REVIEW

published: 13 December 2019

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
Edited by: monitored diligently by scientists for decades. Health assessment examinations have
Robert James Ossiboff, developed a comprehensive knowledge base of dolphin biology, population structure,
University of Florida, United States
and environmental or anthropogenic stressors affecting their dynamics. Bottlenose
Reviewed by:
Alex M. Costidis,
dolphin health assessments initially started as stock assessments prior to acquisition.
Virginia Aquarium & Marine Science Over the last four decades, health assessments have evolved into essential conservation
Center, United States management tools of free-ranging dolphin populations. Baseline data enable comparison
Juan Manuel Campos Krauer,
University of Florida, United States of stressors between geographic locations and associated changes in individual and
*Correspondence: population health status. In addition, long-term monitoring provides opportunities for
Ashley Barratclough insights into population shifts over time, with retrospective application of novel diagnostic
[email protected]
tests on archived samples. Expanding scientific knowledge enables effective long-term
Specialty section:
conservation management strategies by facilitating informed decision making and
This article was submitted to improving social understanding of the anthropogenic effects. The ability to use bottlenose
Zoological Medicine,
dolphins as a model for studying marine mammal health has been pivotal in our
a section of the journal
Frontiers in Veterinary Science understanding of anthropogenic effects on multiple marine mammal species. Future
Received: 06 September 2019 studies aim to build on current knowledge to influence management decisions and
Accepted: 26 November 2019 species conservation. This paper reviews the historical approaches to dolphin health
Published: 13 December 2019
assessments, present day achievements, and development of future conservation goals.
Citation:
Barratclough A, Wells RS, Keywords: dolphin, Tursiops truncatus, conservation, health assessment, veterinary medicine
Schwacke LH, Rowles TK,
Gomez FM, Fauquier DA,
Sweeney JC, Townsend FI, INTRODUCTION
Hansen LJ, Zolman ES, Balmer BC
and Smith CR (2019) Health
Assessment of marine mammal health is complex, both from an accessibility standpoint and from
Assessments of Common Bottlenose
Dolphins (Tursiops truncatus): Past,
the diverse array of factors influencing both individual and population survival. Baseline data are
Present, and Potential Conservation particularly crucial to evaluate whether population, or in some cases species, health is deteriorating
Applications. Front. Vet. Sci. 6:444. by providing points of comparison to assess trends in disease, mortality, and reproductive rates (1).
doi: 10.3389/fvets.2019.00444 From a veterinary perspective, a hands-on physical exam is the optimal approach to provide critical

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Barratclough et al. Bottlenose Dolphin Health Assessments

