TYPE Original Research

PUBLISHED 22 November 2024

DOI 10.3389/fmars.2024.1454656

Co-occurrence of harmful algal

OPEN ACCESS blooms and whale deaths
EDITED BY
Rochelle Diane Seitz, Gregory K. Silber 1* and Katy M. Silber 2
College of William & Mary, United States

REVIEWED BY
1
Independent Researcher, Washington Grove, MD, United States, 2 Institute for Applied Ecology, Santa
Kathi Lefebvre, Fe, NM, United States
National Oceanic and Atmospheric
Administration (NOAA), United States
Jessica Huggins,
Cascadia Research Collective, United States Marine harmful algal blooms (HAB) have been implicated in marine mammal die-
offs; but the relationship between sub-lethal algal toxicity and marine mammal
*CORRESPONDENCE
Gregory K. Silber vulnerability to human activities has not been assessed. HAB toxins can result in
[email protected] compromised neurological or muscular systems and we posit these conditions
RECEIVED 25 June 2024 can expose marine mammals to increased likelihood of entanglement in
ACCEPTED 25 October 2024 commercial fishing gear or ship strike. To investigate whether HABs and large
PUBLISHED 22 November 2024
whale injuries and deaths were associated, we assessed the spatiotemporal co-
CITATION occurrence of HAB events and large whale mortalities/injuries in U.S. east (from
Silber GK and Silber KM (2024)
Co-occurrence of harmful algal
2000-2021) and west (2007-2021) coastal waters. The number of mortalities/
blooms and whale deaths. injuries was frequently higher in years with large-scale or severe HABs. We found
Front. Mar. Sci. 11:1454656. statistically significant relationships between the occurrence of HABs and whale
doi: 10.3389/fmars.2024.1454656
mortalities/injuries in west coast waters – at least three additional whale deaths/
COPYRIGHT
© 2024 Silber and Silber. This is an open-
injuries were detected near an active HAB than in areas where a HAB was not
access article distributed under the terms of reported. This relationship was similarly positive but weaker for east coast waters,
the Creative Commons Attribution License a difference that may be attributable to differing oceanographic features, or
(CC BY). The use, distribution or reproduction
in other forums is permitted, provided the approaches used in whale data collection, between coasts. Saxitoxin-producing
original author(s) and the copyright owner(s) Alexandrium was the most common causative agent on both the east (64.1%) and
are credited and that the original publication
in this journal is cited, in accordance with
west (57.8%) coasts; and domoic acid-producing Pseudo-nitzschia was more
accepted academic practice. No use, common along the west (33.3%) than the east coast (8.7%). Algal toxins can be
distribution or reproduction is permitted entrained in marine ecosystems, including in whale prey, and can chronically
which does not comply with these terms.
persist in marine mammals. Given many whale deaths/injuries result from fishing
gear entanglement and vessel strikes, algal-induced morbidities may diminish
whale capacities to detect or avoid fishing gear and approaching vessels. While
there was much interannual variability, general increasing trends were observed
in both whale death/injury and HAB datasets which may be attributable to
increased monitoring or rising ocean temperatures. HAB prediction modeling
has become increasingly sophisticated and could be used as a tool to reduce
whale mortality by limiting human activities (e.g., curtailing fishing operations)
when HABs, whale occurrence, and maritime activities are expected to overlap.
Additional systematic data collection is needed to track and model mechanisms
underlying relationships between HABs and incidental whale mortality.

KEYWORDS

harmful algal blooms, whale deaths, whale entanglement, ship strikes, marine algal
toxicity, climate change

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Silber and Silber 10.3389/fmars.2024.1454656

1 Introduction Anderson et al., 2021). Numerous whale, pinniped, and dolphin

deaths occurring on the west coast of North America and elsewhere
Marine Harmful Algal Blooms (HAB) are naturally occurring have been attributed (though not always firmly established) to acute
events involving toxic components that can be lethal to marine HAB exposure (e.g., Scholin et al., 2000; Fire et al., 2010;
organisms. Numerous marine alga (as well as diatoms, Häussermann et al., 2017; de la Riva et al., 2009). An early and
dinoflagellates, collectively referred to as HABs) can proliferate well-documented mortality event occurred in 1987 in which the
rapidly under certain conditions, can involve multiple marine trophic deaths of 14 humpback whales (Megaptera novaeangliae) in
levels, and are responsible for various physiological syndromes in Massachusetts waters was attributed to whale consumption of
humans and marine vertebrates. HABs are commonplace along both saxitoxin in their finfish prey (Geraci et al., 1989).
coasts of North America especially in spring to fall. Exposure to algal However, lethal toxicity thresholds, biological pathways, and
toxins may be quite common as aggregations of marine mammals physiological effects for individuals with sublethal HAB toxin levels
utilize these waters for feeding, migrating and other purposes. Shellfish are not well understood and doses that can become lethal are not
and some finfish species may tolerate, but bioaccumulate, algal always known. Mechanisms for transmission and accumulation
biotoxins and transfer them to other organisms through food web through trophic levels are likely complex as not all HABs result in
interactions. Detection of certain thresholds of these substances in widespread mammal deaths, and not all mammals that exhibit
shellfish or water column sampling can prompt closures of commercial detectable toxin levels succumb. In addition, a large-scale mammal
and recreational fisheries for public safety reasons. mortality event (involving primarily sei whales, Balaenoptera borealis)
Numerous naturally occurring species of dinoflagellate algal was attributed to a HAB during an El Nino year (Häussermann et al.,
species (including, for example, the genera Alexandrium and 2017); but left unexplained are why die-offs of this magnitude do not
Pyrodinium) produce potent saxitoxins (STX) that can result in also occur in other El Nino years or do not consistently occur in the
potentially life-threatening Paralytic Shellfish Poisoning (PSP) in presence of or large scale or particularly toxic HABs. And while
humans and may lead to various neurological symptoms including symptoms of sublethal morbidity can be severe, apparently scores of
numbness in extremities and loss of motor control (e.g., Anderson marine mammal species chronically carry toxins with HAB origins yet
et al., 1990). Human consumption of shellfish contaminated with exhibit no clinical signs of acute neurotoxicity (e.g., Lefebvre et al.,
domoic acid (DA) (from the diatom Pseudo-nitzschia) can, in acute 2002a; Danil et al., 2021; Fire et al., 2021; Hendrix et al., 2021).
phases (e.g., amnesic shellfish poisoning), cause dizziness, Impaired neurological or sensory systems from sub-lethal effects
disorientation, lethargy, seizures, memory loss, and a degeneration involving compromised neurological, musculature, and sensory
of neurons controlling sensory and motor functions (Teitelbaum systems may make marine mammals susceptible to additional threats
et al., 1990; Fire and Van Dolah, 2012) (see, also, Box 1). in their habitats. Whale and dolphin exposure to broadly distributed
Toxins from HABs have been detected in numerous marine HAB events, on local or regional scales, may, for example, lead to
mammal species (e.g., Landsberg, 2002; Danil et al., 2021) and individuals’ elevated vulnerability to fishing gear entanglement or being
relatively high levels have been reported in sea turtle (e.g., Capper struck by a moving vessel because of an indifference to the threats, or as
et al., 2013), and seabird species (e.g., Shumway et al., 2003; Gibble a consequence of diminished ability to detect or avoid them.
et al., 2021). Among marine mammals, adverse effects from toxic Entanglement in commercial fishing gear and collisions with
algal exposure have been reported for manatees (Bossart et al., 1998; sea-going vessels are significant threats to large whale populations
Flewelling et al., 2005; Capper et al., 2013) and cetaceans (e.g., (e.g., Reeves et al., 2013; Erbe et al., 2020) and likely inhibit the
Twiner et al., 2011; Fire et al., 2021). growth and recovery of some depleted populations (e.g., Thomas
Mortality and morbidity related to HAB exposure have been et al., 2016; Carretta et al., 2023). Fishing gear entanglements and
reported for hundreds of California sea lions (Zalophus ship strikes can account for hundreds of whale deaths and injuries
californianus) along U.S. west coast beaches in multiple years in each year in U.S. waters; globally, mortality rates are likely in the
the 1990s to 2010s (Scholin et al., 2000; McCabe et al., 2016; thousands from these sources (Read et al., 2006; Schoeman et al.,

BOX 1 Effects of algal toxins.

