Elsevier

Water Research

Volume 47, Issue 15, 1 October 2013, Pages 5783-5793
Water Research

Mechanistic and statistical models of total Vibrio abundance in the Neuse River Estuary

https://doi.org/10.1016/j.watres.2013.06.050Get rights and content

Highlights

  • Presented a new statistical model for Vibrio abundance in the Neuse River Estuary.

  • Generated a five-parameter mechanistic model of Vibrio abundance.

  • Longest study-period of Vibrio in the Neuse River Estuary.

  • Incorporates data from extreme events such as storms, floods, and droughts.

Abstract

Bacteria in the genus Vibrio are ubiquitous to estuarine waters worldwide and are often the dominant genus recovered from these environments. This genus contains several potentially pathogenic species, including Vibrio vulnificus, Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio alginolyticus. These bacteria have short generation times, as low as 20–30 min, and can thus respond rapidly to changing environmental conditions. A five-parameter mechanistic model was generated based on environmental processes including hydrodynamics, growth, and death rates of Vibrio bacteria to predict total Vibrio abundance in the Neuse River Estuary of eastern North Carolina. Additionally an improved statistical model was developed using the easily monitored parameters of temperature and salinity. This updated model includes data that covers more than eight years of constant bacterial monitoring, and incorporates extreme weather events such as droughts, storms, and floods. These models can be used to identify days in which bacterial abundance might coincide with increased health risks.

Introduction

The numerous and highly variable members of the bacterial genus Vibrio are routinely found in marine and estuarine systems as indigenous flora and can be nearly 35% of the culturable bacterial population during warm months (Oliver et al., 1982, Thompson and Polz, 2006). While there are dozens of species within the Vibrio genus, there are four human pathogens of note included in this group: Vibrio cholerae, Vibrio vulnificus, Vibrio parahaemolyticus, and Vibrio alginolyticus. Because infections caused by this genus are associated with recreational, occupational, and transportational uses of estuarine and marine waters, the examination of the population dynamics of these bacteria is required to reduce infection without limiting access to economically important waterways. Monitoring coastal waters for Vibrio bacteria is an effective method for determining the abundance of these potential pathogens, but this is both costly and time consuming. Alternatively, by creating predictive models for the abundance of these bacteria, the periods when infection risks are elevated could be identified with relative ease and nominal costs.

Individual Vibrio spp. respond differently to environmental factors, but typically water temperature and salinity are two of the most important in determining population concentration or distribution (Tantillo et al. 2004). Seasonality among vibrios is observed, with culturable cells being greatly diminished or non-existent during winter and ubiquitous during summer months (Oliver et al., 1982, Tantillo et al., 2004, West, 1989). While some vibrios like V. cholerae can be found in fresh water, most vibrios have a minimum salinity requirement for growth and persistence and all have a maximum salt tolerance, usually around 25‰ (Baker-Austin et al., 2012, Froelich and Oliver, 2013, Gomez-Gil and Roque, 2006, Thompson and Polz, 2006). As average global temperatures rise, increases in precipitation could reduce estuarine salinity while there is a simultaneous increase in water temperature (Baker-Austin et al., 2012, Hakkinen, 2002, IPCC, 2007). This combination would broaden the areas permissive for survival of these pathogens (Baker-Austin et al. 2012).

Estuaries are utilized for a variety of reasons. Their high biological activity makes them an important resource for fish, shellfish, and other seafood, providing more than 75% of the U.S. commercial fish catch (Lauff, 1967, National Safety Council's Environmental Center, 1998). Recreational uses include swimming, boating, wildlife observation, and sport fishing. Estuaries also serve as shipping and transportation centers for local and international commerce (National Safety Council's Environmental Center, 1998). All of these uses introduce the risk of infection by Vibrio bacteria. The Neuse River estuary (NRE), located in eastern North Carolina (Fig. 1), is a coastal plain estuary that is subject to extreme environmental conditions, including droughts, hurricanes, and tropical storms (National Oceanic and Atmospheric Administration, 1999). Prediction of Vibrio populations in this ecosystem has always been important, as changes in environmental conditions could cause unexpected lengthening of the seasonal period of maximal Vibrio concentrations, placing more users of this vital waterway at risk. An empirical model of Vibrio in the NRE was developed by Hsieh et al. (2008) using data collected covering 19 months. Here we present modeling efforts conducted using a large Vibrio monitoring data set spanning more than eight years along multiple sites in the NRE. From these data, we have developed a five-parameter mechanistic model of Vibrio abundance using the Environmental Fluid Dynamics Code or EFDC (Hamrick, 1992). The mechanistic model allows for testing of processes that produce bacterial abundance dynamics. We have also created a broad statistical model that predicts Vibrio spp. concentrations from measured salinity and temperature. By using both of these approaches in conjunction, we have gained a better understanding of Vibrio dynamics in the NRE and have improved upon our ability to predict Vibrio populations.

Section snippets

Environmental sampling

The NRE is part of the second largest estuarine complex in the United States and empties into the Pamlico Sound (Luettich Jr. et al. 2002). Flow in the NRE is dominated by river input and wind while tidal influence is minimized by barrier islands (Luettich et al., 2000, Peierls et al., 2012). The NRE has been extensively monitored for more than two decades though several projects including the NRE Modeling and Monitoring program known as ModMon (http://www.unc.edu/ims/neuse/modmon/index.htm).

Mechanistic Vibrio model

The five-parameter mechanistic model of total Vibrio abundance was formulated using the dye tracer constituent within EFDC. Dye transport simulations were also used to estimate hydrodynamic travel times from the bottom waters of the model boundary with Pamlico Sound. Median values for transport times from the downstream boundary varied from less than 20 days for the most downstream station (Station 180) to more than 40 days for the two upstream stations (Stations 0 and 30, Figs. 1 and 2). As

Discussion

Previous Vibrio modeling efforts of the NRE have been limited to short time spans, spatially limited sampling regimes, or did not contain extreme events such as storms and droughts. These limitations narrow the pool of data from which the models were generated (Hsieh et al., 2008, Pfeffer et al., 2003, Wetz et al., 2008). The models presented here were developed utilizing a data set covering eight years, spanning the full length of NRE, and includes data collected after tropical storms,

Conclusions

The North Carolina Department of Health and Human Services (2012) lists Vibrio infections as reportable diseases and makes efforts to educate anyone who is exposed to seawater or brackish water on the symptoms of these infections. Nefarious pathogens, such as V. vulnificus, V. parahaemolyticus, and V. alginolyticus, are naturally on the list of vibrioses under surveillance but this list also includes Vibrio mimicus, Vibrio fluvialis, Vibrio furnissii, Vibrio hollisae, and Vibrio damsela (NC

Acknowledgments

We thank the following: Denene Blackwood, Monica Greene, Rodney Guajardo, Sydney Brothers, Stephen Fries, Zachary Williams, Jennifer Wetz, Tamer Helmy, Kathy Conn, Reagan Converse, Curt Stumph, Sarah Hatcher, Sarah Rhodes, Sarah Hiser, Luke Meyers, Casey Taylor, Asia Nowakowski, Emma Crill, and Eric Binder for sample processing; Joe Purifoy, Claude Lewis, and Stacy Davis for marine operations; Rick Luettich, Greg Characklis, John Paul, Jim Oliver and David Weber for collaborative input. We

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