The ecology of the mussel Mytilus edulis chilensis from three sites in the Falkland Islands Andrea

311 Pages·2017·20.87 MB·English

Mytilus
The the edulis chilensis
ecology of mussel
in the Falkland Islands
from three
sites
by
Andrea Patricia Gray
(BSc. University Wales, Bangor)
of
A thesis presented in partial fulfilment of the requirements of the University of
Wales for the degree Doctor in Philosophy
of
University Wales, Bangor
of
School Ocean Sciences
of
Menai Bridge
Gwynedd LL59 5EY
United Kingdom'
February 1997
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Summary
An Mytilus from three in
ecological study of populations of edulis chilensis study sites
the Falkland Islands.
Mytilus is dioecious incidence hermaphroditism
edulis chilensis with no recorded of
females. Reproductive
and with approximately equal numbers of males and
development is initiated during (August September)
spring whilst a single major
-
during the (December March). The timing
spawning period occurs southern summer
-
broadly
of peak reproductive condition coincides with mean maximum summer
temperatures (12 14°C). Whilst M. (190 2000
settlement of e. chilensis spat pm)
- -
filamentous low levels throughout the
onto artificial substrate units occurs at year with
during the low (> 2 into
a single peak austral summer, relatively numbers mm) settle
the in fashion, bearing little to the
established populations a sporadic often relation
timing the Reproductive the three
of reproductive cycle. output of study populations
2,
between 0.439 109 Camilla Creek, 1.771 10
ranged x eggs. M-2, at and x eggs. m at
Darwin.
The deposition bands to be the the
of microgrowth appears under control of spring
-
lunar The individual
neap cycle. age and growth rate of mussels as well as the age
the determined from
composition of study populations were winter growth checks
identified the layer. Size increase
within prismatic shell and growth rate with
decreasing tidal longevity tidal level.
elevation, whilst exhibits no such relationship with
L_ k between 36.3 91.4 0.198 0.702,
and values range and mm and and respectively.
The from Darwin Goose Green
populations and consisted mainly of older mussels (3
-
8 those from Camilla Creek (1
years old), whilst were generally younger years old).
-2
Allometric growth of M. e. chilensis appears to be controlled principally by age and food
supply.
A hitherto undescribed association between the isopod, Edotia
valviferan
doellojuradoi, M. is The
and e. chilensis reported. relationship between a green alga,
Coccomyxa (Chlorococcales, Coccomyxaceae)
parasitica its host M.
and e. chilensis
is documented.
also
Acknowledgements
Firstly, I like to thank Ray Seed Chris Richardson, for their
would my supervisors, and
throughout the this funded
support and encouragement course of project which was
by the Commonwealth Association the Falkland Island Government. Special
and
thanks to Conor Nolan for
go assistance with routine monthly sample collections at
times it for to be in the Islands. Also thanks to those
when was not possible me who
to times Conor
risked gale and snow conditions collect samples at when was also
Carole Bedford, Gus Melanie Clausen.
unavailable, and
Thanks to Tony McMullen Landholdings Goose Green (Falkland Islands) for
and at
lab facilities, to John Lee for the
providing make-shift ensuring water supply was
sufficient; Patrick Minto for sorting the electricity every time I blew the fuse; Owen Lee,
Chris Taylor, Jason Alazia Clint Short for to keep during
and conversation me awake
those long dissection Thanks to Brook Eileen Hardcastle, Sally
evenings. also and and
Albert McLeod, Bobby Lindsay Short Sophia Clausen for
and and accommodation
during field to Bill Ginge Kidd for
my many visits; also and many thawing cups of
days the Low Pass;
coffee after sampling at and anyone else who lent a helpful hand
during field in the Falklands.
my visits
I would like to thank the Department of Agriculture (Falkland Islands), Diane
especially
and Gordon for use of their laboratory facilities. Thanks to British Antarctic Survey
also
for transporting frozen samples back to UK. Terry Betts, funds for
who provided
temperature loggers, thank
you.
