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Coleman and Hockey 08
Austral Ecology (2008) 33, 232–240
Effects of an alien invertebrate species and wave action
on prey selection by African black oystercatchers
(Haematopus moquini)
R. A. COLEMAN1* AND P. A. R. HOCKEY2
1
School of Biological Sciences, University of Southampton, Southampton SO16 7PX, UK; and
2
DST-NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology, University of
Cape Town, Rondebosch 7701, South Africa
Abstract Shorebirds foraging in the intertidal have been shown to exert a significant effect on assemblage level
processes; this is particularly true of the oystercatcher–limpet–algae system. The African black oystercatcher
(Haematopus moquini) is endemic to the southern African coastline, where it plays a significant role in ecosystem
processes as a rocky-shore predator, especially of mussels and limpets. This understanding was based on studies of
a rocky shore environment that has since been considerably modified following invasion of an alien mussel (Mytilus
galloprovincialis). This invasion has not only changed the relative proportions of different food types on the shore,
but has also greatly increased overall food biomass. We tested the previous model that food selection by oyster-
catchers reflected prey abundance and that intake by male and female oystercatchers differed owing to bill
morphology. We predicted that this difference would persist despite the changed nature of the food base. We also
predicted that wave action would modify prey selection as a result of both its influence on prey behaviour and its
impact on searching and handling times of the birds. Overall, both sexes consumed more limpets than expected by
encounter rate alone, but contrary to prediction, the relative proportions of different prey types taken post invasion
did not differ between the sexes. Dietary convergence is interpreted as a result of greatly increased food biomass on
the shore, which is also reflected in increased oystercatcher densities since the invasion. Also contrary to prediction
there was no evidence that waves acted as indirect modifiers of the interaction between oystercatchers and their
prey. The results of this study indicate that models of trophic cascades will need to be altered in the event of a
significant change in a trophic level, which then effects behavioural changes in the key predator.
Key words: feeding behaviour, limpet, mussel, rocky shore, shorebird.
INTRODUCTION problem with this model of opposing predation and
productivity forces is that there is the assumption of
Much of our understanding of how trophic interac- the players being drawn from a pool of species local to
tions influence assemblage level processes comes from the system under investigation. This is not always the
studies carried out on rocky shore systems (Wootton case. In some systems changes in prey and/or preda-
1993; Menge 2000), including some of the most cited tors, often owing to invasions, can seriously disrupt
works in ecology (for example Paine 1974). This trophic structures (Strayer et al. 2006) with concomi-
understanding of the role of predators led to the tant effects on putative cascades. Here we examine the
trophic cascade debate in the early 1990s (e.g. Strong effect of the establishment of an invasive species on
1992), which is still ongoing. The key context of this what has been held up as one of the key examples of
debate is the relative strengths of the often opposing trophic cascades (Bosman & Hockey 1988; Wootton
forces of predation removing grazers and/or space 1993; Menge 2000; Thompson et al. 2002).
occupiers which then releases algae or other space Birds are significant predators on rocky shores (e.g.
occupiers, leading to a shift in community state. The Hockey et al. 1983; Marsh 1986; Wootton 1992) and
alternative force derives from the ability of primary understanding how prey populations interact with the
producers to outgrow, reduce or tolerate grazers. The ecology of their bird predators is fundamental to
understanding ecosystems in which birds are impor-
tant predators. Studies of wading birds in general and
*Corresponding author. Present address: Centre for Research
on Ecological Impacts of Coastal Cities, Marine Ecology Labo-
oystercatchers (Haematopodidae) in particular have
ratories (A11), The University of Sydney, NSW 2006, Australia contributed much to our understanding of foraging
(Email: ross.coleman@bio.usyd.edu.au) theory (e.g. Sutherland 1996) and of how predators
Accepted for publication March 2007. modify their foraging behaviour in response to adverse
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 233
weather. Most of these studies, however, have been (Hockey & Underhill 1984; Hulscher 1996). Cold,
carried out in estuarine habitats, characterized by soft rain and strong winds can influence the physiology and
sediments and a lack of wave action. hence the behaviour of prey, thus changing their avail-
The African black oystercatcher Haematopus moquini ability to oystercatcher predators independently of
Bonaparte 1856 is southern Africa’s second rarest their abundance. For example, during rainy periods
coastal bird, with approximately 3000 breeding pairs when salinity is lowered, mussels close their valves
distributed around the coast of southern Africa from (Shumway 1977; Davenport 1979). Under similar
Lüderitz, Namibia to southern KwaZulu-Natal, South conditions, limpets clamp down on the rock to reduce
Africa (Hockey et al. 2005). Foraging by H. moquini osmotic shock from fresh water (Arnold 1957) thus
has been well studied (Hockey 1981a,b; 1984a; are much harder to remove (Coleman et al. 2004).
Hockey & Branch 1984; Bosman et al. 1989), as has Similarly, extreme cold depresses prey metabolic levels
their ecological role as predators on rocky shores leading to lowered respiration rates, necessitating
(Bosman & Hockey 1988; Bosman et al. 1989). reduced gas exchange and leading in turn to a smaller
However, at the time of these studies, the rocky shore gap between the valves of mussels and between the
invertebrate communities of western South Africa shell and the substratum in limpets. This will again
(where the studies were carried out) were different to reduce availability.
those of today. Since the early 1980s, southern Africa’s The role of waves in modifying prey availability to
rocky shores have been invaded, and many are now wading birds is understudied. As wave amplitude
dominated, by the alien Mediterranean mussel Mytilus increases, so the extent of wave wash over the shore
galloprovincialis (Lamarck) (Branch & Steffani 2004). increases (Helmuth & Denny 2003). A foraging bird
In recent years, African black oystercatchers have can no longer see its potential prey and may risk being
undergone a dietary shift as a result of this invasion. washed away. The interaction of wave period and wave
The alien mussel now dominates their diet, and addi- amplitude will determine how much of the foraging
tionally has altered the spatial distribution of the area is accessible and for how long. Thus, in periods of
limpet Scutellastra granularis (L) – another important strong wave action, emersions at low tide will be
prey item (Hockey & Underhill 1984) – by direct reduced and it would be expected that foraging oys-
competition for primary space (Hockey & Van Erkom tercatchers would take fewer limpets, which potentially
Schurink 1992). In the late 1970s and early 1980s, require a long in situ attack phase (Coleman et al.
