Using δ15N values in algal tissue to map locations and potential sources of anthropogenic nutrient inputs on the island of Maui, Hawai‘i, USA

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Abstract

Macroalgal blooms of Hypnea musciformis and Ulva fasciata in coastal waters of Maui only occur in areas of substantial anthropogenic nutrient input, sources of which include wastewater effluent via injection wells, leaking cesspools and agricultural fertilizers. Algal δ15N signatures were used to map anthropogenic nitrogen through coastal surveys (island-wide and fine-scale) and algal deployments along nearshore and offshore gradients. Algal δ15N values of 9.8‰ and 2.0–3.5‰ in Waiehu and across the north-central coast, respectively, suggest that cesspool and agricultural nitrogen reached the respective adjacent coastlines. Effluent was detected in areas proximal to the Wastewater Reclamation Facilities (WWRF) operating Class V injection wells in Lahaina, Kihei and Kahului through elevated algal δ15N values (17.8–50.1‰). From 1997 to 2008, the three WWRFs injected an estimated total volume of 193 million cubic meters (51 billion gallons) of effluent with a nitrogen mass of 1.74 million kilograms (3.84 million pounds).

Introduction

Anthropogenic nitrogen (N) loading to the nearshore marine environment through sewage and fertilizer runoff are known to increase primary productivity in coastal systems (Doering et al., 1995, Taylor et al., 1999, Thornber et al., 2008). In extreme cases, excess nutrient loading in coastal regions has resulted in the formation and proliferation of large scale opportunistic macroalgal blooms (Brittany France, Briand, 1989; Puget Sound Washington USA, Thom and Albright, 1990; Venice Lagoon Italy, Sfriso et al., 1993; Jamaica and southeast Florida USA, Lapointe, 1997, Paerl, 1997, Valiela et al., 1997; Ebro River Delta Spain, Menendez and Comin, 2000; Ythan Estuary Scotland, Raffaelli, 2000; Kaneohe Bay Hawaii USA, Stimson et al., 2001, Lapointe et al., 2005, Morand and Merceron, 2005; Sacca di Goro Italy, Viaroli et al., 2005; southeastern Gulf of California USA, Pinon-Gimate et al., 2009). Ecosystem impacts of large scale algal blooms include diminished water column oxygen levels, negative effects on seagrass beds, fisheries and benthic community composition and increased microbial abundance (Barnes, 1973, Johannes, 1975, Smith et al., 1981, Rosenberg, 1985, Burkholder et al., 1992, Zaitsev, 1992, Alber and Valiela, 1994, Morand and Briand, 1996, McCook, 1999, Raffaelli, 2000).

Sources of additional N entering the ocean are often difficult to detect with many water quality assessment tools (ambient nutrient and salinity measurements) because the ocean is a dynamic environment where currents, wave activity and general mixing events can rapidly dilute potentially elevated nutrient levels. Additionally biological uptake of nutrients may occur at rates similar to input rates making the detection of nutrient flux extremely difficult. The United States Environmental Protection Agency (US EPA) recommends the use of bioassays, biological and habitat data in addition to chemical data for water quality assessments (US EPA, 2002). The use of natural stable isotopes of N (15N:14N, expressed as δ15N) to distinguish between natural and sewage derived N is well established (see Risk et al., 2009 for a recent review) because natural (atmospheric) and fertilizer N sources have generally low signatures (ranging from 0–4 and −4 to 4‰, respectively, (Owens, 1987, Macko and Ostrom, 1994)). Sewage N is enriched in 15N because bacteria preferentially use 14N (Heaton, 1986) thereby elevating sewage derived wastewater in 15N relative to 14N. The extent of 15N enrichment in sewage is therefore dependant upon on the level and type of treatment (i.e. the greater the denitrification via bacterial activity the higher the δ15N value). Consequently, sewage derived δ15N values in the literature from various sources of sewage range from 7‰ to 38‰ (Kendall, 1998, Gartner et al., 2002, Savage and Elmgren, 2004; summarized in Table 1).