At the School Ocean Sciences life
of have been
would not the
same without several
familiar faces, Sarah, Jon, Alex, John, Richard, Craig, Steve, Sharon, Karen
and
Miguel all of whom helped to keep the high jokes flowing,
moral and
particularly at
coffee time! Special thanks to Graham Walker, Ian Lucas Jon Russell, both for
and
histology
and electron microscopy tips
as well as encouragement. Also thank to
you
the technicians, in Berwyn
particular Gwyn.
and
Finally
I
and most of all, must thank Mum, Dad, Johan and Gus for their love
and
throughout
support the
course of my studies in the UK.
iv
Contents
ii
Summary
iii
Declaration
iv
Acknowledgements
Page Contents v
of
List Plates viii
of
A
List Tables
of
List Figures xiv
of
1
Chapter 1. General Introduction
Chapter 2. Site description, environmental characteristics and
general methods
10
2.1 Site descriptions
10
2.1.1 Darwin
13
2.1.2 Camilla Creek
13
2.1.3 Goose Green
2.2 Mussel density dispersion indices 13
and
population
2.3 Meteorological data 18
25
2.4 Tidal
pattern and aerial exposure
2.5 Salinity, food 27
currents and supply
2.6 Statistical 31
methods
Chapter 3. Reproduction,
condition and settlement
3.1 Introduction 32
3.2 Materials 35
and methods
3.2.1 Gonad index fraction 35
condition, gonad and gamete volume
3.2.1.1 Sample
treatment 35
collection and
3.2.1.2 Assessment
36
of gonad condition
3.2.1.3 Sex
40
ratios
3.2.1.4 Gonad index
40
3.2.1.5 Gamete fraction
volume 40
3.2.2 Assessment
of condition index tissue 41
and weight
3.2.2.1
Sample
collection and treatment 41
3.2.2.2
Analysis data
of 41
3.2.3 Settlement
42
V
42
3.2.3.1 Artificial (ASU)
substrate units
43
3.2.3.2 Length frequency distributions
43
3.2.4 Fecundity and reproductive output
45
3.3 Results
45
3.3.1 Gonad maturation, sex ratios and mussel size
46
in
3.3.2 Seasonal changes reproductive condition
57
3.3.3 Condition indices and dry tissue weight
86
3.3.4 Settlement
93
3.3.5 Fecundity and reproductive output
97
3.4 Discussion
3.4.1 Conclusions
Chapter 4. Growth
absolute and allometric
-
109
4.1 Introduction
114
4.2 Materials
and methods
114
4.2.1 Absolute
growth
4.2.1.1 Shell internal 114
growth surface rings and growth patterns
-
114
4.2.1.1.1 Sample
collection, marking experiments and shell sections
4.2.1.1.2 Estimation from 116
of growth shell sections
4.2.1.2 Length frequency 117
analysis
4.2.2 Allometric 117
growth
4.3 Results 119
4.3.1 Absolute 119
growth
4.3.1.1 Shell internal 119
growth surface rings and growth patterns
-
4.3.1.1.1 Description interpretation band 119
and of microgrowth
patterns
4.3.1.1.2 Seasonal longevity 125
growth and
4.3.1.2 Length frequency distributions 139
4.3.2 Allometric
146
growth
4.4 Discussion
153
4.4.1 Conclusions
166
Chapter 5. Ecological between
the isopod
relationships
valviferan
Edotia doellojuradol Giambiagi, 1925, its host
and
Mytilus
edulis chilensis
5.1 Introduction
168
5.2 Materials
and methods 168
5.2.1
Sample
collection and treatment 168
vi
169
Isopod
5.2.2 examination
171
Effect host
5.2.3
on
171
Results
5.3
171
Edotia doellojuradoi
5.3.1 Occurrence and abundance of
176
5.3.2 Size distribution Edotia doellojuradoi
and of
181
5.3.3 Effect host
on
181
5.4 Discussion
185
5.4.1 Conclusions
(Chlorococcales,
Chapter 6. Coccomyxa
parasitica
its Mytilus
Coccomyxaceae)
