Technical Memorandum:
Review of MWRA Water Quality
Monitoring Results to Address Potential for
Harmful Effects of the Deer Island
Discharge on Threatened and Endangered
Species in Massachusetts Bay
EPA/600/R-22/063
Review Team
James Hagy1, CEMM/ACESD
Tim Gleason1, CEMM/ACESD
Autumn Oczkowski1, CEMM/ACESD
Avery Tatters2, CEMM/GEMMD
Yongshan Wan2, CEMM/GEMMD
1U.S. Environmental Protection Agency, Center for Environmental Measurement and Modeling,
Atlantic Coastal and Environmental Sciences Division, Narragansett, Rl
2U.S. Environmental Protection Agency, Center for Environmental Measurement and Modeling,
Gulf Environmental Measurement and Modeling Division, Gulf Breeze, FL
August 4, 2022
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Purpose
To assist the U.S. Environmental Protection Agency (EPA) Region 1 in addressing questions and
concerns related to reissuance of the administratively continued National Pollution Discharge
Elimination System (NPDES) discharge permit for the Massachusetts Water Resources
Authority's (MWRA) Deer Island Treatment Plant (DITP), EPA Region 1 requested that a review
team from EPA's Office of Research and Development (ORD) evaluate the data and analyses
included in recent MWRA water column monitoring reports. The charge to the team was to
evaluate how these data and analyses address the potential for the discharge to cause
environmental effects that could harm North Atlantic right whales (Eubalaena glacialis).
Several other threatened and endangered species utilize habitats in Massachusetts Bay,
including Atlantic sturgeon (Acipenser oxyrinchus), shortnose sturgeon (Acipenser
brevirostrom), leatherback sea turtle (Dermochelys coriacea), loggerhead sea turtle (Caretta
caretta), kemp's ridley sea turtle (Lepidochelys kempii), green sea turtle (Chelonia mydas), and
fin whale (Balaenoptera physalus). While many of the issues and questions we address in this
report could apply to these species, not all apply identically. We retained our focus on North
Atlantic right whales.
EPA Region 1 separately requested that the review team consider what if any changes may be
recommended to the continency plan and ambient monitoring plan required under the Deer
Island discharge permit to better monitor environmental responses or impacts potentially
related to the discharge. This is addressed in a separate technical memorandum.
EPA Region 1 did not request that the ORD team complete a comprehensive review of the
available science relating environmental effects of the DITP discharge to North Atlantic right
whales in Massachusetts Bay. EPA Region 1 also did not request that ORD create a new or
revised design for the ambient monitoring program.
Disclaimer
The views expressed in this document are those of the review team members and do not
necessarily represent the views or the policies of the U.S. Environmental Protection Agency.
This document has been reviewed in accordance with U.S. Environmental Protection Agency
policy and approved for distribution.
Suggested Citation
Hagy, J., T. Gleason, A. Oczkowski, A. Tatters, and Y. Wan. 2022. Technical Memorandum:
Review of MWRA Water Quality Monitoring Results to Address Potential for Harmful Effects of
the Deer Island Discharge on Threatened and Endangered Species in Massachusetts Bay. US
Environmental Protection Agency, Office of Research and Development, Narragansett, Rl.
EPA/600/R-22/063. 20 pp.
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Key Conclusions
• The MWRA reports do not show evidence that the discharge is currently harmful to
North Atlantic right whales (Eubalaena glacialis) or that it is likely to cause harm in the
future. However, these data also do not provide evidence for the opposite, namely that
such an impact is not already occurring or that it would be unlikely in the future.
• These data and additional evidence documenting related biological changes across the
Gulf of Maine suggest that Massachusetts Bay is experiencing a shift in biological and
oceanographic regimes. The regime shift increases the scientific uncertainty regarding
the role of the discharge in supporting harmful algal blooms (HABs) in Massachusetts
Bay and resulting effects of HABs on the marine food web supporting whales.
• The MWRA water column monitoring results document biological changes both near the
discharge and across Massachusetts Bay principally characterized by seasonal increases
in the abundance of several HAB species including the dinoflagellates Alexandrium
catenella since 2005 and Karenia mikimotoi since 2017.
• Although there is little evidence that HABs are harming whales in New England, North
Atlantic right whales in New England are currently exposed to saxitoxin and domoic acid,
HAB toxins that elsewhere in the world have harmed and killed whales and other marine
mammals, seabirds, and marine fisheries.
• Ship strikes and entanglement in fishing gear are the main anthropogenic cause of
mortality of North Atlantic right whales; however, oceanic regime shifts may
significantly impact prey (Calanus finmarchicus) availability and marine HABs currently
present a relatively unpredictable, increasing, and potentially serious threat to North
Atlantic right whales. Therefore, a cautious approach is warranted that includes
continued monitoring of ecological changes near the outfall and in the surrounding
areas of Massachusetts and Cape Cod Bays. Monitoring should be adjusted to focus on
the most pertinent and prospective environmental concerns and their potential
relationship to the discharge.
Background
The Massachusetts Water Resources Authority (http://www.mwra.com) operates a wastewater
treatment facility on Deer Island in Boston Harbor. The facility, known as the Deer Island
Treatment Plant (DITP) discharges into Massachusetts Bay via a 15-km effluent outfall tunnel
that at nearly 400 million gallons per day (16.6 m3 s"1) is among the largest publicly owned
treatment works (POTW) discharges in the United States. The National Pollution Discharge
Elimination System (NPDES) permit for the discharge, which was issued on May 20, 1999, and
modified on July 10, 2000, is now administratively continued. EPA Region 1 is tasked with
reissuing the NPDES permit which, among other requirements, will involve a request to the
National Oceanic and Atmospheric Administration, National Marine Fisheries Service for re-
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initiation of the original Biological Opinion (National Marine Fisheries Service 1993) for the
MWRA permit based on new data, updates to the status of ESA-listed species, including the
North Atlantic right whales (Eubalaena glacialis) and their critical habitat, and listing of a new
species (Atlantic sturgeon).
Under the 2000 NPDES Permit (EPA 2000a), MWRA was required to develop and implement an
ambient monitoring plan (MWRA 1997) and contingency plan (MWRA 2001) for responding to
any negative impacts not directly addressed by the effluent limits in the DITP permit. A key
objective of the ambient monitoring plan is to "evaluate whether the environmental impact of
the treated sewage effluent discharges at the MWRA outfall in Massachusetts Bay is within the
bounds of the Supplemental Environmental Impact Statement" (Libby et al. 2020). These plans
have been revised overtime, reflecting resolution of questions by the monitoring program,
identification of new questions or concerns, and an evolving environmental context for the
discharge and its potential impacts (MWRA 1991, MWRA 2021). Some key concerns of the
water column monitoring program are reflected in parameters that have Contingency Plan
threshold values. These include bottom dissolved oxygen, rate of bottom oxygen decline, and
near-field (i.e., near the discharge) concentrations of chlorophyll-a, and the HAB taxa Pseudo-
nitzschia pungens1 and Alexandrium catenella (Libby et al. 2020). Additional aspects of the
monitoring program focus on the health of the marine benthos, including fluxes of nutrients
between the water and sediments.