A suite of naturally occurring dinoflagellate species (including Alexandrium spp., Gonyaulax spp., among others) produce potent saxitoxins (STX) that can lead to life-
threatening neurological symptoms in humans. Sub-lethal STX toxicosis can include numbness in extremities, weakening of muscles, and loss of motor control. Human
consumption of shellfish contaminated with domoic acid (DA) can result in dizziness, disorientation, lethargy, seizures, memory deficits, and a degeneration of neurons
controlling sensory and motor functions (Teitelbaum et al., 1990; Fire and Van Dolah, 2012).
In marine mammals, STX acts by affecting neuromuscular junctions (IWC, 2017) and can result in decreased sensory functions, compromised muscle coordination,
or listlessness, among other symptoms (Landsberg, 2002; Scholin et al., 2000. Flewelling et al., 2005). Exposure to DA in marine mammals can result in disorientation,
uncoordinated movements, and seizures (McHuron et al., 2013; IWC, 2017). Spatial memory deficits, lethargy, and perseverative (repetitive) behavior have been described
in California sea lions following sub-lethal exposures to DA (Goldstein et al., 2008; Cook et al., 2015, 2016). In other mammalian taxa, laboratory trials involving chronic
low-level exposure of DA lead to structural and chemical changes in the brain in macaque monkeys (Macaca fascicularis, Petroff et al., 2019) and spatial memory
impairment in mice (Lefebvre et al., 2017). Our analysis suggests that debilitating features of these toxins may also contribute to large whale entanglements and ship strikes.

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2020). Impacts from these threats could be worsened if large whales Of the records accessed, 357 were removed from analysis
are disoriented, are experiencing diminished physiological or because they were outside the date ranges of corresponding
sensory systems thereby reducing detection and avoidance of periods for available whale death and injury data (2000-2021 for
vessels or fishing gear within their habitat. the U.S. east coast; 2007-2021 for U.S. west coast records). We
The goal of this analysis was to determine the extent to which removed all HAB event records involving lakes and inland rivers.
HAB events co-occur with large whale injuries/mortalities from Records of HAB events at the mouths of estuaries or semi-enclosed
ship strikes or entanglement in fishing gear. Specifically, we sought bodies of water (e.g., Puget Sound (Washington), the Straits of Juan
to test the hypothesis that sub-lethal exposures to HABs may de Fuca (British Columbia), San Francisco Bay (California), the
disorient or desensitize large whales, thereby increasing the Chesapeake Bay (Maryland/Virginia)) or large river mouths were
likelihood that they will suffer injury or death from interactions retained in our analyses because toxins originating here could be
with human activities. We used existing datasets of HAB events in expected to enter coastal marine systems from these sources, and
U.S. east and west coastal waters and records of large whale deaths because in some cases large whale species might be expected to enter
and injuries to evaluate the timing and locations of recovered or or utilize some bays (e.g., San Francisco Bay or the Straits of Juan de
reported whale injuries and deaths from human interaction (e.g., Fuca) or large river mouths.
fishing gear entanglement and ship strikes) in relation to timing and Regarding the Chesapeake Bay proper, records involving rivers
locations of HAB events (especially severe or large-scale events). and their tributaries entering the Bay were eliminated from analysis
This broad-scale analysis provides compelling evidence, but does reasoning that planktonic toxins from a localized HAB event would
not confirm, that large whales may be at higher risk of ship strike or have to be transported tens (or perhaps to hundreds) of miles to
fishing gear entanglement after exposure to a HAB event. enter a fully marine ecosystem. However, blooms described as
having occurred at the mouth of the Chesapeake Bay (e.g.,
Norfolk/Hampton, Virginia locations) were included in our
2 Materials and methods analysis because these might exit the Bay with tidal fluxes.
Records from various monitoring sites with HAB data extending
2.1 Acquiring and processing HAB data along the length of Long Island Sound (New York) were included
because, while some sites involved lagoon systems, they adjoin and
Toxic aquatic algae can have adverse consequences for human readily connect with marine waters and can be areas of relatively
health; consequently, HAB monitoring programs have been high whale concentrations.
established in hundreds of countries globally. Observations from Additional records were also eliminated that lacked specificity
these programs are provided annually to a central repository, the or sufficient information (e.g., reported an absence of toxins, did not
Harmful Algal Event Database (HAEDAT), curated by UNESCO’s include information about toxin concentration levels), or provided
Intergovernmental Oceanographic Commission (HAEDAT; http:// only general information (e.g., merely noted ongoing monitoring
haedat.iode.org/). In the United States, routine HAB event programs with no accompanying information), or included
monitoring is conducted primarily by state agencies, academic comments such as ‘blooms have occurred in this area nearly
institutions, and coastal municipalities whose data are also annually.’ HAB events that involved the occurrence of brown
provided to the HAEDAT global data base. Standardized HAB tides (e.g., the algae Aureococcus sp.) were eliminated from our
monitoring observations generally include, but are not limited to, analysis since the occurrence of brown tides have no known toxic
information on location, dates of observations (and in some cases, effects on vertebrates.
the cessation of a bloom), the results of diagnostic testing for the Not all records included specific latitude/longitude coordinate
causative agent, and toxic concentrations (generally reported as, for information for sampling locations. For records that lacked specific
example, ‘mouse unit’ bioassays, or amount per unit of water). In location data, we determined latitude and longitude information using
many locations, negative results, i.e., absence of a detectable bloom descriptions for each record (e.g., county, nearest municipality, or other
during routine monitoring, are also reported. physical landmarks such as named beaches, bays, or islands) as
Using the HAEDAT web site search function, we downloaded indicated in Google Earth.
records in designated grids for all coastal continental U.S. waters Reasoning that concentrations in seafoods that were of
from northern Maine to southern Florida, and along the U.S. Pacific sufficient toxicity to be potentially unsafe for human consumption
Coast from northern Washington to southern California for the might also be detrimental to marine mammals, all HAB events that
period 1969 to 2021. involved toxicity levels that exceeded nationally established
We excluded HAB observations for the Gulf of Mexico because thresholds that prompt fishery closures (e.g., ≥80 μg/100g STX
we were interested in possible impacts of HAB events primarily on and >20ppm DA in shellfish tissue; see, for example, standards
large whale species occurring (e.g., in feeding or migrating established by the Food and Agriculture Organization of the United
locations) along the U.S. continental shelves (i.e. records from Nations (FAO: https://www.fao.org/3/y5486e/y5486e0d.htm#:~:
Alaska were excluded) and coastal margins. However, records text=The%20limit%20for%20PSP%20toxins,mg%20STX%20eq%
from the coastline of eastern Florida were included. 2F100%20g) and elsewhere (e.g., Oregon Department of Fish and
A total of 1,026 records were downloaded (on 14 Wildlife https://myodfw.com/articles/shellfish-and-biotoxins) were
December 2022). included in our analysis. In addition, all HABs that resulted in a

