Near-Annual Fish Kills in Small Embayments: Casual vs. Causal Factors

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Near-Annual Fish Kills in Small Embayments: Casual vs. Causal FactorsAuthor(s): Allison Skinner McInnes and Antonietta QuiggSource: Journal of Coastal Research, Number 265:957-966. 2010.Published By: Coastal Education and Research FoundationDOI: http://dx.doi.org/10.2112/JCOASTRES-D-10-00006.1URL: http://www.bioone.org/doi/full/10.2112/JCOASTRES-D-10-00006.1

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Near-Annual Fish Kills in Small Embayments: Casual vs.Causal Factors

Allison Skinner McInnes{ and Antonietta Quigg{{

{Department of OceanographyTexas A&M University3146 TAMUCollege Station, TX 77843, [email protected]

{Department of Marine BiologyTexas A&M University at Galveston5007 Avenue UGalveston, TX 77551, U.S.A.

ABSTRACT

McINNES, A.S. and QUIGG, A., 2010. Near-annual fish kills in small embayments: casual vs. causal factors. Journal ofCoastal Research, 26(5), 957–966. West Palm Beach (Florida), ISSN 0749-0208.

Fish kills are reported throughout the nation and a great deal of research is conducted in an attempt to determine thecause of these mortality events. Low dissolved oxygen concentrations, eutrophication, and/or harmful algal blooms aremost commonly cited as causative factors. Lake Madeline and Offatt’s Bayou on Texas’ upper coast have low mixingenvironments due to their relatively small areal size, deep basins, small tidal inlets, and restricted exchange with thenearby Galveston Bay estuary complex. These physical attributes, along with near annual fish kills, make them an idealstudy area for understanding the causes and effects of hypoxia and phytoplankton blooms on fish kills. We measuredphysical, chemical, and biological parameters twice weekly over the course of two summers. Fortuitously, a fish killoccurred in the summer of 2005 but not in 2006, which allowed us to narrow down the likely contributing factors that ledto the kill, consisting of .10,000 Brevoortia partonus (Gulf menhaden). Large amounts of detritus from a cyanobacterialbloom, in conjunction with the strong stratification and hypoxic bottom waters, led to the fish mortality event in 2005.While the system was also stratified during the summer of 2006, chlorophyll and phaeophytin concentrations were 15-fold lower and no fish kill was observed. The combination of factors that led to the observed fish kill demonstrates theimportance of interdisciplinary approaches to investigating the causes of ecological disturbances.

ADDITIONAL INDEX WORDS: Fish kill, cyanobacteria, hypoxia, Texas estuaries, stratification, Gulf menhaden(Brevoortia patronus).

INTRODUCTION

Fish kills are reported throughout the nation and much

research is conducted in an attempt to determine the cause of

these mortality events. The most common causes cited are low

dissolved oxygen (DO) concentrations (hypoxic waters,

,2 mg L21), eutrophication, harmful algal blooms (HABs),

and/or a combination of these factors (Diaz and Rosenberg,

1995; Graneli and Turner, 2006; Lowe et al., 1991; Reynolds-

Fleming and Luettich, 2004; Thronson and Quigg, 2008).

Beyond the obvious loss, large-scale fish kills are indications of

serious ecological disturbances. They are an apparent sign that

conditions within the affected water body have deteriorated to

such a degree that fish life is no longer supported. The

occurrence of a fish kill often affects other trophic levels,

resulting in mass ecosystem dysfunction, public health risk(s),

and in some cases, economic losses.

Hypoxic conditions are commonly reported as the primary

cause of fish kills. Many organisms are unable to cope with the

physiological stress associated with depleted oxygen conditions

(Eby et al., 2005; Ritter and Montagna, 1999; Thronson and

Quigg, 2008; Wannamaker and Rice, 2000). Hypoxia in

estuarine systems has been linked to water column stratifica-

tion (Paerl et al., 1998), with low DO concentrations typically

confined to deeper waters below the pycnocline, leaving the

waters above this density gradient well mixed and oxygenated.

The upper water column serves as a refuge for mobile fauna.

Hypoxia alone as a cause of mass mortality events of mobile

species seems unlikely. Reynolds-Fleming and Luettich (2004)

offered a possible mechanism to account for the death of pelagic

fishes due to hypoxic water, that is, one of wind-driven lateral

upwelling and downwelling. This mechanism was observed in

the Neuse River estuary, North Carolina, U.S.A. The sudden

inundation of hypoxic water to the refuge at the surface

trapped mobile fauna, leading to sufficient stress as to cause a

mass mortality event.

Eutrophication begins with an increase in nutrients and

dissolved organic matter loading, which leads to increases in

detritus throughout the water column. This detritus typically

originates from bacteria, phytoplankton, and zooplankton.

