Download 07 JMS 329-341 Ansell

DYNAMICS OF AGGREGATIONS OF A GASTROPOD
PREDATOR/SCAVENGER ON A NEW ZEALAND HARBOUR BEACH
ALAN D. ANSELL*
Scottish Association for Marine Science, PO Box 3, Oban PA34 4AD, Argyll, UK
(Received 25 August 2000; accepted 25 January 2001)
ABSTRACT
Observations of a New Zealand harbour beach revealed that aggregative feeding behaviour was common in the buccinid gastropod Cominella glandiformis (Reeve, 1847). The majority of such aggregations
are associated with either the tellinid bivalve Macomona liliana (Iredale, 1915) or the venerid cockle
Austrovenus stutchburyi (Wood, 1828). Marking experiments indicate that aggregations persist for one
tidal cycle. This information, together with the density of aggregations associated with each ‘prey’
species allows the calculation of rate of predation by Cominella glandiformis and of the mortality of
M. liliana and A. stutchburyi at different stations on the beach. Averaged over spring periods, when predation and mortality are reduced, and summer, the calculated rates suggest that between 2 to 16% of
M. liliana and 3 to 9% of A. stutchburyi fall prey to Cominella each year. The majority of bivalves at the
centre of aggregations appeared to be tightly shut and undamaged, suggesting that the gastropods are
predators attacking live prey, although late arrivals may be attracted as scavengers by leaking body
fluids. Aggregated feeding may provide the gastropod with both competitive and metabolic benefits.
INTRODUCTION
The buccinid gastropod Cominella glandiformis
(Reeve, 1847) is an abundant member of the fauna of
sheltered harbour beaches in New Zealand, appearing
either as solitary individuals or in aggregations of tens
or sometimes hundreds. Morton & Miller (1968)
described C. glandiformis as the universal scavenger of
mudflats which ‘converge in scores on dead animal
remains, and may also be active carnivores, thrusting
the long proboscis through the narrow siphonal
fissures of Chione and other bivalves’. The short term
dynamics of C. glandiformis aggregations on the shore,
and the nature of the relationships between C. glandiformis and the bivalves with which aggregations are
most often associated, have not previously been studied. It is interesting to establish whether these aggregations are scavenging or preying on the animal around
which they are all assembled. This paper attempts such
a study on Cominella aggregations on a typical harbour
beach in the North Island of New Zealand.
MATERIAL AND METHODS
Study location
The study was carried out on the beach at Matua, within
Tauranga Harbour, a large natural harbour inlet on the east
* Sadly Alan Ansell died in 1999 before this paper was completed. The
manuscript was completed by Drs M. Barnes and E.M. Harper and Mrs L.
Robb.
J. Moll. Stud. (2001), 67, 329–341
coast of the North Island of New Zealand (Fig. 1). At this
location, protective gabions restrict the upper intertidal zone
so that the area exposed at low tide lies between low water (of
spring or neap tides) and a little below high water of neap
tides. At its seaward edge, the intertidal region is bounded by
the deeper water channel draining the Wairoa River. The
topography of the shore shows slight seasonal changes
depending on deposition and erosion from localized channels
and sand banks.
Observations were carried out over two periods: in summer, 4–13 February 1998; and in spring, 5 September–5
October 1998. At low water of spring tides during the summer period, the exposed intertidal area that was accessible
comprised an outer sand bar bordering the channel, separated by a shallow trough from an inner sand bar which in
turn was separated from a final shallow-sloping inshore area
of muddier sand by a second trough. Much of this inner
trough, which drained at low tide apart from some residual
shallow pools, supported a relatively strong growth of eelgrass (Zostera sp.) and consequently the sediment was muddier and wetter than that of the bars on the upper intertidal
area. The outer trough retained a shallow flow of water at low
tide and had an abundant mix of shell debris with some
attached growth of algal sporelings. The overall extent of the
intertidal was about 250 m, of which the inshore flat and inner
and outer bars each comprised some 70 m. This situation
remained largely unchanged during the spring period apart
from some deepening of the inner trough. The inshore flat
and inner and outer bars remained as consistent fairly uniform areas. On each tide the inshore flat remained immersed
for 7 h and the inner and outer bars for up to 9h. Tides in
Tauranga Harbour are semi-diurnal with a vertical extent of
about 1.9 m at spring tides. Details of physical conditions
within the Harbour are given by Park & Donald (1994).