The distinct δ15N value of N sources allows for source determination in the marine environment through algal bioassays (Costanzo et al., 2005) despite the potential of isotopic fractionation by algal metabolism. Although phytoplankton have demonstrated strong isotopic preferences for 14N over 15N in N-rich conditions (Pennock et al., 1996), experiments with the macroalga Enteromorpha intestinalis determined that both 14N and 15N were taken up in N-rich conditions and this uptake was in proportion to the supply provided in the experimental treatments (Cohen and Fong, 2005). However if isotopic fractionation were to occur in algae under N-rich conditions, their resulting δ15N value (‰) may be lowered by several parts per thousand and could possibly confound the interpretation of the results (Waser et al., 1998, Cole et al., 2004). In addition, the enzymatic process of N assimilation involving nitrate reductase may also affect algal δ15N values (Mariotti et al., 1982).

Increasingly the view that algae incorporate new N from their environment with little to no isotopic fractionation or discrimination of source (anthropogenic or natural) is gaining support (Gartner et al., 2002, Cohen and Fong, 2005) especially in tropical settings where the natural sources of N are exceptionally low. Algal δ15N values are likely to represent the integration of all available nitrogen sources over time scales of days to weeks. Such responsiveness allows for transplantation studies to determine the variety of N input into a coastline. For example, Costanzo et al. (2005) determined that algae expressed higher δ15N values in a short time frame (∼4 days) when collected from a natural area and relocated to a sewage affected location. Over the past decade, algal δ15N values have increasingly been used in a variety of ecosystems across the world to successfully discriminate between anthropogenic and natural N sources and map the range of anthropogenic impact on alongshore and nearshore–offshore gradients (Lapointe, 1997, McClelland et al., 1997, France et al., 1998, Jones et al., 2001, Gartner et al., 2002, Umezawa et al., 2002, Savage and Elmgren, 2004, Steffy and Kilham, 2004, Barlie and Lapointe, 2005, Deutsch and Voss, 2006, Lin et al., 2007, Thornber et al., 2008, Pitt et al., 2009; Table 1). The values of δ15N for algae growing directly in front of sewage outfalls are often enriched with values ranging from 8‰ to 19‰ (Costanzo et al., 2001, Jones et al., 2001, Gartner et al., 2002, Barlie and Lapointe, 2005, Lin et al., 2007, Thornber et al., 2008, Pitt et al., 2009). Currently the highest reported algal δ15N value is 25.7‰ from the heavily polluted (including sewage) Scheldt Estuary in The Netherlands (Riera et al., 2000). Because the process of denitrification releases N2 into the atmosphere, some wastewater treatment plants use denitrification (in combination with nitrification) or Biological Nitrogen Removal (BNR) to reduce nitrogen levels in the wastewater (Wiesmann, 1994, Zumft, 1997). It is highly likely that facilities employing this method of N removal produce wastewater effluent with highly enriched δ15N values.

Nuisance macroalgal blooms of Hypnea musciformis (Rhodophyta) and Ulva fasciata (Chlorophyta) are problematic in shallow coastal waters around many urbanized and agricultural regions of Maui, Hawai‘i. Beaches in bloom areas are regularly covered with extensive buildups of rotting algal biomass. In addition to obvious ecological impacts, these nuisance algal blooms cost the County of Maui $20 million US dollars annually as a result of clean-up costs and lost revenue due to reduced property values and occupancy rates in the city of Kihei alone (Van Beukering and Cesar, 2004). Recent research has determined that accelerated growth of H. musciformis and U. fasciata is driven by excess nutrients (Dailer and Smith, submitted for publication). Because of the proximity of the algal blooms to human population centers and agricultural regions on Maui, we hypothesized that the blooms are a result of sewage and agricultural pollution to shallow coastal regions.

