REVIEW
published: 13 December 2019
doi: 10.3389/fvets.2019.00444
Frontiers in Veterinary Science | www.frontiersin.org 1 December 2019 | Volume 6 | Article 444
Edited by:
Robert James Ossiboff,
University of Florida, United States
Reviewed by:
Alex M. Costidis,
Virginia Aquarium & Marine Science
Center, United States
Juan Manuel Campos Krauer,
University of Florida, United States
*Correspondence:
Ashley Barratclough
ashley[email protected]
Specialty section:
This article was submitted to
Zoological Medicine,
a section of the journal
Frontiers in Veterinary Science
Received: 06 September 2019
Accepted: 26 November 2019
Published: 13 December 2019
Citation:
Barratclough A, Wells RS,
Schwacke LH, Rowles TK,
Gomez FM, Fauquier DA,
Sweeney JC, Townsend FI,
Hansen LJ, Zolman ES, Balmer BC
and Smith CR (2019) Health
Assessments of Common Bottlenose
Dolphins (Tursiops truncatus): Past,
Present, and Potential Conservation
Applications. Front. Vet. Sci. 6:444.
doi: 10.3389/fvets.2019.00444
Health Assessments of Common
Bottlenose Dolphins (Tursiops
truncatus): Past, Present, and
Potential Conservation Applications
Ashley Barratclough
1
*
, Randall S. Wells
2
, Lori H. Schwacke
1
, Teresa K. Rowles
3
,
Forrest M. Gomez
1
, Deborah A. Fauquier
3
, Jay C. Sweeney
4
, Forrest I. Townsend
5
,
Larry J. Hansen
1
, Eric S. Zolman
1
, Brian C. Balmer
1
and Cynthia R. Smith
1
1
National Marine Mammal Foundation, San Diego, CA, United States,
2
Chicago Zoological Society’s Sarasota Dolphin
Research Program, Mote Marine Laboratory, Sarasota, FL, United States,
3
NOAA, National Marine Fisheries Service, Office
of Protected Resources, Silver Spring, MD, United States,
4
Dolphin Quest, San Diego, CA, United States,
5
Bayside Hospital
for Animals, Fort Walton Beach, FL, United States
The common bottlenose dolphin (Tursiops truncatus) is a global marine mammal
species for which some populations, due to their coastal accessibility, have been
monitored diligently by scientists for decades. Health assessment examinations have
developed a comprehensive knowledge base of dolphin biology, population structure,
and environmental or anthropogenic stressors affecting their dynamics. Bottlenose
dolphin health assessments initially started as stock assessments prior to acquisition.
Over the last four decades, health assessments have evolved into essentia l conservation
management tools of free-ranging dolphin populations. Baseline data e nable comparison
of stressors between geographic l ocations and associated changes in individual and
population health status. In addition, long-term monitoring provides opportunities for
insights into population shifts over time, with retrospective application of novel diagnostic
tests on archived samples. Expanding scientific knowledge enables effective long-term
conservation management strategies by facilitating informed decision making and
improving social understanding of the anthropogenic effects. The ability to use bottlenose
dolphins as a model for studying marine mammal health has been pivotal in our
understanding of anthropogenic effects on multiple marine mammal species. Future
studies aim to build on current knowledge to influence management decisions and
species conservation. This paper reviews the historical approaches to dolphin health
assessments, present day achievements, and development of future conservation goals.
Keywords: dolphin, Tursiops truncatus, conservation, health assessment, veterinary medicine
INTRODUCTION
Assessment of marine mammal health is complex, both from an accessibility standpoint and from
the diverse array of factors influencing both individual and population survival. Baseline data are
particularly crucial to evaluate whether population, or in some cases species, health is deteriorating
by providing points of comparison to assess trends in disease, mortality, and reproductive rates (
1).
From a veterinary perspective, a hands-on physical exam is the optimal approach to provide critic al
Barratclough et al. Bottlenose Dolphin Health Assessments
information for a comprehensive understanding of both
individual and population-level health status. Knowledge gained
from physically examining smaller cetaceans can be extrapolated
to larger, less-accessible cetaceans to improve understanding of
the complexities of adverse health impacts on marine mammal
conservation. The common bottlenose dolphin (Tursiops
truncatus) is an effective model species for understanding both
cetacean and marine ec osystem health.
The overarching aim of conservation is to actively preserve
habitats and the diversity of species dwelling t h erein (
2). Effe ctive
conservation benefits from a foundation of sound scientific
understanding of species’ biology, population dynamics, and
stressors impacting the ecosystem (3). Marine ecosystem health
is particularly challenging to assess due to immense biological
diversity, as well as t he vast scale and connectivity of the ocean
environment. Multiple factors threaten marine mammal health
(
4); therefore, improving k nowledge of the interplay of these
factors and predicting their long-term effects are essential for
successful conservation.
The emerging discipline of conservation physiology is
particularly important in the marine environment, as it allows
a mechanistic understanding of the drivers of conservation
obstacles at an ecosystem level, in addition to species-specific
challenges. Understanding how species physiologically respond
to environmental alterations is important for successful tailored
conservation strate gies (5). The rate of expansion of the human
population is exacerbating the challenges faced by wildlife with
frequently detrimental consequences to their health (6). The
unprecedented changes occurring in the environment on a
global s cale require novel mitigation strate gies to ensure effective
conservation actions and sustainable wildlife populations (
7).
There is limited understanding of the scale of the negative
anthropogenic impact on marine mammal biodiversity.
