Coral Reefs (2008) 27:583–591
DOI 10.1007/s00338-008-0366-7
REPORT
Relationships between butterflyfish (Chaetodontidae) feeding
rates and coral consumption on the Great Barrier Reef
M. A. Gregson Æ M. S. Pratchett Æ M. L. Berumen Æ
B. A. Goodman
Received: 4 April 2007 / Accepted: 25 February 2008 / Published online: 28 March 2008
Ó Springer-Verlag 2008
Abstract This study explored differences in the feeding
rate among 20 species of coral reef butterflyfishes (Chaetodontidae) from Lizard Island, Great Barrier Reef.
Feeding rate, measured as bites per minute (b.p.m.), varied
between 2.98 ± 0.65 and 12.29 ± 0.27 (mean ± SE)
according to species and was positively related to the
proportional consumption of coral (r2 = 0.40, n = 20,
P \ 0.01), independent of phylogeny (standardised independent contrasts r2 = 0.29, n = 19, P \ 0.05). All
species fed actively throughout the day, with obligate corallivores having a higher feeding rate at all times than
either facultative corallivores or non-corallivores. The
feeding rate of the obligate corallivores was also highest
during the middle of the day. For eight of the species for
which data was available, there was a positive correlation
between bite rate and competitive dominance (r = 0.71,
Communicated by Ecology Editor Professor Peter Mumby.
M. A. Gregson (&)
Department of Environmental Sciences, Institute for Water
and Environmental Resource Management, University
of Technology, Sydney, Broadway, NSW 2007, Australia
e-mail: [email protected]
M. S. Pratchett M. L. Berumen
ARC Centre of Excellence for Coral Reef Studies, James Cook
University, Townsville, QLD 4811, Australia
M. L. Berumen
Biology Department, Woods Hole Oceanographic Institution,
Woods Hole, MA 02543, USA
B. A. Goodman
School of Marine and Tropical Biology, James Cook University,
Townsville, QLD 4811, Australia
P \ 0.05). Chaetodon ephippium was the only species for
which the feeding rate of pairs was higher than for solitary
individuals.
Keywords Competition Corallivore Diurnal variation Feeding guild Group behaviour Prey quality
Introduction
Energy acquisition is fundamental to the biology and
ecology of all living organisms. Accordingly, choices
regarding the type and relative quantities of prey consumed, as well as when and where to feed, greatly
influence distributions, abundances, and fitness of most
species (Krebs 1978; Hughes 1980). Prey capture is a
major component of the time budget for most species,
though actual feeding rates (the average number of bites
per unit of time) vary greatly. Potential sources of variation
include ambient temperature, which can directly affect
activity levels of poikilotherms (Meeuwig et al. 2004), the
size/maturity of the animal, where ontogenetic changes
may include dietary shifts (Choat and Clements 1993), and/
or time of day (Ikeda 1977). An animal’s feeding rate also
tends to reflect its individual energy requirement relative to
the energy obtained from selected food items (Sterner and
Hessen 1994; Zharikov and Skilleter 2004). Given equal
energetic requirements, organisms feeding on poor-quality
prey must feed more frequently and/or ingest a greater
volume of food (Birkeland and Neudecker 1981; Beamish
and Medland 1986; Lares and McClintock 1991; but see
Lawrence et al. 1989). Where energy intake is limited by
the time available for feeding, animals must make
increasingly stringent decisions to optimise feeding
behaviour (Lucas 1983).
123
584
Aside from energetic return, feeding rates of animals are
influenced by the distribution and abundance of prey
(relating to interfeeding search times), and time required to
capture and consume individual prey (handling times). For
predatory animals, search and handling times are viewed as
major limits on feeding rates (Holling 1959). Feeding
behaviour may be further constrained by biological interactions with competitors and/or predators, which limit
access to certain areas or prey types (Krause and Godin
1994) and reduce overall time available for feeding.
Behavioural adaptations, such as group foraging, may
counteract the constraints imposed by competition and
predation, but there are still likely to be significant energetic costs associated with behaviours to minimise
competition and predation (e.g., Lima and Dill 1990; Vahl
et al. 2005). In aquatic environments, many teleost fishes
have adopted group foraging behaviours, presumably
because it reduces predation risk (Godin 1986) and/or
increases feeding efficiency (Pitcher et al. 1982).
