,
This paper not to be cited without prior reference to the author
International Council for
the Explorationof the Sea
CIl i 971 /E:27
Fisheries Improvement Committee
Ref.:K (Shell. & Benth. Cttee)
L (Plankton cttee)
.... ...
Results of the 1971 monitoring programme for munsel
on the north-east coast of Britain
by
P. A. Ayres
Fisheries LaboratorY1 Burnham-on-CrouCh. Essex
INTRODUCTION
Follouing an outbreak of paralytic shellfish poisoning associated
with musseIs from the north-east coast of Britain in the summer .of 1968
•
(McCollumet .§l. 1968, ~lood emd Hason 1968, \food 1968) an ·annual monitorins programme 1~as' cstablished~ 11ith special emphasis on the area' cf
the 1968 outbreak. Results of this prog~amDe in 1969 and 1970 (Wood
1969, Wood and Ayres 1970) suGgested that development of toxi~ity in the
... - -.
north-east might be an,annual .feature, only occasionally leading to clinical manifestations. Investigations in 1970 confirmed earlier suggestions
that major concentrations of dinoflagellatcs were confined to offshore
regions and that littoral molluscs were probably influenced cnly by the
marein of this offshore population. Tho prosence of low conccntrations
:
of dinoflagellates, particularly Gonyaulax tamarensis, suggestcd that
toxicity of littoral molluscs rcsultod from movement of, offshore 1vater
towards the coast. Because of the inherent difficulties in corre.1ating
toxicity of l~ttoral mussels with phytoplankton observations in t~e near
and offshore wators, the pattern of samplinG for thecurre~t year has
been modified fromthat used proviously. AS.in. previousyears.
. .-. samplcs
of littoral musseIs have been cxamincd at;intervals for toxicity, but, to
establish the presence of phytoplankton ~rganisms,w~tcr sampIes were
abandoned in favour of direct examination o~ museel gutcontents in an
attempt to find a more direct correlationbetwecntoxicity.
and phytoplank...
.
to~.c~ntent.of theshellfish.
This report summarizes the results of this
programme
and attcmpts a preliminary. evaluation of . the data collected.
\
The':coopcration of the North-:-.Eastern Sen FiGherics Committee,: the Uinistry's
Dist~ict Inspectors and others, in the.collcction.of material, is gratefully
aclmouledgod.
.'
•
'
\
,:."
. '
"
,
".
MErHODS
(.i)
Determination of toxici ty of shellfish
Arrangements were made, carly in the ycar~ for provision of sampIes
at app~oximatcly we~kiy' intervals from stations along 240 km of thc northeast coast, an area stretching from Benrick in the north to Bridlington in
the south. Since examination ofthc gut contents was to be a significant
part of thc investigation the praetico of samplihgtissues, removed from
thc shell at sourco, was discontinucd, and sampIes of 12-18 musscls in the
shell, packcd in watertight containers und sent for analysis, were taken
instcad. In this
at the laboratory
injection of acid
(MeFarren, 1959).
way samplos were usually received in a frcsh condition
the following day. Toxin was assayed by intra-peritoneal
extracts into femala mice - 18 to 20 g body weight
The concantration of toxin was expressed as mouse units/
100 g of tissuc, 400 m.u/100 g baint; regarded as .thc maxim~ ~,afe concentration. 'Sampling commenced in U3.rch und continued until the end of
August, ponding any reappearance of toxi~ity.
•
(ii)
Examination of gut contents
Six muss eIs were takcn at random from each samplc und opcned cürefully
witha scalpel. The bind gut and stomach were dissected out separatelyand
the contents expressed into a clean petri dish. The'gut centcnts of six
musseIs nore poolod together and miXed \iithO.04 m1 of soa ..rater, previously
filtcred" th~ough a 0.4iJ.m filter, and 2 dr~ps of this oixture from a caIi";
brated Pasteur pipette .(tota~ volume'o-D.04 'ml) were removed on to a slide
for subscquent microscopicai examination. Using a Zeiss photomicroscope,
a prelimimry examination under the x40 objective 1-ras made to identify
thc'dominant genera ofphytoplankton prescnt in thc sampIes. Uherc'possibla,identification bf dinoflagellates 'las continued to specieslevel.