Approach
We reviewed the water column monitoring data and analysis resulting from the Massachusetts
Water Resources Authority's (MWRA) ambient monitoring program as reported in 2016 to 2020
reports from the MWRA's Environmental Quality Department (Libby et al. 2017, Libby et al.
2018, Libby et al. 2019, Libby et al. 2020, Libby et al. 2021) to address the question: do the data
and analyses included in the MWRA reports provide evidence that environmental effects of the
DITP discharge are not likely to have an adverse effect on North Atlantic right whales. We
focused on the report that details 2019 monitoring results (Libby et al. 2020), which covered
the last year of normal monitoring prior to COVID-19, while also considering the most recent
report (Libby et al. 2021) and additional references from MWRA and the peer-reviewed
literature to support or provide context for our analysis. We have not conducted a full review of
all relevant literature.
1 Although this species-level identification is the contingency plan threshold (Libby et al. 2020), this level of
identification is not possible using light microscopy, which MWRA reports is used for identification.
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Findings
1. Consistent with prior conclusions, the DITP discharge does not create a
eutrophic condition in Massachusetts Bay
The MWRA water column data and analysis suggest that the discharge does not cause a broadly
eutrophic condition in Massachusetts Bay. Water quality impacts commonly associated with
eutrophication such as high or increasing algal biomass and hypoxia have not normally occurred
since operations at Deer Island began and have not been attributed to the discharge during the
past two decades. Our perspective is consistent with earlier reviews of the effects of the
discharge (Oviatt 2007, Hunt et al. 2010). Moreover, the diversion project led to relatively
modest impacts on Massachusetts Bay, while causing dramatic environmental improvements
within Boston Harbor (Taylor et al. 2020, MWRA 2021).
Although local effects of the discharge on nutrient concentrations have been noted in the
MWRA data, including elevation of NH4 and PO4 concentrations within 5 km of the discharge,
concentrations declined beyond that distance to levels observed across Massachusetts Bay
(Figure 3-1 in Libby et al. 2020). The results of early simulation models showed that changes to
the concentrations at the boundaries of Massachusetts Bay had a much greater effect on the
Bay than presence or absence of the discharge (Bearsdley et al. 1995), which implies that for
the nutrient budget of the entire Bay the discharge is not a dominant nutrient source. Recent
simulation modeling of Massachusetts Bay implements more sophisticated hydrodynamic
modeling than earlier models (Deltares 2022) but did not simulate scenarios that explicitly
evaluate water quality with and without inputs from wastewater (e.g., Kessouri et al. 2021),
which would provide better insight into any more subtle larger scale effects of the discharge.
Nonetheless, observations alone demonstrate that dissolved oxygen concentrations have not
been depressed near the discharge and did not regularly reach levels expected to impact
aquatic life (EPA 2000b) in any region of Massachusetts Bay, either before or after operation of
the discharge (Libby et al. 2020). Similarly, 2019 chlorophyll-a fluorescence both near and at
some distance from the discharge were within the range of variability observed from 1992-
2018 (Figure 2-14 in Libby et al. 2020), spanning a period before and after operation of the
discharge. One notable incidence of eutrophication-related impacts is an episode of hypoxia
that occurred in Cape Cod Bay in 2019 (Libby et al. 2020), which we discuss later.
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2. A new biological oceanographic regime, characterized by an increased frequency
and intensity of harmful algal blooms, may be emerging in Massachusetts Bay. If it
persists, this new regime will create a new environmental context for potential
impacts of the DITP discharge.
Biological regimes2, or "dynamic regimes," can be thought of as an ecosystem state to which
the ecosystem tends to return to over time. The ecosystem state may be defined in terms of
multiple community attributes such as biological community biomass and composition and
ecological process rates. A biological community often varies from its typical state within
normal limits of variability, whether perturbed by an external driver or due to internal
dynamics. Though variable, community composition and function within a biological regime
tend to return to the normal state over time, maintained by internal relationships and
feedbacks involving species and their environment (Mayer et al. 2004). Ecological time series,
such as the data collected by MWRA during the past several decades, can document biological
regimes and characterize their associated patterns of biological variability. The MRWA reports,
taken as a whole, advance the view that Massachusetts Bay has a biological regime and that
much of the ambient monitoring data falls within the normal bounds of that regime (Libby et al.
2020, Libby et al. 2021). We agree that this description applies to many aspects of the ecology
of Massachusetts Bay.
Even though many aspects of the ecology of Massachusetts Bay have not changed, important
changes are documented by the data and analysis in recent MWRA water column monitoring
reports. These data provide evidence that a new biological oceanographic regime could be
emerging in Massachusetts Bay. The new biological regime can be characterized by increased
frequency and intensity of harmful algal blooms (HABs), shifts in the seasonal and spatial
distribution of harmful algae, and incipient trophic and water quality impacts related to HABs.
As an example of the latter, changes in the zooplankton community may have occurred in
response to phytoplankton community changes and other ecological trends occurring at a
variety of spatial scales in response to drivers that include climate change (Meyer-Gutbrod et al.
2021, Pershing et al. 2021). Climate change has been projected to have detrimental effects on
the density of Calanus finmarchicus, a zooplankton species particularly important to North
Atlantic right whales (Grieve et al. 2017). Additionally, bottom water hypoxia occurred in
2 Biological regime shifts have been defined as pronounced and abrupt changes in ecosystems that persist for a
substantial period, extend across a large spatial scale or extent, and involve multiple characteristics of the
biological system. Such shifts have been described in a variety of biological systems, including ocean ecosystems
(Biggs, R., S. R. Carpenter, and W. A. Brock. 2009. Turning back from the brink: detecting an impending regime shift
in time to avert it. Proc Natl Acad Sci U S A 106:826-31.). Consistent with the concept of biological regime, a regime
shift implies that the changed system no longer tends to return to the original state, but instead varies around a
different state, with dynamics mediated by a new and changed set of internal ecological relationships. Where
external drivers, such as temperature, have changed, the new regime occurs within the context of those changes.