After an algal bloom, the amount of detritus may be of such

high concentrations that it cannot be diluted by the system’s

natural mechanisms (Paerl, 1996; Quigg et al., 2009). As excess

detritus sinks, it is degraded by bacteria; this degradation

process is the primary culprit in the depletion of DO in the water

column. Unless DO is resupplied by physical mixing processes,

this breakdown of detritus often leads to hypoxia and/or anoxia

(Gray, Wu, and Or, 2002; Wassmann and Olli, 2004).

DOI: 10.2112/JCOASTRES-D-10-00006.1 received 11 January 2010;accepted in revision 15 May 2010.Published Pre-print online 11 August 2010.’ Coastal Education & Research Foundation 2010

Journal of Coastal Research 26 5 957–966 West Palm Beach, Florida September 2010

Harmful algal blooms are those that cause a variety of

deleterious effects on aquatic ecosystems, including negative

aesthetic effects such as beach fouling and poisoning of various

organisms (Smayda, 1997). Direct effects include oxygen

depletion, nonchemical effects (clogging of fish gills, leading

to suffocation and oxygen starvation), and chemical effects

(from toxin producing species), which can all lead to fish kills

(Graneli and Turner, 2006; Smayda, 1997). HABs are typically

associated with toxin producing phytoplankton. The most

commonly reported effects are paralytic, diarrhetic, amnesic,

and neurotoxic shellfish poisoning (Graneli and Turner, 2006).

Such toxicity can cause shellfish intoxication (leading to

human fatalities) as well as vectoral intoxication (whereby

toxins are accumulated and transported through pelagic food

webs). The most common and well known culprits involved in

fish kills are the dinoflagellates Gambierdiscus toxicus,

Prorocentrum sp., Ostreopsis sp., Karenia brevis, Alexandrium

sp., and Pfiesteria sp. (Burkholder et al., 1992; Graneli and

Turner, 2006; Wassmann and Olli, 2004). Prymnesium par-

vum, a golden alga, produces toxins responsible for massive

fish and bivalve deaths in brackish water, particularly in Texas

(Roelke et al., 2007). Of the cyanobacteria, Microcystis spp. are

most commonly associated with human and livestock poisoning

as well as fish kills. Under optimal conditions (such as high

light, warm waters, and calm weather, usually in summer),

Microcystis spp. and other cyanobacteria form blooms that are

so dense they appear to form a mat on the surface of the water

(Graneli and Turner, 2006; Paerl, 1996). These blooms,

regardless of the phytoplankton species responsible, affect

water quality and human health.

A study conducted by the U.S. National Oceanic and

Atmospheric Administration (NOAA) compiled the causes

and locations of reported fish kills in the United States (Lowe

et al., 1991). Of the 22 coastal states in the United States, Texas

was ranked highly, not only for having the greatest number of

recorded fish kills, but also for total fish killed (Lowe et al.,

1991). In a study of 4500 fish kill records reported in Texas from

1951 to 2006, the majority of deaths were found to have

occurred in Galveston County, reporting approximately 141

million dead fish (Thronson and Quigg, 2008). A recent meta-

analysis of the Pollution Response Inventory and Species

Mortality (PRISM) database found that in Texas bays, the

majority of fish kills (57%) over a 55-year period were caused by

low levels of DO, while biotoxins such as those produced by

HABs accounted for 7% of deaths and temperature, typically

cold snaps, caused 13% of kills (Thronson and Quigg, 2008).

In many bays and bayous found in Galveston Bay, fish kills

occur annually. Bayous appear to be particularly susceptible

given their inherent sluggish nature and long water residence

times. Fish kill events in Dickinson Bayou (south of Houston,

Texas) are often observed, primarily associated with phyto-

plankton blooms and low water column DO, particularly in the

summer (Quigg et al., 2009). The fish most often affected is

Brevoortia patronus (Gulf menhaden). In the majority of

situations, however, studies are conducted after a fish kill

event, rather than before or during an event—leaving

scientists and resource managers to speculate and surmise on

the events and causal factors that were important in each fish

kill event.

Lake Madeline and the adjoining Offatt’s Bayou (LMOB;

Figure 1) are located in the lower portion of Galveston Bay

(south of Houston, Texas) as an embayment in Galveston

Island (population 57,247 according to the 2000 Census).

Although fish kills have been documented in these waterways

since the early 1960s, the causes remain largely unknown. Like

other bayous, LMOB provides an important habitat for many

finfish and shellfish. Offatt’s Bayou is, however, unique in that

it also serves as an important recreational area for nearby

residents and visitors. In this study we tested the hypothesis

that low DO concentrations are the primary causative factor of

the fish kills occurring during the late summer months in

LMOB. To test this hypothesis, a combination of physical,

chemical, and biological parameters were measured over the

course of two summers (2005 and 2006). The low mixing

environment of LMOB, because of its relatively deep basin,

small tidal inlet, and its restricted exchange with nearby

Galveston Bay estuary, made it an ideal study area for

understanding the causes and effects of hypoxia and phyto-

plankton blooms, both of which are thought to be significant

factors in the near annual fish kills observed in this system.