Currently 29.2% of marine mammal species are classified as
data deficient according to the International Union for the
Conservation of Nature (8). As a result, shifts in population
viability can be difficult to detect, as the basic natural history
of the species has not been documented (9). Intrinsic traits of
species can be more important predictors of risk than extrinsic
environmental factors, as they provide a measure of the species’
inherent susceptibility to human impacts and the ability of
species to recover from them (
10). The bottlenose dolphin is
one of the most closely studied and widely distributed marine
mammal species and provides an opportunity to extrapolate
knowledge and understanding to other marine mammal species.
HISTORICAL PERSPECTIVE
Initially the first common bottlenose dolphin captures occurred
for acquisition for public display, research, or for stock
assessment prior to collection. Over time health assessments
of inshore dolphins have been utilized to better understand
endemic disease, establish baseline physiological measures,
and evaluate exposure to, and potential effects of, chemical,
biological, and physical stressors. Historically, health assessments
developed as additions to existing capture-release efforts for
other purposes, such as marking/tagging and population-lev el
studies to understand movement patterns and site fidelity.
Starting in 1979, Hubbs/SeaWorld Research Institute began
collecting bottlenose dolphin health data in the Indian River
Lagoon of east Florida during capture-release operations to
assess potential population-level impacts in advance of upcoming
zoologic colle ct ions (Figure 1) (
11). Analyses from the samples
and data collected included morphometrics, blood biochemistry,
hematology and reproductive endocrinology, microbiology,
genetics, and life history studies (12). Similar research was
initiated by Marine Animal Productions in 1982 in Mississippi
Sound, with the inclusion of skin, blubber, and liver tissue
sampling in some cases, t o establish a health baseline for dolphins
inhabiting this area, again prior to collections and for comparison
with managed animals (13).
The Sarasota Dolphin Research Program (SDRP) began
incorporating additional biological samples and measurements
in 1984 to their original capture-release program. This supported
tagging and telemetry studies in Sarasota Bay, Florida, which
were initiated in 1970. The inclusion of additional biological
samples shifted the focus from studies of population range
and social patterns to broader scientific investigations of life
history, population dynamics, body condition and health, social
structure, communication, reproductive success, and effe cts of
human interactions. Samples and measurements included in-
depth bloodwork analyses, genetic tests for population structure
and paternity, ultrasonic measurement of blubber thickness,
weight measurement, age determination (tooth growth layer
group counts), further development of tags and tag attachments,
and post-rele ase population monitoring (
14–19).
In 1992, the Marine Mammal Health and Stranding Response
Program was formalized within the National Marine Fisheries
Service (NMFS) through an amendment to th e Marine Mammal
Protection Act (MMPA), establishing the stand ards for sample
collections and promoting collaboration and standardization
of bottlenose dolphin health assessments (20). In 1995, NMFS
conducted health assessments in response to the 1987–88
mortality event along the east coast of the U.S., in which over
600 bottlenose dolphins stranded as a result of a large-scale
morbillivirus epizootic (21–25). Additional studies were also
conducted to investigate unusual increases in dolphin strandings
near Matagorda Bay, Texas in 1992 (
26), and in the Florida
Panhandle in 2005–2006 (27) (Figure 1) (Table 1).
Supplementary c apture-release studies were initiated by the
National Oceanic and Atmospheric Administration (NOAA) in
support of stock assessment on the east coast, which was by
that time a requirement for NOAA’s NMFS (23, 24). Subsequent
capture-release studies used telemetry to understand population
structure along the Atlantic coast (39) following increased
dolphin mortality (40) which was eventually determined to be
associated with morbillivirus (22, 30). The studies found positive
morbillivirus titers in some dolphins sampled in estuarine and
coastal waters near Beaufort, NC, with no positive titers observed
in dolphins sampled in estuaries near Charleston, SC (
30).
This provided crucial information to understanding dolphin
population structure and interaction along the U.S. east coast,
with a mosaic of migratory, non-migratory but coastal, and
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Barratclough et al. Bottlenose Dolphin Health Assessments
FIGURE 1 | Bottlenose dolphin capture-release health assessment locations in the U.S.
small estuarine stocks rather than a single large population as
initially presumed. In addition utilizing archived Sarasota Bay
samples to retrospectively assess morbillivirus titers facilitated
further understanding of virus exposure, seroconversion, and
population naivety (41). Incorporating health assessments
informed scientists that at least some small, estuarine stocks
along the Atlantic coast were naïve to morbillivirus and therefore
particularly vulnerable (38).
In 2003, the Health and Environmental Risk Assessment
(HERA) population monitoring project was initiated for
bottlenose dolphins in the Indian River Lagoon, Florida (IRL),
and waters surrounding Charleston, South Carolina (CHS) (
42).
For both the IRL and CHS field sites, health assessments
were conducted to establish baseline data and to compare
morbidity temporally and across two geographic sites (
34,
43). Higher concentrations of persistent organic pollut a nts
(POPs) including legacy [e.g., dichlorodiphenyltrichloroethanes
(DDTs), polychlorinated biphenyls (PCBs)] as well as “emerging”
contaminants [polybrominated diphenyl ethers (PBDEs) and
perfluorooctane sulfonate (PFOS) compounds] were detected in
CHS dolphins as compared to IRL dolphins (43, 44). Mercury
concentrations in the blood and skin of IRL dolphins were
extremely high, approximately five times higher than those
in CHS dolphins. Higher exposure to many pathogens (e.g.,
morbillivirus and lobomycosis) was also observed for the IRL
dolphins (34).
The incorporation of health assessments into existing capture-
release protocols provided the collection of baseline health
data across multiple populations, thus allowing for investigation
of geographic variability in he a lth parameters (32, 42). The
methodologies established and samples collected during these
earlier projects formed the b asis for developing a risk assessment
framework to quantify the impacts for dolphins affected by
anthropogenic threats (e.g., Deepwater Horizon oil spill) in
geographical areas where baseline data were not available (
36).