information for a comprehensive understanding of both other purposes, such as marking/tagging and population-level
individual and population-level health status. Knowledge gained studies to understand movement patterns and site fidelity.
from physically examining smaller cetaceans can be extrapolated Starting in 1979, Hubbs/SeaWorld Research Institute began
to larger, less-accessible cetaceans to improve understanding of collecting bottlenose dolphin health data in the Indian River
the complexities of adverse health impacts on marine mammal Lagoon of east Florida during capture-release operations to
conservation. The common bottlenose dolphin (Tursiops assess potential population-level impacts in advance of upcoming
truncatus) is an effective model species for understanding both zoologic collections (Figure 1) (11). Analyses from the samples
cetacean and marine ecosystem health. and data collected included morphometrics, blood biochemistry,
The overarching aim of conservation is to actively preserve hematology and reproductive endocrinology, microbiology,
habitats and the diversity of species dwelling therein (2). Effective genetics, and life history studies (12). Similar research was
conservation benefits from a foundation of sound scientific initiated by Marine Animal Productions in 1982 in Mississippi
understanding of species’ biology, population dynamics, and Sound, with the inclusion of skin, blubber, and liver tissue
stressors impacting the ecosystem (3). Marine ecosystem health sampling in some cases, to establish a health baseline for dolphins
is particularly challenging to assess due to immense biological inhabiting this area, again prior to collections and for comparison
diversity, as well as the vast scale and connectivity of the ocean with managed animals (13).
environment. Multiple factors threaten marine mammal health The Sarasota Dolphin Research Program (SDRP) began
(4); therefore, improving knowledge of the interplay of these incorporating additional biological samples and measurements
factors and predicting their long-term effects are essential for in 1984 to their original capture-release program. This supported
successful conservation. tagging and telemetry studies in Sarasota Bay, Florida, which
The emerging discipline of conservation physiology is were initiated in 1970. The inclusion of additional biological
particularly important in the marine environment, as it allows samples shifted the focus from studies of population range
a mechanistic understanding of the drivers of conservation and social patterns to broader scientific investigations of life
obstacles at an ecosystem level, in addition to species-specific history, population dynamics, body condition and health, social
challenges. Understanding how species physiologically respond structure, communication, reproductive success, and effects of
to environmental alterations is important for successful tailored human interactions. Samples and measurements included in-
conservation strategies (5). The rate of expansion of the human depth bloodwork analyses, genetic tests for population structure
population is exacerbating the challenges faced by wildlife with and paternity, ultrasonic measurement of blubber thickness,
frequently detrimental consequences to their health (6). The weight measurement, age determination (tooth growth layer
unprecedented changes occurring in the environment on a group counts), further development of tags and tag attachments,
global scale require novel mitigation strategies to ensure effective and post-release population monitoring (14–19).
conservation actions and sustainable wildlife populations (7). In 1992, the Marine Mammal Health and Stranding Response
There is limited understanding of the scale of the negative Program was formalized within the National Marine Fisheries
anthropogenic impact on marine mammal biodiversity. Service (NMFS) through an amendment to the Marine Mammal
Currently 29.2% of marine mammal species are classified as Protection Act (MMPA), establishing the standards for sample
data deficient according to the International Union for the collections and promoting collaboration and standardization
Conservation of Nature (8). As a result, shifts in population of bottlenose dolphin health assessments (20). In 1995, NMFS
viability can be difficult to detect, as the basic natural history conducted health assessments in response to the 1987–88
of the species has not been documented (9). Intrinsic traits of mortality event along the east coast of the U.S., in which over
species can be more important predictors of risk than extrinsic 600 bottlenose dolphins stranded as a result of a large-scale
environmental factors, as they provide a measure of the species’ morbillivirus epizootic (21–25). Additional studies were also
inherent susceptibility to human impacts and the ability of conducted to investigate unusual increases in dolphin strandings
species to recover from them (10). The bottlenose dolphin is near Matagorda Bay, Texas in 1992 (26), and in the Florida
one of the most closely studied and widely distributed marine Panhandle in 2005–2006 (27) (Figure 1) (Table 1).
mammal species and provides an opportunity to extrapolate Supplementary capture-release studies were initiated by the
knowledge and understanding to other marine mammal species. 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
HISTORICAL PERSPECTIVE capture-release studies used telemetry to understand population
structure along the Atlantic coast (39) following increased
Initially the first common bottlenose dolphin captures occurred dolphin mortality (40) which was eventually determined to be
for acquisition for public display, research, or for stock associated with morbillivirus (22, 30). The studies found positive
assessment prior to collection. Over time health assessments morbillivirus titers in some dolphins sampled in estuarine and
of inshore dolphins have been utilized to better understand coastal waters near Beaufort, NC, with no positive titers observed
endemic disease, establish baseline physiological measures, in dolphins sampled in estuaries near Charleston, SC (30).
and evaluate exposure to, and potential effects of, chemical, This provided crucial information to understanding dolphin
biological, and physical stressors. Historically, health assessments population structure and interaction along the U.S. east coast,
developed as additions to existing capture-release efforts for 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 morbillivirus and lobomycosis) was also observed for the IRL
initially presumed. In addition utilizing archived Sarasota Bay dolphins (34).
samples to retrospectively assess morbillivirus titers facilitated The incorporation of health assessments into existing capture-
further understanding of virus exposure, seroconversion, and release protocols provided the collection of baseline health
population naivety (41). Incorporating health assessments data across multiple populations, thus allowing for investigation
informed scientists that at least some small, estuarine stocks of geographic variability in health parameters (32, 42). The
along the Atlantic coast were naïve to morbillivirus and therefore methodologies established and samples collected during these
particularly vulnerable (38). earlier projects formed the basis for developing a risk assessment
In 2003, the Health and Environmental Risk Assessment framework to quantify the impacts for dolphins affected by
(HERA) population monitoring project was initiated for anthropogenic threats (e.g., Deepwater Horizon oil spill) in
bottlenose dolphins in the Indian River Lagoon, Florida (IRL), geographical areas where baseline data were not available (36).
and waters surrounding Charleston, South Carolina (CHS) (42).
For both the IRL and CHS field sites, health assessments THREAT IDENTIFICATION AND
were conducted to establish baseline data and to compare ASSESSMENT
morbidity temporally and across two geographic sites (34,
43). Higher concentrations of persistent organic pollutants Dolphin capture-release projects provide a unique perspective
(POPs) including legacy [e.g., dichlorodiphenyltrichloroethanes to assess individual animal health and extrapolate to overall
(DDTs), polychlorinated biphenyls (PCBs)] as well as “emerging” health of the surrounding population, species, and ecosystem.
contaminants [polybrominated diphenyl ethers (PBDEs) and Over the past 40 years in the U.S., there have been numerous
perfluorooctane sulfonate (PFOS) compounds] were detected in stressors that have impacted bottlenose dolphin populations, for
CHS dolphins as compared to IRL dolphins (43, 44). Mercury which dolphin capture-release projects have been integral to
concentrations in the blood and skin of IRL dolphins were threat identification and quantification of impacts from a given
extremely high, approximately five times higher than those stressor (e.g., biotoxins, disease, environmental contaminants, oil
in CHS dolphins. Higher exposure to many pathogens (e.g., 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 Population assessment (11)