METHODS

Study Site

Offatt’s Bayou was created by the city of Galveston in the

early part of the 1900s as a borrow pit for landfill when

Galveston Island was raised (Cooper and Morse, 1996). The

bayou is approximately 5 km long with a maximum width of

1 km and an average depth of 5 m (Figure 1). Offatt’s Bayou is

deeper than the surrounding West Bay, with the deepest

portion (indicated by the darkest grays; Figure 1) on the

eastern side, rising to the west to a shallow, narrow, sill-like

inlet as the only means of exchange with neighboring waters of

Galveston Bay. Lake Madeline is a small connected water body

with a similar bathymetry to that of the main bayou, which

tends to magnify any anomalies that the adjoining Offatt’s

Bayou may experience (Figure 1). The deepest portion of Lake

Madeline is the southwest corner; the bathymetry rises to a

similar, shallow, narrow, sill-like mouth, the only means for

exchange between Lake Madeline and Offatt’s Bayou.

Meteorological Data

Wind data (knots) were obtained from the closest NOAA

meteorological monitoring station (Galveston Pleasure Pier,

approximately 1 km away). Hourly data were averaged for each

day and the entire sampling period of each summer. Rainfall

data (cm) was obtained from Scholes Field regional airport

located on Offatt’s Bayou’s south shore (Figure 1). Days on

which the airport recorded rainfall as ‘‘trace’’ amounts were

represented as 0.025 cm, for the purposes of visualizing the

data.

Field Sampling

Fifteen to seventeen sample sites (Figure 1) throughout

LMOB were visited twice each week to obtain a comprehensive

overview of the system’s physical and chemical characteristics.

958 McInnes and Quigg

Journal of Coastal Research, Vol. 26, No. 5, 2010

All trips were conducted between CST 0800–1200 hours unless

weather conditions did not permit. A Seabird 19 SBE

Conductivity Temperature and Depth instrument (CTD) was

used to measure water column profiles of temperature (uC),

salinity, and DO concentrations (mg L21). The CTD data were

downloaded and converted from binary code to ASCII format

using SBE software. These data were further processed by bin-

averaging pressure for every 0.25 m; this format was used in all

calculations and plots in subsequent postprocessing. Surface

water samples were collected (0–0.3 m) and immediately stored

on ice. Plankton tows (67 mm net) in surface waters were

transferred to 50-mL centrifuge tubes and stored on ice.

Plankton tows were collected from random, high turbidity

sites in 2005, but from predefined sites in 2006 (Stations 3, 4, 7,

10, 14, and 17; Figure 1). In 2006, additional samples were

collected when turbidity was high or other interesting

phenomena were observed.

Laboratory Measurements

Water samples were filtered onto 25-mm Whatman GF/F

filters and frozen immediately (220uC). Chlorophyll a (chl a)

and phaeophytin a (phae a) concentrations were measured

using a Turner 10-AU fluorometer. Calibration and measure-

ment techniques were performed according to Arar and Collins

(1997) with some modifications. Filters were extracted with a

50/50 solution of 90% acetone/DMSO and kept overnight in the

dark at 4uC. Filters were removed and samples centrifuged for

5 min to pellet any particulates. After measuring the initial

fluorescence, samples were acidified with 10% HCl and the

fluorescence was measured a second time.

Phytoplankton Identification

Plankton samples were preserved with formalin (final

solution 3%) and kept in a dark, cool place. Phytoplankton

Figure 1. Lake Madeline and Offatt’s Bayou (LMOB) with sites and bathymetry; squares indicate sites sampled both summers (2005 and 2006), circles

indicate sites sampled only in 2006. Darker gray indicates deeper portions while lighter grays represent shallow areas.

Near-Annual Fish Kills 959


were identified to genus level using Tomas (1997). Preserved

plankton tows were allowed to settle before being examined. All

phytoplankton were identified to genus level; ,1% of phyto-

plankton could not be successfully identified. Simpson’s

diversity index and the Shannon index were calculated for

each sampling trip as well as for each summer.

Hypoxia Ratio

To estimate the extent of water column hypoxia at each

sampling site on each sampling trip, we calculated a hypoxia

ratio using the following equation:

Depth of water column { depth in water where hypoxiað

beganÞ=depth of water column:

The depth in water column where hypoxia began is defined by

the depth at which DO was ,2 mg L21. Ratios closer to 0

indicate less or no hypoxia while those nearer to 1 indicate

more hypoxia.

RESULTS

A fish kill was observed on August 26, 2005 (Julian Day 238)

in LMOB. Because of its proximity to campus (,5 min), we

were able to begin sampling while the kill was progressing. The

mortality event consisted of .10,000 fish confined predomi-

nately to Lake Madeline and the channel leading to Offatt’s

Bayou; however, no dead fish were found in Offatt’s Bayou.