THREAT IDENTIFICATION AND
ASSESSMENT
Dolphin capture-release projects provide a unique perspective
to assess individual animal health and extrapolate to overall
health of the surrounding population, species, and ecosystem.
Over the past 40 ye a rs in the U.S., there have been numerous
stressors that have impacted bottlenose dolphin populations, for
which dolphin capture-release projects have been integral to
threat identification and quantification of impacts from a given
stressor (e.g., biotoxins, disease, environmental contaminants, oil
spills, etc.).
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Barratclough et al. Bottlenose Dolphin Health Assessments
TABLE 1 | Historical list of previous capture locations according to Figure 1 including number of animals examined or health assessments (HA) performed, purpose of
captures, and references.
Date Location Number of dolphins Purpose References
1979–1981 Indian River Lagoon FL 27
109 total HA
Population assessment (11)
1982 Mississippi Sound MS 57 Commercial assessment (
13, 28)
1984–2019
(ongoing)
Sarasota FL 289 individuals
811 total HA
Biological sampling, technique
development, reference
population
(
29)
1987 Virginia Beach VA 23 Mass mortality investigation (
21)
1992 Matagorda Bay TX 36 Mortality investigation (
26)
1995 Beaufort NC 31 HA post CeMV outbreak (
24)
1998 Virginia Beach VA 1 Stock assessment NOAA unpublished
data
1999 Charleston SC 14 Stock assessment (
30)
1999*
2000*
2006*
Beaufort NC 6
11
19
Stock assessment (
31)
(
30)
(
32)
2002–2003 Brigantine NJ 12 Stock assessment (
30)
2004 Holden Beach NC 10 Persistent organic pollutant
assessment
(
33)
2003–2018 Charleston SC
Indian River Lagoon FL
118
246
Comparative health studies (
34)
2005–2006 St. Joseph Bay FL 30 UME investigation (
27)
2009 Brunswick GA 29 HA legacy environmental
contamination
(
35)
2011–2018 Barataria Bay LA 202 DWH investigation (
36)
2013 Mississippi Sound MS 20 DWH investigation (
37)
2015 Brunswick GA 19 UME investigation (
38)
2018 Dauphin Island AL 18 DWH investigation
*
The numbers provided are for those where samples were used and published it does not necessarily provide a list of the total numbers of animals handled in this location.
Unusual Mortality Events
An unusual mortality event (UME) is defined under the
U.S. Marine Mammal Protection Act as “a stranding that is
unexpected; involves a significant die-off of any marine mammal
population; and demands immediate response.” The UME
program was officially established under Title IV of the MMPA
in 1992. Increased recognition of the occurrence of large scale
dolphin mortality events in the late 1980s spurred the application
of dolphin health assessments beyond population monitoring, to
investigating causes and effects of such mortality events (
21, 24).
Since 1999, a series of UMEs occurred along the northwestern
Florida coastline (Florida Panhandle) including St. Joseph Bay
(45). NOAA conducted two dolphin health assessments during
2005 and 2006 in response to these UMEs in which 30
dolphins were sampled and subsequently t agged (27) (Table 1).
The initial mortalities were tentatively attributed to biotoxins
from red tide algae (Karenia brevis) (
46). Eosinophilia was
obser ved in 23% of sampled dolphins, with associated increased
neutrophil phagocytosis and T-lymphocyte proliferation (27).
Chronic low-level exposure to another algal toxin, domoic acid,
produced by the diatom Pseudo-nitzschia spp., previously linked
to eosinophilia, was also identified (
47). Prior to these UMEs,
little was known about dolphin abundance, distribution, and
site fidelity in this region, and thus, it was unclear which
population(s) of dolphins were impacted (
48, 49). Post-health
assessment tagging data suggested that the timing and spatial
extent of biotoxin events and other potential stressors in the
Florida Panhandle may greatly influence the severity of future
UMEs (50). Cetacean post-mortem examinations can provide
insight into identifying the underlying cause of a UME in
addition to baseline data on disease presence and anthropogenic
causes of mortality (51–53). Increased integration of live animal
assessment with post-mortem findings encourages the transfer
of information from the dead to the living, informing scientists
of the underlying pathophysiological mechanisms faced within
free-ranging populations (
54).
Chemical Pollutants
The presence of PCBs and other lipophilic contaminants have
been recorded to be accumulating in the tissues of bottlenose
dolphins and other odontocetes for decades (
31, 55–59). Many
marine mammals, particularly piscivorous species, have a high
potential to biomagnify pollutants (
33), with increased levels
resulting from the high trophic position and blubber acting as
a reservoir for lipophilic contaminants (
60). Bot h experimenta l
and observational studies support the correlation between
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Barratclough et al. Bottlenose Dolphin Health Assessments
increased PCB levels and endocrine dysfunction, compromised
immunity, and/or reproductive failure (61–66). However, the
common co-occurrence of similarly acting compounds and
uncertainty regarding species-specific dose response functions
makes assessment of th e effects of these contaminants at a
population level challenging (
60, 67).
In addition to their applicability to investigating UMEs,
dolphin health assessments have also been used to investigate
health of populations at risk from environmental contaminants.
For example, dolphins along the Georgia coast have been
identified wit h some of the highest concentrations of PCBs in
the world, and these levels are site-specific to a Superfund Site
in Brunswick, Georgia (60, 68, 69). In 2009, NOAA conducted
health assessments on 29 dolphins in the region and identified
a high proportion (26%) of sa mpled individuals suffered
from anemia (66). In addition, these dolphins had reduced
thyroid hormone levels with total thyroxine, free t hyroxine, and
triiodothyronine negatively correlated with increased blubber
PCB concentrations. T-lymphocyte proliferation and indices of
innate immunity decreased with blubber PCB concentration,
suggesting an increased susceptibility to infectious disease (
66).