© The Malacological Society of London 2001
ALAN D. ANSELL
Figure 1. Location of Matua beach within Tauranga Harbour, New Zealand.
The intertidal fauna was typical of North Island protected
harbour beaches as described by Morton & Miller (1968) and
other authors (e.g. Grange, 1977). The dominant large
bivalves present were the tellinid Macomona liliana (Iredale,
1915) and the venerid cockle Austrovenus stutchburyi (Wood,
1828). The crabs Helice crassa Dana, 1851, Macrophthalmus
hirtipes (Heller, 1862) and Hemigrapsus crenulatus Milne
Edwards, 1837 were common in the muddier areas of the
upper beach and troughs. The last was less common in the
more loosely compacted and well sorted sand of the bars.
The gastropod Zeacumantus lutulentus (Kiener, 1841) was
abundant on the surface of the upper beach. At all levels,
aggregations of Cominella glandiformis were a distinctive
feature of the intertidal fauna, especially during the summer
period, usually associated with intact or partially or completely consumed Macomona liliana or Austrovenus stutchburyi.
Field methods
The observations made aimed to determine the distribution
of aggregations and solitary individuals of Cominella glandiformis and of the larger bivalves with which they are
commonly associated, and to examine the nature of the
relationship between them. Observations were made at three
stations: 1) on the crest and nearshore slope of the outer sand
bar, 2) on the crest and nearshore slope of the inner sand bar,
and 3) on the inshore flat for each of the seasons (Table 1).
The density of aggregations of C. glandiformis was determined by counting within replicate marked areas of between
25 and 200 m2 depending on the perceived density. At each
station, the density of large Macomona liliana and Austrovenus stutchburyi, and of individual C. glandiformis was
determined by sieving five replicate 0.5-m2 samples through a
0.95-cm mesh sieve. To avoid changes in distributions
around this sampling influencing other results, quantitative
benthic sampling was not carried out until other observations
were completed in each period. The size distributions of
Macomona liliana and Austrovenus stutchburyi present at
each site were determined by measuring animals from the
benthic samples. Representative groups were also weighed to
provide biomass estimates. Individuals over the entire size
range represented from the spring benthic sampling were
used to provide relationships between ash-free dry weight of
tissue (AFDW) and shell length (L) or height (H) for each
species (Equations 1, 2, 3).
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GASTROPOD AGGREGATIONS
Table 1. Characteristics of the stations sampled at Matua beach, Tauranga Harbour.
*Figures in parentheses show number of replicates.
**Figures in parentheses show mean density where there was no significant difference between summer and spring
numbers.
CD = Chart Datum.
Inshore flat
Depth versus CD (m)
Time immersed (h)
Sea-water temp. (C)
Summer
Spring
7.0
23–25
0.75
7.0
13–14
Density (No.m–2)
Cominella aggregates*
0.005 (4)
Cominella individuals** 20[14]
Macomona **
178
Austrovenus **
372 [320]
For Macomona liliana:
log AFDW 2.99 log L–2.27
For Austrovenus stutchburyi:
log AFDW 2.62 log L–1.80
For Cominella glandiformis:
log AFDW 2.89 log H–1.96
Inner bar
Summer
7.0
0.035 (5)
8
54
268
0.156 (20)
22 [13]
164 [175]
248 [389]
Equation 1
Equation 2
Equation 3
Aggregations were sampled at each station and the following information was recorded: the number of Cominella
glandiformis present, their size distribution, and the identity
of the ‘prey’ organism present in each case. The persistence
of individual aggregations was monitored through the lowand high-water periods, by marking them with canes inserted
a short distance shoreward of the group to prevent interference by floating algae that became trapped by the markers.
Aggregations were marked on ebbing tides, or at low tide,
and revisited as the tide rose and during the subsequent low
tide period where possible. Further information on the
dynamics of aggregation was obtained by exposing damaged
and undamaged Macomona liliana and Austrovenus stutchburyi on the surface of the inshore flat or in the inner trough
during the ebb tide and examining the rates of aggregation
and disaggregation of Cominella glandiformis attracted to
them.