109 total HA
1982 Mississippi Sound MS 57 Commercial assessment (13, 28)
1984–2019 Sarasota FL 289 individuals Biological sampling, technique (29)
(ongoing) 811 total HA development, reference
population
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* Beaufort NC 6 Stock assessment (31)

2000* 11 (30)
2006* 19 (32)
2002–2003 Brigantine NJ 12 Stock assessment (30)
2004 Holden Beach NC 10 Persistent organic pollutant (33)
assessment
2003–2018 Charleston SC 118 Comparative health studies (34)
Indian River Lagoon FL 246
2005–2006 St. Joseph Bay FL 30 UME investigation (27)
2009 Brunswick GA 29 HA legacy environmental (35)
contamination
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 site fidelity in this region, and thus, it was unclear which
An unusual mortality event (UME) is defined under the population(s) of dolphins were impacted (48, 49). Post-health
U.S. Marine Mammal Protection Act as “a stranding that is assessment tagging data suggested that the timing and spatial
unexpected; involves a significant die-off of any marine mammal extent of biotoxin events and other potential stressors in the
population; and demands immediate response.” The UME Florida Panhandle may greatly influence the severity of future
program was officially established under Title IV of the MMPA UMEs (50). Cetacean post-mortem examinations can provide
in 1992. Increased recognition of the occurrence of large scale insight into identifying the underlying cause of a UME in
dolphin mortality events in the late 1980s spurred the application addition to baseline data on disease presence and anthropogenic
of dolphin health assessments beyond population monitoring, to causes of mortality (51–53). Increased integration of live animal
investigating causes and effects of such mortality events (21, 24). assessment with post-mortem findings encourages the transfer
Since 1999, a series of UMEs occurred along the northwestern of information from the dead to the living, informing scientists
Florida coastline (Florida Panhandle) including St. Joseph Bay of the underlying pathophysiological mechanisms faced within
(45). NOAA conducted two dolphin health assessments during free-ranging populations (54).
2005 and 2006 in response to these UMEs in which 30
dolphins were sampled and subsequently tagged (27) (Table 1). Chemical Pollutants
The initial mortalities were tentatively attributed to biotoxins The presence of PCBs and other lipophilic contaminants have
from red tide algae (Karenia brevis) (46). Eosinophilia was been recorded to be accumulating in the tissues of bottlenose
observed in 23% of sampled dolphins, with associated increased dolphins and other odontocetes for decades (31, 55–59). Many
neutrophil phagocytosis and T-lymphocyte proliferation (27). marine mammals, particularly piscivorous species, have a high
Chronic low-level exposure to another algal toxin, domoic acid, potential to biomagnify pollutants (33), with increased levels
produced by the diatom Pseudo-nitzschia spp., previously linked resulting from the high trophic position and blubber acting as
to eosinophilia, was also identified (47). Prior to these UMEs, a reservoir for lipophilic contaminants (60). Both experimental
little was known about dolphin abundance, distribution, and 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 if these findings were correlated with the recent environmental
immunity, and/or reproductive failure (61–66). However, the exposure (75, 77, 78).
common co-occurrence of similarly acting compounds and Determining a causal link for the multiple pathologies
uncertainty regarding species-specific dose response functions observed post DWH oil exposure has been via a diagnosis of
makes assessment of the effects of these contaminants at a exclusion; concluding the toxic effects of the oil spill as the
population level challenging (60, 67). primary differential to both the observed pathologies and the
In addition to their applicability to investigating UMEs, increased dolphin mortality (71, 75). Other differential diagnoses
dolphin health assessments have also been used to investigate that were the potential causes of previous GoM UMEs were also
health of populations at risk from environmental contaminants. ruled out including biotoxins (79), POPs (68), and infectious
For example, dolphins along the Georgia coast have been disease (45, 73, 80, 81). Successive health assessments during
identified with some of the highest concentrations of PCBs in 2016–2018 have provided additional insight into the chronic
the world, and these levels are site-specific to a Superfund Site health effects. Longitudinal photo-ID surveys allowed estimation
in Brunswick, Georgia (60, 68, 69). In 2009, NOAA conducted of post-spill survival rate (0.80–0.85) and reproductive success
health assessments on 29 dolphins in the region and identified (20%), the latter was very low for this population (82, 83).
a high proportion (26%) of sampled individuals suffered Long-term consequences from oil contamination are difficult to
from anemia (66). In addition, these dolphins had reduced assess but have been suggested in other marine mammals such
thyroid hormone levels with total thyroxine, free thyroxine, and as the killer whale (Orcinus orca) and the sea otter (Enhydra
triiodothyronine negatively correlated with increased blubber lutris nereis) (84–87). Future research efforts will aim to improve
PCB concentrations. T-lymphocyte proliferation and indices of understanding of the transgenerational or in utero exposure
innate immunity decreased with blubber PCB concentration, effects in addition to the direct exposure of those animals alive
suggesting an increased susceptibility to infectious disease (66). at the time of the oil spill.
As with previously described health assessments, telemetry and Currently there is limited knowledge of the pathophysiology
photo-ID data provided perspective on ranging patterns relative of reproductive failure in bottlenose dolphins. Improved
to exposure, subsequent reproductive success, and effects of understanding of the normal physiological changes occurring
long-term impacts from cumulative stressors (70). In 2015, during gestation in successful pregnancies will aim to elucidate
another health assessment was conducted in Georgia to look at possible mechanisms of reproductive failure and identify
potential impacts associated with a recent morbillivirus-caused abnormalities occurring during failed pregnancies. This
UME and extremely high levels of PCBs that were identified from knowledge will be essential to help understand reproductive
previous studies. Dolphin morbillivirus titers differed between challenges, not only for common bottlenose dolphins,
dolphins sampled in coastal and estuarine waters, and tagging but also for the future management of other cetaceans,
data identified some degree of overlap between these individuals. some critically endangered, to help to understand the
This study suggested that estuarine dolphins in this region may reproductive challenges faced in these species and improve
be highly susceptible to future morbillivirus infections as a result future conservation management.
of elevated PCB levels and spatial overlap between coastal and
estuarine dolphins that would facilitate disease transmission (50).