As with previously described health assessments, telemetry and
photo-ID data provided perspective on ranging patterns relative
to exposure, subsequent reproductive success, and effects of
long-term impacts from cumulative stressors (70). In 2015,
another health assessment was conducted in Georgia to look at
potential impacts associated with a recent morbillivirus-caused
UME and extremely high levels of PCBs t hat were identified from
previous studies. Dolphin morbillivirus titers differed between
dolphins sampled in coastal and estuarine waters, and tagging
data identified some degree of overlap between these individuals.
This study suggested that estuarine dolphins in this region may
be highly susceptible to future morbillivirus infections as a result
of elevated PCB levels and spatial overlap between coastal and
estuarine dolphins that would facilitate disease transmission (
50).
Petroleum Toxicity
In 2010, the largest marine oil spill in the history of the U.S., the
Deepwater Horizon oil spill (DWH), occurred in the northern
Gulf of Mexico (GoM). Subsequently a multidisciplinary
approach for evaluating the impacts upon cetaceans was
undertaken (
71, 72). Bottlenose dolphins were the focal cetacean
species examined due to the accessibility of dolphins in shallow
coastal and estuarine waters, and the heavy oiling in some of
those same nearshore areas. Health assessments in heavily oiled
areas, particularly Barataria Bay, Louisiana, were initiated as
part of NOAA’s Natural Resource Damage Assessment (NRDA).
Veterinary clinical assessment of dolphins living within the
oil spill footprint found significant lung pathology, impaired
stress responses, high reproductive failure, and altered functional
immunity, as compared to findings from un-oiled reference
populations (35, 73–75). After the DWH oil spill, an abnormally
high prevalence of lung and adrenal gland pathologies were
documented in post-mortem examinations (
73, 76). Identifying
the baseline incidence of disease in stranded dolphins and
diagnosing pathology in live dolphins through the application of
enhanced health assessment protocols was required to determine
if these findings were correlated with the recent environmental
exposure (75, 77, 78).
Determining a causal link for the multiple pathologies
obser ved post DWH oil exposure has been via a diagnosis of
exclusion; concluding the toxic effects of the oil spill as the
primary differential to both the observed path ologies and the
increased dolphin mortality (
71, 75). Other differential diagnoses
that were the potential causes of previous GoM UMEs were also
ruled out including biotoxins (79), POPs (68), and infectious
disease (45, 73, 80, 81). Successive health assessments during
2016–2018 have provided additional insight into the chronic
health effects. Longitudinal photo-ID surveys allowed estimation
of post-spill survival rate (0.80–0.85) and reproductive success
(20%), the latter was very low for this population (82, 83).
Long-term consequences from oil contamination are difficult to
assess but have been suggested in other marine mammals such
as the killer whale (Orcinus orca) and the sea otter (Enhydra
lutris nereis) (
84–87). Future research efforts will aim to improve
understanding of the transgenerational or in utero exposure
effects in a ddition to the direct exposure of those animals alive
at th e time of the oil spill.
Currently there is limited knowledge of the pathophysiology
of reproductive failure in bottlenose dolphins. Improved
understanding of the normal physiological changes occurring
during gest a tion in successful pregnancies will aim to elucidate
possible mechanisms of reproductive failure and identify
abnormalities occurring during failed pregnancies. This
knowledge will be essential to help understand reproductive
challenges, not only for common bottlenose dolphins,
but also for the future management of other cetaceans,
some critically endangered, to help to understand the
reproductive challenges faced in these species and improve
future conservation management.
CAPTURE AND HANDLING
METHODOLOGY
The standard approach to capt ure small (1–5) numbers of
bottlenose dolphins in shallow waters is by encirclement with
a seine net up to 500 m long and 7 m deep (
88, 89). Shallow
water (<1.5 m), minimal currents, and a solid seafloor are
optimum for safe capture and restraint. The seine net is deployed
from a specially designed boat at high speed around the target
dolphin(s), creating a compass (Figure 2A), with well-trained
handlers distributed around the circumference to provide aid
and restraint when the dolphins contact t he net (Figure 2B)
(29). If capture occurs in deep water (>1.5 m), the net compass
can be pulled into nearby shallow water, or th e dolphins are
handled from the side of response vessels and moved onto
specially designed floating mats that are eith er towed to shallow
water or directly onto a processing vessel for sample collection
(Figure 2C). Capture of individual dolphins in waters exceeding
the depth of seine nets has been performed via tail grabs
or hoop-nets, which are placed over the head of bow-riding
bottlenose dolphins or smaller cetacean species as they surface to
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Barratclough et al. Bottlenose Dolphin Health Assessments
FIGURE 2 | Capture methodology with (A) seine net deployed from a specially designed boat creating a compass in the center of the image, with chase boats circling
outside to help contain the animals before completion of the compass and to deliver handlers to the net (two dolphins are visible inside the compass on the left side).
(B) Shallow water set, well-trained handlers distributed around the circumference of the compass to provide aid and restraint when the dolphins contact the net. (C)
Deep water set, dolphin is placed onto a floating mat and disentangled from the net for transport to the processing vessel. All photos taken under NMFS MMPA/EAS
permit No. 18786-03.
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Barratclough et al. Bottlenose Dolphin Health Assessments
breathe (88–90). Once dolphins are s afely restrained, veterinary
examinations and sampling are performed.