The purpose of this study was to compare and contrast
feeding behaviour among sympatric butterflyfishes (family
Chaetodontidae), at Lizard Island, in the northern Great Barrier Reef of Australia. Butterflyfishes are a conspicuous and
relatively common family of coral reef fishes, which exhibit
considerable diversity in feeding habits. Butterflyfishes may
feed on corals (hard and/or soft), algae, benthic invertebrates
(motile or sedentary, including polychaete worms and crustaceans), and/or plankton (Reese 1977; Anderson et al. 1981;
Sano 1989). In general, quantifying and comparing feeding
rates among different species are often complicated by differences in feeding mode and gross morphology.
Butterflyfishes, however, represent a monophyletic group of
fishes with highly conserved jaw morphology (Ferry-Graham
et al. 2001). Aside from a few species with elongate jaws,
butterflyfishes have short robust jaws, adapted for biting corals
and other attached prey (Motta 1988). Feeding mostly
involves grabbing and tearing small pieces of soft tissue from
benthic invertebrates, while some species supplement their
diet by taking small discrete prey items, such as crustaceans.
The various specialised morphologies of these fishes do not
readily indicate what they feed on (Motta 1988). Butterflyfishes are, therefore, an ideal group to compare feeding rates on
different prey types, independent of differences in morphology and foraging mode.
This study tested several predictions using data on feeding
rates obtained for 20 sympatric species of butterflyfishes at
Lizard Island: (1) Do feeding rates of butterflyfishes correlate positively with the proportion of bites taken on hard
coral? If coral tissue is a poor-quality food source (sensu
Tricas 1989a), it would be expected that obligate corallivores
compensate by feeding at much faster rates compared to
facultative corallivores and non-corallivores. Conversely,
obligate corallivores might compensate for poor-quality
123
Coral Reefs (2008) 27:583–591
prey by feeding for a greater proportion on each day (Zekeria
et al. 2002); (2) Do feeding rates vary through the day? It was
predicted that there would be significant diurnal variation in
bite rates of butterflyfishes, as shown for several other coral
reef fishes (Taborsky and Limberger 1980), relating to variation in prey quality; (3) Do species-specific differences in
social structure (i.e., solitary, paired, or grouped) or degree of
competitiveness influence feeding rate? If feeding rates of
butterflyfishes are limited by predation, solitary fishes might
be expected to feed much more slowly compared to fishes
feeding in pairs or larger groups (Magurran and Pitcher
1983). The theory of competitiveness and its relationship
with feeding rate is more complicated. It was expected that
competitively dominant species would be less constrained
and/or able to monopolise high-quality prey items, and thus
feed more rapidly in the presence of con-specifics (Milinski
and Parker 1991). However, it could also be argued that
competitively dominant fish spend more time defending
territories than their subordinates, and hence have a
depressed feeding rate (Elliott 2002).
Materials and methods
Feeding rates of butterflyfishes were obtained from feeding
observations conducted between January 1995 and February 2002, at Lizard Island (14°400 S, 145°270 E), in the
northern section of the Great Barrier Reef, Australia.
Feeding observations were conducted for a total of 20
different species, including species from three distinct
feeding guilds: obligate corallivores, facultative corallivores, and non-corallivores, categorised following
Pratchett (2005). Feeding observations were conducted for
at least 23, and up to 314, haphazardly selected individuals
of each species (Table 1). During feeding observations,
individual butterflyfish were followed for 3 min, recording
the number of bites taken from each species of scleractinian (hard coral), alcyonarian (soft coral), or any other
macro-invertebrate (e.g., Tridacnid clams). The number of
bites taken on unidentified prey items from consolidated
reef pavement, coral rubble, or sandy substrate was also
recorded. These species were most likely feeding on small
invertebrates (Zekeria et al. 2002), but no attempt was
made to identify the specific source of prey for butterflyfishes feeding on these reef substrates. Observers moved
through the study sites methodically to avoid resampling
individual fishes. More detailed descriptions of sampling
methodology are provided in Berumen and Pratchett
(2006) and Pratchett (2005).