Petroleum Toxicity CAPTURE AND HANDLING

In 2010, the largest marine oil spill in the history of the U.S., the METHODOLOGY
Deepwater Horizon oil spill (DWH), occurred in the northern
Gulf of Mexico (GoM). Subsequently a multidisciplinary The standard approach to capture small (1–5) numbers of
approach for evaluating the impacts upon cetaceans was bottlenose dolphins in shallow waters is by encirclement with
undertaken (71, 72). Bottlenose dolphins were the focal cetacean a seine net up to 500 m long and 7 m deep (88, 89). Shallow
species examined due to the accessibility of dolphins in shallow water (<1.5 m), minimal currents, and a solid seafloor are
coastal and estuarine waters, and the heavy oiling in some of optimum for safe capture and restraint. The seine net is deployed
those same nearshore areas. Health assessments in heavily oiled from a specially designed boat at high speed around the target
areas, particularly Barataria Bay, Louisiana, were initiated as dolphin(s), creating a compass (Figure 2A), with well-trained
part of NOAA’s Natural Resource Damage Assessment (NRDA). handlers distributed around the circumference to provide aid
Veterinary clinical assessment of dolphins living within the and restraint when the dolphins contact the net (Figure 2B)
oil spill footprint found significant lung pathology, impaired (29). If capture occurs in deep water (>1.5 m), the net compass
stress responses, high reproductive failure, and altered functional can be pulled into nearby shallow water, or the dolphins are
immunity, as compared to findings from un-oiled reference handled from the side of response vessels and moved onto
populations (35, 73–75). After the DWH oil spill, an abnormally specially designed floating mats that are either towed to shallow
high prevalence of lung and adrenal gland pathologies were water or directly onto a processing vessel for sample collection
documented in post-mortem examinations (73, 76). Identifying (Figure 2C). Capture of individual dolphins in waters exceeding
the baseline incidence of disease in stranded dolphins and the depth of seine nets has been performed via tail grabs
diagnosing pathology in live dolphins through the application of or hoop-nets, which are placed over the head of bow-riding
enhanced health assessment protocols was required to determine 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 safely restrained, veterinary tagged individual (70, 111). These tags provide fine-scale data on
examinations and sampling are performed. individual animal movements for several months, post-release,
and can provide additional insight into the cause of health effects
identified during the veterinary examination (37, 38, 117). The
VETERINARY PROCESSING movement pattern data from these electronic tags can also be
used to conduct follow-up monitoring to assess individual animal
Current health assessment examinations require collaboration health, survival, reproductive success, habitat use, and exposure
among scientists from multiple disciplines and veterinary to threats (82).
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 MULTIDISCIPLINARY APPROACHES FOR
successful management of dolphins in human care. Sampling ASSESSING POPULATION HEALTH
varies according to research questions, but typically a suite of
baseline data are collected to maximize knowledge obtained from Utilizing a multidisciplinary approach to combine clinical
a single veterinary exam (Table 2) (91). Ensuring a standardized veterinary knowledge with epidemiological analyses and
approach to highlight the importance of inter-lab comparability population modeling enables long-term forecasting of population
and sharing information between multiple institutions has trajectories (36). In UMEs, modeling to estimate mortality based
been paramount in the success of developing field collection on the number of stranded carcasses can provide insight into
methodologies and subsequent sample analysis procedures (32, the immediate losses to the population (71, 123–125). However,
113). As described below, additional field procedures have been integration of available health information and veterinary
incorporated over the decades as technology, field techniques, interpretation of sublethal, chronic conditions, which are likely
and analytical assays have advanced, and as management needs to influence long-term survival and reproductive potential, can
have evolved. provide a more accurate interpretation of the likely long-term
Determination of reproductive status (e.g., pregnancy, ovarian impacts on the population (36). Aside from impacts from acute
activity, or testis size as an indicator of sexual maturity) using events such as oil spills, modeling has been used to simulate
diagnostic ultrasound was first applied in Sarasota Bay in the likely population-level consequences from sublethal effects
1989 (26, 114). Full-body ultrasound has subsequently been of chronic contaminant exposure (60, 67). Estimation of long-
proven to be an invaluable, real-time tool during dolphin term population effects resulting from mortality or morbidity
