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NOAA Technical Report NMFS 143

Characteristics and Causes

ofTexas Marine Strandings

Edited by

Roger Zimmerman

u.s. Department ofCommerce

December 1998
u.s. DEPARTMENT

OF COMMERCE

WIUJAM M. DALEY

SECRETARY

National Oceanic and

Atmospheric Administration

D.James Baker

Under Secretary for

Oceans and Atmosphere

National Marine

Fisheries Service

Rolland A Schmitten

Assistant Administrator

for FISheries

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NOAA Technical Report NMFS 143

Characteristics and Causes

of Texas Marine Strandings

Roger Zimmerman (editor)

December 1998

U.S. Department of Commerce

Seattle, Washington
Suggested reference

Zimmerman, Roger (ed.). 1998. Characteristics and causes of Texas

marine strandings. U.S. Dep. Commer., NOAA Tech. Rep. NMFS 143,

85 p.

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CONTENTS

INTRODUCTION

P. S. BONTEMPI

C. A. N. LYONS

K. A. STEIDINGER

D. A. STOCKWELL

E. W. TRUBY

WJ. WARDLE

Q. DORTCH

F. M. VAN DOLAH

R.J. ROBICHAUX

Q. DORTCH

J. H. WRENN

W. G. DENTON

D. BUZAN

J. MAMBRETTI

K. RICE

K. QUINONEZ

WJ. WARDLE

W G. DENTON

D. E. HARPERJR.

F. M. VAN DOLAH

G.J. DOUCETTE

T. A. LEIGHFIELD

K. A. STEIDINGER

G. A. J. WORTHY

D.J. SHAVER

A. A. COLBERT

M. H. FULTON

J. LANDSBERG

J. NEWl'ON

J. CULLEN

G. I. SCOTT

A. C. CANNON

v

An assessment of oxygen, salinity, and phytoplankton distributions 1

near an area off Sabine Pass, Texas, characterized by demersal fish

and marine mammal mortalities

Phytoplankton blooms off Louisiana and Texas, May-June 1994 1~

Occurrence of Gymnodinium sanguineum in Louisiana 19

and Texas coastal waters, 1989-94

Fish kills in the northwestern Gulf of Mexico, 26 April-27 June 1994 27

An account of the 1994 phytoplankton blooms and mass 33

mortalities of marine animals along the western Louisiana and

northern Texas coast, with comparison to similar events of 1984

Assessment of the involvement of algal toxins in the 1994 41

Texas fish kills

Patterns of bottlenose dolphin, Tursiops lruncalus, strandings in Texas 47

Sea turtle strandings along the Texas coast, 1980-94 57

Ecotoxicology and histopathology conducted in response to sea 73

turtle and fish mortalities along the Texas coast: May-June ]994

Gross necropsy results ofsea turtles stranded on the upper Texas 81

and western Louisiana coasts, 1January-31 December 1994

III

INTRODUCTION _

Three major mass mortality events occurred on the

upper Texas coast during- ] 994, from January through

the second week of May. These events were distinguished

by unusually large numbers of dead dolphins, sea turtles,

and fishes washing ashore on Texas beaches. The beach

stranding of dead animals began inJanuary with bottlenose dolphins. By the end of March, 142 dolphins had

washed ashore as compared to about 40 expected. By

the latter part of April, dolphin mortalities declined

butstranding ofdead and comatose sea turtles increased.

By the end of April, at least 127 sea turtles had stranded

on the Texas coast since the beginning of the year,

about double the expected number. Then, during May

and June, a third mortality event began with a massive

fish kill and more turtle deaths. By the middle of May,

mortalities of all species as indicated by beach strandings

returned to wi thill expected levels. Nevertheless, 1994

stood out as a recOl-d year of marine mass mortalities in

the northwestern Gulf of Mexico.

Due to the magnitude and across-class nature of the

mass mortalities, and concurrent with living marine

resource responsibilities, the National Oceanographic

and Atmospheric Administration (NOAA) /National

Marine Fisheries Service (NMFS) and the State ofTexas

Parks and Wildlife Department convened a post-event

conference of experts in Galveston, Texas. The purpose of the conference was to characterize the events

and discuss probable causes of the deaths of dolphins,

sea turtles, and fishes and their association with coincident harmful algal blooms. This OAA Technical Report

details much of the information gathered hy the conference experts, based upon what was known at that time.

From the 1994 conference, Paula Bontempi and Carrie Lyons report on the offshore hydrographic and

phytoplankton transects across the Texas-Louisiana shelf

provided by the LATEX Data Office at Texas A&M

University (p. 1-12). The physical conditions leading to

the 1994 events appeared to be similar to conditions of

a June 1984 harmful algal bloom which was linked to

extensive kills of two demersal fish species, threadfin

and croaker (Harper and Guillen, 1989). Similarities

between the incidents included a high volume of freshwater runoff, strong prevailing onshore winds, stratification ofsurface and bottom waters, and hypoxia. William Wardle, Winston Denton, and Donald Harper compare physical and biological conditions between the

1984 and 1994 events (p. 33-39).

Phytoplankton blooms, low oxygen levels in bottom

waters, and fish kills were observed to coincide during

1994. Karen Steidinger, Dean Stockwell, Earnest Truby,

v

William Wardle, Quay Dortch, and Frances Van Dolah

describe sampled associations of dinoflagellate blooms

with mortality of demersal fishes (p. 13-17). Occurrence of the numerically-dominant toxic dinoflagellate

identified as G. sanguineum (=G. splendens) is elaborated

by Randy Robichaux, Quay Dortch, and John Wrenn

(p. 19-25). The extent of the May and June 1994 fish

kills are described by Winston Denton, Dave Buzan,

Jerry Mambretti, Ken Rice, and Karen Quiiionez (p.

27-31). Frances Van Dolah, Gregory Doucette, Tod

Leighfield, and Karen Steidinger report on toxicity assays of natural water samples with C. sanguinewn present

(p.41-45).

The deaths of dolphins and sea turtles began before

mortality of fishes. Graham Worthy describes the mortality event involving the bottlenose dolphin, Tursiops

lruncalus, and its association with the disease morbillivirus (p. 47-55). He emphasizes the difficulty in finding a definitive cause due to the advanced state of

decomposi tion ofthe stranded carcasses (condi tion code

4). Morbillivirus has been associated with mass deaths

of dolphins before, including the deaths of 10,000+

dolphins in the Mediterranean Sea in 1990-91. However, the offshore area in which most of the 1994 dolphin mortalities occurred also coincided with the area

in which toxic dinoflagellates were found.

Donna Shaver describes record setting sea turtle

strandings and association with the shrimp fishery (p.

57-72). A significant relationship between sea turtle

strandings and nearshore shrimping effort has continued even after the implementation of Turtle Excluder

Devices (TED's) in shrimp trawls (Caillouet et aI., 1996).

The implication is that TED's are not infallible and that

technical problems may occur even when TED's are

installed in commercial shrimp nets. During the summer of 1994, technical problems in TED's were observed and corrected thereafter by NMFS. Also, TED's

may be illegally disabled by a shrimp vessel operator

and only enhanced enforcement seems to lessen this

problem.

During April and May of 1994, six comatose sea turtles

were found stranded and all had reduced heart rates

and exhibited poor muscular control. Five of the six

turtles could not breathe on their own, so their lungs

were mechanically ventilated. Resuscitation attempts

failed and all of these turtles died wi thin 1 to 4 days.

The possibility remains that exposure to waters with

blooms of toxic dinoflagellates may have affected these

and other sea turtles and increased mortality due to

capture in shrimp trawls, even when operational TED's
were present. Ann Colbert, M. Fulton, J. Landsberg,

J. Newton,J. Cullen, and G. Scott report on analyses of

water and animal tissue samples and essentially eliminate as a causative factor man-made toxins such as

pesticides (p. 73-79). Andrea Cannon confirms that

the primary cause ofsea tUl-tle mortality was not eviden t

by gross necropsy (p. 81-85).

Harmful algae, low oxygen, and shrimp trawling are

implicated as factors, acting together or singly, that led

to the mass mortality of marine animals in waters off

the upper Texas coast and western Louisiana during

1994. The synergism among these factors and other

causes could have accounted for the higher than normal mortality rates encountered. It is also likely that

exposure to algal biotoxins and unfavorable environmental conditions made these marine animals more

susceptible to succumbing to disease and other stresses.

Five years after the record setting mass mortality even ts

of 1994, the record stills stands. Other mortality events

in the Gulf of Mexico and investigations since 1994

yil':ld some insights. In separate events during 1996,

manatee deaths in Florida and dolphin deaths in Mississippi were associated with red tide toxic algal blooms.

Also, it is now known that after the 1993 Mississippi

River flood, the summer hypoxic zone on the Louisiana

shelf, sometimes called the "Dead Zone," doubled in

area up to 7,000 square miles (Rabalais and Turner, in

press).

Nonetheless, the evidence for cause-and-effect implicating harmful algal blooms and hypoxia in the 1994

mass mortality cases remains circumstantial. Yet, the

perturbations of Mississippi River discharge, such as

over-enrichmen t of nitrates, presence oftoxic dinoflagellates, and bottom-water hypoxia (Rabalais et. aI., 1996),

continue in Louisiana and Texas shelf waters and the

risk is high that mass mortality events among the same

species will return. A follow-up conference to evaluate

the state of knowledge of mass mortality events among

marine animals in the Gulf of Mexico would be of

benefit to science and management. Better yet would

be a dedicated NOAA-funded program to develop credible information on cause-and-effect relationships leading

to mass mortalities of northwestern Gulfshelfspecies.

Literature Cited

Caillouet, C. W.,Jr., D.J Shaver, Wendy G. Teas,J M. Nance,

D. Revera, and A. Cannon.

1996. Relationship between sea turtle stranding rates and

shrimp fishing intensities in the northwestern Gulf of Mexico:

1986-1989 versus 1990-1993. Fish. Bull. 94:237-249.

1[arpcr, D., and G. Guillen.

19"9. Occurrence of a dinoflagellate bloom associated with

an influx of low salinity water at Galvcston, Texas, and

coincident mortalities of demersal fish and benthic invertebrates. Contrib. Mar. Sci. 31:]47-J61.

Rabalais,~. ~., and R. E. Turner (cds.).

In press. The effects of hypoxia on living resources. with

emphasis on the northern Gulf of Mexico. Coastal and

Estuarine Studies. Am. Ceophys. Union, Washington, D.C.

Rabalais, 1\:. N., W.J. WisemanJr., R. E. Turner, D.Justic,

B. K. Scn Gupta, and Q. Dortch.

1996. Nutrient changes in the Mississippi River and system

responses on the adjacent continental shelf. Estuaries 19:

3R6-407.

Roger Zimmerman

Galveston Laboratory

Southeast Fisheries Science Center

National Marine Fisheries Service, NOAA

4700 Avenue U

Galveston, Texas 77551
An Assessment of Oxygen, Salinity, and Phytoplankton

Distributions Near an Area off Sabine Pass, Texas, Characterized

by Demersal Fish and Marine Mammal Mortalities

PAULA S. BONTEMPI* and CARRIE A. N. LYONS

lJepartment of Oceanography

Texas A&M University

College Station, Texas 77843-3146

ABSTRACT

Three years of springtime hydrographic and phytoplankton data were collected on

transects across the Texas-Louisiana con tinental shelf from 1992-94 as part of lATEX

(Louisiana-Texas Shelf Physical Oceanography Program). Waters located offshore of the

LATEX study area, about 3 km from the Sabine River mouth, were marked by a mortality

incident involving demersal fishes, dolphins, and sea tunles in April 1994. The LATEX

transect near the affected area originates slightly southwest (16 km) from the Sabine River

mouth and follows along 94°W longitude. Possible causes of the 1994 fish kill were compared with proposed causes of a fish kill that occurred in a similar area on the TexasLouisiana shelf in 1984. Harper and Guillen (1989) speculated that the cause of theJune

1984 fish kill was linked to hydrogen sulfide production stemming from anoxic conditions.

Anoxic conditions were said to be caused by the inOux of fresh Mississippi River water and

resultant water column stability, in conjunction with the spring phytoplankton bloom and

aerobic decomposition of organic matter produced in the hloom. Dissolved oxygen and

salinity data from the first week of May 1994 did not indicate hypoxia or hydrogen sulfide

production had taken place. No unusual trends were found in hydrographic and phytoplankton data from 1994 when compared with May 1992 and May 1993 data. The

presence of toxic algal species was not detected, nor was a phytoplankton bloom identified

in 1994. During the spring of 1992, 1993, and 1994, dominant phytoplankton on the inner

shelf along 94°W longitude included chain-forming diatoms, dinoflagellates of the family

Gymnodiniaceae, and several cryptomonad species. It is unlikely that phytoplankton were

the cause of the 1994 fish kill.

Introduction

Mortality events involving several species of sea turtles,

dolphins, and demersal fishes occurred in the northwest Gulf of Mexico in late April 1994. A second mortality incident occurred during .June 1994. Both events

first appeared near Sabine Pass at the border of Texas

and Louisiana and extended west to Freeport, Texas

(Fig. 1). The first even t was marked by brown-colored

patches of water 2-3 km offshore of Sabine Pass near

Cameron, Louisiana. As increasing numbers ofdead hardhead and gafftopsail catfish (Ariusfelis and Bagre marinus,

respectively) washed up on the beaches, and sea turtle

and dolphin strandings increased in these areas, state

and federal agencies were called in to investigate.

Initial theories formulated by the National Marine

Fisheries Service and Texas Parks and Wildlife Department were similar to those stated in a study done by

Harper and Guillen (1989) regarding a fish kill that

occurred off the Texas-Louisiana coast in .J une 1984.

The 1984 fish kill not only occupied the same area, but

targeted benthic and demersal fishes and invertebrates

as during April 1994. The most supported cause of the

1984 fish kill was a bloom of the dinoflagellate

Gymnodinium splendms, which was related to increased

springtime Mississippi-Atchafalaya river runoff (Harper

* Current address: Graduate School of Oceanography, L'nivt>rsity of

Rhode Island, Narragansen Bay Campus, South Ferry Rd., l\arragansen, RJ 02882.
2 NOAA Technical Report NMFS 143

96°W

300N

28'N

26°N

94°W

'"

.!:

...J

.!:

...J

Figure I

Map of the Texas-Louisiana continental shelf with lATEX A cruise track and station locations. Station 071 location

is indicated by a star on Line 4. The May 1992 cruise included only the first four easternmost transects.

and Guillen, 1989). The 1984 bloom and low-salinity

water mass were carried to the area off Sabine Pass by

downcoast alongshore currents which prevail neal- shore

during the spring (Cochrane and Kelly, 1986). It was

speculated that Mississippi-Atchafalaya river runofflowered salinities and delivered nutrients onto the shelf,

supporting the phytoplankton bloom. As phytoplankton die and settle to the bottom, decay processes occur

as bacterial respiration takes place (Harper and Guillen,

1989), decreasing oxygen levels. Harper and Guillen

(1989) stated that oxygen depletion and stratification

resulting from freshwater flow may have facilitated the

1984 fish kill, and water column stratification was in tensified due to calm weather. The presence of hydrogen

sulfide associated with anaerobic silt in the area of the

fish kill off Galveston, Texas, may have affected demersal fish and benthic invertebrates and caused the fish

kill (Harper and Guillen, 1989).

In 1994, several possible causes for the observed fish

kill and turtle and dolphin strandings were explored,

including the 1984 hypotheses. Other potential causes

included the presence of a toxic dinoflagellate bloom,

effects of shrimp trawling, toxic wastes, pesticides associated with agricultural and river runoff, menhaden

purse seining, and the production of hydrogen sulfide

stemming from anoxic conditions (brought on by freshwater runoff, resulting water column stability, and decomposition of fluxed organic materials). While initial

sample collection and tests were being run on fish,

turtles, dolphins, and phytoplankton in the affected

area offshore from Sabine Pass, scientists working on

the LATEX program were contacted for dissolved oxygen, salinity, and phytoplankton data near the initial

mortality incident area. The purpose of this paper is to

examine theories of previous mortality events while

establishing oceanographic conditions within the vicinity of the fish kill area.

Materials and Methods

The Texas-Louisiana shelf was surveyed in late April!

early May 1994 during a spring LATEX A (Texas-Louisiana Shelf Circulation and Transport Processes Study)

hydrographic cruise at the time of the initial mortality

incident off of Sabine Pass. The spring 1994 LATEX A

cruise was the third spring cruise in a series ofseasonal

hydrographic surveys covering the shelf since 1992.
Bontempi & Lyons: Assessment of Oxygen, Salinity & Phytoplankton Distributions Near Sabine Pass, Texas 3

The L\TEX A database included three consecutive

years of hydrographic information from 1992 through

1994. The spring 1992 and 1994 hydrographic cruises

took place aboard the RjV ('Yre, and the spring 1993

cruise was aboard the RjV j. W. Powell.

The sampling grid was arranged in several cross-shelf

transects covering the area from Terrebonne Bay, Louisiana, to Brownsville, Texas (Fig. 1). The transect near

the fish kill area, Line 4, began at the] 0 m isobath

along 94°W longitude, approximately] 2 km seaward of

the fish kill. Discolored water associated with the area

of the mortality incident was found about 2-3 km offshore ofSabine Pass. The lATEX A data is from an area

near, but not within, the mortality incident area.

Twenty-eight stations were occupied on the transect

line along 94°W during each cruise (Fig. 1). At each

station, a Sea-Bird Electronics-911/J{us' CTD was used

to collect continuous profiles of temperature, conductivity, dissolved oxygen, transmissometry (SeaTech 2000

m), fluorescence (SeaTech 3000 m), optical backscatterance (D&A Instruments OBS-3), and downwelling

irradiance (Biospherical Instruments QSP-200L) with

depth. An altimeter (Datasonics PSA-900) was attached

to the CTD-Rosette (General Oceanics 12 place) frame.

Coupled with the CTD package were twelve ]O-L General Oceanics Lever Action Niskin Bottles on the Rosette. An Acoustic Doppler Current Profiler (ADCP)

recorded data continuously as well. At predetermined

stations, continuous data profiles were collected by the

CTD on the downcast, and iskin bottles were tripped

on the upcast at various depths. Discrete water samples

were drawn from the Niskin bottles to measure a host of

hydrographic parameters, including dissolved oxygen

and salinity. Levels of dissolved oxygen were determined by micro-Winkler titration (Carpenter, 1965)

and salinity determined by a Guildline Autosal onboard

the ship.

Aside from the host of hydrographic data collected

during LATEX A surveys, preserved phytoplankton

samples and net tows were collected at the same locations as hydrographic data (near the area of the initial

mortality incident). Phytoplankton data were for a

complementary program supported by the Office of

Naval Research (ONR).

During the May 1992 (92A) and May 1993 (93E)

cruises, five stations along Line 4 were chosen for microscopic enumeration and taxonomic identification

of phytoplankton. A 250 ml water sample was collected

from the surface and chlorophyll maximum at each

station. Samples were preserved in a] % glutaraldehyde

solution and stored at 5°C until enumerated according

to the Utermohl technique (Utermohl, 1958). GlutaralI Mention of trade names or commercial firms does not imply endorsement by the I\;ational Marine Fisheries Service, NOAA.

dehyde was chosen as a preservative for the phytoplankton after evaluation of the ONR study or~jectives and

consultation with Greta A. Fryxell at Texas A&M University. For the spring] 994 cruise, station 071 on Line 4

was examined (Fig. 1). This station is located about 12

km seaward from the mouth of the Sabine River. Surface and chlorophyll maximum phytoplankton samples

were enumerated, and a vertical net tow sample (27J.1nl

mesh) was examined for phytoplankton species composition. Phytoplankton were identified to species level

wherever possible, and raw count data was converted to

abundance numbers (cells·L- 1). Springtime dissolved

oxygen, salinity, current flows, ancl surface phytoplankton distributions were reviewed for anomalous e\'ents

during the April/May ]994 cruise period on Line 4 (30

April-] May), after being compared with April/May

1992 (1-3 May) and 1993 (2-3 May) Line 4 cruise data.

Results and Discussion

Circulation

The Mississippi and Atchafalaya rivers introduce large

volumes of fresh water onto the Texas-Louisiana shelf.

Combined outflow from these two rivers accounts for

up to 94% orthe fresh water flow onto the shelf (Dinnel

and Wiseman, 1986), and spring is the time of highest

river flow. All other riverine input for the Texas-Louisiana shelf (15 rivers) is significantly lower than the Mississippi-Atchafalaya river system (Nowlin~). These minor inputs are not likely to have an effect on shelf

hydrography in localized areas near the outflows, such

as the Sabine River. River discharge influences hydrographic parameters such as salinity and nutrients, and

the phytoplankton community can respond to these

hydrographic changes within the water column (Riley,

1937; Edmond et aI., 1981; Malone et aI., 1983; Fransz

and Verhagen, 19H~; Xiuren et aI., 1988; Lohrenz et aI.,

1990; Bidigare et aI., 1993; euhard, 1994; Bontempi,

1995).

A cyclonic gyre circulation pattern prevails over most

of the year on the Texas-Louisiana shelf. This pattern

occurs throughout most of the winter and spring, breaking down in the summer months due to shifts in wind

direction (Cochrane and Kelly, 1986). This circulation

pattern has been confirmed with LATEX hydrographic

data collected during seasonal cruises (Fig. 2). Ceopotential anomaly contours clearly show the general

circulation stated by Cochrane and Kelly (1986) for

each of the spring cruises, May 199~ (Fig. 2A), May

1993 (Fig. 2B), and May 1994 (Fig. 2<:). Downcoast flow

Nowlin, W. 1994. Departrnent of Oceanography, Texas .\&M

University, College Station, TX 7784')-3136.
4 NOAA Technical Report NMFS 143

Figure 2

Geopolential anomaly contours for the

(A) May 1992 (92A-3db/70db), (B) May

1993 (93E-3db/200db), and (C) May 1994

(94H-3db/200db) LATEX hydrography

cruises.
__ Bontempi & Lyons: Assessment of Oxygen, Salinity & Phytoplankton Distributions Near Sabine Pass, Texas 5

was observed on the inner shelf for all years, as was the

cyclonic gyre circulation. Downcoast flow distributes

lower salinity river water and associated (higher) nutrient levels across the Texas-Louisiana shelf.

Salinity

Figure 3A shows a vertical profile ofsalinity from spring

] 992. The freshest water (S = 26.5) was found on the

inner part of the shelf, and extended from near shore

out to the 40 m isobath (Fig. 3A). In spring 1993, the

freshest water was also found on the inner shelf within

the study area (Fig. 3B), and was even less saline than in

1992 (5 = 20.5). Low salinity waters on the inner shelf

during 1993 are most likely due to record high flows

from the Mississippi and Atchafalaya rivers for that year

(Army Corps of Engineers~) (Fig. 4). The freshwater

lens extended further seaward in May 1993 than in May

1992 as a result of the increased volume of river water

flowing onto the shelf, which was also directed westward by the down coast flow.

In the spring of 1994, the lowest salinity waters were

observed at the inner shelf again (Fig. 3C). A surface

salinity of 14.5 reflected the greater volume of fresh

water from the Mississippi and Atchafalaya rivers in the

first four months of 1994 than during previous years

(U.S. Army Corps of Engineers'l). Again, the influence

of the predominan t down coast circulation in May 1994

was reflected in the surface salinity, indicating fresh

river water located in a narrow band along the coast

(Fig. 5). Possible localized riverine influences as evidenced by low salinity waters (Sabine River), are presen t

on the innermost shelf area near the Texas coast along

94°\1\' longitude.

Dissolved Oxygen

Hypoxia can result frum a coupling of biological and

physical processes on the Texas-Louisiana continental

shelf (Rabalais et aI., 1991). Texas-Louisiana hypoxia

development is contingent upon the flow and freshwater volume of the Mississippi River, and is defined as the

presence of water having a dissolved oxygen concentration below 1.4 ml·L- 1 (Rabalais et aI., 1991). Hypoxic

conditions occur mainly in bottom waters, and are often found on the Louisiana continental shelf during

:l C.S. Army Corps of Engineers. 1993. Mississippi River flow database. '\lew Orleans District, C.S. ,\rmy Corps of Engineers, P.O.

Box 60267, 'ew Orleans, LA 70160-0267.

I \" .5. Army Corps of Engineers. 1994. Mississippi River flow database. New Orleans District, C.S. Armv Corps of Engineers, P.O.

Box 60267, ;";ew Orleans, LA 70l60-0267.

the summer and can persist through October (Rabalais

et aI., 1991). These conditions may develop in the spring,

but are generally confined to a limited area at that

time. Fresh water on the shelf is warmed by increasing

temperatures, creating a stable water column due to

density differences in the watt'r masses. Resultant stratification inhibits transport of oxygen to the lower layers

of the water column, making tht' setting prime for

hypoxic conditions to develop. Phytoplankton organic

material from the spring bloom can sink, fueling respiration processes in both the water column and benthic

environment. Respiration can utilize any available oxygen (Rabalais et aI., 199]) and cause hypoxia to occur.

Increased freshwater volume during the spring flood

coupled with spring phytoplankton hlooms can create

conditions conducive to hypoxia. However, there were

no bloom concen trations of any phytoplan kton species

detected in 1994 near the mortality area (lATEX A

station 07] ).

The highest levels of dissolved oxygen in the three

years of the study period were located on the inner

shelf of Line 4 during May] 992 (Fig. 6A). On this

transect, dissoh-ed oxygen concentrations near the coast

were 7.5 ml-L- 1, and levels c1ecreased along the bottom

of Line 4 and from the inner to middle shelf. Vertical

salinity contours indicated very little stratification on

Line 4 during May 1992 (Fig. 6A), and no evidence of

hypoxia was present on Line 4 at that time.

Dissolved oxygen values for May 1993 (Fig. 6B) were

lower overall when compared with May 1992, and the

amount of fresh water was greater during 1993. The

highest concentration of dissolved oxygen in May] 993

was 5.5 ml·L- 1, 2 ml·L- 1 lower than in May] 992. Dissolved oxygen values ranged from 5.5 ml·L- 1 at the surface to 45 ml·L- 1 ncar the bottom during May 1993.

Some stratification was present at that time, however,

no evidence of hypoxic or anoxic e\'ents was found on

Line 4 during spring 1993.

The May 1994 Line 4 rlissolvecl oxygen contoUl- (Fig.

6C) shows only the seven lATEX 1\ stations closest to

shore near the area of the mortality incident. Dissolved

oxygen concen trations at these stations wert' the lowest

of the 3 study years across the inner and middle shelf

where the freshest water resided. Dissolved oxygen values on the innermost part of the shelr during May 1994

were 3.5-4 mJ-L- 1 lower than dissolved oxygen levels in

1992 and 1993, but were not indicative of hypoxic or

anoxic bottom waters. Very weak stratification was present

in May 1994 on l.ine 4 when compared to May 1993.

The water column near Sabine Pass, Texas, was mixed

in 1992, and had less fresh water and higher dissolved

oxygen levels present. In 1994, the lowest levels of dissolved oxygen were present when the water column was

weakly stratified. No hypoxia was detected on l.ine 4 in

the three years of springtime data.
6 NOAA Technical Report NMFS 143 _

Figure 3

Salinity contours of Line 4 for the (A) May

1992, (B) May 1993, and (C) May 1994

LATEX hydrography cruises.

A

SO L..---'----'----Jl---Jl----:l

so

l---J---..l..---'----1---J

1oo

(~

E

..c

....

c.

Q)

c

B

so so 100

0 ... I f

~~ 7/

,

~.

c

40 so 100

Distance (km)
__ Bontempi & Lyons: Assessment of Oxygen, Salinity & Phytoplankton Distributions Near Sabine Pass, Texas 7

50

: , -1992

45 - - 1993

40 -1994

35

.... , ... •(/) 30 , M I •

E 25 I • 0

0

20

15

10

5

0

30 60 90 120 150 180 210 240 270 300 330 360

Julian Day

Figure 4

Mississippi-Atchafalaya river flow (1000 m1·s-l

) versus Julian Day for the

years 1992-94. The bars indicate the beginning and end of the cruise

period.

Phytoplankton

Several species of phytoplan kton are known to be toxic,

but approximately 60 species of dinoflagellates arc

known to cause red tides (Texas A&M Univ. Sea Crant,

1986). About 30 of these dinoflagellate species can

produce a toxin which could cause a major fish mortality event as occurred in ] 994. Two toxic dinoflagellates

common to Texas waters and known to cause red tides

are ('Ymnodiniw1l brevis (G. breve) and Gonyaulax monilala

(Alexandrium monilala).

Phytoplankton samples were examined from springtime 1992 to 1994 near the area of the fish kill in an

attempt to identify the presence of the aforementioned

or any toxic dinoOagellate or diatom species, any dominant or bloom concentrations of phytoplankton, and

phytoplankton species typically present during spring

near Sabine Pass. Toxic phytoplankton could be a direct cause of the mortality event, while bloom concentrations of phytoplankton were speculated by Harper

and Guillen (1989) to facilitate development of anoxic

conditions and hydrogen sulfide production. Establishing the resident phytoplankton species and their abundances in the study area during spring may dispel any

suspicion that a typically resident species may have

caused the mortality incidents. For the three study years,

phytoplankton abundances were highest within inner

Texas-Louisiana shelf waters adjacent to the coast and

river outflows. Greatest abundances were found in the

springtime due to increased river flows and associated

nutrient loads (Bontempi, 1995).

Line 4 (94°W) surface phytoplankton distributions

from May] 992 are shown in Fig. 7. Inner and middle

shelf ahundances ha\e been divided by 200 to enable a

view of offshore group distributions. In May 1992, the

abundance of phytoplankton was highest on the innn

shelf, and diatoms were dominant. Dominant diatom

species included a C>ralal.llina species, rf. bergo1lu

(pelagica), (;uinardia }laccida, and several Thalassiostra

spE'cies. Dominant dinoflagellates included species of

the family Gymnodiniaceae (the majority under 20 pm

in length) and some Prororenlrwn species. CJ)'ptomonads

composed 47% of the microflagellates. These genera

and species are common to the inner shelf on Line 4

during 1992. No known toxic algal species were prcsE'nt

in May 1992 along Line 4 (94°W).

In May 1993, the highest surface abundance of phytoplankton was found on the inner shelf (Fig. 8), as

observed in May 1992. Diatoms again composed the

majority of the phytoplankton on the inner shelf. Dominant diatoms included Shelelonema costalum and a

Thalassiosira species, and S. coslalum was thE' most dominant diatom at the innermost station along 94°W in

1993. This cosmopolitan species is found to in habit neritic waters of the world in a range of salinities and temperatures (Winsborough and Ward\ Malone et a1., 1983;

Marshall and Cohn, 1987; Xiuren et a1., 1988; Medlin et

" Winsborough, B. M., and c. H. Ward. 1979. Phytoplankton

distribution and community structure in Trinity Bay, Tt'xas. Suhmitted by Espey, Huston and Associates, Inc. Presented at Firsl

Winter ~eeting, American Society of Limnology and Oceanography. Corpus Christi, Texas.
8 NOAA Technical Report NMFS 143

30'N

29'N

28'N

27'N

Figure 5

Surface salinity contour for the May 1994 (94H) lATEX hydrography cruise. Note the location of the fresher Mississippi,

Atchafalaya, and Sabine river water along the coast.

al., 1991) and colonizes well in culture on different media

(Villac6). Colonization ofthe inner shelf area by S. rostatum

may be a consequence of increased river flow and resultant change in the shelf environment (salinity, nutrients,

etc.). In 1993, Gymnodiniaceae were the majority of the

dinoflagellates, and cryptomonads composed the majority of microflagellates, as in 1992. No known toxic algal

species were presen t on Line 4 in May 1993.

Diatoms dominated the phytoplankton population

at station 071 in May 1994 (Fig. 9). Dominant diatoms

included three species of Chaetuceroceae and S.

costatum. Again, increased freshwater volume on the

shelf probably created an environment in which a cosmupolitan diatom species, S. costaturn, could proliferate. Three species of cryprumonads composed 94% of the

microflagellates. Gymnodiniaceae and a Protoperidinium

h Villa" C. 1994. l·niversidade Federal do Rio de Janeiro, Rio de

Janeiro, Brazil. Personal commun.

species were dominant dinoflagellates. 0 toxic algae

wcre fuund to be present at the station nearest the

mortality site during May 1994.

Abundance numbers of phytoplankton were highest

on the inlier shelf along Line 4 in 1992 and 1993, and

most likely during 1994 as well. No bloom concentrations of a single phytoplanktun species were identified,

however. Cryptomonads contributed significantly to the

Line 4 inner shelf microflagellate population during

the spring period, and Gymnodiniaceae were common

dinoflagellates. No known toxic algal species of diatoms

or dinoflagellates were identified on the inner shelf

along 94°W during May 1992, ] 993, or ] 994.

Percent Transmission and Wind

Water samples examined from May ]994 were very

heavily sedimented and an 80% dilution was necessary
__ Bontempi & Lyons: Assessment of Oxygen, Salinity & Phytoplankton Distributions Near Sabine Pass, Texas 9

A

50L-.--l---'--.L-.-.L-.-..l......-.L-._'--_-'--_-'---.J

SO 100

E

...

c.