S. granularis made up about 35% of the oyster- 1999), and take more mussels, which, once the poste-
catchers’ diet. As the M. galloprovincialis invasion rior adductor muscle has been severed (Hockey
progressed, this proportion decreased substantially 1981a), can be rapidly removed from the mussel bed
and the indigenous mussel Aulacomya ater (Mollina), for handling in a safer location (Hulscher 1996).
which was a significant preinvasion prey item (Hockey The aim of this study was to assess how the diet
& Underhill 1984; Hockey & Van Erkom Schurink spectrum of oystercatchers reflects prey abundance on
1992), all but disappeared from the diet (Hockey & the shore after successful dominance by an alien inver-
Van Erkom Schurink 1992). For about 8 years (mid tebrate invader. Specifically, we tested the hypothesis
1980s to mid 1990s) oystercatcher diet remained con- that diet directly reflects prey abundance (Krebs
stant (60–65% M. galloprovincialis) (Hockey & Van 1978). A second aim was to assess whether prey choice
Erkom Schurink 1992). Although M. galloprovincialis would be further modified by the effect of the most
alters the demography of the S. granularis population, significant environmental hazard during the non-
high recruitment success (limpets settling on the shells breeding season, that of high waves. We predicted that
of M. galloprovincialis) increases both the biomass choices would be modified by wave action as foraging
and reproductive output of S. granularis providing oystercatchers would have less time to handle prey
mussel cover of the shore does not exceed about 75% when attempting to feed in between waves breaking on
(Griffiths et al. 1992). the shore. Relative to the prey spectrum taken under
Shorebird predators may forage differently when calm conditions, reduction in search time was antici-
facing extremes of wind, rain and/or cold (see Goss- pated to force selection of an increased proportion of
Custard et al. 1996 for review). This is due to the common, smaller but less profitable items.
interactive effects of changing prey abundance and/or
availability in response to cold or rain (Hulscher 1996)
and increased demands on the birds to maintain a METHODS
sufficiently high daily energy intake (Goss-Custard
et al. 1996). In respect of oystercatchers on rocky The study was carried out at Marcus Island (33°3′S,
shores, however, patterns are less clear. Most oyster- 17°58′E – Fig. 1) during the austral winter of 1997,
catchers utilizing rocky shore habitats primarily during the non-breeding period for H. moquini.
consume molluscs (mostly limpets and/or mussels), Marcus Island is a small (11 ha) granitic island, with
with some polychaetes and other unshelled items a predominantly rocky coastline representative of
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
234 R . A . C O L E M A N A N D P. A . R . H O C K E Y
Fig. 1. Location of Marcus Island, Saldanha Bay within Southern Africa and positions of observation sites. The dotted line
indicates the extent of the intertidal. The wave recorder is located in the entrance to Saldanha Bay some 2 km south-west of
Marcus Island. The prevailing swell direction is from the south-west.
Benguela rocky coastlines (Bustamante & Branch real time into a dictaphone, which was then later
1996). Coastal exposure to wave action ranges from transcribed into a computer using The Observer
moderate to severe (Hockey & Underhill 1984). At the behavioural recording software (Noldus Technology,
time of the study, the island supported a population of Wageningen, the Netherlands) for analysis. The 60¥
approximately 35–40 pairs of African Black Oyster- telescope allowed visual determination of prey choice
catchers, with small numbers of non-breeding birds even when oystercatchers were foraging in mussel beds
present. The African Black Oystercatcher differs from where the prey may not be lifted clear of the
the European Oystercatcher (H. ostralegus), in being substratum. The sizes of prey (mussel or limpet) taken
territorial year-round (Hockey 1996), hence it was were estimated relative to bill lengths of males and
relatively easy to fix the numbers of birds observed. As females (Hockey 1981b), and observations were cali-
each study site on the island was occupied by one or brated by comparison with shells from observed pre-
two territorial pairs of birds, it was possible to sex dation events. The concern of Ens (1982) that shell
individuals based on bill morphology (Hockey 1981b). collection underestimates the proportion of small prey
The amount of time the birds spent foraging was taken is not valid here because the use of a powerful
assessed by instantaneous scans (Altman 1974) at telescope allowed precise locations of shells from
15-min intervals from dawn to dusk for each of the predation events to be identified; furthermore, the
four designated sites (Fig. 1) on four separate occa- immediacy of recovery meant nearly all shells were
sions (two when high tide occurred at mid-day, and collected.These and size estimates for the same prey in
two when low tide occurred at mid-day, all tides inter- the field at the time of capture were used to calculate
mediate between neap and spring), interspersed with energy yield from the regressions of prey size versus
the focal animal observations detailed below. energy yield.
Focal animal (Altman 1974) observations were con- Prey distributions in each of the study sites were
ducted for 10 min immediately following a predation mapped and described. Forty 0.5 ¥ 0.5 m quadrats
event (Coleman et al. 1999). Oystercatchers foraging were randomly placed on the rock at each site (Fig. 1),
in the four sites where the distribution of prey was but at site 4, the smallest site, only 25 quadrats were
known were observed from a vantage point (far used. Within each quadrat, the percentage cover of
enough away to avoid disturbing the birds) through a mussels and bare rock was determined from a 7 ¥ 7
60¥ telescope. Prey choice data were described in intersection grid, and the numbers, sizes and species of
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 235
all limpets present in the quadrat were recorded. Dif- refraction meant we could assume, and was confirmed
ferences in prey density (number of limpets per square on site (R. Coleman, pers. obs. 1997), that at the scale
metre and percentage cover of mussels) were assessed which could influence oystercatchers, all sites were
using anova with sample size randomly adjusted to 25 more or less equally exposed. Data on maximal wave
to give a balanced dataset and homogeneity of vari- height and period during focal bird observations were
ances checked by Cochran’s test, where appropriate obtained from a nearby wave recorder (approx. 2 km
separation of significant factors was achieved by SNK seaward of Marcus Island). This gave us a single figure
tests (Underwood 1997). The size structure of mussel for wave height comparable across all sites. First, the
populations at each site was obtained by taking five hypothesis that maximal wave height and period were
random 0.1 ¥ 0.1 m samples of mussel bed, removed correlated was checked from three wave heights and
using a paint scraper. All mussels present (>16 mm) periods at three randomly chosen times for all the
were measured using vernier callipers. As mussels less observation days. Wave height usually has greater
than 16 mm long are not eaten by oystercatchers variation than periodicity and thus a major effect on
(Hockey & Underhill 1984), these were simply exposing and covering of the oystercatcher’s foraging
counted. The energy values for all available sizes of arena, so this was regressed against the proportion of
each prey species were obtained by collecting speci- mussel prey in the diet (arcsin transformed). In the
mens of all sizes for each prey type (78 mussels and 88 event of wave height explaining prey selection for each
limpets) and drying to a constant weight at 60°C for sex, the relationship between regression lines would be
48 h. This was then converted to energetic values by tested using homogeneity of slope tests and ancova
determining the energetic value of known amounts of procedures based on samples which were randomly
mussel or limpet flesh using bomb calorimetry (DDS adjusted to give a balanced set (Underwood 1997).