health assessments, pioneered by the National Marine Mammal events is critical to inform restoration or recovery plans, and
Foundation and the U.S. Navy Marine Mammal Program also to appreciate the magnitude of the impact of UMEs on
(Figure 3) (77, 97, 101–103). In addition, pregnancy may also population numbers or of environmental contaminants on the
be diagnosed remotely by using blubber biopsy hormone levels surrounding ecosystem. Advances in modeling application to
(115, 116). In some cases, post-release visual monitoring and marine mammal stock assessments will greatly shape the future
photographic-identification (photo-ID) have allowed researchers of marine mammal conservation.
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). ADVANCES IN TECHNOLOGY AND
A holistic approach of including dietary assessment into CONSIDERATIONS FOR ANIMAL
the health exam along with urinalysis, blood (Figure 4), and WELL-BEING
blubber sampling can aim to elucidate underlying causes
of health abnormalities. In the field, urinary catheterization Dolphin health assessments provide fine-scale information on
has enabled comparison with dolphins in managed care and individual animals that can be extrapolated to evaluate overall
further developed the understanding of the development of population health. While much can be learned from hands-
renal pathology in dolphins, especially when differences in on health assessments, a major driver of current research is
diets have been considered (91, 97–99). Important ecological to develop techniques to obtain maximum health assessment
perspectives can be obtained from dietary assessments, along information from remote sampling and observations. The
with information regarding prey availability and potential shifts methodology for safely handling, sampling, and releasing
in environmental pressure affecting the ecosystem (118–121). dolphins is continually evolving to minimize the risk to both the
Further research is needed in this area to develop a more dolphins and researchers, as well as maximize the data collected.
standardized nutritional status indicator which can integrate However, health assessments are still expensive, logistically
multiple measures. This could be used for example to improve challenging, have limited target populations, and there is an
understanding of the effects of prey instability or environmental inherent risk when handling large animals (126, 127). The
stressors (122). development of remote sampling technologies is essential to
Electronic tagging technology to assess individual movement build upon the data collected during hands-on studies and to
or habitat use has rapidly advanced over the past 40 years so that expand our ability to efficiently and comprehensively assess the
now small satellite-linked tags can be attached via a single-pin to health of dolphin populations beyond nearshore waters, as well
the dorsal fin and have minimal to no long-term effects on the as the health of larger, less tractable cetacean species.

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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 Obtained from the periarterial rete on the Biochemistry (23, 29, 30, 74, 91–93)
(Figure 4) ventral aspect of the tail fluke Hematology
Blood gas analysis
Endocrinology
Immunology
Serology
Genetics
Surgical biopsy Full thickness wedge biopsies of skin and Genetic population structure (skin) (31, 33, 49, 57, 94–96)
blubber are routinely taken via an inverted Foraging ecology (skin)
“L” block under local anesthesia from the Chemical contaminants (blubber)
left lateral body wall caudal to the dorsal fin Hormone levels (blubber)
Microbiome
Urinalysis Bladder catheterization Renal function assessment (91, 97–99)
Dietary analysis
Tooth extraction Single tooth extracted under local Age determination (17, 100)
anesthesia
Ultrasonography Thoracic and abdominal internal Lung pathology (77, 97, 101–103)
(Figure 3) assessment Reproductive Assessment
Full abdominal exam including renal
assessment
Blubber thickness
Electrocardiography Adapted field use in and out of water Cardiac assessment (104)
(Figure 6)
Morphometrics Standardized full body measurements: Assess body condition and growth rates (105)
(Figure 7) lengths, girths, weight
Auditory evoked Portable unit adapted for field assessment Assess hearing range and sensitivity (106)
potential audiograms
Lesion biopsy Sample of abnormal skin lesions e.g., pox Histopathology (57, 93)
or freshwater lesions
Blow analysis Exhaled breath vapor Pathogen and hormonal analysis (107, 108)
(Figure 5) Metabolites
Respiratory function testing
Microbiology Swabs/culture plates from oral respiratory Bacteriology (109)
or genital orifices Virology
Freeze brand Dorsal Fin Identification (110)
Feces and urine Swabs or catheter Biotoxin analysis (46)
collection
Skin biopsy Skin sample from biopsy or during dorsal Genetics, sex, stable isotopes identification (70, 111, 112)
Electronic and/or fin tagging Ranging patterns reproductive status
roto tagging Survival