(1)

C

B

50'L---I.-----:---'---I.--5-1;0.-----I.-~---'----'----J100

40'-----L---L-----;S:l=0---...L------l.--~..J100

Distance (km)

Figure 6

Dissolved oxy~en contours (ml·L- 1

) of Line 4

for the (A) May 1992, (B) May 199:1, and (C)

May 1994 lATEX hydrography cruises.
10 NOAA Technical Report NMFS 143

LOCATION

e_lnner

/200

LOCATION

e_lnner

Line4

/200

/200

8053 /200

Line4

dJn/Mid

LINE

Dinos J

SiFlag _

!ZZZl Diatoms

~Other

_ Cocco

r:::~n: I!!R Microfla

------------~

Dinos l ~SiFlag

!ZZZl Diatoms

~Other

_ Cocco

I!!R Microtia

LINE

Plankton:

Figure 7

Phytoplankton abundance (cells-L- 1) and group distributions at the surface of the Texas-Louisiana continental shelf in May 1992. View looking from the outer shelf

towards the shore, with the inn{'r to the middl{' shelf

abundances divided by 200 to {'nable a view of outer

sh{'lf phytoplankton groups.

Figure 8

Phytoplankton abundance (cells-L-I) and group distributions at the surface of the Texas-Louisiana continental shelf in May 1993. View looking from the outer shelf

towards the shore, with the inner to the middle shelf

abundances divided by 200 to {'nable a view of outer

shelf phytoplankton groups.

Diatoms 72.55%\

Microflagellates 21.24%

Dinoflagellates 6.21 %

Figure 9

Percent composition of phytoplankton groups (diatoms, microflagellates, dinoflagellat{'s) near the mortality event at station 071 on Line 4 in May 1994.

in May 199~ and 1993, the percent transmiSSIOn was

36% and 47%, respectively. High turbidity may have

been occurring in the water column during May 1994.

Turbiditv may have resulted from mixing due to increased Mississippi River flow in 1994, and could be

refleeted in the lack of stratification on the inner shelf as

shown in the May 1994 vertical salinity contour (Fig. 3).

During the period from 4 April to 11 May 1994, mean

monthly wind directiun was from the south and southeast (Howard?). During SE-SSE winds, current flow is

down coast and surface waters move shoreward in an

Ekman layer (Howard?). There were a few very short wind

events (maximum 24 hour duration) occurring on or

around 15 April, ]8 April, 25 April, 2-3 May, and 5 May

when willds were from a north/northeasterly direction.

Conclusions

to enable identification of phytoplankton from that

cruise. Heavy sedimentation was reflected in the percent light transmission contour for Line 4 during May

1994 (Fig. 10). On the inner shelf around station 071,

light transmission was about 20%. In this area on Line 4

We have not identified a cause for marine mortality

events near the Sabine River in May and June 1994

7 lIoward, M. 1993. Department of Oceanography, Texas A&M

University, College Station, TX 77843-3146. Personal commun.
__ Bontempi & Lyons: Assessment of Oxygen, Salinity & Phytoplankton Distributions Near Sabine Pass, Texas II

O.---.~-,--rr-,--,-"---.....,,,.--------r--------r------,

40 Distan~~ (km) 100

Figure 10

Percent transmISSIon contours for Line 4 during the May 1994

(94H) lATEX hydrography cruise.

based on the LATEX A and 0 R data reported here.

However, we can conclude that in ] 994, seaward of the

fish kill area, the water column was not strongly stratified and no hypoxia, toxic phytoplankton species, or

bloom concentrations of phytoplankton were detected.

Oxygen levels were too high for hydrogen sulfide to

form in the LATEX A study area during 1994. Further

examination of data from within the actual mortality

incident area, including dissolved oxygen, phytoplankton abundance, and species composition, and wind and

current data may help identify probable causes.

Some phytoplankton may be characteristic of the

inner Texas-Louisiana shelf area, including chain-forming diatoms, LeptocJlindrus danicus and Skeletonema

costaturn, dinoflagellates of the family Gymnodiniaceae,

and several species of cryptomonads. The increased

freshwater volume in 199:) and ]994 may be identifiable by the dominance of S. costalum.

Station 07] in May 1!:l94 was about 6-7 km from the

initial mortality incident area, so data presented here

may provide some insight into features and processes

occurring on the Texas-Louisiana shelf seaward of the

10-m isobath under differen t flow re!1;imes of the Mississippi River. Studies conducted within the actual mortality incident area by the National Marine Fisheries Service and the Texas Parks and Wildlife Department may

identify a direct cause of the mortality events.

Acknowledgments _

Thanks to Ann Jochens, the LATEX Deputy Program

Manager at Texas A&M University for her initial insights on this work, and Yongxiang Li at Texas A&M

University for the dissolved oxygen, salinity, and

geopotential anomaly contours. Thank you to Denis A.

Wiesenburg and Kelly R. Thornton at the University of

Southern Mississippi's Center for larinc Sciences for

their insight, review. and editorial work; Matt Howard

at Texas A&M University for the wind information; and

to Greta A. Fryxell at Texas A&M University for her

opinions regarding the toxic phytoplankton ami reel

tide information. This work was funded by the Minerals

Management Service lATEX program (OeS contract

number 14-35-0001-30509) and the Office of Naval Research contract number NOOO] 4-93-1-05] 30.

Literature Cited

Bidigare, R. R., ~1. E. Ondrusek, andJ. M. Brooks.

1993. Influence of the Orinoco River outflow on distributions of al?;al pigments in the Caribb. Sea.J Ceophvs. Res.

9R:2259-2269.

Bontempi, P. S.

19Y5. Phytoplankton distributions and species composition

across the Texas-Louisiana continental shelf during two flow

regimes of the \1i"issippi River Master's thesis, Texas A&M

Univ., College Station.

Carpenter,J. II.

1965. The Chesapeake Bay Instiwte technique for the Winkler

titration dissolved oxy?;en method. Limnol. Oceano?;r.

10:141-143.

Cochrane,J. D., and F.J. Kelly.

1986. Low-frequency circulation on the Texas-! .ouisiana continental shelf.J. Geophys. Res. 91 (C9): 10645-10659.

Dinnel, S. P., and W. J. Wiseman.

1986. Fresh water on the Louisiana and Texas shelf. Continent. Shelf Res. 6(6):765-7H4.
12 NOAA Technical Report NMFS 143

Edmond J. M., E. A. Boyle, B. Grant, and R. F. Stallard.

J91' i. The chemical mass balance in the Amazon plume I: :he

I1lwients. Deep-Sea Res. 28A( 11) :1339-J 374.

Fransz, H. G., and]. 11. G. \'erhagen.

1985. Modelling research on the production cycle of phvtoplankton in the Southern Bight of tht, North Sea in relation to river-borne nutrient loads. :\'etherlands.J. Sea Res.

19(3/4) :24) -250.

Harper, D. E.,Jr., and G. Guillen.

1989. Occurrence of a dinoflagellate bloom associated with

an influx of low salinity water at Galveston, Texas, and

coincident mortalities of demersal fish and benthic invenebrates. Contrib. Mar. Sci. 31:147-161.

Lohrenz, S. E., M. J. Dagg. and T. E. vl,'hitledge.

1990. Enhanced primary produCl.ion at the plume/oceanic

interface of the Mississippi River. Continent. Shelf Res.

10(7):639-664.

Malone, T. C., P. G. Falkowski, T. S. Hopkins. G. T. Rowe. and

T. E. Whitledge.

1983. Mesoscale response of diatom populations to a wi ld

event in the plume of the Hudson River Deep-Sea Rt's.

30(2A):149-170.

Marshall, H. G., and .1. S. Cohn.

1.987. Phytoplankton distribution along the eastern coast of

the USA. Part V1. Shelf wat.ers between Cape f1enry and

Cape May.]. Plankt. Res. 9(1):139-149.

Merllin L. K., H.J. Elwood, S. Stickel, and M. L. Sogin.

1991. Morphological genet.ic variation within the diatom

Skdelonellta coslalu.m (Bacillariophyta): evidence for a new

species, SkeLelnnema pseudocoslalum. J. Phycol. 27:514-524.

"Ieuhard, C. A.

1994. Phytoplankton distributions across the Texas-Louisiana shelf in relation to coastal physical processes. Mast.er's

thesis, Texas A&M eniv., College Station.

Rabalais, :\. "I., R. E. Turner, W.J. Wiseman, and D. F. Boesch.

1991. A brief summary of hypoxia on t.he northern Gulf of

Mexico continental shelf: 19H5-19H8. In R. V. Tyson and T.

II. Pearson (eds.), Modern and ancient continental shelf

anoxia, p. 3!'i-47. Geol. Soc. Spec. Pub!. 51'.

Ril"y, G. A.

1937. The significance of the Mississippi River drainage for

biological conditions in the northern (;ulf of Mexico. J.

:\1ar. Res. 1(1):60-74.

Texas A&M University Sea Grant.

19H6. Red tide in Texas. An explanation of the phenomenon. T,\MC-SG-87-:i02, Texas A&M Univ. Sea Crant Coil.

Progr.. College Place.

J'termahl, II.

195H. Zur Vervollkominnung der quantitativen Phytoplankton-methodik. Mitt. In. Ver. Theor. Angew. Limnol. 9:1-38.

Xiuren, 1'\., D. Vaulot, 1.. Zhensheng and L. Zilin.

191'8. Standing stock and production of phytoplankton in

the estuary of the Changjiang (Yangtse River) and the adjacent East China Sea. Mar. Ecol. Progr. Ser. 49:141-150.
Phytoplankton Blooms off Louisiana and Texas, May-June 1994

KAREN A. STEIDINGER

Florida Department ofEnviron mmlal Prolprlion

Florida Marine ReseaTch Inslitule

100 Eighlh A VI'. SI:',

.'II. Pelnsburg, florida 3370 I

DEAN A. STOCKWELL*

The UnivPTsily of Texas Marine Science Inslitu.ll'

750 Channplview

Port Aransas, Texas 78373

EARNEST W. TRUBY

Florida Deparlmenl of f.nviTOn menial Prolalion

Florida Marine Rl'searrh Inslitule

lUO Eighlh Ave. SL

51. Pelersburg, FloTida 337Ul

WILLIAM J. WARDLE

Deparlm.ent of Marine Biology

Texas A & M UniveTsity al Galveston

P. O. Box 1675

Galveslon, Tpxas 77553

QUAY DORTCH

I"ouisiaaa UnivPTsilies Marine ConsoTlium

8124 Highway 56

Chauvin, l"ouisiana 70344

FRANCES M. VAN DOLAH

Charleston f-aboTatm)'

Nalional Marine Fisheries Servire

P.O. Box 12607

Charleslon, South Carolina 29412

ABSTRACT

Phytoplankton blooms were coincident with mass mortalities of fish and crustaceans

along the Louisiana and northeast Texas coasts in May and June 1994. Phytoplankton

communities in water samples collected from fi h kill and adjacent areas were composed of

mixed diatom, dinoflagellate, and microflagellate species common to Gulf of Mexico

coastal waters. However, two species clearly dominated; both species have pre\"iously been

associated with fish kills. HeleTosigma cf. akashiwo dominated Louisiana samples and

Gymnodinium sanguineum dominated Texas samples. Both species can be noxious and are

potentially toxic. Although the cause(s) of this marine mortality event has not been determined, one likely scenario involves the direct or indirect effects of phytoplankton blooms.

* Present address: School of Fisheries and Ocean Sciences, L;niversity of Alaska, Fairbanks, P.O. Box 757220, Fairbanks, AK Y9775.

13
14 NOAA Technical Report NMFS 143

Introduction

Unusually high mortalities of dolphins and sea turtles

occurred on the Texas coast between January and May

1994, followed by ma% mortalities uf fishes and crustaceans

along the upper Texas coast to Louisiana. Coincident with

mass mortalities in May and June, tea-colored patche~ of

water were observed near- and offshore. A phytoplankton

bloom was suspected as the cause ofsea-surtace discoloratiun as well as the mortalities of black drum, Pogur,ias

cromis, pompano, Trachinotus carolinius, blue crabs,

Callinectesspp., and bottom-dwelling fishes, including- hardhead, Anus felis, and g-afftopsail catfish, Bagre marinus.

Catfish were the most abundant dead fish stranded on

beaches and showed none uf the abrasions and marks

associated with fish that have been discarded from net

hauls; fishing activity was therefore ruled out as a cause.

Methods and Materials

Surface samples were collected 9 May and 12 May from

nearshore waters off Cameron, Louisiana (live, Lugol's

fixative, and/or glutaraldehyde); 12 May from discolored

water in Rollover Pass, Texas; 16 May (Lugol's) off Sabine

Pass and Galveston; 3June (live and Lugol's) from discolored water and clear water off Sabine Pass; and 22 June

and 24 June (live, Lugol's, and gluteraldehyde) from

discolored water, boundary water, and clear water off

Sabine Pass. Salinities of these water samples ranged from

1~-33%o; inshore samples had the lowest salinities. Standard light microscopy techniques, e.g., bright field, phase

contrast, differential interference, and epifluorescence

optics, were used to identify the dominant phytoplankton.

lumerical abundance of t.he dominant species was estimated by counting whole I-ml or O.I-ml aliquots uflive or

preserved material in duplicate, when possible. Scanning

electron microscopy techniques followed the method of

Steidinger et al. (1989), which is a simultaneous GTAOS04 at 4°C where the osmolality of the fixative and

buffer is acljusted to the osmolality of the sample. Criticalpoint-dried and coated material was observed with a Leical

Stereoscan 240 SEM.

Most of the phytoplankton taxa identified are illustrated in Steidinger and Williams (1970), Fukuyo et al.

(1990), and Steidinger (1996).

Results _

The 12 May sample collected off Cameron had a mixed

phytoplankton community characteristic of brackish or

I Mention of trade names or commf'rcial firms does not implv f'ndorsemcnt by the National Marine Fisheries Service, 0l0AA

estuarine water. One of the dominant flagellates was

Hl'lerusigrna cf. akashiwo at cell counts of x 106 L-I.

In addition to this raphidophyte, a mixed community

of diatoms, dinoflagellates, and microflagellat.es was

present. Many of the species were in the smaller size

class of <20 pm. There were small centric diatoms such

as ihalassiosim, euglenoids, chloromonads, and the

following dinoflagellates: Kalodinium glaucum,

/fpterocapsa rotundata (=Kalodinium rotundatum), H. cf.

fJJgmaea, HpterocafJsa sp., Woloszynskia spp., Scrippsifdla

sp., Oblea sp., Proloperidinium sp., ('.yrodinium spp. (heterotrophs), ('.ymnodinium spp. (heterotrophs), and a

I1('W peridinioid species. Most of the small peridinioid

cells (8 10 15 pm) appeared to be unarmored

gymnodinioid forms at the light microscope level of

resolution, but scanning electron microscopy showed

them to be either armored or of the Woloszynskia type

(sec Steidinger et al. 1996b). Many of the dinoflagellates lacked chloroplasts and were considered heterotrophic. The 12 May Rollover Pass sample was dominated by Gymnodinium sanguine1l1n (=G. splendens, G.

nelsonii) at 1.9 x 105 cells L- 1

; H. cf. akashiwowas present

butnotabulldant.

Samples collected ] 6 May off Sabine Pass and

Galveston Bay had no dominant phytoplankton bloom

organism.

Three samples collected 3 June off Sabine Pass contained Gymnodinium sanr;uineum (13 x 101 to 1.23 X 106

cells L-I ), Dinophysis caudala (5 to 8 x ]03 cells L-I ),

PrnmcPntmmcf. comfJressum, P. gracile, Katudiniumglaucum,

,\rrippsiella cf. trochoidea, hngulodinium polyedra, Gonyaulax

polygramma, Ceralium hircus, C. Jusus, Torodinium robustum,

Pseudusolenia (= Rhizosolenia) calcar-avis, Prnbo5cia

(= Hhizosolenia) alata, Rhizosolenia delicatula, Cyclotella spp.,

Thalassiosira spp., Chaetoceros spp., and other phytoplankters. Thc- sample from the discolored water had the

highest concentration of phytoplankton.

Sam plcs collected 22 June west of Sabine Pass, Texas,

were from (1) a discolored water patch, (2) at the edge

of the discolored water, and (3) in clear water. Both the

discolored and edge samples had similar species composition, but the edge sample had less dense populations. The most abundant species were ('.ymnodinium

sanguineum (5.8 x 104 to 5,5 x] 06 cells L-l), Prorocentrum

minimum (var. triangulatum) (up to 1 x 105 cells L-1 ), P.

minimum (var. minimum), P. compressum, P. rnicans,

Ceratium hircus, Scrippsiella trochoidea, Heterocapsa

rotundata, H. cf. niei, Jjngulodinium polyedTa, two

1'-'utreptiella spp. (euglenoids) (up to 4.3 x 106 cells L-I),

small peridinioid dinoflagellates (up to 5 X 105 cells L-1),

Victyocha sp. (silicoflagellate), and tin tinnids. Water

samples collected 24June contained resuspended sediments, pennate diatoms, centric diatom frustules, fecal

pellets, pollen, sand, euglenoids, dinoflagellate cysts

and cyanobacteria but no planktonic bloom.
Steidinger et al.: Phytoplankton Blooms off Louisiana and Texas, May-June 1994 15

Discussion

Louisiana Samples

Heterosigma cf. akashiwo was the dominant phytoplankter in the 12 May Cameron, Louisiana, sample. A bloom

of H. cf. akashiwo was also observed in estuarine and

coastal waters off Terrebonne Bay, Louisiana, in March

1994 (Dortch and Robichaux2). The species can be

associated with areas in which freshwater runoff is high

and levels of dissolved oxygen are low (Honjo, 1992).

In certain areas and evidently under varied environmental conditions, H. akashiwo can cause fish kills. At

certain growth phases, a Japanese isolate produces hydrogen peroxide and bioactive superoxide radicals that

can kill fish under experimental conditions (Yang et

aI., 1993). A geographic isolate of H. cf. akashiwo from

Louisiana coastal waters (or sediments) should be cultured to determine its potential toxicity to fish and to

further characterize its physiological tolerances and

requirements in relation to growth and life history.

This species produces bottom-resting stages (Tomas,

1978) that may be significant as a seed source. Resting

stages were found in a May 1994 Cameron water sample.

The Cameron sample also contained small (8 to 20

pm) dinoflagellates that were lightly armored; some of

them are new species. Scanning electron microscopy

had to be employed for the Cameron sample to rule

out the presence of the phantom-type dinoflagellate,

Pfiesteria pisricida, recently found in North Carolina and

east coast estuarine waters, that causes fish kills

(Burkholder et aI., 1992; Steidinger et a!., ] 996a). When

fish kills are associated with high concentrations of

small "gymnodinioid"-appearing dinoflagellates, particularly those <15 pm, scanning electron microscopy is the

only tool currently available for positive identification.

In the future, various molecular probes may be used to

identify harmful or toxic species biochemically, e.g.,

through cell-surface recognition with immunoassays.

Texas Samples

Samples collected in discolored-water patches offTexas

were dominated by the small- to medium-sized

unarmored dinoflagellate Gymnodinium sanguineum. This

species has previously caused discolored-surface-water

events worldwide and has even been associated with

mass marine mortalities. Most of the fish kills were

attributed to respiratory failure brought on by physical

2 Dortch, Q. (I.ouisiana Uni\"ersities Marine Consortium, 8124 Highway 56, Chauvin lA 70344), and R. J. Robichaux (Louisiana Department of Environmental Quality, Bayou Regional Office, 104

Lococo Dr., Raceland, LA 70394). Unpubl. data.

impairment of the gills or by low levels of dissolved

oxygen in the seawater that were caused by the dinoflagellate bloom. This species is thought to be nontoxic and has even been used successfully as larval fish

food (Scura and Jerde, ] 977). However, Tindall et al.

(19R4) found that extracts of a Caribbean isolate of G.

sanguineum were toxic to mice, and G. sanguineum has

been implicated in mortalities of oyster larvae and juveniles (Cardwell et aI., 1979; Bricelj et a!., 1992). Algal

extracts from water samples collected from discoloredwater patches off Texas were non-toxic when assesst'd

by mouse bioassay and cytotoxicity assays but displayed

PbTx-like activity in a receptor assay (see Van Dolah et

aI., 1998).

ProTocentrum minimum and Dinophysis caudata are recognized toxic dinoflagellate species associated with shellfish poisonings. In addition, P. minimum has been associated with fish kills off Florida's west coast, but the

cause was thought to be anoxic conditions (Smith, 1976).

Both of these species co-occurred with G. sanguineum in

some samples. Another toxic dinoflagellate, G. mikimotoi

(=G. nagasakiense, G. cf. aUTeolum), was tentatively identified in initial live samples but was not verified in

preserved samples nor in subsequent live and preserved

samples. It has been recorded from the Gulf since the

1960's (see Steidinger and Williams, 1970, vymnodinium

E) and can reach bloom concentrations.

Gymnodinium sanguineum is so variable in size and

shape that it can be difficult to irlenrify because some of

the morphs may appear to be different species. In loggrowth concentrations, G. sang'lI ineum typically has a

very characteristic shape with a dorsoventrally flattened

cell that has a broad conical or semiht'mispherical

epitheca (=epicone), a bilobed hypotheca, a median

slightly displaced cingulum, and a characteristic cytology. In bloom concentrations and in stationary growth

of cultures, G. sanguineum is extremely pleomorphic,

ranging from circular in cross section to lightly pigmented to lacking the bilobed hypotheca although there

may be an indentation (see Steidinger and Williams,

1970). It may be that some ofthese forms represen t lift'-

cycle stages or variants induced by different salinities or

by growth phase. Although the position of the nucleus

and the shape and positioning of chloroplasts call vall'

with age and environmental conditions (e.g., turbulence), they often help in identifying morphs within a

bloom. In one sample at the edge ofa bloom (22Junt'),

cells were enclosed by a prominent mucoid halo, and

again, this condition could have represented a life-cycle

stage (e.g., a resting stage). VoltoJina (1993) attributl'rl

recurring blooms of G. sanguineum in a British Columbia lagoon to overwintering cysts, or resting stages, of

an undescribed nature.

Gymnodinium sanguineum has previously bloomed

along the Texas coast under similar environmental COI1-
16 NOAA Technical Report NMFS 143

ditions. Harper and Guillen (1989) reported on a G.

sanguineum (as G. splendens) bloom inJune 1984 in lowsalinity water from Galveston, Texas, to Cameron, Louisiana. The bloom was also associated with mortalities of

fishes and crabs along that coastline. The mass mortalities were preceded by heavy runoff from the Mississippi-Atchafalaya rivers, along-shore downcurrent transport induced by winds, and the appearance of a G.

sanguineum bloom. These authors attributed the kills to

hypoxia and/or hydrogen sulfide resulting from the

bloom. Although the fish species affected in the 1984

and 1994 bloom events differed, most of them would be

susceptible to hypoxic conditions. Hypoxia along the

northern Gulf of Mexico shelf is a documented event.

Shelfwide surveys in April of 1992 and 1993 and July of

1985-1994 show that bottom water oxygen concen trations of <2 mg L-1 do not extend as far west as Calcasieu

in the spring and usually not in the summer (Rabalais

et aI., ] 991; Rabalais et aI. 3). While this argues against

annual, shelfwide hypoxia (Rabalais et aI., 1991) as a

cause, it does not rule out a small-scale hypoxic event

specifically related to the bloom. In all likelihood, the

causes of the 1984 and 1994 mass mortality even ts are

very similar. Data about the toxicity of G. sanguineum,

the distribution of oxygen during the blooms, and the

mass mortalities are insufficient to determine a cause in

either year. Because this is a recurrent phenomenon, a

plan for future response should be prepared.

Acknowledgments

We thank the following people for providing logistics

and samples: Ann Colbert, Andrea Cannon, Dickie

Rivera, and Jim Carpenter ( ational Marine Fisheries

Service); Dave Buzan and Winston Denton (Texas Parks

and Wildlife Department); and the U.S. Coast Guard.

Literature Cited

Bricelj, V. M.. S. E. Ford, F. J. Borrero, F. O. Perkins, G. Rivara,

R. E. Hillman, R. A. Elston, andJ. Chan?;.

1992. L ne"xplained mortalities of hatchery-reareo,juvenik oysters, Crassostrea virginica (Gmelin).J. Shellfish Res. 11:331-347

Burkholder,J. M., E.J. Noga, C. II. Hobbs, H. B. GlasgowJr., and

S. A. Smith.

1992. New 'phantom' dinoflagellate is the causative agent of

major estuarine fish kills. Nature 30R:407-411. Errata, '\fature 360:768.

Cardwell, R. D., S. Olsen, M. I. Carr, and E. W. Sanborn.

1979. Causes of oyste"r larvae" mortality in South Puget Sound.

" Rabalais,: '. N., R. E. Tunwr, and W.J. WisemanjJ'. 1994. Louisiana

Cniversities Marine Consortium, 8124 Highway 56. Chau\'in, LA

70344. Personal commun.

TM ERI. MESA-39, NOAA Mar. Ecosystems Analys. Progr.,

Boulder, Colo., 73 p.

Fukuvo, v., H. Takano, M. Chihara, and K. Matsuoka (eds.).

1990. Red tide organisms inJapan· An illustrated taxonomic

?;uide. Uchida Rokakuho, Tokyo, 430 p.

Harper, D. E., Jr., ano G. Guillen.

1989. Occurrence of a oinoflagellate bloom associated with

an influx of low salinity water at Galveston, Texas, and

coincident mortalities of demersal fish and benthic invertebrates. Contrib. Mar. Sci. 31: 147-161.

f1onjo, T.

1992. Harmful red tides of Helerosigma akashiwo. In R. S. Svrjcek

(ed.), Conlrol of disease in aquaculture: Proceedings of the

nineteenth U.5.;Japan meeting on aquaculture, Ise, Mil"

Prefecture, Japan, 29-30 October] 990, p. 27-32. NOAA

Te"ch. Rep. NMFS 111.

Rabalais, N. N., R. E. Turner, W.J. WisemanJr., and D. F. Boesch.

1991. A brief summary of hypoxia on the northern Gulf of

Mexico continental shelf: ]985-1988. In R. V. Tyson and T.

II. Pearson (eds.), Modern and ancient continental shelf

anoxia, p. 35-47. Geol. Soc. Spec. Publ. 58.

Scura, E. D., and C. W. Jerde.

]977. Various species of phytoplankton as food for larval

northern anchovy, ~'ngraulis mordax, and relative nutritional

value of the dinoflagellates r.ymnodinium splendens and Gonyaulax polyedra. Fish. Bull. 75:577-583.

Smith, G. B.

1976. The impact of fish-killing phytoplankton blooms upon

mideastern Gulf of Mexico reeffish communities. In H. R.

BullisJr. and A. c.Jones (eds.), Proceedin?;s: colloquium on

snapper-grouper fishery resources of the western central

Atlantic Ocean, p. IR5-]91. Florida Sea Grant College Prog.

Rep. 17.

Steidinger, K. A.

1996. Dinoflagellates. In C. Tomas (ed.), Identifying marine

diatoms and dinoflagellates, p. 387-584. Acad. Press, San

Diego.

Steidinger, K. A., and J. Williams.

1970. Dinoflagellates. Mem. Hourglass Cruises, Vol. n. 251 p.

Steidinger, K. A., C. Babcock, B. Mahmoudi, C. Tomas, and E. Truby.

1989. Consernrive taxonomic characters in toxic dinoflagellate species identification. In T. Okaichi, D. M. Anderson,

and T. N"malo (eds.), Red tides: biolo?;y, environmental

science, and toxicolo?;y, p. 285-2R8. Elsevier Sci. Publ., N.V.

Steidinger, K. A..J. M. Burkholder, H. B. Glasgow Jr., C. W. Hobbs,

J. K. Carrett, E. W. Truby, F.J. Noga, and S. A. Smith.

1996a. Pfiesleria IJiscicida gen. et sp. nov. (Pfiesteriaceae fam.

nov.), a new toxic dinofla?;ellat.e with a complex life cycle

and hehavior. J. Phycol. 32: 157-164.

St.cidinger, K. A.,J. H. Landsber?;, E. W. Truby, and B. A. Blakesley.

1996b. The use of scanning electron microscopy in identifying small "?;ymnodinioid" dinofla?;ellat.es. Nova Hedwigia

112:415-422.

Tinoall, D. R., R. W. Dickey, R. D. Carlson, and G. Morey-Gaines.

19X4. Ciguatoxigenic dinoflagellates from the Caribbean Sea,

In E. P. Regalis (eel.), Seafood toxins, p. 225-240. ACS

Symposium Ser. 262, Am. Chem. Soc., Washington, D.C.

Tomas, C. R.

197R. Olithodiscus lute-us (Chrysophyceae) [I. Formation and

sun'ival ofa benthic stage.J. Phycol. 14:3]4-3]9.

Van Dolah, F. M., G.J. Doucette, T. A. Lei?;hfield, and

K. A. Steidinger.

1998. Assessment of the involvement of the algal toxins in the

1994 Texas fish kills. In R. Zimmerman (ed.), Characteristics and causes ofTexas marine strandings, p. 41-45, NOAA

Tech. Rep. NMFS ]43.
Steidinger et al.: Phytoplankton Blooms off Louisiana and Texas, May-June 1994 17

Voltolina, D.

1993. The origin ofrecUlTent blooms of Gymnodiniumsangl.tineum

Hirasaka in a shallow coastallagoon.J. Exp. Mar. BioI. Ecol.

168:217-222.

Yang, C. Z., A. M. Yousif, T. Perkins, and L. J. Albright.

1993. The mode of action of the toxic phytoplankter,

Heterosigma akashiwo on juvenile sockeye salmon (Oncorhynchus nerka). Sixth International Conference on Toxic Marine Phytoplankton, Nantes, France, October 18-22, 1993,

p. 227 (Abst.)

Addendum

Since the submission of this manuscript, another phytoplankton bloom occurred in June 1996. A bloom

sample from the Gulf of Mexico near Sabine Pass, Texas,

had a similar Gymnodinium sanguineum bloom (1.5 x 106

cells L-1) that discolored the sea surface. An adjacent nondiscolored water area had 3 x 103 G. sanguineum cells L-I,

Occurrence of Gymnodinium sanguineum in

Louisiana and Texas Coastal Waters, 1989-94

RANDYJ. ROBICHAUX AND QUAY DORTCH*

Louisiana UniveTsities Manne ConsoTtium

8124 Hi{;hway 56

Chauvin, I,ouisiana 70344

JOHN H. WRENN

CenterfOT Excellence in Palynology

DepaTtment of Geology and Geophysics

Louisiana State University

Baton Rouge, Louisiana 70803

ABSTRACT

An area of discolored water, caused by a bloom of Gymnodinium sanguineum, and an

associated fish kill occurred on the upper Texas and western Louisiana coasts in June 1994

in the same area where a similar bloom and fish kill occurred in June 1984. Because of the

recurring association hetween blooms of C. sanguineum and fish kills, the distribution and

ecology of this dinof1a~ellate was examined. The purpose was to summarize what is now

known about this or~anism and to sug~est areas that require further research. Data collected in the Louisiana-Texas coastal zone from 1989 to 1994, both prior to and in response

to this event, indicates that G. san{;uineum was present in approximately 8% of all samples. It

is most often found in the summer at low salinities in the plumes of the Mississippi and

Atchafalaya rivers. By comparison with environmental conditions associated with G.

sanguineum elsewhere, it is hypothesized that C. sanguineum prefers stable environments

with high nutrient availability. Live samples from the bloom site, incubated for one month,

produced cyst-like structures. Their role in seeding blooms cannot be assessed until more is

known about the nature of the cysts and the overall life cycle of r;. sanguineum. Finally, the

relationship between C. sanguineum and fish kills cannot be d<:termined until the possible

toxicity of C. sanguineum is investigated.

Introduction

A series of fish kills occurred from April to June j 994

along the upper Texas and western Louisiana coasts,

sometimes associated with discolored waters (Denton

et al., 1998). Finally, in lateJune, there was an extensive

fish kill associated with "tea-colored" water. The fish

mortalities, consisting primarily of demersal finfish, were

believed to be linked to the bloom events. Steidinger et

al. (1998) identified a suite of potentially toxic phytoplankton from samples taken over the course ofthese

episodes, with the dinoflagellate Gymnodinium sanguineum, reaching bloom proportions in the "tea-colored" water in late June. Fish kills associated with algal

blooms have been observed in the past on the upper

Texas coast (Wilson and Ray, 19!'>6; Wardle et al., 1975;

Harper and Guillen, 1989), and G. sanguineum was also

associated with one ofthese events inJune 1984 (Harper

and Guillen, 19R9).

We report here on the temporal and spatial distribution of G. sanguineum, determined from sampling the

Louisiana-Texas shelf and Louisiana estuaries from] 989

to 1994. In addition, we present evidence for the formation of a possible cyst by G. sanf!:Uineum in water samples

from the bloom. Our purpose is to put the bloom and

fish kill event into a larger regional context and to

summarize what is now known about the growth habits

" Author contact [or this article.

19
20 NOAA Technical Report NMFS 143

ofthis organism.in order to hypothesize the factors that

may lead to blooms and fish kills.