and relationship with
edulis chilensis
188
6.1 Introduction
189
6.2 Materials
and methods
189
6.2.1 Sample treatment
collection and
6.2.2 Preparation infected tissue 190
and observations of mussel
190
6.2.3 Effect host
on
190
6.3 Results
190
6.3.1 Description the Coccomyxa
of alga parasitica
6.3.2 Occurrence Coccomyxa 191
and abundance of parasitica
6.3.3 Effect host 198
on
6.4 Discussion 198
6.4.1 Conclusions 201
Chapter 7. General discussion 202
7.1 Further 210
work
References 212
Appendices 233
vii
List Plates
of
2.1 Darwin; A. Photograph the beach taken from the bridge; B.
of at mid-low water,
Schematic diagram the Scale bar 30
of study site. = m
2.2 Camilla Creek; A. Photograph the B. Schematic diagram
of gravel spit at mid water;
the Scale bar 25
of study site. = m
2.3 Goose Green; A. Photograph the beach low B. Schematic diagram the
of at water; of
Scale bar 30
study site. = m
3.1 Photomicrographs Myfilus
of sectioned male gonads of edulis chilensis at various
development, 250. A Developing 1, islands tissue the
stages of x male stage of germinal within
tissue filled B. Developing 2, larger follicles
connective with spermatogonia. stage slightly
C. Developing 3, few darkly
containing spermatocytes and spermatids. stage a stained nuclei
between the larger D. Ripe 5, follicles
of spermatozoa are scattered cells. stage packed with
in lamellae, few
spermatozoa arranged a residual spermatocytes and spermatids are present
the E. Spawning 4, has taken
around periphery. stage partial release of gametes place,
lamella F. Spawning 1, follicles
although remaining gametes retain arrangement. stage are
virtually empty, and considerably reduced in size. G. Resting or spent stage 0, no follicles are
the tissue. H. Redeveloping 2, layer
present within connective stage a of undifferentiated early
line the follicle.
stage spermatogonia empty
3.2 Photomicrographs
female Mytilus
of sectioned gonads of edulis chilensis at various
stages of development, x 250. A. Developing stage 1, islands of germinal tissue with a few
small oogonia basally attached to the follicle wall. B. Developing stage 3, larger oocytes still
basally attached to the germinal epithelium. C. Ripe stage 5, little or no connective tissue
visible, oocytes at maximum size and compressed into polyhedral shape due to increased
pressure within follicles. D. Spawning stage 4, the release of some gametes has reduced the
the follicles
pressure within and remaining oocytes have become spherical in shape. E.
Spawning 2, few large
stage a oocytes remain and some cytolysis is taking place. F. Spawning
1, follicles have
stage
collapsed and only residual ova remain, considerable cytolysis can be
G. Redeveloping
observed. 1, layer
stage a of undifferentiated line the
early stage oogonia
empty follicles. H. A ripe gonad which has partially spawned as a result of chemical stimulation,
100.
x
4.1 A. Schematic
illustration
of a shell section of Mytilus edulis chilensis; B.
Photomicrograph illustrating
the
position of a winter growth check within the prismatic shell layer
of a mussel from the low shore population at Darwin; C. Photomicrograph illustrating the
disturbance
position of a the
check within prismatic shell layer of a mussel from the low shore
population at Darwin; D. Photomicrograph illustrating
the lines
presence of growth within the
umbone region of a mussel from the low shore at Goose Green; E. Photomicrograph illustrating
the lines
presence of annual within the nacreous shell layer of a mussel from the low
shore at
Goose Green;
p, periostracum, u, umbone; pr, prismatic denote
shell; n, nacreous shell; arrows
growth checks and lines. Scale bar = 500 pm (B, C); 100 (D, E).
pm
4.2 A. Photomicrograph
illustrating
the
band
microgrowth the
pattern within prismatic shell
viii
layer Mytilus file-marked for 24 hours (large
of a edulis chilensis, which was and emersed
0.82 datum Camilla Creek for 56 days. P,
periostracum,
arrow) and grown at m above chart at
PL, layer, S, N, the large indicates the 24 hour
prismatic spring period; neap period; arrow
emersion band, whereas the smaller arrows indicate the position of this band within the shell
the indicates band deposited at low tide during a
section; medium-sized arrow a prominent
high temperature, highlight this band within the
period of anomalously air whilst small arrows
in A
Scale bar 100 B. Schematic diagram the
shell section. = pm. of photomicrograph above
to highlight the 24 hour emersion band, the proximity of the growth banding during spring and
tides the defined band deposited during high
neap and clearly emersion when an anomalously
line
air temperature occurred. C. Predicted tidal cycle during the experimental period; solid
the the d. D. Continuous
marks position of mid shore experimental cage, c. =+0.82 m.
temperature logged by TinyTalk temperature logger (Orion Ltd).
seawater and air records
Astern highlights the anomalously high temperature (20 th January 1996) which occurred when
the for hours during low On the
mussel was emersed several a spring water. other occasions
there temperatures.
mussels were not emersed when were unusually elevated air
4.3 Photographs the Mytlus A.
of shell surface of edulis chilensis; with clear surface
checks, from the low shore population at Goose Green; B. with severe abrasion, from the mid
shore population at Goose Green; C. with blisters on the shell surface due to the infestation by
boring Scale bar 10
shell algae. = mm.
4.4 Photographs the Mytilus A. intact
of shell surface of edulis chilensis; with an
but from the low Darwin; B.
periostracum, no clear surface checks, shore population at with a
poor record of surface checks in a relatively old, slow growing individual from the high shore
Goose Green. Scale bar 10
population at = mm.
