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The effects of predation on the condition of soft corals

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Coral Reefs
https://doi.org/10.1007/s00338-020-01967-x
REPORT
The effects of predation on the condition of soft corals
Stephanie Garra1 • April Hall1 • Michael J. Kingsford1
Received: 31 December 2019 / Accepted: 7 June 2020
Ó Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract Soft corals are well known for producing toxic
and unpalatable compounds to deter predation. In spite of
these antipredation defences, a suite of specialised preda-
tors has coevolved to feed on soft corals. Direct quantifi-
cation of this predation, however, has been minimal and the
influence of predation on soft corals is yet to be investi-
gated. In this study, the intensity and importance of pre-
dation by fishes on soft corals were evaluated across two
locations using descriptive and experimental approaches.
Thirty-six percent of soft coral colonies surveyed in the
Palm Islands were found to have bite marks, with up to 40
bite marks observed on a single colony. Soft coral was also
the major dietary component of the two fish species stud-
ied, representing up to 90% of bites taken by Chaetodon
melannotus and 87% of bites by Neoglyphidodon melas,
despite constituting less than 30% of the substratum.
Simulated predation in manipulative experiments was
found to have no clear effects on colony condition for two
soft coral genera of contrasting morphology (Litophyton:
branching and upright colonies, and Lobophytum: massive
and lobate colonies). Both species showed a high capacity
for recovery, with bites healing over the duration of the
experiments and in most instances within 31 days. In
contrast to the widespread assumption that predatory
Topic Editor Michael Lee Berumen
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s00338-020-01967-x) contains sup-
plementary material, which is available to authorized users.
& Stephanie Garra
stephanie.garra@my.jcu.edu.au
1 using specialised enzymes (e.g. common egg cowrie Ovula
ARC Centre of Excellence for Coral Reef Studies and
College of Science and Engineering, JCU, Townsville,
QLD 4811, Australia
interactions between fishes and soft corals are minimal, the
results of this study indicate that predation can be intense
but is not immediately important to soft coral colonies
under current climatic conditions.
Keywords Corallivory  Reef fishes  Soft coral  Predation
Introduction
Soft corals (Order Alcyonacea) are a key component of the
coral reef benthos, ranked second in abundance only to
hard corals (Alderslade and Fabricius 2019). While typi-
cally constituting 2–25% of the substratum (Dinesen 1983;
Fabricius and Alderslade 2001), soft corals can represent
greater than 80% of benthic cover (Fabricius 1997).
Despite their abundance, soft corals have been considered
of low importance to reef-associated organisms, especially
fishes. Lacking a protective external skeleton, soft corals
rely on the production of an array of compounds that
function as a chemical defence against potential predators
(La Barre et al. 1986). These compounds are widespread
across the Alcyonacea and highly effective: 90% of soft
coral species are estimated to deter feeding by fishes, and
50% are considered ichthyotoxic (La Barre et al. 1986). For
this reason, habitat associations and biological interactions
with soft corals, particularly predation, are traditionally
considered minimal.
Although this chemistry appears capable of deterring the
majority of predators, both fish and invertebrate predators
of soft coral have nonetheless coevolved. These specialists
target soft corals and may detoxify harmful compounds
ovum [Mollusca]: Coll et al. 1983; Teardrop butterflyfish
Chaetodon unimaculatus [Perciformes]: Maldonado et al.
123

2016). The intensity and importance of this predation,
however, have not been determined.
In systems such as coral reefs where competition for
space is intense, predation and herbivory represent chronic
controls over space utilisation and community composition
(Benayahu and Loya 1977). Benthic organisms may be
subject to consistent predation that implicates a continual
loss of tissue rather than direct immediate mortality and
can, in some cases, result in a substantial loss of an indi-
vidual’s biomass (Ayling 1981; Meesters et al. 1994).
Energy and other resources for demographic processes are
often diverted to healing and regeneration following injury
(Meesters et al. 1997) causing sub-lethal effects such as
reductions in growth rate (Meesters et al. 1994; Rotjan and
Lewis 2005) and fecundity (Priori et al. 2015). By influ-
encing reproduction as well as growth, predation has the
capacity to not only influence colony health and survival,
but the abundance and distribution of populations (Neu-
decker 1979; Cox 1986; Grottoli-Everett and Wellington
1997).
Studies of hard coral also suggest that colony condition
and prior damage may stimulate further feeding by
predators. Several hard corallivores are highly selective
towards injured corals (e.g. Tubelip wrasse Labrichthys
unilineatus: McIlwain and Jones 1997; butterflyfish
Chaetodon auriga, C. ephippium, C. vagabundus: Pratchett
2005). It has been suggested that predators respond to
olfactory attractants released with mucus from injury sites
(McIlwain and Jones 1997). Griffith (1994) suggested that
soft coral predators visually select colonies with bite scars,
based on the observation that the majority of colonies with
bite scars had more than one. The response of soft coral
predators to colony injury, however, is yet to be formally
assessed or quantified.
As a major component of the reef benthos, soft corals
interact and compete for space with other habitat-forming
organisms such as hard corals. An understanding of the
factors influencing their health, abundance and distribution
is therefore critical to predicting shifts in fitness and
dominance on the reef substratum, both now and into the
future. Changes in abundance in turn influence the reef
fauna which rely on habitat resources such as shelter and
food, and thus affect the overall reef assemblage. Predation
therefore represents a currently overlooked yet potentially
important mechanism regulating soft coral populations and
the reef community.
The overall objective of this study was to evaluate the
intensity of predation experienced by soft corals and the
impacts of predation on the condition of soft coral colonies.
The specific aims were to: (1) quantify the intensity of
predation on soft corals using behavioural observations of
two known soft coral predators (Chaetodon melannotus
and Neoglyphidodon melas) in conjunction with
123
Coral Reefs
quantitative surveys of soft coral availability and bite mark
occurrence on soft coral colonies, and (2) use manipulative
experiments to determine the impact of predation on two
genera of soft corals of contrasting morphology (Litophy-
ton sp. and Lobophytum sp.) and examine predatory
behaviour following tissue damage. In this study, the term
‘soft coral’ will be used to refer to all members of the
Order Alcyonacea with the exception of gorgonian corals,
which differ morphologically by possessing a supportive
internal axis (Fabricius and Alderslade 2001).
Materials and methods
Intensity of predation on soft corals
The intensity of predation on soft corals was quantified
with two methods: behavioural observations of soft coral
predation by fishes and surveys of bite marks on soft coral
colonies.
Observations of soft coral predation by fishes
The blackback butterflyfish Chaetodon melannotus and the
black damselfish Neoglyphidodon melas were selected as
study species as both have been previously defined as soft
coral-feeding fishes (C. melannotus: Epstein and Kingsford
2019; Pratchett 2005, 2007; N. melas: Chan 2007; Epstein
and Kingsford 2019) and were abundant in the study areas.
The feeding behaviour of C. melannotus and N. melas
was observed and quantified across multiple sites (Table 1)
in the Palm Island group and Capricorn Bunker group, two
locations separated by approximately 800 km on the Cen-
tral and Southern Great Barrier Reef. Sites within each
location were chosen to encompass variation in the pro-
portional cover of soft and hard corals; however, all sites
had a minimum of 5% soft coral cover. This design
allowed for the generality of soft coral predation to be
assessed at a range of spatial scales and across variation in
the composition of benthic habitats. N. melas observations
were only conducted at four sites within the Palm Island
group due to low abundance.
Prey consumed by fishes was quantified for a minimum
of four individuals of each species. Fish were randomly
encountered and observed for 6–10 min at each site, with
the resultant data expressed as the percentage of total bites
per prey category. A minimum distance of 2 m was
maintained in order to limit disruption of natural beha-
viours by the observer. All observations were conducted
between 0830 h and 1730 h on three days between
February and May 2018.
During each observation period, the total number of
bites taken from soft corals and any other benthic
Coral Reefs