Data from these studies was used to calculate the predation
rate by C. glandiformis and the equivalent mortality rates
of Macomona liliana and Austrovenus stutchburyi at each
station during each period.
RESULTS
Density of solitary and aggregated gastropods and
of bivalves
During the summer period the density of Cominella
glandiformis aggregations differed markedly among
Outer bar
Spring
0.75
7.0
0.013 (5)
4
186
530
Summer
9.0
0.022 (7)
<1 [<1]
36 [42]
8 [6]
Spring
0.52
8.5
0 (5)
<1
48
4
the three stations with the greatest density on the inner
bar and the lowest on the inshore flat (Table 1, Fig. 2).
At this time, isolated individuals of C. glandiformis
were most abundant on the inshore flat and inner bar.
During the spring period the overall density of aggregations was much reduced except on the inshore flat
which at this time had the greatest density recorded at
any location or time. In spring isolated individuals
were seen on the sediment surface at all stations, with
the greatest density on the inshore flat.
The distributions and abundances of Macomona
liliana and Austrovenus stutchburyi were similar during
both the summer and spring experimental periods at all
sites except for the former taxon on the inshore flat
where the summer density was at least triple that
recorded in the spring. In all other cases the quantitative samples were combined to provide the mean data
given in Table 1. Comparing the distribution of the two
bivalve taxa, A. stutchburyi was more abundant than
M. liliana on the inshore flat and inner bar but less
abundant on the outer bar.
Size distributions of Macomona liliana and
Austrovenus stutchburyi
Figure 3 shows the distribution of the size classes (for
individuals of over 0.95 cm) of individuals of Maconoma liliana and Austrovenus stutchburyi for each of
the three study sites, with the exception of A. stutchburyi. Maconoma liliana from the outer bar had a
greater modal size than those from the inner bar and
inshore flat, whilst there were no differences among
stations in the modal sizes of A. stutchburyi from the
inner bar and the inshore flat. Using the biomass data
(Table 2), it was apparent that the greatest biomass of
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ALAN D. ANSELL
M. liliana was found on the inner bar and the lowest on
the outer bar in summer, whilst for A. stutchburyi the
greatest biomass was on the inshore flat and the lowest
on the outer bar in summer. In spring the greatest
biomass of both M. liliana and A. stutchburyi was on
the inner bar.
Composition of aggregations
Of those Cominella glandiformis that occurred in aggregations, in summer, on the inshore flat, more were
associated with Austrovenus stutchburyi than with
Macomona liliana; on the inner bar the numbers of
aggregations associated with each was about equal; on
Figure 2. Distribution of Cominella glandiformis (solitary and aggregated), Macomona liliana and Austrovenus stutchburyi at three sites on
Matua beach, Tauranga Harbour, New Zealand, in spring and summer. IF inshore flat, IB inner bar, OB outer bar.
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GASTROPOD AGGREGATIONS
the outer bar most aggregations were associated with
M. liliana (Table 3). In spring, most aggregations on
both the inshore flat and the inner bar were associated
with A. stutchburyi; on the outer bar the numbers of
aggregations associated with each was about equal. In
both summer and spring, the numbers of C. glandiformis per aggregation varied greatly both among
stations and depending on the ‘prey’ bivalve (Table 3).
Overall, the numbers in aggregations associated with
M. liliana were greater than those associated with A.
stutchburyi with the largest number in any one aggregation reaching 206. In some aggregations the ‘prey’
bivalve appeared to be undamaged; others showed all
stages of consumption to a completely empty shell. In
some cases the associated C. glandiformis had clearly
begun dispersing and were distributed at short distances in all directions around the empty shell valves.
The modal sizes of individuals of C. glandiformis associated with M. liliana were generally greater than those
associated with A. stutchburyi (Fig. 4).
Behaviour of Cominella glandiformis in
aggregations
In aggregations exposed at low tide, the gastropods
formed a loose group with the lower individuals buried,
especially in large aggregations, whilst many of those
on top were completely uncovered with dry shells.