Ongoing monitoring of the biological community can be expected to document new patterns of variability
associated with the new biological regime.
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southern Cape Cod Bay in 2019 and 2020, resulting in mortality of lobsters and fish, and may be
related to changes in the prevalence of HABs among other possible environmental factors
(Fraser 2020, Libby et al. 2020, Libby et al. 2021).
While the available evidence may suggest that a new biological regime has emerged or is
emerging, we are not aware of evidence that this change has been caused by the MWRA
discharge. On the contrary, the observed ecological changes, such as increased frequency of
harmful algae, have occurred across the entire Gulf of Maine, a much larger scale than it is
reasonable to attribute to the discharge (Anderson et al. 2021). Significant HAB events also
have occurred in other ocean basins (e.g., McCabe et al. 2016), although it is not yet clear that
coastal HABs have increased globally (Hallegraeff et al. 2021). The data and analysis presented
by MWRA alone do not suggest that the discharge has exacerbated or accelerated the observed
biological changes in Massachusetts Bay. The potential that a biological regime change has
occurred implies that internal ecosystem dynamics, including biological responses to external
drivers such as the discharge, may also have changed or may be in the process of changing.
Because this new ecological regime is less well characterized and understood, the data
accumulated by the MWRA over the past 2 decades of monitoring provide less certain
inference regarding the potential for future impacts of the Deer Island discharge on biological
communities in Massachusetts Bay than if the biological regime was entirely unchanged.
We did not find evidence in the MWRA data to conclude that the observed increase in HABs is
currently impacting North Atlantic right whales in Massachusetts Bay, nor did the MWRA
reports show that such impacts are likely in the future. However, these data also do not provide
evidence for the opposite, namely that such an impact is not already occurring or that it would
be unlikely in the future. This would be difficult to evaluate definitively in any situation and may
be even more challenging to evaluate due to the ongoing biological changes in the region. The
ambient monitoring program was designed to assess management objectives directly related to
the point source such as permit compliance and potential public health risks. It was seen as a
less effective approach to addressing issues of regional concern, including risks to living
resources across Massachusetts and Cape Cod Bays and the Gulf of Maine (MWRA 1991).
To further examine these ideas, we examine several key aspects of the biological communities
in Massachusetts Bay, examine how they relate to potential impacts on North Atlantic right
whales, and address what evidence is present in the recent MWRA data.
3. Toxin-producing algae are an increasingly important component of the
Massachusetts Bay plankton community, reflecting regional-scale trends
Recent MWRA water column monitoring reports pointed to recent increases in the abundance
of the HAB-forming dinoflagellates Alexandrium catenella and Karenia mikimotoi in
Massachusetts Bay. The 2019 water column report also noted an exceptional abundance of
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another toxin-producing dinoflagellate, Dinophysis norvegica, which reached an abundance 10-
times higher than the long-term average (Libby et al. 2020).
A time series graph of Alexandrium abundances in Massachusetts Bay included in both the 2019
and 2020 MWRA water column reports (Fig 1) provides a useful perspective on long-term
changes in this species (Libby et al. 2019, Libby et al. 2021). Beginning with a notable bloom in
2005, Alexandrium abundance more often exceeded the caution threshold of 100 cells L 1 and
attained maximum abundances several orders of magnitude higher than before 2005.
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Fig 1. Nearfield abundance of Alexandrium, reproduced from Figure 2-27 in Libby et al. (2021). After the significant
bloom in 2005, Alexandrium blooms occurred more regularly.
Karenia mikimotoi is a harmful dinoflagellate that first appeared in Massachusetts Bay in 2017
and thereafter has increased in abundance and persistence (Libby et al. 2020). A bay-wide
bloom in August and September 2019 achieved an abundance 2-fold higher than the previous
maximum observed in Boston Harbor. Both the abundance and seasonal distribution of K.
mikimotoi increased further in 2020 (Libby et al. 2021). In other areas of the world major
coastal blooms have occurred, K. mikimotoi has caused mass fish mortality events via a variety
of mechanisms and caused significant ecological and economic losses (Li et al. 2019). Although
the most severe impacts have been associated with abundances still higher than those
observed in Massachusetts Bay, Libby et al. (2021) suggested that organic carbon from un-
grazed Karenia cells could have been a factor contributing to the 2019 and 2020 hypoxia events
in nearshore bottom waters of southwestern Cape Cod Bay.
The dinoflagellate Dinophysis norvegica, which produces diarrhetic shellfish poisoning toxins
(DSPs) or dinophysis toxins (DTXs), reached an abundance of 58,000 cells L 1 in July 2019.
Although there is not a Contingency Plan threshold for Dinophysis, this abundance is 580 times
higher than a trigger level specified by the Food Standards Agency in Scotland
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(https://www.gov.scot/publications/scotlands~marine~atlas~information~national~rnarine~
plan/pages/18/). which should make this high abundance noteworthy and a human and
environmental health concern.
Changes in individual species abundances may fail to illustrate broader changes affecting many
species, reflected as changes in community composition. MWRA used multi-dimensional scaling
(MDS)3 to depict temporal shifts in the phytoplankton community structure of Massachusetts
Bay from the late 1990s to through 2019 (Figure 3-4 in Libby et al. 2020). Others have used
MDS to characterize community changes across seasons or regions (Anderson et al. 2007).
MWRA's MDS analysis identified three major groups of years. One group includes many of the
most recent years, including 2013 and 2015-2019, while another encompasses 2000-2012 and
the third the late 1990s. Grouping of the most recent years into a single area of the MDS-space
is one line of evidence suggesting a broad community shift, although this interpretation is
muddied to some extent by the position of recent years on the MDS place between
observations from the 1990s and the 2000-2012 period. One potential limitation of MDS as a
tool for visualizing changes associated with HABs is that the ecological impact of HAB species
can be much larger than their abundances suggest. For example, the 2005 Alexandrium bloom
brought high toxin levels to southern New England and provoked a Federal disaster declaration
in Maine and Massachusetts (Anderson et al. 2005), but 2005 did not stand clearly apart from
other years in MWRA's MDS plot because even with peak Alexandrium abundances of 10,000 to
1,000,000 cells L 1 Alexandrium did not numerically dominate the phytoplankton community on
an annual scale in 2005 (Anderson et al. 2007). Experts recognize the challenge of quantifying
"minor presence" HABs, but analytical solutions are not recommended (Wells et al. 2020). The
impact of rare taxa is an active area of study in microbial ecology and might be a source of
relevant analytical methods.