CP 500 Digital Oxygen Bomb Calorimeter, Digital
Data Systems Ltd, Northcliff, South Africa). Previous
work (R. Coleman, unpubl. data 1997) had shown that RESULTS
the best regression for explaining the relationship
between limpet length and energy yield was a power Sites 3 (72.0 per square metre, SEM = 6.77, n = 40)
function, hence this was used here. and 4 (3.28.6 per square metre, SEM = 4.26, n = 25)
While it was relatively easy to observe species con- had significantly fewer limpets than sites 1 (93.6 per
sumed by oystercatchers, it was not always possible to square metre, SEM = 4.26, n = 40) and 2 (95.4 per
determine sizes of mussels because, in some cases, the square metre, SEM = 7.8, n = 40) (anova, square-root
birds did not detach the shells and consumed the transformed data to correct for homogeneity of vari-
contents in situ. In order to estimate energy intake, ances; F3,96 = 21.30, P < 0.001), and all sites differed
these mussels of unknown sizes were allocated to the in percentage cover of mussels (F3,96 = 2.77, P < 0.05)
most frequent mussel size (20–24 mm, Fig. 4) and (Site 1: 38.8, SEM = 2.84, n = 40; Site 2: 59.9,
allocated an energy value accordingly. This was sup- SEM = 3.97, n = 40; Site 3: 59.4, SEM = 4.75, n = 40;
ported by observations that the birds only removed Site 4: 48.5, SEM = 6.82, n = 25). Power functions of
large mussels from the bed. This allowed a realistic prey size significantly explained 87% of the variation in
estimate of energy intake, which was compared with energy yield of limpets (Fig. 2a) and 92% of the varia-
energy available from prey present on the shore and tion in energy yield of mussels (Fig. 2b) with limpets
tested using a log-likelihood (G) test (Sokal & Rohlf yielding more energy for a given prey size than
1995). In order to test the strength of this relationship, mussels.
a second analysis was carried out whereby the mussels In total, 43 focal bird observations were made of
of unknown size were allocated to the largest possible females and 31 of males across all sites. The number
size class and the intake compared with the potential of observations for each sex was independent of site
energy available on the shore using the same test (G = 2.29, c2(3, 0.05) = 7.82, not significant) which indi-
structure. Prey other than mussels and limpets, includ- cated no sex-site bias. Over the period of the study, the
ing polychaetes, worms and whelks (mainly Nucella birds foraged actively for 35% of the time available
dubia) were also taken occasionally. These events were (there was no difference between the sexes, data dis-
noted but no shells collected. In the few cases where cussed in Leseberg et al. 2000). During this period
prey identification was not possible, prey were classi- mussels constituted about 65% of all the prey items
fied as unknown. Formal statistical comparison with consumed which represented an increase of about
prey records from an earlier study (Hockey & Under- 14% relative to the period 1979–1980 (Table 1,
hill 1984) was not logical as the data in that study were Hockey & Underhill 1984). For female taking limpets
not obtained in a comparable manner. (15 observed events) the prey size taken closely
It was hypothesized that wave action may modify matched that on the shore, whereas males took limpets
prey choice. The prevailing swell direction is from the of sizes from the smaller end of the distribution: when
south-west. The small size of the island and wave they did take larger (>30 mm) limpets these were
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
236 R . A . C O L E M A N A N D P. A . R . H O C K E Y
(a) G = 200.5, d.f. = 40, P < 0.001) than would be
50 expected on the basis of available energy alone. This
difference in energy intake remained significant even if
the mussels of unknown size were allocated to the
40
largest, rather than the average size class.
Energy (kJ)
Wave height was weakly correlated with period
30 (r = 0.32, d.f. =76, P < 0.05). From three randomly
selected times on 15 randomly selected days, the
20 average maximal wave height was 1.92 m (n = 45,
SD = 0.83) and the period was 12.58 s (n = 45,
10
SD = 2.22). The standard deviations represented 43%
of the mean for wave height and 17.6% of the mean for
wave period, respectively; hence the use of wave height
0 instead of period as the independent variable for
0 10 20 30 40 50 60
examining prey choice was justified. Wave action had
Limpet Size (mm)
(b) no effect on prey choice (Fig. 5). The proportion of
mussels consumed in any one foraging bout was not
35 affected by wave height. Neither of the regressions
30 significantly explained any variation with respect to
wave height in the proportion of mussels taken by
25 males or females (males: proportion of mussels in
Energy (kJ)
the diet = -0.829 ¥ wave height + 65.83, r2 = 0.027,
20
F1,29 = 0.023, not significant; for females: proportion of
15 mussels in the diet = -1.476 ¥ wave height + 75.176,
r2 = 0.015, F1,29 = 0.006, not significant). Tests for
10 homogeneity of slopes or analyses of covariance were
therefore not applicable.
5
0
0 10 20 30 40 50 60 70
Mussel Size (mm) DISCUSSION
Fig. 2. Energy yield from prey as a function of maximum
length (mm). (a) Length (mm) – energy (kJ) regression for In all branches of biology, samples are taken from a
limpets Scutellastra granularis at Marcus Island (Energy = population (in a statistical sense) to be representative
0.0001 length3.0956, r2 = 0.868, F1,86 = 597.80, P < 0.0001). of that population (Underwood 1997). Sample size is
(b) Length (mm) – energy (kJ) regression for mussels Mytlius then a limit of resources, complexity of work involved
galloprovincialis at Marcus Island (Energy = 0.0002 and primarily the needs of any hypotheses under test.
length2.9235, r2 = 0.910, F1,86 = 774.85, P < 0.0001). Here, while the sample size was small – six males and
six females, the sample was representative of oyster-
catchers on Marcus Island in terms of behaviour and
taken at a size frequency similar to that present on the of food supply. Studies have shown the birds on
shore (Fig. 3). When feeding on mussels, both sexes Marcus Island to be representative of the population as
took mainly medium-sized mussels (24–36 mm), a whole (Hockey 1981b,a; 1983; 1984a,b,), hence
despite the fact that these were relatively scarce there is no reason to regard the data from this study as
(Fig. 4). Historically, when foraging on the larger unrepresentative on the basis of small sample sizes.
Choromytilus meridionalis, the sizes of mussels selected This study aimed to assess patterns of food selection
by oystercatchers closely mirrored availability, with a by oystercatchers following establishment of a success-
modal size of 35–40 mm (Hockey 1981a). Eighty-one ful invertebrate invader that changed the absolute and
per cent of females’ energy intake was derived from relative abundance of food types on the shore. Addi-
mussels and 19% from limpets. Mussels contributed tionally, the hypothesis that increased wave action
79% of males’ energy intake and limpets 21%. These would reduce the proportion of limpets taken by for-
values were significantly different from the energy aging oystercatchers was tested. Mussels were the
intake expected if oystercatchers matched intake to most frequent prey item in the diet, although limpets
availability (males’ G = 621.8, d.f. = 40, P < 0.001; were taken more often than would be expected on the
females’ G = 600.5, d.f. = 40, P < 0.001). The propor- basis of encounter frequency alone.The results did not
tion of energy obtained from limpets was greater support the hypothesis of an effect of wave height on
(males’ G = 92.2, d.f. = 40, P < 0.001; females’ prey selection by oystercatchers.