Where aggregations could be observed in shallow water,
the gastropods were seen to change position frequently
around the ‘prey’ nucleus. Although it was difficult to
observe individuals without disturbance to the group,
but on many occasions the proboscis was seen to be
extended into the shell cavity of a tightly closed bivalve,
most frequently through the siphonal aperture of
Macomona liliana or through the dorsal commissure of
Austrovenus stutchburyi.
Persistence of aggregations
Re-examination of marked aggregations showed that,
in summer, at all stations, the aggregations persisted
throughout that period of low tide for which they were
accessible, but that in most cases the aggregations had
dispersed completely when revisited on the next low
tide. In spring a greater proportion of marked aggregations survived a single tidal cycle, but all had dispersed
before the second low tide period following marking,
indicating a slightly longer average persistence at this
time (Table 4).
Attraction to damaged and undamaged bivalves
Damaged Macomona liliana or Austrovenus stutchburyi
exposed in shallow water during the ebb tide or placed
on the wet surface of the inshore flat rapidly attracted
Cominella glandiformis from downstream (Fig. 5).
Generally, in excess of 20 gastropods reached the
bivalve ‘bait’ within 15 min of its exposure; the tissues
were consumed completely within 20 min for Austrovenus and between 20 and 35 min for Macomona
depending on the bivalve’s size. The gastropods then
dispersed rapidly. Intact bivalves (Macomona) placed
on the surface attracted very few or no Cominella
glandiformis and generally reburrowed.
Rates of predation by C. glandiformis and mortality
of Macomona liliana and Austrovenus stutchburyi
The observations made here on the persistence of
aggregations allow an estimate to be made of the minimum rate of mortality resulting from ‘predation’ by
Table 2. Biomass estimates for the bivalves Macomona liliana and Austrovenus stutchburyi on
Matua Beach, Tauranga Harbour.
Inshore flat
Summer
Macomona
no.m–2
mean wet weight (g)
total wet weight (g m–2)
Austrovenus
no.m–2
mean wet weight (g)
total wet weight (g m–2)
Total bivalves
wet weight (g m–2)
178
916
372
837
1753
Inner bar
Spring
54
5.14
278
268
2.25
603
881
Summer
Spring
Summer
Spring
164
186
5.68
1057
36
48
11.0
528
932
248
433
1365
333
Outer bar
530
1.75
926
1983
396
8
14
410
4
1.75
7
535
ALAN D. ANSELL
Cominella glandiformis. Aggregations present throughout the low tide period had dispersed in summer
following the subsequent high tide period of 7 or 9 h,
suggesting that the maximum time needed for aggrega-
tion followed by complete consumption of either
bivalve species is one tidal period. The minimum ‘predation’ rate (R no. ‘prey’. m–2 .day–1) may be calculated on this basis as: R Fagg 24/12.5 % species
Figure 3. Modal sizes of Macomona liliana and Austrovenus stutchburyi at three sites on Matua beach.
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GASTROPOD AGGREGATIONS
A/100, where Fagg is the number of C. glandiformis
aggregations m–2 and % species A is the percentage of
the total aggregations associated with prey species A.
Predation rates calculated on this basis (Table 5) indicate that in summer the highest rates of predation
occurred on the inner bar and affected both bivalve
species more or less equally. On the inshore flat in
summer, predation rates on Austrovenus stutchburyi
exceeded those on Macomona liliana while on the
outer bar the reverse was the case. In spring, predation
rates were generally much reduced except on the
inshore flat.
Figure 4. Size distribution and percentage of population of Cominella glandiformis associated with Macomona liliana, Austrovenus stutchburyi
and Mesodesma at three sites on Matua beach.
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ALAN D. ANSELL
Table 3. Percentage of all aggregations at each station associated with each type of ‘prey’ organism and mean numbers of gastropod in each type of aggregation. Range given in parenthesis.
Inshore flat
Summer
% with
Macomona
Austrovenus
Other
20.0
60.0
20.0
Inner bar
Spring
Summer
8.0
74.0
18.0
No. of Cominella per aggregation associated with
Macomona
9.0
42.2
(8.96)
Austrovenus
10.0
14.3
(8–13)
(2–38)
Outer bar
Spring
Summer
Spring
29.6
37.0
33.3
24.0
72.0
4.0
86.7
6.7
6.7
44.4
33.3
22.2
62.0
(6-206)
28.4
(13–50)
29.3
(8–100)
7.8
(2–29)
58.7
(13–175)
35.0
22.6
(5–66)
17.5
(5–28)
Table 4. Number of marked aggregations remaining after one or two tidal
periods at stations at Matua beach, Tauranga Harbour.
