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EcoHealth 1, 246–254, 2004

DOI: 10.1007/s10393-004-0094-6

 2004 EcoHealth Journal Consortium

Bottlenose Dolphins as Marine Ecosystem Sentinels:


Developing a Health Monitoring System

Randall S. Wells,1 Howard L. Rhinehart,2 Larry J. Hansen,3 Jay C. Sweeney,4 Forrest I. Townsend,5
Rae Stone,4 David R. Casper,6 Michael D. Scott,7 Aleta A. Hohn,8 and Teri K. Rowles9
1
Sarasota Dolphin Research Program, Chicago Zoological Society, c/o Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236
2
Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236
3
US Fish and Wildlife Service, Stockton, CA 95205
4
Dolphin Quest, 4467 Saratoga Avenue, San Diego, CA 92107
5
Bayside Hospital for Animals, 251 N.E. Racetrack Road, Fort Walton Beach, FL 32547
6
Long Marine Laboratory, University of California, Santa Cruz, CA 95060
7
Inter-American Tropical Tuna Commission, c/o Scripps Institute of Oceanography, La Jolla, CA 92037
8
National Marine Fisheries Service, Beaufort, NC 28516
9
National Marine Fisheries Services, 1315 East-West Highway, Silver Spring, MD 20910

Abstract: Bottlenose dolphins (Tursiops truncatus), as long-lived, long-term residents of bays, sounds, and
estuaries, can serve as important sentinels of the health of coastal marine ecosystems. As top-level predators on
a wide variety of fishes and squids, they concentrate contaminants through bioaccumulation and integrate
broadly across the ecosystem in terms of exposure to environmental impacts. A series of recent large-scale
bottlenose dolphin mortality events prompted an effort to develop a proactive approach to evaluating risks by
monitoring living dolphin populations rather than waiting for large numbers of carcasses to wash up on the
beach. A team of marine mammal veterinarians and biologists worked together to develop an objective,
quantitative, replicable means of scoring the health of dolphins, based on comparison of 19 clinically diagnostic
blood parameters to normal baseline values. Though the scoring system appears to roughly reflect dolphin
health, its general applicability is hampered by interlaboratory variability, a lack of independence between some
of the variables, and the possible effects of weighting variables. High score variance seems to indicate that the
approach may lack the sensitivity to identify trends over time at the population level. Potential solutions to this
problem include adding or replacing health parameters, incorporating only the most sensitive measures, and
supplementing these with additional measures of health, body condition, contaminant loads, or biomarkers of
contaminants or their effects that can also be replicated from site to site. Other quantitative approaches are also
being explored.

Key words: bottlenose dolphin, ecosystem health, sentinel species, risk assessment

INTRODUCTION

Published online: May 28, 2004 Bottlenose dolphins (Tursiops truncatus), can serve as
Correspondence to: Randall S. Wells, e-mail: rwells@mote.org important barometers of the health of marine ecosystems.
Bottlenose Dolphins as Ecosystem Sentinels 247