VETERINARY PROCESSING
Current health assessment examinations require collaboration
among scientists from multiple disciplines and veterinary
specialties to obtain the maximum amount of information from
a single snapshot in time while the animal is in-hand. The
development of veterinary field techniques was enhanced by the
successful management of dolphins in human care. Sampling
varies according to research questions, but typically a suite of
baseline data are collected to maximize knowledge obtained from
a single veterinary exam (Table 2) (
91). Ensuring a standardized
approach to highlight the importance of inter-lab comparability
and sharing information between multiple institutions has
been paramount in the success of developing field collection
methodologies and subsequent sample analysis procedures (
32,
113). As described below, additional field procedures have been
incorporated over the decades as technology, field techniques,
and analytical assays have advanced, and as management needs
have evolved.
Determination of reproductive status (e.g., pregnancy , ovarian
activity, or testis size as an indicator of sexual maturity) using
diagnostic ultrasound was first applied in Sarasota Bay in
1989 (26, 114). Full-body ultrasound has subsequently been
proven to be an invaluable, rea l-time tool during dolphin
health assessments, pioneered by the National Marine Mammal
Foundation and the U.S. Navy Marine Mammal Program
(Figure 3) (
77, 97, 101–103). In addition, pregnancy may also
be diagnosed remotely by using blubber biopsy hormone levels
(115, 116). In some cases, post-release visual monitoring and
photographic-identification (photo-ID) have allowed researchers
to track the outcome of the pregnancy (that was determined by
ultrasound or remotely) and determine whether a viable calf was
produced (82, 116, 117).
A holistic approach of including dietary assessment into
the health exam along with urinalysis, blood (Figure 4), and
blubber sampling can aim to elucidate underlying causes
of health abnormalities. In the field, urinary catheterization
has enabled comparison with dolphins in managed care and
further developed the understanding of the development of
renal pathology in dolphins, especially when differences in
diets have been considered (
91, 97–99). Important ecological
perspectives can be obtained from diet a ry assessments, along
with information regarding prey availability and potential shifts
in environmental pressure affecting the ecosystem (118–121).
Further research is needed in this area to develop a more
standardized nutritional status indicator which can integrate
multiple measures. This could be used for example to improve
understanding of the effects of prey instability or environmental
stressors (122).
Electronic taggi ng technology to assess individual movement
or habitat use has rapidly advanced over the past 40 years so that
now small satellite-linked tags can be attached via a single-pin to
the dorsal fin and have minimal to no long-term effects on the
tagged individual (
70, 111). These tags provide fine-scale data on
individual animal movements for several months, post-rele ase,
and can provide additional insight into the cause of health effects
identified during the veterinary examination (37, 3 8, 117). The
movement pattern data from these electronic tags can also be
used to conduct follow-up monitoring to assess individual animal
health, survival, reproductive success, habitat use, and exposure
to th reats (
82).
MULTIDISCIPLINARY APPROACHES FOR
ASSESSING POPULATION HEALTH
Utilizing a multidisciplinary approach to combine clinical
veterinary knowledge with epidemiological analyses and
population modeling enables long-term forecasting of population
trajectories (36). In UMEs, modeling to estimate mortality based
on the number of stranded carcasses can provide insight into
the immediate losses to the population (71, 123–125). However,
integration of available health information and veterinary
interpretation of sublethal, chronic conditions, which are likely
to influence long-term survival and reproductive potential, can
provide a more accurate interpretation of the likely long-term
impacts on t he population (
36). Aside from impacts from acute
events such as oil spills, modeling has been used to simulate
the likely population-level consequences from sublethal effects
of chronic contaminant exposure (60, 67). Estimation of long-
term population effects resulting from mortality or morbidity
events is critical to inform restoration or recovery plans, and
also to appreciate the magnitude of the impact of UMEs on
population numbers or of environmental contaminants on the
surrounding ecosystem. A dvances in modeling application to
marine mammal stock assessments will greatly shape the future
of marine mammal conservation.
ADVANCES IN TECHNOLOGY AND
CONSIDERATIONS FOR ANIMAL
WELL-BEING
Dolphin health assessments provide fine-scale i nformation on
individual animals that can be extrapolated to evaluate overall
population health. While much can be learned from hands-
on health assessments, a major driver of current research is
to develop techniques to obtain maximum health assessment
information from remote sampling and observations. The
methodology for safely handling, sampling, and releasing
dolphins is continually evolving to minimize t h e risk to both the
dolphins and researchers, as well as maximize the data collected.
However, health assessments are still expensive, logistically
challenging, have limited target populations, and there is an
inherent risk when handling large animals (
126, 127). The
development of remote sampling te chnologies is essential to
build upon th e data collected during hands-on studies and to
expand our ability to efficiently and comprehensively assess the
health of dolphin populations beyond nearshore waters, as well
as the health of larger, less tractable cetacean species.
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Barratclough et al. Bottlenose Dolphin Health Assessments
TABLE 2 | List of veterinary processing sample collection from hands-on physical examinations during common bottlenose dolphin health assessments.