Inshore flat
Summer
No. marked
8
No. (%) remaining
after 1 tide
after 2 tides
0
0
Spring
Summer
Spring
23
28
47
3 (13%)
0
Mortality in the population expressed as the proportion of the bivalve population consumed day–1 was
greatest in summer on the outer bar. In spring, mortality was much reduced on the outer and inner bars,
but increased slightly on the inshore flat (Table 5). The
equivalent rates expressed on an annual basis are
summarized in Table 5. Averaged over spring and
summer, these rates suggest that between 2 to 16% of
M. liliana and 3 to 9% of Austrovenus fall prey to
Cominella each year at different stations on the beach.
These figures indicate that C. glandiformis is associated
with significant rates of natural mortality of both
bivalve species in this area.
DISCUSSION
Qualitatively, the fauna of the Matua intertidal zone
conforms closely to the description of New Zealand
harbour flats given by Morton & Miller (1968) with the
larger macrofauna being dominated by the two burrowing bivalves Macomona liliana and Austrovenus
stutchburyi. Quantitatively, there is little published
Inner bar
1 (3.6%)
0
12 (25.5%)
0
information on population density of these species
with which to compare the data obtained herein. However, Park & Donald (1994) give data for many sites
around Tauranga Harbour and Hewitt, Thrush, Cummings & Pridmore (1996) for Manukau Harbour,
which suggest that densities of adult bivalves are of the
same order as those found at Matua. Both species were
found throughout the exposed intertidal zone, but at
different densities, both being progressively less abundant from the inshore flat to the inner and outer bars
with the density of Austrovenus stutchburyi showing a
greater decrease than that of M. liliana. A. stutchburyi
is a suspension feeder that burrows only superficially.
This is reflected in the high proportion of individuals
that bear epizoans (chiefly the anemone Anthopleura
aureoradiata Stuckey, 1909, the spionid worm Boccardia acus (Rainer, 1973), the barnacle Elminius modestus
Darwin, 1854 and the limpet Notoacmea helmsi (Smith,
1894) on the posterior region of the shell. One result of
this shallow burrowing habit is that individuals may be
readily exhumed during strong tides (which particularly affect the outer sand bar) leaving them exposed
to epifaunal predators. One unresolved question
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GASTROPOD AGGREGATIONS
regarding the relationship between A. stutchburyi and
Cominella glandiformis is whether gastropods also feed
on all or any of these regular epizoans associated with
this species. The deposit feeding M. liliana, by contrast
to A. stutchburyi, occupies burrows of up to 10 cm
depth and is thus less likely to be exposed by strong
tidal currents.
The exact nature of the relationship between
Cominella glandiformis and these bivalves is difficult to
define. Field observations of individuals of C. glandiformis feeding on dead crabs, and the willingness of
others to attack damaged bivalves in these experiments
show that they are at least facultative scavengers. However, the predominance of bivalves with undamaged
shells at the core of the aggregations, the frequency of
aggregations around still apparently tightly closed
Figure 5. Aggregation and dispersion time of Cominella glandiformis around damaged and undamaged bivalve ‘bait’. Macomona, damaged—
series 1, 2, 3; Macomona, undamaged—series 4; Austrovenus, damaged—series 5,6. Arrow heads indicate dispersion after all bait consumed.
Table 5. Estimates of the mortality rates (% of population day–1) of Macomona liliana and Austrovenus stutchburyi from ‘predation’ by Cominella glandiformis, and of predation rates (no.eaten
day–1m–2) by C. glandiformis on Macomona liliana and Austrovenus stutchburyi at Matua beach,
Tauranga Harbour.
