Are toxins from harmful algae a factor involved in the decline of harbour seal populations in Scotland?
Abstract
Firstly this study builds on the investigation initiated by Hall and Frame (2010),
which found that Scottish harbour seals were exposed to domoic acid (DA), a
potent natural neurotoxin produced by phytoplankton. Using the same sample
collection technique to gather urine and faecal material from various
populations around Scotland with differing population trajectories (Lonergan et
al., 2007), the objective was to investigate not only exposure to DA, but also
other groups of toxins such as paralytic shellfish poisoning (PSP) toxins and
the lipophilic toxins okadaic acid (OA) and dinophysis toxins (DTXs). Toxins
from harmful algae are thought to be potential causative factors in the ongoing harbour seal decline in some regions of Scotland (Hall and Frame,
2010).
This investigation was initiated because Pseudo-nitzschia (which produces
DA) in particular was found to be highly prevalent in the phytoplankton
communities in Scotland (Fehling et al., 2004; Stobo et al., 2008) and indeed
was first observed at increased concentrations at around the time the harbour
seal populations were observed as declining (Lonergan et al., 2007; Stobo et
al., 2008). Prior to 2000 harbour seal populations in Scotland were largely
stable or increasing. In addition DA exposure has had a devastating effect on
the California sea lions (CSL) from the US west coast, where morbidity and
mass mortality has occurred as a result of exposure (Goldstein et al., 2008;
Gulland et al., 2002; Lefebvre et al., 1999; Scholin et al., 2000). In addition to
the toxin analysis in urine and faecal samples, blood samples were collected
and health parameters such as white blood cell and differential cell counts
were investigated. Plasma cortisol concentrations and parasite faecal egg
counts were additionally investigated as parameters indicative of adrenal
function and parasite burden. CSL exposed to DA have significantly lower
blood cortisol levels and higher eosinophil counts (Gulland et al., 2012) so it
was possible that these indicators of effects might also be seen in the harbour
seals. High parasite loads are often associated with high eosinophil levels
(Klion and Nutman, 2004) so these data were needed to ensure any positive relationships found were linked to DA and were not a consequence of parasite
burdens.
The work presented in this thesis highlights the effect of exposure to the
neurotoxin DA and documents that Scottish harbour seals are exposed to
multiple toxins such as PSP toxins, OA and DTX-2 (Chapter 2, Chapter 4).
Immunomodulatory effects of DA exposure such as lymphocytopenia and
monocytosis are also reported. In general, harbour seals from the east coast
and Northern Isles, where the decline in abundance has been greatest, had
higher levels of DA in their excreta than animals from the west coast. The
concentrations in the faeces and urine samples were generally low but time
since exposure was unknown. Uptake of DA, PSP toxins, OA and DTXs in
randomly selected fish from the east coast of Scotland in the Firth of Forth
was investigated (Chapter 3), where benthic, flat and pelagic fish are shown
to be vectors of toxin transfer and emphasis is drawn to flatfish as they seem
to accumulate higher levels of toxins than the other species analysed. This
indicates that harbour seals foraging off the east coast are likely to regularly
encounter toxic prey that could impair their health.
In addition to live captured harbour seals, samples from dead stranded marine
mammals (including cetaceans and in particular harbour porpoise) found a
range of species in Scottish waters were exposed to both DA and PSP toxins
(Chapter 4). A monitoring tool to rapidly determine chronic DA exposure in
blood samples was published recently for DA exposed CSLs and in Chapter 5
this monitoring technique was attempted in phocid seals, and where it failed to
be replicated or validated which questions its function as a DA monitoring tool.
Questions regarding how quickly a marine mammal excretes DA from the
body have been discussed in the literature and in Chapter 6 an experiment
was set up to measure the clearance of DA by using a biomarker (Iohexol).
Iohexol was successfully measured in plasma samples from captive harbour
seals following oral intake, where concentration and time of the iohexol peak
was identified together with the calculation of its half-life. These results
indicate the approximate elimination rate of DA (and potentially other
hydrophilic toxins) and can be used to better interpret urine levels of DA measured in wild caught harbour seals. Collectively the results of this
research will enable the risk posed by the ingestion of various toxins present
in the Scottish marine food chain to marine mammals (particularly harbour
seals but also harbour porpoise and grey seals) to be assessed.
Type
Thesis, PhD Doctor of Philosophy
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