Bite rates of butterflyfishes (specifically, the mean number of bites taken in each 3-min observation) were compared
among species and among feeding guilds. Three distinct
feeding guilds were recognised based on proportional
Gonochaetodon
Megaprotodon
Corallochaetodon
Discochaetodon
Tetrachaetodon
Discochaetodon
Exornator
Rabdophorus
Lepidochaetodon
Tetrachaetodon
Lepidochaetodon
Rabdophorus
Rabdophorus
Rabdophorus
Rabdophorus
Rabdophorus
Rabdophorus
Rabdophorus
Chelmon
Rabdophorus
C. baronessa
C. trifascialis
C. lunulatus
C. aureofasciatus
C. plebius
C. rainfordi
C. citrinellus
C. rafflesi
C. kleinii
C. speculum
C. unimaculatus
C. melannotus
C. ulietensis
C. lunula
C. ephippium
C. vagabundus
C. semion
C. auriga
Ch. rostratus
C. lineolatus
NC
NC
NC
NC
NC
NC
FC
FC
FC
FC
FC
FC
FC
FC
OC
OC
OC
OC
OC
OC
Guild
0.000
0.008
0.000
0.060
0.047
0.043
0.660
0.308
0.400
0.321
0.595
0.637
0.227
0.802
0.901
0.965
0.923
0.991
0.999
1.000
Proportional bites
on hard corals
2.98 (27), 0.65
4.32 (32), 0.38
5.97 (23), 0.67
5.16 (105), 0.31
6.41 (110), 0.24
7.56 (48), 0.62
3.26 (28), 0.28
4.8 (30), 0.47
4.9 (46), 0.4
4.92 (32), 0.66
5.33 (25), 0.86
7.06 (94), 0.35
7.85 (35), 1.61
8.32 (114), 0.36
5.94 (40), 0.56
6.88 (105), 0.37
7.8 (41), 0.99
10.22 (302), 0.3
12.29 (314), 0.27
11.25 (71), 0.61
Total mean b.p.m.
(n), ±SE*
3.19 (16), 0.38b
1.69 (15), 0.36b
5.69 (14), 0.53a
4.58 (12), 1.27a
3.83 (2), 2.17b
5.74 (14), 0.95
5.85 (38), 0.57
7 (33), 0.52
8.67 (6), 1.65
2.83 (4), 0.4
4.88 (11), 0.84
5.67 (16), 0.84
2.94 (6), 0.84
4.76 (7), 0.64
7.55 (31), 0.56
12.33 (13), 4.0
8.09 (34), 0.50
5.28 (25), 0.67
6.34 (29), 0.75
6.33 (9), 0.91
4.75 (36), 0.54
6.22 (47), 0.34
7.5 (39), 0.71
3.25 (20), 0.34
4.59 (17), 0.48
4.29 (28), 0.41
5.41 (22), 0.89
5.95 (14), 1.44
6.71 (30), 0.68
5.42 (16), 0.51
7.76 (48), 0.61
7.04 (15), 0.95
6.46 (46), 0.51
6.97 (12), 1.86
10.04 (100), 0.53b
11.78 (111), 0.45
9.03 (22), 0.98
4.8 (31), 0.44
6.07 (30), 0.44
6.11 (3), 2.47
3.75 (4), 0.98
6.17 (2), 4.83
7.33 (2), 0.0
5.17 (4), 1.22
4.17 (4), 1.69
6.91 (33), 0.58
4.61 (6), 1.76
9.42 (32), 0.73
8.04 (30), 0.72
8.00 (19), 1.54
11.32 (142), 0.46b
7.92 (60), 0.51a
8.43 (10), 1.88
13.06 (134), 0.40
12.6 (24), 1.04
11.6 (69), 0.58
11.91 (25), 1.06
5.29 (58), 0.43
2.19 (14), 0.72
4.55 (11), 0.64
1.19 (7), 0.18
4.21 (21), 0.48
5.01 (47), 0.44
6.25 (57), 0.33
9.05 (32), 0.73a
4.89 (15), 0.76b
6.59 (53), 0.37
3.45 (17), 0.39
5.03 (11), 0.83
4.97 (12), 0.97
5.35 (17), 0.71
5.44 (15), 1.12
7.07 (46), 0.52
8.68 (24), 2.28
8.79 (60), 0.52
5.00 (9), 1.01
6.85 (50), 0.53
10.21 (14), 2.03
10.61 (231), 0.36
12.06 (200), 0.33
10.12 (27), 1.04
2.97 (11), 0.38
4.67 (19), 0.58
4.72 (32), 0.44
4.79 (13), 1.32
5.17 (10), 1.4
7.04 (48), 0.47
6.63 (10), 1.05
7.78 (51), 0.52
6.22 (31), 0.66
6.91 (54), 0.53
6.65 (26), 1.05
8.72 (68), 0.47
12.64 (111), 0.45
11.94 (44), 0.75
Paired
Alone
1400–1800 h
0600–1000 h
1000–1400 h
Mean b.p.m. by social unit (n), ±SE
Mean b.p.m. by time of day (n), ±SE
a,b
Statistically similar values within each comparison (a = 0.05)
* Data set with significantly different values (see Table 2 for post-hoc results)
Total b.p.m., b.p.m. arranged by time of day, and b.p.m. arranged by social unit are reported. The proportional number of bites on hard corals is also reported. Subgenera are from Smith et al.
