Timothy Alexander Rawlings, 1989 .... b) P r e d a t o r - e x c l u s i o n e x p e r i m e n t s. 85 ...... F=0.57, p>0.25), Seppings and Ross Islets snails laid capsules.
FUNCTIONAL MORPHOLOGY OF EGG CAPSULES IN A MARINE
GASTROPOD
NUCELLA EMARGINATA
By Timothy B.Sc. ( H o n s . ) /
Alexander
Rawlings
U n i v e r s i t y o f B r i t i s h Columbia,
THESIS SUBMITTED I N PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (ZOOLOGY)
We a c c e p t t h i s a s c o n f o r m i n g to the required
standard
THE UNIVERSITY OF B R I T I S H COLUMBIA August Timothy
1989
A l e x a n d e r R a w l i n g s , 1989
1986
In
presenting
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at
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or
this thesis
for
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Z o o l
The University of British C o l u m b i a Vancouver, Canada
DE-6 (2/88)
I further
purposes
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permission.
Department of
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of
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It
is
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Library shall make
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granted
be
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by
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understood
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allowed
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it
extensive of
my
copying
or
my written
ii ABSTRACT
Egg
c a p s u l e s o f t h e marine whelk N u c e l l a emarqinata
were
examined w i t h r e s p e c t t o i n t r a s p e c i f i c v a r i a t i o n i n c a p s u l e morphology and r e s i s t a n c e t o i n t e r t i d a l Capsules separated weight,
predators.
were c o l l e c t e d from t h r e e i n t e r t i d a l
along a wave-exposure g r a d i e n t .
and p r o t e c t i v e q u a l i t y o f c a p s u l e s
populations
Wall thickness, dry differed
e x t e n s i v e l y among t h e s e p o p u l a t i o n s ; h o w e v e r , t h e s e
capsular
p r o p e r t i e s d i d not r e f l e c t d i f f e r e n c e s i n wave-exposure levels.
Capsule
s i z e was f o u n d
to wave-sheltered s i z e among
shores
and p a r a l l e l e d d i f f e r e n c e s i n s n a i l
sites.
Laboratory
experiments,
p r e d a t o r - e x c l u s i o n cages,
and f i e l d t e s t s i n c o r p o r a t i n g
were u s e d t o d e t e r m i n e
p r e d a t i o n on N u c e l l a e m a r q i n a t a capsule predators. i n t e r t i d a l predators and
t o i n c r e a s e from wave-exposed
isopods,
Capsule such
a t two s t u d y
c a p s u l e s and t o i d e n t i f y
c a s e s were r e g u l a r l y e a t e n by
as shore
Idotea wosnesenskii.
r e s p o n s i b l e f o r opening sites.
the extent of
c r a b s , Hemiqrapsus spp., These i n v e r t e b r a t e s were
a maximum o f 3 2 % o f c a p s u l e s
D e s p i t e d i f f e r e n c e s i n t h i c k n e s s and
s t r e n g t h o f c a p s u l e s among p o p u l a t i o n s , no c a p s u l e s completely
present
r e s i s t a n t t o t h e s e p r e d a t o r s ; however,
were
thick
c a p s u l e w a l l s d i d a p p e a r t o c o n v e y some p r o t e c t i v e a d v a n t a g e . Preliminary laboratory tests indicated that thin-walled c a p s u l e s were p r e f e r e n t i a l l y
opened by I d o t e a
wosnesenskii.
iii TABLE OF CONTENTS Page ABSTRACT
i
TABLE OF CONTENTS
i
L I S T OF TABLES
i
i
i
v i i
L I S T OF FIGURES
viii
ACKNOWLEDGEMENTS
x
GENERAL INTRODUCTION
1
CHAPTER 1. I N T R A S P E C I F I C VARIATION I N CAPSULE MORPHOLOGY INTRODUCTION
3
STUDY S I T E DESCRIPTIONS
7
MATERIALS AND METHODS
12
I. Differences II.
i n s n a i l m o r p h o l o g y among s i t e s . . .
Capsule morphology
12 12
1. R e l a t i o n s h i p b e t w e e n s n a i l capsule s i z e
s i z e and
12
2. M i c r o m o r p h o l o g y o f L . e m a r g i n a t a egg 3.
capsules
15
I n t r a c a p s u l a r v a r i a t i o n i n w a l l t h i c k n e s s 15
4. V a r i a t i o n i n c a p s u l e among p o p u l a t i o n s 5. V a r i a t i o n i n c a p s u l e
wall
thickness
wall
thickness
16
w i t h i n a n d among c l u t c h e s
17
6. V a r i a t i o n i n d r y w e i g h t o f c a p s u l e s
17
I I I . V A R I A T I O N I N CAPSULE CONTENTS AMONG S I T E S . . . 18 1. E g g number a n d v o l u m e 2. Number a n d s i z e o f h a t c h i n g IV.
CAPSULE STRENGTH 1. R e s i s t a n c e
t o puncturing
18 snails
19 19 . 19
iv Page 20
2. R e s i s t a n c e t o s q u e e z i n g RESULTS
22
I . D i f f e r e n c e s i n s n a i l m o r p h o l o g y among s i t e s . . .
22
II.
22
Capsule morphology 1. R e l a t i o n s h i p b e t w e e n s n a i l capsule size
size
and
22
2. M i c r o m o r p h o l o g y o f tL_ e m a r q i n a t a egg c a p s u l e s
27
3.
27
Intracapsular variation i n wall thickness
4. V a r i a t i o n i n c a p s u l e w a l l among p o p u l a t i o n s
thickness 30
5. V a r i a t i o n i n c a p s u l e w a l l t h i c k n e s s w i t h i n and among c l u t c h e s l a i d by different snails
33
6. V a r i a t i o n i n d r y w e i g h t o f c a p s u l e s
35
I I I . VARIATION IN CAPSULE CONTENTS AMONG S I T E S . . . 1. Egg
number and v o l u m e
2. Number and
s i z e of hatching s n a i l s
I V . CAPSULE STRENGTH
37 37 39 41
1. R e s i s t a n c e t o p u n c t u r i n g
41
2. R e s i s t a n c e t o s q u e e z i n g
41
DISCUSSION Advantages of t h i c k ,
43 strong capsule w a l l s
43
Intraspecific differences i n capsular structure..
44
E f f e c t s of environmental
47
Tradeoffs i n capsule
structure
E f f e c t s of environmental REFERENCES
s t r e s s e s on e m b r y o s
s t r e s s e s on a d u l t s n a i l s
48 49 51
V Page CHAPTER 2. LABORATORY AND F I E L D TESTS OF PREDATION INTRODUCTION
.
MATERIALS AND METHODS
55 58
I . LABORATORY EXPERIMENTS....
58
II.
59
III.
IV.
F I E L D CENSUSES OF PREDATION 1. G r a p p l e r I n l e t
59
2. R o s s I s l e t s
60
3. S e p p i n g s I s l a n d
61
F I E L D EXPERIMENTS
61
1. G r a p p l e r I n l e t
63
2. R o s s I s l e t s . . . . .
64
S U S C E P T I B I L I T Y OF CAPSULES TO PREDATORS
RESULTS
65 67
I . LABORATORY EXPERIMENTS .
67
II.
73
III.
F I E L D CENSUSES OF PREDATION 1. G r a p p l e r I n l e t
73
2. R o s s I s l e t s
78
3. S e p p i n g s I s l a n d
79
F I E L D PREDATION EXPERIMENTS
80
1. G r a p p l e r I n l e t
80
a) P i l o t e x p e r i m e n t s
IV.
80
• b) P r e d a t o r - e x c l u s i o n e x p e r i m e n t s
82
2. R o s s I s l e t s
82
a) P i l o t E x p e r i m e n t s
82
b) P r e d a t o r - e x c l u s i o n e x p e r i m e n t s
85
S U S C E P T I B I L I T Y OF CAPSULES TO PREDATORS
87
vi Page DISCUSSION
89
Resistance of intact capsules t o predators
89
Digestibility
91
and p a l a t a b i l i t y
P r e d a t i o n on e g g c a p s u l e s Susceptibility
of thick-
capsules t o predators REFERENCES GENERAL CONCLUSIONS
of capsule w a l l s . .
i n the f i e l d
92
and t h i n - w a l l e d 94 97 100
vii LIST OF TABLES Page CHAPTER 2 I. II.
III. IV.
Summary o f t h e s p e c i e s t e s t e d f o r p r e d a t o r y a c t i v i t y on N u c e l l a e m a r g i n a t a e g g c a p s u l e s i n t h e l a b o r a t o r y . .
68
D e n s i t y o f N u c e l l a emarginata, t h e i r egg c a p s u l e s , and c a p s u l e p r e d a t o r s a t s t u d y s i t e s i n G r a p p l e r I n l e t and Ross I s l e t s
74
Summary o f e g g c a p s u l e s c e n s u s e d a t G r a p p l e r and Ross I s l e t s t u d y s i t e s
76
Inlet
Summary o f N u c e l l a e m a r g i n a t a e g g c a p s u l e s o p e n e d b y predators i n p i l o t experiments a t Grappler I n l e t , J u n e 1988
81
viii LIST OF FIGURES Page
CHAPTER 1 1.
2. 3. 4. 5.
6.
L o c a t i o n of study s i t e s along the southern s h o r e s o f B a r k l e y Sound on t h e w e s t c o a s t o f V a n c o u v e r I s l a n d , B.C
8
N u c e l l a e m a r g i n a t a egg c a p s u l e , i l l u s t r a t i n g t h e t h r e e measurements t a k e n f o r each c a p s u l e
14
T e c h n i q u e s u s e d t o compare t h e s t r e n g t h o f egg c a p s u l e s
21
Size-frequency histograms from each study s i t e
23
o f 50 s n a i l s
collected
R e l a t i o n s h i p between c a p s u l e body l e n g t h and l e n g t h f o r l a b o r a t o r y l a i d capsules f o r each study s i t e
snail 24
R e l a t i o n s h i p between c a p s u l e - c h a m b e r volume and snail
length for laboratory populations
7.