They are long-lived, long-term coastal residents in tropical toring efforts benefit from the fact that at least 60% of
and temperate regions throughout the world (Wells and inshore dolphins on the west coast of Florida are individ-
Scott, 1999; Reynolds et al., 2000). Long-term research on ually identifiable from dorsal fin features, facilitating direct
such a species allows one to document the history of counts and mark-recapture estimates (Wells, 2002; Wells
exposure to ecosystem perturbations and their effects. They and Scott, 1990; Wells et al., 1996a, 1996b, 1997). Using
are top-level predators on a wide variety of fishes and photographic identification techniques (Scott et al., 1990b;
squids, and thus concentrate contaminants through bio- Würsig and Jefferson, 1990) it is possible to define indi-
accumulation and integrate broadly across the ecosystem in vidual ranges (e.g., relative to contaminant sources) and
terms of exposure to environmental impacts. Dolphin measure female reproductive success as well as monitor
health and population status not only reflect the effects of population-level trends in abundance, losses, and other
natural and anthropogenic stressors on the species, but they vital rates (Wells and Scott, 1990). In addition, the shallow
serve as sentinels of the health and status of lower trophic waters of much of the habitat of inshore bottlenose dol-
levels in the marine ecosystem. phins facilitate safe capture and release operations, in which
Over the last 17 years, another reason to monitor bot- dolphins can be examined by veterinarians and sampled for
tlenose dolphin health and population status has emerged subsequent health-related analyses. This article focuses on
due to the occurrence of large-scale dolphin mortality the information for health assessment that can be derived
events. During 1987–1988, it was estimated that half of the from directly examining and sampling dolphins.
putative coastal migratory stock of bottlenose dolphins died
along the mid-Atlantic coast of the U.S. (Scott et al., 1988),
leading to a designation of this stock as ‘‘depleted.’’ Other APPROACH
unusual dolphin mortality events occurred in the northern
Gulf of Mexico in 1990, 1992, and 2000, in which hundreds Dolphins are captured for examination and sampling by
of bottlenose dolphins died (Hansen, 1992). A variety of encircling them with a 500 m · 4 m seine net in shallow
factors, such as environmental contaminants, natural bio- waters where handlers can safely stand and support dol-
toxins (Geraci, 1989), and morbillivirus (Duignan et al., phins as necessary. One at a time, each dolphin is trans-
1996; Lipscomb et al., 1996), have been suggested as prob- ferred to foam pads on the shaded deck of a boat, where it
able agents responsible for the mortalities. In each of these is weighed and a standard series of length and girth mea-
cases, conclusive determination of the cause of death was surements is collected. Adult females are first given an
hampered by a shortage of fresh carcasses to allow all desired ultrasound examination for pregnancy before a decision is
tests to be performed. Evaluation of the impacts of the made to bring them aboard the vessel. Throughout the
mortalities was hampered by inadequate background examination, behavior and respiratory patterns are closely
information on dolphin stock structure, abundance, life monitored, and water is sponged over the animals. Blubber
history, and vital rates prior to the mortalities. The lesson depth is measured ultrasonically at standard sites.
reinforced by each subsequent investigation is that a pro- Abdominal and thoracic organs are evaluated via ultra-
active approach to evaluating risks by monitoring living sound examination. Core body temperature is measured
dolphin populations would be preferable to waiting for large through a colonic probe. Blood samples (up to 320 ml) are
numbers of carcasses to wash up on the beach. collected through venipuncture from a vessel in the fluke.
The authors have been developing methods for Blood samples are: 1) analyzed for standard chemistry,
assessing the population status and health of coastal bot- hematology, and reproductive hormones; 2) used for
tlenose dolphins, not only to monitor the risks to the immunological studies; 3) applied to genetic studies
populations themselves, but also to be able to use them as including paternity analyses; 4) examined for circulating
sentinels of the health of marine ecosystems. Much of this levels of environmental contaminants; and 5) stored for
work has occurred in Sarasota Bay, Florida, where research retrospective investigations of disease processes. Urine is
on the resident dolphin community has been ongoing since obtained through sterile catheterization. Milk is expressed
1970, and where four generations of identifiable individuals into a custom suction collection system for compositional
of known gender, age, and genetic relationships are cur- analyses and measurements of environmental contami-
rently under study (Irvine and Wells, 1972; Irvine et al., nants. Samples for evaluation of the presence or absence of
1981; Scott et al., 1990a; Wells, 1991). Population moni- a suite of microorganisms are collected from the blowhole,
248 Randall S. Wells et al.