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 237
Table 1. Proportions of prey items in foraging bouts of adult prebreeding Haematopus moquini (authority) observed on Marcus
Island, South Africa
1979/80 1997
Prey Males Females Males Females
Limpet 23.7 (6.9) 3.1 (2.1) 15.8 (0.9) 6.5 (0.3)
Mussel (all) 50.5 (17.5) 62.9 (24.5) 68.4 (1.1) 63.4 (0.7)
Mytilus galloprovincialis Not present Not present 68.4 (1.1) 63.4 (0.7)
Aulacomyer auter 8.7 (8.2) 10.9 (10.9) 0 (0) 0 (0)
Chroromytilus 41.9 (25.7) 51.9 (35.4) 0 (0) 0 (0)
meridionalis
Others 25.8 (24.4) 34.1 (26.5) 15.8 (0.7) 30.1 (0.6)
Data (means with standard errors in parentheses) for 1979/80 were calculated from Hockey and Underhill (1984) from
2 m f-1 pairs of birds. Data for 1997 are means, with standard errors in parentheses, for six males (31 observations) and six
females (43 observations) observed over a month period for 10 min each.
300
20
Male
Frequency of limpet sizes on sites 1 - 4
Female
16
Frequency of limpet sizes in diet
200
12
8
100
4
0 0
13.00 19.00 25.00 31.00 37.00 43.00 49.00 55.00 61.00 68.00
Limpet sizes (mm)
Fig. 3. Relative abundance of limpets (Scutellastra granularis) of different sizes compared with the size-frequency of prey items
eaten by adult non-breeding African black oystercatchers. The bars refer to limpet abundance and are from 145 ¥ 0.25 m2
quadrats across four sites. The lines are from observed predation events.
On rocky shores, oystercatchers are presented with a phology is finer and more suited to stabbing (sensu
choice of prey items and prey on a wide diversity of Tinbergen & Norton-Griffiths 1964). By contrast,
species (Hulscher 1996). They are known predators of male H. moquini favour limpets because their blunter-
limpets and mussels on rocky shores in South Africa ended bill is more suited to removal of limpets from
(e.g. Hockey & Underhill 1984; Hockey & Van Erkom the substratum. The evidence from this study does not
Schurink 1992), NW Pacific coasts (e.g. Wootton support this model for individuals – no one bird was
1992), the UK (e.g. Harris 1967; Lewis & Bowman faithful to any one prey type. On occasions, individuals
1975; Coleman et al. 1999), Australia (Lane & Davies would take all mussels on one day and all limpets the
1987) and New Zealand (Baker 1974). On many rocky following day. Across all observations there was a dif-
shores, limpets and mussels are direct competitors ference of 9.3% in the proportion of limpets in the
for space, hence understanding the role of predator diets between males and females. This is a substantial
and prey selection becomes important in predicting reduction in difference from 20% in 1979/80 (Table 1,
changes in assemblage structure in response to preda- Hockey & Underhill 1984) which suggests that
tor behaviour or changes in prey abundance (Wootton the current superabundance of food (especially of
1993). It has previously been argued (Hockey 1981b) M. galloprovincialis) has resulted in intersexual dietary
that female H. moquini favour mussels (Table 1, convergence, regardless of intersexual differences in
Hockey & Underhill 1984) because their bill mor- bill morphology.
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
238 R . A . C O L E M A N A N D P. A . R . H O C K E Y
200 20
Male
Female
Frequency of mussel sizes in diet.
Frequency of mussel sizes on sites 1 - 4
16
Unknown prey
size frequencies
12
Male, 96
100 Female, 179
8
4
0 0
16.00 20.00 24.00 28.00 32.00 36.00 40.00 44.00 50.00
Mussel sizes (mm)
Fig. 4. Relative abundance of mussels Mytilus galloprovincialis of different sizes compared with the size-frequency of prey items
eaten by adult non-breeding African black oystercatchers. The bars refer to limpet abundance and are from 145 ¥ 0.25 m2
quadrats across four sites. The lines are from observed predation events across the whole investigation.
this system may affect the competitive interaction
Arcsin transformed percentage
100
between M. galloprovincialis and S. granularis by dif-
80 ferential removal of either prey species (Steffani &
Branch 2005). Hockey and Van Erkom Schurink
60 (1992) proposed that there was an oscillation between
mussel consumed
peaks of abundance of the different prey species, a
40 Male pattern that has persisted in the 15 years since that
Female study was published (P. A. R. Hockey, unpubl. data
20 2007).
Wave action is a significant abiotic influence on
0
rocky shore ecosystems. Classical studies have shown
that assemblages on exposed sites differ markedly from
0.0 0.5 1.0 1.5 2.0 2.5 3.0 those at more sheltered locations (see Hawkins &
Wave Height (m) Hartnoll 1983 for review). More recently, the impact
of waves have been shown to modify species’ biologies
Fig. 5. Proportion of mussels in foraging bouts of adult
via phenotypic plasticity such as modifying the shape
non-breeding Haematopus moquini as affected by wave action
based on observed known predation events. Numbers of of algae (Fowler-Walker et al. 2006), influencing the
birds and observations are given in Table 1. As regression shape of limpets (Denny 2000) or even the morphol-
lines are non-significant, they are not shown. ogy of barnacle cirri (Arsenault et al. 2001). In a par-
allel development, ecologists have come to understand
that indirect interactions whereby predators influence
In this study, oystercatchers took far more limpets assemblages by modifying the behaviour of animals
than would be expected on the basis of either their from lower trophic levels can be as important as direct
relative biomass on the shore or their encounter fre- predation effects in modifying assemblage processes
quency by oystercatchers.The levels of mussel removal (Wootton 1993). For example, the presence of a
(by H. moquini) are highly unlikely to affect mussel feeding crab can modify the behaviour of nearby snails
numbers on the shore at Marcus Island because of the such that grazing effects are changed (Trussell et al.
high level of natural mortality due to crowding effects 2002). Here, we tested whether wave action modifies
as the mussels grow (Griffiths et al. 1992), but the the foraging behaviour of oystercatchers, such that
substantial numbers of limpets eaten may deplete strong wave action would change the relative abun-
their numbers significantly (Hockey & Branch 1984; dance of the two prey species in the diet. If this were
Bosman & Hockey 1988) facilitating the spread of true and representative of areas where oystercatchers
mussels. It has been suggested that oystercatchers in are significant predators of grazers (Hockey et al.