M i c r o s t r u c t u r e of N u c e l l a emarginata
8.
V a r i a t i o n i n w a l l t h i c k n e s s a l o n g t h e c a p s u l e chamber of f i e l d - c o l l e c t e d N u c e l l a emarginata capsules V a r i a t i o n i n w a l l t h i c k n e s s and c a p s u l e w i d t h w i t h i n one N u c e l l a e m a r g i n a t a c a p s u l e f r o m G r a p p l e r I n l e t . . . .
31
V a r i a t i o n i n c a p s u l e w a l l t h i c k n e s s w i t h c a p s u l e body l e n g t h f o r 30 N u c e l l a e m a r g i n a t a c a p s u l e s f r o m e a c h laboratory population
32
11.
V a r i a t i o n i n w a l l t h i c k n e s s w i t h i n and between c l u t c h e s of N u c e l l a emarginata capsules
34
12.
D r y w e i g h t o f empty c a p s u l a r c a s e s as a f u n c t i o n o f c a p s u l e b o d y l e n g t h f o r e a c h l a b o r a t o r y p o p u l a t i o n . . . . 36
13.
R e l a t i o n s h i p b e t w e e n t h e number o f e g g s p e r c a p s u l e . . . 38 and t h e v o l u m e o f t h e c a p s u l e - c h a m b e r f o r S e p p i n g s , Ross I s l e t s , and G r a p p l e r c a p s u l e s .
14.
Mean h a t c h i n g s i z e o f embryos a s a f u n c t i o n o f t h e number o f e m b r y o s c o n t a i n e d w i t h i n e a c h c a p s u l e f o r Seppings, Ross I s l e t s and G r a p p l e r p o p u l a t i o n s
9. 10
egg c a p s u l e s
26 28 29
40
ix
Page CHAPTER 2 1.
P r e d a t o r e x c l u s i o n c a g e s , i l u s t r a t i n g : a) t h e c a g e b a s e a n d d e t a c h a b l e f r a m e , a n d b) t h e f i v e c a g e t y p e s used t o exclude v a r i o u s s i z e - c l a s s e s of predators
62
Mean number o f N u c e l l a e m a r g i n a t a e g g c a p s u l e s r e m a i n i n g i n t a c t a f t e r 5 days exposure t o : a) i s o p o d s , I d o t e a w o s n e s e n s k i i (n = 11) a n d b) t h r e e s i z e - c l a s s e s o f H e m i g r a p s u s n u d u s
69
C h a r a c t e r i s t i c s o f s p e c i e s - s p e c i f i c p r e d a t i o n on N u c e l l a emarginata capsules by: Idotea wosenesenskii H e m i g r a p s u s s p p . , M o p a l i a s p p . , a n d an unknown predator
71
4.
R e s u l t s of the p r e d a t o r - e x c l u s i o n experiments G r a p p l e r I n l e t , J u l y 1988
in
83
5.
R e s u l t s of t h e p r e d a t o r - e x c l u s i o n experiments I s l e t s , S e p t e m b e r 1988
i n Ross
2.
3.
6.
Mean number o f t h e f i r s t f i v e c a p s u l e s o p e n e d b y I d o t e a w o s n e s e n s k i i when g i v e n a c h o i c e o f f e e d i n g on c a p s u l e s f r o m t w o d i f f e r e n t s t u d y s i t e s .
86
88
X ACKNOWLEDGEMENTS
First,
I w o u l d l i k e t o t h a n k my s u p e r v i s o r D r . Thomas
C a r e f o o t f o r h i s a d v i c e and h e l p d u r i n g t h e c o u r s e o f t h i s study.
I w o u l d a l s o l i k e t o t h a n k my c o m m i t t e e
Dr. Jamie Smith and Dr. John G o s l i n e , this project. the
Much c r e d i t
fortheir
input
many h o u r s s h e s p e n t s h o w i n g me how t o d e v e l o p
Lois Hollett
mention
into
i s due a l s o t o G l e n y s G i b s o n f o r
and a l s o f o r h e r m o r a l s u p p o r t d u r i n g t h i s up.
members,
photographs
long-winded
write-
and E l i z a b e t h Carefoot deserve a s p e c i a l
f o r t h e i r help i n producing the figures.
I am a l s o
i n d e b t e d t o D r . J o h n S t e e v e s f o r a l l o w i n g me t o u s e h i s m i c r o s c o p e a n d c a m e r a s y s t e m t o p h o t o g r a p h my c a p s u l e w a l l sections.
Finally,
I would l i k e t o acknowledge
the director
a n d s t a f f o f B a m f i e l d M a r i n e S t a t i o n who made my s t a y a n extremely e n j o y a b l e and rewarding e x p e r i e n c e .
1 GENERAL INTRODUCTION
Marine gastropods e x h i b i t a v a r i e t y o f r e p r o d u c t i v e and developmental patterns in the reproductive
(Webber, 1 9 7 7 ) .
ecology
evolution of internal
o f these
fertilization
Neogastropoda
( G a l l a r d o and Perron,
fertilization
has allowed
reproductive patterns stage,
An i m p o r t a n t
advance
organisms has been t h e i n t h e Meso- a n d 1982).
Internal
f o r t h e d e v e l o p m e n t o f new
associated with a non-pelagic
larval
such as t h e d e p o s i t i o n o f eggs i n t o p r o t e c t i v e
g e l a t i n o u s envelopes o r i n t o e l a b o r a t e egg c a p s u l e s . meso- a n d n e o g a s t r o p o d s e m b r y o s a r e c o n f i n e d w i t h i n egg
capsules
period.
f o r some, i f n o t a l l , o f t h e i r
The a d a p t i v e
I n many benthic
developmental
s i g n i f i c a n c e o f such s t r u c t u r e s i s
g e n e r a l l y t h o u g h t t o be a s s o c i a t e d w i t h a r e d u c t i o n i n t h e development t i m e o f embryos w i t h i n t h e p l a n k t o n and, consequently, (Pechenik, The
a n i n c r e a s e i n t h e s u r v i v o r s h i p o f embryos
1979) .
c o n f i n e m e n t o f embryos w i t h i n b e n t h i c egg c a p s u l e s ,
h o w e v e r , h a s i t s own r i s k s .
Embryos f r e e o f m o r t a l i t y
a s s o c i a t e d w i t h a p l a n k t o n i c e x i s t e n c e a r e exposed t o a v a r i e t y o f new e n v i r o n m e n t a l marine environment. these
Little
stresses within the benthic i s known a b o u t t h e i m p o r t a n c e o f
s t r e s s e s on t h e s u r v i v o r s h i p o f e n c a p s u l a t e d
embryos.
R e c e n t s t u d i e s , h o w e v e r , h a v e shown t h a t t h e w a l l s t r e n g t h o f many n e o g a s t r o p o d e g g c a p s u l e s time o f encapsulated
embryos
i s r e l a t e d t o t h e development (Perron,
1981).
These
results
2 suggest that greater
variation
goals
stresses.
o f t h e p r e s e n t s t u d y w e r e : 1) t o e x a m i n e
i n t h e morphology o f egg c a p s u l e s
of the i n t e r t i d a l
snail Nucella
among
This
emarginata, and
embryos from
predators.
t h e s i s i s d i v i d e d i n t o two c h a p t e r s .
presents
d a t a on t h e m o r p h o l o g y o f N u c e l l a
capsules
c o l l e c t e d from t h r e e
gradient.
Differences
s i t e s along
i n egg c a p s u l e
Chapter 1
emarginata egg a wave-exposure
wall thickness are
e x a m i n e d w i t h i n a n d among s i t e s a n d c o r r e l a t e d measurements o f c a p s u l e
strength.
with
reference
to the possible
extra-embryonic structures. of predation Potential
i n t e r t i d a l predators
predator
preferences
examined.
The e x t e n t
morphology.
capsules.
s t u d i e s , and evidence o f
i n the f i e l d
i s described.
of f i e l d predation
i s discussed
may h a v e p l a y e d
o f such
are i d e n t i f i e d through a
f o r t h i c k - o r t h i n - w a l l e d egg
e m a r g i n a t a egg c a p s u l e s predation
function(s)
e m a r g i n a t a egg
and l a b o r a t o r y
species-specific predation
wall thickness are
Chapter 2 i n v e s t i g a t e s the extent
on i n t e r t i d a l N u c e l l a
combination of f i e l d
with
The i m p l i c a t i o n s o f i n t r a -
i n t e r s p e c i f i c d i f f e r e n c e s i n capsule
discussed
are
populations
t o determine the e f f e c t i v e n e s s of these s t r u c t u r e s i n
protecting developing
and
a
s t r u c t u r e may a l s o be c o r r e l a t e d w i t h d i f f e r e n c e s i n
l e v e l s of s p e c i f i c environmental The
2)
d e v e l o p m e n t t i m e s may be a s s o c i a t e d w i t h
r i s k o f embryonic m o r t a l i t y and, hence, d i f f e r e n c e s i n
capsular the
longer
Also,
capsules
on N u c e l l a
i n terms o f t h e r o l e
i n the evolution of
capsule
that
3 CHAPTER 1 FUNCTIONAL MORPHOLOGY OF MARINE GASTROPOD EGG I N T R A S P E C I F I C VARIATION
IN SIZE,
CAPSULES:
WALL THICKNESS
STRENGTH OF NUCELLA EMARGINATA EGG
AND
CAPSULES
INTRODUCTION
The c o n f i n e m e n t is
o f d e v e l o p i n g embryos w i t h i n e g g
a common phenomenon among m a r i n e i n v e r t e b r a t e s .
N e o g a s t r o p o d m o l l u s c s e n c l o s e t h e i r embryos structurally
complex p r o t e i n a c e o u s
their
larval
life.