feces, and genital tracts. Small blubber wedges (4-cm long ·


Table 1. Data Sources for Development of Health Assessment
3-cm wide · up to 1.5-cm deep) are obtained under local
Protocol of Bottlenose Dolphins (Tursiops truncatus) in Sarasota
anesthesia from a standard location below the dorsal fin,
Bay, Florida
for contaminant analyses. Most of the Sarasota Bay resi-
dents are of known age through observation, but a tooth is Collected from Sarasota
collected under local anesthesia from individuals of un- Data Bay dolphins since
known age for sectioning and counting of growth layer Blood chemistry and hematology 1987
groups (Hohn et al., 1989). A full examination and sam- Microbiology 1990
pling program typically requires about 1 hour, and then the Results of physical examinations 1984
dolphin is returned to the water and released. More than Sex, age, morphometrics, life history 1984
180 individuals have been examined in Sarasota Bay to Body condition: weight, 1986
date. Similar sampling was conducted by the National girth, blubber depth
Marine Fisheries Service (NMFS) in Matagorda Bay, Texas Diagnostic ultrasound examination 1990
Results of necropsies performed 1985
in 1992 (n = 36 dolphins) and near Beaufort, North Car-
by Mote Marine Laboratory
olina in 1995 (n = 31 dolphins) (Hansen and Wells, 1996).
Population vital rates 1980
The bottlenose dolphin health assessment program ini-
Behavior: ranging and social patterns 1970
tiated 17 years ago continues to evolve. Blood sampling for Blubber biopsy wedges 1997
health assessment was begun in Sarasota Bay in 1987 in order Blood/milk for contaminant analyses 1988
to develop medical histories and track cases involving the Urinalysis 1993
well-known Sarasota Bay residents, and to develop a baseline
for comparison with dolphins at other sites and held in
zoological park settings. With the advent of large-scale dol-
The workshop participants, including marine mammal
phin mortalities in the late 1980s and early 1990s, the vet-
veterinarians, an epidemiologist, and biologists specializing
erinary team developed a health evaluation system, assigning
in life history, behavioral ecology, physiological ecology,
a grade to each dolphin based on a clinical assessment. This
and microbiology considered and integrated the following
system was first applied in response to the Matagorda Bay
kinds of data in their evaluation of the health of the indi-
mortality event in 1992. Building upon this concept, a
vidual dolphins and the Sarasota Bay dolphin community
NMFS-sponsored workshop was held in Sarasota in October
(Table 1). Records for each individual dolphin were com-
1993 to attempt to apply information on health parameters
piled, sorted, summarized, and distributed to a set of
for free-ranging bottlenose dolphins to the development of a
experienced marine mammal veterinarians in advance of
method for evaluating the health of dolphin populations.
the workshop (Rhinehart et al., 1991, 1992). The veteri-
The specific goals of the workshop were as follows:
narians graded each of the dolphins based on all of the
1. Develop and refine a ‘‘grading system’’ for the health of available information from each capture. The grading sys-
individual animals examined and sampled during the tem evaluated each animal as if it were a captive dolphin
annual Sarasota bottlenose dolphin capture–release with access to regular veterinary attention.
project, based on consideration of the full range of At the workshop, the biologists worked with the vet-
health and condition parameters measured. The grading erinarians to evaluate their grading system, and to identify
system should be based on defensible, objective criteria; the most informative health parameters of those that have
2. Develop and refine a system to extrapolate the individ- been or could be measured regularly and reliably in the
ual animal grades to a seasonal grade for the population field. The authors evaluated a variety of potential assess-
as a whole based on the animals sampled during a given ment parameters, including 56 blood hematology and
season; chemistry measures, weight, girths, blubber depths, and the
3. Identify the indicators of greatest value in assessing the presence or absence of 80 microorganisms. These param-
overall health of an individual or population; and eters were evaluated relative to the sex, age, and repro-
4. Relate trends in population health grades to trends in ductive condition of each individual, and the type of
population parameters such as mortality or loss rates, sample (serum vs. plasma) and the analytical laboratory
natality, and fecundity. used (Specialty Veterinary Laboratory Services [SVLS],
Bottlenose Dolphins as Ecosystem Sentinels 249