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commercial or recreational seafood fishery closure were included in the U.S. west coast dataset included exclusively those records in which
our analysis1. whale deaths/injuries resulted from known interaction with human
Following the winnowing processes described here, a total of activities (e.g., fishing gear entanglement or ship strike); whereas the
194 records of HAB events were used in this analysis. U.S. east coast data included classifications regarding cause of death/
injury as, for example, ‘natural causes’ or ‘unknown.’ We did not
include these latter cases in our analysis, using only those records in
2.2 Whale injury and mortality data which interactions with human activities were noted. Doing so
rendered the east and west coast datasets more comparable as the
Whale injury and death data were obtained from programs west coast data was focused primarily on those cases involving known
managed by NOAA’s National Marine Fisheries Service (NMFS) for human interactions. As such, the large whale strandings data analyzed
2000-2021 for U.S. east coast waters; and from 2007-2021 for U.S. west here includes only cases in which interaction with some type of human
coast waters. Under authority of the U.S. Marine Mammal Protection activity was identified as the source of injury or death.
Act, NMFS administers the National Marine Mammal Health and Using these datasets, we analyzed a total of 850 records of whale
Stranding Response Program (https://www.fisheries.noaa.gov/national/ injury and mortality occurring in waters off the U.S eastern
marine-life-distress/marine-mammal-health-and-stranding-response- seaboard, and 566 records for the U.S. west coast.
program) which relies on extensive stranding networks involving all Locations (i.e., latitudes and longitudes) for most of the whale
U.S. coastal states and other partners. The Program endeavors to, recovery or observation site were provided in the east coast whale
among other things, quantify every marine mammal mortality and data set (A. Henry, pers comm.; and as indicated, for example, in
injury event in U.S. waters, including dead or injured but not Henry et al., 2022). For those without location information, we
stranded (i.e., offshore ‘floaters’) large whale. Data sources include assigned coordinates for these data (for the purposes of plotting the
opportunistic reports and observations and from systematic Federal locations) using landmarks that accompanied the data and as
and state aircraft- and ship-based surveys which are in turn curated indicated in Google Earth. Location data were available for some,
by the stranding networks and central repositories. In addition, but not all, of the whale injury/mortality data from the U.S. west
efforts are made to conduct detailed necropsies of dead whales to coast (J.V. Carretta, pers comm.), and where location data were
determine cause of death, when possible. Determinations are also absent, we ascribed location information as described above.
made of ‘serious’ versus ‘non-serious’ injuries through a review Dates and locations generally denoted when and where the
process involving personnel at the NMFS’s Science Centers and injured or dead animal was initially observed or washed ashore.
Regional Offices, and designated external Scientific Review Group Therefore, locations (and to a certain, but lesser extent, the dates)
panels as dictated by NMFS policy directives which include specific provided for these records should be regarded as approximations of
guidelines for making such determinations (NMFS, 2012; NMFS, where the death or injury may have actually occurred. They may
2023; and https://media.fisheries.noaa.gov/dam-migration/02- represent, for example, the location where a whale beach-stranded,
238.pdf). As such, considerable effort is made to ensure large but where it did not necessarily die; where it was first observed
whale death and injury event data, and subsequent assessments of entangled in fishing gear whereas the actual entanglement may have
those records, are systematically collected and managed. However, occurred some miles distant; or where a whale may have been
not all whale fatalities and injuries are detected, reported, or observed struck by a vessel but succumbed to its injuries elsewhere.
provided to publicly available data repositories. Those limitations Thus, these observations may have lacked the spatial specificity we
notwithstanding, the datasets analyzed here can be viewed as or others have ascribed to them (i.e., they were translated into
reliable representations of those events for our analytical purposes. specific locations on a map). But because HABs can span tens,
There are some differences between the U.S. west coast and east hundreds, in some cases thousands, of square miles, we believe
coast whale data: for example, the likelihood of detecting whale approximate locations for whale mortality and injury observations
injuries/mortalities distant from shore (primarily off New England) were sufficient for the scales of analysis used here (e.g., up to 100
are enhanced by systematic aircraft surveys used to determine miles radius, as described below).
abundance, distribution, and incidents of fishing entanglement to aid Similarly, inclusive dates of potential whale exposure to HAB
(primarily) North Atlantic right whale conservation efforts. In addition, toxins were assumed to have occurred for the duration of an active
HAB, i.e., the dates in which detectable levels of toxins occurred in
the environment as determined and reported by various state and
1 While criteria were developed for inclusion of HAB records for in the federal monitoring programs. The durations and concentrations of
analysis in this study, they were not dissimilar from those used by Anderson exposures that result in serious consequences for marine mammals
et al. (2021) in a study of past and current HABs, namely the bloom was to is not well established; and while not much is known about toxin
have been ‘…associated with a negative impact or management action. These residency times in mammal tissue, it can be reasonably assumed
could include: 1) toxin accumulation in seafood above levels considered safe that marine mammals are exposed for at least the duration of an
for human consumption; 2) water discoloration, scum or foam sufficient to active bloom (Lefebvre et al., 2002a). Saxitoxin agents can remain in
cause ecosystem damage or a socioeconomic impact; 3) any event where various bivalve species for days or weeks (e.g., Chou et al., 2005;
humans, animals or other organisms are negatively affected by the bloom; or Leblad et al., 2017; Medina et al., 2018). While some organisms,
4) precautionary closures of harvesting areas based on predefined thresholds such as blue mussels (Mytilus edulis) are capable of depurating
of toxic phytoplankton cells in the water.’ (reducing or eliminating) DA in hours to days (Krogstad et al.,

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2009), in razor (Siliqua patula), purple varnish clams (Nuttallia number of whale injuries/mortalities within each given timeframe
obscurata), and other organisms DA can persist much longer and distance for each HAB, then calculated the mean for each
(Adams et al., 2000; Lefebvre and Robertson, 2010). Lefebvre timeframe and distance. Finally, we fit a simple linear regression to
et al. (2002a) detected DA in krill near feeding whales as well as determine if the occurrence of HAB events was increasing through
in numerous fish species ranging from benthic sanddabs to pelagic time along each coast. Analyses were completed in R (version 4.3.1).
anchovies, sardines, and albacore; they concluded that DA
permeates benthic as well as pelagic communities. Fish (e.g.,
anchovies, Engraulis spp.) tend to depurate DA concentrations 3 Results
rapidly but can be potent DA vectors while a bloom is ongoing
(Lefebvre et al., 2002b). Therefore, we can reasonably assume that 3.1 Summaries of whale and HAB data sets
the dates used in our analysis – beginning with the first detection
and quantifying of a HAB event – would overlap with whale A total of 11 algal genera were represented in the HAB database
exposure to HAB toxins for the duration of the bloom. for the study periods (Table 1). Only three of these (Alexandrium,
Pseudo-nitzschia, and Dinophysis) occurred on both U.S. coasts.
The saxitoxin-producing Alexandrium was the dominate HAB
2.3 HAB and whale data analysis causative agent and comprised 60.1% (n=118 total blooms) of the
entire sample from both coasts, followed by the diatom Pseudo-
To determine if whale deaths and injuries were more likely to co- nitzschia (n=42), and various other dinoflagellate species (n=31
occur with reported HABs, we conducted three analyses. First, we fit a combined blooms). Diversity of HAB causative agents was greater
simple linear regression to assess correlations between the number of in east coast waters than off the west coast; and while Alexandrium
reported HAB occurrences and the number of human-related large blooms were nearly equally represented on both coasts, those
whale deaths and injuries each year in waters off the U.S. west and involving Pseudo-nitzschia were more common in U.S. west coast
east coasts. We fit separate models for the east and west coasts, with waters (n=34) than off the east coast (n=8) (Table 1).
the number of reported HABs each year as a predictor and the A total of nine species appeared in the whale human-related injury
number of reported large whale deaths and injuries each year as the and mortality databases analyzed here (Table 2). Interaction with
response. In addition, we summarized the average density of whale fishing gear and vessel strikes were the most common sources (when
mortality/injuries that occurred within the reported onset (i.e., first the cause was known) of whale injuries and mortalities (Table 3). Of
detection) and up to 30 days following conclusion (i.e., reported end the 556 records of whale mortality and injury for the U.S. west coast,
date) of a bloom, and in areas of 10, 50, 100, and 200 miles fisheries interactions were involved in 422 (75.9% of all causes; most of
surrounding a HAB event. We estimated the average density as the these were interactions in which the type of gear could not be

TABLE 1 Causative agents involved in harmful algal blooms (HAB) and the number and percentage caused by each for U.S. west coast waters, 2007-
2021; and U.S. east coast waters, 2000-2021.

Group Genus West coast East coast Total HABs

Dinoflagellates

Alexandrium 59 (57.8%) 59 (64.1%) 118 (60.1%)

Cochlodinium 0 7 (7.6%) 7 (3.6%)

Dinophysis 7 (6.9%) 7 (7.6%) 14 (7.2%)

Pyrodinium 0 2 (2.3%) 2 (1.0%)

Margalefidinium 0 6 (6.5%) 6 (3.1%)

Amphidinium 1 (1.0%) 0 1 (0.5%)

Prorocentrum 0 1 (1.1%) 1 (0.5%)

Karenia 0 1 (1.1%) 1 (0.5%)

Diatoms

Pseudo-nitzschia 34 (33.3%) 8 (8.7%) 42 (21.6%)

Raphidophytes

Chattonella 0 1 (1.1%) 1 (0.5%)

Haptophytes

Algirosphaera 1 (1.0%) 0 1 (0.5%)

TOTAL 102 92 194

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TABLE 2 Large whale species in U.S. west (A) and east coast (B) mortality and injury data bases and number of mortalities/injuries for each species.