4.5 A. Photograph
the high Mytilus from Darwin,
of shell surface of a shore edulis chilensis
for in
which was grown one year a subtidal cage suspended from the bridge at Darwin. The
arrow denotes the time of marking and transplantation. Scale bar = 10 mm. B. Growth of the
natural population of mussels from the high shore at Darwin (closed circles), together with the
(± I length
mean standard error) of mussels subsequently transplanted to subtidal cages at
Darwin (open circles), FIPASS in Stanley (open triangles) the Vicar Brae' Goose
and of at
Green (open
squares).
5.1 Edofia doellojuradoi, dorsal view (A, B, C) (D, E, F) female
and a ventral view of male,
juvenile isopods,
and respectively; P position of penis, 0 indicates one of three pairs of
marsupial oostigites on the second fourth thoracic Scale bar
segments.
- =1 mm
5.2 Edotia tuberculata, dorsal (A, B, C)
view and a ventral view (D, E, F) of male, female
juvenile isopods,
P
and respectively; position of penis, 0 indicates three
one of pairs of
marsupial oostigites on the second fourth thoracic Scale bar
segments.
- =2 mm
6.1 A. A
photomicrograph of a section of My61us edulis chilensis mantle tissue showing the
Coccomyxa
presence of a'colony' of parasitica within the connective tissue. Scale bar 100
=
pm. B. and C. Transmission electron microscope images C.
of parasitica cells within
M.
e. chilensis connective tissue. c, chloroplast;
m, mitochondrial
profiles; s, starch grain; v,
dense
electron vesicle; rer, rough endoplasmic reticulum; n, nucleus. Scale bar = 500 nm.
ix
6.2 A. Transmission
images dividing Coccomyxa
electron microscope of a parasitica cell.
The large double highlight the the large indicates
arrows animal cell membrane; single arrow
the algal cell parental membrane; small double arrows show the algal daughter cell
membrane. B. and C. low power transmission electron microscope images of mussel tissue
leukocytes
with containing algal cells. mv, multi-vesiculate body; ml, multi-lamellar body; I,
leukocyte. Scale bar 500
= nm.
X
List Tables
of
2.1 Density, biomass and indices of dispersion for Mytilus edulis chilensis at three study
in the Falkland Islands
sites
2.2 Aerial exposure (%) and estimated height above chart datum (c. d. ) for high, mid and
low the beds the three in the Falkland Islands.
regions of mussel at study sites
2.3 An day the total
eight average of suspended solids and chlorophyll a concentrations
in from Darwin bridge the Vicar Brae' in January 1995.
and of
water samples collected
3.1 Distribution of gonad stages in monthly samples of Mytilus edulis chilensis from
Darwin.
3.2 Distribution in Mytilus from
of gonad stages monthly samples of edulis chilensis
Camilla Creek.
3.3 Distribution in Mytilus from Goose
of gonad stages monthly samples of edulis chilensis
Green.
3.4 Correlation from Spearman Rank Order index
coefficients correlation analysis of gonad
(G. I. ), fraction (GVF), index (C. I. ), dry tissue temperature
gamete volume condition weight and
(T'C) A. Darwin, B. Camilla Creek, C. Goose Green.
at and
3.5 Seasonal in index length, log transformed dry tissue
variation condition with and weights
with length, for monthly samples of Mytilus edulis chilensis from Darwin. Log transformed
regression constants are derived from the equation y= ax' where y is dry tissue weight as the
dependent is length the independent
variable and x shell as variable.
3.6 Seasonal variation in condition index with length, and log transformed dry tissue weights
length, for Mytilus
with monthly samples of edulis chilensis from Camilla Creek. Log
transformed regression constants are derived from the is dry tissue
equation y= ax° where y
weight as the dependent variable and x is shell length as the independent variable.
3.7 Seasonal variation in condition index with length, log transformed dry tissue
and weights
length, for Mytilus
with monthly samples of edulis chilensis from Goose Green. Log
transformed regression constants are derived from the is dry tissue
equation y= ax' where y
weight as the dependent variable and x is shell length as the independent
variable.
3.8 A. ANOVA table for the linear
general between
model with size as a single covariate
index
23
condition and size on selected monthly samples of Mytilus edulis chilensis from
Camilla Creek. B. The departure
of single regression slopes from the
average slope as
determined by the linear
general model presented in Table 3.8A.
3.9 A. ANOVA table for the linear
general between
model with size as a single covariate
dry tissue
weight and size on 28 selected monthly Mytilus from
samples of edulis chilensis
Darwin. B. The departure
of single regression slopes from the determined by
average slope as
XI