Gastropod
c o n s i d e r e d t o be " p r o t e c t i v e " P e r r o n and Corpuz,
1982),
against i s unclear. thought
t o reduce
(Pechenik, osmotic 1988), shock
However,
(Pechenik,
1979; P e r r o n ,
(Pechenik,
bacterial
attack
in
(Lord,
1982; 1983, H a w k i n s a n d
( S p i g h t , 1977; P e c h e n i k , 1986),
1978),
Hutchinson, temperature (Perron,
o n l y a few s t u d i e s h a v e s p e c i f i c a l l y
examined
factors
1978; 1982; 1983; B r e n c h l e y ,
1984; L o r d , 1986; H a w k i n s a n d H u t c h i n s o n ,
field
situations.
1982;
1988)
i s known a b o u t t h e s u r v i v o r s h i p o f e n c a p s u l a t e d
actual
1986),
a n d wave a c t i o n
( S p i g h t , 1977; P e c h e n i k ,
little
1981;
s t r e s s e s as: p r e d a t i o n
t h e r e s i s t a n c e o f e n c a p s u l a t e d embryos t o t h e s e
Davies,
all,
Commonly, t h e e g g c a p s u l e s h a v e b e e n
( S p i g h t , 1977; P e c h e n i k ,
1981).
some, i f n o t
egg c a p s u l e s a r e f r e q u e n t l y
such environmental
desiccation
embryos
b u t what t h e y p r o t e c t e m b r y o s
1979; P e r r o n , 1 9 8 1 ) ,
changes
within
c a p s u l e s , and
develop w i t h i n these capsules f o r at l e a s t of
capsules
and embryos
4 An
examination of i n t r a -
the
s t r u c t u r e o f egg
the
r o l e that capsules
Variation capsular
i n capsule
be
can
w a l l s may
play
be
useful in
i n gastropod
w a l l s t r e n g t h and
positively
(Perron,
1981).
life-histories.
the
Furthermore, capsule
and
Corpuz, 1982).
a c c o u n t f o r a l m o s t 50%
capsules
(Perron,
have e v o l v e d
energy i n v e s t e d
Perron
As
long encapsulated
been
i n some s p e c i e s
of the
development
capsular
energy i n v e s t e d i n
cases
intact
1981), s t r o n g , t h i c k - w a l l e d capsules
may
f o r increased p r o t e c t i o n of encapsulated
and
in
w a l l s a r e known t o
w i t h long-term exposure to environmental s t r e s s e s 1981;
assessing
c o r r e l a t e d w i t h embryonic developmental
t h i c k e r i n Conus s p e c i e s w i t h
(Perron
interspecific variation in
c a s e s among s p e c i e s w i t h i n t h e g e n u s Conus has
f o u n d t o be time
capsule
and
Corpuz, 1982).
I f s e l e c t i o n has
embryos
(Perron, also
responded t o i n t e n s i t y of these environmental f a c t o r s , then i n t r a s p e c i f i c comparisons of capsular
s t r u c t u r e across
a
v a r i e t y of h a b i t a t s could r e v e a l d i f f e r e n c e s a s s o c i a t e d s p e c i f i c sources of m o r t a l i t y . specifically
examined i n t r a -
As
s p e c i e s may
be
i n the
s t u d i e s have
or i n t e r s p e c i f i c v a r i a t i o n i n
structure of gastropod capsules Differences
y e t , no
s t r u c t u r e o f egg
capsules
within a
separated
sharp environmental gradients,
s u c h as
Stresses
o r g a n i s m s a r e known t o
intertidal
(Menge, 1 9 7 8 a ;
Menge and
Sutherland,
h a v e shown t h a t
increases
i n w a v e - e x p o s u r e a r e m a t c h e d by:
predation
intensity,
Studies
along
wave-exposure.
g r e a t l y along wave-exposure g r a d i e n t s 1987).
the
among d i f f e r e n t h a b i t a t s .
most a p p a r e n t among p o p u l a t i o n s
i m p o s e d on
with
differ 1978b;
1) d e c r e a s e s i n
as wave a c t i o n g e n e r a l l y t e n d s t o
disrupt
5 predator foraging a c t i v i t i e s
( K i t c h i n g e t a l . , 1959;
1 9 7 8 a ; 1978b; R o b l e s ,
and
stress, 1971;
as a r e a s
1987),
2) d e c r e a s e s
Wave-action i t s e l f
i s known t o
s e v e r e p h y s i c a l s t r e s s e s upon i n t e r t i d a l
abrasion Wright, to
(Denny, 1985,
(Craik, 1986).
organisms,
1980),
Denny e t a l . , 1985;
and w a t e r - b o r n
rocks
impose to
Etter,
1987),
(Shanks
and
capsules are
stresses similar to sessile
a w a v e - e x p o s u r e g r a d i e n t may
(Dayton,
o r g a n i s m s due
A s s u m i n g t h a t b e n t h i c egg
environmental
in desiccation
s p l a s h e d by waves s u f f e r l e s s d r y i n g
Menge, 1 9 7 8 a ) .
dislodgement
Menge,
exposed
intertidal
provide a
convenient
means o f c o m p a r i n g c a p s u l e s t r u c t u r e a c r o s s a r a n g e
of
environmental c o n d i t i o n s . In
order that i n t r a s p e c i f i c d i f f e r e n c e s i n capsule
s t r u c t u r e c a n be
interpreted,
i t i s essential to
understand
c e r t a i n c o n s t r a i n t s i m p o s e d on t h e m o r p h o l o g y o f g a s t r o p o d capsules. et
F o r i n s t a n c e , i t i s known f r o m t h e work o f
a l . (1974),
S p i g h t and E m l e n
(1976) and P e r r o n and
c a p s u l e s i s r e l a t e d t o female
size.
(Strathmann
gastropod
C o n s t r a i n t s may
be p l a c e d on c a p s u l e s t r u c t u r e by t h e r e q u i r e m e n t s d e v e l o p i n g embryos
and C h a f f e e ,
oxygen or waste p r o d u c t s H e n c e , t h e r e may
restrict
and t h u s r e d u c e
1984).
For low
the d i f f u s i o n
embryo
also
of
i n s t a n c e , t h i c k c a p s u l e w a l l s or c a p s u l e shapes w i t h s u r f a c e a r e a t o v o l u m e r a t i o s may
Spight Corpuz
(1982) t h a t t h e l e n g t h , v o l u m e and w a l l t h i c k n e s s o f egg
egg
of
survivorship.
be t r a d e o f f s i n c a p s u l e d e s i g n , s u c h
that
t h i c k - w a l l e d c a p s u l e s p r o t e c t embryos b e t t e r from p r e d a t i o n o r physical
s t r e s s , b u t may
surviving.
l i m i t t h e number o f e m b r y o s
T h e r e f o r e , a s t u d y o f c a p s u l e f u n c t i o n must
6 i n v o l v e a knowledge o f t h e i n t e r r e l a t i o n s h i p s between
capsule
morphology, c a p s u l e w a l l t h i c k n e s s , and t h e packaging o f embryos w i t h i n The
capsules.
marine i n t e r t i d a l
snail,
common i n h a b i t a n t o f r o c k y s h o r e s and
ranges
isa
from C a l i f o r n i a t o A l a s k a
across wide extremes i n wave-exposure.
s n a i l s d e p o s i t eggs w i t h i n which
N u c e l l a emarginata,
These
6-10 mm-long v a s e - s h a p e d c a p s u l e s ,
they a t t a c h d i r e c t l y t o the substratum.
T h r e e t o 35
embryos a r e e n c l o s e d w i t h hundreds o f n u r s e eggs, u s e d as f o o d by t h e d e v e l o p i n g l a r v a e . 1966),
A f t e r approximately
80 d a y s
(Emlen,
e m b r y o s emerge f r o m t h e e g g c a p s u l e s a s j u v e n i l e
snails. In t h i s
study,
I examined i n t r a s p e c i f i c v a r i a t i o n i n
c a p s u l e m o r p h o l o g y w i t h i n a n d among p o p u l a t i o n s o f N u c e l l a emarginata.
P o p u l a t i o n s were c h o s e n from t h r e e
separated along a g r a d i e n t o f wave-exposure.
sites
Data were
c o l l e c t e d o n : 1) t h e s i z e a n d s h a p e o f s n a i l s w i t h i n a n d among populations,
2) i n t r a s p e c i f i c d i f f e r e n c e s i n c a p s u l e s i z e a n d
w a l l t h i c k n e s s , 3) v a r i a t i o n i n t h e p a c k a g i n g
o f eggs and
e m b r y o s w i t h i n c a p s u l e s , a n d 4) t h e r e l a t i o n s h i p b e t w e e n c a p s u l e w a l l t h i c k n e s s and c a p s u l e s t r e n g t h , f o r each
site.
7 STUDY SITE DESCRIPTIONS
T h i s p r o j e c t was c o n d u c t e d
at t h e Bamfield Marine S t a t i o n
on t h e w e s t c o a s t o f V a n c o u v e r I s l a n d (125°10'N, Fig.l).
48°50'W;
S t u d y s i t e s w e r e e s t a b l i s h e d i n B a r k l e y Sound f o r t h e
purpose o f c o l l e c t i n g N u c e l l a emarqinata capsules.
a d u l t s and t h e i r egg
Three l o c a t i o n s were chosen t o r e p r e s e n t a g r a d i e n t
o f wave-exposure from s h e l t e r e d t o exposed: G r a p p l e r Ross I s l e t s ,
and Seppings I s l a n d .
s t u d i e s have ranked
these
areas
Although
Inlet,
no e m p i r i c a l
i n B a r k l e y Sound w i t h
respect
t o w a v e - e x p o s u r e , my r a t i n g s y s t e m , b a s e d on v i s u a l observations, corresponded
w i t h s u b j e c t i v e exposure s c a l e s
e m p l o y e d b y o t h e r s i n t h e same g e o g r a p h i c Druehl,
and Haven, 1971; K i t c h i n g ,
1. G r a p p l e r The
region (Austin,
1976; C r o t h e r s ,
Inlet
Grappler
Inlet
exposed study area
s i t e represented the least
(Fig. 1 ) . Although
considerable t i d a l
r e p r e s e n t e d an e x t r e m e
(Crothers, Grappler
exchange.
distributional
which a r e n o r m a l l y absent 1984).
i t was s u b j e c t t o a
c u r r e n t due t o t h e c o n s t r i c t e d w i d t h o f t h e
and l a r g e volume o f t i d a l
emarqinata,
wave-
t h e a c t u a l s i t e was t o o
f a r up t h e i n l e t t o r e c e i v e o c e a n i c s w e l l ,
channel
1984).