Once:thc genera and species had been cstablished the sampIe 'las scanned
under the'x10 objective for 5 minutes, and counts wera made of the organisms preseht. This did not yield a strictiy'quantitativo assessment ef
thenumbero andtypes prescnt~ but thc examinations were made'by one per'sorikder'stitndard conditions and so enabledcoinparative assessments of'
types and ab~d.ance to be made bct\feen Olle s~pie and another.' Although
the' 'extent of 10ss of the more fragile' ferms is difficult to a8sess; thc
variety of intact und idcntifiablc cells foundin the' gut analysis sug'gests tha't this i~ an effective techniquo far further investigations.·
2
•
RESULTS
Ci)
Toxicityofmussels
Atthe time of writing (middle of August) a total of 81 sampIes of
muss eIs from thc north-east coast bave been examined and the results of
thc bioassay are summarized in Table 1.
Sampling at Holy Island, the locus
of the 1968 outbrcik, cornmenced in March but toxicity was not
det~~~ed
until·tmmrds the end of Hay, whon·a samplo containod 226 units/100 g.
A similar 'level of toxicity was detected nt this time in a sampIe of mus. sels from Borvlick, 25 km north of Holy Island.· A ueok later, toxicity at
Holy Islanq had.~eclincd to 197 units/100.g and a n~f locus appeared at
vlhitby, 150'km to thc south.
The toxin lovel in Uhitby musseIs then
reached 488 units and up to thc present time this has not been excceded
•
at any sampling station; however, within two ueeks toxin had declined to
an undetectable level.
Thc absence of toxicity in sampIes between Holy
Island and lVhitby, i.here the wo loci appcnred, is a phenomcnon not
observed in the sampling of previous years. Apart from these four sampIes, no further toxicity ,;ras detected until nid-July ';lhen
an2t~e:r:l<?c~
appeared at Hartlepool, 45 km north of Whitby. A töxici~. of .454~its/
'100g had fallen to 415 units by the end of July, but no furthe:r:.q.Q.mples
have been examined from .this. station.
DurL'"lg the current ycar's experi-
ments, close' observation of mice after injoction revenled thet mild
.. paralytic responses (excitability, muscle tvti tches, gaping reflex), which
although not fatal were indicative of sub-lethal toxin concentrations, .
gavo advanced ,mrning of increasing toxicity.
•
that this type of
It can be seen fromTable.1
respo!).seo~gurred,.1"!ithsanpIes
from a nunber of stations
at the same time, particularly from tho Holy Island area. This suSgosts
that smnll numbcrs of toxic organisns were widoly dis tribut cd along the
north-east coast during April und Bay, reaching conccntrations causing
measurable toxicity towards the end of May.
(ii) . Examination of gut contents
The rcsults of tho
phytoplankto~ exaninntion
are presented in Table 2,
and levels of toxin observcd in the muss cIs cxamincd are included for comparison with the organisns present. No obvious correlation between
toxicity und any one species or genera of dinoflagellate or diatom is
evident, but a nunber of interesting points have emerged.
It is likely
thnt the majority
of Gonyaulax recorded
as Gonyaulax .np. were in fact
.
,
Q. tamnrensis, but these have only been recorded as such when a positive
identification was possible.
If one assumes that the organism occurx±Dg
----------------,
in thc grentest nunber is thc most signifieant, the importnnee of
Q..
Em2!'2F~
invostigation.
obnorvcd in past years is not upparent inthe eurrent
The appcarnnee of toxicity at Holy Inland was marlccdby
thc prescnee of incrensing nunbers of unidentified dinoflagcllate cysts,
whieh deelincd as toxin levels beerunc undeteetablc.
However, sinee
Gonyaulax sp. also appcared atthis time it is possible that the eysts
obser~ed
were of this genun.
It is perhaps sienificnnt that eysts were
present with a grenter frequeney nt all stations thnn any other organiso
obscrved~
though the nunber rceordcd nt Holy Island whon tox~city appcared
has not been exceedcd elsowherc.
Howevor, at BCTIviek Gonyaulax sp. were
dominant when a toxin level of 216 .units/100
e was reeorded, nnd this
level ,mn similarly not oxccoded elsm'lhere.
The toxiei ty of musseIs . at
iihitby (the highest level rceordcd this yoar) eould not be reInted to
phytoplankton abundnnee, uhieh was particularly 101'T in snmples from'
this station.
At the remaining station yiolding toxie sampIes, Hnrtlepool,
•
sampIes showed some eorrclntion between toxin and hieh numbers of
Prorocentrum micans, 12 dnyo prior to
th~
dcteetion of toxin.
Two weeks
later E. mieans hnd virtually disnppenred und toxicity had also deelined.
The Exuviaella sp. observed periodically, partieularly in the Holy IslandBudle Bny area, vTere identificd as Exuviaella balticu, but were replaeed at
the beginninG of August by!. marina, "hen a count of 132 units (the highest
count of any single speeicn or genera recordcd to date) was made in a sampIe from IIoly Island. It is perhaps typic2l.1 of the observations made this
year that by the following lTeck this species had been replaced by niLlilur
numbcrs of another dinoflagellate, Dinophysis acuta.