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 239
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doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
Effects of an alien invertebrate species and wave action
on prey selection by African black oystercatchers
(Haematopus moquini)
R. A. COLEMAN1* AND P. A. R. HOCKEY2
1
School of Biological Sciences, University of Southampton, Southampton SO16 7PX, UK; and
2
DST-NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology, University of
Cape Town, Rondebosch 7701, South Africa
Abstract Shorebirds foraging in the intertidal have been shown to exert a significant effect on assemblage level
processes; this is particularly true of the oystercatcher–limpet–algae system. The African black oystercatcher
(Haematopus moquini) is endemic to the southern African coastline, where it plays a significant role in ecosystem
processes as a rocky-shore predator, especially of mussels and limpets. This understanding was based on studies of
a rocky shore environment that has since been considerably modified following invasion of an alien mussel (Mytilus
galloprovincialis). This invasion has not only changed the relative proportions of different food types on the shore,
but has also greatly increased overall food biomass. We tested the previous model that food selection by oyster-
catchers reflected prey abundance and that intake by male and female oystercatchers differed owing to bill
morphology. We predicted that this difference would persist despite the changed nature of the food base. We also
predicted that wave action would modify prey selection as a result of both its influence on prey behaviour and its
impact on searching and handling times of the birds. Overall, both sexes consumed more limpets than expected by
encounter rate alone, but contrary to prediction, the relative proportions of different prey types taken post invasion
did not differ between the sexes. Dietary convergence is interpreted as a result of greatly increased food biomass on
the shore, which is also reflected in increased oystercatcher densities since the invasion. Also contrary to prediction
there was no evidence that waves acted as indirect modifiers of the interaction between oystercatchers and their
prey. The results of this study indicate that models of trophic cascades will need to be altered in the event of a
significant change in a trophic level, which then effects behavioural changes in the key predator.
Key words: feeding behaviour, limpet, mussel, rocky shore, shorebird.
INTRODUCTION problem with this model of opposing predation and
productivity forces is that there is the assumption of
Much of our understanding of how trophic interac- the players being drawn from a pool of species local to
tions influence assemblage level processes comes from the system under investigation. This is not always the
studies carried out on rocky shore systems (Wootton case. In some systems changes in prey and/or preda-
1993; Menge 2000), including some of the most cited tors, often owing to invasions, can seriously disrupt
works in ecology (for example Paine 1974). This trophic structures (Strayer et al. 2006) with concomi-
understanding of the role of predators led to the tant effects on putative cascades. Here we examine the
trophic cascade debate in the early 1990s (e.g. Strong effect of the establishment of an invasive species on
1992), which is still ongoing. The key context of this what has been held up as one of the key examples of
debate is the relative strengths of the often opposing trophic cascades (Bosman & Hockey 1988; Wootton
forces of predation removing grazers and/or space 1993; Menge 2000; Thompson et al. 2002).
occupiers which then releases algae or other space Birds are significant predators on rocky shores (e.g.
occupiers, leading to a shift in community state. The Hockey et al. 1983; Marsh 1986; Wootton 1992) and
alternative force derives from the ability of primary understanding how prey populations interact with the
producers to outgrow, reduce or tolerate grazers. The ecology of their bird predators is fundamental to
understanding ecosystems in which birds are impor-
tant predators. Studies of wading birds in general and
*Corresponding author. Present address: Centre for Research
on Ecological Impacts of Coastal Cities, Marine Ecology Labo-
oystercatchers (Haematopodidae) in particular have
ratories (A11), The University of Sydney, NSW 2006, Australia contributed much to our understanding of foraging
(Email: ross.coleman@bio.usyd.edu.au) theory (e.g. Sutherland 1996) and of how predators
Accepted for publication March 2007. modify their foraging behaviour in response to adverse
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 233
weather. Most of these studies, however, have been (Hockey & Underhill 1984; Hulscher 1996). Cold,
carried out in estuarine habitats, characterized by soft rain and strong winds can influence the physiology and
sediments and a lack of wave action. hence the behaviour of prey, thus changing their avail-
The African black oystercatcher Haematopus moquini ability to oystercatcher predators independently of
Bonaparte 1856 is southern Africa’s second rarest their abundance. For example, during rainy periods
coastal bird, with approximately 3000 breeding pairs when salinity is lowered, mussels close their valves
distributed around the coast of southern Africa from (Shumway 1977; Davenport 1979). Under similar
Lüderitz, Namibia to southern KwaZulu-Natal, South conditions, limpets clamp down on the rock to reduce
Africa (Hockey et al. 2005). Foraging by H. moquini osmotic shock from fresh water (Arnold 1957) thus
has been well studied (Hockey 1981a,b; 1984a; are much harder to remove (Coleman et al. 2004).
Hockey & Branch 1984; Bosman et al. 1989), as has Similarly, extreme cold depresses prey metabolic levels
their ecological role as predators on rocky shores leading to lowered respiration rates, necessitating
(Bosman & Hockey 1988; Bosman et al. 1989). reduced gas exchange and leading in turn to a smaller
However, at the time of these studies, the rocky shore gap between the valves of mussels and between the
invertebrate communities of western South Africa shell and the substratum in limpets. This will again
(where the studies were carried out) were different to reduce availability.
those of today. Since the early 1980s, southern Africa’s The role of waves in modifying prey availability to
rocky shores have been invaded, and many are now wading birds is understudied. As wave amplitude
dominated, by the alien Mediterranean mussel Mytilus increases, so the extent of wave wash over the shore
galloprovincialis (Lamarck) (Branch & Steffani 2004). increases (Helmuth & Denny 2003). A foraging bird
In recent years, African black oystercatchers have can no longer see its potential prey and may risk being
undergone a dietary shift as a result of this invasion. washed away. The interaction of wave period and wave
The alien mussel now dominates their diet, and addi- amplitude will determine how much of the foraging
tionally has altered the spatial distribution of the area is accessible and for how long. Thus, in periods of
limpet Scutellastra granularis (L) – another important strong wave action, emersions at low tide will be
prey item (Hockey & Underhill 1984) – by direct reduced and it would be expected that foraging oys-
competition for primary space (Hockey & Van Erkom tercatchers would take fewer limpets, which potentially
Schurink 1992). In the late 1970s and early 1980s, require a long in situ attack phase (Coleman et al.