Santa Cruz, CA vs. SmithKline-Beecham, locations only one of alanine amino transferase (ALT), gamma
throughout the US). From this list, we selected a set of the glutamyl transferase (GGT), and aspartate aminotransfer-
most indicative parameters that allowed us to develop a ase (AST) was used for any given score (the highest value of
quantitative measure of the health of each individual. A the three was used), but in the absence of any two of these,
mean annual health score for the population as a whole was the other was acceptable for scoring. The higher of the
calculated. The scores provided a set of tentative baseline values for hemoglobin and hematocrit was selected. Simi-
values for comparison with other populations. larly, the total leukocyte count (WBC) would have dupli-
cated scoring of the leukocyte differential, so only the
differential was scored.
HEALTH ASSESSMENT SCORING SYSTEM The reproductive condition, age class, and analytical
laboratory affected some variables. Hemoglobin and
The workshop participants developed a dolphin health hematocrit were scored differently for lactating vs. non-
assessment scoring system. The ontogeny of the system lactating females. Alkaline phosphatase (AP) was scored
involved several steps. In its initial form, the concept of an differently for calves/juveniles, subadults, and adults.
‘‘expert system’’ in which health grades were assigned Comparisons of health scores between age classes within
subjectively by the members of a team of marine mammal genders found a significant difference (P < 0.01) only be-
veterinarians was explored. The need for a replicable, tween adult and subadult females, with subadults exhibit-
objective system led to the integration of the clinical ing better health (mean = 3.0, SD = 2.70, n = 25 vs. adult
experience approach with a mathematical approach. As a female mean = 5.6, SD = 4.64, n = 38).
result, an algorithm using a weighted scoring for values of a Consistent differences between the two laboratories
selected set of 19 blood parameters was derived (Table 2). used prior to the workshop (SVLS and SmithKline-Bee-
The 19 blood parameters were selected on the basis of their cham) led to different scoring for albumin, globulin, and
stand-alone value as indicators of dolphin health and po- bilirubin. SmithKline-Beecham was selected as our stan-
tential facility of replicable measurement across field sites. dard laboratory due to widespread availability of linked
‘‘Normal’’ baseline ranges were established for each laboratories throughout the U.S. However, after 1995
parameter, based on the clinical experience of the veteri- SmithKline-Beecham no longer performed analyses on
narians and on the values obtained from the free-ranging veterinary samples. Subsequent analyses were performed by
Sarasota dolphins. Values presented in the ‘‘0 Points’’ a variety of laboratories (University of Miami, Sea World,
column of Table 2 were considered ‘‘normal.’’ Each Cornell University) in an attempt to find one that was both
parameter was scored on the basis of its deviation from easily accessible and would perform reliably all 19 of the
‘‘normal’’ range. Scores were weighted according to the analyses required by the scoring system. For example, some
relative medical importance of the particular parameter, as laboratories would not perform analyses for iron or
assigned by the veterinarians. Each animal then received a erythrocyte sedimentation rate. As a result, the data pre-
grade that was based on the sum of the point scores for sented here reflect only the 1990–1995 period during which
each of the parameters. The four possible grades included: a consistent laboratory (SmithKline-Beecham) performed
all 19 analyses.
A (0–4 points)—The dolphin is apparently in good health,
with no obvious medical problems or need for follow-up
medical attention. EVALUATION OF THE HEALTH SCORING
B (5–9 points)—The dolphin would benefit from a follow- SYSTEM
up veterinary examination.
C (10–19 points)—The dolphin would benefit from The 1990–1995 dataset yielded 145 health scores from 80
medical treatment. different dolphins. These were collected during seven
D (>20 points)—The dolphin has a serious medical sampling sessions: June of 1990 (n = 20), 1991 (n = 29),
problem that requires treatment. 1992 (n = 27), 1993 (n = 17), 1994 (n = 24), and 1995 (n =
13), and during February of 1993 (n = 6) and 1994 (n = z9).
Several parameters were considered to be duplicative In total, 130 scores were from summer samplings and 15
and therefore interchangeable if necessary. For example, were from winter samplings. Sampled dolphins included
250 Randall S. Wells et al.

Table 2. Baseline Blood Values, and Points Scored If Outside of the Baseline Values of Bottlenose Dolphins (Tursiops truncatus) in
Sarasota Bay, Floridaa