Procedure Description Use References
Blood sample
(Figure 4)
Obtained from the periarterial rete on the
ventral aspect of the tail fluke
Biochemistry
Hematology
Blood gas analysis
Endocrinology
Immunology
Serology
Genetics
(
23, 29, 30, 74, 91–93)
Surgical biopsy Full thickness wedge biopsies of skin and
blubber are routinely taken via an inverted
“L” block under local anesthesia from the
left lateral body wall caudal to the dorsal fin
Genetic population structure (skin)
Foraging ecology (skin)
Chemical contaminants (blubber)
Hormone levels (blubber)
Microbiome
(
31, 33, 49, 57, 94–96)
Urinalysis Bladder catheterization Renal function assessment
Dietary analysis
(
91, 97–99)
Tooth extraction Single tooth extracted under local
anesthesia
Age determination (
17, 100)
Ultrasonography
(Figure 3)
Thoracic and abdominal internal
assessment
Lung pathology
Reproductive Assessment
Full abdominal exam including renal
assessment
Blubber thickness
(
77, 97, 101–103)
Electrocardiography
(Figure 6)
Adapted field use in and out of water Cardiac assessment (
104)
Morphometrics
(Figure 7)
Standardized full body measurements:
lengths, girths, weight
Assess body condition and growth rates (
105)
Auditory evoked
potential
Portable unit adapted for field assessment
audiograms
Assess hearing range and sensitivity (
106)
Lesion biopsy Sample of abnormal skin lesions e.g., pox
or freshwater lesions
Histopathology (
57, 93)
Blow analysis
(Figure 5)
Exhaled breath vapor Pathogen and hormonal analysis
Metabolites
Respiratory function testing
(
107, 108)
Microbiology Swabs/culture plates from oral respiratory
or genital orifices
Bacteriology
Virology
(
109)
Freeze brand Dorsal Fin Identification (
110)
Feces and urine
collection
Swabs or catheter Biotoxin analysis (
46)
Skin biopsy
Electronic and/or
roto tagging
Skin sample from biopsy or during dorsal
fin tagging
Genetics, sex, stable isotopes identification
Ranging patterns reproductive status
Survival
(
70, 111, 112)
Application of new technologies to improve remote sampling
opportunities and maximize information obtained from cetacean
health assessments is pushing the boundaries of current marine
mammal science. Blow samples previously established when in-
hand (Figure 5) can now be obtained remotely utilizing UAVs
(unmanned aerial vehicles). Drones can be used to obt ain
aerial images to perform photogrammetry to assess health
via body condition in large whales unable to be examined
physically (107, 128). Drones can also be used in cetacean
disentanglement approaches to provide accurate assessment of
exact entanglement points and facilitate more informed decisions
on disentanglement methodology. Thermography has been used
to assess dolphin dorsal fin temperatures, as a measure of
individual health status representing appropriate integumentary
thermoregulation (
129), and now thermal imaging from drones
is being developed to apply to large whale health assessments.
Remote temperature assessment will be of increased value in
the future when potential climate change impacts could result
in cetaceans being exposed to higher or lower environmental
temperatures (
130–132).
Historically, the st a nd ard method of estimating the age
in dolphin health assessments is via tooth extraction under
local anesthesia and counting the growth layer groups present
on longitudinal section (17). Dental radiography has been
pioneered in an effort to replace the tooth extraction technique,
and validation of the technique is ongoing. Bone density
assessment has also been explored as a possible aging method,
however correlation with age across the entire lifespan was
limited (
133). A promising new methodology is the use of
pectoral flipper radiography to assess bone maturation (134).
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Barratclough et al. Bottlenose Dolphin Health Assessments
FIGURE 3 | Ultrasound examination of a lymph node on board the veterinary examination and sampling vessel (MMPA ESA Permit No. 18786-03).
FIGURE 4 | Blood sample collection from the peri-arterial rete on the ventral aspect of the tail fluke (MMPA ESA Permit No. 18786-01).
The dolphin pectoral flipper displays both hyperphalangy and
paedomorphosis enabling this method to be applied throughout
the entire lifespan due to the predictable chronological osteogenic
changes occurring to the metacarpal and phalangeal bones. This
non-invasive technology could facilitate age estimation for older
animals, replacing tooth extraction.
Additional biological information from remote biopsy dart
sampling is expanding on the knowledge gained from each
individual sample (
135). Currently, sex and population structure
of the animal can be determined from genetic analyses of
skin (112), and contaminant concentrations and stress and
reproductive hormone levels can be measured from blubber
biopsy (33, 116, 136). Present efforts are working toward using
skin to assess the epigenetics of the individual to give an
estimation of age (137). The NMMF are expanding on this even
further in line with recent human advancements to provide an
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Barratclough et al. Bottlenose Dolphin Health Assessments
FIGURE 5 | Exhaled breath sample collection for cytology (MMPA ESA Permit No. 18786-03).
FIGURE 6 | ECG leads attached during sampling and processing to closely
monitor the dolphin’s heart rate and assess cardiac function (MMPA ESA
Permit No. 18786-03).
indication of biological age (138). This emerging technology
could provide a means to assess increased environmental
pressure or poor health status (
139–141).
FIGURE 7 | Dolphin suspended in a stretcher for weight measurement via
load cell on board the veterinary processing vessel. This image was published
with permission of MMPA ESA Permit No. 18786-01 for the identifiable
individuals in the image.
Remotely deployed suction cup satellite-linked tags c an
provide short-term (<24 h) data on bioenergetics, respiratory
measures and cardiac data (
142, 143). An additional remote
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Barratclough et al. Bottlenose Dolphin Health Assessments
tool in development is the use of remotely attached single-
pin satellite-linked tags. These techniques will be particularly
useful in marine mammals where capture-release is impractical
due to size, species intolerance to handling or cost restraints.
Future research aims to combine different disciplines to expand
scientific knowledge further and inter-species application of new
technologies, for example, studying acoustic communication as a
proxy to changes in health status (
144, 145).
DISCUSSION
Health assessments with an epidemiological focus can aim
to understand the pathophysiology of disease and interpret
the demographic, anthropogenic, and ecological pressures
contributing to individual disease susceptibility (
146).
Extrapolating from individual health assessments to accurately
understand population health status, requires a strategic
epidemiological approach (
41, 147, 148). Inte grat ion of post-
mortem examinations within the health assessment framework
can provide additional projections from both diagnostic and
scientific perspectives aiming to contribute to identifying the
underlying cause of mortality and also predicting the future
impacts on the population. Performing pro-active marine
mammal health assessment examinations allows an opportunity
to examine population health under natural environmental
conditions, as opposed to during a mass stranding or UMEs.
