis DeYoe et Stockwell, to the US east coast
Harmful Algae
(2013) - et al.
The interactive roles of nutrient loading and zooplankton grazing in facilitating the expansion of harmful algal blooms caused by the pelagophyte, Aureoumbra lagunensis, to the Indian River Lagoon, FL, USA
Harmful Algae
(2015) - et al.
The concept of an estuary: a definition that incorporates systems which can become closed to the ocean and hypersaline
Estuar. Coast. Shelf Sci.
(2010) - et al.
Seasonal variability of the Texas “brown tide” (Aureoumbra lagunensis) in relation to environmental parameters
Estuar. Coast Shelf Sci.
(1999)
Photochemical production of ammonium and transformation of dissolved organic matter in the Baltic Sea
Mar. Chem.
El Niño-Southern Oscillation impacts translated to the watershed scale: estuarine salinity patterns along the Texas Gulf Coast, 1982 to 2004
Estuar. Coast. Shelf Sci.
Water quality dynamics in an urbanizing South Texas estuary: relationships with watershed land use coverage
Mar. Poll. Bull.
The Theil-Sen estimator with doubly censored data and applications to astronomy
J. Am. Stat. Assoc.
Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas)
Mar. Ecol. Prog. Ser.
Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems
Aquat. Microb. Ecol.
Baffin Bay Sediment Core Profiling for Historical Water Quality
Effects of Nutrient Enrichment in the Nation's Estuaries: a Decade of Change
DON as a source of bioavailable nitrogen for phytoplankton
Biogeosciences
Disruption of grazer populations as a contributing factor to the initiation of the Texas brown tide algal bloom
Limnol. Oceanogr.
The role of hypersalinity in the persistence of the Texas “brown tide” in the Laguna Madre
J. Plankton Res.
The decline and recovery of a persistent Texas brown tidal algal bloom in the Laguna Madre (Texas, USA)
Estuaries
Significant Anthropogenic-induced Changes of Climate Classes since 1950
Our evolving conceptual model of the coastal eutrophication problem
Mar. Ecol. Prog. Ser.
The inability of the Texas “brown tide” alga to use nitrate and the role of nitrogen in the initiation of a persistent bloom of this organism
J. Phycol.
Habitat degradation from intermittent hypoxia: impacts on demersal fishes
Mar. Ecol. Prog. Ser.
Temperature and phytoplankton growth in the sea
Fish. Bull.
Human development is linked to multiple water body impairments along the California coast
Estuar. Coasts
The relationships among man's activities in watershed and estuaries: a model of runoff effects on patterns of estuarine community metabolism
Estuaries
Cited by (43)
Assessment of water quality of Netravathi-Gurupur estuary, India through chemometric approach for fisheries sustainability
2024, Marine Pollution BulletinCoastal residential canals harbor distinct water quality conditions and phytoplankton community composition
2024, Estuarine, Coastal and Shelf SciencePhytoplankton biomass and community composition in three Texas estuaries differing in freshwater inflow regime
2022, Estuarine, Coastal and Shelf ScienceCitation Excerpt :This is consistent with work showing that low inflow estuaries such as BB can be particularly susceptible to eutrophication (Bricker et al., 2008; Scavia and Liu, 2009). Although it had low inorganic N concentrations, BB had relatively high DON concentrations, some of which is accessible to mixotrophic phytoplankton (Wetz et al., 2017). New work has also indicated the potential for high rates of photoammonification in BB, which would further increase bioavailability of the DON (Liu and Shank, 2015, H. Abdulla, unpubl.
Challenges and perspectives for the Brazilian semi-arid coast under global environmental changes
2021, Perspectives in Ecology and ConservationResponse of planktonic communities to environmental stress in the eutrophic waters of Xiaoping Island in China
2021, ChemosphereCitation Excerpt :Therefore, we should make an effort to investigate the dynamic of mesozooplankton in response to phytoplankton blooms (Alhashmi et al., 2015), and its abiotic stress on the environment (Gobler et al., 2004; Zhou et al., 2008). Many studies focused on the single factor effect on the plankton, such as physical (light or temperature), chemical (nitrogen or phosphorus), and biological factors(predation pressure) (Granéli and Turner, 2006; Wells et al., 2015; Wetz et al., 2017). Under eutrophic environments, the abundance of plankton was influenced by the nutrients (nitrogen and/or phosphorus), predators, and hypoxic/anoxic environment (Ekau et al., 2009; Reed et al., 2016).