Inshore flat
Inner bar
Outer bar
Summer
Spring
Summer
Spring
Summer
Spring
% Mortality
Macomona
Austrovenus
0.0017
0.0018
0.0100
0.0155
0.0507
0.0285
0.0015
0.0046
0.0880
0.0476
0.0009
0.0044
Predation rate
Macomona
Austrovenus
0.0019
0.0058
0.0054
0.0497
0.0887
0.1108
0.0060
0.0180
0.0366
0.0028
0.0004
0.0000
Equivalent annual % mortality
Macomona
0.6205
Austrovenus
0.6570
3.6500
5.6575
18.5055
10.4025
0.5475
1.6790
32.1200
17.3740
0.3285
1.6060
Average annual mortality
Macomona
Austrovenus
2.1353
3.1423
9.5265
6.0408
337
16.2243
9.49
ALAN D. ANSELL
bivalves, and the observation of the gastropod proboscis extended into the mantle cavity of the bivalve
through the slight siphonal gape (Macomona) or
through the dorsal commissure (Austrovenus) all point
to a predator-prey relationship, although it is probable
that as flesh is progressively removed, leaking body
fluids may attract scavenging individuals. Despite
reports of drilling behaviour by Cominella (Peterson &
Black, 1995), no indication of drilling predation by
Cominella glandiformis was found in Tauranga Harbour (Ansell, 2000). The ability to both scavenge and
actively predate suggest that C. glandiformis is an
opportunist feeder.
Two factors suggest that the rates of predation and
their impact on the bivalve populations as calculated
here might underestimate the actual rates. First, the
observation of the rate at which C. glandiformis is
attracted to damaged bivalves and their subsequent
dispersal following consumption of the soft tissues
show that aggregation, consumption and dispersal can
take place in a much shorter time (1 h) than the 7–9 h
for which the intertidal stations were immersed. Morton & Britton (1991) made similar observations for
Cominella eburnea (Reeve, 1846) and C. tasmanica
(Tenison Woods, 1878) on Australian beaches. This
would imply that aggregation, consumption and dispersal could occur repeatedly through the high tide
period, greatly increasing the estimated predation
impact, although attractive cues may be difficult to
follow on a rising or high tide which might lessen this
effect (J.C. Britton, personal communication). A similar problem has been noted in assessing the diets of
other intertidal predatory gastropods by Fairweather
& Underwood (1983). In this study, natural aggregations were rarely associated with damaged bivalves;
many bivalves appeared intact and were still firmly
adducted, but proved on examination to have been
partially consumed. It is reasonable, therefore, to conclude that aggregation around and consumption of
intact bivalves takes place much more slowly than is
the case with damaged bivalves. This view is supported
by observations made by P. Smythe & R. Black
(unpublished observations) for the Australian species
C. eburnea. They measured times needed to ‘infiltrate’
and consume the bivalve Katelysia scalarina Lamarck,
1818 in aquaria of 13 h 8.5, 22.2 h 6.9 and 24 h for
20 mm, 15 mm and 10 mm Cominella eburnea, respectively. Secondly, the size of the bivalve may affect the
time taken for complete consumption to occur following aggregation. Consumption of Macomona liliana,
which are generally larger than Austrovenus stutchburyi, especially on the outer bar, might then be expected to take longer although this may be offset by the
generally larger numbers of Cominella glandiformis
found in aggregations around the former (Table 3) and
their larger size (Fig.4). However, the fact that some
aggregations remain intact on the shore at the next low
tide, indicating a time for completion of 12.5 h, especially in spring, implies a lower mortality rate than that
calculated.
Although the aggregations of Cominella glandiformis
are a conspicuous feature especially during the summer, they represent only a small proportion of the total
population of the gastropod present over much of the
intertidal, the exception being the outer sand bar.
Aggregations accounted for only some 0.27% of the
total over the inner flat in summer (Table 6), for some
22.4% of the total on the inner sand bar, but almost
100% of the total on the outer sand bar, where solitary
individuals were not found in the quantitative benthic
samples, but were seen on the sand surface or partly
buried, during the low tide period. It follows that for
most of the time C. glandiformis on the inshore flat are
not aggregated while those of the inner bar are aggregated for some 3% of the time. It is difficult to account
for these differences unless it is assumed that alternative, presumably smaller, items of prey that do not
involve aggregated feeding, are more important in the
inner bar and inshore flat areas.