Materials and Methods

Phytoplankton Surveys

Phytoplankton samples were collected and counted

during 19 shelf-wide cruises from 1989 to 1993, spanning all months except Nov.- Feb. The sampling locations are given in Fig. 1, but not all stations were sampled

on all cruises. Stations in the eastern area between the

Mississippi and Atchafalaya rivers were sampled much

more frequently than those to the west. From 1990 to

]993, a station in the coastal zone (28°52.]8'N,

900 28.94'W) was sampled at least monthly except in the

winter. Weekly sampling was conducted at three stations

in the Terrebonne Bay estuary from 1993 to the present.

After the discolored water and fish kill occurred alongshore off Sabine Pass, samples were taken from a number of other Louisiana estuaries by us and by the Louisiana Department ofWildlife and Fisheries. The purpose

was to determine the geographical distribution of the

organism and especially to determine if bloom concentrations were occurring in nearby areas.

Bloom Samples

Surface samples were collected by the Texas Parks and

Wildlife Department on 22 June 1994 from areas of

discolored water near Sabine Pass and sent to Louisiana

Universities Marine Consortium. One sample was collected for live cells and another was fixed with

gluteraldehyde. Upon arrival, live samples were placed

in an incubator on a 14/10 light/dark cycle at 28.5°C,

to provide conditions as similar as possible to those

experienced in the field. After one month of incubation, an aliquot of the live sample was preserved and

the rest was split. One half was kept in the incubator as

before; the other half was put in the dark at 22.6°C.

Fixed samples were counted as described below.

Preservation and Counting

The fixed samples were preserved and counted according to a method adapted from Murphy and Haugen

(1989) and Shapiro et al. (1989). Samples were preserved using 0.5% gluteraldehyde and kept refrigerated in the dark for at least one hour. Aliquots were

stained with 0.03% proflavine hemisulfate, filtered

through 8.um polycarbonate filters, and mounted on slides

in low fluorescence immersion oil. Phytoplankton were

then counted using an Olympus1 epifluorescence microscope with blue, green, and transmitted light.

Palynological Processing

Preserved samples, both from the initial bloom sample

and from subsequent incubations, were processed us1 Mention of trade names or commercial firms does not imply endorsement by the National Marine Fisheries Service, NOAA.

30.0

29.8

29.6

xxx • x 29.4

x •• x

x x Xx ·x X x 29.2

\ X X X

x

i x .\ 29.0 x

! x x )I(

)( x xX 28.8

J( x

I )I( x 28.6 x Absent x XX X ,. • Present x )I(~ 28.4 x x x

x x

28.2

95.5 94.5 93.5 92.5 91.5 90.5 89.5 88.5

Figure 1

Stations sampled from 1989-93 at which G. sanguineum was present or absent.
___ Robichaux et al.: Occurrence of Gymnodinium sanguineum in Louisiana & Texas Coastal Waters, 1989-94 2 I

Cysts

8/22/94

1.26 x 10 1

63 x 47

39 x 39

Cysts

7/20/94

6.50 X 10"

48 X 40

40 x 28

Cells

6/22/94

5.37 x 106

61 x 55

28 x 28

Date

Concentration (cells I-I)

Maximum size Cum)

Minimum size ().1m)

Table 1

Numbers and sizes (length x width) of vegetative cells

in original, preserved sample and cyst-like structures in

the live sample incubated in the light at 2S.5°C (22

June 1994 to 20 July 1994) and the dark at 22.6°C (20

July 1994 to 22 Septembel' 1994)

1987). One month later (Table 1), the sample in the

light contained neither vegetative cells nor cyst-like

structures. The sample in the dark at a lower temperature had cyst-like structures, but concentrations had

decreased and the morphology had changed over the

course of t.he month. Alt.hough they st.ill retained the

red accumulation body, the nucleus was no longer pronounced; they were rounder and not surrounded by an

Figure 2

Single cyst-like structure showing red accumulation body (I OOOx). Dimensions of outer structure arc 44 pm x 34 pm. Dimensions of internal

structure are 30 pm x IS pm.

Cyst Formation in the Bloom

Sample

Results

The dominant phytoplankter in the

bloom sample was identified by Steidinger et al. (1998) as C. sanguineum

(= C. splendens), which was present at

concentrations of 5.37 x 106 cells I-I.

However, morphology and cell size

(Table I) were quite variable. Only 1%

of the cells were the characteristic dorsoventrally flattened cell with a bilobed

hypo theca. The rest were round cells

lacking any indentation of the hypotheca. Nucleus position and chloroplast

arrangement were similar among the morphological

variants. Steidinger et al. (1998) made similar observations from other samples taken at the bloom site. The

difference in morphology was most evident when live

cells were observed in motion. The smaller, round cells

swam in a consistent helical path, whereas the larger,

flattened cells swam in one plane, only rotating occasionally. Other dinoflagellates were also present in the

sample, including Pmrocentrum micans (1 x 103 cells 1-1),

P. comp1'essum (8 x 103 cells 1-1), Ceratium hircus (J x 103

cells I-I), and Scrippsiella sp. (1.8 xl 05 cells I-I).

Mter one month there were no vegetative cells in the

live sample placed in an incubator in the light, but cystlike structures (Fig. 2) were present at concentrations

of 6.50 x 105 cysts \-1 (Table 1). All contained a typical

dinoflagellate nucleus and a red accumulation body,

similar to that observed in cysts of another naked dinoflagellate (Anderson et aI., 1988). The sample was

then split; one portion was incubated in the light as

before and the other was incubated in the dark at a

lower temperature. Tn general it is believed that cysts

remain dormant in the dark at temperatures below the

normal growth temperature (Pfiester and Anderson,

ing standard palynological acid digestion procedures to extract and concentrate any acid resistant, organic-walled

cysts that might be present. This consisted of treatment with cold 10% hydrochloric acid (HCl), cold concentrated hydrofluoric acid (HF, 51 %),

and hot concentrated HCI (38%). Residues were rinsed three times with distilled water after each digestion step. Permanent microscope slides were made of

the residue following each digestion and

examined with a light microscope.
22 NOAA Technical Report NMFS 143

12

14

177

9

800

42

(;. sanguineum was observed in 7.5% of 1,962 samples

taken in Luuisiana and Texas coastal waters between

1989 and ] 993. The rounded morphulogical varian t

that dominated in theJune ] 994 bloom was observed in

some of these samples, although it was usually not as

dominant as it was in the bloom. No cysts of the type

seen after the incubations were noted in these routinely collected samples, although Steidinger et al.

(199H) saw similar structures in water samples from the

bloom.

C. sanguineumoccurred more commonly in nearshore

areas, especially those directly influenced by the plumes

of the Mississippi or Atchafalaya rivers (Fig. ]). Th us, it

is more likely to be observed along the Louisiana coast

than along the Texas coast. It can occur at any time of

the year (Fig. 3), but is present most frequently in the

months ofJune through September. vVhile its apparent

absence in some months is due to a lack of sampling

(Jan. and Nov.), it is sparse in other months for which

adequate samples were collected. The sampling may

have been concentrated in areas where G. sanguineum

occurs less frequently.

Salinity measurements taken in the area of "tea-colored" water on the west Louisiana shelf in June ]994

ranged from 15 to 20%0 (Denton et aI., 1998). Phytoplankton samples taken from the Louisiana and Texas

coastal zones and Louisiana estuaries from 1989-93

show that G. sanr;uineum can tolerate salinities from 0.5

to 36%0 (Fig. 4), but is significantly more abundant at

low salinities.

Distribution of G. sanguineum Along the

Louisiana-Texas Coast 1989-93

28

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Month

Figure 3

Percer t frequency uf G sanguinr1lnl (number ufsamples with G sanguineurn/

total number of samples). Numbers above each bar indicate the number

of samples for each month.

20.,......-----------------------,

18

16

14

; 12

5- 10

e 8 u..

6

4

2

o o +---+-

At approximately the same time as the bloom off uf

Sabine Pass, high numbers of G. sanKuineum (101-105

cells/liter) were observed in routine sampling at the

lowest salinity station in the Terrebonne Bay estuary

and at a much higher salinityjust outside ofTerrebonne

Bay. Because of possible negative impacts of G

sanguineum on oysters and oyster larvae (Cardwell ct aI.,

1979; BriceU et aI., 1992), more widespread estuarine

sampling was conducted by us and by the Louisiana

Department of Wildlife and Fisheries. G. sanguineum

was observed in low numbers 002-103 cells/liter) at

62% of 16 sites sampled over the next month. Among

the sampling areas were Calcasieu Lake, Calcasieu Pass,

and a station just offshore ofCalcasieu Pass onJuly 19,

1994. Although this was one of the areas implicated

earlier as the source of the G. sanr;uineum bloom

(Buzan2) along the west Louisiana shelf, G. sanp;uineum

was present at the stations in the lake and the pass onl~'

at very low concen trations (102 cells/liter). Thus, around

the time of the bloom and fish kill along the LouisianaTexas border, the same species was widely distributed,

sometimes, but not always, at high concentrations.

2 Buzan. D. 1994. Texas Parks and Wildlife Department. 4~OO Smith

School Road, Austin, TX 78744. Personal rommun.

G. sanguineum Distribution in Louisiana Coastal

Waters at the Time of the Bloom

outer layer, and they contained one or

more round, green-fluorescing bodies.

No cysts were observed at any stage

in the palynological processing, indicating that cysts were not coated with

acid-resistan t material, such as sporopollenin. However, it was noted that G.

sanguineum vegetative cells were resistant to all acid digestion except immersion in concentrated HCI. The flagella remained attached to the theca

after digestion in cold 10% HCI. Since

the flagella is attached to the outer

membrane, that must also still be

present after cold 10% HC] treatment.

Minor degradation was noted on specimens subjected to HF digestion, mainly

a partial detachment of the transverse

flagella from the cingulum. But the

theca appeared to be in overall good

condition. Digestion in concentrated

HCl, hot or cold, resulted in destruction of almost all vegetative cells of G. sanguineum. The

rare specimens observed were nearly unrecognizable

because the overall structure was degraded.
___ Robichaux et al.: Occurrence of Gymnodinium sanguineum in Louisiana & Texas Coastal Waters, 1989-94 23

100000 • 0

• • I· E;tuarine zon1 • • • 0 I 0 Coastal Zone

10000 • a 0 L- 0 (1) CO • o. 0 ° '8 °

• 8 • ]i I------ n • 0 "''0 0 0

°

Qj 1000 • 0<9 0 0

• n 0 0°13 0 u • 0 0 o rl) 0

p • • • • • 000 0 OV ° • •• • ° 0O

0 (1) • • • • °0Q)

0 00 0 0 • 0 0 0 00 c: 100 0 0 00 0 0 0

C'll 0 00 00 '0 ° c: ° 0 Q) 0 0

:J 0

.c

« 10

o 5 10 15 20

Salinity

25 30 35 40

Figure 4

Numbers of r.. sanguineum vs. salinity from 1989-93 on the l.ouisiana-Texas shelf and in 1993-94

[rom a Louisiana estuary. Samples with no G. san,e;uineum were assi~ned a value of one so they would

appear on a semi-lo~ plot. [For all the non-zero data, the Lo~ Cell Number = -0.0291249 salinity +

3.3622; r~ =0.1109, n = 148; P-value of slope =0.0004.]

Discussion

Association of G. sanguineum with Fish Kills

Two fish kills have occurred in the same location on the

upper Texas/western Louisiana coasts, both associated

with C. sanKUineum (Harper and Guillen, 1989; this

study). Several hypotheses have been proposed to explain this association. The first su~~ests that the fish kill

was caused by low oxygen conditions, induced either by

death, sinking, and decomposition of the bloom or dil"l

vertical migration of the bloom organism and its respiration in bottom waters at night. The second hypothesis

is that G. sanguineum produces ichthyotoxins which

directly cause fish mortality. There is insufficient data

obtained during this fish kill to determine if either of

these mechanisms is the cause of the fish kill. Evidence

from the literature supports the possihility that either

or both could occur.

Mass sinking of dinoflagellates has caused hypoxic/

anoxic events and mass mortalities elsewhere including

one off the coast of Peru associated with a bloom of G.

sanKuineum (Dugdale et aI., 1977). The G. sanguineumassociated fish kill in 1984 off the Texas-Louisiana coast

was attributed to oxy~en depletion due to decomposition of the algal hloom, althou~h the evidence for low

oxygen was indirect (Harper and Guillen, 19H9).

G. sanguineum is also well known for its strong vertical

migration under some conditions (Kiefer and Lasker,

1975; Blasco, 1979; Cullen and Horrigan, 19H1), although the possibility that its respiration in bottom

waters at night could deplete the oxygen sufficiently to

cause a fish kill has never been investigated.

G. sanguinrum is not generally thou~ht of as a toxic

dinof1a~ellate, and in fact has been considered a good

food source for a variety of marine animals (e.g., Lasker

et aI., 1970; Paffenhofer, 1970, 1971; Scura and Jerde,

1977). On the other hand, there are studies indicating

it is a very poor food source, has ne~ati\'e effects for

other marine animals, or is toxic (Cardwell et aI., 1979;

Tindall et aI., 1984; Sellner and Olson, 198?i; Bricelj et

a\., 199'2; Turner e:-t aI., 1996), but no mechanism has

been determined. Samples of C. sanguineum from the:-

latest bloom and fish kill were not cytotoxic (Van

Dolah 3), but oyster samples tested with the mouse bioassay showed some toxicity (Denton et a\., 199H). Given

the widespread occurrence of this organism in coastal

areas, its use as a food source in aquaculture, and the

recurring bloom/fish kill association, further studies of

its possible toxicity are necessary.

:l Van Dolah, F. 1994. Marine Biotoxins Prugram, Charleston l.aboratory, National Marine Fisheries Service. P.O. Box 12607, Charleston, SC 294~2-2607. t'npubl. data.
24 NOAA Technical Report NMFS 143 _

Cysts and the Life Cycle of G. sanguineum

In the sample held for a month in the incubator in the

light, structures similar to typical dinoflagellate cysts

formed. None of the other dinoflagellate species present

at the time the sample was put in the incubator would

have formed a cyst of that size or structure. It is, of

course, possible that some other species bloomed and

formed cysts during the month when the sample was

not examined. However, cyst formation by this species

had been hypothesized previously. Voltolina (1993)

demonstrated that sediment samples, taken from a lagoon on the west coast ofCanada with recurring blooms

of G. sanguineum, led to growth of vegetative cells. Despite a failure to isolate cysts, it was concluded that the

blooms recurred because of reseeding from cyst beds.

Moreover, Steidinger et al. (1998) described a similar

cyst-like body in samples collected at the edge of the

discolored water from the June 1994 bloom along the

Louisiana-Texas coast. Thus, it seems likely that the

observed structure was a cyst, although it's unclear what

type of cyst. The red accumulation body is typical of a

dinoflagellate hypnozygote. On the other hand, its rapid

disappearance from the incubated sample, even in the

dark at lower temperatures, argues that it is a temporary cyst.

The vegetative cells were surprisingly resistant to

chemical degradation, much more so than the cyst-like

structures. Since vegetative dinoflagellate cells are not

usually subjected to standard palynological treatments,

there is no way to know if this resistance is unusual.

Further, it is difficult to extrapolate from resistance to

chemicals in the lab to resistance to decomposition in

the natural environment.

The G. sanguineum observed in this bloom has a

number of characteristics which suggest that life cycle

studies would be useful for understanding its distrihution. The vegetative cell can occur in distinctly different

morphological forms and is chemically quite resistant.

It forms at least one type of cyst, which does not appear

to be very persisten t. Cysts or vegetative cells in sediments could provide the seed population for recurring

blooms, but a better understanding of the life cycle is

necessary before this hypothesis can be evaluated.

Predicting Blooms of G. sanguineum

G. sanguineum is often associated with water discoloration events and may be considered a Harmful Algal

Bloom (HAB) species due to its association with mortality events. Blooms of many HAB species are thought to

be increasing in coastal areas, perhaps as a result of

increasing coastal eutrophication. Consequently, there

is considerable interest in understanding the environmental conditions which lead to blooms, in order to

predict their occurrence (WHOI, 1995).

In the northern Gulf of Mexico, G. sanguineum occurs primarily at low salinities near shore during the

summer. Association with the Mississippi and Atchafalaya

River plumes, which have much higher nutrient loads

than other freshwater sources entering the Gulf (Turner

and Rabalais, 1991; Rabalais, 1992) suggests that it may

not specifically be the low salinity conditions, but perhaps the higher nutrient availability, that is stimulating

G. sanguineum growth. This is supported by evidence

that G. sanguineum blooms in high salinity upwelling

areas, such as the coasts of Peru and California (Blasco,

]975). It also blooms aperiodically in the highly

eutrophic Chesapeake Bay during the summer

(Bockstahler and Coats, 1993). It appears to prefer

periods of higher water stability and/or reduced wind

stress, even in upwelling areas (Keifer and Lasker, ] 975;

Rojas de Mendiola, 1979; Robinson and Brown, 1983;

this study). further studies are needed to determine if

its growth is stimulated by high nutrient availability. If

that is the cause, blooms of this species are likely to

increase simultaneously with coastal eutrophication.

Conclusions _

G. sunguineum is a HAB species which is sometimes

associated with fish kills, may produce cysts, and may be

stimulated to grow when nutrient availability is high.

Further study of its life cycle, possible toxicity, and

nutrient requirements are necessary in order to predict

hlooms and their possible consequences.

Acknowledgments _

This research was funded by 1 OAA Coastal Ocean Program Office, Nutrient Enhanced Coastal Ocean Productivity (NECOP) grant no. A90AA-D-SG691 to the

Louisiana Sea Grant College Program (award no.

MAR02 and MAR92-02 to Quay Dortch); Department

of Interior Minerals Management Service Mississippi

River Plume Hydrographic Study, contract no. 14-35-

0001-:W63~ to Louisiana State University (subcontract

no. R158977 to LUMCO ); and Louisiana Board of

Regents grant no. LASER 86-LUM (1)-083-13. We thank

the Texas Parks and Wildlife Department and the Louisiana Department of Wildlife and Fisheries for sampling and data during and after the current bloom, N.

N. Rabalais and 1'. M. Soniat for help with the coastal

and estuarine surveys, and Rhonda Schaubhut, Dana

Milsted, and Suzan Pool for technical assistance.
___ Robichaux et al.: Occurrence of Gymnodinium sanguineum in Louisiana & Texas Coastal Waters, 1989-94 25

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Fish Kills in the Northwestern

Gulf of Mexico, 26 April-27 June 1994

DAVE BUZAN, WlNSTON G. DENTON,

JERRY MAMBRETTI, KE RICE, and KAREN QUINONEZ

Tpxas Parhs and Wildlife Department

4200 Smith School Road

Austin, 'Texas 78744

ABSTRACT

Two fish kills during May and June 1991 occurred in nearshore waters of the northwestern Gulf of Mexico from Freeport, Texas, east to Cameron, l.ouisiana. The number of fish

killed exceecled 1,400,000. The causes of the fish mortality were never conclusively determined. Investigations during the inciclents suggested that causes of the mortalities may have

included a toxic algal bloom, low dissolved oxygen, and commt'rcial fishing.

Biologists for the Texas Parks and '''''ildlift' Department accessed aerial surveys, field

observations, water chemistry analysis, laboratory toxicity bioassays, biological samples,

histopathological and parasitological analysis, and biotoxin tissut' testing to determint' the

cause of the fish die-offs. Aerial surveys located patches of dis,olored water where freshwater

enters the nearshore Gulf of Mexico. NUITlnous dead fish were floating in and ncar the

discolored water. Elevated dissolved oxygen and chlorophyll concentrations in areas of

discolored water were consistent with phytoplan kton bloom conditions. Biotoxin analysis of

oysters collectt'd from the Sabine Pass jetties indicated the presence of an unidentified

toxin in oyster tissut's. Histopathological and parasitological analyses were negative. Toxic

substances were not detected in water.

Introduction

Texas Parks and Wildlife Department (TPV\'D) biologists investigate as many as 200 fish kills each year.

Historically, low dissolved oxygen has caused the most

fish kills, statewide. The largest kills in recent years have

occurred in Texas coastal waters, resulting from rapiel

onset of extreme low temperatures and from toxic dinoflagellate blooms. Rapid drops in water temperatures to near freezing occurred three times, from 1983

to ] 990, and resulted in die-offs of o\'er 28 million fish. I

A massive bloom of Gymnodinium bTevis from Gah'eston,

Texas, to the Rio Grande killeel over 22 million fish in

bays and the Gulf of Mexico, from August 19H6 through

January] 987 (Trebatoski, ] 988).

I Mambrelli ..J. TPV\ll, 4200 Smith School Road..\ustin. TX 78741.

Unpubl. data.

During ]976, a fish kill involving more than 10 million fish was reported frorn the same area (TNRCC:!).

The 1\:176 kill was reportedly caused by a red tide. A fish

kill in Gulf waters between Galveston anc! Freeport,

Texas during the spring and summer of J984 was attributed to hypoxia and possihle elevated hydrogen sulfide

which may have been caused by a massive bloom of

Gymnodinium splendens (Harper and Guillen, J9H9).

Seventeen fish kills have occurred along the uppn

Texas Gulf coast since 1970 (T;-..JRCC:!). Fourteen of

these were between Galveston Beach, Calveston County,

and Sea Rim State Park beach in Jefferson County.

Sixteen of the] 7 documented kills occurrcel ouring

summer. Seven kills were attributed to mortality of the

TNRCC. 1994. Fi;h kill repon database retrie\ al. Texa, :'-lallil al

Resource Conservation COll1mi,sion. P.O. Box l'lOH7.•\lIslin. TX

78711-3087.
28 NOAA Technical Report NMFS 143

bycatch from commercial fishing for shrimp and menhaden. Other causes of fish mortality included red tide

(2 incidents) and spawning stress (1 incident). Causes

for seven of the fish kills were not iden tified.

Federal, state, and local environmental investigat.ors

rarely have resources needed to adequately investigate

Gulf fish kills. Consequently very limited data are available from the majority of these kills. Many of the kills

are suspected to have result.ed from commercial fishing

for shrimp and menhaden which t.akes place during

much of the spring and summer along the north Texas

Gulf coast. Commercial fishing certainly has the capabilit.y to result in the accidental deaths oflarge numbers

offish. On 5 September ]994,1.4 million menhaden

and over 300 adult red drum washed ashore dead when

the contents of a menhaden purse seine were lost just

off t.he Gulf beach east. of Galveston.

The first of the two fish kills reported in t.his document began in lat.e April and early May] 994 and the

second began during lat.e June ]994. The first event

included an estimated 650,000 fish, mostly hardhead

catfish, Ariusfelis, and gafftopsail cat.fish, Bagre marinus.

Sea turtle and bottlenose dolphin mortalities were elevated above normal during the same time and in the

same locations as t.he dead fish.

The second event, which began during the last half

of June ]994, killed over 800,000 of mostly bottomfeeding sciaenids. Estimates of dead fish during these

incidents did not include fish that. washed ashore on

Louisiana beaches. Dolphin and sea turtle mortalities

were not as high in theJune fish kill as during the May

fish kill. Visual observations and personal communications with Stat.e of Louisiana regulatory personnel suggested t.hat unusually large numbers of dead fish were

observed along western Louisiana's beaches during both

the May andJune incidents.

TPWD biologist.s invest.igated bot.h kills to iden tify

t.he cause(s) of mortality. Despite t.hose efforts, insufficient. data were collected for TPWD biologists t.o identify conclusively t.he cause(s) of the kills. Evidence suggest.s the most likely cause (s) was either t.oxicity from a

toxic algal bloom, low dissolved oxygen, commercial

fishing, or a combination of these.

Materials and Methods

May 1994

On 9 May ]994 Texas Natural Resource Conservation

Commission (TNRCC) and TPyVD personnel measured

water quality and collected Gulfwater samples approximately 1.6 km east of the Sea Rim Stat.e Park beach for

chemical and phytoplankton analysis. One set ofsamples

was collected and measurements were made in a patch

of discolored wat.er about 75 m long and 300 m wide.

Ot.her patches of discolored water were observed nearby.

Dead fish were observed float.ing in the discolored wat.er.

A second set ofsamples was collected and measurements

were made nearby but out.side the area of visibly discolored wat.er. Water depth was 2.4 m at. bot.h sites. Vertical

profiles ofwater physicochemist.ry were made in situ with a

multiparameter meter. Water samples were collected at

depths of 0.3 m below the sUlface and approximately 0.3

m above the bottom. Wat.er samples for chemical analysis

were collected, preserved, and analyzed according to standard procedures (TNRCC2). Analyses for heavy metals

and volatile organics were conducted at the Texas Depart.-

ment of Health (TDH) Environmental Chemist.ry Lab in

Austin. Analyses for nutrients, chlorophyll, salts, and total

and volat.ile suspended solids were conducted at the

TNRCC laboratory in Houst.on. Beached dead fish were

not. extensively counted during t.he first incident.

June 1994

Dead fish were counted by TPWD biologist.s on 23, 26,

and 27June 1994 on the Gulfbeach. Counts were made

according to the American Fisheries Society Special

Publication Number 24, "lnvest.igation and Valuation

of Fish Kills" (American Fisheries Society, 1992). Dead

organisms were counted in six linear t.ransects, totaling

320 m, along the beach from High Island east. t.o Sea

Rim State Park, a distance of 48 km.

Water quality testing for salinity and dissolved oxygen was conducted by TPWD biologist.s at. several sites

in the Gulf of Mexico in the area between Galveston

and Sabine Pass. The measurements were taken both at

the surface and near the bottom at each site.

Three oyster, (;rassostrea sp., t.issue samples were collectee! by TPWD biologist.s on 28 June 1994 from inside

Sabine Pass at the Sabine Pilot. station. Oyster tissues

were analyzed by mouse bioassay following American

Public Health Association procedures for biotoxin at

the TDH laboratory in Aust.in. 3

Results

May 1994 Fish Kill

On 2 May 1994, TPWD received citizen reports of dead

hard head catfish along the Gulf beach on Galvest.on

Islane!. Similar report.s and observations continued

through the first week in May. On 7 May 1994, extremely large numbers of dead hardhead catfish washed

:1 Ordner, M. 1994. Texas Department of Health, 1100 W. 49th

Street, Austin, TX 787,,6. Personal commun.
___________ Denton et aJ.: Fish Kills in the Northwestern Gulf of Mexico, 26 April-27 June 1994 29

ashore at TPWD's Sea Rim State Park in Jefferson

County. TPWD and U.S. Coast Guard staff conducted

an aerial survey on 8 May 1994 which revealed approximately 36 kilometers ofTexas beach lined with dead fish

and several sea turtles. The aerial survey revealed an area

of reddish discolored water offshore of Sabine Pass between Louisiana and Texas. Similar areas of discolored

water were observed offshore of Rollover Pass in Texas

and Cameron Pass in Louisiana. These areas of discolored

water were also observed during aerial surveys conducted

by TPWD personnel on 9,11, and 12 May 1994. A TPWD

biologist counted 574 hardhead catfish, 16 Gulf menhaden, Brevoortia patronus, and 7 Atlantic croaker,

Micropogonias undulatus, on an area of beach at Sea Rim

State Park, 7.6 m by 7.6 m, on 8 May 1994. AnotherTPWD

biologist observed over 200 dead hardhead catfish on the

Gulf beach near the mouth of the San Bernard River on

the same date. TPWD staff seined in the surf at Sea Rim

State Park during the morning of 9 May 1994, and collected relatively high numbers of apparently healthy hardhead catfish. One seine haul captured 125 fish.

In excess of 650,000 fish were estimated to have

washed ashore on Texas' Gulf beach from Galveston

Island east to Sabine Pass during the first two weeks in

May 1994. The total area affected included the Gulf

beach from the mouth of the San Bernard River in

Brazoria County, Texas, east to Sabine Pass, Jefferson

County, Texas, a distance of nearly 190 km. Estimates

of dead fish included only the fish reponed from the

Gulf beach from Galveston east to Sabine Pass. The

greatest concentrations of dead fish, equaling 75 dead

fish/linear meter of beach, were found from Sea Rim

State Park east to Sabine Pass. The majority ofdead fish on

Sea Rim State Park beaches washed ashore on 7 May 1994.

Hardhead catfish comprised the majori ty of the dead

fish. Hardheads ranged in size from 15 to 41 cm and

some were identified as gravid females. Dead Atlantic

croakers were juveniles ranging from 10 to 15 cm. Gulf

menhaden that were killed were primarily adults.

Water Quality

Dissolved oxygen in the discolored water ranged from

12.5 to 12.8 mg/l, top to bottom. In nearby waters that

were not discolored, dissolved oxygen was 8.0-8.4 mg/

I. The discolored water also had a pH of 8.4 compared

to an average 8.0 in nearby water of normal appearance. Salinity was 16%0 at both sampling locations.

Chlorophyll concentration from a depth of 0.3 m in the

discolored water was 61 ,ug/1. 4 Analyses for volatile or4 Graham, W. 1994. Texas Natural Resource Conservation Commission. 3870 Eastex Freeway, Suite 110, Beaumont, TX 77703. Personal commun.

ganic compounds and heavy metals in water samples

from near the surface and bottom did not reveal elevated concentrations.

TPWD personnel conducted routine fish monitoring

in Gulf waters near Sabine Pass on I R April (8 sites), 4

May (3 sites), and 5 May (5 sites) 1994. Salinities at

trawl sites during trawling ranged from 10-21 %0. Dissolved oxygen concentrations near the bottom at trawl

sites were 6.4-8.4 mg/1. Live, healthy fish were captured in all 16 trawls.

Bacteria, Virus, and Parasite Analysis

Three specimens each of moribund and healthy hardhead catfish, collected from Sea Rim State Park Gulf

beaches by TPvVD person nel on 8 and 9 May 1994, were

analyzed at the Texas Agricultural Extension Service Fish

Disease Laboratory for bacterial, viral, and parasitic infections.5 All direct stains ofinternal tissues for bacteria were

negative and no apparent lesions of microbial nature were

observed. Parasitic lesions were absent and no important

parasites were seen. Gills were reported reacting in a

manner consistent with bacterial challenge. Internal tissues did not show evidence of bacterial challenge.

Laboratory Toxicity

Some of the water samples collected on 9 May 1994 (at

1640 hrs) by TNRCC and TPWD personnel from an

area of discolored water off Sea Rim State Park beaches

were analyzed for toxicity by the U.S. Environmental

Protection Agency laboratory in Houston. They were

analyzed using the nine-day chronic laboratory bioassay

for sheepshead minnow, Cyprinodon variqia1us, eggs and

larvae. 6 The samples were collected 0.3 m below the

surface and 0.3 m from the bottom. When compared to

the control, the samples showed no significant effect.

June 1994 Fish Kill

An aerial survey conducted on 10June 1994 by TPWD

personnel revealed discolored waters in the Gulf near

Sabine Pass and Cameron Pass. Each area was estimated to exceed two square kilometers. On ~1 June

1994, the park manager reported large numbers of

dead fish on the beach west of Sea Rim State Park.

5 Johnson, K. 1994. Texas Agricultural F,xtension Service Fish Disease I.ahoratory, Texas A&M University, College Station, TX 77843.

Personal commun.

6 Hollister, T. 1994. C.S. Environmental Protection Agency, 1062;)

Fallstone Road, Houston, TX 77099. Personal commun.
30 NOAA Technical Report NMFS 143

TPWD conducted an aerial survey on 22June 1994 and

reported the areas of discolored water again near the

mouths of Sabine and Cameron passes. Thousands of

floating dead fish were observed during the 22 June

aerial survey in nearshore Gulfwaters between Sea Rim

State Park and High Island. TPWD personnel trawled

the bottom for 10 minutes in an area of discolored

water near Sabine Pass on 1RJune 1994 but did not

capture any apparently stressed or dead fish.

A total of 5,485 dead fish and crabs, representing 16

species, were counted in transects along the beach from

High Island east to Sea Rim State Park. Counts of dead

animals were expanded to an estimate of over R20,000

dead fish and crabs on the beach.

The majority, over 96%, of fish were Atlantic croaker,

silver perch, Bairdiella chrysOUTa, and star drum, Stelhfer

lanceolatus, ranging in size from 8 to 13 cm total length.

Two percent of the dead fish were Atlantic spadefish,

Chaetodipterusfaber, with total lengths also measuring R-13

em. Atlantic bumper, Chloroscombrus chrysurus, bighead

searobin, Prionotus tribulus, striped mullet, Mugil rephalus,

inland silverside, Menidia berylina, Gulf menhaden, hardhead catfish, shrimp eel, Ophichthussp., blue crab, Callinectes

spp., purse crab, Persephona sp., spider crab, Libinia sp.,

spotted seatrout, Cynoscion nelJ'Ulosus, and sand trout,

C;ynoscion arenarius, were also found dead on the beach.

Water Quality

Limited water quality t.ests were conducted by TPv\'D

biologists in one area of discolored water near Sabine

Pass on 22June 1994 (Mambretti, personal commun.).

Measurement.s were made at 1200 hI'S in water 4.0 m

deep. Salinity was 1~%o at the surface; 15%0 at the

bottom. Dissolved oxygen was 15.4 mg/I at the surface;

9.2 mg/I near the bottom.