(2003); feeding guilds (OC = obligate corallivores, FC = facultative corallivores, and NC = non-corallivores) are from Pratchett (2005)
Subgenus
Species
Table 1 Mean bites per minute (b.p.m., ±SE ) of all Chaetodontid species
Coral Reefs (2008) 27:583–591
585
123
586
Coral Reefs (2008) 27:583–591
ns
ns
ns
ns
ns
*
ns
ns
ns
ns
ns
*
ns
*
ns
ns
*
ns
ns
ns
*
*
*
*
*
*
ns
ns
ns
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
*
*
ns
ns
ns
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
*
*
*
ns
ns
ns
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
*
*
*
*
*
ns
*
*
*
ns
ns
ns
ns
*
*
ns
ns
ns
ns
*
*
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
ns
ns
ns
*
*
C. vagabundus
C. ephippium
C. lunula
C. ulietensis
C. melannotus
C. unimaculatus
*
*
*
ns
ns
ns
*
ns
*
ns
*
*
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
ns
ns
ns
ns
*
*
*
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
*
*
ns
*
ns
*
ns
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
ns
*
C. lineolatus
ns
ns
*
*
*
*
*
ns
ns
ns
*
*
*
*
*
*
ns
ns
ns
ns
ns
Ch. rostratus
*
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
*
*
*
ns
ns
ns
ns
C. speculum
*
*
ns
ns
ns
*
C. auriga
ns
ns
ns
ns
ns
ns
ns
ns
*
ns
ns
ns
*
ns
*
*
*
*
ns
ns
C. semion
*
*
*
ns
C. kleinii
ns
ns
ns
ns
ns
ns
ns
ns
ns
*
ns
ns
ns
ns
ns
*
C. plebius
C. aureofasciatus
C. lunulatus
*
*
*
ns
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
C. rafflesi
ns
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
ns
C. citrinellus
ns
ns
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
C. rainfordi
C. baronessa
C. trifascialis
C. lunulatus
C. aureofasciatus
C. plebius
C. rainfordi
C. citrinellus
C. rafflesi
C. kleinii
C. speculum
C. unimaculatus
C. melannotus
C. ulietensis
C. lunula
C. ephippium
C. vagabundus
C. semion
C. auriga
Ch. rostratus
C. lineolatus
C. trifascialis
C. baronessa
Table 2 Tukey post-hoc analysis results for multiple contrasts ANOVA comparing bite rates of Great Barrier Reef butterflyfish (Chaetodontidae) species
*
*
*
ns
ns
ns
*
ns
*
ns
ns
ns
ns
ns
*
ns
ns
ns
*
*
*
*
*
*
*
*
*
ns
ns
*
*
ns
*
*
*
*
ns
ns
* Significant difference in bite rate, ns indicates no significant difference (a = 0.05)
consumption of hard (scleractinian) corals: (1) obligate corallivores, which take [80% of bites from corals, (2)
facultative corallivores, which take between 20 and 70% of
bites from hard corals, and (3) non-corallivores, which take
\5% of bites from hard corals. Assignment of species to
feeding guilds follows Pratchett (2005). Interspecific variation in the bite rates of butterflyfishes were analysed using a
two-way nested ANOVA with species nested within feeding
guild to test for variation both within and among feeding
guilds. However, related species do not represent statistically independent data, such that comparisons involving
conventional statistics may be invalid (Felsenstein 1985;
Harvey and Pagel 1991). For example, the obligate corallivores in this study belonged to a single monophyletic group
(Fessler and Westneat 2007). To circumvent this problem,
phylogenetic analyses were undertaken using a pruned
phylogeny of a recent molecular phylogeny of the butterflyfishes (Fessler and Westneat 2007) that included 18/20
species examined in this study. As Chaetodon aureofasciatus and Chaetodon lunulatus were absent from the
phylogeny these species were placed with their closest relative/sibling species (i.e., Chaetodon rainfordi and
Chaetodon trifasciatus, respectively) (Kuiter 1995).