The Clean Water Act (CWA) (also referred to as the Federal Water Pollution Control Act, 2002 as amended and codified at 33 U.S.C. Section 1251) is the primary federal law regulating anthropogenic sources of water pollutants, including nutrients. The CWA requires state water quality management and pollution control programs to have water quality goals (standards). The State of Hawai‘i water quality standards include criteria related to algal blooms expressed as numeric criteria for nutrients, turbidity, and chlorophyll a and narrative criteria requiring that state waters be free of substances attributable to domestic, industrial, or other controllable sources of pollutants which produce undesirable aquatic life. The State of Hawai‘i water quality standards for Class AA marine waters includes the support and propagation marine life, conservation of coral reefs, compatible recreation and aesthetic enjoyment (SH DOH, 2004). None of these goals are attained when a coast is subjected to algal blooms. If water quality standards are not attained, the waters are considered impaired, and the State of Hawai‘i Department of Health (SH DOH) and US EPA are required to determine the Total Maximum Daily Load (TMDL) for pollutants that are causing the impairment. A TMDL determines the maximum pollutant mass from all sources combined that can be discharged daily to a waterbody while still attaining water quality standards. A TMDL establishes a pollutant budget with wasteload allocations for point sources, load allocations for nonpoint sources; and a margin of safety.

TMDL = WLA + LA + MOS, where: WLA = wasteload allocation for point sources, LA = load allocation for nonpoint sources and MOS = margin of safety.

Through the determination of tissue δ15N values of common algae, this study aimed to (1) identify coastal regions of anthropogenic N enrichment on the island of Maui via an island-wide coastline survey (2) use additional fine-scale surveys in identified areas of concern to map the extent of anthropogenic N along the coastline and (3) determine the extent of anthropogenic N across the coral reef adjacent to the highest δ15N values found. An additional goal of this study was to determine the amount of effluent injected and corresponding nitrogen point source load estimates for the County of Maui Wastewater Reclamation Facilities over the past 11 years.

Section snippets

Study area

The island of Maui has a population of 143,574 (US Census Bureau 2008) and an annual visitor flux of approximately 2 million people (2,089,738 in 2008 http://hawaii.gov/dbedt/info/visitor-stats/ni-stats). The majority of the island remains in a relatively natural undeveloped state (the northwest and eastern regions). Wastewater on Maui is released primarily by underground disposal through shallow injection wells and cesspools. An injection well (IW) is a bored, drilled or driven shaft, or a dug

Island-wide coastline survey

In the summer of 2007, an island-wide survey of intertidal algal δ15N values from all accessible coastlines on Maui was conducted to locate areas and potentially identify sources of anthropogenic N enrichment. Maui has approximately 190 km of coastline with the majority of the population residing in a few discrete regions (Kahului, Waiehu, Kihei, Maalaea, Lahaina, Kaanapali, Kahana and Napili). Survey intervals occurred every 1.5 km in populated areas and every 8 km in unpopulated areas. Where

Island-wide coastline survey

Multiple common genera from the major macroalgal divisions were collected from 45 sites to determine if differences in δ15N values occurred among algae from the same site. Differences (or variability) of δ15N values in algae at the same site could arise from physiologically different nitrogen uptake rates and storage capacities (Wallentinus, 1984) and pigment complexes because phycobilin pigments in the Division Rhodophyta require more nitrogen atoms than other pigments (Graham and Wilcox, 2000

Discussion

Foliose and filamentous macroalgae are excellent indicators of nitrogen sources in marine environments, because they (1) have high nutrient uptake rates and therefore quickly respond to pulses of nutrients (Wallentinus, 1984) (2) acquire and integrate all sources of water column nutrients over extended periods of time (Costanzo et al., 2005, Cohen and Fong, 2005, Lin and Fong, 2008), (3) are attached to the benthos and therefore represent a specific area and potential relationships with

Implications

This work demonstrates the usefulness of algal δ15N values to distinguish between natural and anthropogenic derived N and to identify the spatial extent of algal blooms that are incorporating anthropogenic derived N sources. The method was identified as an assessment tool with potential for use by the State of Hawai‘i’s ongoing Integrated Water Quality Reporting to Congress (SH DOH, 2009). Perhaps more importantly from a management perspective, this work provides a significant nexus between a

Acknowledgements

This work was funded in part by the following agencies: Experimental Program to Stimulate Competitive Research (EPSCoR, #EPS0554657), the Hawai‘i Coral Reef Initiative (HCRI, #NA07NOS4000193), ECOHAB CSCOR, NOAA Publication #322 and the Federal Aid in Sport Fish Restoration Program, through the State of Hawai‘i, Division of Aquatic Resources (#F-17-R-33). We are grateful for the cooperation of the County of Maui, Division of Environmental Management for the use of their data. We also thank

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