TPWD personnel conducted routine fish monitoring

in Gulfwaters near Sabine Pass on ]4June (8 sites), IH

June (5 sites), and 20 June (3 sites) ]994. Salinities 2t

trawl sites were 7-21 %0. Dissolved oxygen concentrations near bottom ranged from 2.6 t.o R.H mg/I. Live

healthy fish were captured in all 16 trawls.

TPv\'D personnel also conducted routine water chemistry testing on 25 and 28June 1994 in the Gulf of Mexico in

the area between Galveston and Sabine Pass. At 17 sites,

salinity ranged from 30 to 42%0 and dissolved oxygen

concentrations in bottom waters was 0.2-9.3 rng/I. Dissolved m..)'gen levels were 1.0 mg/I or less at 8 of the sites.

Toxicity

Oyster tissues collected from Sabine Pass near the Sabine

Pilot Station did indicate the presence of a toxin; hoY'"

ever, the results were near the sensitivity limitations for

the test procedure. The results for the three samples

ranged from less than 8.7 Mouse Units to less than 13

Mouse Units.

Discussion

Two major fish die-offs occurred during 1994 along

Gulf of Mexico beaches from Freeport to Sabine Pass,

Texas. The first incident occurred during the first two

weeks of May and the second during the third week of

June. The estimated total number of dead fish on the

beaches during both incidents was over 1,400,000. During May, over 90% of the dead fish were hardhead

catfish. During the June inciden t, over 96% of the dead

fish were the sciaenids, Atlantic croaker, star drum, and

silver perch. Algal blooms, giving the water a reddish

brown color, were observed near the passes from bays

into the Gulf during both incidents.

TPWD field personnel made a large number of field

observations and participated in several sampling efforts during May and June associated with the two fish

kills. Negative results from the Fish Disease Laboratory

for analysis of samples for bacteria, virus, and parasite

infections suggest the May fish kill was not caused by a

Widespread bacterial, viral, or parasitic disease. Laborat.ory bioassays and chemical analysis of Gulf wat.ers during the May incident failed to show either acute or

chronic toxicity or the presence of heavy metals or

man-made compounds in potentially toxic concentrations. Limited dissolved oxygen measurements prior to

anrl during the May and June kills failed to reveal low

levels of dissolved oxygen that would be lethal to fish.

There was, however, no sampling of dissolved oxygen

concentrations in the vicinities of the dead fish during

early morning hours, when oxygen concentrations would

be expected to occur at minimal levels.

Commercial fishing for menhaden and shrimp was

observed during the May kill while commercial fishing

for mt'nharlen was observed during the June incident.

Purse seining for menhaden and trawling for shrimp

are known to result in the capture and subsequent

mortality of nontarget species. Anecdotal information

from beach users and TPWD biologists during the May

incident suggested shrimping activity may have been

conducted closer to the beach than in previous years.

Observations of intensive shrimp trawling, combined

with the awareness that mortality of nontarget species

can result from trawling, suggest some of the dead fish

observerl during May 1994 resulted from commercial

fishing.

It is unlikdy commercial fishing contributed to observed mort.ality during the June 1994 incident. The

relatively small size of the fish observed would have
____________ Denton et al.: Fish Kills in the Northwestern Gulf of Mexico, 26 April-27 June 1994 31

allowed them to be harvested with any menhaden if

they had been caught in a purse seine. The commercial

shrimping season was closed during June 1994, making

it. unlikely that shrimping was responsible for fish mort.alit.ies during t.hat. incident.

Oyster t.issues containing toxin were collected from

the Sabine Pass area which experienced an algal bloom

obser-ved several t.imes from the air during May and

June. These data suggest a t.oxic algal bloom may have

been present in Sabine Pass for some period preceding

2RJune 1994.

Acknowledgments _

The following individuals provided information and/

or support for TPWD's response to the May and June

1994 fish kills: Wade Graham of the TNRCC Beaumon t

provided water chemistry sampling during the May incident; staff of the TPWD's Sea Rim State Park provided

notification of incidents, access to sampling sites, and

sample transport to the Extension Fish Disease Laboratory; Terry Hollister, U.S. Environmental Protection

Agency Laboratory in Houston, provided laboratory

bioassay analysis of May water samples; Ken Johnson,

Texas Agricultural Ext.ension Service at College Station, provided analysis of fish for parasites, bacteria,

and viruses; TPWD coastal fisheries biologists from Port.

Art.hur and Seabrook provided fish community data,

water chemist.ry data, and aerial observations of impacted waters; Roy Lehman at Texas A&M University at

Corpus Christi and Dean Stockwell at the University of

Texas at Austin Marine Science Institut.e provided rapid

analysis of plankton samples from bloom zones.

Literature Cited

American Fisheries Societv.

1992. Sourcebook for Investigation and Valuation of Fish

Kills. American Fisheries Society Spec. Pub!. 24 (supp!.),

151 p.

Ilarper, D., and C. Guillen.

1989. Occurrence of a dinoflagellate bloom associated with

an influx of low salinity water at Galveston, Texas, and

coincident mortalities of demersal fish and benthic invertebrates. Contrib. Mar. Sci. 31:147-161.

Trebatoski, B.

19R8. Observations on the 19H6-1987 Texas red tide Plyrfwdiscus brevis. Tex. Water Comm. Rep. 88-02, 48 p.

An Account of the 1994 Phytoplankton Blooms and Mass

Mortalities of Marine Animals along the Western Louisiana and

Northern Texas Coast, with Comparison to Similar Events of 1984

WILLIAM]. WARDLE

Department ofMarine Biology

Texas A&M University at Galveston

5700 Avenue U

Galveston, Texas 77551

WINSTON G. DENTON

Texas Parks and Wildlife Department

P. O. Box 8

Seabrook, Texas 77568

DONALD E. HARPERJR.

Department of Marine Biology

Texas A&M University at Galveston

5700 Avenue U

Galveston, Texas 77551

ABSTRACT

Early summer phytoplankton blooms preceded mass mortalities of primarily demersal

fishes and crustaceans from Calcasieu Pass, Louisiana, to the vicinity of Galveston, Texas, in

1984 and again in 1994. The 19R4 event occurred in June and was evenly distributed along

the affected coastline. The bloom was dominated by the dinoflagellate Gymnodinium

sanguineum Hirasaka, not previously known to cause mortality. There ensued a late June

mass mortality of demersal fishes and crustaceans, principally Atlantic threadfin, Polydactylus

octonemus. The 1994 events featured separate phytoplankton blooms that developed adjacent to the estuarine passes. The dominant species of phytoplankton differed among the

blooms and did not include toxic species previously known to cause mass mortality. Two

temporally separate mass mortalities occurred: An early May mortality, principally affecting

hardhead catfish, Ariusfelis, and a late June mortality principally affecting Atlantic croaker,

Micropogonias undulatus. Due to the lack of highly toxic, mass mortality-producing phytoplankters, it seems unlikely that dinoflagellate toxins caused the mortalities in either year.

The demersal nature of nearly all fishes and crustaceans involved in both years suggests that

low dissolved oxygen levels in bottom waters might be a possible cause. Comparison is made

between the 1984 and j 994 events and a phenomenon known as a 'Jubilee." Additional

possible causes or contributing factors, such as commercial by-catch, disease, pollution, and

underwater explosions, are also considered.

Review of the Mass Mortality Event of 1984 __

Phytoplankton Bloom

Harper and Guillen (1989) reported the occurrence of

a brown-colored phytoplankton bloom that appeared

along the western Louisiana and upper Texas coast in

June 1984. The bloom was initially observed from the

Galveston beachfront on 10 June. An aerial survey on

19June revealed patches of discolored water extendin~

southwestward from Calcasieu Pass to the southwestern

end of Galveston Island. These extended seaward to a

33
34 NOAA Technical Report NMFS 143

distance of ] 0 km (Fig. 1) and persisted for two weeks

until disappearing on 27 June.

During the early stages of the bloom, Harper and

Guillen (1989) reported coastal salinities as low as 9

ppt. They indicated that this condition resulted from

high spring discharge from the mouths of the Mississippi and Atchafalaya Rivers, which lie to the northe2st,

associated with westerly coastal currents and southeasterly (onshore) wind patterns. They detected hypo:,ic

«~ ppm) water masses at depths below 5 m off

Galveston. In addition, they observed a layer of black,

hydrogen sulfide-laden, anaerobic silt covering the sediment surface just prior to the disappearance of the

bloom. This layer extended seaward to a distance of200

m. Samples of the discolored water were provided to L.

A. Loeblich who identified the dominant phytoplankter as the dinoflagellate l.ymnodinium splendens Lebaur,

presently known as l.ymnodinium sanguineum Hirasaka.

Louisiana

Gulf of Mexico

Texas

.......... :...

", '.":

. 0:' '.'

50 km

---------- .::".::::-:-:-.:--

Figure I

Distribution of phytoplankton blooms along the western Louisiana and northern Texas coast in June 1984 (stippled area)

and as initially observed in May 1994 (dashed areas). Br = Brazos River, Bo =Bolivar Roads, R = Rollover Pass, S =Sabine

Pass, C = Calcasieu Pass.
__ Wardle et aI.: 1994 Phytoplankton Blooms & Mass Mortalities of Marine Animals along the W. Louisiana & N. Texas Coast 35

Mass Mortality

On 23 June, Harper and Guillen (1989) recorded a

mass mortality of predominantly demersal fishes and

crustaceans 13 days after the bloom was first observed.

Dead organisms occurred along the entire bloom-affected shoreline (Fig. 2) and continued to accumulate

on shore for five days. The mortality ceased with the

disappearance of the discolored water. The Atlantic

threadfin, Polydactylus octonemus, accounted for 80% of

the estimated thirteen million individuals killed. The

remainder consisted of several other species of primarily demersal fishes and crabs.

An Account of the 1994 Phytoplankton

Bloom and Mass Mortality _

Bloom Development and Composition

The] 994 bloom was observed on 1 May and consisted

of successive bands (0.4 hectare) of reddish-colored

water parallel to the shoreline. Plumes consisting of

many bands extended in an easterly direction from the

mouths of CaJcasieu, Sabine, and Rollover passes (Fig.

1). Within a few days, the plumes expanded to a distance of 3.2 km from shore and began to extend southward from the mouths of the passes, then eventually

southwestward. Blooms persisted in the CaJcasieu and

Sabine Pass areas until late June but the bloom in the

Rollover Pass area disappeared by the end of May.

Uncharacteristically low coastal salinity readings of less

than 20 ppt were recorded. Daytime dissolved oxygen (DO)

readings varied considerably but low readings (2.8 and 4.1

ppm) were recorded off the Sabine Passjetties on 1July.

Samples of discolored water were obtained from the

separate blooms at CaJcasieu, Sabine, and Rollover

passes. Light and electron microscopic examination

(Steidinger et al., 1998) revealed that blooms at Sabine

and Rollover passes were dominated by the dinoflagellate

Gymnodinium sanguineum Hirasaka. Also present were the

dinoflagellate Prorocenl'rum minimum, the raphidophyte

Heterosigma sp., euglenophytes, and silicoflagellates. The

bloom at Calcasieu Pass, however, was quite different in its

composition, being dominated by Heterosigma sp., with

lesser concentrations of other dinoflagellates, diatoms,

cryptomonads, and prymnesiophytes.

Gymnodinium sanguineum, a well-known cosmopolitan species, is not known to be toxic. Although some

species of Prorocentrum are known to cause paralytic

shellfish poisoning, P. minimum has no history of toxicity. P. minimum has been recorded in bloom proportions in large areas of Mississippi Sound and adjacent

waters (Perry and McClelland, 1981) with no attendant

mortality of marine organisms. Heterosigma akashiwo

(Hada) is reported to produce red tides in the western

Pacific which are toxic to juvenile salmon (Yamochi,

1983). There are no previous records ofmortality caused

by any species of Hfteros(f!;ma in the Gulf of Mexico.

Furthermore, Heterosigma sp. was detected in significant

numbers only in the Calcasieu Pass area bloom in ]994

and was not recorded in 1984.

Mass Mortality of Demersal Fishes and Crustaceans

Two separate mass mortalities of predominantly demersal fishes and crustaceans occulTed in conjunction

with the 1994 blooms. The events were temporally separate and spatially different (Fig. 2).

The first mortality became evident on 2 May, one day

after discolored waters were initially observed at the

mouths of the passes. Dead fishes and crustaceans were

found floating in coastal waters and accumulating on

the shore from Cakasieu Pass to Bolivar Roads (Fig. 2).

The event resulted in deaths of an estimated 630,000

catfishes, predominantly hardhead catfish, Ariusfelis, with

a small but not-precisely-determined number ofgafftopsail

catfish, Bagle marinus, as well. ]n addition, approximately

19,000Atlan tic croaker, Micropogonias undulatus, and lesser

numbers of other demersal fishes and crustaceans perished (Table 1). An estimated 650,000 organisms succumbed over two weeks, ending on 15 May.

The second mass mortality occurred over an 8-day

period, 22-30 June 1994. Demersal fishes and crustaceans accumulated on the shoreline from Sabine Pass

eastward, a distance of 45 km (Fig. 2). This event resulted in the deaths of an estimated 800,000 individuals

but, unlike the first mortality, Atlantic croaker was the

dominant species affected. Other species occurring in

the second event were similar in type to those observed

in the first, except that catfishes were not observed.

Comparison of the 1984 and 1994 Events __

Abiotic Conditions

Currents in the 1984 bloom area moved westward along

the coast, bringing low salinity water from Louisiana

(Harper and Guillen, 1989). ]1'1 ]994, the sources of

low-salinity water appear to have been local passes

(Calcasieu, Sabine, and Rollover). This is supported by

the following: (1) Plumes of discolored water (Fig. 1)

appeared at the mouths of the passes and were initially

observed extending seaward in an easterly direction

and (2) the phytoplankton blooms in ] 994 differed in

species composition from pass to pass, suggesting that

each of the three blooms was nurtured individually by

local waters from an adjacent pass. In 1984, by contrast,
36 NOAA Technical Report NMFS 143

Louisiana

Texas

50km

Gulf of Mexico

Figure 2

Distribution of mass mortalities of fishes and crabs along the western Louisiana and northern Texas coast in 1984 and

1994. The dominant organisms for each mortality are shown from left to right: Polydactyl-us octonernus, Ariusfelis, Micropogonias

undulatus. Br = Brazos River, Bo =Bolivar Roads, R = Rollover Pass, S =Sabine Pass, C =Calcasieu Pass.

blooms were apparently nurtured by a single westwardflowing water mass.

Low salinity coastal water (less than 20 ppt), probably

resulting from recent freshwater runoff, was recorded

during the 1984 and 1994 events. Normally, salinities

along the northern Texas coast exceed 20 ppt during

the months of May, June, and July (Pullen et aI., 1971;

Harper and Wardle, 1972-present, personal observ.).

Southeasterly (onshore) wind patterns prevailed during May and June 1994 (personal observ., present investigators). These may have served to hold low salinity

water masses close to shore, as in 1984 (Harper and

Guillen, 1989).

Low dissolved oxygen (DO) readings «2 ppm) were

recorded in association with the bloom in 1984. In

1994, somewhat low DO readings of 2.8 and 4.1 ppm

were recorded. Although these are not hypoxic levels,

they are surprisingly low considering that they were

taken during daytime in bloom areas of presumably

intense photosynthetic activity and oxygen production.
__ Wardle et al.: 1994 Phytoplankton Blooms & Mass Mortalities of Marine Animals along the W. Louisiana & N. Texas Coast 37

Table 1

Composition and estimated magnitude of mass mortalities of fishes and crustaceans on the western Louisiana and

northern Texas coast in 1994.

26 April-15 May 1994

Ariusfelis

Ba!fl'e marinus

Micropogonias undulalus

BTevoO,.tia patronus

Sciaenops ocellala

Pogonias cromis

Ophichthus gomesii

Callinectes spp.

Total = 656,220

Percent

85

5

3

<1

<I

<I

<l

<l

100

22-30June 1994

Mirropogonias undulatus

Slellifer lanceolalus

BaiTdielia chrysum

Chaetodipterus fabe,.

La,.imus fasciatus

PTionolus lTibulus

Cynoscion a,.enmius

Anusfelis

Mugil cephalus

Echiophis sf!.

Callinecles spp.

Libinia sf!.

Penef!hona sp.

Total = 827,130

Percent

90

4

2

2

<l

<1

<I

<1

<I

<l

<1

<l

<l

100

Hydrogen sulfide accumulation on bottom sediments

was detected in 1984. No comparable sediment sampling was performed in 1994.

Bloom Development and Composition

The phytoplankton blooms of 1984 and 1991 were similar in regard to their seasonal timing and general location. They differed, however, as to uniformity and pattern (Fig. 1). The bands of discolored water in the 1984

bloom were distributed uniformly along the shoreline

from Calcasieu Pass to the southwestern end of

Galveston. The 1994 event, however, featured several

isolated blooms that remained in the vicinity of the

estuarine passes throughout their duration. In 1984,

the single bloom lasted only 17 days. The 1994 blooms

persisted for about 60 days in the vicinity of Calcasieu

and Sabine passes.

The] 984 bloom was dominated by a single species,

the dinoflagellate Gymnodinium sanguineum. G.

sanguineum was also a key species in the 1994 event in

blooms at Sabine and Rollover passes. At Calcasieu

Pass, however, the dominant species was the raphidophyte Heterosigma sp.

Mass Mortality of Demersal

Fishes and Crustaceans

The mass mortalities of 1984 and 1994 were similar in that

both involved primarily demersal fishes and crustaceans.

In 1984 only a single mass mortality event was recorded,

while in 1994 there were two temporally separate and

spatially different mass mortalities. The chief victims of

the 1984 mortality were Atlantic threadfin while the primary victims of the first and second] 994 mortalities were

hardhead catfish and Atlantic croaker, respectively.

An estimated 13 million fishes and crustaceans were

killed in 1984 whereas total deaths in 1994 were only

one-tenth that number. The Atlantic threadfin that perished in the 1984 mortality were far smaller in body size

than the hardhead catfish and Atlantic croaker killed in

the 1994 mortalities, thus the total biomass that perished

in 1984 may be comparable to that killed in 1994.

Discussion

Harper and Guillen (1989) concluded that hypoxia or

hydrogen sulfide poisoning, rather than dinoflagellate

toxins, were the most likely causes of the 1984 mortalities. They noted that the dominant phytoplankter had

not been previously associated with mass mortalities,

and that the list of species killed included primarily

demersal types. A broader spectrum of species would

be expected to be killed by a less selective red tide toxin

such as the "brevetoxin" produced by the c1inoflagellate

(>ymnodinium breve (Davis). This toxin has a history of

causing periodic mass-mortalities of fishes along the

Texas coast (Wilson, 1956; Texas A&M Univ. Sea Grant,

1987).

The 1984 and 1994 events are similar in having occurred in the same geographic area at more or less the

same time of the year. They are also comparable in

having been associated with low salinity and, possibly,

low DO levels. The occurrence of phytoplankton blooms

followed hy mass mortality of predominantly demersal
38 NOAA Technical Report NMFS 143

fishes and crustaceans is also similar. The two events

differ, however, as to the apparent sources of the low

salinity waters in which blooms developed. They differ

also in patterns of bloom distribution, taxonomic composition of the bloom organisms, and bloom duration.

The numbers and types of demersal nekton affected

during the two events were also quite different.

The saxitoxin-producing dinoflagellate Alexandrium

monilatum (Howell) (formerly Gonyaulax monilata

Howell) is known to have caused blooms along the

Galveston coast in previous years. Those were followed

by mass mortalities of demersal fishes and macr'Jinvertebrates (Wardle et a!., ] 975). Although the 1984

and] 994 bloom waters were not tested for the presence

of saxitoxin, it is unlikely that saxitoxin was a factor

because Alexandrium monilatum cells were not recorded

in plankton samples taken during either event. Other

dinoflagellates were found (as summarized in Steidinger

et a!., 1998), however, none, including Gymnodinium

sanguineum which was prominent in both the] 984 and

1994 even ts, is known to have sufficien t t.oxin-produ:-

ing capability t.o have caused such mortality.

The 1984 and 1994 events along the Louisiana-Texas

coast. share some characteristics with a previously-reported northern Gulf of Mexico inshore phenomenon

known as a 'Jubilee." Loesch (] 960) and Gunter and

Lyles (1979) observed t.hatjubilees involve concentrations of live demersal fishes and crustaceans in shallow

estuarine waters. These concentrat.ions are due to the

presence of hypoxic condit.ions in adjacent. deeper waters where t.hese animals normally reside. The hypoxia

results either from high biological oxygen demand generated by decomposing organic mat.ter, or from nighttime respiration of phytoplankton in bloom areas.Jubilees may be associated wit.h blooms of non-toxic dinoflagellat.es and characterist.ically occur in waters of

less than 20 ppt salinity. Hypoxic conditions associated

wit.h jubilees are often alleviated before mass mort.alities occur. Otherjubilees are more prolonged, causing

mass mortalities of fishes and crustaceans; some jubilees occasionally cause deaths of pelagic forms, i.e.

menhaden, Brevoortia patronus.

The events of] 984 and] 994 along the west.ern Louisiana and nort.hern Texas coast cannot be regarded as

jubilees in the classic sense for they did not occur ill

inshore waters and were of much larger scale in area,

duration, and magnitude of mortality. The 1984 and

] 994 events do, however, share some characteristics

wit.h jubilees, i.e. t.he dominant phytoplankton bloom

species were non-t.oxic. The species affected in 1984

and 1994 are comparable to those affected by jubilees.

In addit.ion, low salinity wat.er «20 ppt) was associat.ed

wit.h t.he 1984 and 1994 events, also charact.eristic of

jubilees. Finally, relatively low dissolved oxygen levels

were observed during both events. The few sporadic

readings t.aken in 1994, however, did not adequately

demonstrate widespread hypoxia.

Ot.her causes for the 1984 and 1994 mass mortalities

must, therefore, be considered. For instance, were mort.alities caused by larger scale seasonal hypoxic event.s in

offshore bottom water? Renaud (1986) and Rabalais et

a!. (1994) have reported such events in th is area. Another possible cause or contributing factor is fishing

industry by-catch. Mortalit.y of nontarget demersal nekton species by commercial fisherrr:en commonly occurs

each year in t.he affected area (Caillouet. et a!., 1991).

The resulting patterns of deposit.ion of organisms on

t.he shore, however, are usually much more intermitt.ent and of far less magnitude than those observed in

the] 9H4 and 1994 mortalities.

Toxicity due to indust.rial pollutants normally would

be expected to affect both pelagic and demersal species. The possibility of the presence of bottom-dist.ributed toxic substances of industrial origin in one or both

mortality years cannot, however, be discounted.

Yfortalit.y due to disease normally would be expected

t.o be confined to a single species or to a few closely

related species. One of the authors (Denton) observed

a mass mortality of catfishes, Arius felis and Bagre marina, along the northern Texas coast in August 1995.

The mort.alit.y occurred over a period in late summer

during which no phytoplankt.on blooms were observed.

This suggests t.he possibility that. disease migh t have played

a significant role, not only in the] 995 mortality, but in t.he

first (May) mass mortality of catfishes in 1994.

An thropogenic underwater explosions associated with

the offshore activities of oil and gas industries are also

common in this area. Such activit.y can result in fish

mortality and could be a possible contributing factor.

The primary cause(s) of t.he 1984 and 1994 mass

mortalities along the western Louisiana and northern

Texas coast.s thus remains essent.ially unknown at this

time. It. is hoped that this document.at.ion and comparison of t.hese events in t.he present report will be useful

in comparisons with similar events occurring in this

area in the future.

Literature Cited

CaillouE't, C, w"Jf., M. J. Duronslet, A. M. Landry Jr., D. B. Rivera,

D. J. ShavE'r, K. M. Stanley, R. W. Heinly, and E. K. Stabenau.

1991. Sea turtle strandingsand shrimp fishing effort in the northwestern Gulf of Mexico, 19H6-1989. Fish. Bull. 89:712-718.

Gunter, G., and C. H. Lyles.

1979. l.ocalized plankton blooms and jubilees on the Gulf

coast. Gulf Research Rep. 6:297-299.

Harper, D. E.,Jr., and G. Guillen.

1Y8Y. Occurrence of a dinoflagellate bloom associated with

an influx of low salinity water at Galveston, Texas, and

coincident mortalities of demersal fish and benthic invertebrates. Contrib. Mar. Sci. 31:147-161.
___ Wardle et aI.: 1994 Phytoplankton Blooms & Mass Mortalities of Marine Animals along the W. Louisiana & N. Texas Coast 39

Loesch, H.

1960. Sporadic mass shoreward migrations of demersal fish and

crustaceans in Mobile Bay, Alabama. Ecology 41:292-29H.

Perry, H. M., and]. A. McClelland.

1981. First recorded observance of the dinoflagellate

Prorocentrum minimum (Pavillard) Schiller, 1933 in Mississippi Sound and adjacent waters. Gulf Res. Rep. 7:83-85.

Pullen, E.]., W. L. Trent, and G. B. Adams.

1971. A hydrographic survey of the Galveston Bay System,

Texas, 1963-1966. NOAA Tech. Rep. NMFS SSRF-639, 13 p.

Rabalais, N. N., W.]. Wiseman Jr., and R. E. Turner.

1994. Comparison of continuous records of near-bottom dissolved oxygen from the hypoxia zone along the Louisiana

coast. Estuaries 17:850-861.

Renaud, M. L.

1986. Hypoxia in Louisiana coastal waters during 1983: implications for fisheries. Fish. Bull. 84:19-26.

Steidinger, K. A., D. A. Stockwell, E. W. Truby, W.]. Wardle,

Q. Dortch, and F. Van Dolah.

1998. Phytoplankton blooms off Louisiana and Texas, MayJune 1994. In R. Zimmerman (ed.), Characteristics and

causes of Texas marine strandings, p. 13-17. NOAA Tech.

Rep. NMFS 143.

Texas A&M Univ. Sea Grant.

1987. Red tide in Texas: an explanation of the phenomenon.

Texas A&M Univ. Sea Grant Progr., Pub\. 87-502,4 p.

Wardle, W.]., S. M. Ray, and A. S. Aldrich.

1975. Mortality of marine organisms associated with offshore

summer blooms of the toxic dinollagellate Gonyaulax monila/a

Howell at Galveston, Texas. In V. R. LoCicero (ed.), Proceedings ofthe First International Conference on Toxic Dinollagellate Blooms, p. 257-263. Mass. Science Techno!. Fow1d., Wakefield.

Wilson, W. B.

1956. The occurrence of Gymnodinium brevis in the western

Gulf of Mexico. Ecology 37:388.

Yamochi, S.

1983. Mechanisms for outbreak of Heterosigma ahashiwo red

tide in Osaka Bay,Japan. Part I. Nutrient factors involved in

controlling the growth of Helerosigma akashiwo I-1ada. ].

Oceanogr. Soc.Japan 39:310-316.

Assessment of the Involvement of Algal Toxins

in the 1994 Texas Fish Kills

FRANCES M. VAN DOLAH

GREGORY]. DOUCETTE

TOD A. LETGHFIELD

Charleston Laboratory * Southeast Fisheril's Science Center

National Marine fIsheries Seroice

2/9Fort Johnson Road

Charleston, South Camlina 29412

KAREN A. STEIDINGER

Florida MarinI' ReseaTCh Institute

Florida Department off:nvironmental Protection

100 Eighth St. SE

St. Petersburg, Florida 3370/

ABSTRACT

Water samples collected from discolored patches east of Galveston, Texas, during MayJuly 1994 were examined for the presence of toxic algae and algal toxins. The dominant

algal species varied between water samples, with the presence of Gymnodinium sanguineum

being the only common denominator. Methanol extracts were analyzed for toxicity by

mouse bioassay and by in vitm cytotoxicity, and further characterized for diarrhetic shellfish

toxins (OSP) and brevetoxin-like activity using pharmacologic assays. one of the algal

samples were toxic by mouse bioassay or cytotoxicity assay. Oysters collected from Sabine

Pass during an intense bloom of Gymnodinium sanguineum and analyzed for in vitro cytotoxicity were also negative. No OSP toxins were found. However, all algal and oyster samples

displayed some activity in a receptor binding assay for brevctoxin-like compounds, which

was not observed in negative controls. Results of toxicity assays are discussed relative to the

algal species present.

Introduction

During April and May J994 large numbers of demersal

gafftopsail, Bagre marinus, and hardhead, Arius felis,

catfishes washed ashore along the upper Texas coast.

The onset of catfish mortalities generally coincided

with an increase in the numbers of dolphin and sea

turtle strandings along the Texas coast. The occurrences offish kills similarly coincided with the presence

of extensive and patchy areas of "coffee-colored" water

located from the shoreline to approximately ten miles

offshore. Blooms of dinoflagellates cause discoloration

of water, resulting in red to brown patches of the nature observed here. Furthermore, a number of dinoflagellate species have been implicated in fish kills

(Anderson, 1994) and marine mammal mortalities (Geraci

et a!., ] 989). Depending on the algal species presen t, fish

kills may result from anoxic conditions, physical damage to gills, or production of specific neurotoxins. This

report summarizes the results of assays for algal toxins

which were performed on water samples collected from

within and outside of discolored patches during May

and June, and on oysters collected in the presence of an

intense algal bloom in Sabine Pass duringJune.

* Laboratory name is now "Center for Coastal Environmental Jlealth

and Biomedical Research, National Ocean Service."

41
42 NOAA Technical Report NMFS 143

Methods _

Water Sample Collection

Water samples (8 L) were collected via Coast Guard

helicopter from coffee-colored patches approximately

1 mile offshore from Sabine Pass and Rollover Pass on

12 May 1994. Subsamples were fixed in Lugol's iodine

for species identification. The remainder ofthe sample

was stored at room temperature for 48 hours before

analysis in the laboratory. Similarly colored water

samples collected on 3 June offshore from Sabine Pass

and on 5July from the Galveston ship channel by Texas

Parks and Wildlife (Winston Denton) were shipped to

Charleston Laboratory for analysis.

Water Fractionation

Water samples were filtered through 250 pm and 20 pm

Nitex1 plankton screens. The fraction retained by the

20 pm filter (containing most phytoplankton) was sonicated in 10 ml methanol for 2 minutes, followed by

centrifugation to remove particulate debris. The methanol was then evaporated to dryness and the sample

dissolved in 100pl fresh methanol for analysis.

Oyster Samples

Oyster extracts were obtained from the Texas Public

Health Department (Mike Ordner). These samples were

extracted using the American Public Health Association (APHA) standard method (Greenberg and Hunt,

1984) and provided in cottonseed oil. An additional

sample of oysters collected from Sabine Pass on 5 July

was extracted in our laboratory using the APHA protocol. In the presence of 5 g NaCI and 1 ml concentrated

HCI, 100 g shellfish homogenate was boiled, followed

by extraction with 400 ml ethyl ether. The ether phase

was evaporated to dryness, and the residue brought up

in 9 ml methanol for analysis. Control oysters collected

in Charleston, S.c., were analyzed in parallel.

Mouse Bioassay

Methanol extract (50 pI) was diluted to 5 ml with 0.9%

saline containing 1% Tween 80. Two-fold serial dilutions were then made and 0.5 ml injections were administered intraperitoneally into female ICR strain mice

(Harlan Sprague Dawley, Inc., Indianapolis, Ind.) weighI Mention of trade names or commercial firms does not imply endorsement by the National Marine Fisheries Service, NOAA.

ing approximately 20 g. Four dilutions were tested, with

four mice injected at each dilution. Results are expressed as (+) or (-) based on mouse symptomology

(incoordination, hind limb paralysis), indicative of

neurointoxication.

Cytotoxicity

General cytotoxicity was determined by the method of

Van Dolah and Ramsdell (1996). GH4Cj rat pituitary

cells were plated in 0.1 ml Hams FI0+ medium in 96-

well plates at a concentration of 0.5 x 106 celis/mi.

Sample extracts were then serially diluted, added to

triplicate wells, and incubated 18 hours at 37°C. For

determination of viability, 15 pI of the tetrazolium dye,

3-( 4,5-dimethylthiazol-2-yl) -2,5-diphenyl tetrazolium

bromide (MTT, 5 mg/ml in PBS), was added and the

cells were incubated for 4 hours at 37°C. The cells were

then solubilized by addition of 10% sodium dodecyl

sulfate (SDS) in 0.1 HCI and absorbance at 570 nm

determined using a 96-well plate reader.

Brevetoxin (PbTx) Receptor Binding Assay

[3H]PbTx binding competition assays were carried out

in 96-well polystyrene plates by the method of Van

Dolah et al. (1994). For generation of PbTx-3 competition curves, 140 pi rat brain synaptosome preparation

(l mg/ml protein) were incubated in the presence of

35 pi [3H] PbTx-3 (5 nM; Chiral Corp., Miami, Fla.)

and increasing concentrations of un labeled PbTx-3 (10-6

to 10- 11 M) in the presence of 50 mM HEPES buffer

(pH 7.4), 130 mM choline chloride, 5.5 mM glucose,

0.8 mM MgS04, 5.4 mM KCI, 1 mg/mlbovine serum

albumin (BSA) , and 0.01 % Emulphor-EL 620. For analysis of algal extracts, 5 pi extract was diluted with 30 pi

sample buffer and added in place of the PbTx-3 standard. The mixture was then incubated at 4°C for 1 hour,

followed by filtration onto a 96-place filter mat and addition ofsolid scintillant. The 96-place filter mat was counted

directly in a microplate scintillation counter.