The key conclusions of the MWRA water quality reports related to phytoplankton abundance
and composition are consistent with other studies in the region. For example, the reported
increase in A. catenella in Massachusetts Bay since 2005 (Fig 1) and the expanded cyst bed in
the Bay (Libby et al. 2021) are consistent with the reported gradual southward expansion and
increased abundance of A. catenella (Anderson et al. 2021). Increased abundance of
Alexandrium cysts, noted by MWRA after the 2019 bloom (Libby et al. 2021) was also noted as
one of several factors contributing to the 2005 bloom (Anderson et al. 2005), evidence that
internal feedbacks are established to sustain the abundance and extent of future Alexandrium
blooms. Fewer studies have examined the trends in the abundance of K. mikimotoi in the Gulf
of Maine and the factors that contributed to it. Although this likely reflects the very short
experience of K. mikimotoi in the region and the uncertain reasons around its arrival (Li et al.
3 MDS is a type of ordination. Ordination refers to a class of quantitative analytical methods used to represent
data from many variables, sites, or populations as points in a two- or three-dimensional coordinate frame. In
multi-dimensional scaling (MDS), distances between points in the 2- or 3-dimensional frame seek to accurately
represent distances between points in the n-dimensional frame defined by the data.
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2019, Record et al. 2021); the recent appearance of K. mikimotoi in Massachusetts Bay in 2017,
2019 and 2020 and documented in the MWRA water column reports is similar to its recent
appearance elsewhere in the Gulf of Maine (Record et al. 2021).
Another recent development related to HABs is the toxic diatom Pseudo-nitzschia australis,
which bloomed in the Gulf of Maine in 2016, resulting in unprecedented levels of domoic acid
(Clark et al. 2019). Although the 2016 bloom did not extend into Massachusetts Bay, domoic
acid, the toxin produced by P. australis and at least half of the 52 known Pseudo-nitzschia
species, has been an ongoing concern since a 1987 event on Prince Edward Island, CA in which
hundreds of people were sickened and three people died following a bloom of Nitzschia
pungens, which is now called P. multiseries (Clark et al. 2019). Pseudo-nitzschia has been
present sporadically throughout New England since the 1980s and MWRA monitors Pseudo-
nitzschia abundance and has a contingency plan threshold for abundance of Pseudo-nitzscia.
(Libby et al. 2020). There is not yet evidence that P. australis is expanding in abundance,
toxicity, or impact in Massachusetts Bay, drawing a contrast with Alexandrium and Karenia.
However, the unexpected arrival of P. australis and subsequent impact in 2016 illustrate the
potential for similar unpredictable changes in the future (Record et al. 2021).
4. Where toxin-producing algae are present in coastal ecosystems, toxins have
been transferred to fish, seabirds. and marine mammals, including North Atlantic
right whales, and in many cases caused harmful effects.
With respect to our charge to examine the potential effects of the MWRA discharge on North
Atlantic right whales, we propose that, if the discharge were to sustain or exacerbate a shift in
the phytoplankton community to more harmful or toxic algae, subsequent harmful effects on
whales could potentially occur via two pathways. One pathway involves disruption by HABs of
key trophic linkages, effectively reducing the food supply available to whales. Whales require
high densities of their preferred high-energy diet, principally the copepod Calanus finmarchicus,
and historical data link long-term changes in the calving rates of whales to variations in prey
availability (Meyer-Gutbrod et al. 2021).
The second pathway for harmful effects on whales involves transfer of algal toxins (Table 1) to
whales via the marine food web, thereby causing a harmful effect due to toxin exposure on a
short-term or cumulative basis. Of the two harmful algal species discussed in detail in the
MWRA reports (Alexandrium catenella and Karenia mikimotoi), Alexandrium produces saxitoxin
(STX), a paralytic shellfish toxin (PST). Outbreaks of PSTs have increasingly occurred in the
northeastern US over the past several decades (Anderson et al. 2021). Although the effect of
Karenia mikimotoi on communities can be severe (Li et al. 2019), the mechanisms responsible
for the toxic effects of Karenia mikimotoi are complex and may not provide for trophic transfer
to whales (Li et al. 2019). Domoic acid (DA), produced by various Pseudo-nitzschia spp. is the
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causative agent of amnesic shellfish poisoning in humans. DA toxicity occurs sporadically in
New England and has achieved locally high concentrations during outbreaks.
Algal toxins produced by HAB-forming species are readily transferred to and accumulated in
copepods, including Calanus finmarchicus, a relatively large zooplankter and preferred diet
component for North Atlantic right whales (Turner et al. 2000). Given that toxins are
transferred to and accumulated in a major diet component of whales, it is not surprising to find
toxins in whales and other marine mammals. A six-year study of North Atlantic right whales in
the western North Atlantic showed that 70% to 80% of whales were exposed annually to STX,
while 25-30% of whales were exposed to DA (Doucette et al. 2012). A study of the prevalence
of algal toxins in 905 marine mammals of 13 different species in Alaska showed that DA was
found in all 13 species and STX was found in 10 of 13 species. Of the species exposed to STX,
the highest prevalence was found in humpback whales (50%) and bowhead whales (32%;
Lefebvre et al. 2016). Seabirds have also been found to be exposed and potentially impacted by
both STX and DA (Van Hemert et al. 2020).
Although whales are exposed to STX and DA when it is present, the evidence relating exposure
to harmful effects is imprecise and often indirect. One line of evidence pointing to the
likelihood of harmful effects is that the mode of action of STX and DA at the cellular level apply
to many species, including fish, birds, and mammals. STX is a potent neurotoxin that interferes
with a variety of nervous system functions, leading to illness or death.4 DA causes excitotoxicity
and neurodegeneration5, resulting in potential for both acute and chronic effects (Doucette et
al. 2012). In humans, excitotoxicity has been implicated in several neurodegenerative diseases,
including amyotrophic lateral sclerosis (ALS), Alzheimer's disease, Parkinson's disease, and
epilepsy (Armada-Moreira et al. 2020). Marine mammal mortality events linked to STX and DA
exposure show that the magnitude of impact is potentially large. In its 1993 biological opinion
related to the MWRA diversion project, NOAA cited the 1987 deaths of 14 humpback whales
(Megaptera novaeangliae) that died in Cape Cod Bay after ingesting Atlantic mackerel (Scomber
scombrus) containing STX (Geraci et al. 1987, National Marine Fisheries Service 1993). Impacts
to marine mammals resulting from DA appear to be more common than impacts due to STX.
Goldstein et al. (2008) described two clinical syndromes in marine mammals associated with DA
exposure, an acute toxicosis often leading to death or stranding, and a second syndrome
related to chronic exposure in which animals developed seizures. Following a large Pseudo-
nitzschia bloom in 2015, large numbers of whales died due to DA exposure in the eastern
Pacific, including 343 sei whales in Chilean Patagonia (Geib 2017).