Points

Parameterb Units 0 2 5 10
1 Sodium mEq/L 140–159 160–165 135–139, >165 <135
2 Potassium mEq/L 2.0–4.4 4.5–4.9 ‡5.0
3 Phosphorus mg/dl <7.0 ‡7.0 (if adult)
4a Albumin (SVLS) g/dl ‡3.5 <3.5
4b Albumin (SmithKline) g/dl ‡3.0 <3.0
5a Globulin (SVLS) g/dl 2.0–3.5 1.5–1.9 <1.5
5b Globulin (SmithKline) g/dl ‡3.0 2.5–2.9 <2.5
6a Bilirubin (SVLS) mg/dl 0.1–0.9 ‡1.0
6b Bilirubin (SmithKline) mg/dl 0.1–0.4 0.5–0.9 ‡1.0
7 Alkaline phosphatase—AP U/L
7a Calf/juvenile (0–4.9 years) U/L ‡150 <150
7b Subadult (5–11.9 years) U/L ‡100 <100
7c Adult (12 + years) U/L ‡50 <50
8a Alanine aminotransferase—ALT (or GGT or AST) U/L <40 40–49 50–99 ‡100
8b Aspartate aminotransferase—AST (or GGT or ALT) U/L <300 300–399 400–999 ‡1000
8c Gamma glutamyl transferase—GGT (or ALT or AST) U/L <30 30–49 ‡50
9 Blood urea nitrogen—BUN mg/dl <70 70–90 >90
10 Creatinine mg/dl <2.6 2.6–2.9 ‡3.0
11a Hemoglobin—Hb (or hematocrit) g/dl ‡13 12.0–12.9 <12.0
11b Lactating female g/dl ‡12.8 11.8–12.7 <11.8
11c Hematocrit—HCT (or hemoglobin) % ‡40 38–39 <38
11d Lactating female % ‡39 37–38 <37
12 Mature neutrophils—Segs /mm3 2000–5999 6000–6499 6500–9999 ‡10,000
13 Band neutrophils—Bands /mm3 <500 500–999 ‡1000
14 Lymphocytes—Lymphs /mm3 ‡1000 800–999 <800
15 Monocytes—Monos /mm3 <400 ‡400
16 Eosinophils—Eos /mm3 <5000 ‡5000
17 Plateletsc /mm3 ‡75,000 50–74,999 <50,000
18 Ironc lg/dl ‡100 80–99 <80
19 Erythrocyte sedimentation rate—ESRc mm/hour <50 ‡50

SVLS, Specialty Veterinary Laboratory Services; SmithKline, SmithKline-Beecham.


a
Health grades are the sums of the scores for each parameter: A = 0–4; B = 5–9; C = 10–19; D = ‡20. Only first capture values were used if recaptured during a
single year.
b
Consider relative to age, body condition, and reproductive condition.
c
Parameters measured since 1990.

both genders (67 male vs. 63 female), and ages ranged from year during the period of our study, but the variance sur-
1 to 49 years. Age classes were assigned on the basis of age rounding these annual means was high (Table 3).
and/or reproductive status (adult = has given birth, has Possible relationships between dolphin health scores
reproductive hormone concentrations indicating maturity, and mortality patterns, as one extreme of health, were
or >10 years old). Samples were classified as 52 from examined using three measures: 1) total number of Tursiops
juveniles and calves (27 male vs. 25 female) and 78 from strandings recovered by Mote Marine Laboratory, as an
adults (40 male vs. 38 female). Population health score indication of health conditions across a broad geographic
means exhibited a high level of consistency from year to area; 2) losses of known Sarasota residents of all ages; and
Bottlenose Dolphins as Ecosystem Sentinels 251

Table 3. Summer Health Scores of the Bottlenose Dolphin


(Tursiops truncatus) Population in Sarasota Bay, Florida, 1990–
1995

Year Mean SE Ranges n


1990 4.9 1.08 0–17 20
1991 4.0 0.85 0–20 29
1992 5.3 0.97 0–16 27
1993 5.5 1.12 0–19 17
1994 6.5 1.45 0–32 24
1995 4.5 1.27 0–12 13