This kill consisted of only Brevoortia partonus (Gulf Menha-

den), primarily fingerlings, approximately 6.5 cm in length.

The fish dying in the channel were older and/or larger (, 26 cm)

than those observed in Lake Madeline and not as abundant.

Fish were not collected for laboratory examination; however, a

visual inspection of the fish in the field revealed no external

lesions. While we arrived at LMOB midmorning of the fish kill

event, it was apparent that the fish kill had proceeded for some

time. Based on our observations and in discussions with LMOB

residents, the fish kill continued well into that evening (G.T.

Rowe, TAMUG, pers. comm.).

Meteorological Data

Rainfall was greater in 2006 than 2005 (Figures 2A and B);

total rainfall for the 2005 study period was 4.34 cm, in 2006

there was three times more rain (13.5 cm). Sporadic drizzles

were common in 2005 (Figure 2A) but uncommon in 2006.

Rainfall events in 2006 generally consisted of a more

significant amount of rain (.2 cm; Figure 2B); such episodes

were not observed in 2005.

The prevailing wind direction during both summers was

from the south-southeast (162u); from the south to the north

Figure 2. Daily average precipitation (cm) for (A) 2005 and(B) 2006 and daily average wind speeds (knots) for (C) 2005 and (D) 2006; daily averages for wind

speed are indicated by the solid black line; the dashed line shows the average wind speed for the study period.



shore of the basin. The primary inlet for exchange with

Galveston Bay is on the western edge; thus the prevailing wind

direction is not likely to assist in exchange with nearby waters.

During the summer of 2005, daily averaged (July 21–August 30;

n 5 41) wind speeds ranged from 2.11 to 6.5 knots (Figure 2C).

On most days (n 5 27), wind speeds were 61.17 knots from the

average wind speed of 3.85 knots. The day of the fish kill was

preceded by several days of low wind (,3 knots). Such a

prolonged period of low average wind speeds was not observed

in 2006 (Figure 2D). Instead, daily averaged wind speeds

during the summer of 2006 (July 27–September 5; n 5 41)

ranged from 2.75 to 9.3 knots and were characteristically faster

on average, 4.92 6 1.58 knots (Figure 2D). On five occasions in

2006, wind speeds were .7 knots (Figure 2D), a daily average

wind speed not attained at all in the summer of 2005.

Physical and Chemical Parameters

Water temperature in the summer of 2005 ranged from

23.6uC to 39.9uC for the entire water column, with an average

temperature of 30.5uC 6 1.18uC (n 5 2631). The average

surface temperature (top 1 m) for the summer of 2005 was

31.5uC 6 1.14uC (n 5 302). The warmest day in 2005 was the

day of the observed fish kill, but it was not appreciably warmer

than other days at any point in the study. Water temperature

in the summer of 2006 ranged from 20.4uC to 32.3uC and had an

average temperature of 29.8uC 61.76uC (n 5 2969). The

average surface temperature (top 1 m) for the summer of

2006 was 30.5uC 6 0.69uC (n 5 369). Figures 3A and D clearly

show that water temperatures did not vary considerably from

one summer to the next.

Salinities during both summers were indicative of the

estuarine nature of LMOB. Water column salinities in 2005

ranged from 23.2 to 47.6 but did not vary substantially from the

mean of 30 6 1.61 (n 5 2631; Figure 3B). Average surface

salinity (top 1 m) in the summer of 2005 (29.2 6 1.81; n 5 302)

was close to the mean. Salinities were more variable in 2006,

with a range of 3.7 to 30.4; however, few values were less than

20. The water column average salinity for the summer of 2006

was 25.6 6 2.59 (n 5 2969) with a surface (top 1 m) average

salinity of 24.6 6 2.48 (n 5 369). Generally lower salinities in

2006 coincide with the greater rainfall that year and with wind

driven mixing events (Figure 2).

Bottom waters throughout LMOB are generally hypoxic

(Figure 3; Table 1). During the summer of 2005, DO through-

out the water column ranged from 0 to 10.6 mg L21, with an

average concentration of 2.9 6 2.36 mg L21 (n 5 2631). Surface

(top 1 m) DO concentrations remained relatively high (5.27 6

1.67 mg L21; n 5 302; Figure 3). During the summer of 2006

recorded average water column DO concentrations (Figure 3F)

were lower than those measured in 2005 (Figure 3C). The

average for the entire water column throughout the summer of

2006 was 2.32 6 2.3 mg L21 (n 5 2969), and the average surface

(top 1 m) concentrations were 3.88 6 2.24 mg L21 (n 5 369) in

2006. The basin did have a greater range of DO concentrations

during the summer of 2006, which was 0–16.5 mg L21

(Figure 3). The higher range of DO concentrations

(.10 mg L21) corresponds to the surface waters on days of

higher wind mixing.