Phosphatase Inhibition Assay

The presence of okadaic acid-like compounds was assessed by the ability of algal extracts to inhibit protein

phosphatase activity in vitro (Ingebritsen et aI., 1983),

where the activity of protein phosphatase 2a was measured by its ability to release 32p from a 32P-labeled

substrate phosphorylase a. Protein phosphatase 2a (Upstate Biotechnology, Saranac, N .Y.) was incubated in

the absence of or presence of algal extracts and 32p_
_______ Van Dolah et aI.: Assessment of the Involvement of Algal Toxins in the 1994 Texas Fish Kills 43

Table 1

Toxicity results on water samples collected.

Mouse

Location Date bioassay Cytotoxicity

Cameron 12 May neg neg

Rollover 12 May neg neg

Sabine (1) Dark water 3June n.d.] neg

Sabine (2) Clear water 3June n.d. neg

Sabine (3) Dark water 3June n.d. neg

Galveston Ship Channel 5July neg neg

I n.d. = not determined.

phosphorylase a at 30°C for 15 minutes. The reaction

was halted by addition of ice cold trichloroacetic acid

(TCA, 10%). Phosphorylase a was then precipitated by

centrifugation and 32p released was quantified by counting an aliquot of the supernatant by liquid scintillation

spectroscopy. Inhibition of the amount of32p released

relative to untreated controls indicates the presence of

phosphatase inhibitor.

Results and Discussion

Water Samples

Phytoplankton identification and toxicity testing were

carried out on water samples collected on three dates,

at approximately one month intervals, during the occurrence of discolored water patches. Discolored water

samples were first collected by helicopter on 12 May

1994 from Cameron, Louisiana, and Rollover Pass,

Texas, approximately one mile offshore. Both water

samples were of low salinity, the Cameron sample at

16%0 and Rollover Pass at 20%0. The water from

Cameron contained a mixed estuarine heterotrophic

assemblage of dinoflagellates (see Steidinger et aI.,

1998), rather than a monotypic bloom. The sample was

dominated by Heterosigma c.f. alwshiwo, which has been

known to cause fish kills by unidentified mechanisms.

In contrast, similarly colored water collected the same

day approximately one mile offshore from Rollover

Pass was dominated by Gymnodinium sanguineum. The

phytoplankton fractions collected in the 20 pm size

filter mesh were negative for toxicity by mouse bioassay

and by in vitro cytotoxicity assays (Table 1).

Additional samples were provided by Texas Parks

and Wildlife Dept. on 3June 1994 offshore from Sabine

Pass, from both within and outside of discolored water

patches. The major microalgal species in two samples

from within the discolored water included dinoflagellates Gymnodinium sanguineum, Dinophysis caudata,

Prorocentrum minimum, and euglenoids Eutreptiella spp.,

while algae cells in the sample from outside the discoloration were sparse. The material collected in the 20

pm fraction from all three samples were negative for

toxicity by mouse bioassay and by in vitro cytotoxicity

assays (Table 1).

Due to growing concerns regarding the potential for

human health impacts associated with the persistence

of discolored water along the Texas coast, and the

presence of Dinophysis sp. in these samples, the 3 June

1994 samples were analyzed for the presence of

diarrhetic shellfish poisoning (DSP) toxins. Analysis of

DSP toxins was based on the action of DSP toxins to

inhibit protein phosphatase 2a. No phosphatase inhibitory activity was observed in the samples from discolored water. Certain Dinophysis sp. are producers of DSP

toxins, and low levels of DSP toxins have been identified in samples of Dinophysis collected from Alabama

waters (Dickey2). However, there is no evidence that

DSP toxins may cause fish kills and no incidents of DSP

have been recorded in the Gulf of Mexico to date.

A third sampling of discolored water was carried out

by Texas Parks and Wildlife on 5 July 1994 from

Galveston shipping channel. This sample, dominated

by G. sanguineum, also tested negative for toxicity in

mouse and in vitro cytotoxicity assays (Table I).

Gymnodinium sanguineum Hirasaka is an estuarine dinoflagellate which has been known to cause extensive

red tides, and fish kills in certain cases. Nevertheless,

this species is an important food source for some zooplankton, as well as larval (Lasker et aI., ] 970) and adult

(Rojas de Mendiola, 1979) anchovy, Engraulis mordax.

Gymnodinium sanguineum is considered to be synonymous with Gymnodinium nelsoni Martin and Gymnodinium

splendens Lebour. It is worth noting that even though its

morphology is highly variable, some researchers still

question whether G. sanguineum is synonymous with G.

splendens based on the original description of the latter

species. In conditions similar to those experienced in

1994, a June 1984 bloom of G. splendens at Galveston

was linked to extensive kills of two demersal fish species, threadfin, Polydactylus oclonemus, and croaker,

Micropogonias undulatus (Harper and Guillen, 1989).

Similarities between the incidents are time of year, high

volume runoff conditions, and wind direction. Since G.

sanguineum is a strong vertical migrator, it does particularly well in stratified water columns. The primary mechanism by which G. sanguineum is believed to cause kills is

through hypoxia and hydrogen sulfide formation during the decay of a bloom (Robinson and Brown, 1983;

Rojas de Mendiola, ] 979). The presence of these conditions was noted during the 1984 fish kill.

2 Dickey, R. 1994. Fisheries Research Branch, FDA, P.O. Box 15H,

#1 Iberville, Dauphin Island, AI. 3652R. Personal commun.
44 NOAA Technical Report NMFS 143

This species has also been reported as being responsible for oyster mortalities through clogging of gills

(Nightingale, ]936). It has not been reported to produce a toxin, however a G. sanguineum extract at high

concentration has been observed previously to cause

low level toxicity in mice (Dickey2). Because of concern

for potential human health impacts associated with the

current G. sanguineum bloom, we analyzed the 20 J1m

fractions from all discolored water samples for the ability to inhibit brevetoxin binding in a receptor binding

competition assay. We found that all sample extracts

caused a partial inhibition of brevetoxin binding. However, further characterization of the receptor in teraction is necessary before any conclusions can be made.

Gymnodinium sanguineum is not believed to produce

brevetoxin-like compounds. Our laboratory is currently

assessing the toxicity of G. san{;uineum in culture.

Oyster Samples

Extracts of oysters collected from reddish colored water

in Sabine Pass on 28 june 1994, concurrent with a fish

kill, were provided to us by Texas Dept. of Health,

along with a control extract of oysters from Lavaca Bay,

Texas, located west of the region impacted by the discolored water. All extracts were mildly toxic when tested

by Texas Dept. of Health using the APHA mouse bioassay protocol (Ordner3), exhibiting borderline mouse

toxicity, indicated as a "+" in Table 2. The extracts were

tested in our laboratory for in vitro cytotoxicity (Table

2). All samples were negative in the cytotoxicity assay.

Additional oysters were collected in Sabine Pass during

an in tense G. sanKUineum bloom on 5 july 1994 by Texas

Parks and Wildlife and shipped to Charleston Laboratory for analysis. These were extracted by a modifica3 Ordner, Mike. 1994. Seafood Safety Division, Texas Dept. of

Health, J J00 W. 49th St., Austin, TX 78756-3199. Personal commun.

Table 2

Toxicity results on oyster samples.

tion of the APHA protocol, in which they were solubilized in methanol rather than cottonseed oil. These

samples were also negative in the cytotoxicity assay.

Control oysters collected from Charleston Harbor,

Charleston, S.c., were analyzed in parallel and showed

no toxicity in either assay. Because of the results observed in the algal samples, we also analyzed the oyster

samples for the ability to inhibit brevetoxin binding to

the voltage dependent sodium channel, using a receptor binding competition assay (Van Dolah et al., 1994).

We found that all oyster samples from Texas, including

the "control" oysters from Lavaca Bay, caused a partial

inhibition of brevetoxin binding in the assay, whereas

control oysters from Charleston Harbor, S.c., had no

inhibitory activity in the receptor assay. However, as in

the case ofthe algal extracts, the nature ofthe brevetoxin

binding inhibition observed in the oyster extracts from

Texas must be further characterized before any conclusion regarding toxin production can be made.

Summary _

One or more algal blooms appear to have occurred on

the upper Texas coast during May-july 1994, based on

the spatial and temporal patchiness of the discolored

water. However, given the diversity of dominant algal

species identified in water samples obtained from similar-looking areas of discoloration, the involvement of a

unialgal bloom in the fish kills is not definitive.

Gymnodinium sanguineum appears to be the on Iy common denominator among samples tested, although it

was not consistently present in bloom proportions. Results of toxicity assays on all algal samples were negative

by mouse bioassay and in vitro cytotoxicity assays. 0

DSP activity was detected in samples containing

Dinophysis sp. Oysters collected from Sabine Pass during

a bloom of G. sanguineum displayed borderline mouse

lethaiity, but were negative in in vitro cytotoxicity assays.

The potential for the production of sodium channel

specific activity in C. sangiuneum is cUtTently under

im·estigation.

Literature Cited

I Data from Texas Health Dept.

2 n.d. = not determined.

Location

Lavaca Bay(#24)

Sabine Pass(#25)

Sabine Pass(#26)

Sabine Pass(#27)

Sabine Pass

Date

28 June

28.June

28June

28June

5 July

Mousel

bioassaY Cytotoxicity

+ neg

+ neg-

+ neg

+ neg

n.d 2 neg

,\nderson, U. M.

1994. Red tides. Sci. Amer. 271:52-58.

Geraci,j. R., D. ,'vi. Anderson, R.j. Timperi, D.j. St. Aubin,

G. :\. Early,j. H. Prescott, and C. A. Mayo.

1989. Humpback whales (Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can. j. Fish. Aquat. Sci.

46: 1tl95-1 tl98.

Greenberg, A. E., and D. A. Hunt.

1984. Laboratory procedures for the examination of seawater and shellfish. Fifth Edition. Amer. Pub!. Health Assoc.,

Washington, D.C.
________ Van Dolah et al.: Assessment of the Involvement of Algal Toxins in the 1994 Texas Fish Kills 45

Harper, D. E.,Jr., and G. Guillen.

1989. Occurrence of a dinoflagellate bloom associated with

an influx of low salinity water at Galveston, Texas, and

coincident mortalities of demersal fish and benthic invertebrates. Comrib. Mar. Sci. 51:147-16l.

lngebritsen, T. S.,]. G. Fowlkes, and P. Cohen.

1983. The protein phosphatases involved in cellular regulation.

2. Glycogen metabolism. Eur.]. Biochem. 132:255-26l.

Lasker, R., H. M. Geder, G. H. Theilacker, and R.C. May.

1970. Feeding, growth, and survival of Engraulis mordax larvae

reared in the laboratory. Mar. BioI. 5:345-353.

Nightingale, H. W.

1936. Red water organisms. Argus Press, Seattle, 24 p.

Robinson, M. G., and L. N. Brown.

1983. A recurrent red tide in a British Columbia coastal lagoon. Can.]. Fish. Aquat. Sci. 40:2135-2143.

Rojas de Mendiola, B.

197(J. Red tide along the Peruvian coast. In D. L. Taylor and

H. Seliger (eds.), Toxic dinoflagellate blooms, Proceedings

of the International Conference (2nd), vol. I, p. 183-190.

Elsevier/North Holland, NY

Steidinger, K. A., D. A. Stockwell, E. W. Truby, W. K. Wardell,

Q. Dortch, and F. M. Van Dolah.

1998. Phytoplankton blooms off Louisiana and Texas, MayJune 1994. In R. Zimmerman (ed.), Characteristics and

causes of Texas marine strandings, p. 13-17. NOAA Tech.

Rep. NMFS 143.

Van Dolah, F. M., and]. S. Ramsdell.

1996. MaitoLOxin, a calcium channel activator, inhibits cell cycle

progression through G l/S and G2/M transitions and prevents

CDC2 kinase activation in GH4

C1 cells.]. Cell. Physiol. 166:4!J-56.

Van Dolah, F. M, E. L. Finley, B. L. Haynes, C.]. Doucette, and

]. S. Ramsdell.

1994. Development of rapid and sensitive high throughput

pharmacologic assays for marine phycoLOxins. Natural Toxins 2:189-196.

Patterns of Bottlenose Dolphin, Tursiops truncatus, Strandings in Texas

GRAHAM A.J. WORTHY

Physiological F:cology and BioenerKetics Research I,ab and

Texas Marine Mammal Stranding Network

Texas A&M University

5001 Avenue U, Suite 105

Galveston, Texas 77551

ABSTRACT

During the spring of 1994, large numbers of bottlenose dolphins, TursiojJs truncatus,

washed ashore along the upper Texas coast. The majority of these carcasses were in an

advanced state of decomposition, indicating that death had occurred some time earlier,

possibly offshore. Despite intensive efforts to determine the cause of death by traditional

pathological examinations, no conclusions could be drawn. Eventually, through the use of

polymerase chain reaction (PCR) techniques, the Armed Forces Institute of Pathology was

able to determine that a large proportion of the animals had an active morbillivirus

infection and that this was likely the cause of death. Compared to normal years, increased

numbers of dead dolphins began washing up on beaches during December 1993, peaking

in March and April 1994 when a total of ] 71 dolphins were retrieved and continuing

through May 1994. Of this total, 89% were retrieved between Matagorda Bay and the

Louisiana state line. The actual impact on the coastal bottlenose dolphin population may

never be known because of a lack of robustness in the population estimates, however,

ongoing surveys of the resident populations in Galveston, Matagorda, and Corpus Christi

Bays do not indicate any decline in local abundance.

Introduction

Bottlenose dolphins, Tursiops lruncalus, inhabit temperate and tropical waters in all of the world's oceans (e.g.

Wlirsig and Wlirsig, 1979; Cockcroft and Ross, 1990;

Corkeron, 1990; van Waerebeek et aI., 1990) and are the

most common coastal marine mammal species found in

the Gulf of Mexico (Blaylock et aI., 1995). This species

exploits a wide variety of habitats (Kenny, 1990; Shane,

1990; Fenl, 1994; Blaylock et aI., 1995) and has been

described as having two distinct forms, or ecotypes; coastal

and offshore (possibly two distinct species-see Curry,

1997). These two forms are recognized to differ in physiology, ecology, and morphology (Duffield et aI., 1983;

Hersh and Duffield, 1990; Mead and Potter, 1990; Curry,

1997). The coastal population of bottlenose dolphins

in the southeastern United States appears to be composed of residen t stocks that reside year round in local

bays, as well as a coastal transient stock which migrates

along the coast on a seasonal basis (e.g. Brager et aI.,

1994; Blaylock et aI., 1995; Mate and Worthy, 1995).

Because of its position at the top of the food chain,

various researchers have described this species as one

that could be useful in monitoring our coastal environment. To this end, it is one of the most widely studied

species of marine mammals in the world. Many investigators have examined life histories, behavior, feeding

habits, movement patterns, and energetics, as well as a

wide variety of other parameters including contaminant accumulation, parasites, and diseases. These latter

areas of investigation are facilitated by the activities of

various stranding networks throughout the world (Odell,

1985; Wilkinson and Worthy, 1999).

The Texas Marine Mammal Stranding Network

(TMMSN) was founded in ]980 with the goal of recovering all dead and live stranded marine mammals which

come ashore along the approximately ],000 miles of

Texas coastline. It is a volunteer organization, comprised of both lay people and professional biologists, as

well as employees offederal agencies (National Marine

Fisheries Services and ational Parks Service personnel), state agencies (Texas Parks and Wildlife Depart47
Table 1

\lumbers of representatives of non-Tursiops species

which have stranded along the Texas coast between

1980 and 1996.

48 NOAA Technical Report NMFS 143

ment, Texas A&M University, and the University of

Texas), and private organizations (Sea World of Texas

and Texas State Aquarium). The TMMSN is divided

into six regions, each of which has a Regional Coordinator. These Regional Coordinators relay data and

samples to the State Operations Coordinator who is

based in Galveston, Texas. This system allows for efficient and effective coverage of the entire Texas coast.

During the history of the TMMSN, the bottlenose dolphin has accounted for approximately 96% of recovered animals with the remainder comprised of] 9 additional species of marine mammals (Table 1), rangi ng

from manatees, TrichfChus manatus (Fernandez and

Jones, 1990) to sperm whales, Physeter macrocephalus

Uones, 1988; Tarpley and Marwitz, 1993).

During the period Decemher 1993 through May 1994,

large numbers of dead bottlenose dolphins washed

ashore on the Texas coast. This paper describes, and

attempts to explain, the temporal and geo?;raphic distribution of strandings of that unusual mortality event.

These types of analyses can lead to a better understanding of the causes of unusual mortality events (e.g. Bodkin and Jameson, ] 991).

Materials and Methods

(lrder Cetacea

Ralaenop/era aru/oros/ra/a

S/enetla coentleoalba

s. aUenua/a

S. longiros/n;

S. dymene

S. fran/atis

S/enetla 'p.

S/eno &redanensis

Lagenodelphis IlOsei

Clobier/Jhala macrorynrhu.s

Pe/Jonore/Jhala elec/ra

PhyseLer macrocephalus

Pseudorra crassidens

Grampus ,Il:nseus

Feresa al/enua/a

.\1esoplodon eurapaeus

liphius wviroslns

Kogia breviceps

K. simus

Kogia sp.

Order Sirenia

Tnrhechus mana/us

I

4

5

5

15

7

17

2

I

1

2

3

3

3

.'i

4

3

8

8

8

4

Repons of stranded dolphins were relayed to the

TMMSN either directly from the public or through

governmental agencies, and a recovery team was dispatched. A coding system was used to identify the degree offreshness of a recovered carcass; code 1 refers to

a live stranding, code 2 is very fresh (less than R-10

hours postmortem), and carcasses decline in freshne~s

to a code 5 animal which is a mummified carcass or

skeletal remains. Such a coding system identifies the

limitations placed on investigators in terms of identifyin?; the cause of death. Once an animal was recovered,

a condition code was assigned, information on ?;ender

and basic morphometrics was obtained, if possible, and

the exact location of the stranding was noted. This was

not possible in the case of many of the code 4 or 5

animals due to advanced decomposition.

Recently dead, fresh animals (condition code 2 or

early code 3) were immediately returned to our necropsy

facility in Galveston where a complete necropsy was

performed. Animals which were more decomposed,

designated as late 3, 4, or 5 condition codes, were

necropsied on the beach, where voucher specimens

were collected as well as samples for toxicological and

virological studies. Some of these latter studies were

undertaken by the Armed Forces Institute of Pathology

(e.g. Kraft et aI., 1995; Lipscomb et aI., 1996). All animals were examined for any indication of fisheries interactions or obvious injuries.

Results and Discussion

During the early years of the Texas Marine Mammal

Stranding Network, an expansion in numbers of participants and public awareness resulted in a ?;reater

de?;ree of coastal covera?;e and increasing numbers of

recovered dolphins (Fi?;. 1). From 1986 through the

present, the intensity of covera?;e has remained constan t and therefore ann ual differences should reflect

actual differences in stranding rates and distribution

(Wilkinson and Worthy, in press). During normal stranding years, the TMMSN recovers approximately 130.7 ±

17.3 (± 95% CI) dolphins (Fig. 1) with non-Tursiops

animals accounting for 4.2 ± 1.2% of total strandings in

an average year (Fig. 1). This mean is based on numbers of dolphins that stranded in 1986-89, 1991, 1993,

and 1995. There have been four years in which abnormally high numbers of dolphins have been recovered

from Texas beaches: 1990,1992,1994, and 1996 (Fig. 1).

Increased numbers of animals in each of these unusual

years were solely a result oflarge numbers of bottlenose

dolphins coming ashore rather than increased reporting effort.

Typically, dolphin strandings follow a seasonal pattern in Texas with more than 60% of animals coming

ashore during the period February through April (Fig. 2).
_____________ Worthy: Patterns of Bottlenose Dolphin, Tursiop~' trnncalus, Strandings in Texas 49

1980 1982 1984 1986 1988 1990 1992 1994 1996

year

_ Tursiops

CJ!!:J non Tursiops

M

"

~dl I

Oct Nov Dec Jan Feb Mar Apr May Jun

month

Figure 1

Total number of cetacean strandings recovered annually, 1980-

96. Tursiops truncatus accounts for approximately 96% of all

strandings. Horizontal lines refer to the average number of

strandings (± 95% el) recovered in a "normal" year (as defined

by those years, 1986-89, \99\, 1993, j 995, in which an "unusual"

event did not occur). Increasing numbers of animals recovered

between j 980 and 1986 are a result of increased coverage of the

coast by the TMMS '.

350

300

rJl 250 £

£

a.

0 200 u

-

0

Q; 150 .c

E

::::l

c 100

50

0

100

80

rJl

C

£

a. 60

0

u

'0

Q; 40 .c

E

::::l

C

20

0

umbers of recovered dolphins decline during the summer months and begin to increa e

again in December and January (Fig. 2). In an

average year, the TMMS recovers 9.4 ± 2.2

dolphins in January, increasing to 38.0 ± ] 2.0

dolphins in March and subsequently declining

to 2.8 ± 1.9 dolphins in June (Fig. 2). While this

general pattern held true for 1993-94, the absolute numbers were significantly higher. A significant increase (t-test, P< 0.05) above nOl-mal

levels was first noted in December 1993 and a

return to normal did not occur untilJune ] 994.

During the peak mon ths of March (n = 90) and

April (n = 81), up to ten dolphins were being

recovered in a single day.

During March and April] 994, a total of 171

animals were retrieved from the entire Texas

coast, but 151 (89%) of those were collected

from beaches east of Matagorda Bay and west

of the Louisiana state line (Fig. 3). Despite

regular vigilance by the public and several agencies, including ground and aerial beach surveys, animals were frequently discovered washing ashore as code 4 animals. Normally, code 4

and 5 animals account for less than 35% of

recovered animals. l In January 1994, 50% of

the recovered animals were either condition

code 4 or code 5. Thi proportion increased

considerably in February (70%) and remained

high through March (65%) and April (53%).

These high proportions of code 4 and 5 animals made identification of sex and the measurement of any morphometries difficult.

Discoveries of these badly decomposed dolphins the day after a beach survey was performed suggests that animals were dying offshore and floating for days before drifting onto

the beach. Taking into consideration ambient

water (55-65° F) and air temperatures (45-65° F)

(TMMSN records), it would take approximately

7 to 10 days for an animal to decompose to

condition code 4. This suggests the possibility

that animals may have died offshore and washed

onto the beach after some period of time. During the period from 1 March until mid-Apl-il

there was significant down coast and onshore

surface water movements,2 and onshore winds,

which resulted in several research drifter buoys

--.- average year

-- 1993-94

I Worthy, G. ] 994. Texas Marine Mammal Stranding

Network, 5001 Avenue U, Suite 105, Galveston TX 77551.

Unpubl. data.

2 Nowlin, W. ]994. Department of Oceanography,

Texas A&M University, College Station, TX 77843. Personal commun.

Figure 2

Mean (± SO) monthly strandings during "normal" years (as

defined in Fig. 1) and the actual numbers of dolphins which

stranded during 1993-94.
50 NOAA Technical Report NMFS 143

February, 1994

March, 1994

A

B

Figure 3

(Left and facing page) Geographic and

temporal distribution of Tttrsiops strandings along the Texas coast: (A) February

1994, (B) March 1994, (C) April 1994,

(0) May 1994. Each point is an individual dolphin.
_______________ Worthy: Patterns of Bottlenose Dolphin, Tursiops truncatus, Strandings in Texas 51

April, 1994

May, 1994

c

D
52 NOAA Technical Report NMFS 143

:\ Zimmerman, R. 1994. A preliminary report on mortalities of

marine animals in Texas during the spring of 1994. NMFS, SEFSC

Galveston I.aboratory, 4700 Avenue C, Galveston TX 77551.

washing ashore east of Galveston at the beginning of

April and into May. The surface current patterns along

the coast between Sabine Pass and Galveston Bay were

atypical during this period and, in conjunction with the

observed strong south and southeast winds, could result in the surface flow being driven into shallowwater. 3

These data suggest that some animals may have died

offshore of western Louisiana and eventually drifted

ashore in east Texas. The time course of strandings

does not suggest a discrete period for the mortality

even t, but rather a protracted period of several weeks

(Fig. 3).

A total of three code I (live-stranding) animals and

six code 2 dolphins were retrieved during the time

course of this event. AJI three live animals tested negative for the presence of active morbillivirus and survived (Bull and Worthy, 1995), two of wh ich were subsequently released and satellite-tracked (Mate and Worthy, 1995). The remaining animal was deemed too young

to be released. None of the tested code 2 animals (two

animals were not tested because they stranded near the

Mexican border and were not likely part of the unusual

length class (em)

event) showed any clinical evidence of morbillivirus4

nor did they test positive using peR techniques

(Lipscomb et aI., 1996).

An examination of length data collected from those

animals which were intact suggest that 22.8% (46/202)

of recovered dolphins were young-of-the-year «110 cm),

10.4% (21/202) were approximately 2 years of age

(>110-<130 cm), 27.7% (56/202) were between the

ages of 2 and 5 years old (130-<230 cm), and the

remaining 39.1 % (79/202) had lengths in excess of230

em and are considered as sexually mature adults (Fig. 4)

(Fernandez, 1992). Relative proportions oflength categories found in the 1994 data are similar to those reported

by Hansens and Fernandez (1992) for bottlenose dolphins in Texas that stranded during the period 1983-90.

One problem in interpreting the sex ratio data relates to the difficulty in assessing the sex of a badly

decomposed code 4 or 5 animal. It is often easy to

identify males under these circumstances because, during the bloating process, the penis is frequently extruded. The sex of an animal that lacks an extruded

penis cannot, however, be assumed to be female. This

results in a large number of animals not being identified as to their sex (45%), and the sex ratio of those

which are identified being skewed toward males (67%

male:33% female). This should not be taken as meaning

there were a greater number of males dying.

Two previous unusual mortality events have

occurred in the Gulf of Mexico, the first

during 1990 and the second in 1992. A total

of 214 dolphins (201 Tursiops) were recovered from Texas beaches in 1990 and 267

dolphins (245 Tursiops) were recovered in

] 992. In ] 990,23 dead dolphins were discovered on a single day in east Matagorda Bay

after an unusually severe cold weather system moved through the area (Miller, 1992).

No definitive cause of death was ever identified for animals which died elsewhere in the

state or throughout the Gulf of Mexico during that year (Hansen, 1992), although a

morbillivirus epizootic has recently been suggested based on preserved samples (Duignan

et a1., 1996). The remaining 178 dolphins

collected during 1990 are still significantly

greater than the number of animals retrieved

during a normal year and were part of a

Gulf-wide event.

100 110 120 130

.. unknown

~male

_ female

90

30

25

V>

c 20

:E

Q.

<5

1:J

a 15

Q;

.0

E

OJ 10 c

5

0

80

Figure 4

Numbers of dolphins collected during 1994 as a function of length

category. Each bar is divided into males, females, and animals of

unknown gender. Animals with lengths greater than 240 em are

considered to be adults (Fernandez, 1992).

4 Cowan, D. 1994. Department of Pathology, University ofTexas Medical Branch, Galveston, TX 77555.

Unpubl. data.

5 Hansen, L. (ed.). 1992. Report on investigation of

1990 Gulf of Mexico bottlenose dolphin strandings.

SEFSC, Miami I.aboratory Contribution MIA-92/93-

21,219p.
_____________ Worthy: Patterns of Bottlenose Dolphin, Tursiops truncatus, Strandings in Texas 53

The 1992 mortality event was restricted to the

Matagorda Bay area and occurred after a series of unusually heavy winter rains. Although no definitive cause

was identified, one working hypothesis was that agricultural run-off contributed to it (Colbert et aI., in press).

A morbillivirus epizootic was not implicated because of

low seroconversion rates observed in live animals

(Duignan et aI., 1996), which were captured as part of a

National Marine Fisheries Service health assessment

operation undertaken during the summer of 1992.

Duignan et al. (1996) incorrectly reported that 220

dolphins died around Matagorda Bay during March

and April 1992. The actual n umber for that time period

was 119; the remainder of the 267 animals that were

recovered in 1992 came from throughout the state over

the balance of the year. 6

Because of the inability to perform a thorough

necropsy, there is considerable difficulty in assessing

actual cause of death in animals which are as decomposed as the majority of the 1994 dolphins were. In

code 4 animals, it is often impossible to even identifY

major organs. The utilization of polymerase chain reaction (PCR) techniques to identify the presence of active

morbillivirus in lung tissue (Lipscomb et aI., ]994b,

1996) was a major advance in the determination of

cause of death. Some dolphins which washed ashore in

Texas were so badly decomposed that nucleic acids

could not even be amplified from the tissues which

were collected (Lipscomb et aI., 1996). In those animals for which amplification was possible, Lipscomb et

a!. (1996) discovered that in excess of 60% (29/57) of

examined dolphins tested positive for the presence of

active morbillivirus. If this proportion is extrapolated

to the total number of dolphins recovered, these "infected" dolphins would account for all of the observed

increase above normal stranding rates seen during early

1994.

Although increased numbers of strandings were not

being reported in Florida when the initial morbillivirus

infected animal stranded alive there in June 1993

(Lipscomb et aI., 1994a), that single stranding event

preceded an increased stranding rate throughout the

Gulf of Mexico during the balance of 1993 and the first

five months of 1994. Increased numbers of dolphins

started coming ashore in Alabama from July through

December 1993 and subsequently in Mississippi from

August through December] 993 (Lipscomb et a!., 1996).

There was no organized stranding network operating

in Louisiana and therefore we have no concept of what

was happening there. Texas dolphins were found to be

infected with morbillivirus throughout the upper Texas

coast, regardless ofthe age ofthe dolphin (Lipscomb et

6 Worthy, G. 1994. Texas Marine Mammal Stranding Network,

500] Avenue U, Suite 105, Galveston TX 77551. Unpubl. data.

aI., 1996), and the temporal and geographic distribution ofstrandings during 1993-94 were consistent with

a westward spread of the virus along the Gulf coast.

This recent outbreak of morbillivirus in the Gulf of

Mexico is the same disease which resulted in the deaths

of] 8,000 harbor seals in northwestern Europe in ]988

(Kennedy, 1990; Markussen, ] 992; Heide-Jorgensen et

aI., ] 992), as well as thousands of striped dolphins in

the Mediterranean in ] 990 (Aguilar and Raga, 1993;

Calzada et aI., 1994). Recently a morbillivirus outbreak

was implicated, using preserved tissues, as the cause of

the ]987-88 U.S. Atlantic coast epidemic that resulted

in a tenfold increase in the mortality of bottlenose

dolphins (Lipscomb et aI., 1994b) and the disease has

been described in several other species found in the

western Atlantic Ocean (Daoust et aI., 1993; Duignan et

aI., ] 995).

Since the proportion of animals which die at sea and

which eventually wash ashore is unknown, it is virtually

impossible to calculate the actual impact of this unusual mortality event. Minimum population estimates

for the western Gulf of Mexico coastal stock is 3,499

dolphins (CV = 0.21), the offshore stock consists of

5,618 dolphins (CV = 0.26), and estimates of resident

populations for Galveston, Matagorda, and Corpus

Christi Bays total fewer than 500 animals (Blaylock et

aI., 1995). Ongoing surveys of resident populations of

bottlenose dolphins found in these bays do not suggest

any impact of the 1994 event on local populations7

(Blaylock et aI., 1995). Due to inadequate knowledge of

the stock structure and/or population numbers (Blaylock et a!., 1995), the true impact on the transient coastal

and/or offshore populations may never be known.

Acknowledgments _

A large number of individuals helped in the recovery

and examination of animals in this study, especially the

TMMSN Galveston Regional Coordinators, Brian Wilson and Lance Clark, and TMMSN State Operations

Coordinator, Elsa Haubold. D. Cowan, University of

Texas Medical Branch, performed necropsies on all

code 2 animals that were recovered. The Environmental Air Force donated their assistance in undertaking

aerial surveys and National Marine Fisheries Service

Southeast Fisheries Science Center's Galveston Laboratory undertook beach surveys. All dolphins were collected under a Letter of Authorization issued by the

National Marine Fisheries Service to Graham A.J. Worthy, Director, TMMSN.

7 Weller, D., and B. Wursig. 1994. Marine Mammal Research Program, Texas A&M University, 4700 Avenue U, BldF;. 303, GalvesLOn

TX 77551. Unpubl. data.
54 NOAA Technical Report NMFS 143

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Sea Turtle Strandings along the Texas Coast, 1980-94

DONNA]. SHAVER

Padre Island National Seashore*

Midwest Science Center

National Biological Service

9405 S. Padre Island Drive

Corpus Christi, Texas 78418-5597

ABSTRACT

During 1980-94, 3,283 stranded sea turtles (2,929 dead, 354 alive) were found along

the Texas coast, including 1,139 Kemp's ridley, I_epidochelys kempii, 1,524 loggerhead, Caretta

caretta, 258 green, Chelonia mydas, 170 hawksbill, I-:retmochelys irnbricata, and 57 leatherback,

Derrnochelys coriacea, turtles and 135 unidentified tunles. More tunles stranded during 1994

than during any year from 1980 to 1993. There were various sources of mortality during

1980-94. A large percel1lage of the strandings were probably due to incidental capture in

shrimp trawls. Fewer stranded tunles were found during the Texas Closure (when some

Gulf of Mexico waters off Texas were closed to shrimp trawling) than before and after the

closure. During 1994, temporal and spatial distributions of the strandings coincided with

nearshore shrimping and the numbers of stranded turtles were inversely related to Turtle

Excluder Device enforcement.