S. granularis made up about 35% of the oyster- 1999), and take more mussels, which, once the poste-
catchers’ diet. As the M. galloprovincialis invasion rior adductor muscle has been severed (Hockey
progressed, this proportion decreased substantially 1981a), can be rapidly removed from the mussel bed
and the indigenous mussel Aulacomya ater (Mollina), for handling in a safer location (Hulscher 1996).
which was a significant preinvasion prey item (Hockey The aim of this study was to assess how the diet
& Underhill 1984; Hockey & Van Erkom Schurink spectrum of oystercatchers reflects prey abundance on
1992), all but disappeared from the diet (Hockey & the shore after successful dominance by an alien inver-
Van Erkom Schurink 1992). For about 8 years (mid tebrate invader. Specifically, we tested the hypothesis
1980s to mid 1990s) oystercatcher diet remained con- that diet directly reflects prey abundance (Krebs
stant (60–65% M. galloprovincialis) (Hockey & Van 1978). A second aim was to assess whether prey choice
Erkom Schurink 1992). Although M. galloprovincialis would be further modified by the effect of the most
alters the demography of the S. granularis population, significant environmental hazard during the non-
high recruitment success (limpets settling on the shells breeding season, that of high waves. We predicted that
of M. galloprovincialis) increases both the biomass choices would be modified by wave action as foraging
and reproductive output of S. granularis providing oystercatchers would have less time to handle prey
mussel cover of the shore does not exceed about 75% when attempting to feed in between waves breaking on
(Griffiths et al. 1992). the shore. Relative to the prey spectrum taken under
Shorebird predators may forage differently when calm conditions, reduction in search time was antici-
facing extremes of wind, rain and/or cold (see Goss- pated to force selection of an increased proportion of
Custard et al. 1996 for review). This is due to the common, smaller but less profitable items.
interactive effects of changing prey abundance and/or
availability in response to cold or rain (Hulscher 1996)
and increased demands on the birds to maintain a METHODS
sufficiently high daily energy intake (Goss-Custard
et al. 1996). In respect of oystercatchers on rocky The study was carried out at Marcus Island (33°3′S,
shores, however, patterns are less clear. Most oyster- 17°58′E – Fig. 1) during the austral winter of 1997,
catchers utilizing rocky shore habitats primarily during the non-breeding period for H. moquini.
consume molluscs (mostly limpets and/or mussels), Marcus Island is a small (11 ha) granitic island, with
with some polychaetes and other unshelled items a predominantly rocky coastline representative of
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
234 R . A . C O L E M A N A N D P. A . R . H O C K E Y
Fig. 1. Location of Marcus Island, Saldanha Bay within Southern Africa and positions of observation sites. The dotted line
indicates the extent of the intertidal. The wave recorder is located in the entrance to Saldanha Bay some 2 km south-west of
Marcus Island. The prevailing swell direction is from the south-west.
Benguela rocky coastlines (Bustamante & Branch real time into a dictaphone, which was then later
1996). Coastal exposure to wave action ranges from transcribed into a computer using The Observer
moderate to severe (Hockey & Underhill 1984). At the behavioural recording software (Noldus Technology,
time of the study, the island supported a population of Wageningen, the Netherlands) for analysis. The 60¥
approximately 35–40 pairs of African Black Oyster- telescope allowed visual determination of prey choice
catchers, with small numbers of non-breeding birds even when oystercatchers were foraging in mussel beds
present. The African Black Oystercatcher differs from where the prey may not be lifted clear of the
the European Oystercatcher (H. ostralegus), in being substratum. The sizes of prey (mussel or limpet) taken
territorial year-round (Hockey 1996), hence it was were estimated relative to bill lengths of males and
relatively easy to fix the numbers of birds observed. As females (Hockey 1981b), and observations were cali-
each study site on the island was occupied by one or brated by comparison with shells from observed pre-
two territorial pairs of birds, it was possible to sex dation events. The concern of Ens (1982) that shell
individuals based on bill morphology (Hockey 1981b). collection underestimates the proportion of small prey
The amount of time the birds spent foraging was taken is not valid here because the use of a powerful
assessed by instantaneous scans (Altman 1974) at telescope allowed precise locations of shells from
15-min intervals from dawn to dusk for each of the predation events to be identified; furthermore, the
four designated sites (Fig. 1) on four separate occa- immediacy of recovery meant nearly all shells were
sions (two when high tide occurred at mid-day, and collected.These and size estimates for the same prey in
two when low tide occurred at mid-day, all tides inter- the field at the time of capture were used to calculate
mediate between neap and spring), interspersed with energy yield from the regressions of prey size versus
the focal animal observations detailed below. energy yield.
Focal animal (Altman 1974) observations were con- Prey distributions in each of the study sites were
ducted for 10 min immediately following a predation mapped and described. Forty 0.5 ¥ 0.5 m quadrats
event (Coleman et al. 1999). Oystercatchers foraging were randomly placed on the rock at each site (Fig. 1),
in the four sites where the distribution of prey was but at site 4, the smallest site, only 25 quadrats were
known were observed from a vantage point (far used. Within each quadrat, the percentage cover of
enough away to avoid disturbing the birds) through a mussels and bare rock was determined from a 7 ¥ 7
60¥ telescope. Prey choice data were described in intersection grid, and the numbers, sizes and species of
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 235
all limpets present in the quadrat were recorded. Dif- refraction meant we could assume, and was confirmed
ferences in prey density (number of limpets per square on site (R. Coleman, pers. obs. 1997), that at the scale
metre and percentage cover of mussels) were assessed which could influence oystercatchers, all sites were
using anova with sample size randomly adjusted to 25 more or less equally exposed. Data on maximal wave
to give a balanced dataset and homogeneity of vari- height and period during focal bird observations were
ances checked by Cochran’s test, where appropriate obtained from a nearby wave recorder (approx. 2 km
separation of significant factors was achieved by SNK seaward of Marcus Island). This gave us a single figure
tests (Underwood 1997). The size structure of mussel for wave height comparable across all sites. First, the
populations at each site was obtained by taking five hypothesis that maximal wave height and period were
random 0.1 ¥ 0.1 m samples of mussel bed, removed correlated was checked from three wave heights and
using a paint scraper. All mussels present (>16 mm) periods at three randomly chosen times for all the
were measured using vernier callipers. As mussels less observation days. Wave height usually has greater
than 16 mm long are not eaten by oystercatchers variation than periodicity and thus a major effect on
(Hockey & Underhill 1984), these were simply exposing and covering of the oystercatcher’s foraging
counted. The energy values for all available sizes of arena, so this was regressed against the proportion of
each prey species were obtained by collecting speci- mussel prey in the diet (arcsin transformed). In the
mens of all sizes for each prey type (78 mussels and 88 event of wave height explaining prey selection for each
limpets) and drying to a constant weight at 60°C for sex, the relationship between regression lines would be
48 h. This was then converted to energetic values by tested using homogeneity of slope tests and ancova
determining the energetic value of known amounts of procedures based on samples which were randomly
mussel or limpet flesh using bomb calorimetry (DDS adjusted to give a balanced set (Underwood 1997).