4 Saxitoxin (STX) functions at the cellular level by binding with high affinity to voltage-gated sodium channels.
Sodium channels are essential for transmitting electrical impulses in nerves, whether in the central nervous system
or the heart muscle and are present in a broad swath of animal life, including humans and whales.
5 Domoic acid (DA) is a glutamate agonist, meaning that DA activates or "agonizes" glutamate receptors), which
leads to the excitotoxic and neurodegenerative effects.
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Table 1. Algal toxins reported in Massachusetts Bay by Libby et al. (2020) and others reported
from the Gulf of Maine.
Toxin Type
Example toxin
HAB Taxa
Paralytic shellfish poisoning
toxins
Amnesic shellfish poisoning
toxin
Diarrhetic shellfish poisoning
toxins
Saxitoxin (STX)
Alexandrium catenella
Domoic acid (DA)
Pseudo-nitzschia spp
Okadaic acid (DA)
Dinophysis norvegica
Dinophysistoxin-1 (DTX1)
Dihyd rodinophysistoxin-1
Dinophysistoxin-2 (DTX2)
Pectenotoxin-2 (PTX2)
Although mentioned only in passing in the 2019 MWRA water column report, Dinophysis
norvegica was observed at very high abundance. Dinophysis can produce okadaic acid or
analogous toxins within the diarrhetic shellfish poisoning (DSP) toxin suite referenced
collectively as Dinophysis toxins or DTXs (Table 1). DTXs cause DSP in humans and more
generally cause harmful effects to the digestive system of exposed animals (i.e., alimentary
intoxication)6. Thus, DTXs present another potential toxic risk to North Atlantic right whales,
provided there is a path for trophic transfer to whales. Studies have identified trophic transfer
mainly to benthos while presenting more equivocal evidence regarding the effects and
bioaccumulation of DTXs in zooplankton (Alves et al. 2018), trophic transfer via zooplankton to
planktivorous fish (Corriere et al. 2021), or trophic transfer to cetaceans, including whales
(Danil et al. 2021). The effects of DTXs on cetaceans remain unknown (Danil et al. 2021).
A significant fraction of the data monitoring algal toxicity in coastal marine food webs is
associated with shellfish monitoring, generally to protect public health. In Massachusetts Bay,
the Massachusetts Division of Marine Fisheries monitors PSP toxicity in shellfish and closes
shellfishing as needed to protect public health. However, whales consume different food items
in different places, compared to shellfish. Thus, toxicity in shellfish may not transfer directly to
whales. For a variety of reasons, including spatial variability resulting from the potentially high
growth rate of Pseudo-nitzschia spp., localized monitoring of shellfish areas may not provide
good resolution of abundance in open water. Moreover, toxin production can vary in response
to a variety of triggers. DA production rates increased 4 to 7-fold in cultures grown at elevated
6 DTXs also inhibit protein phosphatases, leading to excessing protein phosphorylation and a variety of additional
toxic effects impacting DNA and cellular components, immune system and nervous system function, and
embryonic development (Valdiglesias, V., M. V. Prego-Faraldo, E. Pasaro, J. Mendez, and B. Laffon. 2013. Okadaic
acid: more than a diarrheic toxin. Mar Drugs 11:4328-49.)
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seawater CO2 or under silica limitation compared with silica-replete cultures (Tatters et al.
2012), a condition potentially exacerbated at least locally by low Si:N and Si:P of the Deer Island
discharge (Maguire et al. 2017).
In summary, toxin-producing algae have been identified in Massachusetts Bay and can produce
at least three toxins or classes of toxin, including domoic acid (DA), paralytic shellfish toxin
(PSTs) including saxitoxin (STX), and Dinophysis toxins (DTXs). North Atlantic right whales in
Massachusetts Bay are repeatedly exposed to DA and STX, although harmful effects of these
toxins have not been documented in Massachusetts Bay. Nevertheless, evidence from around
the world indicates that algal toxins can cause acute and chronic impacts on whales, including
the potential for large scale mortality events.
5. An increase in HAB species in Massachusetts Bay could lead to reduced
abundance of zooplankton. including Colon us finmarch icus. the preferred diet of
North Atlantic right whales, harming right whales by reducing their food supply.
In addition to effects of algal toxins transferred via the marine food web to North Atlantic right
whales, another possible pathway whereby HABs could have a harmful effect on whales is
disruption of the marine food web, resulting in reduced production of preferred prey items.
Two related lines of evidence suggest that this mechanism could be important. First, an analysis
of the biomechanics and bioenergetics of feeding by baleen whales, which includes North
Atlantic right whales, indicates that obtaining the energy needed for healthy growth and
reproduction depends critically on whales finding and feeding in waters with a high abundance
of energy-rich foods (Goldbogen et al. 2017). Based on the dependence on high food
abundance, one might expect that changes in abundance of this critical food would be
associated with changes in growth or reproduction of North Atlantic right whales. The second
line of evidence is that data from 2000-2010 and 2010-2019, which show that reduced
abundance of Calanus finmarchicus during 2010-2019 was associated with reduced numbers of
right whale calves and, at least in 2 years, an increase in numbers of right whale carcasses
(Meyer-Gutbrod et al. 2021). However, Meyer-Gutbrod et al. (2021) attribute the observed
changes in abundance of Calanus to climate change, especially a pattern of warming, rather
than HABs.
Although regional trends have been noted, the reviewed MWRA reports do not show declining
Calanus finmarchicus abundance in Massachusetts Bay, providing less systematic references to
changes in their abundance. For example, Libby et al. (2020) noted that "there were typically
low abundances of Calanus finmarchicus at all stations for most of the year except for March,"
and also "Calanus finmarchicus are often the most abundance zooplankton taxa during
summer." These general comments do not provide information about long term trends. Libby
et al. (2020; Fig. 3-5) does show a 25-year time series for total zooplankton abundance, but this
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includes all taxa. Moreover, the time series of total zooplankton did not show a long-term
decline, and instead showed a period of relatively high zooplankton abundance from 2016 to
2019.
A potential scenario for impacts to Calanus resulting from HABs involves Alexandrium catenella
acting as a stressor on C. finmarchicus, leading overtime to reduced production and
abundance. Experimental evidence shows that Calanus feeding on diets rich in A. catenella had
reduced egg production and egg viability (Roncalli et al. 2016), contributing to lower
reproductive output, an effect also seen for other copepods (Dutz 1998). Also, when Calanus
ingested toxic Alexandrium cells, adults produced enzymes to prevent assimilation of the toxin,
imposing an energetic cost or reallocation of energy, and implemented other adaptive
measures to reduce the effect of the toxin7 (Roncalli et al. 2017).