Morton & Britton (1991) calculated the area from
which C. eburnea were attracted to prey on Australian
beaches as: Area Mean no. Cominella per aggregation / mean density of solitary Cominella on the beach.
Perhaps more accurately such calculations should
include both solitary and aggregated Cominella density
(Table 6). Calculations for C. glandiformis yield similar
areas of attraction for this species on the inner bar
and inshore flat at Matua (Table 6). Observations in
shallow tide pools with weak residual tidal currents
indicate that C. glandiformis are attracted mainly from
the areas downstream of bait, often from considerable
distances ( 4m, pers. obs.).
The adaptive value of group feeding in vertebrates
(e.g. Bernard & Sibly, 1981) has been investigated more
than for various invertebrate taxa. Aggregated feeding
is a common phenomenon among scavengers (Britton
& Morton, 1994) including gastropod molluscs of the
families Nassariidae and Melongenidae where individuals are rapidly attracted to carrion, feed rapidly to
satiation and are replaced by other individuals until the
food resource is exhausted. The aggregated feeding by
Cominella glandiformis described herein seems to differ
fundamentally from this pattern since groups of
individuals are formed around live prey and remain
together for a more extended periods until the food
resource is exhausted before dispersing. Aggregative
338
GASTROPOD AGGREGATIONS
predation by muricid gastropods has been reported in
Nucella lapillus (Linnaeus, 1758) (Hughes & Dunkin,
1984), Stramonita haemastoma (Gray, 1839) (Brown
& Alexander, 1994) and Thais clavigera (Küster) and
T. luteostoma Holten, 1802 (Taylor & Morton, 1996).
In a detailed study specifically focussed on group feeding, Brown & Alexander (1994) found although a high
proportion (40–58%) of feeding S. haemostoma were
found in aggregations around large oysters in the field,
laboratory experiments showed that group feeding
decreased the flesh yield per capita and that there was
no decrease in prey handling time, although the overall
amount of prey tissue removed was greater in groups
than in solitary predators. They suggested that there
were no measurable costs to the individual involved in
feeding in groups on prey items with a flesh yield
greater than that required to satiate a single predator,
and, in any case, an individual had no means of defending its the prey from interlopers. They did suggest that
group feeding might provide a mechanism for feeding
on larger prey, however, their experiments demonstrated that single individuals were capable of overcoming and feeding on these items. Taylor & Morton
(1996) found that aggregations of T. clavigera and T.
luteostoma on a boulder shore in Hong Kong formed
around relatively small prey items and suggested that
group feeding, in this instance, might result from prey
shortage. It is possible that these arguments might apply
to the formation of aggregates of feeding C. glandiformis. Alternatively, aggregated predation may provide them with a number of definite advantages. First,
observations of the aggregation process show that,
when sufficient numbers of Cominella have reached a
damaged bivalve, other small scavengers such as the
crab Hemigrapsus crenulatus (Milne Edwards, 1837)
are excluded and prove unable to share the food avail-
able. Secondly, as a predation process, aggregation
presumably may allow the gastropod to overcome the
prey more quickly. Aggregated feeding allows a food
resource such as a large bivalve to be shared efficiently
between individuals, generally over a single tidal
period. Most predatory gastropods are limited in the
size of prey they can successfully attack as individuals.
Aggregated feeding allows C. glandiformis to escape
such a restriction and exploit large prey. A similar
strategy is adopted by some other invertebrate predators, e.g., the starfish Anasterias rupicola (Verrill, 1876)
feeding on the large limpet Nacella delesserti Hedley,
1916 at Marion Island (Blankley, 1984) and other
Anasterias species at McQuarie Island (Simpson,
1976). Perhaps the most spectacular recorded example
of aggregated feeding by a gastropod is that of the
South African whelk Burnupena sp. at Marcus Island
successfully attacking the rock lobster Jasus lalandii
Milne Edwards, 1837 (Barkai & McQuaid, 1988).
Barkai & McQuaid reported that each rock lobster was
killed within 15 min by more than 300 Burnupena that
removed all the flesh in less than 1h.