3) losses of known Sarasota residents of >1 year of age (the


category most directly comparable to the set of animals
sampled for the health assessment scoring). No correlation Figure 1. Seasonal distribution of bottlenose dolphin (Tursiops
was found between the total number of strandings and truncatus) strandings investigated by Mote Marine Laboratory in
health scores for any given year. Positive correlations were the Sarasota Bay area during 1990-1995. Residents are known from
obtained between annual health scores and losses of known long-term research based on individual identification (n = 17
Sarasota dolphins when 19 blood parameters were con- residents).
sidered, but the correlations were not statistically signifi-
cant. When only 16 blood parameters were considered FB19, an adult female, maintained a ‘‘B’’ grade during five
(reflecting limitations provided by some laboratories), no samplings from 1988 through 1991. She declined to a ‘‘C’’ in
correlation was found. These results suggest that the health June 1993, and died, at 50 years of age, in January 1994.
index might benefit from further refinement through the FB97, a dependent female calf, received a ‘‘C’’ score in June
inclusion of additional parameters. 1989, and disappeared several months later. FB206, a
Significant seasonal variations in health scores were stranded adult male, arrived at Mote Marine Laboratory in
identified for Sarasota Bay dolphins, and these matched the June 1993 with a score of 42 (‘‘D’’). He underwent medical
seasonal patterns for mortality and physiological measures. treatment for 107 days, before being reintroduced to the
The mean summer population 19-parameter health score for wild. Upon release, his score had improved to 9 (‘‘B’’) and he
the period 1990–1995 (mean = 5.5, SD = 5.89, n = 65) was was observed in the wild 6 months later in apparently good
significantly (P < 0.01) greater than the mean winter health condition. Thus, the scoring system appears to accurately
score for the same period (mean = 3.3, SD = 2.02, n = 15), track individual medical conditions in at least some cases.
scoring each individual only once. The season of highest
health scores (=poorest health), spring/summer, corre-
sponds to the period of highest mortality of Sarasota Bay FUTURE OF THE HEALTH SCORING SYSTEM
dolphins as indicated from recovery of carcasses of known
residents (Fig. 1). Similarly, higher metabolic rates were Though the scoring system in its current form appears to
measured for Sarasota Bay dolphins during summer than in roughly reflect dolphin health, its general applicability is
winter (Costa et al., 1995), suggesting the occurrence of hampered by several factors. Interlaboratory variability is
thermal stress during summer associated with difficulties in perhaps the most serious problem associated with the
dumping heat that might contribute to health challenges. blood parameter health scoring method. The requirement
The summer period of poorer health follows a seasonal de- of using the same laboratory/analytical techniques in order
crease in blubber thickness. The possibility that this decrease to be able to identify trends over time within a site/indi-
may involve the mobilization of stored contaminants, with vidual or to make valid comparisons across sites has been
potential health consequences, warrants further attention. problematic. Variability due to different analytical tech-
The validity of the scoring system approach was further niques across laboratories, changes in laboratory availabil-
supported anecdotally by several case histories. For example, ity, and the occasional lack of availability of analyses of
252 Randall S. Wells et al.

some of the critical blood parameters can negate the utility size was small. Though as yet unconfirmed, one possible
of this additive approach. Missing values potentially bias explanation for the high rate of first-born calf mortality in
the health scores downward. The blood parameter algo- Sarasota Bay (Wells et al., 2001, 2003) may relate to transfer
rithm also suffers from a lack of independence between of environmental contaminants from mother to calf, as
some of the variables, and the possible effects of weighting described by Cockcroft et al. (1989) for dolphins in South
variables remain to be evaluated. Africa. Vedder (1996) provided some support for this
The high variance associated with the scores resulting hypothesis in her findings from analyses of Sarasota Bay
from the current health assessment scoring system seems to dolphin milk from females of different ages and repro-
indicate that the approach may lack the sensitivity to ductive histories, in which she noted apparent depuration
identify trends over time at the population level. We are of contaminants. Similarly, Küss (1998) found elevated
examining several potential solutions to this problem. One PCB and chlorinated pesticide concentrations in carcasses
refinement might be to consider adding or replacing health of young Sarasota Bay resident dolphins followed by a
parameters, incorporating only the most sensitive mea- decline in maturing individuals, and subsequent increase as
sures. The initial approach of limiting the scoring system to males aged, and decline or steady state at lower concen-
blood parameters was in part an attempt to obtain objec- trations as females reared offspring. Schwacke et al. (2001)
tive, quantitative, comparable measures regardless of the and Wells et al. (2003) identified a similar pattern from
specific composition of the investigating team or the analysis of blubber samples from living Sarasota Bay dol-
location of the research site. However, it may be advisable phins. Significant challenges remain in identifying the
to identify a subset of blood parameters of clinical signifi- specific chemicals, congeners, concentrations, interactive
cance that can be measured most reliably across laborato- effects, and biomarkers (e.g., DNA damage: Gauthier et al.,
ries, and supplement these with additional health or body 1999) of greatest importance to dolphin health, and the
condition measures that can also be replicated from site to most appropriate and accessible sites for sample collection,
site. For example, age/sex/season-specific weights, girths, recognizing that contaminants are not distributed uni-
and blubber depths could provide important measures of formly through blubber (O’Shea, 1999).
body condition. Measures of thermal characteristics from The authors are also beginning to approach the con-
colonic temperatures, surface temperatures, heat flux, or cept of population health assessment from a different
thermal imaging could provide indications of health status quantitative perspective. Given that large-scale health
(Meagher, 2001). Measures of immunocompetency could problems typically do not affect all members of a popula-
also be incorporated (Lahvis et al., 1993; Erickson et al., tion to the same degree or at the same time, it may be more
1995). Integration of data about skin lesions could be useful appropriate to examine health scores by looking in detail at
as well (Wilson et al., 1999). Ultrasonic imaging of organs individuals that are outliers, rather than at population
and microbiological cultures give insights into health, but means. Changes in the proportions of outliers over time
the means to quantify these data for inclusion in a scoring may provide a more meaningful and sensitive evaluation of
system remain to be developed. population trends and risks, as the outliers themselves may
As we begin to understand more about the effects of serve as potential sentinels of environmental problems.
environmental contaminants on dolphin health (O’Shea, This approach would also eliminate the need to compare
1999), incorporating measures of contaminant loads or specific parameter values directly from year to year, as the
biomarkers of contaminants or their effects becomes most important parameter comparisons would be within-
increasingly important. Even in a relatively nonindustrial- year. It should be possible to test this approach both within
ized area such as Sarasota Bay, inorganic and organic the Sarasota Bay reference population and across study sites
pollutants may be health factors. Rawson et al. (1993, 1995) as expanded bottlenose dolphin health assessment pro-
related mercury-associated pigment granules and liver grams are planned for the next several years.
disease to concentrations of mercury in stranded dolphins
from the Sarasota Bay area. Lahvis et al. (1995) reported an
apparent relationship between increasing concentrations of ACKNOWLEDGMENTS
organochlorine contaminants (PCBs and DDT metabolites)
and decreasing Sarasota Bay male immune system function Veterinary examinations and sampling were conducted
as indicated by lymphocyte proliferation, but their sample through the support of the National Marine Fisheries
Bottlenose Dolphins as Ecosystem Sentinels 253