CP 500 Digital Oxygen Bomb Calorimeter, Digital
Data Systems Ltd, Northcliff, South Africa). Previous
work (R. Coleman, unpubl. data 1997) had shown that RESULTS
the best regression for explaining the relationship
between limpet length and energy yield was a power Sites 3 (72.0 per square metre, SEM = 6.77, n = 40)
function, hence this was used here. and 4 (3.28.6 per square metre, SEM = 4.26, n = 25)
While it was relatively easy to observe species con- had significantly fewer limpets than sites 1 (93.6 per
sumed by oystercatchers, it was not always possible to square metre, SEM = 4.26, n = 40) and 2 (95.4 per
determine sizes of mussels because, in some cases, the square metre, SEM = 7.8, n = 40) (anova, square-root
birds did not detach the shells and consumed the transformed data to correct for homogeneity of vari-
contents in situ. In order to estimate energy intake, ances; F3,96 = 21.30, P < 0.001), and all sites differed
these mussels of unknown sizes were allocated to the in percentage cover of mussels (F3,96 = 2.77, P < 0.05)
most frequent mussel size (20–24 mm, Fig. 4) and (Site 1: 38.8, SEM = 2.84, n = 40; Site 2: 59.9,
allocated an energy value accordingly. This was sup- SEM = 3.97, n = 40; Site 3: 59.4, SEM = 4.75, n = 40;
ported by observations that the birds only removed Site 4: 48.5, SEM = 6.82, n = 25). Power functions of
large mussels from the bed. This allowed a realistic prey size significantly explained 87% of the variation in
estimate of energy intake, which was compared with energy yield of limpets (Fig. 2a) and 92% of the varia-
energy available from prey present on the shore and tion in energy yield of mussels (Fig. 2b) with limpets
tested using a log-likelihood (G) test (Sokal & Rohlf yielding more energy for a given prey size than
1995). In order to test the strength of this relationship, mussels.
a second analysis was carried out whereby the mussels In total, 43 focal bird observations were made of
of unknown size were allocated to the largest possible females and 31 of males across all sites. The number
size class and the intake compared with the potential of observations for each sex was independent of site
energy available on the shore using the same test (G = 2.29, c2(3, 0.05) = 7.82, not significant) which indi-
structure. Prey other than mussels and limpets, includ- cated no sex-site bias. Over the period of the study, the
ing polychaetes, worms and whelks (mainly Nucella birds foraged actively for 35% of the time available
dubia) were also taken occasionally. These events were (there was no difference between the sexes, data dis-
noted but no shells collected. In the few cases where cussed in Leseberg et al. 2000). During this period
prey identification was not possible, prey were classi- mussels constituted about 65% of all the prey items
fied as unknown. Formal statistical comparison with consumed which represented an increase of about
prey records from an earlier study (Hockey & Under- 14% relative to the period 1979–1980 (Table 1,
hill 1984) was not logical as the data in that study were Hockey & Underhill 1984). For female taking limpets
not obtained in a comparable manner. (15 observed events) the prey size taken closely
It was hypothesized that wave action may modify matched that on the shore, whereas males took limpets
prey choice. The prevailing swell direction is from the of sizes from the smaller end of the distribution: when
south-west. The small size of the island and wave they did take larger (>30 mm) limpets these were
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
236 R . A . C O L E M A N A N D P. A . R . H O C K E Y
(a) G = 200.5, d.f. = 40, P < 0.001) than would be
50 expected on the basis of available energy alone. This
difference in energy intake remained significant even if
the mussels of unknown size were allocated to the
40
largest, rather than the average size class.
Energy (kJ)
Wave height was weakly correlated with period
30 (r = 0.32, d.f. =76, P < 0.05). From three randomly
selected times on 15 randomly selected days, the
20 average maximal wave height was 1.92 m (n = 45,
SD = 0.83) and the period was 12.58 s (n = 45,
10
SD = 2.22). The standard deviations represented 43%
of the mean for wave height and 17.6% of the mean for
wave period, respectively; hence the use of wave height
0 instead of period as the independent variable for
0 10 20 30 40 50 60
examining prey choice was justified. Wave action had
Limpet Size (mm)
(b) no effect on prey choice (Fig. 5). The proportion of
mussels consumed in any one foraging bout was not
35 affected by wave height. Neither of the regressions
30 significantly explained any variation with respect to
wave height in the proportion of mussels taken by
25 males or females (males: proportion of mussels in
Energy (kJ)
the diet = -0.829 ¥ wave height + 65.83, r2 = 0.027,
20
F1,29 = 0.023, not significant; for females: proportion of
15 mussels in the diet = -1.476 ¥ wave height + 75.176,
r2 = 0.015, F1,29 = 0.006, not significant). Tests for
10 homogeneity of slopes or analyses of covariance were
therefore not applicable.
5
0
0 10 20 30 40 50 60 70
Mussel Size (mm) DISCUSSION
Fig. 2. Energy yield from prey as a function of maximum
length (mm). (a) Length (mm) – energy (kJ) regression for In all branches of biology, samples are taken from a
limpets Scutellastra granularis at Marcus Island (Energy = population (in a statistical sense) to be representative
0.0001 length3.0956, r2 = 0.868, F1,86 = 597.80, P < 0.0001). of that population (Underwood 1997). Sample size is
(b) Length (mm) – energy (kJ) regression for mussels Mytlius then a limit of resources, complexity of work involved
galloprovincialis at Marcus Island (Energy = 0.0002 and primarily the needs of any hypotheses under test.
length2.9235, r2 = 0.910, F1,86 = 774.85, P < 0.0001). Here, while the sample size was small – six males and
six females, the sample was representative of oyster-
catchers on Marcus Island in terms of behaviour and
taken at a size frequency similar to that present on the of food supply. Studies have shown the birds on
shore (Fig. 3). When feeding on mussels, both sexes Marcus Island to be representative of the population as
took mainly medium-sized mussels (24–36 mm), a whole (Hockey 1981b,a; 1983; 1984a,b,), hence
despite the fact that these were relatively scarce there is no reason to regard the data from this study as
(Fig. 4). Historically, when foraging on the larger unrepresentative on the basis of small sample sizes.
Choromytilus meridionalis, the sizes of mussels selected This study aimed to assess patterns of food selection
by oystercatchers closely mirrored availability, with a by oystercatchers following establishment of a success-
modal size of 35–40 mm (Hockey 1981a). Eighty-one ful invertebrate invader that changed the absolute and
per cent of females’ energy intake was derived from relative abundance of food types on the shore. Addi-
mussels and 19% from limpets. Mussels contributed tionally, the hypothesis that increased wave action
79% of males’ energy intake and limpets 21%. These would reduce the proportion of limpets taken by for-
values were significantly different from the energy aging oystercatchers was tested. Mussels were the
intake expected if oystercatchers matched intake to most frequent prey item in the diet, although limpets
availability (males’ G = 621.8, d.f. = 40, P < 0.001; were taken more often than would be expected on the
females’ G = 600.5, d.f. = 40, P < 0.001). The propor- basis of encounter frequency alone.The results did not
tion of energy obtained from limpets was greater support the hypothesis of an effect of wave height on
(males’ G = 92.2, d.f. = 40, P < 0.001; females’ prey selection by oystercatchers.