DISCUSSIon
With the appearance of toxieity at the €nd of May, thin year's
observations promised to be similar to those made
ar~ually
DinGe 1968.
However, toxieity did not inerease, although three separate loci in turn
appcared und declined to undetectable levels.
In 1969-1970 -tox-ici ty
developed in April-Nny, rcaehing a I::12Ximum in nid-June and declining during July. Thin yc~r none factor or combination of factorn prevented the
inereane in. toxieity seen in previoun ycars. Instead, three distinct
areaS of toxicity appoarcd (two in late May at Be~fiek/Holy Island und
Whitby, and one in mid-July at Hartlcpool), but at no time did levels of
toxin rcnch tho3e~observed·prcviously. No single species of dinofl~gollate
domi,nated the plankton, but sporadie outbursts of vuriouz specics oecurred
4
•
und supported thc vicw that a considerable deviation from previous years
(i.c. 1968-1970) had occurred.
Climntically the month of June, when peak
toxi~ity
"lUS
'\-lUG
oxpocted to 'oceur,
noted an being -exccptionally wet nnd
cold, und tho daily noteorologieal records from Tyncmouth (midway boh,een
Holy Island ['..nd 1Jhitby) confirm this.
Tnble 3 sUI:lLl3I'izes the Junc nir
tempornture, sunshine nnd rninfnll dnta for the years 1967-71 inclusive.
".
.
.
,.
'
'..
0
Tho menn maximum air tcmperature for June 1971 "las 2.7 C below the menn
average for this station, und tho lowest naximum nnd mili.Ji:rum'~i;emp~raturos
ovor the period 1967-1971 for the month of Junonlso occurred'm 1971.
Sunshinc in June was only 78 per cent of the nverage for that nonth since
records were started in 1937, nnd
~ounted
to 56 hours less for the month
th2ll the prcvious lowest value for June during the period 1967-1971.
•
Rain
fell on more dnys than in nny June GinGe 1967, and the total was 136 per
cent of tho average for June observations nt thin station (sinco records
startod in 1864). Thereforo it would appear that June 1971 wns abnormal
in having 101, air temperD.tures, lo~, sunshine nnd high rninfall - conditions
which could nccount in part for the suddBn disappearancc of toxicity at a
time when it was cxpectcd to be increasing rapidly. Tho scattered outbursts
of dinoflagellates which occurred, and thc rclBtive abundance of cyst forms,
",ould support thc appnrent disruption of an established developmcnt sequence
of phytoplankton off the north-east coast.
No unusual biological 8vents associated vri th toxic phytoplankton l'Tere
rcported in the area, apart frou two reports of discoloured uater.
The
first, off Scahounes nnd BCetdnell, coincidcd ,dth the first toxie sanpIe
from Holy IslOlld, but no nntorinl could bCi obtained for examination.
•
A
second bloon, reported fron the Holy Island c.roa nt thc boginning cf June,
revealcd Oll nlmost pure culture of n pink pigmcnted copepod.
Thc maximum
levels of toxicity rcachcd during 1971 (454-488 units) Hore nueh louer
than those obscrved in 1970 (2100-4100 units) nnd 1969 (3800-6000 units)
and baroly significOllt compared with the 1968 valucs (20.000-27.000
units).
No toxieity ",,'as observed at Blyth, '\Ihore peak vnlues had been
obtnined in pravious ycetrs, but this is biascd by the absence of mnny sanpIes fron this station.
Fron tho data presented here it seems likely that tho clina.tic conditions are thc
n~in
factor influencing the developncnt of toxicity.
Thera
would appear to be a nced to extend these obserlntions und to relnte then
to optioal conditions for grcw-th of potcntinlly toxic phytoplankton, as
dotcrnincd fro~ ficld and/or laboratory cxpcrinents.
5
REFERENCIS
MeCOLLm~,
J. P. K., PEARSOH, R. C. H., INGHAH, H. R., \lOOD, P. C. and
DtWAR, H. A., 1968.
An
Lfu~C1T,
east Englnnd.
MeFARREN, E. F., 1959.
epide~ic
Oet. 5, pp 767-770.
Report on coilaborative studios of thebioassay
for paralytic shellfish poison.
pp
of fiussel poisoning in north-
J. Ass. of agric. ehern.. ~ 42,
263-271.
WOOD, P. C., 1968.
Dinoflngellate crop in the North Sea.
lntroduetion.
Nature, Lond., 220, p 21.
WOOD, P. C. and
t~SON,
J., 1968.