Service, the U.S. Environmental Protection Agency, the Irvine B, Wells RS (1972) Results of attempts to tag Atlantic
bottlenose dolphins (Tursiops truncatus). Cetology 13:1–5
National Science Foundation, Earthwatch Institute, Dol-
Irvine AB, Scott MD, Wells RS, Kaufmann JH (1981) Movements
phin Quest, and the Chicago Zoological Society. W. and activities of the Atlantic bottlenose dolphin, Tursiops
Jarman, J. (Vedder) Greene, and associates conducted truncatus, near Sarasota, Florida. Fishery Bulletin (U.S.) 79:671–
preliminary analyses of contaminant levels in blood and 688
Küss KM (1998) The occurrence of PCBs and chlorinated pesti-
milk samples. The participation of J. Buck, C. Driscoll, J.
cide contaminants in bottlenose dolphins in a resident com-
Reif, and G. Worthy in the 1993 Bottlenose Dolphin Health munity: comparison with age, gender and birth order. M.Sc.
Assessment Workshop provided valuable input for devel- Thesis, Nova Southeastern University, Ft. Lauderdale, FL
opment and evaluation of the approach. The field sampling Lahvis GP, Wells RS, Casper DR, Via CS (1993) In vitro lym-
phocyte response of bottlenose dolphins (Tursiops truncatus):
in Sarasota Bay benefited greatly from the efforts of B. mitogen-induced proliferation. Marine Environmental Research
Irvine, L. Fulford, K. Urian, S. Hofmann, K. Hull, and S. 35:115–119
Nowacek, along with a host of collaborating researchers Lahvis GP, Wells RS, Kuehl DW, Stewart JL, Rhinehart H, Via CS
(1995) Decreased lymphocyte responses in free-ranging bottle-
and volunteer dolphin handlers. This research was con- nose dolphins (Tursiops truncatus) are associated with increased
ducted under Scientific Research Permits Nos. 417, 655, concentrations of PCB’s and DDT in peripheral blood. Envi-
ronmental Health Perspectives 103:67–72
945, and 522-1569 issued by the National Marine Fisheries
Lipscomb TP, Kennedy S, Moffett D, Krafft A, Klaunberg BA,
Service. Lichy JH, et al. (1996) Morbilliviral epizootic in bottlenose
dolphins in the Gulf of Mexico. Journal of Veterinary Diagnostic
Investigation 8:283–290
Meagher EM (2001) Respiration, heart rate and heat flux across
the dorsal fin in bottlenose dolphins, Tursiops truncatus. M.Sc.
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