Application of new technologies to improve remote sampling is being developed to apply to large whale health assessments.
opportunities and maximize information obtained from cetacean Remote temperature assessment will be of increased value in
health assessments is pushing the boundaries of current marine the future when potential climate change impacts could result
mammal science. Blow samples previously established when in- in cetaceans being exposed to higher or lower environmental
hand (Figure 5) can now be obtained remotely utilizing UAVs temperatures (130–132).
(unmanned aerial vehicles). Drones can be used to obtain Historically, the standard method of estimating the age
aerial images to perform photogrammetry to assess health in dolphin health assessments is via tooth extraction under
via body condition in large whales unable to be examined local anesthesia and counting the growth layer groups present
physically (107, 128). Drones can also be used in cetacean on longitudinal section (17). Dental radiography has been
disentanglement approaches to provide accurate assessment of pioneered in an effort to replace the tooth extraction technique,
exact entanglement points and facilitate more informed decisions and validation of the technique is ongoing. Bone density
on disentanglement methodology. Thermography has been used assessment has also been explored as a possible aging method,
to assess dolphin dorsal fin temperatures, as a measure of however correlation with age across the entire lifespan was
individual health status representing appropriate integumentary limited (133). A promising new methodology is the use of
thermoregulation (129), and now thermal imaging from drones pectoral flipper radiography to assess bone maturation (134).

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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 individual sample (135). Currently, sex and population structure
paedomorphosis enabling this method to be applied throughout of the animal can be determined from genetic analyses of
the entire lifespan due to the predictable chronological osteogenic skin (112), and contaminant concentrations and stress and
changes occurring to the metacarpal and phalangeal bones. This reproductive hormone levels can be measured from blubber
non-invasive technology could facilitate age estimation for older biopsy (33, 116, 136). Present efforts are working toward using
animals, replacing tooth extraction. skin to assess the epigenetics of the individual to give an
Additional biological information from remote biopsy dart estimation of age (137). The NMMF are expanding on this even
sampling is expanding on the knowledge gained from each 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 FIGURE 7 | Dolphin suspended in a stretcher for weight measurement via
monitor the dolphin’s heart rate and assess cardiac function (MMPA ESA load cell on board the veterinary processing vessel. This image was published
Permit No. 18786-03). with permission of MMPA ESA Permit No. 18786-01 for the identifiable
individuals in the image.