To examine the evolution of mean bite rate in response
to the % hard coral consumed by 20 species of
123
butterflyfishes, standardised phylogenetic independent
contrasts were calculated using PDTREE (Garland et al.
1992). Traits were standardised by dividing the independent contrast of each trait by the standard deviation of the
branch length (square root of the corrected branch lengths)
of that trait (Garland et al. 1992). As there were no significant linear or non-linear trends in the data, all branch
lengths were deemed adequately standardised as required
under a Brownian motion model of evolution. Percentages
were converted to proportions and arcsine square-root
transformed prior to analyses to achieve normality Quinn
and Keough (2002). The independent contrasts of ‘mean
bite rate’ and ‘% hard coral’ consumed were compared
using regression analysis.
Independent ANOVA was then used to test for variation in
bite rates within species, both between solitary versus paired
individuals and at different times through the day. Bonferroni-corrected alpha-levels were used to assess significance
across the 20 separate analyses. Feeding rates of solitary
versus paired individuals were analysed separately for each
species, using one-way ANOVA. To further test the influence of competition on feeding rates of butterflyfishes,
interspecific variation in feeding rates of butterflyfishes was
related to a dominance hierarchy derived by Berumen and
Pratchett (2006), where competitive dominance was
Coral Reefs (2008) 27:583–591
14.00
12.00
Mean Bites per Minute
Fig. 1 Mean number of bites
per minute of butterflyfishes
(±SE) in the genera Chaetodon
and Chelmon. Colour coding
represents feeding guilds
(OC = obligate corallivores,
black bars; FC = facultative
corallivores, grey bars;
NC = non-corallivores, white
bars)
587
10.00
8.00
6.00
4.00
2.00
C
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ar
on
es
C
sa
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as
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C
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is
C
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C
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C
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C
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C
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C
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0.00
quantified based on the proportion of aggressive interactions
between individual fish. Rank correlation was used to test
whether feeding rates of butterflyfishes were related to
competitive dominance across 8 different species for which
competitive interactions have been directly quantified.
Feeding observations were conducted throughout the
day, with approximately equal sampling within each of
three pre-designated time periods: morning (0600–1000 h),
mid-day (1000–1400 h), and afternoon (1400 h–1800 h).
No nocturnal foraging was ever witnessed, or has ever been
recorded, for the 20 species considered in this study (cf.
Zekeria et al. 2002). To test for diurnal variation in feeding
rates of butterflyfishes, average feeding rates of each species were compared among the three different time periods
using a series of one-way ANOVAs. Data collected for
each species were essentially independent, but Bonferronicorrected alpha-levels were still used to test for significance across the 20 separate analyses. All data were
square-root transformed prior to analyses to satisfy
assumptions of normality and univariate homogeneity.
Results
Mean bite rates varied significantly among species (Fig. 1)
(F19, 1602 = 23.4, P \ 0.01), ranging from 2.98 (±0.65 SE)
bites per minute (b.p.m.) for Chaetodon lineolatus, up to
12.29 (±0.27 SE) b.p.m. for Chaetodon baronessa (Tables 1
and 2). Much of the variation in feeding rates was ostensibly
related to differences in major dietary items. Notably, mean
bite rates varied significantly among feeding guilds (F2,
1619 = 6.56, P \ 0.001), where obligate corallivores had the
highest rate of feeding, taking a mean of 10.34 (±0.18 SE)
b.p.m., compared to 6.53 (±0.23 SE) b.p.m. for facultative
corallivores, and 5.7 (±0.18 SE) b.p.m. for non-corallivores
(Table 3). There was no significant difference in the feeding
rates between facultative corallivores and non-corallivores.
Obligate coral-feeders (C. aureofasciatus, C. baronessa, C.
lunulatus, Chaetodon plebius, C. rainfordi, and C. trifascialis) also represent a single monophyletic group, distinct
from facultative and non-coral feeders, so independent
contrasts were necessary to separate effects of ecology and
phylogeny. Bite rates of butterflyfishes were significantly
and positively related to the proportion of bites taken on hard
corals by each of the 20 species (r2 = 0.40, n = 20,
P \ 0.01, Fig. 2), and the results from the phylogenetically
corrected data were congruent with the uncorrected data.