A. U.S. West Coast

Common name Latin binomial # of mortalities/injuries % of mortalities/injuries

Blue whale Balaenoptera musculus 24 ~4%

Gray whale Eschrichtius robustus 177 ~32%

Fin whale Balaenoptera physalus 31 ~6%

Humpback whale Megaptera novaeangliae 259 ~47%

Minke whale Balaenoptera acutorostrata 5 <1%

Sperm whale Physeter macrocephalus 12 ~2%

Unidentified 48 ~9%

B. U.S. East Coast

Common name Latin binomial # of mortalities/injuries % of mortalities/injuries

Blue whale Balaenoptera musculus 2 <1%

Bryde’s whale Balaenoptera spp. 1 <1%

Fin whale Balaenoptera physalus 60 ~7%

Humpback whale Megaptera novaeangliae 469 ~55%

Minke whale Balaenoptera acutorostrata 137 ~16%

Right whale Eubalaena glacialis 143 ~17%

Sei whale Balaenoptera borealis 17 ~2%

Unidentified 23 ~3%

identified); 122 (21.9% of all causes) involved vessel strikes. Of the 850 (Figure 1). HABs tended to be relatively evenly distributed along the
observed east coast injuries and mortalities involving human U.S. west coast but were spatially more like to occur in relatively higher
interactions (723 records were removed from analysis in which the latitudes (i.e., Chesapeake Bay mouth, north) along the U.S. east coast.
cause of injury/death was ‘unknown’ or resulted from ‘natural causes’), They were frequently (i.e., in multiple years in our study period)
645 (75.9%) instances involved fishing gear entanglement and 203 reported in coastal Maine and Gulf of Maine waters; and reported in
(23.9%) resulted from vessel strikes (Table 3). We note that while the most years along the Massachusetts coasts, along the southern coasts of
cause of death or injury was listed as ‘unknown’ or ‘natural causes’ in Long Island, and near the mouth of the Chesapeake Bay. Whale deaths/
many U.S. east coast records, in no instance was exposure to a HAB injuries were generally evenly distributed along the U.S. west coast
indicated as a cause of death. coastal waters (Figure 1). Records of whale deaths/injuries on the U.S.
east coast were weighted toward New England waters and in some
cases were reported tens of miles from the shoreline.
3.2 Coincidence of HABs and whale We found a positive relationship between the occurrence of
mortalities/injuries HABs and large whale deaths and injuries in waters off the U.S. west
coast and east coast (Figure 2). This relationship was statistically
Graphical representation of HAB events and whale deaths/injuries significant in west coast waters (b = 3:853, SE = 0:934, p = 0:001)
indicate an overlap of these on both coasts of the United States but not in east coast waters (b = 2:133, SE = 1:202, p = 0:091).
These results suggest an increase of at least three large whale
TABLE 3 Sources of large whale mortality and injury for U.S. west and deaths or injuries for each additional HAB off the west coast.
east coast waters. There was much interannual variation in both the number of
HABs and whale injuries/mortalities (Figure 3).
Cause of mortality or West East Total
serious injury Coast Coast On average, about two human-caused whale injuries/deaths
occurred within 10 miles of an active HAB in west coast waters
Fisheries interaction 422 645 1067
(Figure 4). This number decreased with time and distance; only about
Vessel strike 122 203 325 one injury/death occurred within 200 miles of an active west coast
Other (i.e., marine debris, illegal hunt, 12 2 14 HAB and almost no whale injuries/deaths occurred after 10 days of an
scientific research) active west coast HAB. On the east coast, patterns are more
TOTAL 556 850 1406
ambiguous, likely due to the manner in which whale injury/
mortality data were collected there (data are collected distant from

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FIGURE 1
Map of harmful algal bloom (HAB) events (denoted by green circles) and reported large whale deaths and injury locations (red dots) for the (A) U.S.
west coast, 2007-2021, and (B) U.S. east coast, 2000-2021.

shore in some locations) and the spatial extents of HAB and whale algal species on the west coast (Table 5). Most injuries/mortalities were
monitoring efforts poorly align spatially (see Methods). More whale coincident – occurring in the vicinity (at ranges of 10-100 miles) – with
injuries/deaths occurred within 200 miles of an active HAB than Alexandrium and Pseudo-nitzschia blooms (Tables 4, 5).
within 10 miles of an active HAB, and almost no injuries/deaths The number of HAB events was highly variable between years,
occurred after 10 days of an active HAB (Figure 4). a feature common to the waters of both coasts (Figure 2).
Reported whale deaths and mortalities were coincident with only Nonetheless, the rate of reported HAB occurrence increased in waters
five toxic algal species on the U.S. east coast (Table 4) and only four of both the east (b = 0:235, SE = 0:065, p = 0:002) and west coasts

FIGURE 2
Co-occurrence of harmful algal bloom (HAB) events and whale injury/deaths. Linear regressions for the number of HAB events and large whale
injuries/deaths per year are shown for U.S. west (in blue) and east coasts (in green). The relationship between the annual number of HABs and whale
deaths/injuries is statistically significant (p = 0.002) for U.S. west coast waters, but not significant for the U.S. east coast.

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FIGURE 3
Number of reported harmful algal blooms (HAB) per year (gray bars) and frequency of reported large whale deaths and injuries (red circles) for
waters off the U.S. west [(A) 2007-2021] and east [(B) 2000-2021] coasts.

(b = 0:450, SE = 0:198, p = 0:040) of the United States in the mortality and injury events, or vice versa (e.g., west coast, 2011;
respective periods of our study (Figure 5). While the rates of increase east coast 2008) (Figure 2). These co-occurrences are discussed
were statistically significant for data from both coasts, we found that the more fully in Section 4.7, below.
increase was more rapid on the U.S. west coast than on the east coast;
roughly five additional reported HABs per decade on the west coast and
about two additional HABs per decade on the east coast. Seasonally, the 4 Discussion
occurrence of both HABs and whale mortalities/injuries were generally
highest in spring to fall (i.e., April-September) (Tables 6, 7). Our analysis provides further evidence that toxic algal blooms
While there was substantial interannual variation, there also of varying scales and severity are increasingly common in U.S.
appeared to be a general increase in the number of human-caused coastal waters. As such, marine mammals using these habitats are
whale mortalities/injuries during the respective study periods likely routinely exposed to HAB toxins, incurring a higher risk of
(Figure 2). In addition, in some years in which large numbers of mortality through direct exposure and loss of neurological function.
(or severe) HABs were reported, whale mortalities/injuries were The established co-occurrence of HABs and whale morbidity/
also high. Among these were, notably, 2016 and 2018 for the U.S. mortality resulting from commercial fishing and shipping
west coast whale data. In U.S. east coast waters both the number of interactions suggests, but does not confirm, that non-fatal
HABs and whale death/injury records were among the highest in concentrations of algal neurotoxins may render whales more
the data sets for the years 2012, 2016, 2017, 2019, and 2020 susceptible to injury from commercial activities by making them
(Tables 6, 7). However, this pattern did not consistently hold for less able to respond to those activities. Additional work is needed to
all years, i.e., years in which large numbers of HABs were reported further elucidate the relative importance of this relationship
were not necessarily accompanied by high numbers of whale compared to direct relationships between HABs and marine

FIGURE 4
Average density of whale injuries and deaths in waters off the U.S. west [(A) 2007-2021] and east [(B) 2000-2021] coasts during and after HABs (days)
and across four distances (miles).

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TABLE 4 Occurrence of whale mortalities and injuries within 10, 50 and 100 miles of U.S. east coast harmful algal blooms (HAB).