indication of biological age (138). This emerging technology Remotely deployed suction cup satellite-linked tags can
could provide a means to assess increased environmental provide short-term (<24 h) data on bioenergetics, respiratory
pressure or poor health status (139–141). 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- of decades of archival samples from multiple populations
pin satellite-linked tags. These techniques will be particularly facilitates retrospective studies to discern between sublethal
useful in marine mammals where capture-release is impractical pathogen levels, assess temporal and spatial trends, and elucidate
due to size, species intolerance to handling or cost restraints. the intricacies of disease susceptibility at a population health
Future research aims to combine different disciplines to expand level. For example, dolphins in Florida are frequently exposed
scientific knowledge further and inter-species application of new to various levels of K. brevis red tides (150, 151). Examining
technologies, for example, studying acoustic communication as a samples from 1994 to 2003 enabled knowledge of baseline levels
proxy to changes in health status (144, 145). of brevetoxin in the dolphin population and demonstrated that
dolphin carcasses not associated with large scale mass mortality
could also contain comparably high levels of brevetoxins (79).
DISCUSSION This information is invaluable for future research when the
duration and intensity of red tides in Florida appears to be
Health assessments with an epidemiological focus can aim increasing (152, 153).
to understand the pathophysiology of disease and interpret An additional benefit of long-term studies and sample
the demographic, anthropogenic, and ecological pressures archives generated by health assessments is the ability to apply
contributing to individual disease susceptibility (146). new technology and diagnostic tests retrospectively enabling
Extrapolating from individual health assessments to accurately advanced monitoring of health changes over time. Identification
understand population health status, requires a strategic of emerging infectious causes of mortality such as cetacean
epidemiological approach (41, 147, 148). Integration of post- morbillivirus requires continued monitoring of levels of herd
mortem examinations within the health assessment framework immunity over long periods of time (81). Sample archives can
can provide additional projections from both diagnostic and be used to establish normal levels and improve understanding
scientific perspectives aiming to contribute to identifying the of emergence, dynamics, and history of pathogens such as
underlying cause of mortality and also predicting the future morbillivirus or retrospective analysis of brucella (23, 30, 73).
impacts on the population. Performing pro-active marine Established baseline data can aid interpretation of normal
mammal health assessment examinations allows an opportunity or increased prevalence of positive antibody titers within
to examine population health under natural environmental the population.
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 Stress of Health Assessments (Alternative
UMEs and ultimately aim to drive mitigation strategies for Perspective)
successful conservation and species management. Health Prior to considering health assessments for a project, there should
assessments are facilitating a pro-active approach to marine be an in-depth discussion of research priorities and if the short-
mammal conservation in addition to a reactive response term capturing of individual dolphins is truly the best tool to
to UMEs. address the goals of the study. The value of the data obtained from
The primary role of wildlife veterinarians is shifting health assessments of free-ranging dolphins needs to be balanced
from management of high mortality disease epidemics to against the potential stress and risk to the individual from the
preventative management and mitigation of anthropogenic capture, handling, and sampling process (154–157). The stress
causes of mortality (7). Unlike terrestrial species where mass of capture often influences baseline data such as blood cortisol
mortalities garner a lot of public attention, marine species can die and aldosterone levels (158). If baseline hormone values are the
in large numbers, and the impact can go unnoticed (149). Sharing focus of a study, remote biopsy sampling of blubber can give
information regarding health and threats to local populations an accurate indication of baseline stress hormone levels without
can facilitate public interest in coastal and estuarine bottlenose the elevation caused by the stress of capture (159). However,
dolphin populations. Increased public awareness and reporting the adrenal response to a stimulus such as capture may be of
of marine mammals in distress can aid understanding of the interest (35), and capture-release studies enable the evaluation
current global changes and interactions between humans and of an individual’s hypothalamic pituitary axis and whether or
wildlife, dictating the efforts required to conserve future marine not the animal is capable of mounting an appropriate stress
populations globally. response (75).
Continuous monitoring of specific populations over time has In general, the molecular physiological response to the stress
the benefit of providing both cross-sectional analyses on an of the veterinary examination is well-documented across species;
annual basis, as well as longitudinal analysis over several decades. it is transient and the valuable information obtained from the
Collecting health data consistently across multiple populations exam typically offsets any acute stress that may be caused.
facilitates an understanding of geographic variability, can help Based on ongoing population monitoring, long-term health
to establish reference ranges that are generalizable across consequences of repeated captures have not been found for
populations, and can provide a gradient of stressor exposures individuals examined as many as 15 times or more (160).
for cross-sectional or correlational studies. The combined Ensuring capture and restraint are relatively brief and as calm
approaches support a robust framework for epidemiological as possible is important, as it has been shown that short
studies to investigate the causal factors for disease. The collection holding times do not induce a significant neuroendocrine stress

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Barratclough et al. Bottlenose Dolphin Health Assessments