Stranding records reveal the importance ofTexas waters for Kemp's ridley tunles. This

species comprised an increasing percentage of the strandings along the Texas coast; 48%

percent of the 527 documented strandings during 1994 were Kemp's ridley turtles. Fewer,

but larger, Kemp's ridley turtles stranded along the middle and lower Texas coast. Based on

analyses of digestive tract contents, some Kemp's ridley turtles in Texas are consuming the

by-catch discarded by shrimp trawls. Tunles may concentrate in areas of shrimping to

exploit that easily obtainable food and thereby become vulnerable to capture by trawls.

Introduction

Stranded sea turtles are dead or live turtles that wash

ashore or are floating; live floating turtles are generally

in a weakened condition (Schroeder, 1988; Teas, 1993).

The Sea Turtle Stranding and Salvage Network (STSSN)

was established in 1980 to document strandings of marine turtles on U.S. beaches along the Gulf of Mexico,

Atlantic Ocean, and Caribbean Sea (Schroeder, 19R8).

Because not all stranded turtles are detected, the numbers reported by the STSSN are considered to be minimum estimates of the total number of strandings

(Schroeder, 1988; Teas, 1993).

Stranded sea turtles along the Texas coast (Rabalais

and Rabalais, 1980; Whistler, 1989) include all five species that occur in the northwestem Gulf of Mexico:

Kemp's ridley, Lepidochelys kempii, loggerhead, Carella

carella, green, Chelonia mydas, hawksbill, Eretmochelys

imbricata, and leatherback, Dermochelys coriacea, turtles.

Several investigations have been conducted to determine causes of the strandings and to study various

attributes of the stranded animals (Heinly et a1., 1988;

Plotkin and Amos, 1990; Shaver, 1990a; Shaver, 1990b;

Caillouet et a1., 1991; Shaver, 1991; Plotkin et a1., 1993;

Sis et a1., 1993). Factors that have been implicated in

sea turtle strandings along the Texas coast include collision with boat propellers (Whistler, 1989), oiling (Whistler, 1989), entanglement (Plotkin and Amos, 1990), ingestion of fishing gear and marine debris (Plotkin and

Amos, 1990), and incidental capture during J-ecreational

or commercial fishing (vVhistler, 1989; Caillouet et a1.,

1991). Although explosives to remove oil and gas platforms during 1986 (G'tschlag and Renaud, 1989) caused

at least 51 strandings, an intensive observer program was

* Current address: Padre Island National Seashore, Columbia Environmental Research Center, U.S. Geological Survey, P.O. Box

181300, Corpus Christi, TX 7R480-1300.

57
58 NOAA Technical Report NMFS 143

instituted in 1987 to prevent such occurrences, and no

strandings have been attributed to that source since then

(Gitschlag and Renaud, 1989; Richardson, 1989; Gitschlag,

1992). Forty-seven turtles stranded as a result ofhypothermic stunning in 1989 (Shaver, 1990a, 1990b). Twenty-five

hatchlings and post-hatchlings stranded in 1986 and 53 in

1990 (Shaver, 1992), probably from being washed ashore

by strong winds and currents.

Incidental capture in shrimp trawls has been identified as a significant source of sea turtle mortality along

the Texas coast and in other areas in the southeastern

United States (Magnuson et al., 1990). To reduce trawlrelated mortality, Turtle Excluder Devices (TED's) have

been phased into mandatory usage in Texas waters

since 1990. Since 1981, some Gulf of Mexico waters off

Texas have been closed to shrimp trawling for 6-1'\

weeks to allow shrimp to grow to a larger size prior to

harvest (termed Texas Closure). This closure has encompassed the entire month ofJune and varying portions of May and July. Reductions in the number of

stranded turtles located during the Texas Closure were

noted prior to the adoption of Turtle Excluder Device

regulations (Magnuson et al., 1990).

Sea tunle strandings along the Texas coast continued after the implementation of TED regulations and

reached unprecedented levels during 1994. This study

was done to examine trends in the numbers ofstrandings

and affected animals, particularly in 1994 and the critically endangered Kemp's ridley turtle, and to determine possible causes ofthe strandings. To provide comprehensive protection of threatened and endangered

turtles, anthropogenic causes of strandings must be

identified and reduced (Magnuson et aI., 1990).

Materials and Methods

Sea Turtle Stranding and Salvage Network

Procedures for locating and documenting stranded

turtles in Texas were described by Whistler (1989).

Stranded turtles were located by network participants

in response to information from beach visitors and

during systematic surveys conducted in some areas of

the state. Few systematic surveys were conducted before

1986. Systematic surveys to locate stranded turtles were

most comprehensive during 1986-90. From 1986 to

1989, the ational Marine Fisheries Service supplemented voluntary efforts by STSSN participants with

systematic, year-round surveys on the Texas coast

(Caillouet et al., 1991). From 1990 to 1994, the survey

areas and frequency were reduced. Little effort was

made to survey in remote regions of the Texas coast

such as the Matagorda Peninsula, SanJose Island, South

Padre Island, and inshore areas. The survey area and

frequency decreased along the upper Texas coast, remained at similar levels on Mustang Island, and increased on North Padre and Matagorda islands.

For each stranded turtle, information was collected on

species, stranding date and location, tag numbers (if applicable), visible injuries, condition, and final disposition

of the animal. The curved carapace length (CCL) and

curved carapace width (CCW) or straight-line carapace

length (SLCL) and straight-line carapace width (SLCW)

of most turtles were measured. Information was recorded

on standardized forms that were forwarded to the state

and subsequently to the national STSSN coordinators.

The Texas STSSN database was queried for records

of stranded turtles found in Texas from 1980 through

1994. Stranded turtles that had been raised in captivity

for about one year (head-started) were excluded from

this analysis because the tempOl-al and spatial distributions of their strandings may have been influenced by

captive rearing and release (Manzella et al., 1988; Teas,

1993). Similarly, turtles that were captured incidentally

(such as in power plant intake canals and by commercial or recreational fishing) were not included in the

total numher ofstrandings (Teas, 1993).

Strandings were categorized as either offshore (on

beaches or waters of the Gulf of Mexico) or inshore (in

the passes and bays) (Teas, 1993). The locations of

offshore and inshore strandings were also categorized

by year and by Shrimp Statistical Zone, established by

the National Marine Fisheries Service. Strandings were

also grouped according to whether they occurred along

the upper Texas coast (Zones 17 and 18) (Caillouet et

aI., 1991), middle Texas coast (Zone 19), or the lower

Texas coast (Zones 20 and 21) (Fig. 1).

Injuries and anomalous conditions of the turtles that

possibly contributed to the strandings were summarizerl from comments on stranding forms. Turtles were

categorized as hatchlings/post-hatchlings when they

were less than 10.0 cm SLCL and as adults when they

exceeded minimum sizes of nesting females. Conversions of minimum nesting sizes to curved measurements were made with regression equations developed

by Teas (1993). Kemp's ridley turtles larger than 58.8

cm SLCL (Marquez-M, 1994) or 62.1 cm CCL [derived with Teas (1993)], loggerhead turtles larger

than 90.0 cm SLCL (Teas]) or 96.5 cm CCL [derived

with Teas (1993)], and leatherback turtles larger than

125.0 cm SLCL (Marquez-M, 1990) were classified as

adults. Turtles were considered juveniles or sub-adults

when they were larger than hatchlings/post-hatchlings

hut smaller than adults. The sexes of adults were determined during necropsies.

I Teas, Wendy. 1994. Miami Laboratory, Southeast Fisheries Science

Center, NMFS, 75 Virginia Beach Drive, Miami, FL 33149. Personal

conlnlUIl.
___________________ Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 59

Necropsies and Digestive Tract

Contents, 1994 32°00·_---..,....---_r_-~-_r_--__;n_---_r__r_,

Live stranded turtles were taken to various

rehabilitation facilities in Texas. From 1980

through 1993, some of the dead stranded

turtles were salvaged for later necropsy or

use in conjunction with foraging ecology

studies (Heinly et al., 1988; Shaver, 1991;

Plotkin et al., ] 993), and the remaining

turtles were either marked, buried, or pulled

behind the dunes. During 1994, only dead

turtles that were extremely decomposed or

found in remote locations were marked, buried, or pulled behind the dunes. All turtles

that died during rehabilitation and most of

the dead stranded turtles that were not highly

deteriorated were salvaged for necropsy and

study during 1994.

General necropsies, similar to those described by Wolke and George (198]), were

performed by a limited number of STSSN

participants and veterinarians. During

necropsy, the sex of the turtle was determined by visual examination ofthe gonads. Most necropsies of the turtles that stranded during 1994 were conducted either at the National Marine Fisheries Service

Laboratory in Galveston, Texas, or at the Padre Island

National Seashore in Corpus Christi, Texas.

At Padre Island, I necropsied 142 stranded turtles

found along the lower Texas coast during 1994, including 59 loggerhead, 47 Kemp's ridley, 3] green, 4 hawksbill, and 1 leatherback turtle. When possible, I removed

the entire digestive tract from each turtle. The contents

were either frozen for later examination or immediately examined. The items ingested by the 37 Kemp's

ridley turtles were identified, categorized into seven

general food groups, baked in a drying oven, and

weighed according to procedures outlined by Shaver

(1991) .

Statistical Analyses

Data were subjected to the Kolmogorov-Smirnov normality test and Bartlett's test for homogeneity of variances before statistical analyses were performed. In all

analyses, differences were considered significant at

P<0.05. SIGMASTAT (1992) statistical software package was used for all statistical procedures. Means are

followed by ± one standard error.

The annual numbers ofstranded turtles located during the Texas Closure in 1981-94 were compared with

the annual n umbers of stranded turtles located during

the same length of time, before and after the closure, in

Texas

11

16 15

Gulf of Mexico

Figure 1

Texas and Shrimp Statistical Zones.

those years. Because the numbers of turtles fuund

stranded before, during, and after the Texas Closure

were not normally distributed (P<O.OO]), non-parametric Kruskal-Wallis one way analyses of variance on ranks

were used to compare the median number of turtles in

each group and Student-Newman-Keuls all pairwise

multiple comparisons tests were used to isolate which

groups differed from the others. Tests were repeated

excluding years when large numbers ofturtles stranded

as a result of identified sources other than incidental

capture in shrimp trawls.

I used t-tests to compare the mean numbers of

stranded turtles found per day in offshore and inshore

waters and during closure and non-closure periuds in

198]-94, and non-parametric Mann-Whitney rank sum

tests to compare the median values of the groups when

the assumptions for parametric tests (normality and

equal variance) were violated. I used t-tests and MannWhitney rank sum tests to compare the percentages uf

stranded turtles that were located in offshore and inshore areas during closure and non-closure periods in

1981-94. Both set of tests were repeated excluding

years when large numbers of turtles stranded as a result

of identified sources other than incidental capture in

shrimp trawls.

SLCL's ofstranded Kemp's ridley turtles found along

the upper, middle, and lower Texas coast between 1980

and 1994 were compared. SLCL's of individuals for

which only CCL's were available were derived with Teas

(1993). Because Kemp's ridley SLCL's were not normally distributed (p':;O.05), non-parametric Kruskal-
60 NOAA Technical Report NMFS 143 _

Wallis one way analyses of variance on ranks were used

to compare median SLCL's of each group and Dunn's

method all pairwise multiple comparisons tests to isolate which groups differed from the others. MannWhitney rank sum tests were used to compare median

SLCL's of Kemp's ridley turtles stranded inshore and

offshore along the upper, middle, and lower Texas coast.

SLCL's of all species stranded during 1994 were compared using non-parametric tests since SLCL's for each

species were not normally distributed (P<0.05). A

Kruskal-Wallis one way analysis of variance on ranks was

used to compare median SLCL's among the species

and a Dunn's method all pairwise comparisons test was

used to isolate which species differed from the others.

I compared the SLCL's, digestive tract content

weights, percent dry masses of crabs, and percent dry

masses offishes in the digestive tracts of37 wild Kemp's

ridley turtles that stranded in 1994 and 50 that stranded

from 1983 to 1989 (Shaver, 1991). Because all four of

the variables failed normality tests (P<O.OOI), I used

non-parametric Mann-Whitney rank sum tests for the

comparisons.

Results

Strandings, 1980-94

From 1980 to 1994, 3,283 stranded sea turtles, including

1,139 (34.7%) Kemp's ridley, 1,524 (46.4%) loggerhead,

258 (7.9%) green, 170 (5.2%) hawksbill,57 (1.7%) leatherback, and 135 (4.1 %) unidentified turtles, were located

along the Texas coast. An additional 252 head-started

Kemp's ridley and 10 head-started loggerhead turtles were

documented but excluded from further analyses.

Three hundred fifty-four (10.8%) of the 3,2H3

stranded turtles were alive and 2,929 (89.2%) were

dead when located. Species composition varied by year;

Kemp's ridley turtles comprised an increasing percentage of the strandings throughout time (Fig. 2A). The

most abundant species found during February was the

green turtle whereas Kemp's ridley and loggerhead

turtles predominated during other months of the year

(Fig.3A).

Of the 3,283 stranded turtles, 2,876 (87.6%) were

located in offshore, 401 (12.2%) in inshore, and 6

(0.2%) in unknown areas (Figs. 2C, 3C). Species composition varied in offshore and inshore areas. The 2,R76

turtles found in offshore areas included 982 (34.1 %)

Kemp's ridley, 1,451 (50.5%) loggerhead, 124 (4.3%)

green, 155 (5.4%) hawksbill, 54 (1.9%) leatherback,

and 110 (3.8%) unidentified turtles. The 401 found

inshore included 156 (38.9%) Kemp's ridley, 72 (18.0%)

loggerhead, 132 (32.9%) green, 13 (3.3%) hawksbill,:3

(0.7%) leatherback, and 25 (6.2%) unidentified turtles.

Most strandings occurred between March and November (Fig. 3C). Strandings decreased during June.

During 1981-94, with and without the excluded years,

the numbers of stranded turtles located during the

Texas Closure were significantly different from the numbers located during the same length of time, before

and after the closure (Table 1). Fewer turtles were

located during the closure than before and after it.

Additionally, fewer were located after the closure than

before it. However, the numbers of stranded turtles

located in inshore areas during the Texas Closure were

not significantly different from the numbers located in

inshore areas during the same length of time, before

and after the closure (Table 1).

During 19RI-94, with and without the excluded years,

fewer stranded turtles were found per day during the

Texas Closure than during the remainder of the year,

when Gulf of Mexico waters were open to shrimp trawling (Table I). Fewer stranded turtles were found per

day in offshore areas during the Texas Closure than in

offshore areas during the remainder of the year. However, the number of stranded turtles found per day in

inshore areas during the Texas Closure and during the

remainder of the year did not differ.

Fewer stranded turtles were found per day in inshore

areas than in offshore areas when Gulf waters were

open to shrimping, during 1981-94 (Mann-Whitney,

7~105, N(small)=14, N(big)=14, P<O.OOI) and during

1981-94 with years 1986, 1989, and 1990 excluded

(Mann-Whitney, 7~66, N(small)= ll, N(big)=l 1,

P<O.OO I). Similarly, fewer turtles were found stranded

per day in inshore areas than in offshore areas during

the Texas Closure from 1981-94 (t-test, t=-4.012, df=26,

P<O.OOl) and during 1981-94 with years 1986, 1989,

and 1990 excluded (t-test, t=-3.609, df=20, P=0.002).

The percentage of stranded turtles located in offshore areas during the Texas Closure was not significantly different from the percentage located in offshore areas during the remainder of the year during

1~81-~4 (Mann-Whitney, 7=189, N(small)=14, N(big) =14,

P=0.534) and during 1981-94 with years 1986, 1989,

and 19~0 excluded (Mann-Whitney, 7=125, N(small)=l 1,

N(big)=11, P=0.947). However, during 1990-94 (the only

years when all Gulf of Mexico waters off Texas were

closed to shrimp trawling out to 322 km) the percentage ofstranded turtles located in offshore areas during

the Texas Closure was smaller than the percentage

located in offshore areas during the remainder of the

year (I-test, 1=4.261, df=8, P=0.003).

The percentage of strandings in inshore areas was

greatest during January, February, and June (Fig. 3C).

The percentage of stranded turtles located in inshore

areas during the Texas Closure was not significantly

different from the percentage located in inshore areas

during the remainder of the year for 1981-94 (Mann-
600

0 Lepidochelys kempii

[] Caretta caretta 500

• Chelonia mydas

III Other

400

l/l

::l

'tl .:; 300

'6

.!:

-

0

Ql 200

.0

E

::l

Z

100

Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 61

A

Figure 2

Annual number of stranded sea tunics

found along the Texas coast from 1980-94

by (A) species, (B) region, and (C) area.

Species include Kemp's ridley, I_epidochelys

kempii, loggerhead, CaTella carella, green,

Chelonia mydas, and other (hawksbill,

t;utmochelysimbricata, leatherback, DermochRlys

coriacea, and unidentified species turtles comhined). Regions include upper Texas coast

(Zones 17, 18), middle Texas coast (Zone

19), and lower Texas coast (Zones 20, 21) .

Areas include inshore and offshore.

600

0 Upper Texas Coast B

0 Middle Texas Coast 500

• Lower Texas Coast

400

l/l

::l

'tl

:~ 300

'tl

t:

'0

:u 200 .0

E

::l

Z

100

600

500

l/l 400

::l

'0.:;:

'6

t: 300

'0

:u.0

E 200 ::l

Z

100

1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994

YEAR
62 NOAA Technical Report NMFS 143 700---,-- ---,

Figure 3

Monthly number of stranded sea turtles

found along the Texas coast from 1980-94

by (A) species, (8) region, and (C) area.

Species include Kemp's ridley, f,epidochelys

kempii, loggerhead, Carella carella, green,

Chelonia mydas, and other (hawksbill,

l':retmochelys iml7ricata, leatherback, Dermochelys coriacea, and unidentified species

turtles com bined). Regions include upper

Texas coast (Zones 17, 1R), middle Texas

coast (Zone 19), and lower Texas coast

(Zones 20, 21). Areas include inshore and

offshore.

600

500

(/)

iii

:I

-0"S: 400

:0

.!:

"5 300

Q;

.0

E

:I

Z 200

'00

A 0 Lepidochelys kempii

flIl Caretta caretta

• Chelonia mydas

III Other

700

B

600

500 (/)

iii

:I

-0

:~ 400

-0

.S

'0

Qj 300

.0

E

:I

Z 200

'00

o Upper Texas Coast

EJ Middle Texas Coast

• Lower Texas Coast

700

e Inshore

600

500

(/)

iii

:I

-0.;; 400

:0

.!:

....

0

Q; 300

.0

E

:I

Z 200

100

Jan. Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec.

MONTH
Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 63

Whitney, T=189, N(small)=14, N(big)=14, P=0.534) and

for 1981-94 with years 1986,1989, and 1990 excluded

(Mann-Whitney, T=125, N(small)=ll, N(big)=ll,

P=0.947). However, inshore strandings comprised an

increasing percentage of the strandings, particularly

during the Texas Closure, throughout time (Figs. 2C,

3C). Additionally, during 1990-94, the percentage of

stranded turtles located in inshore areas during the

Texas Closure was larger than the percentage located

in inshore areas during the remainder of the year (ttest, t=-4.621, df=8, P=0.002).

Strandings were distributed throughout the state; 52

(1.6%) were in Zone 17,939 (28.6%) in Zone 18, 548

(16.7%) in Zone 19, 1,327 (40.4%) in Zone 20, 415

(12.6%) in Zone 21, and 2 (0.1%) in unknown areas

(Figs. 2B, 3B). Grouping strandings into regions of the

Texas coast, 991 (30.2%) occurred on the upper Texas

coast, 548 (16.7%) on the middle Texas coast, and 1,742

(53.1 %) on the lower Texas coast. Strandings per region

varied for different years and months (Figs. 2B, 3B).

More stranded Kemp's ridley turtles were located

along the upper Texas coast (613), than the middle

Table I

Test 1: Kruskal-Wallis one way ANOVA on ranks to compare the number of stranded turtles found during the Texas

Closure (DC) versus the number found during the same number of days before the closure (BC) and after the closure

(AC), followed by Student-Newman-Keuls method all pairwise multiple comparisons to isolate which groups differ. Test 2:

Mann-Whitney rank sum tests to compare the number of stranded turtles found per day during the Texas Closure (C)

versus the number found per day during the remainder of the year (0). Median numbers found during BC, DC, AC, C,

and 0 are in parentheses. * designates significant difference, P<O.05.

Areas and years

All waters, 1981-94

BC (52.0) vs. DC (18.5) Test 1

DC (18.5) vs. AC (42.5) Test 1

BC (52.0) w.AC (42.5)TeMl

C (0.390) vs. 0 (0.555) Test 21

All waters, J981-94 (exclusions) 2

BC (47.5) \'5. DC (18.0) Test 1

DC (18.0) vs. AC (36.5) Test 1

BC (47.5) vs. AC (36.5) Test 1

C (0.380) vs. 0 (0.520) Test 2

Offshore waters, 1981-94

BC (50.0) vs. DC (13.5) Test J

DC (13.5) vs. AC (33.5) Test I

BC (50.0) vs. AC (33.5) Test 1

C (0.245) vs. 0 (0.485) Test 2

Offshore waters, 1981-94 (exclusions)2

Be (47.5) \'s. DC (12.5) Test 1

DC (12.5) vs. AC (29.5) Test 1

BC (47.5) vs. AC (29.5) Test 1

C (0.240) vs. 0 (0.430) Test 2

Inshore waters, 1981-94

C (0.050) vs. 0 (0.060) Test 2

Inshore waters, 1981-94 (exclusion)3

C (0.040) vs. 0 (0.030) Test 2

Test statistic

H=16.43

q=5.708

q=4.938

q=3.574

H=J4.05

q=5.288

q=4.368

q=3.511

H=20.883

q=6.449

q=5.247

q=4.370

H=17.871

q=5.97"1

q=4.572

q=4.327

H=0.464

Test J

df

2

2

2

2

p

<0.001 *

<0.05 * <0.05 *

<0.05 *

<0.001 *

<0.05 * <0.05 *

<0.05 *

<0.001 *

<0.05 * <0.05 * <0.05 *

<0.001 * <0.05 *

<0.05 * <0.05 *

0.793

Test statistic

1'=145

T=142

1'=198

1'=178

Test 2

,V(small), N(big)

14,14

11,11

14,14

11, II

14,14

13,13

p

0.008 "

0.021 *

0.005 "

0.025 *

0.835

0.918

1 Results for each Test 2 are presented across from the preceding group heading.

2 For Test 1, years 1986 and 1990 were excluded because large numbers of tunles stranded in offshore waters as the result of identified

sources other than incidental capture in shrimp trawls (see Discussion) during the comparison dates. For Test 2, years 1986 and 1990

were excluded because of the preceding reasons and 1989 was excluded because large numbers of lUnles stranded in inshore waters as

the result of identified sources other than incidental capture in shrimp trawls, during dates not encompassed in Test 1.

3 Test 1 was not conducted because no exclusions were necessary (no large numbers of tunles stranded in inshore waters as the result of

identified sources other than incidental capture in shrimp trawls during the comparison dates). For Test 2, year 1989 was excluded

because large numbers of turtles stranded in inshore waters as the result of identified sources other than incidental capture in shrimp

trawls, during dates not encompassed in Test 1.
64 NOAA Technical Report NMFS 143

Table 2

Straight-line carapace lengths (em) ofstranded Kemp's ridley turtlcs, [,epidochelys kernpii, found on the Texas coast during

1980-94. Statistical comparisons of the lengths of these individuals are summarized in Table 3.

All indi"idual, , 0 individuals < 10.0 cm SLCL

Area Mean (I':, SE) Code l Mean (N,SE) Code

Overall (offshore and inshore areas) .\ D

Cpper Texas coast 37.4 (527,0.5) 1 37.5 (525,0.5) 10

Middle Texas coasl 47.6 (151, 1.~) 2 48.2 (149, 1.2) 11

I.ower Texas coast 38.2 (317,1.2) 3 48.0 (244,O.Y) 12

Offshore waters B E

Cpper Texas coasl 37.5 (493,0(,) 4 ~7.6 (491,0.6) 13

Middle Texas coast 51.6 (ill,16) 5 52.8 (79,1.4) 14

Lower Texas coast 37.8 (294, 1.3) 6 48.6 (221, 1.0) 15

Inshore walers C F

Cpper Texas coast 35.il (33.1.8) 7 358 (33, 1.8) 16

Middle Texas coast 43.0 (70, 1.7) 8 43.0 (70, 1.7) 17

Lower Texas coast 43.1 (23,30) 9 43.1 (23,3.0) 18

1 Each leuer code designates a subset of the strandings thaI is comprised of the three geogTaphical areas, designated by number codes,

listed below it.

350 -,---------------------------------,

Figure 4

Straight-line carapace lengths (SLCl.'s) of stranded Kemp's ridley

Lepidochelys kernfii, found on the Texas coast from 19S0-94 (N=1,l39).

turtles,

70.U - 79.9

• Lower Texas Coast

o Upper Texas Coast

o Middle Texas Coast

SO.O - 59.9 60.0 - 69.9

SLCL

20.0 - 29.9 30.0 - 39.9 ~O.O· '-9.9

than those located along the upper Texas coast.

Stranded Kemp's ridley turtles found in inshore areas

along the middle Texas coast were significantly smaller

than those found in the offshore areas. However, those

found in inshore areas along the upper and lower Texas

0.0 - 9.9 10.0·19.9

;0

100

250

300

"-o

ISO

J:).

E

:l

Z

OJ'"

:l

"t:l

.~ 20u

:;

.:

(185) or lower (341) Texas

coast. Although more Kemp's

ridleys were located stranded

in offshore areas along the upper Texas coast (570) than in

offshore areas along the middle

(100) and lower (312) Texas

coast, more were found in inshore areas along the middle

Texas coast (85) than the upper (42) and lower (29) Texas

coast.

The size of stranded Kemp's

ridley turtles varied in the state

(Tables 2, 3). The smallest individuals, hatchlings/posthatchlings, were located almost

exclusively along the lower

Texas coast. From] 980 to 1994,

73 were found on the lower

Texas coast, 2 on the upper

Texas coast, and 2 on the

middle Texas coast (Fig. 4).

Stranded Kemp's ridley turtles

located in offshore areas and

overall (offshore and inshore

areas collectively) along the

middle Texas coast were significantly lalger than those

located in the areas along the uppel- and lower Texas

coast (Tables 2, 3). However, with hatchlings and pOSthatchlings excluded, Kemp's ridley turtles from the

middle and lower Texas coast were significantly larger
Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 65

Table 3

Kruskal-Wallis one way A OVA on ranks, Dunn's method all painvise multiple compari ons, and Mann-Whitney rank sum

tests used to compare median straight-line carapace lengths of stranded Kemp's ridley turtles found on the Texas coast

from 1980-94; * designates significant difference, P<0.05. SLCL group codes are presented in Table 2.

Codes

A

B

C

D

E

F

1 vs. 2

2 vs. 3

I vs. 3

4 vs. 5

5 vs. 6

4 vs. 6

7 vs. 9

10 vs. 11

II vs. 12

10 vs. 12

13 vs. 14

14 vs. 15

13 vs. 15

16 vs. J8

4 vs. 7

5 vs. 8

6 vs. 9

13 vs. 16

14 vs. 17

15vs.lR

Test

Kruskal-Wallis

Kruskal-Wallis

Kruskal-Wallis

Kruskal-Wallis

Kruskal-Wallis

Kruskal-Wallis

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's methud

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Dunn's method

Mann-Whitney

Mann-Whitney

Mann-Whitney

Mann-Whillley

Mann-Whitney

Mann-Whitney

Test statistic

11;51.611

11;51.268

11;8.572

11;111.700

11;116.600

11;8.572

Q=7.1ti4

Q=5.156

Q=2.156

Q=7160

Q=5917

Q= 1.572

Q=2.276

Q=tiOOO

Q=0.602

Q=8.777

Q=8.232

Q=2.334

Q=8.543

Q=2.276

T=R419

T;4417

T;3953

T;R353

T;4277

T=2274

dfor N

df;2

df;2

df;2

df;2

df;2

df;2

N=33, N=493

N=70, N=81

N=23, =294

N;33, N;49J

N;70, i -79

N=23, N;221

p

<0.00 I *

<0.00 I *

0.014*

<0.001 * <0.00 I*

0.014*

<0.05*

<0.05*

>0.05

<0.05*

<0.05*

>0.05

>0.05

<0.05*

>0.05

<0.05*

<0.05*

>0.05

<0.05*

>0.05

0.744

<0.00 I*

0.485

0.714

<0.00 I*

0.092

Table 4

Stranded sea turtles found on the Texas coast during 1994.

May May

Species Jan. Feb. Mar. Apr. 1-14 15-31 June July Aug. Sep. Oct. ov. Dec. Total

Lepidochelys kempii (Kemp's ridley turtle) 0 2 I 54 64 12 19 32 35 10 11 11 3 254

Carella carella (Loggerhead turtle) 3 1 5 41 15 9 8 57 23 11 6 9 6 194

Chelonia mydas (Green turtle) 0 0 2 R 3 3 3 8 2 5 3 7 4 48

Eretmochelys imbricata (Ilawksbill tunle) 0 0 0 0 1 0 2 I 2 7 0 0 1 14

Dermochelys c01"iacea (Leatherback turtle) 0 0 0 1 2 0 0 0 0 0 0 0 0 3

Unknown 0 0 0 J I 2 2 :l 2 2 0 0 J 14

Total 3 3 R 105 86 26 34 101 64 35 20 27 15 527

coast were only slightly smaller than those found In

offshore areas there.

Strandings, 1994

Along the Texas coast, 527 wild sea turtles were found

stranded during 1994 (Table 4), only 14 fewer than the

number stranded during the years ] 991, 1992, and

1993 combined (541) and more than during any previous year on record for the Texas STSSN (Fig. 2A-C).

Previous yearly totals ranged from 83 in 1980 to 358 in

1990. During 1994, monthly stranding totals for April,

May, June, July, and August (Table 4) exceeded numbers previously documented during those months for

all years of record. Although 33 head-started Kemp's

ridley turtles and 2 head-started loggerhead turtles were

also documen ted stranded during 1994, these turtles
66 NOAA Technical Report MFS 143

60-.,-------------r- ...,.- -----,

Figure 5

Weekly number of stranded sea turtles found on the Texas coast during 1994 by

(A) region and (B) area. Regions include upper Texas coast (Zones 17, 1R),

middle Texas coast (Zone 19), and lower Texas coast (Zones 20, 21). Areas

include inshore and offshore.

increases were also detected aJong the

upper Texas coast. Although

strandings decreased along the

lower Texas coast by early May,

they continued at high levels

along the upper Texas coast until 14 May. Strandings abruptly

decreased and remained at relatively low levels throughout the

state until 10 July (week 28),

when another peak was detected. Strandings during the

July peak were concentrated

in the Galveston, Matagorda

(middle Texas coast), and Mustang island areas. Although

strandin~sdecreased during late

July (week 30), another peak

occurred during late August

(weeks 34-35). Most of the

turtles documented during the

August peak were found in the

vicinity of Galveston Island.

Strandings remained at relatively

low levels dwing the last 4 months

of the year (weeks 36-52).

Of the 527 strandings, 463

were documented from offshore areas, 63 from inshore

areas, and 1 from an unknown

area (Fig. 5B). From 15 May

through 9 July (weeks 20-27),

27% of the strandings were

documented from inshore areas, compared with only 10%

from inshore areas during

other times of the year.

Species composition of the

527 stranded turtles included

254 Kemp's ridley, 194 loggerhead, 48 green, 14 hawksbill, 3

leatherback, and 14 of unknown species (Table 4). Fortyeight percent of the turtles

found were Kemp's ridley, the

highest percentage of this species recorded for Texas in

STSSN history (Fig. 2A).

B

A

Oct. Nov. Dec.

Strandings increased dramatically during early April

(week 14) and continued at high levels through mid May

(week 19) (Fig. 5A, B). From April through mid May,

strandings were concentrated on Galveston (upper Texas

coast), Mustang (lowerTexas coast), and North Padre (lower

Texas coast) islands. Increases in strandings were first

detected along the lower Texas coast in early April. About

one week later,

Feb. Mar. Apr. May June July Aug. Sept.

o Upper Texas Coast

IIIl Middle Texas Coast

• Lower Texas Coast

D Texas Closure

1234567891111111111222222222233333333334444444444555

0123456789012345678901234567890123456789012

WEEK

Jan.

50

10

UI

iii 40 ::J

"t:l .:;

:a

.!: 30

'0

...