This
limit
site
f o r Nucella
from p r o t e c t e d
inlets
A g e n e r a l s e a r c h f o r N. e m a r q i n a t a
along
I n l e t r e v e a l e d t h a t t h e y were p r e s e n t
a r e a s : a t my s t u d y
o n l y i n two
l o c a t i o n a n d on r o c k y b e a c h e s a r o u n d t h e
mouth o f t h e i n l e t . The
s i t e was l o c a t e d i n a n i n t e r t i d a l
channel,
a b o v e z e r o c h a r t datum, c o n n e c t i n g t h e m a i n l a n d
1.6m
and a s m a l l
8
FIGURE 1. The l o c a t i o n of study s i t e s a l o n g the southern shores of B a r k l e y Sound on the west c o a s t of Vancouver I s l a n d , B.C. Study l o c a t i o n s were chosen a l o n g a wave-exposure g r a d i e n t . Wave-exposure l e v e l s were p r e d i c t e d t o be lowest at G r a p p l e r I n l e t , h i g h e s t at Seppings I s l a n d , and i n t e r m e d i a t e at the Ross I s l e t s s i t e .
9 piece of land isolated at high t i d e .
The
intertidal
s u b s t r a t e c o n s i s t e d o f f i n e s i l t y mud o v e r l a i d b y c l a m and
a meshwork o f m u s s e l - a n d b a r n a c l e - c o v e r e d
edulis,
Balanus qlandula
e m a r q i n a t a were p r e s e n t t i d a l height
and Semibalanus c a r i o s u s ) . throughout t h e channel
of approximately
Other gastropods present dira,
channel.
2.6m
(Mytilus Nucella
and ranged t o a
above z e r o
chart
datum.
were N u c e l l a l a m e l l o s a , S e a r l e s i a
Onchidella borealis,
chitons Mopalia
rocks
shells
and v a r i o u s l i m p e t
species.
The
spp. were a l s o abundant t h r o u g h o u t t h e
The p o l y c h a e t e s ,
N e r e i s v e x i l l o s a and s e v e r a l
s p e c i e s o f s c a l e worms w e r e a s s o c i a t e d w i t h t h e m u s s e l - a n d barnacle-covered ubiquitous.
rocks, while
Three i s o p o d
s e v e r a l nemertean s p e c i e s
s p e c i e s were
present:
Gnorimosphaeroma oreqonense, C i r o l a n a h a r f o r d i , wosnesenskii.
Hemigrapsus oregonensis
t h e c o m p a c t mud f o u n d i n h i g h e r H. n u d u s w e r e r a r e l y be
seen.
were
and Idotea
burrows were e v i d e n t i n
intertidal
Hermit crabs
regions;
however,
(Pagurus spp.) c o u l d
f o u n d i n amongst t h e meshwork o f m u s s e l s , b a r n a c l e s a n d
rocks.
Fucus and U l v a were t h e p r e d o m i n a n t i n t e r t i d a l
2. R o s s This
Islets s i t e was c h o s e n t o r e p r e s e n t
intermediate
wave-exposure
(Fig. 1).
a region
these
waves b r e a k i n g
areas
channel.
s i t e s received only small swells r e s u l t i n g
from
on t h e s o u t h - f a c i n g s h o r e s o f t h e i s l e t s a n d on
a r e e f between two n e i g h b o u r i n g The
with
The c o l l e c t i n g
w e r e l o c a t e d on b o t h s i d e s o f a w a v e - p r o t e c t e d Normally
algae.
intertidal
islands.
substrate i n this
g r a n i t e bedrock, w i t h a boulder
region consisted of
beach c o v e r i n g
some o f t h e
10 lower r e g i o n s . intertidally:
Three b a r n a c l e s p e c i e s were p r e s e n t Balanus
Chthamalus d a l l i . patchy
clumps.
g l a n d u l a , S e m i b a l a n u s c a r i o s u s and
M y t i l u s c a l i f o r n i a n u s were p r e s e n t
N u c e l l a emarginata
high- i n t e r t i d a l
were found
z o n e s b e t w e e n 1.8
- 3.1
i n the mid-
lamellosa,
Other
Tegula
limpet species.
littoral
gastropods
funebralis, The
boulder
p r e s e n t were N u c e l l a
S e a r l e s i a d i r a and
c h i t o n s , M o p a l i a spp.,
o c c a s i o n a l l y on g r a n i t e p r o m o n t o r i e s .
various
were seen
Intertidal
and n e m e r t e a n s w e r e s p a r s e , w i t h N e r e i s v e x i l l o s a Emplectonema g r a c i l e b e i n g t h e o n l y o b v i o u s these groups.
The
p u r p l e shore
porcelain crabs, P e t r o l i s t h e s in
t h e b o u l d e r b e a c h e s and
Starfish,
polychaetes and
r e p r e s e n t a t i v e s of
c r a b s , Hemigrapsus nudus,
spp. were abundant u n d e r
i n some h i g h e r i n t e r t i d a l
distichus,
The
predominant h i g h i n t e r t i d a l
3. S e p p i n g s T h i s was
a l g a was
2.6
- 2.9
t h e most w a v e - e x p o s e d s i t e
(Fig. 1).
l o c a t e d i n a large b o u l d e r - l i n e d channel,
facing a r e l a t i v e l y unobstructed oceanic bordered
on t h e o t h e r by a l a r g e r o c k y p r o m o n t o r y c o v e r e d
Mytilus californianus.
on one
swell.
and
- 2.0
tide
The
c h a n n e l was
0.3
Fucus
m a b o v e z e r o c h a r t datum.
The
from
boulder
Island
c o l l e c t i n g a r e a was 10 m w i d e ,
rocks
d i s t r i b u t e d i n a d i s t i n c t v e r t i c a l band at a
height of approximately
and
crevices.
P i s a s t e r - o c h r a c e u s , w e r e a l s o common i n t h e
beach area.
to
m above z e r o c h a r t
datum, and w e r e p r e s e n t o c c a s i o n a l l y i n t h e l o w e r beach r e g i o n .
in
Boulders
m diameter.
s i d e by a h i g h g r a n i t e w a l l
i n the channel
ranged
During w i n t e r storms,
o f t e n were r e d i s t r i b u t e d t h r o u g h o u t
with
the i n t e r t i d a l
in size
boulders area
by
11 wave
action. The c o l l e c t i n g c h a n n e l
barnacles dalli,
(Balanus
was c h a r a c t e r i z e d by a v a r i e t y o f
g l a n d u l a , Semibalanus c a r i o s u s , Cthamalus
and P o l i c i p e s p o l y m e r u s ) ,
N. c a n a l i c u l a t a , gastropods
whelks
(Nucella
emarginata,
and C e r a t o s t o m a f o l i a t u m ) and o t h e r
(Ocenebra l u r i d a ,
Tegula
funebralis,
Calliostoma
l i g a t u m and v a r i o u s l i m p e t s p e c i e s ) .
Idotea wosnesenskii
the only i n t e r t i d a l
Hemigrapsus nudus were
present
isopods present.
i n l a r g e numbers u n d e r n e a t h t h e r o c k y b o u l d e r s ,
were s m a l l h e r m i t
crabs
(Pagurus
(Petrolisthes cinctipes).
Algae
i n the high i n t e r t i d a l
as
spp.) a n d p o r c e l a i n c r a b s consisted of Laminaria
I r i d a e a s p e c i e s i n t h e low i n t e r t i d a l limitata
were
and
a r e a , and P e l v e t i o p s i s
regions.
12 MATERIALS AND METHODS
I . DIFFERENCES
I N SNAIL MORPHOLOGY AMONG SITES
Shell-length t o aperture-length
r a t i o s were u s e d t o
compare s h e l l m o r p h o l o g y among s i t e s ,
as t h e s e . r a t i o s a r e t h e
q u i c k e s t and s i m p l e s t method o f d e t e r m i n i n g variation
i n t h e genus N u c e l l a
were c o l l e c t e d from each s t u d y
shell-shape
(Crothers, 1984). area
Nucella
e m a r q i n a t a from a g i v e n a r e a t o a v o i d any b i a s e s size,
o r shape.
Snails considered
( l e s s t h a n 10 mm i n l e n g t h ) variation
i nshell
were r e p l a c e d ,
s h a p e i s known t o o c c u r
j u v e n i l e development (Crothers,
1984).
l e n g t h s were measured t o t h e n e a r e s t calipers.
for shell
t o be j u v e n i l e s as c o n s i d e r a b l e during early
S h e l l and a p e r t u r e -
0.1mm w i t h v e r n i e r
S h e l l - l e n g t h was d e f i n e d a s t h e maximum
between t h e s h e l l
snails
i n t h e s p r i n g o f 1988.
C o l l e c t i o n s w e r e made b y r e m o v i n g a l l l i v i n g
colour,
Fifty
length
apex and a n t e r i o r t i p o f t h e s i p h o n a l
canal,
w h i l e a p e r t u r e - l e n g t h was t h e maximum d i s t a n c e b e t w e e n t h e p o s t e r i o r corner siphonal
II.
o f the aperture
l i p and a n t e r i o r t i p o f t h e
canal.