The relationship between standardised independent contrasts for mean bite rates versus standardised independent
contrasts for % coral consumption was weaker compared to
the uncorrected data, but nonetheless significant (r2 = 0.29,
n = 19, P \ 0.05, Fig. 3).
All butterflyfishes were active during daylight hours and
spent virtually all their time feeding. Only C. lunulatus,
Table 3 Mean bites per minute (b.p.m., ±SE) and mean b.p.m. arranged by time of day for three Chaetodontid feeding guilds
Feeding guild
Total mean b.p.m. (n), ±SE
Mean b.p.m. by time of day (n), ±SE
0600–1000 h
Obligate Corallivores
Facultative Corallivores
Non-corallivores
a,b
a
9.79 (194), 0.35
6.53 (404), 0.23b
7.31 (87), 0.43b
10.34 (873), 0.18
5.7 (345), 0.18
b
5.4 (66), 0.32
1000–1400 h
b
1400–1800 h
a
11.09 (380), 0.28
9.73 (299), 0.30b
5.77 (195), 0.267a
7.18 (122), 0.52b
6.04 (157), 0.28
5.43 (122), 0.32
Statistically similar values within each comparison (a = 0.05)
123
588
14.00
12.00
Mean Bites per Minute
Fig. 2 Regression of mean
number of bites per minute
against proportional bites on
scleractinian corals (r2 = 0.40,
P \ 0.01). Each data point
represents the mean bite rate of
all individuals studied for each
of 20 species. Colour coding
represents feeding guilds
(OC = obligate corallivores,
black dots; FC = facultative
corallivores, grey dots;
NC = non-corallivores, white
dots)
Coral Reefs (2008) 27:583–591
10.00
8.00
6.00
4.00
2.00
0.00
0.00
0.10
0.20
0.30
0.40
0.50
0.60
0.70
0.80
0.90
1.00
Proportional Number of Bites on Scleractinian Corals
10
Standardised independent contrasts of mean bite rates
Fig. 3 Regression of mean
number of bites per minute
(standardised for independent
contrasts) against proportional
bites on scleractinian corals
(standardised for independent
contrasts) (r2 = 0.29, P \ 0.05)
8
6
4
2
0
-0.4
-0.3
-0.2
-0.1
0
0.1
0.2
0.3
0.4
0.5
-2
-4
-6
-8
Standardised independent contrasts of % coral consumption
Chelmon rostratus and C. lineolatus displayed significant
diurnal variation in feeding rates. For C. lunulatus, mean
bite rates were much higher at mid-day (11.32 ± 0.46 SE
b.p.m.) and during the afternoon (10.04 ± 0.53 SE b.p.m.),
than in the morning (7.92 ± 0.51 SE b.p.m.) (F2,
302 = 10.82, P \ 0.01) (Table 1). Mean b.p.m. for Ch.
rostratus and C. lineolatus were significantly higher at
mid-day (5.69 ± 0.53 SE, 4.58 ± 1.27 SE, respectively),
than morning (3.83 ± 2.17 SE, no morning data for C.
lineolatus) or afternoon (3.19 ± 0.38 SE, 1.69 ± 0.36 SE,
respectively) (F2,.32 = 6.99, P \ 0.01; F2, 27 = 5.8,
P \ 0.05, respectively) (Table 1).
The diurnal feeding behaviour of each feeding guild was
also explored. Both facultative and obligate corallivores
displayed diurnal variation in bite rate: obligate corallivores had a higher bite rate during the mid-day time period
(F2, 870 = 7.36, P \ 0.01), while facultative corallivores
had a significantly lower bite rate during the same mid-day
period (F2, 401 = 6.54, P \ 0.01) (Table 3). In both guilds,
123
the morning and afternoon bite rates did not differ significantly from each other (Table 3).
In addition to differences among feeding guilds, there
was also significant variation in feeding rates of butterflyfishes within each feeding guild (F17, 1602 = 23.40,
P \ 0.01), accounting for 22% of overall variation. Interspecific variation in bite rates of butterflyfishes was partly
attributable to differences in the proportional targeting of
corals.
The influence of other butterflyfish on the feeding rate of
a focal fish was investigated in two ways during this study.
First, competitive behaviour towards another butterflyfish
was related to feeding rate. There was a positive correlation
(Pearson’s coefficient = 0.71, P \ 0.05) between mean
bite rates and competitive dominance (measured as
aggressive interactions) for eight of the species of butterflyfish examined in this study for which competitive
dominance has been previously quantified (Chaetodon
auriga, C baronessa, Chaetodon citrinellus, C. plebius, C.