Q)

.0

E

::J 20 Z

60

D Inshore

• Offshore 50

D Texas Closure

UI

iii 40

::J

"t:l .:;

:a

.!: 30

-

0

Qj

.0

E 20 ::J

Z

10

were not included in stranding totals and analyses presented herein.

Ofthe 527 strandings, 219 (41.5%) were located on the

upper Texas coast, 101 (19.2%) on the middle Texas

coast, and 207 (39.3%) on the lower Texas coast (Fig. 5A).

For those located in the upper Texas coast, 13 were from

Zone 17 and 206 from Zone 18. Lower Texas coast strandings included 157 from Zone 20 and 50 from Zone 21.
Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 67

Table 5

Straight-line carapace lengths (SLCL's) (cm) of stranded sea turtles found on the Texas coast during 1994.

Species Mean N SE Median Range Code'

I.epidochelys kempii (Kemp's ridley turtle) 39.0 192 0.9 35.2 4.5-66.6 1

Caretta caretta (Loggerhead turtle) 65.7 157 1.2 66.1 5.2-101.3 2

Chelonia mydas (Green turtle) 32.4 38 1.2 30.3 23.7-60.9 3

Fretmochelys imbricata (Hawksbill turtle) 12.8 1] 2.2 9.7 5.3-26.2 4

Dennochelys wriacea (Leatherback turtle) 2 134.2-138.0

I *designates significant difference, P<0.05. Median SLCL's of species (codes 1-4) are different (Kruskal-Wallis one way ANOYA on

ranks, H;217.400, df;3, P<0.001 *). Dunn's method all pairwise multiple comparison: 1 vs. 2, 0' 12.408, P<0.05*; 2 vs. 3, 0'9.642,

P<0.05*; 2 vs. 4,0'8.013, P<0.05*; 1 vs. 4,0'3.731, P<0.05*; 1 vs. 3, 0'2.269,1'>0.05; 3 vs. 4,0'2.202, P>0.05.

Of the 527 stranded turtles, 490 were found dead and

37 alive. The 37 live stranded turtles included 7 Kemp's

ridley, 5 loggerhead, 14 green, 10 hawksbill, and 1

unidentified species. Only 3% of the stranded Kemp's

ridley and loggerhead turtles were found alive. However, 29% of the green and 71 % of the hawksbill turtle

strandings were of live individuals. Of the 37 turtles

found alive and taken to various rehabilitation facilities

in Texas, 15 died, 11 were rehabilitated and released,

and 11 were held for prolonged rehabilitation.

Most of the live Kemp's ridley and loggerhead (9 of

12) died during rehabili tation efforts, whereas most

live green and hawksbill turtles (18 of 24) were successfully rehabilitated and released or are still being held.

Most of the stranded Kemp's ridley turtles were subadults (Table 5, Fig. 6). Other Kemp's ridley turtles

found included 29 adults (including five males, nine

females, and 15 of unknown gender), four hatchlings/

post-hatchlings, and a few juveniles. Among the nine

adult females, four possessed tags that were placed on

them at the nesting beach in Rancho Nuevo, Mexico,

and one contained 39 eggs. Similarly, most loggerhead

turtles were sub-adults. However, nine adults (including one male, one female, and seven of unknown gender), two hatchlings/post-hatchlings, and a few juveniles were also found. Green turtles found were juveniles and sub-adults. Seven of the stranded hawksbills

were post-hatchlings, and the other seven were juveniles.

Both leatherbacks measured were adults (including one

female and one of unknown gender). Stranded loggerhead turtles were significantly larger than stranded Kemp's

ridley, green, and hawksbill turtles (Table 5).

According to STSSN forms, four ofthe stranded turtles

had ingested hooks, four were found alive lodged in

rocks, 24 had boat propeller injuries, 13 were entangled

in marine debris, 12 had been bitten by sharks, and 20

had straight-edged cuts at the bases of missing appendages, typical of human-inflicted mutilation (Heinly et

aI., 1988). In most instances the STSSN participant

could not determine whether the bites and mutilation

occurred before or after death. Two dead green turtles

were found in abandoned illegal gill nets offshore from

the southern end of Padre Island National Seashore.

Eleven turtles were found with water coming out of the

mouth or froth in the trachea.

Necropsies have been completed [or all of the

stranded sea turtles that were salvaged during 1994.

The deteriorated condition of most of the salvaged

turtles prohibited conclusive determination of the cause

of death in most instances. Although marine debris was

found in several of the turtles necropsied, in most instances the amounts were minimal and were probably

not the cause of stranding or death. Only a few of the

turtles found stranded were apparently ill for an extended period prior to their demise, as evidenced by

emaciation, encrustation with epizoans, large quantities of internal parasites, or lack of appreciable quantities o[ ingested food items.

Kemp's Ridley Digestive Tract Content Analyses

None of the 37 wild Kemp's ridley turtles analyzed for

digestive tract con ten ts from 1994 appeared to have

been ill prior to death. Gut contents were present in all

individuals analyzed, indicating recent foraging. Gut

con ten t weigh ts from the 1994 Kemp's ridley turtles

were significantly greater than weights from the 1983-

89 Kemp's ridley turtles (Mann-Whitney, 1'=1900,

N(small)=37, N(big)=50, P=0.020), even though there

was no significant difference between SLCL's of the two

groupings (Mann-Whitney, 1'=1744, N(small)=36,

N(big)=50, P=0.120).

Turtles from the 1983-89 and 1994 groupings had

similar percent dry mass of the seven food categories

(Table 6). Crabs composed 95% ofthe dry mass in both

groups of ridleys. There was no significant difference

between the percent dry mass of crabs between the two

groups (Mann-Whitney, 1'=1716, N(small) =37, N(big)=50,

P=0.451). Fish were consumed by 24% of the 1994
68 NOAA Technical Report NMFS 143

90-99 100-109

Prior to the adoption of regulations requiring the usage of TED's, correlations were found between

shrimping effort and strandings of sea turtles in Texas

CWhistler, 1989; Caillouet et aI., 1991; Sis et aI., 1993).

Magnuson et al. (1990) estimated that 70-80% of the

turtles stranded during the shrimping season in Texas

were caught and killed in shrimp trawls and that as

many as 44,000 turtles were killed annually by shrimp

trawls in U.S. coastal waters of the Atlantic Ocean and

the Gulf of Mexico. Magnuson et al. (1990) also concluded that incidental capture of sea turtles in shrimp

trawls was the major cause of mortality associated with

human activities and resulted in the death of more sea

turtles than all other human activities combined.

Beginning in 1990, TED's were phased into mandatory usage, in an attempt to reduce trawl-related mortality. Documented turtle strandings in Texas decreased

during 1991, ]992, and 1993.

However, the pattern of higher

numbers of strandings before

and after the Texas Closure

and reduced strandings during

the closure (Magnuson et aI.,

1990) continued and more

turtles were found stranded

during 1994 than during any

previous year on record for the

Texas STSSN.

Comparisons of stranding

numbers among years must be

qualified. Varying effort was

made to detect turtles between

] 980 and ] 994 and stranding

totals for some years were

skewed by events such as hatchling/ post-hatchling strandings

and hypothermic stunnings.

When these conditions are considered, the relative number of

turtles found stranded during

1994 is even more substantial.

Numbers detected during

the early 1980's were probably

low because the STSSN was not

fully operational at that time

(Whistler, 1989). The two preDiscussion

89 group, marine debris composed less than 0.1 % of

the total gut content dry mass for the two groups (Table

6). Only minute amounts of debris were found, and in

no instance did it appear that ingestion of marine debris led directly to the demise of the animal.

50·59 60 - 69 70·79 80 - 89

SLCL(CMJ

00-09 10 - 19 20 - 29 30 - 39 40 - 49

o Carelta carelta

- • Lepidochelys kempii

o Chelonia mydlls

-

-

-

-

-

,-

,. I I

,- I

I h Ih

I

h

I I

n In I

10

20

70

60

80

Figure 6

Straight-line carapace lengths of stranded loggerhead turtles, Carella carella,

(N=153), Kemp's ridley turtles, Lepidochelys kempii, (N=192), and green turtles,

Chelonia mydas, (N=38) found on the Texas coast during 1994.

'I>

'"

::l 50

"0.;;:

:;;

.5 40 .... o

...

'"E 30

::l

Z

Table 6

Percent dry mass and percent frequency offood groups

found in digestive tract contents of wild Kemp's ridley

turtles, Lepidochelys kempii, from south Texas during

1983-89 (N=50; Shaver, 1991) and 1994 (N=37).

Percent dry mass Perccn t frequency

Item 1983-89 1994 J9il3-89 1994

Crabs 95.22 95.56 80.00 83.7R

Mollusks 1.56 1.62 58.00 89.19

Fishes 0.08 0.72 14.00 24.32

Vegetation 0.14 0.21 56.00 54.05

Shrimp O.IR 0.02 4.00 8.JJ

Other materials 2.74 1.82 72.00 67.57

Marine debris 0.08 0.05 34.00 18.92

ridleys compared with 14% of those from 1983-89.

However, fishes composed less than 1% of the total gut

content mass for the 1983-89 and 1994 Kemp's ridley

turtles (Table 6), and no significant difference was

found in the percent dry mass of fishes between the two

groups (Mann-Whitney, T=1742, N(small)=37, N(big)=

50, P=0.313).

Although marine debris was ingested by 19% of the

1994 Kemp's ridleys compared with 34% by the 1983-
___________________ Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 69

vious years of most numerous strandings in Texas were

1986 (349) and 1990 (358). Systematic surveys to locate

stranded turtles were most comprehensive during the

period 1986-90. Additional, undetected turtles probably stranded on the Matagorda Peninsula and San Jose

Island during 1994 because numerous strandings were

documented in adjacent areas receiving more comprehensive STSSN coverage.

More hatchling and post-hatchling sea turtles were

found stranded along the Texas coast during 1986 (25)

and 1990 (53) than during any other years of the STSSN

(Shaver, 1992). Forty-seven of the 257 turtles found

stranded during 1989 were located during or shortly

after periods of freezing temperatures and were probable victims of hypothermic stunning (Shaver, 1990a).

In contrast, only 13 hatchling/post-hatchling turtles

and no hypothermic-stunned turtles were found

stranded during 1994.

Comments listed on STSSN forms revealed possible

causes for strandings of 47 of the 527 turtles found

during 1994, including boat propeller injuries (24),

debris entanglement (13), hook ingestion (4), entanglement in abandoned illegal gill netting (2), and being

lodged in rocks (4). Although 11 turtles were found

with water coming out of the mouth and or froth in the

trachea, this condition has been disputed as conclusive

evidence of drowning. Based on necropsies, illness and

marine debris ingestion probably caused stranding of

relatively few of the 527 turtles. Thus, no readily

discernable cause was identified for most strandings

from the STSSN forms and necropsies.

Several other possible causes for the strandings were

suggested and investigated but were dismissed because

of lack of supportive evidence (Shaver, 1994b;

Zimmerman2). Among the unlikely contributing factors proposed were seismic exploration, oil and gas

platform removal, menhaden fishing, anoxia (low water oxygen), poilu tan ts, toxic wastes, dinoflagellate

blooms, and ingestion of fish killed by any of the preceding factors.

A large percen tage of the 1994 strandings was probably due to incidental capture in shrimp trawls. Stranding patterns closely followed nearshore shrimping patterns (Zimmerman2). When shrimping activity increased

along the Texas coast during April and boats were most

numerous in nearshore waters off Galveston, Mustang,

and North Padre islands, strandings were most numerous in those areas. Strandings and nearshore shrimping

effort were relatively low for the Matagorda Island area

during April and for the North Padre Island area from

May through the remainder of the year.

2 Zimmerman, Roger. 1994. Galveston Laboratory, Southeast Fisheries Science Center, NMFS, 4700 Ave. U, Galveston, 'IX 77551.

Personal commun.

Strandings greatly decreased from 13 May to 7 July,

when Gulf waters were closed to shrimping activities

out to 322 km for the Texas Closure. When shrimping

resumed in Gulf waters, large numbers of turtles were

found stranded. Strandings at that time ~ere concentrated in the Galveston, Matagorda, and Mustang island

areas, where nearshore shrimping effon was high.

The apparent relationship between strandings and

TED enforcement activities also supports the theory

that many of the 1994 strandings were due to shrimping

activity. In the latter part ofJuly (week 30), when intensive TED enforcement and education activities occurred

and nearshore shrimping effort decreased, strandillgs

decreased. However, strandings increased again during

late August (weeks 34-35), when TED enforcement

activities decreased because U.S. Coast Guard enforcement personnel were shifted to Florida to deal with the

Cuban refugee crisis. Strandings immediately decreased

when TED enforcement activities increased during early

September (week 36). Enforcement activities continued during September and strandings remained at relatively low levels for the rest of the year.

Operational or installation problems with TED's probably resulted in a large number of the strandings during 1994. Although 95% of the shrimp vessels inspected

during April 1994 had TED's present in their nets,

operational problems detected with the TED's may have

caused turtles to be retained (Zimmerman2). rnstallation or operational problems were noted in half of the

vessels inspected during mid July (Zimmerman 2).

Turtles may also have stranded as a result of capture

and retention in trawls equipped with TED's since these

devices are only 97% effective at excluding sea turtles

(Zimmerman2). Soft and bottom shooting hard TED's,

used by a large percentage of the shrimp fleet during

1994, may have been even less effective at excluding

turtles (Zimmerman 2). Repeated capture and release

from TED-equipped trawls, capture in trawls with intentionally disabled TED's, and capture in try nets (which

are not required to have TED's) may also have contrihuted to the turtle strandings. The shift of shrimping

effort to nearshore areas may have increased the number of encounters that turtles had with trawlers.

Of the 65 stranded turtles found during the Texas

Closure, 48 were documented from offshore beaches

and 17 from inshore beaches. Many of the 48 found on

offshore beaches may have succumbed prior to the

closure and then may have taken several days to wash

ashore and be detected. Also, some may have stranded

during the closurf' as a result of being weakened by

capture and release from trawls prior to the r:losure.

Incidental capture in shrimp trawls probably resulted

in a large proportion of the offshore and inshore

strandings along the Texas coast from 1980 to 1994.

Nearly 88% of the strandings during this time were
70 NOAA Technical Report NMFS 143

located in offshore areas and a large number of those

were probably due to incidental capture in shrimp trawls.

From 1981 to 1994, fewer turtles were located (overall

and in offshore areas) during the Texas Closure than

before and after the closure. Perhaps fewer were located after the closure than before it because a large

proportion of the resident and transient turtles died

prior to the closure, leaving fewer available to strand

later in the year. Fewer turtles were found stranded per

day (overall and in offshore areas) during the Texas

ClosUl-e than during the remainder of the year, when

Gulf of Mexico waters were open to shrimp trawling,

for the years 1981-94. Additionally, fewer stranded in

offshore areas during June, the only full month of the

Texas Closure, than during all other spring, summer,

and fall months, even though turtles are of equal or

greater abundance during June (Shaver, 1994a).

Inshore shrimp trawling probably resulted in inshore

strandings. During the Texas Closure, shrimp trawling

was permitted in inshore waters, where TED's were not

mandatory until December 1994. During 1990-94, the

only years that all Gulf of Mexico waters off Texas were

closed to shrimp trawling out to 322 km, inshore

strandings comprised 35% of all strandings during the

Texas Closure. Also during these years, the percentage

ofstrandings that were located inshore was higher during the Texas Closure than during the remainder of the

year. During 1994, 27% of the inshore strandings were

found during the 8-week Texas Closure; 27% of the

strandings during the closure were located in inshore

areas compared with only 10% in inshore areas during

other times of the year.

It must be noted that several other factors were identified as causing sea turtles to strand in Texas from 1980

to 1994 (Gitschlag and Renaud, 1989; Whistler, 1989;

Plotkin and Amos, 1990; Shaver, 1990a; Shaver, 1990b;

Caillouet et aI., 1991; Shaver, 1992). Collision with boat

propellers and hypothermic stunning resulted in numerous strandings and continue to be significant threats

to sea turtles in Texas inshore areas.

From 1980-94, sea turtle strandings were distributed

throughout the state, with 991 found along the upper

Texas coast, 548 along the middle Texas coast, and

1,742 along the lower Texas coast. This stranding pattern may reflect greater turtle abundance or mortality

along the lower Texas coast. Alternatively, it may reflect

the variability in detection efforts for the STSSN. During the early 1980's, efforts to detect stranded turtles

were probably greater along the lower Texas coast because the STSS Texas coordinator was based out of

that location. The majority of the middle Texas coast

received Ii ttle systematic coverage to documen tstranded

turtles (except during 1986-89). However, a large portion of the lower Texas coast also received limited coverage. Lastly, the differences in stranding numbers could

reflect differences in offshore beach length between

the three regions. Although offshore beach length is

nearly equal for the middle and lower Texas coast, it is

approximately one-third smaller for the upper Texas

coast.

Only 12% of the strandings were located in inshore

areas from 1980 to 1994. However, inshore areas were

not systematically surveyed for stranded turtles and some

individuals probably were not detected. Inshore

strandings comprised an increasing percentage of the

overall strandings, perhaps reflecting increased abundance or mortality of turtles in inshore areas, or increased reporting ofsea turtles found stranded there. It

is possible that some of the turtles found inshore may

have succumbed in the GulfofMexico and either drifted

inshore or been deposited there intentionally. Similarly, some ofthe turtles killed in inshore areas, particularly near pass entrances, could have drifted into the

Gulf of Mexico and later washed ashore on offshore

beaches.

Stranding records demonstrate the importance to

Kemp's ridley turtles of coastal waters throughout Texas.

Although 35% ofthe stranded turtles documen ted from

19HO to 1994 were Kemp's ridley, this species comprised an increasing percentage of the Texas sea turtle

strandings since the initiation of the STSSN in 1980,

peaking at 48% during 1994.

Kemp's ridleys were found in both inshore and offshore areas, comprising 34% of the offshore strandings

and 39% of the inshore strandings. Although more

Kemp's ridley turtles were found stranded along the

upper Texas coast than along the middle or lower

Texas coasts, those located along the middle and lower

coasts (exclusive of hatchlings and post-hatchlings) were

larger than those along the upper coast. Additionally,

all recent records of Kemp's ridley nests and nesting

emergences in Texas have been located along the lower

Texas coast (Shaver, 1992; Shaver, 1995). Protection of

larger sub-adults and adults is critical for efforts to

increase the critically endangered Kemp's ridley population (Crouse et aI., 1987).

Overall food consumption seemed to be similal- between the 1994 and 1983-89 stranded Kemp's ridley

turtles. Nassanus sp. were found in 14 of the 37 Kemp's

ridleys from 1994 and 11 of the 50 from 1983-89.

Nassanus sp. are scavenging gastropods that feed on

dead and decaying crabs and fish (Fotheringham and

Bruenmeister, 1989). Plotkin et aI. (1993) stated that

the presence of Nassanus acutus in loggerhead gut contents may indicate that the fish and shrimp consumed

by these turtles, which probably could not have captured them alive, were dead when eaten. Presence of

these mollusks in stranded Kemp's ridley turtles may

also indicate consumption of dead food items, such as

those discarded as shrimp trawl by-catch (Shaver, 1991).
Shaver: Sea Turtle Strandings along the Texas Coast, 1980-94 71

Shaver (1991) noted the possibility that Kemp's ridley

turtles inhabiting Texas waters may forage on shrimp

trawl by-catch, as speculated for loggerhead turtles in

Georgia (Shoop and Ruckdeschel, 1982). Kemp's ridley and loggerhead turtles may be attracted to shrimping

areas because of the easily obtainable forage available

there. This attraction may increase their susceptibility

to capture in shrimp trawls that continue to operate in

the area.

Numbers ofKemp's ridley turtles may be rising, based

on recent increases detected in nesting at Rancho

Nuevo, Mexico (Byles3). If the Kemp's ridley population is growing, the importance of Texas waters to this

species will also increase and these turtles will in teract

with trawls more frequently. Results of comprehensive

conservation programs undertaken on behalf of this

species could be negated if large numbers of this species continue to be killed in the marine environment

from shrimp trawls and other anthropogenic sources.

The wide dispersion of stranding records (for various

sized individuals) and nesting records should be considered prior to development of any protection measures for Kemp's ridley turtles in Texas.

Education, enforcement, and research and development activities related to TED's must be continued.

Strandings of loggerhead turtles in South Carolina decreased as a result ofTED usage (Crowder et aI., 1995).

Proper installation and usage of TED's, coupled with

sustained TED education and enforcement activities,

should also reduce sea turtle strandings in Texas. However, if such measures fail to reduce strandings, it may

be necessary to temporarily close certain nearshOl-e

waters to shrimping to ensure turtle survival. STSS

efforts to document stranded turtles and investigate possible sources of mortality should be expanded so that

anthropogenic sources can be identified and reduced.

Acknowledgmen~ __

I thank the agencies, organizations, and individuals

that assisted with the documentation and salvage of

turtles for the Sea Turtle Stranding and Salvage Network, investigation of possible causes for the strandings,

and attempts to reduce the strandings: the Sea Turtle

Stranding and Salvage Network, Marine Mammal Stranding Network, National Marine Fisheries Service, U.S.

Fish and Wildlife Service, U.S. Coast Guard, University

ofTexas, Texas A&M University, National Park Service,

National Biological Service, Texas Parks and Wildlife

Department, Help Endangered Animals Ridley Turtles

3 Byles, Richard. 1994. U.S. Fish and Wildlife Service, Endangered Species Section, Box 1306, Albuquerque, NM 87103. Personal commun.

(H.E.A.R.T.), Center for Marine Conservation, and

Earth Island Institute.

I am grateful to Wendy Teas, national coordinator of

the Sea Turtle Stranding and Salvage Network, for verifying the total numbers ofstrandings and for providing

me with computerized versions of the stranding databases. I thank John Miller for logistical support and

Darrell Echols for preparing the figures for this manuscript. Richard Byles and an anonymous reviewer provided suggestions regarding this manuscript.

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Ecotoxicology and Histopathology Conducted in

Response to Sea Turtle and Fish Mortalities

along the Texas Coast: May-June 1994

A. A. COLBERT AND M. H. FULTON

Charleston Laboratory *

Southeast Fisheries Science Center

National Marine Fishe'ries Semice

219 FortJohnson Rd.

Charlrston, South Carolina 29412

J. LANDSBERG

Florida Marine Research Institute

Florida Department ojr,'nvironmPntal Protrction

10U 8th A venur SE

St, Petersburg, Florida 3370 I

J. NEWTON

Department of Pathobiology

Auburn University

/66 Greene Hall

Auburn, Alabama 36849

J. CULLEN

College of Veterinary Medicine

North Carolina State University

4700 Hillsborough St,

Raleigh, North Carolina 276U6

G. T. SCOTT

Charlrston I>aboratory'"

Southeast Fisheries Science Crnter

National Marine Fisheries Semicr

219 Fort Johnson Rd.

Charleston, South Carolina 294 J2

ABSTRACT

Investigative and analytical support was provided during a period of unusual mortalities of various marine species, including protected dolphins, endangered sea tunles, and

fish, along the Texas coast during 1994, An ecotoxicological evaluation of the area and an

examination of sea turtle and fish carcasses were conducted as part of the emergency

response to investigate potential causative factors of a sudden increase in marine species

mortalities, continued

* Laboratory name is now "( :enler for (:oaslal Environmental Ilealth

and Biomedical Research, l\;alional Ocean Service,"

73
74 NOAA Technical Report NMFS 143

Water samples collected from the upper Texas coast between Sabine Pass and Lavaca

Bay were analyzed to determine if agricultural runoff was involved in the mortalities.

Analytical results indicated that pesticides were not likely causative factors. Fish brain tissue

was analyzed for acetylcholinesterase activity but no inhibition was detected, reducing the

likelihood that the fish had been exposed to organophosphate or carbamate compounds in

the recent past. Necropsies were conducted on sea turtles and fish. Histopathology results

did not indicate causes of death of sea turtles or fish, and suggested there was no known

common disease factor among any of the animals sampled. Lack of available fresh-dead

carcasses severely limited the sample size. Based on the limited number of individual

animals analyzed, it appeared that a common causative disease agent was not involved.

Because investigating mortalities due to unknown causes requires a scientifically-based

process of elimination, it is important in evaluating results of the entire emergency investigation that none of the potential factors examined during this response could be positively

linked to observed unusual mortalities.

Introduction

During spring 1994, reported strandings of sea turtles

(multiple species) along the Texas and Louisiana coasts

increased markedly in comparison to historical databases (Shaver and Teas!). The increase in mortality

resulted in a total of 527 stranded sea turtles for] 994

relative to a previous record high of 358 dead turtles in

1990 (Shaver, ]998). On 10 May] 994 during the period ofincreased sea turtle mortality, an unusually large

fish kill (Denton et aI., ]998) occurred along the same

coastal area of Texas. Because it was not known if the

mortalities were related and whether threatened and

endangered species were being severely impacted by

unknown factors, an emergency response was initiated

by the National Marine Fisheries Service ( MFS). A

forensic investigation was conducted by out-of-state personnel to evaluate the situation and determine the

types of samples and analyses needed to examine potential causative factors. Results of ecotoxicology and

histopathology are described in this paper. Other aspects of the investigation are presented separately: analysis of samples collected from an algal bloom that was

present in the area of mortality (VanDolah et aI., ] 998),

assessment of fish kills (Den ton et aI., 1998), and fishery interaction issues (Zimmerman2 ).

Methods

The emergency investigation was designed to examine

scientifically all possible causative factors, eliminate poI Shaver, D. (National Biological Service, Padre Island Natioral

Seashore, Padre Island, Texas) and W. Teas (Nat.ional Marine

Fisheries Service, Southeast Fisheries Science Center, Miami I.aborat.ory, Miami, Florida). 1994. Personal communications.

2 Zimmerman, Roger. 1994. NMFS Galvest.on Laboratory, 4700 Ave.

L.:, Galveston, TX 77551. Personal commun.

tential causes based on information obtained during

the investigation, and use forensic guidelines, such as

chain-of-custody, to protect the integrity of the samples

and information collected. Aerial surveys of the region

were used to evaluate the geographical extent of the

mortalities of marine species and determine the status

of agriculture and other industrial activities in the area

relative to the deaths. More than ]5 water samples and

numerous marine animal tissues were collected from

the Texas and Louisiana coasts and distributed for analyses, including toxicology, biotoxin screening and bioassay (Van Dolah et aI., 1998), physiological biomarkers,

and histopathology. Water samples and fish tissues were

analyzed for the presence of chemical contamination.

The contents of five waste drums that washed ashore in

the areas of the fish kill during the on-site sample collection period were also analyzed for priority pollutants.

Water Sampling for Pesticides

Water samples (250 ml) were collected from 17 stations

located along the coast of Texas between Sabine Pass

and Port Lavaca (Table ]) and analyzed for selected

insecticides and herbicides (Table 2) using polyclonal

antihody test kits (i.e. EnvirogardR 3, Millipore) and gas

chromatography-electron capture and nitrogen-phosphorous detector systems. The specific compounds were

selected based upon results from previous investigations conducted along the Texas coast (Colbert et aI.,

In press). Samples were collected from sites where large

concentrations of dead fish were observed along Gulf

Coast heaches, at estuarine/bay sites adjacent to active

agricultural areas, and inland along major agricultural

drainage areas.

:1 Mention of trade names or commercial firms does not imply endorsement. by t.he Kational Marine Fisheries Service, NOAA.
_ Colbert et aI.: Ecotoxicology & Histopathology Conducted in Response to Sea Turtle & Fish Mortalities along the Texas Coast 75

Table I

Sampling sites for surface water samples along the northern Texas coast.

Site

Site I

Site 2

Site 3

Site 4

Site 5

Sire 6

Site 7

Sire 8

Site 9

Site 10

Sire 11

Site 12

Sire 13

Site 14

Sire IS

Site 16

Site 17

ECOTOX #

94-112

94-113

94-114

94-115

94-116

94-117

94-118

94-119

94-120

94-121

94-122

94-123

94-124

94-125

94-126

94-127

94-128

Site description

Hwy R7 detour; of ICW bridge; drainage ditch (near Stowell)

Agricultural drainage ditch (near Winnie)

Hwy R7 detour; under lew bridge at Galveston County line; public boat landing

Surf sample; 1 mi past barrier on washed-out Highway 87, northeast of High Island; sea turtle retrieval area

Bay side of Rollover Pass

ICW near Crystal Beach; Siever's Cove

Rice field drainage ditch; 1st one on Hwy 124N (southwest of Beaumont)

Sabine Channel; 200 yd upstream from Hwy 82 bridge

Hwy 73 (south of Beaumont); large creek/drainage ditch; agriculture

Rollover Pass; same as Site 5

San Luis Pass; bay side at bridge around beach curve at south end of Galveston Island

Freeport Channel at Surfside Beach

Colorado River; Bay City at bridge

Just south of Site 13; drainage ditch at rice field

Point Comfort Boat Landing

Formosa Beach on Lavaca Bay; park jetty

Brazos River; under I-1wy 322 bridge

Biomarker Analysis: Acetylcholinesterase

Eleven hardhead catfish, Anusfelis, were collected from

various locations where dead fish were observed along

washed-out Highway 87 near Sea Rim Park. These fish

were collected live, sacrificed, and then frozen and

shipped on dry ice to the NMFS Charleston Laboratory

for analysis of brain acetylcholinesterase, an enzyme

which is often inhibited in aquatic organisms exposed

to organophosphate or carbamate insecticides, using

methods described by Fulton (1989). Five hardhead

catfish were also collected from South Carolina waters

to serve as a reference control group.

Chemical Analysis of Beached Waste Barrels

On 17 May 1994 during field sampling, chemical waste

barrels were discovered on the beach and beside washedout Highway 87 near Sea Rim Park. These barrels,

which were not present the previous day, were collected by a clean-up contractor (EMTECH of Pasadena,

Texas) for the Texas Natural Resources Conservation

Commission. EMTECH was contracted to sample these

waste barrels to determine whether or not the contents

of the barrels might have been factors in the mortalities. The samples were archived, and five subsamples

from the archive were analyzed for industrial and priority pollutants (PCB's, pesticides, phenols, cyanide, trace

metals, volatile organics, and semi-volatile organics) by

a certified analytical laboratory (Pace Environmental,

Houston, Texas).

Table 2

Preliminary pesticide analysis of surface water samples

from the northern Texas coast. Minus (-) indicates

sample was < lower limits of detection (LLOD). Plus (+)

and double plus (++) indicates samples were> LI.QO and

> positive control spike, respectively. For triazine herbicides, ++ indicates> 1.00 J.1g/L; + indicates:S; 1.00 J.1g/L but

;:00.10 J.1g/L.

Site ECOTOX# Aldicarb Carbofuran Triazines

Site I 94-112

Site 2 94-113

Site 3 94-114 +

Site 4 94-115

Site 5 94-116

Site 6 94-117 +

Site 7 94-118

Site 8 94-119

Site 9 94-120 +

Site 10 94-121

Site II 94-122 +

Site 12 94-123 +

Site 13 94-124 ++

Sire 14 94-125 +

Site 15 94-126 ++

Sire 16 94-127 ++

Site 17 94-12R ++

Examination of Fish and Sea Turtles

Though live fish in distress were reported during the

fish kill, none had been collected. Live fish from the
76 NOAA Technical Report NMFS 143

same area were collected as soon as possible and kept

alive in a tank until shipped. Because sampling of animals occurred as part of an emergency response and

logistical problems were encountered, the live fish examined were collected approximately 2 days after the

fish kill occurred. Fish including one black drum,

Pogonias cromis, one pompano, Trachinotus carolinius,

and approximately 20 hardhead catfish, Ariusfelis, were

collected live from the surfat the location ofthe 10 May

1994 fish kill along washed-out Highway 87. The fish

were kept alive in a holding tank over a weekend. The

pompano, black drum, and four catfish were sent unfrozen on ice, as requested by the analyst, to the Florida

Marine Research Institute for pathology, parasitology,

and bacteriology. At the Institute, the pompano, black

drum, and two catfish were processed after being on ice

approximately 18 hours. Bacteriological swabs were

taken from external lesions and kidney of the fish and

plated out onto TCBS (thiosulfate-citrate-bile salts-sucrose agar) or TSA (trypticase soy agar) media. Fish

were examined by routine diagnostic procedures ann

samples of gills, liver, kidney, spleen, pancreas, and gall

bladder were processed for histopathology. Tissues were

fixed in 5% paraformaldehyde in 0.1 M phosphat.e

buffer, dehydrated in a graded et.hanol series, and embedded inJB-4 glycol methacrylate resin. Sections were

cut to 3.5 J1m on an LKB 2218 Hist.orange microt.ome

and were stained in Weigert's hematoxylin and eosin

(H & E), or in thionin stain adapted to glycol methacrylate (Nagle and Quintero-Hunter)4. Brain tissue from

each fish was wrapped in aluminum foil and immediately stored frozen. The remains of the examined fish

and two intact catfish were archived. Formalin-fixed gill

and liver tissues from five hardhead catfish were examined by another researcher. The remaining fish were

archived.