In summary, there is evidence that a mechanism exists to link a biological regime shift favoring
increased abundance of toxin producing HABs, including Alexandrium, to reduced production of
Calanus finmarchicus, and that such a shift could impact North Atlantic right whales. However,
evidence currently linking food web impacts to whales appears to focus on climate change as
the principal driver rather than HABs, and in any case is not linked to the Deer Island discharge.
Summary
We examined the data and analyses included in recent MWRA water column monitoring
reports to evaluate the potential for MWRA's Deer Island discharge to cause environmental
effects that could harm North Atlantic right whales (Eubalaena glacialis). MWRA's reports by
design provide information that is especially relevant to the potential impacts of the discharge.
We considered additional scientific literature that provides useful context and is especially
useful for understanding ecological risks that could be present, but not yet realized in
Massachusetts Bay.
The environmental effects of the discharge have been monitored and evaluated for nearly
three decades. The results show that wastewater diversion from Boston Harbor has had the
intended effect of greatly improving water quality within the harbor, while causing modest and
apparently localized water quality changes in Massachusetts Bay.
With the perspective of several decades of monitoring, careful attention to predict, monitor,
and understand potential effects of the discharge has been a hallmark of MWRA's planning and
operations. Notably, potential impacts to whales were considered prior to construction of the
Deer Island plant and outfall (National Marine Fisheries Service 1993), spurred in part by a
major whale morality event (Geraci et al. 1987). Three decades later, the North Atlantic right
7 Whereas STX targets voltage-gated sodium channels (Nav) causing paralysis, the copepod produces an alternative
variant of Nav that is resistant to the toxin (Roncalli, V., P. H. Lenz, M. C. Cieslak, and D. K. Hartline. 2017.
Complementary mechanisms for neurotoxin resistance in a copepod. Sci Rep 7:14201.)
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whale remains one of the most endangered large whale species in the world. Despite
international protection of the species more than 80 years ago, the population has not
recovered appreciably. Ongoing human-caused mortality is a major reason for lack of recovery
and has been attributed exclusively to injuries resulting from vessel strikes (42%) and
entanglement in fishing gear (58%; Sharp et al. 2019).
In this context, we considered if evidence points to current or future risks to whales associated
with the discharge. We conclude that this is not likely, but also cannot be excluded
categorically. A possible effects pathway is as described below, with associated statements of
confidence.
(1) Regional and climate related factors continue to create an environment favorable to
harmful algal blooms, reinforcing a biological regime shift that may already be underway. This
has been examined scientifically and is likely.
(2) The discharge provides a steady output of nutrients to a generally nutrient-limited coastal
environment. Although the discharge may not have caused significant effects to date, the HAB-
dominated regime responds to the discharge differently than in the past and the discharge
makes HABs worse. This is very uncertain. Absent this link, much of the potential pathways to
harmful effects on whales likely has little to do with the discharge.
(3) More extensive and intense HABs increase already-documented exposure of whales to
saxitoxin and domoic acid, causing chronic impacts on whales, or in a worst-case scenario,
causing a significant mortality event impacting North Atlantic right whales. This is documented
elsewhere in the world affecting other whale species and is not hypothetical, but significant
whale mortality events caused by HABs have not occurred recently in the northwest Atlantic.
(4) More extensive and intense HABs disrupt a marine food web already impacted by climate
change, reducing food availability to North Atlantic right whales, reducing their rate of
reproduction. Ongoing changes in the marine food web due to climate change is likely and
already documented, but exacerbation of effects due to HABs is based mainly on results of
laboratory experiments and the magnitude of present or future impacts is less certain.
As we will examine in a separate document, our major recommendation is that the emerging
scientific evidence suggests that a cautious approach regarding the potential impact of the
discharge is warranted. Caution may be demonstrated by focusing ambient monitoring on
current environmental risks to a greater extent. Appropriately targeted monitoring will provide
improved ability to understand prospective environmental risks and trends in Massachusetts
Bay.
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References
Alves, T. P., and L. L. Mafra, Jr. 2018. Diel Variations in Cell Abundance and Trophic Transfer of
Diarrheic Toxins during a Massive Dinophysis Bloom in Southern Brazil. Toxins (Basel)
10.
Anderson, D. M., P. S. Libby, M. J. Mickelson, D. G. Borkman, R. He, and D. J. McGillicuddy 2007.
The 2005 New England red tide of Alexandrium fundyense: observation, causes and
potential outfall linkages. Massachusetts Water Resources Agency Report 2007-10.
Pages 85 pp. + Appendices. Massachusetts Water Resources Agency, Boston.
Anderson, D. M., B. A. Keafer, D. J. McGillicuddy, M. J. Mickelson, K. E. Keay, P. Scott Libby, J. P.
Manning, C. A. Mayo, D. K. Whittaker, J. Michael Hickey, R. He, D. R. Lynch, and K. W.
Smith. 2005. Initial observations of the 2005 Alexandrium fundyense bloom in southern
New England: General patterns and mechanisms. Deep Sea Research Part II: Topical
Studies in Oceanography 52:2856-2876.
Anderson, D. M., E. Fensin, C. J. Gobler, A. E. Hoeglund, K. A. Hubbard, D. M. Kulis, J. H.
Landsberg, K. A. Lefebvre, P. Provoost, M. L. Richlen, J. L. Smith, A. R. Solow, and V. L.
Trainer. 2021. Marine harmful algal blooms (HABs) in the United States: History, current
status and future trends. Harmful Algae 102:101975.
Armada-Moreira, A., J. I. Gomes, C. C. Pina, O. K. Savchak, J. Goncalves-Ribeiro, N. Rei, S. Pinto,
T. P. Morais, R. S. Martins, F. F. Ribeiro, A. M. Sebastiao, V. Crunelli, and S. H. Vaz. 2020.
Going the Extra (Synaptic) Mile: Excitotoxicity as the Road Toward Neurodegenerative
Diseases. Front Cell Neurosci 14:90.
Bearsdley, R., E. E. Adams, D. Harleman, A. E. Giblin, J. R. Kelly, J. E. O'Reilly, and J. F. Paul 1995.
Report of the MWRA hydrodynamic and water-quality model evaluation group. MWRA
Environmental Quality Department Miscellaneous Report no. ms-37. Pages 58 pp.
Massachusetts Water Resources Authority, Boston, MA.