The quantitive aspects of aggregated feeding can be
examined in terms of the organic tissue available from
Macomona liliana or Austrovenus stutchburyi of different sizes (Equations 1and 2, Fig. 3), the organic content
of Cominella glandiformis of different sizes (Equation
3), and the nutritional requirements of individual
Cominella. Table 7 shows the number of C. glandiformis of mean size for each station that a single
Macomona liliana or Austrovenus stutchburyi of the
mean size for that station could provide with its daily
maintenance requirements, assuming a daily maintenance requirement of 3% of body weight (see Morton
& Britton, 1991). The numbers range from 67 to 208 for
Macomona liliana at different stations and from 22 to
Table 6. Calculation of apparent areas of attraction of Cominella glandiformis to ‘prey’
at Matua beach, Tauranga Harbour.
Inshore flat
Inner bar
Summer
Spring
Summer
Spring
Density Cominella
Aggr.m–2
Mean no.aggr–1
0.005
11.00
0.035
20.70
0.156
40.90
0.013
7.10
Total number of aggregated Cominella
Density solitary Cominella (no m–2)
0.055
20
0.725
8
6.380
22
0.085
4
Total Cominella (no m–2)
% aggregated Cominella
20.055
0.274
8.725
8.309
28.380
22.481
4.085
2.081
0.550
2.558
1.859
1.775
Area of attraction (m2)
339
ALAN D. ANSELL
Table 7. Calculation of the number of Colminella glandiformis of modal size supported by a
bivalve of modal size at stations on Matua beach, Tauranga Harbour, assuming a maintenance
requirement of 3% of body weight–1.
Inshore flat
Inner bar
Outer bar
Spring
Spring
Spring
17.5
28.6
17.5
28.6
–
–
32.5
178
37.5
273
47.5
554
Modal size Cominella associated with Austrovenus
mm shell height
12.5
mg AFDW
16.2
17.5
42.9
–
–
Modal size Cominella associated with Macomona
mm shell height
mg AFDW
22.5
88.7
22.5
88.7
22.5
88.7
Number of Cominella supported
by Austrovenus
by Macomona
59
67
Modal size Austrovenus
mm shell length
mg AFDW
Modal size Macomona
mm shell length
mg AFDW
59 for Austrovenus stutchburyi; numbers of the same
order as those actually found in the field.
Much remains to be learned about the dynamics and
other components of this process. For example, little is
known about how Cominella locate and eventually
attack ‘prey’, especially the deeper burrowing Macomona. Nothing is known of the sensory processes
involved in the early stages of formation of aggregations, especially since many aggregations can be found
that are centred on what appears to be an undamaged
bivalve. Possibly secretions of pheromones attract
other conspecifics to the aggregation even before the
release of possible attractants derived from damage to
the ‘prey’. The time involved in these processes remains
to be further examined.
Aggregated feeding intertidally by gastropods
appears to be a particular feature of Australasian
beaches. One factor allowing the build-up of gastropod
aggregations on these beaches may be the absence of
larger more aggressive scavengers. The crabs that are
present, for example, are all relatively small when
compared with the common shore crabs of European
beaches. Some Hemigrapsus crenulatus (Milne Edwards,
1837) were attracted to damaged bivalves exposed on
the shore, but the Cominella glandiformis soon formed
a compact mass that excluded these relatively small
crabs, indicating that the gastropods can outcompete
the crabs in exploiting even carrion. Few other preda-
22
103
–
208
tors of Macomona liliana and Austrovenus stutchburyi
have been reported. Thrush, Pridmore, Hewitt & Cummings (1991, 1994) report that birds and rays are
predators in Manukau Harbour, the former taking
mainly small bivalves such as newly-recruited Macomona and the latter larger bivalves. Pits caused by the
activities of rays were seen on the beach at Matua
during this study, especially during summer, and a
variety of birds are seasonally abundant. Gastropod
predation, however, seems to be a significant component of bivalve mortality.
ACKNOWLEDGEMENTS
I am grateful for the support of Drs Phillip and Janet Thwaite
and Dr Derry and Mrs Jenny Seddon who provided support
and access facilities to the beach at Matua for this study.
Sharon Capon (Cambridge Earth Sciences) kindly re-drafted
Figure 1 and Geoff Read gave helpful advice about the taxonomy of the New Zealand fauna. This paper is for Jamie
Thwaite who already shows a lively scientific curiosity for the
beach habitat.
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