By calculating a hypoxia ratio (Table 1), we were able to look

at trends in oxygen profiles across LMOB. In general, Stations

3 and 4, located at the opening of Offatt’s Bayou, experienced

Figure 3. DO (mg L21), temperature (uC), and salinity water column profiles for Offatt’s Bayou (top) and Lake Madeline (bottom). Black lines show the water

column measured on August 26, 2005 (the day of the fish kill), gray lines show 6 1 SD from the mean calculated from both years.



little or no hypoxia (ratio close to zero) because of tidal

exchange. In the most restricted corners of Offatt’s Bayou

(Stations 16 and 17) and in Lake Madeline (Stations 9, 10, and

11), the hypoxia ratio indicated that water column DO was low

and hypoxic conditions were present (ratio close to 1). Station

14, also known locally as the ‘‘black hole’’ for its year-round

hypoxic conditions, had hypoxic ratios between 0.43 and 0.68 in

2005 and 0.45 and 0.92 in 2006 (Table 1), which is consistent

with hypoxic water extending almost to the surface of the water

column. Hypoxia ratios for August 26, 2005, the day of the

observed fish kill, show the most restricted water column—

with hypoxia ratios for most stations higher than the sampling

effort either before or after (Table 1).

Based on water column DO profiles (Figure 3) and hypoxia

ratios (Table 1), there was greater overall bottom water

hypoxia late in the summer of 2005, which corresponded to

the shallowing of the pycnocline aligning with prolonged

periods of low wind mixing and small amounts of rainfall

(Figure 2). Conversely, during the summer of 2006, the year

without a fish kill, the water column was found to generally be

more hypoxic, with hypoxia ratios typically greater than 0.53,

especially in the more restricted parts of LMOB, and

particularly, Lake Madeline (Table 1). Because of the degree

of hypoxia below the pycnocline, the intermittent episodes of

degradation of the pycnocline from high wind forcing and

rainfall during the summer of 2006 resulted in hypoxic waters

reaching higher into the water column (Table 1).

The average surface water column temperatures, salinities,

and DO did not vary markedly from one summer to the next

(Figure 3), and the water column profiles of temperature and

DO indicate that the water column was generally well

stratified. A greater fraction of the water column was

oxygenated in 2005 than in 2006 (above 2.5 m compared with

above 1.5 m; Figure 3) in most parts of LMOB. At times of high

wind forcing and rainfall (Figure 2), the strong pycnocline was

broken in LMOB, resulting in mixing between surface and

bottom waters. This was observed in 2006 but not in 2005

(Figure 2; Table 1).

Biological Parameters

Chlorophyll a and Phaeophytin a Concentrations

Low concentrations of chl a (,15 mg L21) and phae a

(,7 mg L21) were measured in LMOB in the summer of 2006

(Figures 4B and D). This was in contrast to the very high

Table 1. Hypoxia ratio calculated for each station visited in the summers of 2005 and 2006. Numbers closer to 0 indicate less hypoxia, numbers near 1

indicate more hypoxia, dash (—) indicate stations where no data was collected for that date.