Biggs, R., S. R. Carpenter, and W. A. Brock. 2009. Turning back from the brink: detecting an
impending regime shift in time to avert it. Proc Natl Acad Sci U S A 106:826-31.
Clark, S., K. A. Hubbard, D. M. Anderson, D. J. McGillicuddy, Jr., D. K. Ralston, and D. W.
Townsend. 2019. Pseudo-nitzschia bloom dynamics in the Gulf of Maine: 2012-2016.
Harmful Algae 88:101656.
Corriere, M., L. Solino, and P. R. Costa. 2021. Effects of the Marine Biotoxins Okadaic Acid and
Dinophysistoxins on Fish. Journal of Marine Science and Engineering 9:293.
Danil, K., M. Berman, E. Frame, A. Preti, S. E. Fire, T. Leighfield, J. Carretta, M. L. Carter, and K.
Lefebvre. 2021. Marine algal toxins and their vectors in southern California cetaceans.
Harmful Algae 103:102000.
16
-------
Delta res 2022. Simulations of 2017 hydrodynamics and water quality in the Massachusetts Bay
system using the Bays Eutrophication Model. Report 2021-12. Pages 107pp.
Massachusetts Water Resources Authority, Boston, MA.
Doucette, G. J., C. M. Mikulski, K. L. King, P. B. Roth, Z. Wang, L. F. Leandro, S. L. DeGrasse, K. D.
White, D. De Biase, R. M. Gillett, and R. M. Rolland. 2012. Endangered North Atlantic
right whales (Eubalaena glacialis) experience repeated, concurrent exposure to multiple
environmental neurotoxins produced by marine algae. Environ Res 112:67-76.
Dutz, J. 1998. Repression of fecundity in the neritic copepod Acartia clausi exposed to the toxic
dinoflagellate Alexandrium lusitanicum: relationship between feeding and egg
production. Marine Ecology Progress Series 175:97-107.
EPA 2000a. Authorization to discharge under the National Pollution Discharge Elimination
System (August 10, 2000). US Environmental Protection Agency, Boston, MA. 33 pp.
https://www3.epa.gov/regionl/npdes/mwra/pdf/mwrafpml.pdf
EPA 2000b. Ambient Aquatic Life Water Quality Criteria for Dissolved Oxygen (Saltwater): Cape
Cod to Cape Hatteras. Pages 1-133. US Environmental Protection Agency, Washington,
DC.
Fraser, D. 2020. 'The Blob': Low-oxygen water killing lobsters, fish in Cape Cod Bay. Cape Cod
Times. Hyannis, MA.
Geib, C. 2017. Death by killer algae. Hakai Magazine. Victoria, CA.
Geraci, J. R., D. M. Anderson, R. J. Timperi, D. J. St. Aubin, G. A. Early, J. H. Prescott, and C. A.
Mayo. 1987. Humpback whales (Megaptera novaeangliae) fatally poisoned by
dinoflagellate toxin). Can J Fish Aquat Sci 46:1895-1898.
Goldbogen, J. A., D. E. Cade, J. Calambokidis, A. S. Friedlaender, J. Potvin, P. S. Segre, and A. J.
Werth. 2017. How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration.
Ann Rev Mar Sci 9:367-386.
Goldstein, T., J. A. Mazet, T. S. Zabka, G. Langlois, K. M. Colegrove, M. Silver, S. Bargu, F. Van
Dolah, T. Leighfield, P. A. Conrad, J. Barakos, D. C. Williams, S. Dennison, M. Haulena,
and F. M. Gulland. 2008. Novel symptomatology and changing epidemiology of domoic
acid toxicosis in California sea lions (Zalophus californianus): an increasing risk to marine
mammal health. Proc Biol Sci 275:267-76.
Grieve, B.D., Hare, J.A. & Saba, V.S. Projecting the effects of climate change on Calanus
finmarchicus distribution within the U.S. Northeast Continental Shelf. Sci Rep 7, 6264
(2017).
Hallegraeff, G. M., D. M. Anderson, C. Belin, M.-Y. D. Bottein, E. Bresnan, M. Chinain, H.
Enevoldsen, M. Iwataki, B. Karlson, C. H. McKenzie, I. Sunesen, G. C. Pitcher, P. Provoost,
A. Richardson, L. Schweibold, P. A. Tester, V. L. Trainer, A. T. Yniguez, and A. Zingone.
2021. Perceived global increase in algal blooms is attributable to intensified monitoring
and emerging bloom impacts. Communications Earth & Environment 2.
17
-------
Hunt, C. D., D. G. Borkman, P. S. Libby, R. Lacouture, J. T. Turner, and M. J. Mickelson. 2010.
Phytoplankton Patterns in Massachusetts Bay-1992-2007. Estuaries and Coasts 33:448-
470.
Kessouri, F., J. C. McWilliams, D. Bianchi, M. Sutula, L. Renault, C. Deutsch, R. A. Feely, K.
McLaughlin, M. Ho, E. M. Howard, N. Bednarsek, P. Damien, J. Molemaker, and S. B.
Weisberg. 2021. Coastal eutrophication drives acidification, oxygen loss, and ecosystem
change in a major oceanic upwelling system. Proc Natl Acad Sci U S A 118.
Lefebvre, K. A., L. Quakenbush, E. Frame, K. B. Huntington, G. Sheffield, R. Stimmelmayr, A.
Bryan, P. Kendrick, H. Ziel, T. Goldstein, J. A. Snyder, T. Gelatt, F. Gulland, B. Dickerson,
and V. Gill. 2016. Prevalence of algal toxins in Alaskan marine mammals foraging in a
changing arctic and subarctic environment. Harmful Algae 55:13-24.
Li, X., T. Yan, R. Yu, and M. Zhou. 2019. A review of karenia mikimotoi: Bloom events,
physiology, toxicity and toxic mechanism. Harmful Algae 90:101702.
Libby, P. S., D. G. Borkman, W. R. Geyer, J. T. Turner, A. S. Costa, J. Wang, and D. Codiga 2019.
2018 Water column monitoring results. Pages 52 pp. Massachusetts Water Resources
Authority, Boston, MA.
Libby, P. S., D. G. Borkman, W. R. Geyer, J. T. Turner, A. S. Costa, J. Wang, D. Codiga, and D.
Taylor 2017. 2016 Water column monitoring results. Pages 56 pp. Massachusetts Water
Resources Authority, Boston, MA.
Libby, P. S., D. G. Borkman, W. R. Geyer, J. T. Turner, A. S. Costa, J. Wang, D. Codiga, and D.
Taylor 2018. 2017 Water column monitoring results. Pages 59. Massachusetts Water
Resources Authority, Boston, MA.