Table 1 Locations of study and sites within locations, number of replicates for feeding observations of Chaetodon melannotus and Neo-
glyphidodon melas and natural bite mark surveys
Location Site Feeding observations (n fish) Bite mark surveys
(n transects)
C. melannotus N. melas

Palm Island Group Pelorus Island North 6 4 2

0 00
18° 37 06 S Pelorus Island South 4 0 2
146° 290 3700 E Pelorus Island North West 0 0 2
OI, Cattle Bay 5 6 1
OI, Pioneer North 6 5 2
OI, Pioneer South 6 4 1
Capricorn Bunker Group Fitzroy Reef 4 0 0
23° 140 5400 S OTI, Wistari 9 0 0
151° 460 4100 E OTI, Long Bank 4 0 0
OTI, South Entrance 4 0 0
OI Orpheus Island, OTI One Tree Island

organisms or substrata was recorded. We were confident
that bites taken from soft coral represented the consump-
tion of soft coral, as close inspection showed that fishes
removed either polyps or pieces of tissue. We did not
attempt to identify the specific prey items consumed from
rubble and pavement substrata with epilithic or crustose
coralline algal cover. While it was expected that fishes fed
on macroinvertebrates present in these substrata, detritus
and algae may also have been ingested. In these cases, prey
type was recorded as ‘turf algae’. As morphological simi-
larities among soft corals impede accurate visual identifi-
cation to species level in the field, soft corals were
identified to genus according to Fabricius and Alderslade
(2001). In the event that a coral or other prey item could
not be identified, photographs were taken for later identi-
fication. Gorgonians, although also members of the order
Alcyonacea, were treated as a distinct category to all other
soft corals due to major differences in morphology.
Evidence of predation on soft corals
Predation intensity was also quantified based on the num-
ber of bite marks on all soft coral colonies, excluding
encrusting forms, within randomly selected 10 m by 2.5 m
areas at six sites within the Palm Island Group (Table 1).
Encrusting forms (e.g. Clavularia, Briareum) generally
formed large mats and tended to retract their polyps if
disturbed. As it was difficult to accurately identify bite
marks, these genera were excluded from surveys. It was
hypothesised that the size of soft coral colonies may
influence the extent of predation according to optimal
foraging theory (Hughes 1980; Pyke 1984). To assess the
influence of colony size, horizontal surface area was cal-
culated assuming all colonies were approximately elliptical
using equation of an ellipse S = p(d1d2)/4, where d1 and d2
are the minor and major colony axes, respectively. To
address the hypothesis that that colony condition may
influence predation, colonies were classified as ‘compro-
mised’ if they displayed wilting, pale tissues or large vol-
umes of mucus, and were otherwise classified as ‘healthy’.
Linear regression was used to assess the strength of the
relationship between the size and number of bite marks on
colonies by genus. Differences in the mean number of bite
marks between ‘healthy’ and ‘compromised’ colonies were
assessed using an unpaired t test.
Importance of predation
It was hypothesised that predation would negatively
influence the condition and survival of soft coral colonies.
To test this, two manipulative experiments were conducted
using two genera of soft coral with contrasting morpholo-
gies. Experiment One utilised soft corals of the genus Li-
tophyton which have an erect, branching form, while
Experiment Two was conducted on the typically massive
and lobate colonies of Lobophytum.
Experimental set-up
For Experiment One, small complete colonies of Litophy-
ton sp. were obtained from the outer edge of the lagoon at
One Tree Island and translocated into the inner lagoon
(approximately 2 by 3 km and 3–6 m deep). This process
was undertaken to isolate discrete colonies and create
distinct experimental units of a similar size (8–10 cm in
height). Colonies were removed by breaking up the rubble
substratum to which small colonies were attached.
Accordingly, each colony was collected intact and attached