Julian

Date

21-

Jul

25-

Jul

27-

Jul

28-

Jul

31-

Jul

1-

Aug

3-

Aug

7-

Aug

10-

Aug

11-

Aug

15-

Aug

17-

Aug

19-

Aug

22-

Aug

24-

Aug

26-

Aug

30-

Aug

31-

Aug

5-

Sep

202 206 208 209 212 213 215 219 222 223 227 229 231 234 236 238 242 243 248

2005 1 0.32 0.29 0.42 0.71 0.01 0.25 0.17 0.46 —

2 0.26 0.23 0.42 0.88 0 0.17 0 0.35 0.25

3 0 0 0.33 0.13 0 — 0 0.29 0.45

4 0 0 0 0 0 0 0 0 0

5 0 0.14 0.2 0.36 0 — 0.05 0.45 0.09

6 0.29 0.39 0.09 0.26 0.2 — 0.4 0.28 0.04

7 0.19 0.29 — 0.25 0.09 0.23 0.17 — —

8 — — — — — — — 0.4 —

9 — — — — — — — — —

10 0.69 0.48 0.55 0.73 0.52 — 0.52 0.7 0.79

11 0.81 — 0.36 — 0 — 0.45 0.25 —

12 0.3 0.33 0.27 0 0.22 0.22 0.36 0.67 0.44

13 — 0.56 0.31 0.33 0.13 0.37 0.33 0.56 0.35

14 0.54 0.68 0.51 0.55 0.47 0.63 0.43 0.63 0.53

15 0.41 0.54 0.31 0.5 0.13 0.56 0.44 0.44 0.58

16 0.65 0.33 0.12 0.53 0.27 0.56 0.69 0.45 0.6

17 0.67 0.5 0.01 0.62 0.58 0.35 0 0.53 0.6

2006 1 0 0.22 0.17 0.05 0.13 0.46 0.43 0.52 0.48 0.61

2 0 0.01 0.14 0.05 0.15 0.96 0.55 0.41 0.27 0.3

3 0 0 0.89 0 0 0 0 0 0.87 0.95

4 0 0 0.88 0 0 0 0 0 0.6 0

5 0 0.09 0 0.04 0.35 0.09 0.19 0.5 0.59 0

6 0.08 0.2 0.63 0.35 0.36 0.2 0.42 0.5 0.92 —

7 0 0.36 0.68 0.24 0.2 0.28 0.46 0.54 0.92 0.08

8 — — 0.64 0.5 0.01 0 0.01 0.4 0.57 0.8

9 — — 0.7 0 0 0.01 0 0.67 0.83 0.75

10 0.44 0.58 0.94 0.48 0 0.38 0.6 0.81 0.5 0.94

11 0.5 0.59 0.24 0.29 0 0 0.62 0.6 0 0.86

12 0 0.31 0.44 0.45 0.15 0 0.56 0.54 0 0.09

13 0.07 0.31 0.89 0.44 0.2 0.23 0.5 0.48 0.23 0.5

14 — 0.45 0.92 0.49 0.46 0.63 0.68 0.7 0.92 0.92

15 0.32 0.89 0.93 0.89 0.26 0.81 0.48 0.5 0.88 0.96

16 0.01 0.06 0.81 0.82 0.53 0.82 0.71 0.81 0.81 0.81

17 0.58 0.25 0.84 0.86 0.53 0.86 0.64 0.65 0.85 0.85



concentrations of chl a and phae a (#260 and #143 mg L21,

respectively), measured in the summer of 2005 (Figures 4A

and C). The elevated chl a and phae a concentrations were

consistent with the presence of a bloom, particularly in Lake

Madeline—peaking on August 22 (Julian Day 234), four

days prior to the fish kill. The bloom had already begun to

decline by the day of the fish kill. Chl a concentrations on

August 26 (Julian Day 238) were nonetheless four times

higher in Lake Madeline (247 mg L21) than those in Offatt’s

Bayou (59 mg L21).

Phytoplankton Community Composition

Phytoplankton identification and counts were used to define

the dominant phytoplankton genera present in LMOB and also

enabled us to determine the presence or absence of potentially

harmful algae. In the summer of 2005, LMOB was dominated

by cyanobacteria (two species of Microcystis spp.), changing

toward the end of summer to a population dominated by

diatoms (primarily Coscinodiscus sp.) (Figure 5). There was a

large fluctuation in phytoplankton community composition on

August 15, 2005 (Julian day 227) corresponding to a period of

increased wind mixing and rainfall (Figure 2). Julian day 235

(August 23) corresponds to the Microcystis spp. bloom

(Figure 5). By August 26, the day of the fish kill (Julian day

238), LMOB was dominated by diatoms in surface waters, but

Microcystis spp. was still highly abundant.

Table 2 shows the Shannon and Simpson’s diversity indices

calculated for each sampling day as well as the entire summer

of 2005 and 2006. Simpson’s diversity index (supported by the

Figure 4. Daily average chl a (mg L21) (black bars) and phae a (mg L21) (white bars) concentrations for Offatt’s Bayou (A) 2005 and (B) 2006, and Lake

Madeline (C) 2005 and (D) 2006; error bars represent standard errors. (No error bars for Lake Madeline; replicates were not taken.)

Figure 5. Dominant phytoplankton taxa measured for the summer of (A)

2005 and (B) 2006. The percentage of Cyanobacteria (black), Bacillar-

iophyta (white), and Euglenophyta and Dinophyta (gray) in each plankton

tow was calculated.



Shannon index) showed a trend from a homogenous ecosystem

(in terms of phytoplankton taxa) early in the summer to one of a

more diverse heterogeneous system after the fish kill in 2005.

On August 23, four days prior to the fish kill, a low diversity of

phytoplankton was observed, consistent with dominance of

Microcystis spp. in surface plankton tows. This was also the day

the bloom peaked as indicated by the high amounts of chl a and

phae a (Figures 4A and C).

Unlike the summer of 2005, diatoms were present through-

out the summer of 2006 in large abundances (Figure 5) and in

more diverse assemblages (Table 2). The increased presence of

diatoms corresponded to periods of high wind mixing and

rainfall (Figure 2); Julian day 215 followed the period of

highest wind mixing while days 229 and 243 both follow periods

of high rainfall. The dominant cyanobacterium in 2006 was

again Microcystis spp. The dominant diatoms were Coscino-

discus sp., Chaetoceros sp.; all of which were also present in

higher abundances than in 2005 (Figure 5). Simpson’s diver-

sity index indicated that the phytoplankton assemblage

present in the summer of 2006 (Table 2) was consistently

heterogeneous, with no group dominating the system at any

time (this was supported by the Shannon index).