CAPSULE MORPHOLOGY 1. R e l a t i o n s h i p b e t w e e n s n a i l
s i z e and capsule
I n o r d e r t o compare t h e s i z e o f e g g c a p s u l e s snails
from each s i t e ,
collected
approximately
from each study
area.
l a i d by
50-100 s n a i l s
were
S n a i l s were b r o u g h t i n t o t h e
laboratory, tagged f o r i d e n t i f i c a t i o n , specific p l a s t i c containers
size
and assigned
(32x26x12cm, w i t h 20x8cm
to sitelmm-pore
13 mesh w i n d o w s i n e a c h o f t h e f o u r s i d e s ) .
Approximately
s n a i l s were h e l d i n each c o n t a i n e r and were p r o v i d e d barnacles
f o r food.
Containers
40-50
with
were k e p t submerged i n
l a b o r a t o r y seawater t a b l e s and s u p p l i e d w i t h a c o n t i n u o u s of f r e s h seawater. every
E a c h l a b o r a t o r y p o p u l a t i o n was c h e c k e d
two days o v e r a s i x - w e e k p e r i o d t o i d e n t i f y
l a y i n g egg c a p s u l e s . egg
capsule
capsule
flow
A s n a i l was r e c o g n i z e d
snails
t o b e l a y i n g an
o n l y i f i t was f o u n d a c t u a l l y m o l d i n g a new
with i t s v e n t r a l pedal
gland.
Such c a p s u l e s
c o u l d be
i d e n t i f i e d r e a d i l y by t h e i r
s o f t w a l l s and m i l k y - y e l l o w
appearance.
were c o l l e c t e d w i t h t h e n e w l y - l a i d
Other capsules
ones o n l y i f t h e y clutch. laid
were c o n s i d e r e d
t o be p a r t o f t h e same
A c l u t c h was d e f i n e d t o b e a n y number o f c a p s u l e s
i n w i t h i n a f e w mm o f one a n o t h e r t h a t w e r e s i m i l a r i n
shape and o r i e n t a t i o n ( G a l l a r d o , 1979). capsules
A maximum o f 5
was c o l l e c t e d f r o m e a c h f e m a l e a t a n y s p a w n i n g c h e c k .
Capsule-laying
f e m a l e s were measured f o r s h e l l
returned t o t h e i r containers.
l e n g t h and
C a p s u l e s were p r e s e r v e d
i n 5%
f o r m a l i n f o r subsequent measurement. Three measurements were t a k e n 1)"capsule
f o r each capsule
body l e n g t h " , w h i c h e x c l u d e d
t h i s was known t o be e x t r e m e l y 1976); 2)"capsule chamber h o u s i n g
(Fig.2):
t h e stem l e n g t h as
v a r i a b l e (Spight and Emlen,
chamber l e n g t h " , r e p r e s e n t i n g t h e l e n g t h o f
t h e e m b r y o s a n d n u r s e e g g s ; a n d , 3) t h e
"maximum c a p s u l e
width",
w h i c h was t h e maximum w i d t h
capsule-chamber.
The " c a p s u l e
using t h e formula
f o ra prolate ellipsoid,
where a = t h e c a p s u l e
chamber v o l u m e " was
ofthe estimated
V=4/37T(a/2) ( b / 2 ) 2 ,
chamber l e n g t h a n d b = t h e maximum
14
Capsular Hug
Capsule Body Length
Capsule Chamber Length
Stem
Maximum Capsular Width 1
2mm
Scale
FIGURE 2. N u c e l l a emarginata egg c a p s u l e , i l l u s t r a t i n g t h e t h r e e measurements taken f o r each c a p s u l e : capsule-body l e n g t h , capsule-chamber l e n g t h , and maximum c a p s u l e width. The c a p s u l a r - p l u g r e g i o n and the stem are a l s o i n d i c a t e d .
15 capsule
width
(Pechenik,
1982).
2. M i c r o - m o r p h o l o g y o f N u c e l l a e m a r g i n a t a egg Representative
egg
capsules
o f N u c e l l a e m a r g i n a t a were
s e c t i o n e d u s i n g a f r e e z e microtome. of each capsule and
was
1968;
capsules
o f N.
lapillus
M a u g e l , 1984;
Intracapsular variation emarginata capsules
was
laboratory, these
maintained before,
(0%)
then i n d i v i d u a l l y
f r o z e n on
were t a k e n
length of the capsule
were t a k e n
at the
capsule-chamber.
1988).
thickness
f r o m any
one
Nucella
C a p s u l e s were minimize
female.
in cylindrical
In
The
and
C a p s u l e s were measured by
removing the
j u n c t i o n between the
as
capsular
a f r e e z e microtome.
plug,
Sections,
a t 10 p e r c e n t i l e i n t e r v a l s chamber.
The
first
sections
opening of the plug region i n t o last
the
vials
2.0x2.5cm lmm-pore mesh p a n e l s )
emptied of a l l contents
along the
(Bayne,
clutches within a s i t e to
i n f l o w i n g seawater.
e a c h 10-12yum t h i c k ,
other muricids
i n the w a l l t h i c k n e s s of
were t h e n p l a c e d
(3.5x3.5x6cm w i t h two
studies
examined f o r each s i t e .
from d i f f e r e n t
microscope
histological
D'Asaro,
the chance of o b t a i n i n g c a p s u l e s
and
and
Intracapsular variation in wall
collected
wall microstructure
e x a m i n e d u s i n g a compound l i g h t
S u l l i v a n and
3.
the
The
i n t e r p r e t e d with respect to previous
on t h e egg
capsules
section
(100%) was
c a p s u l e - c h a m b e r and
were mounted i n a s e a w a t e r - s o l u b l e
taken stem.
m o u n t i n g medium
the
close to Sections and
measurements t a k e n
u s i n g a compound m i c r o s c o p e w i t h c a l i b r a t e d
ocular micrometer.
E i g h t measurements o f w a l l t h i c k n e s s were
16 taken at a p p r o x i m a t e l y equal i n t e r v a l s around each c a p s u l e section.
The
average w a l l t h i c k n e s s w i t h i n each s e c t i o n
used i n a l l subsequent
was
data analyses.
4. V a r i a t i o n i n c a p s u l e w a l l - t h i c k n e s s among p o p u l a t i o n s . I n o r d e r t o e x a m i n e w a l l t h i c k n e s s d i f f e r e n c e s among a l a r g e number o f egg c a p s u l e s , a l a b o r a t o r y p o p u l a t i o n o f s n a i l s was
e s t a b l i s h e d from each s i t e .
S n a i l s w e r e s e x e d by
a l l o w i n g e a c h a n i m a l t o a t t a c h t o a r o c k s u r f a c e and gently p u l l i n g the s h e l l
60
away f r o m t h e b o d y mass.
then
A male
c o u l d be i d e n t i f e d b y t h e p r e s e n c e o f a p e n i s l a r g e r t h a n i t s right tentacle Palmer,
1984).
(rather than the smaller penis of the female; F i v e m a l e and f i v e
female s n a i l s
s i t e were a l l o c a t e d t o each o f s i x r e p l i c a t e
from
each
cages
(26x16.5x13cm, w i t h 8x16cm lmm-pore mesh p a n e l s i n e a c h and were s u p p l i e d w i t h b a r n a c l e s f o r f o o d .
Female s n a i l s
s e l e c t e d so t h a t e a c h r e p l i c a t e c a g e h a d a s i m i l a r mean size
( G r a p p l e r : X=3.0 cm;
X=2.0 cm).
side)
R o s s I s l e t s : X=2.3 cm;
were
snail
Seppings:
A l l cages were k e p t c o m p l e t e l y . i m m e r s e d i n f l o w i n g
seawater. E v e r y two weeks f r e s h l y
l a i d c a p s u l e s were c o l l e c t e d
placed i n small mesh-panelled v i a l s .
V i a l s were
d a t e d , and immersed i n f l o w i n g s e a w a t e r u n t i l needed.
and
labelled,
c a p s u l e s were
C a p s u l e s c o n t a i n e d i n t h e s e " c a p s u l e v i a l s " were u s e d
i n s e v e r a l e x p e r i m e n t s as
follows.
To e x a m i n e v a r i a t i o n i n c a p s u l e w a l l t h i c k n e s s w i t h i n among p o p u l a t i o n s , each r e p l i c a t e v i a l
f i v e c a p s u l e s were s e l e c t e d randomly (n=30 c a p s u l e s / s i t e ) .
C a p s u l e s were
and
from
17 measured i n d i v i d u a l l y
and marked a t a p o i n t 70% a l o n g t h e
length of the capsule
chamber w i t h a f i n e S t a e d t l e r L u m o c o l o u r
pen.
Previous
capsule
data
on w a l l t h i c k n e s s v a r i a t i o n w i t h i n a
i n d i c a t e d that capsules
thickness
were t h i n n e s t and w a l l
least variable i n this region.
C a p s u l e s were
e m p t i e d by removing t h e p l u g and t h e n s e c t i o n e d microtome.
Sections
on t h e f r e e z e -
w e r e c o l l e c t e d o n l y when t h e b l a d e
reached the p o r t i o n of the capsule
chamber m a r k e d w i t h i n k .
F i v e s e c t i o n s , e a c h 10-12yum t h i c k , w e r e t a k e n f o r e a c h and
capsule
one s e c t i o n was c h o s e n f o r m e a s u r e m e n t .
5. V a r i a t i o n i n c a p s u l e clutches
w a l l t h i c k n e s s w i t h i n a n d among
l a i d by d i f f e r e n t females
I n t r a - and i n t e r c l u t c h v a r i a b i l i t y
i n wall thickness
examined t o determine i f females w i t h i n a p o p u l a t i o n
was
laid
capsules
of different wall thicknesses.
capsules
was c o l l e c t e d f r o m e a c h o f f i v e r e p l i c a t e c a g e s f o r
each o f t h e three by its
One c l u t c h o f e g g
s i t e s t o e n s u r e t h a t a l l c l u t c h e s were
d i f f e r e n t females.