123
 Coral Reefs

at the base to a fragment of substrate. Securing the base
substrate to the experimental arrays allowed colonies to be
attached without contact with colony tissue. It was esti-
mated that the distance between colonies reflected that
observed within natural systems, with no artificial effects
of crowding. Care was taken to ensure replicates of each
treatment included a range of sizes and locations on the
array to prevent bias. Five replicate arrays of six colonies
were installed within the lagoon. The location of the arrays
was protected from swell and surge, and at least 3 m deep
at all times. An acclimation period of 48 h was allowed,
following which all colonies showing evidence of necrosis
were either replaced or excluded.
Experiment Two was conducted in situ at Pelorus Island,
in the Palm Island Group. Lobophytum was chosen as the
experimental genus at this site, since a large percentage
(53%) of colonies had bite marks, bite marks were clear,
and the relatively simple lobate morphology of colonies
was conducive to monitoring for changes in condition.
Furthermore, the discrete nature of colonies allowed each
to be considered an independent experimental replicate and
enabled the in situ design of the experiment. A total of 24
colonies located on large bommies between 5 and 9 m in
depth were labelled and randomly assigned to the five
treatments (Table 2). To avoid potential influences of size,
care was taken to ensure colonies selected for the experi-
ment were within a narrow size range (100 and 1000 cm2
in surface area); data from the bite surveys indicated no
strong relationship between colony size and bite numbers
within this range. As it was unavoidable for coral colonies
to have some existing bite marks at the commencement of
the experiment, treatments were randomly allocated among
colonies so that the number of pre-existing bite marks
would not bias the results. The number of existing bite
marks on a colony was considered the baseline condition,
with ongoing assessments based on changes in time from
that point.
Experimental predation methods
To test the null hypothesis that predation does not nega-
tively influence colony condition and survival, soft coral
colonies were subjected to experimental predation regimes
involving artificial bites designed to replicate the intensity
and frequency of bites observed for each genus. As the
predominant bite type for Litophyton was small bites by
predators such as C. melannotus, predation was simulated
by using fine dissection scissors to remove a small group of
1–3 polyps from the apical point of the cluster of polyps at
the end of a single branch. In each case, the cluster was

Table 2 Experimental treatments applied to experimental Litophyton colonies at One Tree Island and Lobophytum colonies at Pelorus Island
Treatment n Frequency Number of To test the effects of and assess colony
recovery from
Bites per Rounds of Bites at
treatment treatments end

Experiment One: Litophyton colonies at One Tree Island

Control 4 NA 0 NA 0 Artefacts of design and underlying natural
fluctuations
Low 3 Once at start of 4 1 4 A single low-intensity predation event
experiment
Moderate 4 Once at start of 8 1 8 A single moderate-intensity predation event
experiment
High 3 Once at start of 16 1 16 A single high-intensity predation event
experiment
Repeat 4 Every 24 h 8 10 80 Chronic moderate-intensity predation
Experiment Two: Lobophytum colonies at Pelorus Island
Control 5 NA 0 NA 0 Artefacts of design, natural fluctuations and
predation
S1 4 Once at start of 1 1 1 A single, low-intensity predation event
experiment
S8 5 Once at start of 8 1 8 A single, high-intensity predation event
experiment
R1 5 F1: Every 48 h, F2: Every 1 F1:5, F2: 4 9 Chronic, low-intensity predation
24 h
R8 5 F1: Every 48 h, F2: Every 8 F1: 5, F2: 4 72 Chronic, high-intensity predation
24 h
F1 first field trip, F2 second field trip

123
Coral Reefs
selected randomly. Lobophytum was observed to be subject
to larger tissue bites, so bites were simulated by removing a
1–2 cm portion of coral tissue from the top of colony lobes
using fine dissection scissors. We were confident that this
replicated the bites observed on colonies of Litophyton and
Lobophytum.
Experimental treatments
For both experiments, colonies were randomly assigned to
treatment levels, which varied in the number and/or fre-
quency of experimental bites applied (Table 2). Treatment
levels were designed to test the effects of varying intensi-
ties of acute and chronic predation events. Treatment levels
in Experiment One were based on observations of feeding
by C. melannotus at One Tree Island, which tended to take
2–5 bites from a small area of the feeding substrate in quick
succession before moving to another colony or a different
area of the same colony. Eight bites were therefore con-
sidered a moderate predation impact, with the remaining
treatments determined around this number (Table 2).
Repeat treatments were applied once a day for 10 con-
secutive days.
In order to assess the long-term effects of predation and
capacity for recovery, Experiment Two was conducted
across three field trips of 10 days, 5 days and 1 day sepa-
rated by periods of 22 days and 387 days, respectively.
Treatments in this experiment were conducted at a low and
high level of one and eight bites, respectively (Table 2),
based on the range of bite marks observed on Lobophytum
colonies (Fig. 2). Treatments were randomly allocated
among colonies so that the number of pre-existing bites
(\ 9) would not bias the results. Single treatments were
designed to investigate the effects of a predation event at a
single point in time and assess recovery following either
one (S1) or eight bites (S8). Repeated treatments were
designed to represent chronic predation at both high and
low levels and determine the effects of continual tissue loss
on colony health. Repeat treatments (R1 and R8) therefore
involved applying experimental bites every 48 h (Fieldtrip
1; total of 5 rounds of treatments applied) and every 24 h
(Fieldtrip 2; total of 4 rounds of treatments applied) to
increase the frequency of injury. No treatments were con-
ducted during the third field trip, which was undertaken to
assess recovery only. A set of unmanipulated control
colonies were used to determine levels of natural variation
in colony condition and the number of bites made by nat-
ural predators (referred to hereafter as ‘natural bites’). As
no experimental bites were taken from the control colonies
(or for S1 and S8 colonies following the initial treatments),
a similar level of disturbance around the colony was per-
formed during each round of treatments in order to account
for effects of diver activity or disturbance at bite treatment
colonies.
Colony condition metrics
It was predicted that stress induced by experimental bites
would decrease colony condition, with colonies under more
intense experimental predation regimes demonstrating
greater declines in condition throughout the course of the
experiment. To assess this, photographs were taken of each
colony at the start of the experiment and before each round
of treatments, and a range of condition metrics were scored
for each colony. Decreases in condition were expected to
be evident as changes in the following metrics: colony
colour, turgidity, mucus load and necrosis (Table 3). The
level of each metric was recorded as a score between one
and five, with one relating to indicators of ‘healthy’ con-
dition and five representing indicators of ‘compromised’
condition.
Colour The expulsion of zooxanthellae (evident as tissue
bleaching) is a symptom of coral stress. Colony tissue
colour was therefore used as an indicator with white tissue
signifying high levels of stress.
Turgidity Colony turgidity was considered as the degree
of wilting and measured as the angle of deviation from the
projected growth axis of colony stems, such that for upright
colonies angles were generally between 0° and 90°, while
from 90° to 180° indicated drooping and the inability for
the colony to maintain turgor. This metric was only applied
to colonies of Litophyton in Experiment One, as the
Lobophytum colonies considered in Experiment Two were
flat and lobate rather than upright and branching.
Mucus load High mucus production is exhibited by corals
under stressful conditions (McIlwain and Jones 1997). Due
to low variation in the mucus category, the categories were
later pooled as either below three or greater than or equal to
three. As increased mucus production has been related to
sedimentation (Stafford-Smith et al. 1992; Stafford-Smith
1993), the level of sediment coverage was also recorded to
address this potential confounding factor.
Necrosis Few diseases have been reported for soft corals
(Slattery et al. 2013), which is generally attributed to their
production of antimicrobial compounds (Gomaa et al.
2016). As the resources required for the production of these
compounds may be diverted to allow for wound healing,
the incidence of necrosis on colonies was therefore also
noted and the extent categorised as a measure of colony
stress.
123
 Coral Reefs