This baseline knowledge of population health status can
aid understanding of post-mortem examinations during
UMEs and ultimately aim to drive mitigation strategies for
successful conservation and species management. Health
assessments are facilitating a pro-active approach to marine
mammal conservation in addition to a reactive response
to UMEs.
The primary role of wildlife veterinarians is shifting
from management of high mortality disease epidemics to
preventative management and mitigation of anthropogenic
causes of mortality (7). Unlike terrestrial species where mass
mortalities garner a lot of public attention, marine species can die
in large numbers, and the impact can go unnoticed (149). Sharing
information regarding health and thre a ts to local populations
can facilitate public interest in coastal and estuarine bottlenose
dolphin populations. Increased public awareness and reporting
of marine mammals in distress can aid understanding of the
current global changes and interactions between humans and
wildlife, dictating the efforts required to conserve future marine
populations glob ally .
Continuous monitoring of specific populations over time has
the benefit of providing both cross-sectional analyses on an
annual basis, as well as longitudinal analysis over several decades.
Collecting health data consistently across multiple populations
facilitates an understanding of geographic variability, can help
to establish reference ranges that are generalizable across
populations, and can provide a gradient of stressor exposures
for cross-sectional or correlational studies. The combined
approaches support a robust framework for epidemiological
studies to investigate the causal factors for disease. The collection
of decades of archival samples from multiple populations
facilitates retrospective studies to discern between sublethal
pathogen levels, assess temporal and spatial t rends, and elucidate
the intricacies of disease susceptibility at a population health
level. For example, dolphins in Florida are frequently exposed
to various levels of K. brevis red tides (
150, 151). Examining
samples from 1994 to 2003 enabled knowledge of baseline levels
of brevetoxin in the dolphin population and demonstrated t hat
dolphin carcasses not associated with large scale mass mortality
could also contain comparably high levels of brevetoxins (79).
This information is invaluable for future research when the
duration and intensity of red tides in Florida appears to be
increasing ( 152, 153).
An additional benefit of long-term studies and sample
archives generated by health assessments is th e ability to a pply
new technology and diagnostic tests retrospectively enabling
advanced monitoring of he alth changes over time. Identification
of emerging infe cti ous causes of mortality such as cetacean
morbillivirus requires continued monitoring of levels of herd
immunity over long periods of time (
81). Sample archives can
be used to est ablish normal levels and improve understanding
of emergence, dynamics, and history of pathogens such as
morbillivirus or retrospective analysis of brucella (23, 30, 73).
Established baseline data c an aid interpretation of normal
or increased prevalence of positive antibody titers within
the population.
Stress of Health Assessments (Alternative
Perspective)
Prior to considering health assessments for a project, there should
be an in-depth discussion of research priorities and if the short-
term capturing of individual dolphins is truly the best tool to
address the goals of the study. The value of the data obtained from
health assessments of free-ranging dolphins needs to be balanced
against the potential stress and risk to the individual from the
capture, handling, and sampling process (
154–157). The stress
of capture often influences baseline dat a such as blood cortisol
and a ldosterone levels (158). If baseline hormone values are the
focus of a study, remote biopsy sampling of blubber can give
an accurate indication of baseline stress hormone levels without
the elevation caused by the stress of capture (
159). However,
the adrenal response to a stimulus such as capture may be of
interest (35), and capture-release studies enable the evaluation
of an individual’s hypothalamic pituitary axis and whether or
not t h e animal is capable of mounting an appropriate stress
response (75).
In general, the molecular physiologica l response to the stress
of the veterinary examination is well-documented across species;
it is transient and the valuable information obtained from the
exam typically offsets any acute stress that may be caused.
Based on ongoing population monitoring, long-term health
consequences of repeated captures have not been found for
individuals examined as many as 15 times or more (160).
Ensuring capture and restraint are relatively brief and as calm
as possible is important, as it has been shown that short
holding times do not induce a significant neuroendocrine st ress
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Barratclough et al. Bottlenose Dolphin Health Assessments
response (154). An experienced team and ongoing training
opportunities among organizations, in both managed and
free-ranging dolphin populations, promote this high standard
of assessment.
Globally, free-ranging dolphins are exposed to a wide range of
anthropogenic stressors including environmental contaminants,
acoustic shipping disturbances, fisheries interactions, habitat
degradation or even loss altogether, exposure to biotoxins,
climate disruption, and human interactions (
161–168).
Variability in the level of anthropogenic stress occurs across
geographical locations. Health assessments provide a portal
into the individual and population health status to facilitate
understanding of ecosystem health, and drive conservation
and management decisions. The cost of each individual health
assessment is offset by the biological information obtained
from each examination. Combining these data with additional
stranding information, such as post-mortem examinations
and field observations, helps to improve understanding and
interpretation of biological health assessment data from a
conservation perspective.
International Perspective
Biologists and veterinarians from around the world have had
the opportunity to part ak e in dolphin health assessments across
U.S. waters with the aim of facilitating capacity building
for global cetacean conservation (
92). Established dolphin
health parameter reference ranges enable comparison between
international locations in an effort to tease apart the healt h effects
of different stressors. Throughout the majority of the world,
health monitoring of dolphins primarily involves post-mortem
exams of stranded cetaceans in Europe, physical exams during
translocations such as out-of-habitat animals in Asia and South
America such as the recent intervention in Bolivia, or during
remote biopsy sampling in photo-identific ation studies in the
Mediterranean (
169–173).