Coral Reefs (2008) 27:583–591
trifascialis, C. lunulatus, Chaetodon vagabundus, Chaetodon kleinii) (Berumen and Pratchett 2006). Second, the
influence of pairing on feeding rate was examined. Within
species, significant variation in feeding rates among individuals related to their social arrangement was expected.
However, only Chaetodon ephippium exhibited significant
variation in feeding rates between solitary and paired individuals. Mean bite rates of paired C. ephippium
(9.05 ± 0.73 SE b.p.m., n = 32), were approximately twice
that of solitary individuals (4.89 ± 0.76 b.p.m., n = 15)
(F2, 47 = 15.24, P \ 0.01).
Discussion
Bite rates of butterflyfishes varied considerably among
species and among trophic groups (Fig. 1), with obligate
corallivores having a higher bite rate compared to facultative corallivores and non-corallivorous butterflyfishes
(Table 3). Moreover, there was a significant positive correlation between standardised independent contrasts for
mean bite rates versus standardised independent contrasts
for % coral consumption across all the 20 species (Fig. 3).
One possible interpretation of this is that corals are poorquality prey, as has been reported previously (Tricas 1985,
1989a). Tricas (1989a) estimated that the energetic intake
for butterflyfishes feeding on corals was 0.21–0.42 J per
bite. In contrast, the energetic intake for butterflyfishes
feeding on motile invertebrates is between 0.08 and 3.25 J
per bite, depending on whether they target smaller (100–
600 lm) or larger ([2 mm) prey items (Botrell and Robins
1984; Fleeger and Palmer 1982). Assuming that non-corallivorous butterflyfishes target larger prey items, then
energetic intake from feeding on motile invertebrates may
be as much as 10 times the energetic intake derived from
coral feeding. In this case, corallivores would indeed need
to have a higher bite rate to obtain a similar energy intake
to non-corallivores, though considerable research is
required to identify specific sources of prey for non-coral
feeding butterflyfishes and quantify the energetic content of
these prey items (Pratchett 2007).
Higher feeding rates among corallivores compared to
non-corallivores may also be related to differences in the
time required to find suitable prey. When feeding on corals,
some butterflyfishes exhibit intense feeding bouts (up to 20
bites in quick succession), after which they tend to move to
a new patch of coral tissue (on either an entirely new
colony or on different parts of larger colonies) and begin
searching (Tricas 1989a), possibly looking for polyp clusters with greatest expansion (Gochfeld 2004). Coralfeeding butterflyfishes typically spend very limited time
searching for prey (Tricas 1985). In contrast, butterflyfishes
feeding on unidentified prey items on non-coral substrates
589
undertake lengthy inspections (up to 1 min) of the substrate
before nearly every bite. The time required to identify
small discrete prey items will certainly constrain the
maximum possible bite rates for non-coral feeders, though
butterflyfishes that bite at exposed tentacles of discrete
coral polyps must carefully choose feeding locations to
maximise the amount of material consumed with each bite
(Gochfeld 2004). Moreover, the morphology of corals
limits the amount of tissue consumed with each bite (Tricas
1989a). Few butterflyfishes have sufficiently robust jaws to
bite into the carbonate skeleton of scleractinian corals and
so bite size is generally limited by tissue depth (Motta
1988). Irrespective of prey ‘‘quality’’, corallivorous butterflyfishes may need to feed at a faster rate or for a longer
time period to ingest similar quantities of food compared to
species feeding on discrete prey items (Birkeland and
Neudecker 1981; Tricas 1985, 1989b).
Many organisms, especially herbivores, exhibit distinct
diurnal patterns of feeding activity (Choat and Clements
1993), tending to maximise feeding when prey is most
valuable (Taborsky and Limberger 1980; Zoufal and Taborsky 1991; but see Zemke-White et al. 2002). This study
indicated that very few butterflyfishes varied their feeding
behaviour through the day; however, obligate corallivores
as a group had a higher bite rate during the middle of the
day than other time periods (Table 3). This pattern is
consistent with studies showing that the nutritional quality
of coral and algal species is highest at mid-day (Crossland
et al. 1980; Zoufal and Taborsky 1991). Similarly, Harmelin-Vivien and Bouchon-Navaro (1983) and Zekeria
et al. (2002) reported that feeding rates of butterflyfish
species vary through the day. Although not explicitly tested, this suggests that corallivores may be exploiting their
prey when most nutritionally beneficial.