Table 3 Metrics used to assess

Metric Metric value
the condition of Litophyton
colonies at One Tree Island in 1 2 3 4 5
Experiment One and
Lobophytum colonies in Experiment One: Litophyton colonies
Experiment Two Colour Pink-brown Brown–pink Pink Pale pink White
Turgidity 0°–29° 30°–59° 60°–89° 90°–119° 120°–180°
Mucus 0–4% 5–25% [ 25%
Necrosis 0–9% 10–19% 20–29% 30–40% [ 40%
Experiment Two: Lobophytum colonies
Colour Dark purple Purple Pink Pale pink White
Mucus 0–4% 5–25% [ 25%
Sediment 0–4% 5–25% [ 25%
Necrosis 0% Localised to bites 25–49% 50–74% 75–100%
Scores range from 1 (healthiest condition) to 5 (poorest condition). Turgidity categorised as angle of
deviation from growth axis. Mucus and sediment expressed as percentage coverage of total colony surface
area. Necrosis as percentage of total colony surface area affected

Experiment Two was also used to assess the likelihood
of a predatory feedback loop. It was predicted that bites on
colonies could stimulate further predation through the
release of olfactory attractants such as mucus. Accordingly,
those colonies receiving more experimental bites (R1 and
R8 treatments) were predicted to receive more natural bites
over the course of the experiment, relative to the control
colonies. To test this prediction, the number of new natural
bite scars evident on colonies was recorded throughout the
experiment for all treatments. Regression analysis was used
to test the nature and strength of the relationship between
the number of experimental bites and the number of natural
bites on R1 colonies, in which case a positive relationship
would be indicative of the stimulation of further feeding in
response to experimental bites. Only R1 colonies were used
for this analysis as tracking R8 bites quickly became highly
complex due to the accumulating number of experimental
bites and different stages of healing. The assumption of
independence for regression (Sokal and Rohlf 2012) was
violated by the data set; however, this was unavoidable and
no other analytical approach was suitable for addressing
this question. The number of bites before and after treat-
ments was also statistically compared using asymmetrical
ANOVA. This allowed variation to be tested both (a) be-
tween the controls and all treatments, and (b) among
treatments only, in two separate tests according to the
procedures outlined by Underwood (1997).
The immediate and short-term response of predators to
experimental predation was also considered by setting up
cameras at all control and R8 colonies. In the first field trip
of the experiment, cameras were started immediately
before treatments and recorded at least 45 min of footage
following treatments. In the second field trip of the
experiment, the cameras recorded 30–60 min of footage
both before and after the treatments. It was also intended
that the footage obtained is used to determine natural levels
of predation experienced by colonies that may not be
detectable from bite marks.
The healing of natural bite marks and experimental bites
over time was also assessed. It was predicted that if pre-
dation represented a substantial cost to colonies, healing
would be minimal. Bite marks were considered ‘healed’ if
the surface of the bite mark was level with surrounding
tissue, and the epithelium had formed over the bite site;
however, it was not required for polyps to have completely
regenerated or to be fully extended. Thus a ‘healed’ bite
mark may still be visible as a scar on the colony surface: a
portion of tissue paler than the rest of the colony with
polyps in the process of regenerating. Healing of bite marks
was also expected to occur more slowly for colonies with
more intense experimental predation regimes.
Results
Intensity of predation
Soft coral predation by fishes
Soft coral was the major dietary component for both fish
species, representing 87.5% of the diet of N. melas in the
Palm Island group on average, and 63.3% and 90.3% of the
diet of C. melannotus in the Palm Island group and
Capricorn Bunker group, respectively (Fig. 1). Average
soft coral cover at these locations was 17.6% (Palm Island
group) and 27.5% (Capricorn Bunker group). Bites were
also taken from gorgonians, Heliopora and sponges within
the Palm Island group; however, these prey types repre-
sented less than 3% of bites, on average, among all sites
and comprised less than 2% of overall benthic cover. N.