U.S. East Coast

Group Genus Within 10 miles of active HAB Within 50 miles of active HAB Within 100 miles of active HAB
Dinoflagellates

Alexandrium 3 (100%) 34 (92%) 57 (78%)

Cochlodinium 0 (0%) 1 (3%) 2 (3%)

Dinophysis 0 (0%) 0 1 (1%)

Pyrodinium 0 (0%) 0 0

Margalefidinium 0 (0%) 1 (3%) 5 (7%)

Amphidinium 0 0 0

Prorocentrum 0 0 0

Takayama 0 0 0

Karenia 0 0 0

Diatoms

Pseudo-nitzschia 0 1 (3%) 8 (11%)

Raphidophytes

Chattonella 0 0 0

Haptophytes

Algirosphaera 0 0 0

TOTAL 6 37 73

Percentages of all recorded whale deaths and injuries occurring within denoted distance ranges of an active HAB (and its respective causative agent) are indicated.

mammal mortality, primarily through ongoing and systematic To our knowledge, there are only two references (one now over
collection of HAB occurrence and severity data, and through two decades old) that alluded to associations between HAB agent
additional and systematic tissue sampling from dead whales. toxicosis and increased vulnerability to human activities: Durbin
et al. (2002) concluded that toxic algae ingestion by North Atlantic
right whales could increase whale susceptibility to collisions with
4.1 Direct and indirect effects of HABs on ships or fouling in fishing gear resulting primarily from diminished
marine mammals respiratory capabilities (and increased periods at the water’s
surface); the other posited a possible link between reduced whale
Events involving the deaths of scores of marine mammals have avoidance of vessels resulting from synergies or co-morbidities
been attributed to exposure to HABs. Algal toxins have been following toxic algal exposure (Savage, 2017). Understanding the
implicated (but generally not fully established) in various large role of toxic algal morbidity in marine mammals relative to human
whale UMEs (https://smdp.com/2015/09/28/increase-whale- commercial activities may help provide a means to limit the
deaths-gulf-alaska/; https://repository.library.noaa.gov/view/noaa/ negative impacts from those activities.
17715), in the deaths of hundreds of California sea lions in
multiple years in the last three decades 2015 (Scholin et al., 2000;
Di Liberto, 2015; Anderson et al., 2021), and in other large-scale 4.2 Impacts of principal causative agents
marine mammal mortality events (de la Riva et al., 2009). Yet,
considering the extent and frequency of occurrences of HABs, Alexandrium was the most common type of bloom, and overall, it
marine mammal die-offs from exposure to HAB toxins appear to may also be the type of bloom putting whales at greatest risk. Pseudo-
be remarkably rare events (Starr et al., 2017). Nonetheless, marine nitzschia blooms were more prevalent in U.S. west coast (34% of all
toxicologists continue to seek associations between HABs and reported blooms) than east coast waters; only 8 blooms were reported
marine mammal die-offs. Instead, we posit that debilitating (7% of all blooms) for east coast waters. However, 11% of whale
consequences from sub-lethal concentrations of HAB toxins may deaths and injuries occurred<100 miles of active blooms involving
be the source of indirect, and perhaps more serious population-level this species in east coast waters, and up to 29% of all U.S. Pacific coast
consequences for marine mammals when also exposed to existing whale mortalities and injuries. Thus, while blooms involving Pseudo-
threats such as commercial fishing and vessel operations. nitzschia occurred less commonly than those involving Alexandrium,

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TABLE 5 Occurrence of whale mortalities and injuries within 10, 50 and 100 miles of U.S. west coast harmful algal blooms (HAB).

U.S. West Coast

Group Genus Within 10 miles of active HAB Within 50 miles of active HAB Within 100 miles of active HAB
Dinoflagellates

Alexandrium 10 (56%) 51 (67%) 86 (68%)

Cochlodinium 0 0 0

Dinophysis 0 2 (3%) 3 (2%)

Pyrodinium 0 0 0

Margalefidinium 0 0 0

Amphidinium 0 0 0

Prorocentrum 0 0 0

Takayama 0 0 0

Karenia 0 0 0

Diatoms

Pseudo-nitzschia 8 (44%) 23 (30%) 37 (29%)

Raphidophytes

Chattonella 0 0 0

Haptophytes

Algirosphaera 0 0 0

TOTAL 18 76 126

Percentages of all recorded whale deaths and injuries occurring within denoted distance ranges of an active HAB (and its respective causative agent) are indicated.

the former may also represent a potent agent involved in indirect locations when HABs were not reported. However, this relationship is
effects on marine mammal populations. not apparent along the east coast. Inconsistent patterns between the two
coasts may reflect differences in the coastal and nearshore biological
oceanography and ecology. For example, the east coast has relatively
4.3 Differences in east and west coast HAB shallower, warmer waters, which may foster disparate conditions for algal
and whale data sets blooms. Patterns may also differ because of variance in algal species
composition and diversity in the data sets from the two coasts.
In U.S. west coast waters, large whale injuries and mortalities In addition, differences between coasts may result from differences
occurred in higher densities near an active HAB than in times and in the extent of marine mammal and/or HAB monitoring between the

FIGURE 5
Rates of increase in harmful algal blooms (HAB) (green circles) in U.S. west coast waters, 2007-2021 (A) and U.S. east coast waters, 2000-2021 (B).
Black lines represent predictions from linear model (HAB occurrence ~ year), and gray shaded area indicates 95% CIs.

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TABLE 6 U.S. West Coast Whale Mortalities/injuries.

> 5 records

Month > 10 records

Year Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total (yr) Avg/Mo.
2007 2 1 0 3 3 3 3 2 3 3 1 0 24 2.0

2008 1 2 3 1 1 1 1 4 1 1 0 1 17 1.4

2009 3 1 2 4 2 2 2 2 2 2 0 0 22 1.8

2010 0 2 4 6 4 1 2 8 2 2 0 2 33 2.8

2011 1 1 0 1 3 1 5 4 1 1 1 1 20 1.7

2012 3 0 2 3 6 3 1 2 0 1 0 1 22 1.8

2013 1 2 3 3 1 5 2 1 1 1 0 0 20 1.7

2014 1 0 1 3 6 3 4 2 9 4 1 0 34 2.8

2015 3 5 7 1 9 5 6 6 10 5 5 1 63 5.3

2016 1 3 3 9 11 12 5 15 5 5 1 1 71 5.9

2017 3 1 3 7 3 7 3 3 3 2 2 2 39 3.3

2018 1 2 4 5 16 5 9 10 7 7 3 1 70 5.8

2019 0 0 4 7 4 4 3 7 3 2 1 2 37 3.1

2020 2 2 0 3 3 1 5 5 3 4 1 0 29 2.4

2021 1 0 2 10 8 6 4 1 1 2 6 2 43 3.6

total 23 22 38 66 80 59 55 72 51 42 22 14 544

Number of large whale deaths and injuries in each month and year in U.S. west coast waters, 2007-2021. The number in each cell is the number of observed whale deaths or injuries by month and
year. Yellow-shaded cells indicated >5 or more deaths/injuries in that month; brown-shaded cells indicate >10 deaths/injuries.

two coasts. Marine mammal surveys off the east coast are more and was the prey responsible for a large-scale mortality event
numerous, systematic, and larger in spatial coverage (including involving humpback whales, and researchers concluded that the
farther from the shore) than in west coast waters. Furthermore, HAB toxin had been transported considerable distances by the mackerel
monitoring near areas of human recreation and nearshore fisheries in (Geraci et al., 1989). The northern anchovy (Engraulis mordax) was
numerous bays, estuaries, and near municipalities appears to have identified as the primary trophic vector of DA in the death of a
occurred at a greater extent along the eastern seaboard relative to the minke whale (Balaenoptera acutorostrata) in waters off California
west. Systematically collected data across space and time could better (Fire et al., 2010). Durbin et al. (2002) concluded that ingestion of
support models that predict the overlap of whale and HAB occurrence PSP-ladened zooplankton was the source of neuropathology
and distribution and help shape management actions to reduce indirect (including muscle paralysis) in North Atlantic right whales with
marine mammal injuries and deaths. In addition, further research on the potential to adversely affect the whales’ respiratory capabilities
this subject, and related subjects, would benefit from standardization of and feeding behavior. Lefebvre et al. (2002a) found algal toxins in
whale mortality data reporting and curation across the various blue and humpback whale fecal material as well as in the krill and
stranding programs, and in providing records to central repositories small bait fish they were consuming and concluded that DA can
that provide for transparency and are generally available for analysis. permeate pelagic as well as benthic communities.
It appears scores of marine mammal species – as indicated in
diets, fecal samples and by other means – are capable of carrying
4.4 Toxin pathways and whale chronic levels of HAB toxins with no clinical signs of acute
natural histories neurotoxicity (e.g., Lefebvre et al., 2002a; Lefebvre et al., 2016);
and toxicity, at levels that are not fatal, appear to be permanent or
HAB toxins are capable of persisting in components of marine semi-permanent features of ecosystems (e.g., Danil et al., 2021;
ecosystems and can be transmitted to cetaceans and other marine Hendrix et al., 2021). In a long-term study involving 23 species in
mammal species via prey items such as krill and finfish (Lefebvre waters off New England, marine mammals experienced significant
et al., 1999). Schooling fish such as the Spanish mackerel and widespread exposure to HAB toxins, but little correlation was
(Scomberomorus spp.) have been identified as the vector for STX found between HABs and HAB-associated marine mammal

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TABLE 7 U.S. East Coast Whale Mortalities/injuries.