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 237
Table 1. Proportions of prey items in foraging bouts of adult prebreeding Haematopus moquini (authority) observed on Marcus
Island, South Africa
1979/80 1997
Prey Males Females Males Females
Limpet 23.7 (6.9) 3.1 (2.1) 15.8 (0.9) 6.5 (0.3)
Mussel (all) 50.5 (17.5) 62.9 (24.5) 68.4 (1.1) 63.4 (0.7)
Mytilus galloprovincialis Not present Not present 68.4 (1.1) 63.4 (0.7)
Aulacomyer auter 8.7 (8.2) 10.9 (10.9) 0 (0) 0 (0)
Chroromytilus 41.9 (25.7) 51.9 (35.4) 0 (0) 0 (0)
meridionalis
Others 25.8 (24.4) 34.1 (26.5) 15.8 (0.7) 30.1 (0.6)
Data (means with standard errors in parentheses) for 1979/80 were calculated from Hockey and Underhill (1984) from
2 m f-1 pairs of birds. Data for 1997 are means, with standard errors in parentheses, for six males (31 observations) and six
females (43 observations) observed over a month period for 10 min each.
300
20
Male
Frequency of limpet sizes on sites 1 - 4
Female
16
Frequency of limpet sizes in diet
200
12
8
100
4
0 0
13.00 19.00 25.00 31.00 37.00 43.00 49.00 55.00 61.00 68.00
Limpet sizes (mm)
Fig. 3. Relative abundance of limpets (Scutellastra granularis) of different sizes compared with the size-frequency of prey items
eaten by adult non-breeding African black oystercatchers. The bars refer to limpet abundance and are from 145 ¥ 0.25 m2
quadrats across four sites. The lines are from observed predation events.
On rocky shores, oystercatchers are presented with a phology is finer and more suited to stabbing (sensu
choice of prey items and prey on a wide diversity of Tinbergen & Norton-Griffiths 1964). By contrast,
species (Hulscher 1996). They are known predators of male H. moquini favour limpets because their blunter-
limpets and mussels on rocky shores in South Africa ended bill is more suited to removal of limpets from
(e.g. Hockey & Underhill 1984; Hockey & Van Erkom the substratum. The evidence from this study does not
Schurink 1992), NW Pacific coasts (e.g. Wootton support this model for individuals – no one bird was
1992), the UK (e.g. Harris 1967; Lewis & Bowman faithful to any one prey type. On occasions, individuals
1975; Coleman et al. 1999), Australia (Lane & Davies would take all mussels on one day and all limpets the
1987) and New Zealand (Baker 1974). On many rocky following day. Across all observations there was a dif-
shores, limpets and mussels are direct competitors ference of 9.3% in the proportion of limpets in the
for space, hence understanding the role of predator diets between males and females. This is a substantial
and prey selection becomes important in predicting reduction in difference from 20% in 1979/80 (Table 1,
changes in assemblage structure in response to preda- Hockey & Underhill 1984) which suggests that
tor behaviour or changes in prey abundance (Wootton the current superabundance of food (especially of
1993). It has previously been argued (Hockey 1981b) M. galloprovincialis) has resulted in intersexual dietary
that female H. moquini favour mussels (Table 1, convergence, regardless of intersexual differences in
Hockey & Underhill 1984) because their bill mor- bill morphology.
© 2008 The Authors doi:10.1111/j.1442-9993.2008.01864.x
Journal compilation © 2008 Ecological Society of Australia
238 R . A . C O L E M A N A N D P. A . R . H O C K E Y
200 20
Male
Female
Frequency of mussel sizes in diet.
Frequency of mussel sizes on sites 1 - 4
16
Unknown prey
size frequencies
12
Male, 96
100 Female, 179
8
4
0 0
16.00 20.00 24.00 28.00 32.00 36.00 40.00 44.00 50.00
Mussel sizes (mm)
Fig. 4. Relative abundance of mussels Mytilus galloprovincialis of different sizes compared with the size-frequency of prey items
eaten by adult non-breeding African black oystercatchers. The bars refer to limpet abundance and are from 145 ¥ 0.25 m2
quadrats across four sites. The lines are from observed predation events across the whole investigation.
this system may affect the competitive interaction
Arcsin transformed percentage
100
between M. galloprovincialis and S. granularis by dif-
80 ferential removal of either prey species (Steffani &
Branch 2005). Hockey and Van Erkom Schurink
60 (1992) proposed that there was an oscillation between
mussel consumed
peaks of abundance of the different prey species, a
40 Male pattern that has persisted in the 15 years since that
Female study was published (P. A. R. Hockey, unpubl. data
20 2007).
Wave action is a significant abiotic influence on
0
rocky shore ecosystems. Classical studies have shown
that assemblages on exposed sites differ markedly from
0.0 0.5 1.0 1.5 2.0 2.5 3.0 those at more sheltered locations (see Hawkins &
Wave Height (m) Hartnoll 1983 for review). More recently, the impact
of waves have been shown to modify species’ biologies
Fig. 5. Proportion of mussels in foraging bouts of adult
via phenotypic plasticity such as modifying the shape
non-breeding Haematopus moquini as affected by wave action
based on observed known predation events. Numbers of of algae (Fowler-Walker et al. 2006), influencing the
birds and observations are given in Table 1. As regression shape of limpets (Denny 2000) or even the morphol-
lines are non-significant, they are not shown. ogy of barnacle cirri (Arsenault et al. 2001). In a par-
allel development, ecologists have come to understand
that indirect interactions whereby predators influence
In this study, oystercatchers took far more limpets assemblages by modifying the behaviour of animals
than would be expected on the basis of either their from lower trophic levels can be as important as direct
relative biomass on the shore or their encounter fre- predation effects in modifying assemblage processes
quency by oystercatchers.The levels of mussel removal (Wootton 1993). For example, the presence of a
(by H. moquini) are highly unlikely to affect mussel feeding crab can modify the behaviour of nearby snails
numbers on the shore at Marcus Island because of the such that grazing effects are changed (Trussell et al.
high level of natural mortality due to crowding effects 2002). Here, we tested whether wave action modifies
as the mussels grow (Griffiths et al. 1992), but the the foraging behaviour of oystercatchers, such that
substantial numbers of limpets eaten may deplete strong wave action would change the relative abun-
their numbers significantly (Hockey & Branch 1984; dance of the two prey species in the diet. If this were
Bosman & Hockey 1988) facilitating the spread of true and representative of areas where oystercatchers
mussels. It has been suggested that oystercatchers in are significant predators of grazers (Hockey et al.
doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia
OY S T E R C AT C H E R S A N D I N VA S I V E M U S S E L S 239
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doi:10.1111/j.1442-9993.2008.01864.x © 2008 The Authors
Journal compilation © 2008 Ecological Society of Australia