123
Coral Reefs

C. melannotus: Palm Island Group (N=28) C. melannotus: Capricorn Bunker Group (N=21) N. melas: Palm Island Group (N=17)
100 100 100
Percentage total bites

80 80 80

60 60 60

40 40 40

20 20 20

0 0 0

H (n= a e
H =10 e

(n ra

Sp =0) a

(n hid
H n= 2 r al

or = 6 l

ar 14 l

o r (n = r a l
Tu (n=0 ns

Tu (n ans
(n ge

Zo (n=0 e
H =26 e

(n r a
H = 2 r al

or = 7 l

Tu (n=3 ns

(n ge

G (n ora

H (n= ora
G (n ora

(n ga

(n r

g
(n g a

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ar 8)

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on

on
=0

=0
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(n c o

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t
=
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ni
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al
=

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ni

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io

io
io

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So
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Major benthic group

Fig. 1 Variation in percentage of total bites on benthic prey by C. percentiles, respectively, with central line indicating median.
melannotus and N. melas at the Palm Island group and Capricorn Whiskers indicate 10–90 quartiles, and outliers were indicated by
Bunker group. Data were pooled across observation periods at all sites hollow circles. N is the total number of fish observed, and n is the
within locations. Upper and lower edges of box indicate 25 and 75 number of fish to have taken bites from each major benthic group

melas took a small number of bites from turf algae and hard 60
Sinularia (n=233)

coral at Pioneer North, which combined represented 25% 50

of total bites, on average. Coverage of these groups was 15
31.1% (turf algae) and 23.4% (hard coral).
10 1 cm
C. melannotus was observed feeding alone or in groups
of up to five individuals and fed on soft corals by taking 5

small, discrete bites that removed either individual or small 0

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40
groups of polyps from coral colonies. Colonies responded
to these bites by retracting polyps neighbouring the bite
Lobophytum (n=70)
site. Due to the small size of polyps and re-extension of
60
Percentage of colonies

polyps following feeding, bites by C. melannotus were 50

barely visible retrospectively (Online Resource 1). C. 40
15
melannotus were sometimes observed returning to the same 1 cm
10
colonies during an observation period. In contrast, N. melas
removed larger portions of tissue, taking larger bites of 5

coral coenenchyme generally from the tips and protrusions 0

of colonies which left conspicuous bite marks (Online 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

Resource 1).
Sarcophyton (n=73)
100

Evidence of predation on soft corals 80

60
Bite marks were visible on 36% of all colonies surveyed, 1 cm
40
which comprised seven soft coral genera: Sinularia,
20
Lobophytum, Sarcophyton, Litophyton, Klyxum, Cladiella
and Xenia. There was variation in the shape and size of 0
0 1 2 3 4 5
bites marks, as well as the location of bite marks among Number of bites per colony

different genera. Bite marks on Lobophytum were generally

located on the top edge of the lobes and ridges or along the
perimeter of the colony and were generally long and thin
(approximately 0.5–4 cm in length and up to 1.5 cm in
width) and scalloped in shape (Fig. 2). On colonies where
lobes appeared more digitate, bite marks were located on
the tips or sides of lobes. Bite marks were rarely observed
on the flat surface of the colony: instead, bite marks on flat
Fig. 2 The frequency of bite marks by colony for all colonies at
the six Palm Island group sites on Sinularia, Lobophytum and
Sarcophyton soft corals as percentage of total colonies surveyed
areas appeared to be locations where lobes or fingers had
been bitten off completely.
Colonies of Sinularia are highly diverse in morphology;
however, those observed at the study sites tended to have
more knob-like or finger-like protrusions than Lobophytum

123

colonies. In most cases, bites on Sinularia were taken from
the tips of fingers or knobs (Fig. 2), occasionally appearing
to have removed the protrusion entirely. Bite marks were
therefore more circular in shape and resembled those
observed being made by N. melas. On colonies of Sarco-
phyton, bite marks were nearly always located on the edge
of the colony oral disc (sensu Hellström and Benzie 2011),
crescent shaped and generally greater than 2 cm in length
(Fig. 2). The size and shape of these bite marks and those
on colonies of Lobophytum were clearly different to those
made by N. melas. This species was unlikely to be the
corallivore responsible; however, no other predator was
identified.
The most bite marks were observed on colonies of
Lobophytum and Sinularia, of which approximately half of
all colonies were found to have evidence of more than one
bite. Colonies generally had between one and ten bite
marks, but up to 31 and 40 bite marks were recorded
(Fig. 2). The majority of Sarcophyton colonies lacked bite
marks and, at most, had a maximum of five bite marks. No
bite marks were distinguishable on colonies of Klyxum and
Litophyton. Only one colony each of Cladiella (n = 3) and
Xenia (n = 5) had bite marks (two and three, respectively);
however, bite marks were more difficult to distinguish on
colonies of these genera, being smaller and less fleshy that
those of alcyoniids.
The relationship between size of colony and the number
of bite marks evident was either weak or not significant.
For Sinularia colonies, the relationship between the num-
ber of bites per colony and size of colony was not signif-
icant (r2 = 0.01139, ANOVA for slope, F1,231 = 2.661,
p = 0.1). Size explained some variation in the number of
bite marks per Lobophytum colony; however, this rela-
tionship only explained 20% of the variation (n = 70,
r2 = 0.2059, ANOVA F1,68 = 17.63, p \ 0.001). There
was no significant difference in the number of bite marks
between healthy (2.02 ± 0.49) and compromised colonies
(3.17 ± 0.67) (t test, df = 198, t = - 1.390, p = 0.166).
Importance of predation
Experiment One
There were no substantial changes in the appearance of
experimental Litophyton colonies that could be attributed
to the different treatments and survivorship across the
experimental period was 100%. While there was variation
in condition among replicates throughout the experiment,
no consistent trends within treatments were detected and
there was little difference in metric values between the
beginning and end of the experiment for the majority of
replicates (Table 4). This was true for both treatments
bitten on a single occasion (low, moderate and high
123
Coral Reefs
treatments) and chronic treatments where bites were taken
at regular intervals (repeat treatment), as well as controls.
In the cases where the condition of replicates did decrease,
it did not reflect the level of damage inflicted by the
treatments applied (Table 4). With the exception of one
colony, the extent of tissue necrosis did not exceed 20% of
total colony surface area. One replicate assigned to the high
treatment had a score of three (20–29% necrosis) which
was maintained over 6 days before necrosis declined. All
other replicates in this treatment exhibited less than 10%
colony necrosis, and there was no evidence of higher levels
of necrosis in replicates of the repeat treatment.
No complete bleaching was observed during the exper-
iment. Although some paling of tissues was observed
across all treatments (including controls), tissue colour
scores were found to both increase and decrease between
assessments, and there were no negative trends in tissue
colour which exceeded three assessments without subse-
quent recovery.
High stochasticity in mucus production and turgidity
was observed across all treatments. High levels of mucus
were only recorded for one replicate with a low number of
bites. All other replicates exhibited variation between low
and medium levels of mucus, and no consistent pattern was
found among treatments or times. Similarly, colony
turgidity and degree of wilting encompassed the complete
range of metric values, but increased and decreased inde-
pendently among colonies. There was no clear effect of
experimental bites on Litophyton colonies relative to the
controls.
Experiment Two
Overall, there were no substantial changes in the appear-
ance of experimental Lobophytum colonies that could be
attributed to the different treatments. No instances of total
mortality were observed, and only 3 of the 24 colonies
showed signs of necrosis. In all cases, necrosis was loca-
lised to bite sites and therefore did not exceed 15% of the
surface area of any colonies.
Among the 19 treatment colonies, a total of 224 bites
were tracked by treatment over time. Eighty-five per cent
of these bites healed within 31 days of being inflicted, on
average healing after 27 days (± 0.4SE) and in a minimum
of 22 days. Recovery was consistent regardless of treat-
ment, with the percentage of bites healing within 31 days
roughly equivalent between R1 (80%, n = 20) and R8
(85%, n = 160) colonies and comparable to that of the S1
(75%, n = 4) and S8 (100%, n = 40) colonies, despite large
differences in the number of bites inflicted. Furthermore,
there was no evidence of an increasing trend in healing
time as bites on R1 and R8 colonies accumulated across
multiple treatment rounds. The remaining 29 bites were
Coral Reefs