E a c h c l u t c h was c o l l e c t e d a n d k e p t i n
own l a b e l l e d m e s h - p a n e l l e d c o n t a i n e r u n t i l
needed f o r s e c t i o n i n g .
laid
Representative
capsules
capsules
were
were s e l e c t e d
randomly from each c l u t c h , measured under a d i s s e c t i n g microscope, and t h e n s e c t i o n e d length of the capsule w e r e made a s d e s c r i b e d
chamber.
at a point Wall
thickness
measurements
previously.
6. V a r i a t i o n i n d r y w e i g h t o f c a p s u l e s Dry
70 % a l o n g t h e
w e i g h t measurements o f c a p s u l e s
among
populations.
were t a k e n f o r each
18 p o p u l a t i o n to determine corresponded
i f d i f f e r e n c e s among
sites
to d i f f e r e n c e s i n capsule w a l l thickness.
For
each p o p u l a t i o n , r e p r e s e n t a t i v e c a p s u l e s were c o l l e c t e d each of s i x r e p l i c a t e capsule v i a l s .
Capsules
and t h e n o p e n e d t o remove a l l c o n t e n t s . from c a p s u l e s t o minimize capsules.
Capsules
variability
from
were measured
Stems w e r e r e m o v e d
i n weight
among
were r i n s e d t w i c e i n d i s t i l l e d water
t h e n d r i e d f o r 48 h r s a t 75°C.
and
A f t e r d r y i n g , c a p s u l e s were
w e i g h e d t o O.Olmg.
I I I . VARIATION IN CAPSULE CONTENTS AMONG SITES 1. Egg Egg
number and
volume
c a p s u l e c o n t e n t s were examined t o d e t e r m i n e
i f the
number o r s i z e o f e g g s p e r c a p s u l e d i f f e r e d w i t h p o p u l a t i o n differences i n capsule structure. were c o l l e c t e d each s i t e
Three newly l a i d
capsules
from each of s i x r e p l i c a t e c a p s u l e v i a l s
(18 c a p s u l e s / s i t e ) .
Capsules
were measured,
sliced
o p e n , and t h e i r c o n t e n t s w a s h e d w i t h f i l t e r e d s e a w a t e r small p e t r i dish.
As n u r s e
eggs t e n d e d
for
into
t o clump t o g e t h e r ,
eggs were g e n t l y a g i t a t e d a p a r t w i t h a p i p e t t e .
A l l nurse
e g g s and e m b r y o s w i t h i n a c a p s u l e w e r e c o u n t e d .
Before
c o u n t s w e r e made, h o w e v e r , e m b r y o s w e r e e x a m i n e d t o t h a t t h e y had not advanced p a s t t h e second LeBoeuf
(1971) and L y o n s and
once p a s t t h i s d e v e l o p m e n t a l f e e d i n g on e n c a p s u l a t e d n u r s e As
egg
Spight
veliger
these
ensure stage.
(1973) h a v e n o t e d
that
s t a g e , e m b r y o s become c a p a b l e eggs.
s i z e w i t h i n a c a p s u l e was
a
relatively
o n l y f i v e eggs were sampled from each c a p s u l e .
constant, Length
and
of
19 w i d t h measurements were t a k e n
f o r each egg.
E g g v o l u m e was
e s t i m a t e d by u s i n g t h e f o r m u l a f o r a p r o l a t e e l l i p s o i d as described previously.
2. Number a n d s i z e To d e t e r m i n e
of hatching
snails.
i f t h e r e was a d i f f e r e n c e i n t h e number o f
embryos p e r c a p s u l e from e a c h s i t e , embryos were a l l o w e d t o hatch i n the laboratory. their
l a r v a e developed
capsule v i a l s u n t i l development neared
this point, individual their
Encapsulated
own m e s h - p a n e l l e d
i n seawater
within
completion.
At
c a p s u l e s from each s i t e were p l a c e d i n vials
(600 yUm mesh p o r e ) a n d s u b m e r g e d
u n t i l t h e embryos h a t c h e d .
Capsules
were
checked
e v e r y two d a y s a n d a s s o o n a s an embryo h a d emerged, t h e c a p s u l e was m e a s u r e d a n d e m p t i e d All
l i v e embryos were c o u n t e d
o f a l l r e m a i n i n g embryos.
and t h e i r
shell-lengths
measured.
I V . CAPSULE STRENGTH MEASUREMENTS 1. R e s i s t a n c e t o p u n c t u r i n g This index determined
the resistance of capsule w a l l s to
p u n c t u r i n g a n d was b a s e d on P e r r o n ' s Conus e g g c a p s u l e s . were t a k e n
(1981) p r o c e d u r e f o r
Newly l a i d N u c e l l a emarginata
from t h e i r
capsules
r e s p e c t i v e c a p s u l e v i a l s , measured, and
t h e n marked a t a p o i n t 70% a l o n g t h e l e n g t h o f t h e c a p s u l e chamber.
Capsules
w e r e t h e n b i s e c t e d by c u t t i n g a l o n g t h e two
seams o f t h e c a p s u l e chamber a n d t h e i r
contents discarded.
E a c h c a p s u l e h a l f was m o u n t e d i n d i v i d u a l l y of p l e x i g l a s s
b e t w e e n two p i e c e s
(8.5x5cm) a n d o r i e n t a t e d s u c h t h a t a 1mm d i a .
20 h o l e i n e a c h p i e c e o f p l e x i g l a s s was p o s i t i o n e d d i r e c t l y t h e marked r e g i o n o f t h e c a p s u l e taken
chamber
(Fig. 3a).
t o i n s u r e t h a t t h e r e w e r e no f o l d s o r c r e a s e s
capsule
s e c t i o n and t h a t i t remained m o i s t .
device, c o n s i s t i n g of a blunt-ended
needle
A
over
Care
was
i n the
puncturing
(0.36 mm^
area)
mounted b e n e a t h a f l a t w e i g h i n g
p a n , was p o s i t i o n e d o v e r t h e
plexiglass
r e s t e d at r i g h t angles
such t h a t t h e needle
exposed capsule w a l l . weighing
Five-gram weights
pan u n t i l t h e n e e d l e
punctured
E a c h c a p s u l e p i e c e was o n l y p u n c t u r e d
2. R e s i s t a n c e This index
to
were added t o t h e the capsule
wall.
once.
squeezing
of capsule
s t r e n g t h measured t h e f o r c e needed
t o squeeze t h e p l u g out o f i n t a c t c a p s u l e s .
Shore crabs
o f t e n seen t o r u p t u r e N u c e l l a e m a r g i n a t a egg c a p s u l e s squeezing
to the
them i n t h e i r c h e l a e .
Laboratory
capsules
were
by were
c o l l e c t e d from r e p l i c a t e c a p s u l e v i a l s and measured. Individual capsules
were mounted w i t h " S u p e r g l u e "
onto a
metal
p l a t e , w h i c h was t h e n b o l t e d t o a v e r t i c a l p i e c e o f p l e x i g l a s s (Fig.
3b).
S t r a i n gauges, g l u e d t o t h e p l e x i g l a s s ,
c o n n e c t e d t o an a m p l i f i e r a n d c h a r t r e c o r d e r .
were
A second
metal
p l a t e was a t t a c h e d t o a s p i n d l e so t h a t t h i s p l a t e c o u l d be h a n d - c r a n k e d t o w a r d s t h e mounted c a p s u l e . provided capsule.
A chart
recorder
a r e c o r d o f t h e f o r c e r e q u i r e d t o r u p t u r e t h e egg T h i s s y s t e m was c a l i b r a t e d w i t h known
weights.
21
a)
Weights Loading Pan
Stand Blunt Pin Plexiglass Plates Clamp Piece of Capsule Wall
b)
Capsule Metal Plate
Metal Plate
Plexiglass with Strain Gauge
immmmimmmn.
Hand Crank
I'i-x-l'i-iji-i-x-w
Metal Spindle
FIGURE 3. Techniques used t o compare t h e s t r e n g t h o f egg c a p s u l e s : a) p u n c t u r i n g method used t o c a l c u l a t e t h e f o r c e r e q u i r e d t o p i e r c e c a p s u l e w a l l s , and b) s q u e e z i n g method used t o determine t h e r e s i s t a n c e o f i n t a c t capsules t o squeezing f o r c e s .
22 RESULTS.
I . DIFFERENCES I N SNAIL MORPHOLOGY AMONG
SITES
The s i z e a n d s h a p e o f s n a i l s d i f f e r e d e x t e n s i v e l y study
sites
Island,
( F i g . 4 ) . N u c e l l a emarginata from Seppings
t h e most w a v e - e x p o s e d a r e a , h a d t h e s m a l l e s t mean
(X=1.9cm) a n d t h e l o w e s t (X / +S.D.=1.42+0.05). L
among
length/aperture Snails
A
collected
size
ratio from t h e l e s s exposed
Ross I s l e t s s i t e had a g r e a t e r range o f s h e l l l e n g t h s , a larger
mean s i z e ,
length/aperture
(X=2.1cm),
r a t i o s than s n a i l s
(X / +S.D.=l.53+0.07). L
and p r o p o r t i o n a l l y from Seppings
Wave-sheltered s n a i l s
A
larger
from Grappler
I n l e t were i n t e r m e d i a t e i n body shape between S e p p i n g s and Ross I s l e t s s n a i l s shell
(X / +S.D.=1.49+0.06), b u t h a d t h e l a r g e s t L
A
lengths of a l l three populations
differences
w i t h wave-exposure, w i t h s h e l l
from wave-exposed t o w a v e - s h e l t e r e d
Changes i n l e n g t h / a p e r t u r e to not
Islet
II.
size
shores.
r a t i o s among s i t e s d i d n o t a p p e a r
r e f l e c t changes i n wave-exposure, as G r a p p l e r follow
These
i n t h e a v e r a g e s h e l l l e n g t h o f s n a i l s showed a n
obvious r e l a t i o n s h i p increasing
(X=2.7cm).
snails did
t h e same t r e n d i n b o d y s h a p e a s S e p p i n g s a n d R o s s
snails.