>5 records >15 records

>10
Month >20 records
records
Year Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total (yr) Avg/Mo.
2000 4 0 4 4 7 8 6 12 3 4 4 3 59 4.9

2001 7 5 4 7 10 9 7 10 4 3 2 4 72 6

2002 1 4 2 7 5 10 9 9 8 6 6 1 68 5.7

2003 5 3 10 5 15 10 14 20 9 7 6 1 105 8.8

2004 1 5 2 3 8 9 5 7 3 3 7 8 61 5.1

2005 4 2 4 4 4 7 17 8 6 5 2 1 64 5.3

2006 6 2 4 8 4 4 11 19 13 2 4 3 80 6.7

2007 6 1 7 2 9 7 17 6 11 3 3 3 75 6.3

2008 9 5 3 2 7 11 13 7 9 5 2 4 77 6.4

2009 2 7 5 7 8 5 6 9 9 5 4 3 70 5.8

2010 3 5 6 5 13 5 5 10 5 2 1 3 63 5.3

2011 8 4 9 8 6 4 22 10 7 7 4 3 92 7.7

2012 11 6 7 6 5 15 17 14 6 4 1 6 98 8.2

2013 7 0 2 10 2 6 6 5 5 5 1 2 51 4.3

2014 4 1 7 8 5 6 9 8 4 4 2 4 62 5.2

2015 0 2 1 4 9 11 12 8 16 6 3 4 76 6.3

2016 10 3 7 7 11 11 13 10 12 6 3 10 103 8.6

2017 7 8 3 10 8 5 12 19 6 19 5 4 106 8.8

2018 4 10 3 3 10 7 16 24 25 5 3 7 117 9.8

2019 2 5 6 4 8 6 11 12 16 12 4 4 90 7.5

2020 6 10 4 7 8 8 13 9 6 5 6 7 89 7.4

2021 7 4 5 3 1 7 12 18 7 7 1 2 74 6.2

total 114 92 105 124 163 171 253 254 190 125 74 87 1752

Number of large whale deaths and injuries in each month and year in U.S. east coast waters, 2000-2021. The number in each cell is the number of observed whale deaths or injuries by month and
year. Yellow-shaded cells indicated >5 or more deaths/injuries in that month; brown-shaded cells indicate >10 deaths/injuries; blue-shaded cells indicate >15 deaths/injuries; re-shaded cells
indicate >20 deaths/injuries.

mortality events (Fire et al., 2021). Nonetheless, of the 458 species In our study, blooms involving DA were relatively infrequently
sampled, 19% tested positive for either DA or STX, or both; reported for the U.S. east coast waters, making it noteworthy that
humpback whales exhibited the highest rates of the presence of DA has been found in animals sampled in offshore habitats and in
DA of all species tested; and DA was also most prevalent in whale bycaught individuals. East coast DA blooms may occur primarily
and dolphin species bycaught in commercial fishing gear and in far from shore, making them less likely to be sampled by coastal
those sampled from waters distant from the coast. Similar findings monitoring programs but at the same time having adverse effects on
were reported in a 2003 study involving Gulf of Maine and Georges cetacean species feeding in offshore habitats.
Bank waters in which high concentrations of DA were found in In our study, the humpback whale was the species most often
water samples as well as dead whales (primarily humpback whales) appearing in whale injury/mortality databases, comprising nearly
(https://www2.whoi.edu/site/andersonlab/past-projects/pseudo- half of all records for both coasts (Table 4). This may reflect,
nitzschia-emerging-hab-threat-in-the-gulf-of-maine/). These primarily, the abundance of this species relative to other baleen
findings appear to support the contention that marine mammals whale species – humpback whales are increasing in abundance,
may tolerate low-level toxicities that (while not lethal) may be globally, and the species can be rather common in many parts of its
detrimental during interactions with human activities. range (Betteridge et al., 2015). Minke whale injuries/mortalities

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were likewise commonly represented (ca. 23% of the records) in the include, for example, whales that were struck or entangled, died at
U.S. east coast data set (but much less frequently occurring in the sea, yet their carcasses were not recovered, or their deaths otherwise
west coast data). Humpback and minke whales are primarily not observed, or records that may exist elsewhere but are not, for
piscivores, while less represented species (e.g., right and blue various reasons, included in these datasets. Threats from those
whales) in the database feed primarily at lower trophic levels (e.g., human activities may be substantially magnified if the sensorimotor
zooplankton). In feeding mostly on schooling fish species (although capabilities of animals that encounter fishing gear or ships in their
they also consume zooplankton), humpback and minke whales are habitats are diminished or debilitated.
likely exposed to higher levels of algal toxins through ecosystemic Given the scope and densities of commercial fishing gear (e.g.,
bioaccumulation than whales feeding at lower trophic levels ‘(e.g., Moore et al., 2021; Richardson et al., 2022) and vessel traffic (e.g.,
blue and right whales; although gray whales are also likely exposed Pirotta et al., 2019; Silber et al., 2021) in U.S. coastal waters – which
to high levels of bio-accumulated HAB toxin concentrations when now encompass staggeringly large areas of marine habitats – it is
feeding on bivalves and other benthic organisms), and this may perhaps remarkable that entanglement and vessel strike rates are
account, at least in part, for their frequency of occurrence in the not far greater than reported as whales attempt to navigate
data sets. these conditions.
Conditions leading to elevated internal toxin loads are likely Numerous factors likely play roles in whales’ negative interactions
dependent on numerous factors – the duration, scale, and severity of with fishing lines and gear or oncoming ships. Very little is known
the bloom, the duration and extent of mammal exposure to the about faculties – if any – a whale might have to detect or avoid fishing
ocean-borne toxins, and the natural history of the mammals (if they gear in the water column or the approach of a vessel. Visual systems,
are primarily piscivores, for example) primary among them. Oceanic for example, are of limited utility in low-light conditions or at depth;
and environmental conditions that drive HAB occurrences and and the sound of oncoming vessels is almost certainly detected by a
trajectories in turn likely involve the interaction of multiple whale, but the animal may perceive the stimuli as benign until it is too
physical (e.g., upwelling) and chemical (e.g., introduced nutrients) late. Whales engaged in vital behavior such as feeding or mating may
oceanic processes. While marine mammals may routinely carry non- have little regard for threats such as a moving vessel or entangling gear.
lethal toxin loads, symptoms of chronic toxicosis may be exacerbated Nonetheless, even relatively rudimentary detection and avoidance
by environmental perturbations, in response to additional or novel strategies may be diminished by sensory, neurological, or motor
environmental stressors, or newly or already compromised disfunction thereby heightening vulnerability to threats from human
immune systems. activities – a situation that further confounds conservation efforts.
Toxic algal species have existed for tens of millions of years and
were a part of marine ecosystems in which whales evolved. Perhaps, as
4.5 Population-level consequences noted, marine mammals can tolerate chronic low levels of toxins – and
of threats this may explain why large-scale die-offs are relatively rare considering
the extent to which marine mammals are routinely exposed to the
Abundances of most large whale populations in U.S. waters are toxins. However, motorized ships and large-scale fishing enterprises are
steadily increasing (https://www.fisheries.noaa.gov/national/ relatively new components of whale habitats and represent novel
marine-mammal-protection/marine-mammal-stock-assessment- threats to which these animals are not adapted.
reports-species-stock), notably those of the humpback whale
(Betteridge et al., 2015). Nonetheless, all large whale species
continue to be negatively affected by entanglement in fishing gear 4.6 Coincidence of severe blooms and
(Reeves et al., 2013; Thomas et al., 2016) and ship strikes worldwide whale deaths & injuries
(Jensen and Silber 2003). Nearly all large whale species remain listed
on the U.S. Endangered Species Act’s List of Endangered and In multiple years, notably high levels of whale mortalities/injuries
Threatened Wildlife and Plants, and the rates of entanglement in coincided with large-scale, persistent, or particularly potent HAB
commercial fishing gear and collisions with vessels remain events. Occurrences of HABs and high levels of whale deaths/injuries
significant challenges for large whale species recovery. For some did not align in all years. For example, although blooms of Pseudo-
populations, including the depleted and probably declining North nitzschia in waters off southern California in 2007, 2011 and 2017
Atlantic right whale, reducing interactions with human activities involved concentrations that were among the highest values reported
remain significant conservation challenges. in the literature (Smith et al., 2018) we found no evidence of elevated
In the two data bases examined in this study alone, 556 U.S. west coast whale deaths/injuries in those years (Tables 6, 7).
west coast whale injuries and mortalities were recorded and 1,667 Nonetheless, in the sections that follow, we describe several
occurred along the U.S. east coast involving at least seven species illustrative cases during which high levels of whale injuries/
(also, see, for example, Henry et al., 2022; Carretta et al., 2023). mortalities coincided with severe HAB events.
(note: in the analysis presented here, we removed records from this
dataset in which human-interaction, i.e., ship strike or fishing gear 4.6.1 2015-2016 U.S. West coast bloom –
entanglement, was not indicated.) Put another way, that is ca. 64 Pseudo-nitzschia
such incidents per year, or about (and at least) 5-6 per month for In 2015-2016 an unprecedented Pseudo-nitzschia bloom
U.S. east and west coast continental margins. These records do not extended from Alaska to southern California (Di Liberto, 2015;