DISCUSSION

This study tested the hypothesis that low DO was the

primary causative factor of the fish kills occurring during the

late summer months in LMOB; given the strong water column

stratification in both summers and the greater preponderance

of hypoxia in 2006 relative to 2005 with no concurrent fish kill,

we rejected our hypothesis. Rather, we found that a complex

combination of physical, chemical, and biological parameters

led to the observed fish kill event. In particular, the declining

bloom of cyanobacteria (dominated by Microcystis spp.)

appears to have played the critical role in precipitating the

fish mortality event in an already stratified, hypoxic environ-

ment.

The most critical parameters affecting survival, movement,

and growth of fish are considered to be water temperature and

DO (Christie and Regier, 1988; Coutant, 1987). For this reason,

hypoxia is a critical parameter to consider when determining

the cause of a fish kill event. Hypoxia is a severe symptom of

eutrophication, the development of which is closely linked to

increased phytoplankton biomass in stratified estuarine

environments (Juhl and Murrell, 2005; Lee et al., 2005) as

well-established pycnoclines impede mixing and DO exchange

with overlying oxygenated waters (Paerl et al., 1998). Hypoxia

is a known culprit in many fish kills nationwide (Paerl et al.,

1998; Quigg et al., 2009; Thronson and Quigg, 2008; Wanna-

maker and Rice, 2000). While fish kills are the most visible of

the detrimental effects of hypoxia, it can have other, more

subtle, effects including reduction in growth rates of Atlantic

menhaden (McNatt and Rice, 2004) and disruption in the

ecology of affected estuaries (Diaz and Rosenberg, 1995; Eby et

al., 2005; Pihl, Baden, and Diaz, 1990).

Hypoxic bottom waters were observed during both summers

of this study. While our surveys were conducted each morning

(CST 0800–1200 hrs), based on other analogous investigations,

hypoxia persisted throughout the water column throughout the

day in LMOB, particularly at sites with restricted circulation

(Stations 16 and 17; Figure 1) and particularly in Lake

Madeline. In 2006, when no fish kill was observed, the bottom

water hypoxia was much more substantial, rising higher in the

water column (Table 1; Figure 3). Tolerances of hypoxia differ

among species and life stages of the same fish species

(Wannamaker and Rice, 2000). For example, Atlantic menha-

den (Brevoortia tyrannus) have a low sensitivity to hypoxia

having adapted to naturally reoccurring episodes over time

(McNatt and Rice, 2004). Many studies have shown that most

finfish are able to detect and avoid hypoxic conditions

(Breitburg, 1994; Renaud, 1986; Wannamaker and Rice,

2000), causing mobile fish to be restricted to oxygenated,

shallow, surface waters (Eby and Crowder, 2002). The greater

spatial extent of hypoxia during the summer of 2006, relative to

2005, allowed us to conclude that hypoxia alone was not the

primary cause of the fish kill observed in 2005. Importantly, it

did contribute by confining the fish to the narrow sanctuary of

oxygenated waters close the surface.

Increases in HABs have been related to the increasing

alterations in nutrient supplies and nutrient ratios in coastal

waters (Buskey, 1997; Nixon, 1995; Nixon et al., 2001). In the

context of this study, HABs are defined as algal blooms that

cause a variety of deleterious effects on aquatic ecosystems,

Table 2. Diversity indices for 2005 and 2006, includes Simpson’s diversity index and Shannon index for each trip and overall indices for the entire summer.

Julian Date

21-

Jul

25-

Jul

27-

Jul

28-

Jul

31-

Jul

1-

Aug

3-

Aug

7-

Aug

10-

Aug

11-

Aug

15-

Aug

17-

Aug

22-

Aug

23-

Aug

24-

Aug

26-

Aug

30-

Aug

31-

Aug

5-

Sep

Summer202 206 208 209 212 213 215 219 222 223 227 229 234 235 235 238 242 243 248

2005

Simpson’s 1.00 0.68 0.34 0.97 0.55 0.31 0.84 0.33 0.39 0.37

Shannon

(H9) 0.00 0.71 1.00 0.00 1.00 1.57 0.43 1.57 1.00 1.40

H9 max 0.00 2.19 2.57 0.69 2.49 2.49 2.64 2.89 1.95 3.26

Evenness 0.00 0.31 0.13 1.40 0.22 0.13 0.32 0.11 0.20 0.11

2006

Simpson’s 0.59 0.31 0.24 0.29 0.47 0.16 0.38 0.23 0.21 0.26 0.18

Shannon

(H9) 0.93 1.38 1.85 1.58 1.23 2.04 1.45 1.92 1.82 1.76 2.09

H9 max 2.57 2.71 2.83 3.09 2.77 2.83 2.77 2.77 2.71 3.43 3.61

Evenness 0.23 0.12 0.09 0.10 0.17 0.06 0.08 0.08 0.08 0.08 0.05



including oxygen depletion, clogging of fish gills (leading to

suffocation), and starvation, and toxin production, which can

all lead to fish kills (Graneli and Turner, 2006; Lee et al., 2005;