CAPSULE MORPHOLOGY 1• R e l a t i o n s h i p b e t w e e n s n a i l s i z e a n d c a p s u l e F i g u r e 5 shows t h e r e l a t i o n s h i p
snail
shell-length
population larger
within
size
between c a p s u l e
a n d among p o p u l a t i o n s .
s i z e and
Within each
females produced s i g n i f i c a n t l y l o n g e r egg
23 16S E P P I N G S ISLAND 12-
8-
4-
R O S S ISLETS 12>
Z3 o LL)
h n G R A P P L E R INLET 12-
4-
m h 1.0
1.5
2.0
2.5
3.0
3.5
4.0
SNAIL LENGTH ( c m )
FIGURE 4. S i z e - f r e q u e n c y histograms o f 50 s n a i l s c o l l e c t e d from each study s i t e i n March, 1988. S n a i l s s m a l l e r than 10 mm i n s h e l l l e n g t h were not included. Wave-exposure l e v e l s i n c r e a s e d from G r a p p l e r I n l e t t o Seppings Island. The mean s h e l l l e n g t h s o f s n a i l s were: 1.9, 2.1 and 2.7 cm f o r Seppings, Ross I s l e t s , and G r a p p l e r I n l e t s n a i l s , r e s p e c t i v e l y .
24
SNAIL LENGTH ( c m )
FIGURE 5. R e l a t i o n s h i p between c a p s u l e body l e n g t h and s n a i l l e n g t h f o r l a b o r a t o r y l a i d c a p s u l e s f o r each study s i t e . S n a i l s s m a l l e r than 1.7, 2.1 and 2.7 cm from Seppings, Ross I s l e t s and G r a p p l e r p o p u l a t i o n s d i d not spawn i n t h e l a b o r a t o r y . R e g r e s s i o n e q u a t i o n s f o r each s i t e a r e : Seppings: Y = 3.185X - 0.111, r =0.740, n = 23; Ross I s l e t s : Y = 3.139X - 1.232, r = 0.867, n = 23; G r a p p l e r I n l e t : Y = 2.206 + 1.481, r = 0.650, n = 20.
25 capsules
than s m a l l e r females.
r e l a t i o n s h i p s d i d not v a r y
The
slopes of
significantly
among s i t e s
f o r s l o p e s ; F=1.20, p > 0 . 2 5 ) , h o w e v e r , s l o p e d i f f e r e d s i g n i f i c a n t l y between the populations
these
elevations
S e p p i n g s and
Ross
Islets
(ANCOVA f o r e l e v a t i o n s ; F=14.84, p < 0 . 0 0 1 ) ,
Seppings s n a i l s producing
disproportionately large
S u b s t a n t i a l d i f f e r e n c e s were a l s o e v i d e n t spawning s n a i l s
i n the
Although
overlapped
i n s i z e range
1.4-2.9cm; G r a p p l e r :
l a b o r a t o r y w e r e 1.7,
l e n g t h f o r Seppings, Ross I s l e t s ,
populations,
respectively.
This
Islets:
range i n s i z e of
females from each p o p u l a t i o n b a r e l y c o i n c i d e d . s n a i l s t o spawn i n t h e
greatly
1.4-2.2cm; R o s s
1.8-3.5cm), t h e
of
as shown i n
laboratory snail populations (Seppings:
with
capsules.
size
from each l a b o r a t o r y p o p u l a t i o n ,
F i g u r e 5.
shell
(ANCOVA
The
2.1,
and
smallest
and
2.7
cm
in
Grappler
suggests t h a t the
r e p r o d u c t i v e m a t u r i t y v a r i e d among s i t e s ,
spawning
onset
of
w i t h wave-exposed
s n a i l s m a t u r i n g a t a much s m a l l e r s i z e t h a n
wave-sheltered
snails. Snail
s i z e was
d i m e n s i o n s , as
also r e f l e c t e d i n other
l a r g e r s n a i l s produced capsules
chamber v o l u m e s t h a n s m a l l e r s n a i l s among s i t e s
capsular
showed t h a t , a l t h o u g h
r e l a t i o n s h i p s d i d not
differ
F=0.57, p > 0 . 2 5 ) , S e p p i n g s and
(Fig. 6).
the
greater
Comparisons
slopes of
significantly
with
these
(ANCOVA f o r s l o p e s ;
Ross I s l e t s s n a i l s l a i d
w i t h l a r g e r chamber v o l u m e s t h a n s i m i l a r - s i z e d s n a i l s Grappler
Inlet
(ANCOVA; F=5.56, p < 0 . 0 1 ) .
As
( S p i g h t and
from
chamber v o l u m e s
a r e known t o r e f l e c t t h e number o f e g g s c o n t a i n e d capsules
capsules
within
Emlen, 1976), such d i f f e r e n c e s i n
the
capsule
26
SNAIL LENGTH ( c m )
FIGURE 6. R e l a t i o n s h i p between capsule-chamber volume and s n a i l l e n g t h f o r l a b o r a t o r y p o p u l a t i o n s e s t a b l i s h e d from each study s i t e . Regression e q u a t i o n s f o r each s i t e a r e : Seppings: Y = 18.245X - 15.257, r = 0.628, n = 23; Ross I s l e t s : Y = 28.193X - 41.722, r = 0.749, n = 23; G r a p p l e r , Y = 24.006X - 37.710, r = 0.690, n = 20.
27 s i z e can
also i n d i c a t e important
of these
populations.
d i f f e r e n c e s i n the
2. M i c r o m o r p h o l o g y o f N u c e l l a e m a r g i n a t a egg The
m i c r o s t r u c t u r e o f IsL. e m a r g i n a t a egg
i n F i g u r e 7.
C a p s u l e w a l l s o f N. (L^, L2
three d i s c r e t e laminae s t r u c t u r e to the M a u g e l , 1984; capsule
(L2)/
wall.
This
as t h i s was lamina
( L 2 b ) , w h i c h was layers the
{l>2a
capsule
e g g s , and of the
a n c
L
T
^
e
chamber and
enclosed
( F i g . 7D).
3.
and of
middle capsule
The
lamina
(L3)
lamina
embryos,
i n the was
capsule,
s t e m and
region
actually composed o f
s t r u c t u r e of these
the
lined
nurse
apical
a p p e a r e d t o be
homogeneous t h r o u g h o u t t h e s e c t i o n s through
homogeneous
capsule
as
i s shown
capsular-plug
( F i g . 7C,D).
Serial
s e c t i o n s along the
in wall thickness. capsule
chamber o f N u c e l l a
e m a r g i n a t a showed c o n s i d e r a b l e v a r i a t i o n
thickest
(Sullivan
from the
transparent,
Sections
p l u g and
Intracapsular variation
(Fig.8).
in
A l l measurements
developing
indicated that this
longitudinal
were s i m i l a r
innermost capsule
similar material
regions
and
solely
two
intracapsular fluid.
not
L3)
F i g . 7A,B).
s a n d w i c h e d by
capsule
by
and
the t h i c k e s t p a r t of the
connected to the
w a l l s was
i s shown
c o n s i s t e d a dense, f i b r o u s middle l a y e r
* 2c^ •
capsule
capsules
emarginata c o n s i s t e d of
w a l l t h i c k n e s s were t a k e n
lamina
capsules
capsule w a l l s of other muricids
D ' A s a r o , 1988;
fecundity
Within
individual
i n t h e p l u g and
capsules,
stem r e g i o n s
i n wall thickness
w a l l s tended to and
be
t h i n n e s t about
75%
a
FIGURE 7. M i c r o s t r u c t u r e o f N u c e l l a emarginata egg c a p s u l e s : a) t r a n s v e r s e s e c t i o n 70 % a l o n g t h e chamber o f a c a p s u l e from Ross I s l e t s (mean t h i c k n e s s = 60juun), b) t r a n s v e r s e s e c t i o n 70% a l o n g t h e chamber o f a c a p s u l e from G r a p p l e r I n l e t (mean t h i c k n e s s = 90^wm), c) l o n g i t u d i n a l s e c t i o n through t h e stem r e g i o n o f a N^. emarginata c a p s u l e , d) l o n g i t u d i n a l s e c t i o n t h r o u g h t h e plug r e g i o n of a e m a r g i n a t a c a p s u l e . O u t e r ( L ^ ) , middle (I^) and i n n e r ( L 3 ) c a p s u l e w a l l laminae a r e i n d i c a t e d , as a r e t h e t h r e e component l a y e r s (l>2a, 2 b , 2 c ^ °^ n^-ddle lamina. The c a p s u l e p l u g (P) and stem (St) a r e a l s o shown. L
L
t
h
e
29
180
40 -I 0
1
1
1
1
1
10
20
30
40
50
1 —
60
1
— i
70
POSITION A L O N G C A P S U L E C H A M B E R
1
80
1
90
100
{%)
FIGURE 8. V a r i a t i o n i n w a l l t h i c k n e s s a l o n g the c a p s u l e chamber of f i e l d c o l l e c t e d N u c e l l a emarginata c a p s u l e s from G r a p p l e r I n l e t , Ross I s l e t s , and Seppings I s l a n d . Values are e x p r e s s e d as X + 1 S.E. f o r n = 8 c a p s u l e s from each p o p u l a t i o n .
30 a l o n g t h e c a p s u l e chamber.