Table 4 Mean and SE of

Treatment Time Metric
metric value of Experiment One
treatments, pooled across Colour Turgidity Mucus Necrosis
replicates, at the start and end of
the experimental period Mean SE Mean SE Mean SE Mean SE

Control Start 2.3 0.5 1 0 2 0.6 1 0

End 2.5 0.3 1 0 1 0 1.3 0.3
Low Start 2.3 0.7 1 0 1 0 1.3 0.3
End 3.3 0.3 3 1 2.3 1.3 1.3 0.3
Moderate Start 2.3 0.5 1 0 1 0 1.3 0.3
End 2.8 0.3 1.8 0.8 2 0.6 1 0
High Start 2 0 2.3 1.3 1 0 1.7 0.7
End 2 0 1.7 0.7 2 1 1.3 0.3
Repeat Start 2.3 0.5 1.5 0.5 3 0.8 1 0
End 2.8 0.5 2.5 1.0 2 0.6 1 0
Metric values represented a score between 1 (healthy condition) and 5 (compromised condition)

observed to have healed by the last field trip (maximum of
422 days after being applied). However, healing would
have occurred at any time between 32 and 422 days post-
treatment. Complete regeneration of lost tissue was evident
in 15 colonies 413–422 days post-treatment (e.g. Fig. 3).
Colour changes were limited only to minor variations,
with few colonies undergoing substantial colour changes
and no colonies exhibiting bleaching or white tissues.
Twenty-one of the 24 colonies exhibited minor variations
in colour which may have been associated with the degree
of contraction of colonies and extension of polyps. Three
colonies changed from pink-orange to a yellow-green
colour that was evident across multiple days and associated
with an increase in tissue rigidity. These colonies were all
part of the repeat treatment groups (R1: n = 2 of 5; R8:
n = 1 of 5); however, this response was not consistent with
other replicate colonies within the respective treatment
groups. This colour change instead appeared associated
with the withdrawing of polyps and contraction of colonies
following disturbance.
Small amounts of mucus were released from bite sites
immediately after tissue was cut during treatments. A thin
layer of mucus was also frequently observed across the
surface of bite marks. Overall level of mucus production,
however, appeared unrelated to treatments (Fig. 4).
Instead, colonies among treatments exhibited similar
changes in mucus load through time. High mucus load on
colonies generally occurred during periods of high turbid-
ity and high sediment load on colonies and therefore was
more linked to environmental conditions (Fig. 5).
Bites from natural predators also occurred on colonies
and healed during the experiment, in one instance within
14 days (Fig. 6, Online Resource 2). No predation events,
however, were captured in over 40 h of remotely recorded
video footage, suggesting that the bite marks observed
were from pulse events. There was no significant difference
in the mean number of natural bite marks among treatments
before manipulations or 96 h after the first treatment
(Fig. 7). Furthermore, no differences were detected either
between controls and treatments or among experimental
treatments (Table 5). No significant relationship was
detected between the number of natural bite marks and
cumulative number of experimental bite marks (linear
regression: r2 = 0.02023, ANOVA F1,43 = 0.89, p = 0.33).

2 days 4 days 30 days 417 days

Fig. 3 Process of healing of experimental bites on an R8 colony two days following infliction of bites, necrosis at bite sites four days after bites
were inflicted, healed bite scars 30 days following bites, completely regenerated tissue 417 days after bites

123
 Coral Reefs

Fig. 4 Examples of variation in

colour and mucus load over
time for select control and R8
replicate colonies

Control
Repeat 8

2 days 8 days 24 days

Mucus level ≥3 Sediment level ≥ 3

6 6

5 5

4 4 Control
Frequency

3 3 S1
S8
2 2
R1
1 1
R8
0 0

0 5 10 25 30 35 420 425 0 5 10 25 30 35 420 425

Days following first treatment Days following first treatment

Fig. 5 Frequency (number of replicates) for which mucus and sediment score were greater than or equal to three throughout the duration of the
experiment by treatment

Fig. 6 Number of natural bite marks on control (left) and repeat 1 marks (i.e. where the number of bites decreased between two
(right) colonies by time. Each line represents an individual replicate consecutive assessments)
colony. Blue lines indicate incidence of recovery by healing of bite