Libby, P. S., D. G. Borkman, W. R. Geyer, J. T. Turner, A. S. Costa, D. I. Taylor, J. Wang, and D.
Codiga 2020. 2019 Water column monitoring results. Pages 60 pp. Massachusetts Water
Resources Agency, Boston.
Libby, P. S., D. G. Borkman, W. R. Geyer, J. T. Turner, A. S. Costa, D. I. Taylor, J. Wang, and D.
Codiga 2021. 2020 Water column monitoring results. Massachusetts Water Resources
Authority, Boston.
Maguire, T. J., and R. W. Fulweiler. 2017. Fate and Effect of Dissolved Silicon within Wastewater
Treatment Effluent. Environ Sci Technol 51:7403-7411.
Mayer, A. L., and M. A. X. Rietkerk. 2004. The Dynamic Regime Concept for Ecosystem
Management and Restoration. Bioscience 54:1013.
McCabe, R. M., B. M. Hickey, R. M. Kudela, K. A. Lefebvre, N. G. Adams, B. D. Bill, F. M. Gulland,
R. E. Thomson, W. P. Cochlan, and V. L. Trainer. 2016. An unprecedented coastwide
toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett 43:10366-
10376.
Meyer-Gutbrod, E. L., C. H. Greene, K. T. A. Davies, and D. G. Johns. 2021. Ocean Regime Shift Is
Driving Collapse of the North Atlantic Right Whale Population. Oceanography 34:22-31.
18
-------
MWRA 1991. Massachusetts Water Resources Authority effluent outfall monitoring plan phase
I: baseline studies. Report 1991-ms-2. Pages 95 pp. Massachusetts Water Resources
Authority, Boston, MA.
MWRA. 1997. Massachusetts Water Resources Authority effluent outfall monitoring plan:
Phase II post discharge monitoring. MWRA Environmental Quality Department
Miscillaneous. Report. No. ms-044. Massachusetts Water Resources Authority, Boston,
MA. 61 pp. https://www3.epa.gOv/regionl/npdes/mwra/pdf/n.pdf
MWRA. 2001. Massachusetts Water Resources Authority Contingency Plan Revision 1.
Massachusetts Water Resources Authority, Boston, MA. Report ENQUAD ms-071. 47 pp.
https://www.mwra.com/harbor/enquad/pdf/2001-ms-71.pdf
MWRA 2021. Ambient monitoring plan for the Massachusetts Water Resources Authority
effluent outfall revision 2.1. August 2021. Report 2021-08. Pages 107 pp.
Massachusetts Water Resources Authority, Boston, MA.
National Marine Fisheries Service 1993. Endangered Species Act - Section 7 Consultation,
Bioloical Opinion on the Boston Harbor Project: Issuance of a National Pollutant
Discharge Elimination System (NPDES) Permit for the Massachusetts Water Resources
Authority (MWRA) Outfall. Pages 88 pp. in N. M. F. S. Northest Region Office, September
8, 1993 (editor).
Oviatt, C. 2007. Production patterns in Massachusetts Bay with outfall relocation. Estuaries and
Coasts 30:45-46.
Pershing, A. J., M. A. Alexander, D. C. Brady, D. Brickman, E. N. Curchitser, A. W. Diamond, L.
McClenachan, K. E. Mills, O. C. Nichols, D. E. Pendleton, N. R. Record, J. D. Scott, M. D.
Staudinger, and Y. Wang. 2021. Climate impacts on the Gulf of Maine ecosystem.
Elementa: Science of the Anthropocene 9.
Record, N. R., P. D. Countway, K. Kanwit, and J. A. Fernandez-Robledo. 2021. Rise of the rare
biosphere. Elementa: Science of the Anthropocene 9.
Roncalli, V., P. H. Lenz, M. C. Cieslak, and D. K. Hartline. 2017. Complementary mechanisms for
neurotoxin resistance in a copepod. Sci Rep 7:14201.
Roncalli, V., J. T. Turner, D. Kulis, D. M. Anderson, and P. H. Lenz. 2016. The effect of the toxic
dinoflagellate Alexandrium fundyense on the fitness of the calanoid copepod Calanus
finmarchicus. Harmful Algae 51:56-66.
Sharp, S. M., W. A. McLellan, D. S. Rotstein, A. M. Costidis, S. G. Barco, K. Durham, T. D.
Pitchford, K. A. Jackson, P. Y. Daoust, T. Wimmer, E. L. Couture, L. Bourque, T. Frasier, B.
Frasier, D. Fauquier, T. K. Rowles, P. K. Hamilton, H. Pettis, and M. J. Moore. 2019. Gross
and histopathologic diagnoses from North Atlantic right whale Eubalaena glacialis
mortalities between 2003 and 2018. Dis Aquat Organ 135:1-31.
Tatters, A. O., F. X. Fu, and D. A. Hutchins. 2012. High C02 and silicate limitation synergistically
increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS One 7:e32116.
19
-------
Taylor, D. I., C. A. Oviatt, A. E. Giblin, J. Tucker, R. J. Diaz, and K. Keay. 2020. Wastewater input
reductions reverse historic hypereutrophication of Boston Harbor, USA. Ambio 49:187-
196.
Turner, J. T., G. J. Doucette, C. L. Powell, D. M. Kulis, B. A. Keafer, and D. M. Anderson. 2000.
Accumulation of red tide toxins in larger size fractions of zooplankton assemblages from
Massachusetts Bay, USA. Marine Ecology Progress Series 203:95-107.
Valdiglesias, V., M. V. Prego-Faraldo, E. Pasaro, J. Mendez, and B. Laffon. 2013. Okadaic acid:
more than a diarrheic toxin. Mar Drugs 11:4328-49.
Van Hemert, C., S. K. Schoen, R. W. Litaker, M. M. Smith, M. L. Arimitsu, J. F. Piatt, W. C.
Holland, D. Ransom Hardison, and J. M. Pearce. 2020. Algal toxins in Alaskan seabirds:
Evaluating the role of saxitoxin and domoic acid in a large-scale die-off of Common
Murres. Harmful Algae 92:101730.
Wells, M. L., B. Karlson, A. Wulff, R. Kudela, C. Trick, V. Asnaghi, E. Berdalet, W. Cochlan, K.
Davidson, M. De Rijcke, S. Dutkiewicz, G. Hallegraeff, K. J. Flynn, C. Legrand, H. Paerl, J.
Silke, S. Suikkanen, P. Thompson, and V. L. Trainer. 2020. Future HAB science: Directions
and challenges in a changing climate. Harmful Algae 91:101632.
20
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