Smayda, 1997). Significant amounts of chl a and phae a were

observed in the days prior to the fish kill in 2005, indicating

that a bloom was in progress (Figure 4). This was associated

with several species of Microcystis spp., which we found

dominated the phytoplankton assemblage. This bloom can be

termed a harmful algal bloom according to the definition set

forth by Smaya (1997) because it was the primary casual factor

in the fish kill. Cyanobacteria have been shown to be abundant

in warm water (Murrell and Lores, 2004) and bloom in aquatic

systems where temperatures exceed 20uC (Paerl, 1996).

Because cyanobacteria have relatively slow growth rates, long

periods of physical stability are essential for the development of

a bloom (Paerl, 1996). Such conditions—low wind mixing, little

rain fall (Figure 2) and warm water temperatures (Figure 3)—

were observed during the summer of 2005 in LMOB (but not in

2006). The actual biomass of Microcystis spp. in the water may

have exceeded that reported because normalizing cyanobacte-

ria concentrations to Chl a (as was done in this study) is likely

to underestimate their actual biomass (MacIntyre et al., 2002).

The bloom was ‘‘crashing’’ on the day of the fish kill as indicated

by the falling concentrations of chl a and phae a (Figure 4) in

surface waters. Blooms have been documented as causing

mortality events upon their collapse (Lee et al., 2005). The

crashing bloom likely loaded the upper water column with

detritus given the highly stratified nature of the water column

in LMOB. Further, Microcystis spp. blooms are known to

produce toxins that cause fish kills (Tango and Butler, 2008);

however, in the context of the current study, we were not able to

measure toxin production and thus cannot comment on

whether microcystin production was also involved in the 2005

fish kill. Because toxin production cannot be ruled out as a

causal factor, it is important to note that if it was present,

microcystin could be a causal factor of such a large scale fish

kill.

Adult menhaden are filter feeders and feed primarily on

phytoplankton (Vaughan et al., 2000). The distribution of

juvenile menhaden has been correlated to the distribution of

phytoplankton (Friedland, Ahrenholz, and Guthrie, 1989).

These fish have been shown to detect and avoid hypoxic waters

(Wannamaker and Rice, 2000) and thus would have been

restricted to the narrow sanctuary available at the surface (Eby

and Crowder, 2002) where the crashing bloom was concentrat-

ed. The large amount of detritus resulting from the breakdown

of the cyanobacteria bloom likely suffocated the fish (as the

primary causal factor to the studied fish kill); this has been

documented previously in other systems (Engstrom-Ost,

Karjalainen, and Viitasalo, 2006; Ochumba, 1990).

CONCLUSIONS

This study was unique in several respects: two summers of

physical, chemical, and biological data were collected on fine

spatial and temporal scales, and the phytoplankton community

was identified to genus level revealing the identity of the

bloom-forming species. The combination of a declining Micro-

cystis spp. bloom along with strong stratification of the water

column were the two most important causal factors leading to

this fish mortality event. Extensive hypoxia, in itself, did not

directly cause the fish kill event because there existed a narrow

(,2.5 m on average) sanctuary of oxygenated water close to the

surface of LMOB. However, the extensive hypoxia reduced the

viable habitat for tens of thousands of Brevoortia patronus,

representing the most important casual factor leading to the

mortality event observed. With the increasing anthropogenic

effects on coastal ecosystems (including divergence of rivers,

dredging, and increased nutrient input to surrounding waters),

fish kills like those observed in this study will likely continue to

increase in frequency. Many studies point to hypoxia as the

primary culprit of fish kills in coastal waters (Quigg et al., 2009;

Thronson and Quigg, 2008). However, this study clearly

demonstrates that while hypoxia was present during the fish

kill, the cause was a more complex combination of physical,

chemical, and biological factors. Thus determination of the

causes of fish kills requires a more encompassing view of the

affected system.

ACKNOWLEDGMENTS

Special thanks to Derek Shultz, Federico Alvarez, Mark

London, and Amanda Thronson for helping collect the data.

My appreciation also goes to Ayal Anis (TAMUG) for the use

of his CTD. Winston Denton (TPWD) helped in the initial

setup of this project. Recognition is also due to Keith Dupuis

and Gaurav Singhal for their assistance with MatLab. My

gratitude is also given to Andrew McInnes with the TAMUG

Coastal Geology Lab for his assistance in collecting and

processing the bathymetry data for the LMOB, as well as help

with data collection in the summer of 2006. A Texas Institute

of Oceanography fellowship was awarded offering support in

the latter stages of this study and in preparing the thesis and

manuscript.

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