Paralytic shellfish poisoning; n short
account of an outbrenk oceurring on the north-east eoast of Britain
in tIay 1968.
\lOOD,
P.
c.,
1969.
leES CH 1968/K: 16 (mimeo).
!'lussel toxicity in Great Britain, 1969.
lCES CfJI 1969/
K:25 (mimeo) •
. WOOD, P. C. and AYRES, P. A., 1970. MusseI toxieity and dinoflagellate
distribution off north-east Britain in 1970. lCES m 1970/K:12
(rümeo) •
6
•
Table 1
Levels of toxin in IDussels, March to August 1971 (mouse units/100 g of tissue)
station*
Week ending
19
26
2
9
16
23
30
+
Holy lsland
BeI..Ück
+
Budle Bay
+
+
+
7
14
21
28
-
+
266
216
197
-
+
4
Aug
Jul
Jun
May
Apr
Mar
11
18
25
2
9
16
23
30
+
6
13
-
+
Blyth
Sunderland
+
454
Hartlepool
Redcar
Whitby
488
+
Lost
Bridlington
- negative sampIe; + non-fatal positive response
*For details of position, see earlier reports to lCES Shellfish and Benthos Committee
(Wood and Mason 1968, Wood 1969, Wood and Ayres 1970)
415
+
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I Navicula Spo
I Chaetoceroa Spo
I Skeletonema. Spo
00
.,I
I\)
I Nitzsc·hia Sp.
I Rhizoaolenia Spo
I
.....
-'"
\J1
I Pleuroaigma. Sp•
.....
.....
.....
~
I Gonyaulax apo
00\0
t:1
lj.
o
tamarensis ~
o
Peridinium spo
~
(l)
I Gonyaulax
\0
f\.)
o
§
...,
'-" 0
(1)
o
~
'<
(I)
\l)
.....
...,.
...,.
~~
s:: m
g'
g
o
~-J
o CD
~
g
c+
(1)
m
b
o
........ tJj
B:.....
~'
::r'
~
[
CD
tJj
.....
~
o
g
N
t1l
e
-'"
-J
-'"
I
I
\
I
I
I P. depressum
~
Po trochoideum
Po granii
I
Gymnodinium (large)
-'"
Gymnodinium (small)
Polykrikos schwarzii
CD
-'"
Dinophysis acuta
N
\J1
~v1
I\)
f\.)
00'1
-J.;..
-'"
-J
Exuviaella ap.
I Unidentified
o
00
Prorocentrum micans
I\)
~
\J11
I Gonyaulax sp.
Gymnodinium lunula
.....
.;..
~
~
-J
.~~
N
~
I
Q
~
c+
tIl
Peridinium depressum
Other sppo
.....
Favella spo
I 0
c+
I5
p-
o
I\)
:E;
:E;
~
(1)
~
~
(1)
~
(1)
~..:
t:1
~~
m
a
...,.
g-
~~
CD
~
(1)
I
m
~
e
Radiolaria
\J1 .....
0'1 N
e
I\)
.....
0'1
a
•s::
•
c+
o
I Minute flagella tee
~
~
~
(1)
t-3
o
M
...,o
.....
c+
'1
M
t;;.
J
,
Table 3
Weather records fram Tynemouth for Jlli~e 1967 to 1971
Air temperature
Mean maximum (Oe)
Difference from average
Hean minimum (0 e)
Difference from average
Highest maximUIJ. (Oe)
Date
Lowest minimum (Oe)
Date
1967
1968
1969
1970
1971
15.3
-0.4
9.7
-0.4
19.8
19
6.9
23
15.7
15.1
-0.6
9.5
-0.6
21. 9
12
13.0
4.5
15.5
-0.2
10.4
+0.3
23.4
20
7.0
6
5
1
2
o
7
13.0
23
186
102
15.8
13
225
124
14.9
12
3
13.8
1
1
233
128
198
109
142
78
21
14
24
43
95
19
18
22
52
21
27
23
57
127
22
10
23
24
53
15
14
19
61
136
0.0
10. 1
0.0
25.5
30
7.5
24
-2.7
8.8
-1.3
20.2
24-25
5.5
9
Sunshme-*
Days of no sunshine
MaximUIJ. daily duration (hours)
Date
Total for month (hours)
the average
%of
14.9
Rainfallt
Days of no rainfall
Maximun fall in 24 hours (rum)
Date
Total for I:lonth
%of the average
116
*Pirst year of records 1937; the highest nUI:l.ber of hours'sunshine
for the month was 265, in 1949, and the lowest 104, in 1954.
tPirst year of records 1864; the highest rainfall for themonth was
115 um, in 1966 and the lowest 2 mn, in 1865.