response (154). An experienced team and ongoing training (108, 177–179). Scientists have improved our understanding of
opportunities among organizations, in both managed and dolphin anatomy and physiology by observing natural behavior
free-ranging dolphin populations, promote this high standard during health assessments and monitoring activity and behavior
of assessment. post handling. Collaboration among scientists, veterinarians, and
Globally, free-ranging dolphins are exposed to a wide range of biologists at different health assessments enables a synergistic
anthropogenic stressors including environmental contaminants, approach to understanding marine mammal health.
acoustic shipping disturbances, fisheries interactions, habitat Universally, comprehensive cetacean conservation benefits
degradation or even loss altogether, exposure to biotoxins, from an integration of all available cetacean assessment
climate disruption, and human interactions (161–168). techniques; hands on veterinary health assessments, post-
Variability in the level of anthropogenic stress occurs across mortem examinations, photo-ID surveys, and field observer
geographical locations. Health assessments provide a portal data. Ideally a collaborative approach among scientists,
into the individual and population health status to facilitate biologists, fishers, local community members, and government
understanding of ecosystem health, and drive conservation officials would achieve maximum success from a management
and management decisions. The cost of each individual health perspective. Increased discussion will aim to improve future
assessment is offset by the biological information obtained inter-disciplinary approaches and address anthropogenic
from each examination. Combining these data with additional impacts on marine mammals.
stranding information, such as post-mortem examinations
and field observations, helps to improve understanding and
interpretation of biological health assessment data from a CONCLUSION
conservation perspective.
The advancement of common bottlenose dolphin health
International Perspective assessments, transitioning from initial population assessments to
Biologists and veterinarians from around the world have had endangered species conservation applications has occurred
the opportunity to partake in dolphin health assessments across over several decades, expanding knowledge of marine
U.S. waters with the aim of facilitating capacity building mammal medicine and science. As veterinary standards for
for global cetacean conservation (92). Established dolphin dolphins in human care have evolved, so have the standard
health parameter reference ranges enable comparison between protocols for handling and monitoring free-ranging dolphins,
international locations in an effort to tease apart the health effects and diagnostics such as clinicopathology, ultrasonography,
of different stressors. Throughout the majority of the world, radiography, electrocardiography, respirometry, microbiology,
health monitoring of dolphins primarily involves post-mortem and morphometry (29, 32, 43, 77, 104, 108, 180, 181). Dolphin
exams of stranded cetaceans in Europe, physical exams during health assessments are a valuable tool to extrapolate from the
translocations such as out-of-habitat animals in Asia and South individual to understanding both population and ecosystem
America such as the recent intervention in Bolivia, or during health. Combining scientific investigation with longitudinal
remote biopsy sampling in photo-identification studies in the population monitoring over multiple dolphin populations
Mediterranean (169–173). provides information to facilitate informed decisions regarding
Increased international collaboration is essential for conservation, regulations, and protection of marine mammals.
mitigating conservation crises and aiming to reduce the Social education regarding the presence, longevity, and
number of marine mammals becoming extinct such as the recent residence of bottlenose dolphins also allows the public to engage
loss of the Yangtze River dolphin, the baiji (Lipotes vexillifer), or with the species and appreciate their intrinsic value within the
the high-risk Mediterranean monk seal (Monachus monachus) ecosystem; dolphins share the same habitat and are impacted
and vaquita porpoise (Phocoena sinus) (4, 174). Knowledge of by some of the same stressors as local human communities.
capture techniques gained from dolphin health assessments in Citizen science and public interest peaks during UMEs when
the U.S. has been applied to alternative species conservation multiple carcasses are observed on the beaches in a short time
approaches, such as with the vaquita, in an effort to temporarily frame. This is an opportunity to engage with people to highlight
remove animals from a dangerous habitat and relocate them the environmental pressures faced by these apex predators and
to a protected environment (175). Marine mammal stranding explain the anthropogenic impacts on these charismatic species.
networks exist world-wide with varying capacity dependent An interdisciplinary and interagency approach is needed to
on funding, degree of public interest, number of strandings fully understand the complexities of the challenges faced by
per year, facilities available, and the extent of inter-agency marine mammals. Shifts in the tide of social attitudes, interests,
cooperation (176). Sharing knowledge and organizational regulations, and funding will have consequences to marine
structure from locations with financial support can aid capacity mammal populations both free-ranging as well as managed.
building in areas where marine mammal stranding networks are Understanding the current global challenges and increasing
currently limited. human and wildlife interactions will dictate the mitigation efforts
From examining dolphin communication to understanding required to conserve future marine populations. Remaining at
energetics, lung capacity, respiratory metabolomics, and the cutting edge of science and advancing the field will aim
the mechanisms involved in deep diving physiology, health to facilitate conservation of marine mammal populations for
assessments are contributing to advancing scientific knowledge future generations.

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Barratclough et al. Bottlenose Dolphin Health Assessments

AUTHOR CONTRIBUTIONS of health assessments in the southeastern U.S. for 35 years.

The authors would also like to thank the significant program
All authors contributed to the past, present, or future support for each health assessment in addition to NOAA’s Marine
development of dolphin health assessments. AB and RW Mammal Health and Stranding Response Program and the Office
completed the manuscript writing with significant contributions of Naval Research. In addition, significant program support
from LS and CS. All authors provided edits and contributed to for health assessments has been received from the Chicago
the final submitted manuscript. Zoological Society, NOAA’s Fisheries Service, National Science
Foundation, Environmental Protection Agency, Marine Mammal
FUNDING Commission, Dolphin Quest, Inc., Disney’s Animal Programs,
Earthwatch, Inc., and the International Whaling Commission.
Waiver received for publication fees to Dr. Randy Wells. The authors also wish to thank the involvement of the U.S. Navy
Marine Mammal Program. This manuscript was made possible in
ACKNOWLEDGMENTS part by a grant from The Gulf of Mexico Research Initiative. The
scientific results and conclusions, as well as any views or opinions
Dolphin health assessments would not have been possible expressed herein, are those of the authors and do not necessarily
without the vast scientific collaboration from a large global team reflect the views of NOAA. Dolphin health assessments were
of scientific colleagues, research assistants, post-docs, graduate conducted under various NMFS research permits for the projects
students, and volunteers. The authors would like to thank described. This is scientific contribution 246 of the National
Larry Fulford, who was the dolphin catcher for the majority Marine Mammal Foundation.

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