123
Coral Reefs
Mean number of natural bite marks (+SE)
5 Before
4
3
2
1 Reef (Fabricius 1995). This indicates that predation rates
0 assemblage and abundance of predators among the sites
Control
(0)
(Number of experimental bites after 96 hours)
Fig. 7 Mean number of natural bite marks evident on colonies (?SE)
before treatments (white) and 96 h after initial treatment (grey), for
replicates pooled by treatment category. R1 and R8 colonies had
received two rounds of treatments after 96 h
Accordingly, the null hypothesis that there was no response
by predators to an increased number of bite marks could
not be rejected.
Discussion
Soft corals are a diverse and ubiquitous component of
reefs, second only to hard corals in abundance (Alderslade
and Fabricius 2019). Despite their prevalence, the interre-
lationships between soft corals and fishes have been largely
overlooked, especially in terms of predation, and our
understanding of the extent to which fishes influence soft
corals through predation is limited. Given the importance
of predation as an ecological control over benthic assem-
blages, the lack of systematic and quantitative study of this
relationship represents a substantial gap in the overall
understanding of ecological dynamics on coral reefs.
Subject to both high-frequency large tissue bites and
loss of polyps, the soft corals in this study can be consid-
ered to be under intense chronic predation. Predation
pressure was found to be the sum of bites by C. melannotus
and N. melas, two species with contrasting feeding
Table 5 Asymmetrical
ANOVA on the number of
natural bite marks on
experimental colonies according
to treatment category, both
before commencement of
treatments and 96 h after initial
treatment
behaviour for which soft coral constituted the major dietary
component, and larger bites by an unknown predator, scars
After 96 hours of which were visible on the surface of colonies. The
proportion of colonies with bite marks (over one third of
colonies, with up to 40 bites observed on a single colony)
was more than 7 times greater than that reported by pre-
vious studies at Heron Island and Beaver reefs (Griffith
1994) and mid- and outer-shelf reefs of the Great Barrier
may vary spatially, most likely due to differences in the
S1 R1 S8 R8 considered by each study, but nonetheless can be intense.
(1) (2) (8) (16)
Treatment Unfortunately, the soft coral predators responsible for the
bite marks observed on Lobophytum colonies in this study
remain unknown despite over 40 h of remotely recorded
video footage. Large-bodied or large-mouthed fishes, based
on the size of bite marks observed, capable of tolerating the
toxic chemistry of soft coral tissue as well as embedded
spicules such as tetraodontids (Hiatt and Strasburg 1960)
and monacanthids (Ayling 1981) are likely candidates.
Other fishes observed to occasionally take bites from soft
corals such as pomacanthids (Konow 2005) were also
observed at the site. Pomacanthids were most abundant in
18–21 m (1.4 ± 0.9 per 400 m2) compared to the experi-
mental area 6–8 m (0 per 400 m2) and in shallow water (0
per 400 m2). Chance observations of siganids (Kuo et al.
2015) and sea turtles (anecdotal) have suggested their role
as soft coral predators; however, they were rarely observed
at the experimental site. The nocturnal mollusc O. ovum is
also a known soft coral predator (Griffith 1994); however,
their bite marks were distinctly different from those
observed. Crown-of-thorns starfish (Acanthaster planci),
despite being a major hard coral predator, rarely feed on
soft corals on the Great Barrier Reef (Keesing 1990) and
were not observed at the experimental site and therefore are
unlikely to be important predators of soft corals at the study
location. Nonetheless, the incidence of new bite marks on
colonies monitored for over a month gave a clear indication
that predation did occur during the experiment. That these
predation events were not observed suggests that predation
is likely to occur in intense, rare events by nocturnal and/or
transient predators.
Source of variation Analysis of variance
Before After 96 h
df Mean sq. F-ratio df Mean sq. F-ratio
Control versus treatments 1 3.88 0.63 1 3.10 0.37
Among treatments 2 6.18 0.98 2 8.45 1.10
Error 19 6.29 19 7.68
All NS for alpha level of 0.05
123