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McCabe et al., 2016). From May 2015 to at least September 2015, The blooms were apparently fueled by an influx of Scotian Shelf
DA concentrations were among the highest recorded to that time water (Clark et al., 2021), suggesting its toxic effects may have been
(McCabe et al., 2016). Harvest closures for numerous shellfish widespread with oceanic origins. Collectively, these waters are also
species were enacted from May-November 2015 at various key summer/fall feeding habitats for humpback and right whales,
locations in British Columbia, Washington, Oregon, and among other species.
California (Ryan et al., 2017). Further, recurring patterns began to emerge. Anomalously high
DA was detected in harbor seals (Phoca vitulina), Northern fur DA levels were detected in waters off Rhode Island in the summers/falls
seals (Callorhinus ursinus), porpoises, dolphins, and whales in of 2017, 2018 and 2019, including a particularly concerning toxic
samples through late 2015 (Di Liberto, 2015) in an area that species, P. australis (Sterling et al., 2022); high DA levels in spring 2017
extended from the Pacific Northwest to southern California. In again closed shellfish harvests in Narragansett Bay, Rhode Island. In
California over 200 sea lions died from exposure to Pseudo- 2017, the first Karenia mikimotoi bloom was identified in Maine waters,
nitzschia; an additional 83 sea lion deaths were reported in 2016. and a rare late fall Pseudo-nitzschia bloom closed Casco Bay, Maine to
Large-scale seabird deaths occurred off California in the same shellfish harvests (https://www.bigelow.org/news/articles/2018-09-
period (Gibble et al., 2018). An ‘Unusual Mortality Event’ (UME) 19.html). Shellfish closures were re-established in fall 2017
was designated for large whale species from May to December 2015 through winter 2018 in eastern and western Maine (Bates et al.,
in the Gulf of Alaska, and from April 2015 to April 2016 in British 2018; http://www.pressherald.com/2017/09/14/algae-bloom-forces-
Columbia (over 50 whales deaths, primarily fin and humpback suspension-of-shellfishing-in542parts-of-down-east-maine/), and
whales, were reported) (https://www.fisheries.noaa.gov/national/ again in the falls of 2018 and 2019 (Clark et al., 2021).
marine-life-distress/2015-2016-large-whale-unusual-mortality- From January 2016 to the present, elevated humpback whale
event-western-gulf-alaska). While the HAB was cited as a possible mortalities have occurred along the Atlantic coast from Maine
contributing factor in the large number of whale deaths, no through Florida (https://www.fisheries.noaa.gov/national/marine-
definitive cause of the UME was identified (Bates et al., 2018). life-distress/2016-2024-humpback-whale-unusual-mortality-event-
In the large whale data set analyzed here, a total of 63 whale along-atlantic-coast). In April 2017 a humpback whale UME was
deaths/injuries were reported for the U.S. west coast in 2015, the designated for the U.S. east coast for the period beginning in
third highest death/injury toll of all years considered in this study January 2016 (https://www.fisheries.noaa.gov/national/marine-life-
(2016 being the overall highest at 71 deaths/injuries; nearly one- distress/2016-2024-humpback-whale-unusual-mortality-event-
quarter of all reported U.S. west coast whale deaths/injuries along-atlantic-coast). The UME is ongoing. While, to date, the
occurred in 2015 and 2016; Table 6). In May-November 2015 cause(s) of the UME have not been (officially) determined, of those
alone, at the height of the bloom, 46 whale deaths/injuries whales for which partial or full necropsy examinations were
resulting from human interactions were reported in Washington, conducted (a total of about 90 individuals) 40% exhibited
Oregon, and California, namely vessel strikes (n=3) and gillnet, pot/ evidence of human interaction, meaning either ship strike or
trap, or unidentified fisheries entanglements (n=43). entanglement mortality.
The whale mortality/injury database indicates that 103, 106, and
4.6.2 2016-2019 East coast blooms – 119 whale deaths and injuries were recorded along the U.S. east
Pseudo-nitzschia coast in 2016, 2017, and 2018, respectively – among the highest
In the fall/winter of 2016-2017 an anomalous bloom of Pseudo- numbers for any year in the sample (Figures 2, 4; Table 7). A cluster
nitzschia resulted in the closure of hundreds of miles of Maine of unusually high number of whale death/injuries occurred in
coastline to shellfish harvests – thus becoming the first regional (i.e., August-October in 2017, 2018, and 2019, including the highest
Gulf of Maine) DA-induced shellfishery closure (Clark et al., 2019). number in the entire database in August and September 2018
In September 2016, nearly 30 tons of commercially harvested (Table 7). The 19 whale deaths and injuries in October 2017 were
shellfish were recalled by the state of Maine (Lewis et al., 2017; the highest for that month in the entire sample and was 3-times
https://www.bigelow.org/news/articles/2018-09-19.html), and the higher than the 22-year monthly average for that month (Table 7).
Canadian Food and Inspection Agency prohibited shellfish
harvesting in swaths of the Bay of Fundy (Canada) in October 4.6.3 2018 U.S. West coast bloom – Alexandrium
2016 (Bates et al., 2018). In its entry in the HAB data base, Maine’s While apparently receiving far less attention in the literature
Department of Marine Resources reported that although ‘low levels than Pseudo-nitzschia blooms described above, the HAB data
of DA had been detected [in this region] in the past … toxicity of records documented a geographically extensive Alexandrium
this scale had never before been recorded.’ This bloom apparently bloom that occurred January to August 2018 in California waters.
began in the Bay of Fundy and progressed southwestward along the The bloom initially developed off central California, occurred
coasts of Maine, Massachusetts, and Rhode Island; consequently, subsequently in northern California waters, and was then
precautionary closures were implemented in significant portions of detected in southern California. Numerous records indicate that
Massachusetts and Rhode Island state waters in October 2016 toxicity levels far exceeded toxicity threshold standards, in some
(Sterling et al., 2022). Bloom toxicity had a rapid onset, with cases by greater than one order of magnitude.
shellfish rapidly accumulating 3-4 times the DA closure limit in Whale mortalities and injuries (n=70) on the U.S. west coast in
(https://www.bigelow.org/news/articles/2018-09-19.html). 2018 were the second highest of all years in our sample (Figures 2,

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Silber and Silber 10.3389/fmars.2024.1454656