The majority of sea turtles that had stranded dead

since the beginning of the event were collected ann

stored frozen by the NMFS Gah'eston Laboratory, thus

standard histopathology was not possible. Many of the

turtles that stranoed before and during the emergency

response were too decomposed to yield much information indicative of cause of death. The decomposed

turtles were identified t.o species, measured, and documented for baseline st.randing information. Five sea

turtles were suitable for histopathology. Tissue was collected in neutral buffered formalin during necropsy.

Fixed tissue was sent to North Carolina State University

for histopathologic evaluation. Tissues were embedded

in paraffin and sectioned and stained with hematoxylin

and eosin.

·1 :--lagle, P., and I. Quintero-Hunter. 1994. Florida Departml"nt of

Environml"ntal Protection, Florida Marine Resl"areh Institutl", 100

8th Avenue, S.E., St. Pl"tl"rsburg, FL 33701. Unpubl. man user.

Results

Pesticide Screening

During May 1994, aerial and ground surveys of the area

along the upper Texas coast showed that many agricultural crops were in early growing stages. Crop dusters

and spraying equipment were observed in use and documented. The rice fields in most areas recently had been

flooded for harvest. Surface water samples collected at

17 sites between Sabine Pass and Lavaca Bay were

screened for two insecticides (carbofuran and aldicarb)

ann one class of herhicides (triazines) using the

EnvirogardR polyclonal antibody assay system (Table

2). None of the samples were positive for either insecticide. Ten of 17 samples were positive for triazine herbicides. Two years of follow-up research, subsequent to

the 1992 event involving bottlenose dolphins along the

mid-Texas coast, demonstrated that triazine herbicides

could be detected in some estuarine/bay systems during most months of t.he year (Pennington, 1996).

Four of the 10 positive samples contained triazine

levels >1.0 ppb. These four samples were also analyzed

by gas chromotography For the presence of four additional insecticides (azinphosmethyl, endosulfan,

chlorpyrifos, and fenvalerate) commonly used in the

area. The results of the analyses were negative in the

four samples for each of the four insecticides.

Water samples obtained for pesticide screening were

collected immediately following rainfall in areas where

agricultural runoff would most likely occur. Results of

the pesticide screening assays were positive only for

atrazine, a triazine herbicide. No other pesticides were

oetected. Because samples were collected under optimum conditions to detect runoff chemicals, it is unlikely that agricultural runoff contributed to the unusual mortalities.

Brain Acetylcholinesterase Activity in

Hardhead Catfish

Cnder certain conditions, activity levels of the enzyme

acetylcholinesterase (AChE) measured in brain tissue

can he used as a Forensic tool to indicate whether or not

an animal has been exposed to cholinesterase-inhibiting compounds such as carbamate and organophosphate insecticides (Coppage and Braidech, 1976). Preliminary results of brain AChE, measured in tissue

samples removed from 11 hardhead catfish, ranged

from 13.21 to 20.20 nmol mg tissue-I min-1 (Table 3).

The mean brain AChE activity in these fish was 16.61

nmol mg tissue-1 min-I. Brain AChE activity in the five

fish collected from South Carolina waters ranged from

15.97 to 18.59 nmol mg tissue-Imin-I. Mean brain AChE
_ Colbert et aI.: Ecotoxicology & Histopathology Conducted in Response to Sea Turtle & Fish Mortalities along the Texas Coast 77

activity in these fish was 17.25 nmol mg tissue-1 min-1.

There was no significant (p = 0.57) difference in brain

AChE activity between the Texas and South Carolina

fish. These results indicate there were no biologically

significant levels of brain AChE inhibition in the Texas

catfish. This greatly reduces the likelihood that the

Texas catfish were exposed to cholinesterase-inhibiting

agents in the recent past.

dermal loss and hemorrhage. Gills showed degeneration

and post-mortem change, most likely due to the shipment

period of approximately 18 hours. The livers of the fish

examined at one facility were found to be normal.

Table 3

Brain AChE activity measured in hard head catfish brain

tissue.

Analysis of Beached Chemical Barrels

The results of chemical analyses conducted on samples

from five waste barrels are shown in Table 4. One drum

may have contained gasoline and a pesticide residue.

Most of the other components detected were thought

to be byproducts of the breakdown corrosion in the

metal barrels. Results of the analyses indicated that the

contents of the drums sampled were most likely not

involved in the marine animal mortalities.

Examination of Fish Tissues

All of the fish that had been collected live exhibited

hemorrhagic fins and epidermal cell loss on the fins.

No inflammation was observed accompanying the epi-

[D number

UM 1-7

UM I-II (l)

UM 1-11 (2)

UM I-II (3)

UM 1-11 (4)

UM 1-2 (3)

UM 1-2 (2)

UM 1-2 (4)

UM 1-4 (4)

UM 1-4 (5)

UM 1-3 (2)

U'vl1-3 (6)

UM 1-3 (9)

UM 1-3 (8)

UM 1-3 (7)

UM 1-3 (10)

Descri ption

Catfish (Charleston, SC)

Catfish (Charleston, SC)

Catfish (Charleston, SC)

Calfish (CharleslOn, SC)

Calfish (Charleslon, SC)

Catfish (Texas)

Catfish (Texas)

Catfish (Texas)

Calfish (Texas)

Catfish (Texas)

Calfish (Texas)

Catfish (Texas)

Catfish (Texas)

Cat(ish (Texas)

Calfish (Texas)

Catfish (Texas)

Brain AChE activity

(nmol mg-I min-I)

18.59

15.97

16.82

17.20

17.66

13.21

13.59

14.90

20.20

14.28

15.90

17.89

1828

18.66

18.20

17.:>9

Table 4

Summal)' of chemical analysis of waste drums washed ashore along the Bolivar peninsula north of Galveston, Texas. Only

compounds with concentration> 1.1.00 are listed.

Barrel

(:rystal Beach #1

Pelican Pier # I

Beau #4

Beau #12

Beau #13

Contaminant

Ni

Zn

Phenolics

Benzene

Ethylbenzene

Toluene

Naphlhalene

Beta BI[C

Zn

Phenolics

Cu

Pb

Zn

Phenolics

Cu

Zn

Phenolics

Zn

Phenolics

Cone. (,ugl Kg)

4,000

:>,000

20,000

:>,200,000

5,ROO,000

18,000,000

53.0UU

1.7

1,000

29,000

4,000

65,000

240,000

13,000

19,000

130,000

4,500

160,000

2,600

Comment

1\0 OI'ganicsl

, primarily rust and corrosion.

This barrel contained gasoline and some Bile.

:'\0 organicsl

, primarily corrosion

1\0 organics], primarily corrosion

No organics*, primarily currosion

] Organics in this case refers to pesticides, PCB, herbicides, fuel oils, and related compounds.
78 NOAA Technical Report NMFS 143

The following conditions were observed in four other

fish examined:

Hardhead catfish #1: Bacterial isolates from the anal

fin included two Aeromonas spp., Vibrio sp., and presumptive Photobacterium angustum. Petechiae present on

the skin may have been associated with infestations of

Caligus haemulonis, a copepod. Aeromonas sp. was also

isolated from the kidney. An inflammatory response

with marked neutrophilia and karyorrhexis was observed

in the interstitial tissue of the kidney. The liver appeared to be congested and was vacuolated in both

defined areas of the tissue as well as in individual hepatocytes. Analysis of the spleen determined that

melanomacrophage centers were large with an increase

in yellowish-brown pigmentation (hemosiderin), and

many nuclei were present (possibly due to increased

lysis of erythrocytes, but erythrocytes in blood vessels

were normal). There was no obvious increase in erythroblasts which might have been present if associated

with hemolysis due to a biological toxin from bacteria

(Vibrio sp.) or dinoflagellates.

Hardhead catfish #2: The edge of the spleen tissue

was degenerate due to postmortem chan?;e. The

melanomacrophage centers were lar?;e, with an increase

in yellowish-brown pigmentation and many nuclei. Erythrocytes in blood vessels were normal with no obvious

increase in erythroblasts. Kidney tissue was beginnin?;

to degenerate, with obvious detached vacuolated epithelial cells from the kidney tubules. Interstitial tissues

contained some karyorrhectic cells and neutrophils,

possibly indicating early inf1ammatory response and

necrosis. Bacterial growth was negative.

Pompano: Gills showed some degeneration of the

secondary lamellae, and low level infestation by the

monogenetic trematode Bicotylophora trachinoti. There

was also a low level infestation of epitheliocystis. There

were myxosporean spores in the gall bladder bile. Vacuolated epithelial cells were detached from the basement membrane of the kidney tubules, sug?;esting degeneration. Interstitial tissue was vacuolate with some

karyorrhectic cells or neutrophils, necrosis, and lar?;e

numbers of eosinophilic granulocytes. Bacterial ?;rowth

was negative. Postmortem degeneration was observed

in spleen samples. Many granulomas were present. Liver

tissue was congested, or filled with red blood cells, and

had vacuolation both in defined areas of the tissue and

in individual hepatocytes. Some karyorrhectic cells were

present in blood vessels. The pancreas was normal.

Black drum: Bacterial isolates from the caudal fin

included two Aeromonas spp. and two Vibrio spp. Gills

were lightly infested with mono?;enetic trematodes,

Microcotyle pogoniae. Aeromonas sp. was also isolated from

the kidney. An inflammatory response with marked

neutrophilia and karyorrhexis was observed in the interstitial tissue of the kidney. The spleen was hemorrhagic, with karryorhectic cells in interstitial tissue, and

was very congested and vacuolate. The liver hepatocytes

were vacuolar with some karyorrhectic cells in blood

vessels and a few melanomacrophage centers. The pancreas was beginning to degenerate.

The hemorrhagic condition of the fish fins is a characteristic generally associated with stress, and not usually used as a diagnostic factor. It could not be determined whether this characteristic resulted during capture and handling of the fish, or whether it developed

prior to capture. The reddish fin condition was observed to worsen during the holding period prior to

shipment and was photographically documented.

Because the fish were placed in a transfer tank for

transport to the laboratory, kept in an artificial system

for 3 days, and examined approximately 18 hours after

time of death, bacteriological results are not necessarily

considered to be representative of the condition of the

fish in their natural environment. The bacterial isolates

were indicative ofsecondary opportunists that may have

infected the fish after other factors had stressed the

fish. The time frame between collection and examination would most likely mask any factors causing an

acute pathological response, however, some disease

a?;ents might still have been detectable had they been

present.

Histopathological Analysis of Sea Turtle Tissues

There were no disease-related histologic lesions seen in

any turtle tissues that indicated a cause of death of the

four Kemp's ridley, Lepidochelys kempi, and one loggerhead, Caretta caretta, submitted. Tissue preservation was

good and histologic detail was maintained in all samples,

so any abnormal conditions present should have been

apparent.

One Kemp's ridley turtle (UMl-12) had minor to

moderate pulmonary edema, with little associated inflammatory response. Because this animal had been

placed on a respirator during its clinical care, the lesion

was attributed to the therapy. A second Kemp's ridley

turtle (UMI-15(2» also had mild edema and an accumulation of mucus within the airway, indicative of respiratory tract irritation but not attributable to a specific

cause. Congestion and edema were found in the lung

of a loggerhead turtle (UMl-15(l), SCC271) and a

Kemp's ridley (UMl-15(3»). The liver of one turtle

(UMl-15(3» had a focus of infarction at the periphery

of the lobe and associated heterophil infiltration.

Overall, there was no specific lesion indicative of a

cause of death in the sea turtles examined. The most

common lesion occurred in the lungs, but edema was

generally mild. Death by drowning could not be determined as the cause of death because control tissue from
_ Colbert et al.: Ecotoxicology & Histopathology Conducted in Response to Sea Turtle & Fish Mortalities along the Texas Coast 79

animals that were known to have died by drowning was

not available.

Discussion and Conclusions _

Histopathological results indicated that there were no

known common disease factors or other common cause

of death among the turtles and fish sampled. To determine the cause of the overall increase in sea turtle and

fish mortality during the period, much more extensive

diagnostic effort would have been necessary at the beginning of the unusual mortality period so that a larger

number of recently dead specimens could have been

obtained. Collection oftissue for histologic and ultrastructural examination must be performed promptly after an

animal dies since autolysis or freezing artifacts seriously

impair an accurate histologic diagnosis. Such a collection

was conducted only near the end of the investigation.

There is no evidence based on examination of fish

and sea turtle tissues collected for this study to indicate

that the fish kill events and sea turtle mortalities were

related. Reports of live fish in distress in the surf may

support the hypothesis that the 10 May 1994 fish kill

occurred relatively close to shore. The majority of fish

collected for examination did not exhibit active signs of

distress but were collected at least 24 hours after the

major fish kill occurred. If fish were exposed to acute

primary stressors such as toxic algal blooms or low

dissolved oxygen, then the pathological and bacteriological changes observed in the fish could be explained

as a secondary response. Such primary stressors could

lead to secondary bacterial infections during the time

course of the investigative response to the fish kill.

However, no obvious causative agents were detected

during initial field observations. The potential for exposure to a natural toxin or impact by some environmental contaminant cannot be completely eliminated

as a factor in the fish kill, and results of watel- analyses

for presence of biotoxins may indicate one potential

causative factor (VanDolah et aI., 1998).

The responses to the unusual 1992 and 1994 mortality events involving coastal and marine species along

the Texas coast underscore the value of the integrated

investigative approach ofwhich these analyses were a part.

It also indicates the need to develop further communications and funding for analytical support of such events.

The two mortality events have created an interest among

numerous local, state, and federal agencies and institutions in responding to such crises along the coast of the

GulfofMexico as early, and as effectively, as possible when

future unusual mortalities of marine species are detected.

Such a planned team approach composed of people already present in an area should help prevent some of the

problems encountered in this response.

Acknowledgments _

The results reported in this paper are due in part to the

dedicated efforts of several individuals. Donna Shaver

of the National Biological Service, Padre Island National Sea Shore, Texas, did an outstanding job during

the period of increased sea turtle mortalities. Wendy

Teas, MFS/SEFSC Miami Laboratory, Regional Coordinator of the Southeast Sea Turtle Stranding and Salvage Network, was also very supportive during the investigation. We greatly appreciate the contributions of

James Daugomah, Wayne McFee, Paul Pennington,

Erich Strozier, Ed Wirth, and Debra Wolf of the MFS/

SEFSC Charleston Laboratory; Charles Caillouet, Eric

Stabenau, Andrea Cannon, Dickie Rivera, and Ron

Wooten of the NMFS/SEFSC Galveston Laboratory;

James Pallias and Pam Nagle of the FDEP/FMRI Laboratory, St. Petersburg; Winston Denton, Mark Foreman,

and Robert MartinezJr.of the Texas Parks and Wildlife

Department/Coastal Fisheries; and Brian Lynch and

Raymond Marlow of the Texas Natural Resources Conservation Commission.

Literature Cited

Colbert, A. A., G. I. Scott, M. II. Fulton,j. W. Daugomah, P. B. Key,

E. D. Strozier, E. F. Wirth, and S. B. Galloway.

In press. Procedures and methods used to investigate unusual mortalities of bottlenose dolphins along the mid-Texas

coastal bay ecosystem during 1992. NOAA Tech. Rep. NMFS.

Coppage, D., and T. Braidech.

1976. River pollution by anticholinesterase agents. Water Res.

10:19-24.

Denton, W., D. Buzan,j. Mambretti, K. Rice, and K. Quinonez.

1998. Fish kills in the northwestern Gulf of Mexico, April 26-

June 27, 1994. In R. Zimmerman (ed.), Characteristics and

causes of Texas marine strandings, p. 27-31. OAA Tech.

Rep. NMFS 143.

Fulton, M. H.

1989. The effects of certain intrinsic and extrinsic variables

on the lethal and sublethal toxicity of selected organophosphorus insecticides in the mummichog, Fundulus heteroclitus,

under laboratory and field conditions. Ph.D. dissert., Univ.

South Carolina, Columbia, 183 p.

Pennington, P. L.

1996. The toxicity of the herbicides atrazine and alachlor on

the estuarine phytoplankter Pavlovasp. (Prymnesiophyceae)

with an emphasis on acute toxicity testing of individual

herbicide mixtures, and multigenerational chronic bioassays. Master's thesis, Univ. Charleston, S.C., 142 p.

Shaver, D.

1998. Sea turtle strandings along the Texas coast, 1980-1994.

In R. Zimmerman (ed.), Characteristics and causes of Texas

marine strandings, p. 57-72. NOAA Tech. Rep. NMFS 143.

Van Dolah, F. M., G.j. Doucette, T. A. Leighfield, and

K. A. Steidinger.

1998. Assessment of the involvement of algal toxins in the

1994 Texas fish kills. In R. Zimmerman (ed.), Characteristics and causes ofTexas marine strandings, p. 41-45. OAA

Tech. Rep. NMFS 143.

Gross Necropsy Results of Sea Turtles Stranded on the Upper Texas

and Western Louisiana Coasts, 1January-31 December 1994

ANDREA CARON CANNON

Galveston Laboratory

Southeast Fisheries Science Center

National Marine Fisheries Service

4700 Ave. U

Galveston, Texas 77551

ABSTRACT

Necropsies were conducted on 194 of the 284 sea turtles stranded on the upper Texas

and western Louisiana in 1994. The species necropsied included 167 Kemp's ridley sea

turtles, Lepidochelys kempii (86.1 % of total); 20 loggerheads, Caretta caretta (10.3%); 6 greens,

Chelonia mydas (3.1 %); and 1 leatherback, Dermochelys coriacea (0.5%). External injuries or

trauma were recorded for 28% of the necropsied turtles. The sex ratio of the necropsied

turtles was 1: I. Gastrointestinal tracts of stranded sea turtles contained primarily fish and

crabs. Fish hooks, plastic beads and bags, and balloons were also found in the stomach and

intestinal tracts. Possible causes of death identified for sea turtles stranded during 1994

include ingestion of fish hooks, congenital deformities, boat propeller injuries, and entanglement in fishing gear. A primary causative agent could not be determined.

Introduction

The National Marine Fisheries Service (NMFS)

Galveston Laboratory has participated in the Sea Turtle

Stranding and Salvage Network (STSSN), conducting

systematic surveys since 1986 (Heinley et aI., 1988;

Duronsolet et aI., 1991). The Galveston Laboratory's

involvement now includes responding to call-in reports,

documenting sea turtle strandings, providing systematic surveys of the upper Texas and western Louisiana

coasts, conducting necropsies on dead stranded sea

turtles, and rehabilitation of live stranded sea turtles.

During spring of 1994, strandings of sea turtles

(Shaverl ) and marine mammals were at record levels.

Over 200 marine mammals, primarily bottle-nosed dolphins, Tursiops truncatus, were stranded dead between

February and May 1994 on the upper Texas coast

(Haubold2). In April marine mammal strandings beI Shaver, Donna. 1994. Padre Island National Seashore, Midwest

Science Center, ational Biological Service, 9405 S. Padre Island

Dr., Corpus Christi, TX 78418. Personal commun.

2 Haubold, Elsa. 1994. Texas Marine Mammal Stranding Network,

4700 Ave. U, Galveston, TX 77551. Personal commun.

gan to decline, and sea turtle strandings increased.

Large numbers of hardhead, Aeriusfelis, and gafftopsail

catfishes, Bagre marinus, were also reported washed

ashore along the upper Texas coast concurrent with sea

turtle strandings.

The purpose of this paper is to report the results of

necropsies from 194 sea turtles which stranded during

1994.

Methods

The turtle's condition was immediately assessed to determine its disposition (Table 1). Dead stranded sea

turtles were brought to the Galveston Laboratory and,

depending on the state of decomposition, either frozen

for gross necropsy at a later date or necropsied immediately. Live stranded sea turtles were retrieved and brought

to the Galveston Laboratory or University of Texas Medical Branch (UTMB), Galveston, for rehabilitation.

Of the 284 sea turtles reported stranded along the

upper Texas and western Louisiana coasts in 1994, 194

were necropsied as described by Rainey (1981) and

Wolke and George (1981). Complete necropsies (including histology and pathology) were performed on

81
82 NOAA Technical Report NMFS 143

Table I

Description of carcass condition and appropriate tissue samples collected,

Condition Disposition Description Tissues collected

Live stranded, died at Necropsy immediately

holding facility

Extremely fresh, no postmortem

changes

Complete suite of histology and

toxicology samples, blood work-up, Cl

tract analyses, determine sex

Fresh dead, no bloating Placed on ice, necropsy

immediately

Stranded dead, no bloating Histology and toxicology samples, GI

tract analyses, determine sex

Moderately decom- Frozen, for gross necropsy

posed

Some bloating, internal organs

identifiable

Toxicology, GI tract analyses, determine sex

Severely decomposed Frozen, for gross necropsy Organs decomposing, not easily

identifiable

GI tract (when possible), determine

sex (when possible)

External Injuries

A variety of external Injuries were reported for dead

stranded turtles but causes of the injuries could not be

determined. One hundred twelve (72.3%) of the 155

heads died within 72 hours of being retrieved for rehabilitation. The seven sea turtles which died within 72

hours of being brought to the NMFS Galveston Laboratory had the greatest potential for identifying possible

causes of the spring 1994 stranding event (Stabenau3).

Two Kemp's ridley, one hawksbill, and one green showed

signs of external trauma. All four were successfully rehabilitated and certified for release by veterinarians.

Two Kemp's ridleys survived more than 72 hours

before dying. Necropsy revealed that both had abnormal development of the lungs. Defects causing inefficient gas exchange were likely contributors to the demise of these two animals.

Table 2

Frequency of tissue types collected,

o

o

o

I

Leatherback

o

o

o

6

2

2

2

18

Loggerhead Green

3

8

9

158

Kemp's

ridley

Blood chemistry

t listology/ pathology

Toxicology

Gross necropsy on ly

Individuals of the five species ofsea turtles occurring in

the Gulf of Mexico were stranded along the upper

Texas and western Louisiana coasts during 1994 (Table

3). Species composi tion of the necropsied turtles was

86.1 % Kemp's ridleys (167), 10.3% loggerheads (20),

3.1% greens (6), and 0.5% leatherbacks (1).

very fresh carcasses (minimal postmortem deterioration) and on any live stranded animals that later died,

Carcasses that were severely decomposed were of

little or no use for histology or pathology and were

frozen for gross examination when time permitted. Toxicology samples, however, were collected from certain of

these carcasses (Table 2), and natural history data (i.e.,

feeding habits, sex ratios) was collected when possible.

Stranded turtles were initially exam,ined for obvious

signs of external trauma. Necropsies included observations of internal organs, qualitative analysis of gastrointestinal tracts, and visual examination of gonads to

determine sex when possible. Tissues for histological

analysis were preserved in 10% neutral buffered formalin and samples for toxicological analyses were frozen.

Histological samples from the first live stranded Kemp's

ridley, which died later, were taken to UTMB for analysis. All other toxicological and histological samples were

shipped to the NMFS Charleston Laboratory, Charleston, S.c., for analysis.

Live Strandings

Results

Nine Kemp's ridleys, three loggerheads, one green,

and one hawksbill, Eretmochelys imbricata, were stranded

alive. Five of the Kemp's ridleys and the three logger3 Stabenau, E, K. 1994, Blood chemistry profiles of live-stranded

and captive reared Kemp's ridley and loggerhead sea turtles.

l'npubl. man user.
__ Cannon: Gross Necropsy Results of Sea Turtles Stranded on the Upper Texas and Western Louisiana Coasts 83

Table 3

Live stranded and dead stranded sea turtles along the upper Texas and western Louisiana coasts during 1994.

Live/died Live/successfully

Species at holding facility rehabilitated Dead Total stranded Total necropsied

Kemp's ridley 7 2 216 225 167

Loggerhead 3 U 47 50 20

Green 0 I 6 7 6

Leatherback 0 0 1 I I

Hawksbill 0 I 0 I 0

Total 10 4 271 284 194

necropsied sea turtles had no external injuries. Seventeen (11.0%) were missing at least one appendage (including head and/or flippers). According to Richard

Henderson4, appendages of two of these turtles may

have been removed mechanically, based on straight

edge cuts on the anterior margins of the carapace. It is

not possible, however, to determine whether this caused

the turtles' deaths or ifit occurred post mortem. Due to

advanced decomposition, we were unable to determine

whether appendages were cut off at sea or removed by

scavengers on the remaining 15 carcasses. Nineteen

(12.3%) carcasses had damage to the carapace consistent with injuries caused by boat propellers. Six (3.9%)

had miscellaneous damage to the head and/or flippers

but again we could not determine the cause of these

injuries. One (0.7%) Kemp's ridley was entangled in

monofilament fishing line which was wrapped around

its head and all four flippers. The extent of the entanglement would likely have impeded ability of the

turtle to swim and surface for air, resulting in asphyxiation. It is possible, however, that the turtle became

entangled after death.

Sex Ratio

The observed sex ratio for necropsied Kemp's ridley

sea turtles in 1994 was 41:48. Fifty-seven Kemp's ridley

carcasses were too severely decomposed to determine

gender. The ratio of females to males varied with size,

ranging from I: 1.5 for Kemp's ridleys 30.0-39.9 cm

straight carapace length (SCL) to 2.5:1 for Kemp's

ridleys greater than or equal to 50.0 cm (Table 4). Of

the 20 loggerheads necropsied, eight were females; the

gender of 11 could not be determined. Gender could

not be determined for the green turtles or the sole

leatherback.

4 Henderson. Richard. 1994. Galveston Island Veterinary Clinic,

Galveston, TX. Personal commun.

Table 4

Sex and size distribution of necropsied sea turtles

stranded during spring 1994.

Straight Kemp's ridley Loggerhead

carapace

length (em) F M F M

20.0-29.9 IJ 13 0 0

30.0-39.9 16 24 U 0

40.U-49.9 9 9 2 0

50.0-59.9 4 2 6 I

>59.9 1 0

Total 41 48 8

Gastrointestinal Tract

The gastrointestinal (Gl) tracts of necropsied turtles

were examined grossly for food items, debris, and possible blockages. Ten of the 176 Kemp's ridleys examined contained no food or debris in the GI tract, and 45

were too severely decomposed to determine Gl tract

contents. Nine of the GI tracts were collected in their

entirety and sent to the MFS Charleston Laboratory

for toxicological analysis. The most commonly occurring food item for all sea turtle species combined was

fish parts (occurring in 40.2% of the turtles), including

bones of hardhead catfish as well as other unidentified

fish species. Crab parts, including blue crabs, Callinectes

spp., stone crabs, Menippe mercenaria, purse crabs,

Persephona mediterranea, and unidentified crabs, occurred

in 38.1 % of the necropsied Kemp's ridleys. Seven ofthe

Kemp's ridleys contained Nassarius spp. (Table 5), a

small gastropod known to scavenge, suggesting that the

turtles may have been feeding on dead and decaying

organisms.

Fish hooks were found in five Kemp's ridleys. One

Kemp's ridley GI tract contained parts of crabs, a bird,

as well as a fish hook embedded in the esophagus. An

abscess 4 cm in diameter was associated with the fish
84 NOAA Technical Report NMFS 143

Table 5

Frequency of items observed in the gastrointestinal

tracts ofsea turtles necropsied during 1994, by species.

Kemp's

Food item ridley Loggerhead Green Total

Fish 74 4 0 78

Crab 70 4 0 74

Plastic 9 1 2 12

Plant 8 1 4 13

Fish hook 5 0 0 5

Shell hash 6 0 0 6

Nassarius spp. 7 0 0 7

Moon snails 3 1 0 4

Bird 1 0 0 1

Tube worms 1 1 0 2

Monofilament line 1 0 0 1

Sea anemones 0 1 0 1

Goose neck barnacles 1 0 0 1

Empty 6 1 0 81

1 Includes the sole leatherback necropsied.

hook. Due to advanced decomposition, however, it was

impossible to determine whether this was the cause of

death. Another Kemp's ridley had a fish hook in the

intestine; there was no sign that it had perforated the

intestine, stomach, or esophagus. Fish hooks were also

found embedded in the esophagus of three additional

Kemp's ridleys. Given decomposition of these three

animals no abscess was noted. Sargassum spp. was identified in four ofthe Kemp's ridley GI tracts. Plastic debris

occurred in ten of the specimens, although it did not

appear to cause any blockage or trauma.

The GI tract offour loggerheads con tained fish bones.

The GI tracts of four of the green sea turtles contained

unknown plant material; one GI tract was empty. Two

of the green's GI tracts also contained plastic. The GI

tract of the leatherback was empty.

Discussion

The cause of death could not be determined by gross

necropsy of any of the sea turtles examined during

1994. Although complete necropsies were not performed on all turtles due to the state of decomposition

of the carcass, gross necropsies on such carcasses can

still yield valuable information. Occasionally a probable

cause or contributing cause of death (particularly if

there is a blockage or perforation of the GI tract) can

be determined. Moreover, possible factors contributing to death can be ruled out.

External Injuries

Although external injuries were reported in 27.7% of

the sea turtles necropsied, it was not possible to attribute deaths to these injuries. Heinley et al. (1988)

reported mutilation rates of 26% and 60% in stranded

sea turtle carcasses collected along the upper Texas

coast, in 1986 and 1987, respectively. They listed several

possible causes of mutilations, i.e. boat propellers, post

mortem scavengers, shark attack, and human induced

injury (at sea or on the beach). We were unable to

determine whether the injuries observed resulted in

death or occurred post-mortem.

Sex Ratio

Sex ratios of 3: 1 for Kemp's ridleys and 2: 1 for loggerheads have been reported from necropsies of 257

stranded sea turtles collected in the western Gulf of

Mexico (Stabenau5). Our investigation failed to show

dominance of females in sex ratios of Kemp's ridleys

and loggerheads. Dave Owens6 has suggested thatjuvenile female sea turtle gonads may decompose faster,

becoming harder to identify than the more denselypacked juvenile male gonads. Varying decomposition

rates of gonadal tissue will yield biased sex ratios and

could account for the 1:1 sex ratio in this study.

Gastrointestinal Contents

Debris (including fish hooks and plastic) was found in

9.0% of the necropsied sea turtles; in no case, however,

was it apparent that debris contributed to the demise of

a turtle. Stanley et al. (1988) reported debris in 26.8%

of turtles necropsied during 1986 and 40.6% of those

necropsied in 1987.

Gross analyses of GI tract contents of Kemp's ridleys

stranded in 1994 were comparable with the findings of

Shaver (1991) who analyzed the contents of 100 Kemp's

ridleys. She reported that juveniles fed on crabs and

fish, appearing to be more opportunistic feeders than

adults. Kemp's ridleys have been observed following

shrimp boats and feeding on discarded by-eatch (Carpenter7). The analyses ofGI tract contents for loggerhead sea

turtles proved consistent with Plotkin et al. (1993), with

loggerheads feeding primarily on crab and fish.

5 Stabenau, Erich K. 1994. NMFS Galveston Laboratory, 4700 Ave.

U, Galveston, TX 77551. Personal commun.

fi Owens, Dave. 1994. Texas A&M University, Dept. of Biology,

College Station, TX 77843. Personal commun.

7 Carpenter,James. 1993. NMFS Galveston Laboratory, 4700 Ave.

U, Galveston, TX 77551. Personal commun,
__ Cannon: Gross Necropsy Results of Sea Turtles Stranded on the Upper Texas and Western Louisiana Coasts 85

The results of the necropsies performed on stranded

sea turtles collected in 1994 did not indicate any primary causative agen t for the strandings along the upper

Texas and western Louisiana coasts during 1994.

Acknowledgments _

I would like to thank the following for their participation in this project: Joseph P. Flanagan, Richard

Henderson, Dickie B. Revera, all STSSN participants,

and all others who reported stranded sea turtles or

assisted in various ways. Special thanks go to Charles W.

CaillouetJr., Clark T. Fontaine, and Erich K. Stabenau,

who reviewed the manuscript.

Literature Cited

Duronslet, M. J., D. B. Revera, and K. M. Stanley.

1991. Man-made marine debris and sea turtle strandings on

beaches of the upper Texas and Southwestern Louisiana

coasts, June 1987 through September 1989. NOAA Tech.

Memo. NMFS-SEFC-279, 47 p.

Heinley, R. W., E. K. Stabenau, A. M. Landry, and M. Duronslet.

1988. Mutilations of stranded sea turtles along the Texas

coast. In B. A. Schroeder (compiler), Proceedings of the

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Biology, p. 33-34. NOAA Tech. Memo. NMFS NOAA-TMSEFC-214.

Plotkin, P., M. K. Wicksten, and A.F. Amos.

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Rainey, W. E.

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Shaver, D.J.

1991. Feeding ecology of wild and head-started Kemp's ridley

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Stanley, K. M., E. K. Stabenau, and A. M. Landry.

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119-121. NOAA Tech. Memo. NOAA-TM-SEFC-2l4.

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NOAA Technical Reports NMFS

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abundance and geographic distribution of fishery resources, to understand and predict fluctuations in the

quantity and distribution of these resources, and to establish levels for their optimum use. NMFS is also

charged with the development and implementation of policies for managing national fishing grounds, with

the development and enforcement of domestic fisheries regulations, with the surveillance of foreign fishing

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policies. NMFS also assists the fishing industry through marketing services and economic analysis programs

and through mortgage insurance and vessel construction subsidies. It collects, analyzes, and publishes

statistics on various phases ofthe industry.

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