Increased international collaboration is essential for
mitigating conservation crises and aiming to reduce the
number of marine mammals becoming extinct such as the recent
loss of the Yangtze River dolphin, the baiji (Lipotes vexillifer), or
the high-risk Mediterranean monk seal (Monachus monachus)
and vaquita porpoise (Phocoena sinus) (
4, 174). Knowledge of
capture techniques gained from dolphin he alth assessments in
the U.S. has been applied to alternative species conservation
approaches, such as with the vaquita, in an effort to temporarily
remove animals from a d angerous habitat and relocate them
to a protected environment (175). Marine mammal stranding
networks exist world-wide with varying capacity dependent
on funding, degree of public interest, number of strandings
per year, facilities available, and the extent of inter-agency
cooperation (176). Sharing knowledge and organizational
structure from locations with financial support can aid capacity
building in areas where marine mammal stranding networks are
currently limited.
From examining dolphin communication to understanding
energetics, lung capacity, respiratory metabolomics, and
the mechanisms involved in deep diving physiology, health
assessments are contributing to advancing scientific knowledge
(
108, 177–179). S c ientists have improved our understanding of
dolphin anatomy and physiology by observing natural behavior
during health assessments and monitoring activity and behavior
post handling. Collaboration among scientists, veterinarians, and
biologists at different health assessments enables a synergistic
approach to understanding marine mammal health.
Universally, comprehensive cetacean conservation benefits
from an integration of all available cetacean assessment
techniques; hands on veterinary health assessments, post-
mortem examinations, photo-ID surveys, and field observer
data. Ideally a collaborative approach among scientists,
biologists, fishers, local community members, and government
officials would achieve maximum success from a management
perspective. Incre ased discussion will aim to improve future
inter-disciplinary approaches and address anthropogenic
impacts on marine mammals.
CONCLUSION
The advancement of common bottlenose dolphin health
assessments, transitioning from initial population assessments to
endangered species conservation applications has occurred
over several decades, expanding knowledge of marine
mammal medicine and science. As veterinary standards for
dolphins in human care have evolved, so have the standard
protocols for handling and monitoring free-ranging dolphins,
and diagnostics such as clinicopathology, ultrasonography,
radiography, electrocardiography, respirometry, microbiology,
and morphometry (
29, 32, 43, 77, 104, 108, 180, 181). Dolphin
health assessments are a valuable tool to extrapolate from the
individual to understanding both population and ecosystem
health. Combining scientific investigation with longitudinal
population monitoring over multiple dolphin populations
provides information to facilitate informed decisions regarding
conservation, regulations, and protection of marine mammals.
Social education re garding the presence, longevity, and
residence of bottlenose dolphins also allows t he public to engage
with the species and appreciate their intrinsic value within the
ecosystem; dolphins share the same habitat and are impacted
by some of the same stressors as loc al human communities.
Citizen science and public interest peaks during UMEs when
multiple carcasses are observed on the beaches in a short time
frame. This is an opportunity to engage with people to highlight
the environmental pressures faced by these apex preda tors and
explain the anthropogenic impacts on these charismatic species.
An interdisciplinary and interagency approach is needed to
fully understand the complexities of the challenges faced by
marine mammals. Shifts in the tide of social attitudes, interests,
regulations, and funding will have consequences to marine
mammal populations both free-ranging as well as managed.
Understanding the current global challenges and increasing
human a nd wildlife interactions will dictate the mitigation efforts
required to conserve future marine populations. Remaining at
the cutting edge of s cience and advancing the field will aim
to facilit at e conservation of marine mammal populations for
future generations.
Frontiers in Veterinary Science | www.frontiersin.org 12 December 2019 | Volume 6 | Article 444
Barratclough et al. Bottlenose Dolphin Health Assessments
AUTHOR CONTRIBUTIONS
All authors contributed to the past, present, or future
development of dolphin health assessments. AB and RW
completed the manuscript writing with significant contributions
from LS and CS. All authors provided edits and contributed to
the fina l submitted manuscript.
FUNDING
Waiver received for publication fees to Dr. Randy Wells.
ACKNOWLEDGMENTS
Dolphin health assessments would not have been possible
without the vast scientific collaboration from a large global team
of scientific colleagues, research assistants, post-docs, graduate
students, and volunteers. The auth ors would like to thank
Larry Fulford, who was the dolphin catcher for the majority
of health assessments in the southeastern U.S. for 35 years.
The authors would also like to thank the significant program
support for each health assessment in addition to NOAA’s Marine
Mammal Health and Stranding Response Program and the Office
of Naval Research. In addition, significant program support
for health assessments has been received from the Chicago
Zoological Society, NOAA’s Fisheries Service, National Science
Foundation, Environmental Protection Agency, Marine Mammal
Commission, Dolphin Quest, Inc., Disney’s Animal Programs,
Earthwatch, Inc., and the International Whaling Commission.
The authors also wish to thank the involvement of the U.S. Navy
Marine Mammal Program. This manuscript was made possible in
part by a grant from The Gulf of Mexico Research Initiative. The
scientific results and conclusions, as well as any views or opinions
expressed herein, are those of the authors and do not necessarily
reflect the views of NOAA. Dolphin health assessments were
conducted under various NMFS research permits for the projects
described. This is scientific contribution 246 of the National
Marine Mammal Foundation.
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Conflict of Interest: JS was employed by the company Dolphin Quest.
The remaining authors declare that the research was conducted in the absence of
any commercial or financial relationships that could be construed as a potential
conflict of interest.
Copyright © 2019 Barratclough, Wells, Schwacke, Rowles, Gomez, Fauquier,
Sweeney, Townsend, Hansen, Zolman, Balmer and Smith. This is an open-access
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BY). The use, distribution or reproduction in other forums is permitted, provided
the original author(s) and the copyright owner(s) are credited and that the original
publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
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Frontiers in Veterinary Science | www.frontiersin.org 18 December 2019 | Volume 6 | Article 444