Although
changes i n c a p s u l e
width
a l s o o c c u r r e d a l o n g t h e l e n g t h o f t h e chamber, t h e s e d i d n o t appear t o correspond
with variation i n wall thickness
Sections through emarginata
capsules
among t h e G r a p p l e r populations. 70%
the w a l l s of f i e l d - c o l l e c t e d N u c e l l a
revealed obvious Inlet,
differences i n thickness
Ross I s l e t s ,
and
Seppings I s l a n d
Comparisons of w a l l t h i c k n e s s data
from a p o i n t
a l o n g t h e chamber chamber i n d i c a t e d t h a t c a p s u l e s
Ross I s l e t s were s i g n i f i c a n t l y t h i n n e r t h a n c a p s u l e s S e p p i n g s and
Grappler
(means o f 61,
ANOVA: F=29.9, p
1+ ON
oi J3 p 03Ul 01
Ml
3
C A P S U L E CHAMBER INTACT Total * of Capsules
Contained Embryos
55(22)
255
88(35)
19
13 (68)
167
43(26)
75(45)
140
26(19)
187
(1.8 m)
MID (2.3 m)
LOW
(1.2 m)
HIGH (2.0 m)
u a LOW INTERTIDAL BOULDERS (1.2 m)
LOW
ROSS ISLETS
Contained Ova
HIGH (2.6 in) ROCKY OUTCROPPING (2.8-3.1 m)
-
C A P S U L E CHAMBER OPENED Hatched Naturally
Opened by Predators
55(22)
47(18)
-
CATEGORIZATION
Hemigrapsus Idotea Predation Predation
2 (4)
20 (43)
OF CAPSULAR
REMAINS
Mopalia Bevelled Predation Holes
1 (2)
8 ( 17)
Misc. Predation
16 (34)
6(32)
6(100)
2(1)
43(26)
36 ( 84)
86 (61)
-
24(17)
22(92)
-
-
2(8)
52 (28)
83(44)
-
20(11)
14(70)
-
-
4(20)
37
17(46)
2(5)
-
-
139
27(19)
18(13)
10
1117
10(100)
2(0)
2(10)
9(24)
9(24)
9(100)
63(45)
31(22)
24 ( 77)
-
-
-
-
1 (2)
-
_
_
_
_
_
_
75(7)
779(70)
242(22)
177(73)
-
-
-
.
1(0)
6 ( 14)
7(23)
_
64(26)
78 drill
holes i n other gastropod The
d e n s i t y of s n a i l s
h i g h t r a n s e c t at Grappler capsule predators
The
Idotea
i n the
percentage
c a p s u l e s was
(Table I I ) .
transect.
the
In c o n t r a s t ,
egg
were n o t a b l y intertidal
o f c a p s u l e s opened i n t h i s showing evidence
region
was
of predation
I I I a l s o shows t h e e x t e n t o f p r e d a t i o n on along the lower
I d o t e a were o f t e n found
a p p e a r e d t o be
capsules
intertidal
amongst t o r n egg
capsules
responsible f o r the m a j o r i t y of predation
capsules.
The
percentage
o f c a p s u l e s opened
p r e d a t o r s r a n g e d f r o m 17 - 26 % on two a l t h o u g h t h e y were l e s s t h a n boulder,
1983).
low a l o n g
Idotea)
lower p a r t s of the
c o l l e c t e d from t h r e e b o u l d e r s
on t h e s e
(Abe,
(Table I I I ) .
Table
and
egg
Inlet
h i g h , w i t h a l l chewed c a p s u l e s by
capsules
( e g . H e m i g r a p s u s and
more a b u n d a n t t h a n channel.
and
egg
approximately
0.5
of the
m apart.
On
by
boulders, the
third
10 m away, o n l y 1 1 % o f c a p s u l e s
had
been opened.
2. R o s s
Islets
Densities of snails
and
egg
capsules varied
among t r a n s e c t s a t t h e R o s s I s l e t s capsules at t h i s overhangs.
The
(Table I I ) . A l l
s i t e were a t t a c h e d t o v e r t i c a l
surfaces
or
e x t e n t o f p r e d a t i o n on c a p s u l e s d e c r e a s e d
i n c r e a s e d t i d a l h e i g h t , and o f H e m i g r a p s u s nudus
corresponded
(0.6 - 2.4
cm
o n l y known p r e d a t o r s o f N u c e l l a egg Although
site
markedly
c r a b s were not p r e s e n t
when c e n s u s e s w e r e t a k e n ,
with
w e l l w i t h the d e n s i t y
i n carapace
width),
capsules at t h i s
the
site.
along the higher t r a n s e c t s
on s u b s e q u e n t v i s i t s c r a b s
were
79 occasionally transects.
found The
i n s m a l l c r e v i c e s a l o n g t h e 2.3
m a j o r i t y o f o p e n e d egg
h a v e b e e n e a t e n by H e m i g r a p s u s s p p .
and
2.6m
capsules appeared t o
(Table I I I ) .
Only
3
c a p s u l e s had b i t e marks s i m i l a r t o t h o s e a s s o c i a t e d w i t h I d o t e a , and study
o n l y one
o f t h e s e i s o p o d s was
ever
found
i n the
area. Censuses of the h i g h i n t e r t i d a l
Islets
i n A u g u s t 1988
o u t c r o p p i n g a t Ross
a l s o i n d i c a t e d t h a t Hemigrapsus
were i m p o r t a n t p r e d a t o r s .
O v e r 22%
of these capsules
spp. appeared
t o h a v e b e e n o p e n e d by p r e d a t o r s , w i t h t h e m a j o r i t y s h o w i n g evidence
3.
o f a t t a c k by
Seppings Egg
Hemigrapsus.
Island
c a p s u l e s from
bite-marks
by b o t h
Seppings
I s l a n d showed e v i d e n c e
I d o t e a and H e m i g r a p s u s .
g r e a t e r l e v e l s o f wave a c t i o n a t t h i s wosnesenskii
site,
Despite
the
Idotea
and H e m i g r a p s u s n u d u s w e r e a b u n d a n t ,
w i t h i n t h e t h i c k beds o f M y t i l u s c a l i f o r n i a n u s .
especially Capsules
a l s o found w i t h b e v e l l e d holes i d e n t i c a l t o those from G r a p p l e r I n l e t
(Fig. 3). to
24%
o f egg
capsules present at the Grappler I n l e t
Ross I s l e t s
sites,
respectively.
Observations
remains i n d i c a t e d t h a t the i n t e r t i d a l wosnesenskii), crabs gastropods
were
collected
I n summary, p r e d a t o r s w e r e f o u n d t o h a v e o p e n e d up 32% and
of
isopods,
and
of capsular (Idotea
( H e m i g r a p s u s o r e g o n e n s i s ) , and
unknown
were r e s p o n s i b l e f o r t h e m a j o r i t y o f p r e d a t i o n a t
G r a p p l e r I n l e t , whereas c r a b s ,
(Hemigrapsus nudus),
o n l y numerous p r e d a t o r s a t t h e R o s s I s l e t s
site.
were t h e
80
III. 1.
F I E L D EXPERIMENTS Grappler
Inlet
a) P i l o t
experiments
Capsules 19 days.
were l e f t w i t h i n
Over t h i s
n = 2 5 c a g e s ) and t h e l o w and possible
frameless cages f o r a p e r i o d of
p e r i o d a mean o f 2 . 0 + 0 . 3
1.8 ±
0.3 c a p s u l e s
h i g h i n t e r t i d a l cages,
8 capsules/cage).
The
respectively
I
T
H
I
N
= 0.73,
t r a n s e c t : ANOVA; F p>0.10).
w i t h cage
(n=50) over c a p s u l e s was
detached
T
due
Table
I
=
N
a two
day
1.53,
p>0.25;
period.
p>0.10;
FJ^JQNG
=
of the
in total
Although
unknown, I s u s p e c t e d
to a failure
high
2.17,
constant
at
from a l l
the cause
crabs
1 9 days.
of
t h a t c a p s u l e s became
glue.
I V shows t h e t y p e o f c a p s u l a r r e m a i n s f o u n d
shore
responsible
A l o n g the low
(Hemigrapsus oregonensis)
i n the
intertidal appeared t o
be
f o r t h e m a j o r i t y o f p r e d a t i o n ; h o w e v e r , i n some
c a s e s t h e p r e d a t o r s o f egg Along
1.34,
c a p s u l e s were " l o s t "
f r a m e l e s s cages a f t e r transect
H
=
position
level.
A mean o f 6.1
lost
I
F^QJJQ
by
(low t r a n s e c t :
Hence, p r e d a t i o n l e v e l s were r e l a t i v e l y
each t i d a l
cages
W
p>0.25;
(out o f a
number o f c a p s u l e s o p e n e d
w i t h i n o r among b l o c k s a l o n g e a c h t r a n s e c t W
1S.E.,
(n=25 cages) were opened i n
p r e d a t o r s d i d not d i f f e r s i g n i f i c a n t l y
ANOVA; F
(X +
c a p s u l e s c o u l d n o t be
the higher i n t e r t i d a l t r a n s e c t , isopods
identified.
(Idotea)
were
t h e c h i e f p r e d a t o r s and w e r e f r e q u e n t l y f o u n d e a t i n g c a p s u l e s . F e w e r c a p s u l e s w e r e o p e n e d by H e m i g r a p s u s o r e g o n e n s i s d r i l l e d by
other predators i n t h i s
region.
or
TABLE IV. Summary o f N u c e l l a emarginata egg c a p s u l e s opened by p r e d a t o r s i n the p i l o t experiment i n G r a p p l e r I n l e t , June 1988. Capsules were c l a s s i f i e d by the b i t e and chew marks l e f t on t h e c a p s u l a r chamber.
CHARACTERISTICS Hemigrapsus Chew Marks
LOW
TRANSECT
(1.2
HIGH
(2.0
m)
Bevelled Holes
REMAINS
Mopalia rasping
Misc. Predation
Total # Eaten
17
-
14
1
19
51
4
22
2
-
16
44
m)
TRANSECT
Idotea Chew Marks
OF CAPSULAR
82 b)
Predator-exclusion
experiments
P r e d a t o r - e x c l u s i o n experiments predators t h e 2.25 The
revealed that the
of capsules at the Grappler cm
s i t e were l a r g e r
e n t r y h o l e s of the l a r g e - h o l e cages
2
major than
( F i g . 4a,b).
number o f c a p s u l e s o p e n e d a f t e r 20 d a y s v a r i e d
significantly
among c a g e t y p e s
( K r u s k a l - W a l l i s One-Way ANOVA:
l o w t r a n s e c t , K=10.41, P