We found no evidence of a predatory feedback loop
from our experimental manipulations. Although the release
of mucus or toxic exudates was predicted to either promote
or deter further predation on soft coral colonies, the num-
ber of additional bite marks on the control colonies was at
least equal to that of any of the treatment colonies across an
experimental period of over 4 weeks. While tissue injury
has been found to be feeding stimulant for hard coral
predators such as the tubelip wrasse L. unilineatus, which
selected damaged tissue and exhibited short-term increases
in feeding intensity following tissue injury (McIlwain and
Jones 1997), there was no evidence of such an effect on
soft coral predators.
This study is the first to directly assess the effects of
predation on soft corals and is unique in the use of
manipulative experiments to quantify predation impacts.
While the effects of predation on gorgonians have been the
subject of past studies, to date the only consideration of the
effects of tissue loss to soft corals has been either the effect
of tissue injuries through crushing on the cold-water
octocoral Gersemia rubiformis (Henry et al. 2003), the
regeneration of Litophyton arboreum microcolonies
(12–15 mm) following dissection from parent colonies
(Tentori et al. 2004), and the asexual propogation of
fragments of Cladiella, Sinularia and Sarcophyton in
recirculating seawater systems following dissection from
parent colonies (Chaitanawisuti and Kritsanapuntu 2019).
The results of the two manipulative experiments presented
here (one conducted in situ and one involving translocation
of colonies) demonstrated that soft corals of two genera of
contrasting morphology were tolerant of tissue loss through
simulated predation, even under intense predation regimes.
While nephtheids are considered pioneer organisms with
rapid growth rates (e.g. Litophyton viridis: linear growth
averages 1.15 cm/month for colonies up to 26 cm; Tursch
and Tursch 1982) and alcyoniids have growth rates com-
parable to that of hard corals (e.g. Sinularia and Sarco-
phyton: 0.5–0.6 cm increase in diameter per year; Fabricius
1995), both species in this study were resilient to predation
and showed great powers of healing regardless of their
growth characteristics.
Lobophytum colonies demonstrated a strong capacity for
healing over relatively short time periods of up to 31 days.
This is perhaps unsurprising given the high regenerative
capacity demonstrated by other modular, sessile reef
invertebrates such as scleractinian corals (Henry and Hart
2005) and metazoans such as sponges (Wulff 2010) and
ascidians (Kürn et al. 2011). Rapid regeneration capacity
has been suggested to have evolved alongside asexual
reproduction strategies such as fragmentation (Karlson
1988), which soft corals generally favour (e.g. Bastidas
et al. 2004). These characteristics may confer tolerance to
tissue loss by predation. The healing capacity recorded for
123
Coral Reefs
Lobophytum in this study was more rapid than that reported
for the soft coral Sarcophyton by Griffith (1994) and
Fabricius (1995), who found that wounds from natural bites
took 2–3 months to heal. This difference cannot be
explained based on the results and may be related to a
number of factors including differences among genera, bite
size and ambient conditions. Similar rates of healing (7–12
days) have been demonstrated under artificial conditions
(within a recirculating seawater system) by fragments of
Cladiella sp., Sinularia sp. (min. 5mm in length) and
Sarcophyton sp. (25mm2) following dissection from parent
colonies (Chaitanawisuti and Kritsanapuntu 2019). Heal-
ing of soft corals in this study was also faster than that
demonstrated by pocilloporid hard corals under simulated
pufferfish predation, which involved inflicting excavating
bites which removed both colony tissue and skeletal car-
bonate (Palacios et al. 2014). While soft tissues may
require less energy and be less costly to regenerate than the
consolidated carbonate skeletons of scleractinians (e.g.
Bonaldo et al. 2011), the soft corals in this study also
demonstrated faster healing than nine different hard corals
subject to bites of comparable sizes from surface tissue
with no damage to the underlying skeleton in nine out of 12
experimental studies (bites of 100–200 mm2: Bak 1983;
Meesters et al. 1992; Van Veghel and Bak 1994; Nagelk-
erken et al. 1999; Fine et al. 2002), as well as three out of
four studies in which bites were 1/10th of the size inflicted
in this study (bites of 10–20 mm2: Isa 1987; Nagelkerken
and Bak 1998; Nagelkerken et al. 1999; Ruesink 1997).
While factors such as colony size and environmental con-
ditions must be assumed to have varied among studies and
therefore limit the accuracy of direct comparison, the
healing capacity demonstrated by soft corals in this study
nonetheless far exceeds that recorded for hard corals and
may confer soft corals greater resilience to predation.
While no immediate effects on the health of individual
colonies were detected, there may be longer-term effects
on soft coral populations. The diversion of resources to
wound healing has been demonstrated to reduce growth
and reproductive output in hard corals (Meesters et al.
1994; Tentori et al. 2004; Rotjan and Lewis 2005). Effects
on fecundity have also been illustrated for the deep-water
gorgonian Corallium rubrum (Priori et al. 2015), but as yet
no assessment of effects on growth or reproductive rates
has been made for soft corals. In this study, the metrics
used were macroscopic indicators of coral health and
determining changes in growth rate and fecundity were
beyond the scope of the experiments. The hydrostatic
skeleton of soft corals allows considerable changes in size,
and as a result, accurate calculations of colony growth rate
in the field are only possible using repeated measurements
over multiple months to allow for error associated with
colony contraction (Fabricius 1995). Furthermore,
Coral Reefs
individual colony growth rates for Sinularia and Sarco-
phyton (two other genera within the family Alcyoniidae)
can be slow (0.5 cm and 0.6 cm per year; Fabricius 1995)
and as such it was unlikely that any change in growth rate
would be perceptible in time frame of the experiments.
Measurements of fecundity require the dissection of polyps
or colonies, and as such tissue sampling before the treat-
ment period would not have been possible without con-
founding control colonies. As reductions in reproductive
output can be expected to reduce population stability and
resilience (Rotjan and Lewis 2008), investigation into the
sub-lethal effects of predation on colony fecundity and
growth rate would increase the understanding of the
importance of predation to soft coral populations.
Nonetheless, the rapid rates of recovery observed on
colonies of Lobophytum suggest that predation does not
represent a substantial cost to colonies under optimal
conditions.
Future increases in water temperature and acidity are
likely to place greater stress on corals and implicate high
levels of coral mortality (Hughes et al. 2003), and evidence
from past bleaching episodes suggests that the bleaching
susceptibility of soft corals is similar to that of hard corals
(Fabricius 1999; Marshall and Baird 2000). With coral
decline, the per capita impact of corallivory may increase
and affect population fitness, recovery and the incidence of
disease (Jayewardene et al. 2009). The high selectivity of
feeding on soft coral also has the potential to influence
community composition under these scenarios (Cox 1986).
In the case of soft coral, we concluded that the species
studied are resilient to predation. In contrast, studies of
chronic predation by fishes on hard corals suggest that
predation may represent an energetic cost sufficient to
influence the abundance and distribution of hard coral
species, particularly under stressful conditions of increased
ocean temperature and acidity (Bonaldo and Bellwood
2011; Bonaldo et al. 2011; Palacios et al. 2014). As such, if
bleaching susceptibility and mortality remain roughly
equivalent between soft and hard corals while predation for
both groups remains high, soft corals may become a more
dominant component of the benthos and predation may
emerge as a factor structuring the succession community
and future reefs.
It is possible that future changes in climatic and dis-
turbance regimes may increase the impact of predation on
soft coral populations, as tolerance to bites and tissue loss
may change under additional stress (Cameron and
Edmunds 2014). However, the results of the experiments in
this study clearly illustrated that two different genera of
soft corals are highly tolerant and resilient to intense pre-
dation and therefore, under current conditions, predation
does not appear to represent an immediately important
control over soft corals populations. Nonetheless,
continued investigation into the relationships between
fishes and soft corals, particularly of soft corals as a food
source and habitat, is necessary to further our understand-
ing of reef ecology and potential changes in community
dynamics under the increasing stressors associated with
global climate change.
Acknowledgements The authors would like to thank G. Gerlach, A.
Bally, J. Schlaefer, J. Breedon, and L. Lazar for their assistance in the
field, and P. Alderslade for assisting with soft coral identification.
Thanks also to the staff of One Tree Island Research Station and
Orpheus Island Research Station for logistical support. This research
was conducted under GBRMPA permit number G16/38425.1.
Funding Funding was provided to M. J. Kingsford by the Australian
Research Council Centre of Excellence for Coral Reef Studies.
Compliance with ethical standards
Conflict of interest All authors declare that they have no conflict of
interest. Sampling and experiments were compliant with the ethics
requirements of James Cook University.
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