3). The monthly average (5.8 whale deaths and injuries per month) acknowledge this may reflect increased monitoring efforts. Yet, it is
for the year was nearly two-fold greater than the monthly average possible that perceived increases in HAB occurrence may reflect, at
(X=3.0) in the 15-year period for which data were available; and the least in part, increased awareness about the detriments of HABs on
highest monthly total number of whale injuries/mortalities in the public health and a subsequent increase in monitoring and
entire sample occurred in May of that year (Figure 3; Tables 6, 7). reporting efforts (e.g., Sellner et al., 2003; Hallegraeff, 2010;
Most (n=55) 2018 whale injuries/deaths were attributed to gillnet Hallegraeff et al., 2021).
and pot fisheries interactions (followed by vessel strikes, n=14, and However, increased monitoring efforts would not account for
marine debris, n=1); and most of these (n=50) occurred in apparent interannual variability in the occurrence of HABs
California waters. (Figure 3). Between year variability, instead, suggests that complex
oceanographic processes, such as variation in physical (e.g.,
4.6.4 2003 U.S. East coast bloom – Alexandrium upwelling, water temperatures) and chemical (e.g., nutrient levels)
and Pseudo-nitzschia conditions, have important roles in inducing HABs. Some of these
Records in the HAB database documented high levels of processes have been identified (e.g., McCabe et al., 2016; Sandoval-
Alexandrium in spring through fall 2003 (in some areas detected Belmar et al., 2023) but a full discussion of these factors remains
as early in the year as January) in New England waters. Numerically, beyond the scope of our study. If, however, HAB frequency is in fact
reported HABs were moderate (i.e., only four blooms were reported rising as related to warming temperatures and other (human-
in 2003 (all involving Alexandrium). However, the geographic induced) factors, greater direct and indirect marine mammal
extent and the severity of the bloom were noteworthy: extending vulnerability to HAB events might be expected. For example, shifts
from Massachusetts Bay, including Cape Cod and the North Shore in distributions of marine mammals and their prey in response to a
(Massachusetts), to western and eastern Maine. changing climate (e.g., Silber et al., 2017; Hudak et al., 2023) or other
In 2003, STX concentrations sampled from shellfish tissue were environmental features (e.g., Santora et al., 2020) could result in
some of the highest indicated in the database; in some instances, increased threats to marine mammals from increased or novel
levels were many-fold greater than prescribed ‘alert’ levels for human exposure to fixed fishing gear or other threats in new aggregation
consumption. Multi-state shellfish harvest closures were established locations (e.g., Santora et al., 2020; Ingman et al., 2021; Meyer-
as a result. Most shellfish closures were relaxed in the region by fall Gutbrod et al., 2023). These are subject areas for further research.
2003, but one record indicated that the Maine offshore quahog
(Mercenaria mercenaria) fishery remained partially closed into 2004.
The U.S. east coast whale database contains 105 records of 4.8 Management implications – the
whale injuries and deaths for the year 2003, among the highest for importance of HAB predictions to
all years represented in the sample (Tables 7). In cases in which whale conservation
source of the interaction was known (those constituting 38% of
those reported in 2003), fishing gear entanglements accounted for Environmental monitoring and various predictive modeling
35 instances and ship strikes for five of them. In May-September approaches are being used worldwide, and with increasing
alone, 68 whale mortalities/injuries were reported (Tables 7). Of sophistication, to identify the interplay of conditions that are
these, over 20 whales (mostly humpback whales) died near Georges antecedent to blooms (e.g., Dabrowski et al., 2016; Glibert et al.,
Bank (a large area offshore and east of Massachusetts) and off the 2018; Litchman, 2022; Sandoval-Belmar et al., 2023). Satellite
Maine coast in July 2003 (https://www2.whoi.edu/site/andersonlab/ imagery and other types of remote sensing are being employed on
past-projects/pseudo-nitzschia-emerging-hab-threat-in-the-gulf- large spatial scales to monitor oceanographic features that can lead
of-maine/). Plankton sampling in those same waters indicated the to harmful blooms (e.g., Stumpf, 2001; Kahn et al., 2021). Similarly,
presence of Pseudo-nitzschia spp., and domoic acid was detected in modeling exercises that predict large whale spatiotemporal
most of the whales sampled, some exhibiting high concentrations occurrence are now established analytical practices in marine
(https://www2.whoi.edu/site/andersonlab/past-projects/pseudo- mammalogy (e.g., Roberts et al., 2016; Redfern et al., 2017). And
nitzschia-emerging-hab-threat-in-the-gulf-of-maine/). the locations and spatial extent of human activities such as vessel
traffic densities (e.g., Silber et al., 2021; Silber and Adams, 2019) and
commercial fishing operations (derived, for example, from fishing
4.7 Increasing occurrence of HABs regulation data, on-board observer data) can be quantified on
various scales. Therefore, by coupling predictive analyses of the
Numerous studies have indicated that the HAB frequency, occurrence and distribution of HABs, large whale occurrence
duration, and severity are increasing on national (e.g., Anderson information, and human activities, whale vulnerability to threats
et al., 2021) and global scales (e.g., Van Dolah, 2000; Anderson et al. from human maritime uses could be reduced. For example, fishing
2012; IWC, 2017; Broadwater et al., 2018); and these rates have gear deployment could be temporarily limited (in geographic scope
often been attributed to rising ocean temperatures (e.g., Hinder or effort) to minimize threats to large whale populations potentially
et al., 2012; IWC, 2017), acidification, and nutrient pollution, exposed to harmful blooms. Any such modeling that seeks to
among other things (e.g., Gobler, 2020; Anderson et al., 2021). characterize whale, human activity, and HAB distributional
Our analysis, too, indicated (apparent) generally increasing trends overlap would also need to account for possible shifts (especially
in HAB occurrence in the last two or so decades (Figure 5); but we those that are climate related) in the occurrence of whales or their

Frontiers in Marine Science 15 frontiersin.org

Silber and Silber 10.3389/fmars.2024.1454656

prey (see, for example, Hare et al., 2010; Wright et al., 2023), www.fisheries.noaa.gov/national/marine-mammal-protection/
anomalous warm water masses (e.g., Santora et al., 2020), and other marine-mammal-stock-assessment-reports-species-stock#cetaceans
types of oceanographic variability. —large-whales.
Ample precedent exists for management actions that curtail,
relocate, or otherwise modify fishing operations (e.g. NOAA, 2021,
2023; Cole et al., 2021) and shipping activities (e.g., Silber et al., Author contributions
2014; Rockwood et al., 2017) through policy actions or rulemaking
to limit whale entanglement and ship strikes. It may be possible to GS: Writing – review & editing, Writing – original draft,
modify or expand such efforts to reduce whale mortality by Methodology, Investigation, Data curation, Conceptualization. KS:
anticipating HAB events, thereby enhancing whale conservation. Writing – review & editing, Writing – original draft, Methodology,
Investigation, Formal analysis, Data curation.

5 Conclusions
Funding
We posit that sub-lethal concentrations of HAB toxins increase
marine mammal vulnerability to some human activities. We found The author(s) declare that no financial support was received for
compelling, but not necessarily definitive, evidence that exposure the research, authorship, and/or publication of this article.
(possibly even at chronic low levels) to HAB toxins can increase the
chances of large whale injury and death from interactions with
moving vessels and commercial fishing gear. Evolutionarily, large Acknowledgments
whales are not well-equipped to detect and avoid such hazards and
faculties they may have – if any at all – to avoid such hazards may be U.S. NOAA Fisheries’ Allison Henry graciously provided a
compromised by symptoms associated with HAB toxins. Increasing comprehensive, carefully assembled, and vetted U.S. east coast
capabilities to forecast the occurrence of HABs based on knowledge whale death and injury database spreadsheet; and James V.
of oceanic conditions that prompt large-scale or severe blooms may Carretta graciously provided the same information for the U.S.
likewise provide an ability to predict the occurrence of fatal west coast. We commend their dedication to their work. We are
interactions with human activities. Predicting bloom occurrence grateful to all those who consistently and tirelessly gather data on
could be a useful tool in developing whale conservation measures, algal blooms and whale strandings.
such as curbing or moving vessel or fishing operations to alternative
locations or times when and where blooms are expected to occur.
Additional work is needed to further determine if whale mortalities/ Conflict of interest
injuries are associated with the blooms – and at scales with finer
resolution than those used in our study. Additional work is also The authors declare that the research was conducted in the
needed to determine if HAB predictive and forecast modeling absence of any commercial or financial relationships that could be
approaches can also be used to reduce the impacts of human construed as a potential conflict of interest.
commercial activities to large whale population recovery. If so,
such an approach could become a potent conservation tool.
Publisher’s note
Data availability statement All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
Publicly available datasets were analyzed in this study. This data organizations, or those of the publisher, the editors and the
can be found here: Harmful Algal Event Database (HAEDAT), reviewers. Any product that may be evaluated in this article, or
UNESCO Intergovernmental Oceanographic Commission claim that may be made by its manufacturer, is not guaranteed or
(HAEDAT; http://haedat.iode.org/); whale mortality data: https:// endorsed by the publisher.

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