In addition to significant interspecific variation in feeding rates among species, there was also significant
variability amongst species within the same feeding guild.
The above-mentioned trade-off between feeding rate and
search time may be responsible for this. Specialised corallivores may take 80 to [99% of their total bites from hard
corals. One species of butterflyfish has been recorded taking
88% of its total number of bites from just one coral species
(Pratchett 2005). Extreme dietary specialisation may facilitate increased feeding rates as fishes inspect only a few
closely positioned coral colonies, reducing search time
(Tricas 1985). However, even among the obligate corallivores, all of which took [90% of bites from scleractinian
corals, there was a greater than two-fold difference in
feeding rate between the fastest and slowest feeders
(Fig. 1). Highest feeding rates were recorded for C. baronessa and C. trifascialis, which are the most specialised
corallivorous butterflyfishes (Pratchett 2007) and are also
competitively dominant (Berumen and Pratchett 2006).
123
590
Competitive dominance is strongly present among butterflyfish species, whereby most corallivorous species
maintain small, non-overlapping feeding territories and
attempt to exclude con-generic corallivores (Berumen and
Pratchett 2006). For this study, competitiveness was
determined from a dominance hierarchy (Berumen and
Pratchett 2006) that details aggressive interactions between
individuals. The results indicate that butterflyfishes feeding
at the highest rates are also highly competitive obligate
corallivores, although this was only restricted to eight of
the species studied. In theory, maintenance of feeding
territories will reduce time available for feeding, but it is
interesting in this study that the most aggressive fishes still
manage to have the highest feeding rates (i.e., obligate
corallivores). Alternatively, if competitive dominant obligate corallivores have higher-quality food within their
territories, then perhaps they obtain more energy per bite.
They would thus be expected to feed less than subordinate
competitors forced to consume poorer-quality resources
with potential impacts on their health (Pratchett et al. 2004;
Berumen et al. 2005). Competitive dominants could also
have exclusive access to areas with greatest prey density,
allowing them to feed more efficiently inside these territories, further reducing the searching time required. For
whatever reason, though, maintenance of feeding territories
seems to be a worthwhile energy investment for these
species.
Pairing is the predominant social strategy employed by
butterflyfishes (Roberts and Ormond 1992) and is largely
related to monogamous breeding (Pratchett et al. 2006).
However, pairing or grouping may also confer other benefits, such as increased foraging efficiency (e.g., Gregson
and Booth 2005), increased efficiency in defending feeding
territories (Roberts and Ormond 1992), and/or increased
vigilance against predators (Wilson 1980). Importantly,
mutual vigilance in con-specific aggregations should
increase the probability of predator detection (Clark and
Mangel 1986), consequently increasing the time each
individual can spend on other activities, such as feeding
(Wilson 1980; Werner and Mittlebach 1981). The results of
the present study, however, suggest that pairing had no
effect on feeding rate for these butterflyfish species (except
for the non-corallivore, C. ephippium, and also see Bonaldo
et al. 2005). For corallivorous butterflyfishes, it appears
that feeding rates are maximised irrespective of social
organisation, and pairing may or may not increase survivorship due to foraging gains (Pratchett et al. 2006).
This study has revealed significant variation in feeding
rates of sympatric butterflyfish species and guilds at Lizard
Island, northern Great Barrier Reef. Social strategy and
time of day influenced the feeding rates of few individual
species, though two of the three feeding guilds exhibited
distinct patterns of feeding through the day. For eight of the
123
Coral Reefs (2008) 27:583–591
study species, there was a positive correlation between bite
rate and aggressive interactions, suggesting that corallivorous species may be a more competitive guild. Apparent
variation in feeding rates between corallivorous and noncorallivorous butterflyfishes may be best explained in terms
of the time required to find their respective prey items,
although the nutritional quality of corals relative to other
potential prey items remains unclear and warrants further
investigation.
Acknowledgements Comments from two anonymous reviewers
greatly improved this manuscript. This research was funded by a
Merit Research Grant from James Cook University awarded to MSP
and a Graduate Research Fellowship from the National Science
Foundation (USA) to MLB. Field assistance was provided by A.H.
Baird, R. Thomas, and S.L. Watson. The authors are grateful to staff
at Lizard Island Research Station for ongoing logistical support.
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