REPORT
Effects of predation on diel activity and habitat use of the coral-reef shrimp Cinetorhynchus hendersoni (Rhynchocinetidae)
Nicolas C. Ory • David Dudgeon • Nicolas Duprey •
Martin Thiel
Received: 3 January 2014 / Accepted: 29 April 2014 / Published online: 17 May 2014
� Springer-Verlag Berlin Heidelberg 2014
Abstract Nonlethal effects of predators on prey behav-
iour are still poorly understood, although they may have
cascading effects through food webs. Underwater obser-
vations and experiments were conducted on a shallow
fringing coral reef in Malaysia to examine whether pre-
dation risks affect diel activity, habitat use, and survival of
the rhynchocinetid shrimp Cinetorhynchus hendersoni. The
study site was within a protected area where predatory fish
were abundant. Visual surveys and tethering experiments
were conducted in April–May 2010 to compare the abun-
dance of shrimps and predatory fishes and the relative
predation intensity on shrimps during day and night.
Shrimps were not seen during the day but came out of
refuges at night, when the risk of being eaten was reduced.
Shrimp preferences for substrata of different complexities
and types were examined at night when they could be seen
on the reef; complex substrata were preferred, while simple
substrata were avoided. Shrimps were abundant on high-
complexity columnar–foliate Porites rus, but tended to
make little use of branching Acropora spp. Subsequent
tethering experiments, conducted during daytime in June
2013, compared the relative mortality of shrimps on simple
(sand–rubble, massive Porites spp.) and complex (P. rus,
branching Acropora spp.) substrata under different preda-
tion risk scenarios (i.e., different tether lengths and expo-
sure durations). The mortality of shrimps with short tethers
(high risk) was high on all substrata while, under low and
intermediate predation risks (long tethers), shrimp mortal-
ity was reduced on complex corals relative to that on sand–
rubble or massive Porites spp. Overall, mortality was
lowest on P. rus. Our study indicates that predation risks
constrain shrimp activity and habitat choice, forcing them
to hide deep inside complex substrata during the day. Such
behavioural responses to predation risks and their conse-
quences for the trophic role of invertebrate mesoconsumers
warrant further investigation, especially in areas where
predatory fishes have been overexploited.
Keywords Rhynchocinetid shrimps � Habitat
complexity � Substratum structure � Predator–prey
interactions � Risk effects � Tethering
Introduction
Predators can affect prey abundance by increasing their
mortality, or by causing sublethal reductions in prey
activity due to behavioural adjustments in response to
predators (i.e., risk effects; e.g., Lima 1998; Creel and
Christianson 2008). A growing body of evidence indicates
that such risk effects can have important effects on
Communicated by Biology Editor Dr. Glenn Richard Almany
Electronic supplementary material The online version of thisarticle (doi:10.1007/s00338-014-1163-0) contains supplementarymaterial, which is available to authorized users.
N. C. Ory (&) � N. Duprey
The Swire Institute of Marine Science, The University of Hong
Kong, Pokfulam Rd, Hong Kong, People’s Republic of China
e-mail: [email protected]
N. C. Ory � D. Dudgeon � N. Duprey
School of Biological Sciences, The University of Hong Kong,
Pokfulam Rd, Hong Kong, People’s Republic of China
M. Thiel
Facultad Ciencias del Mar, Universidad Catolica del Norte,
Larrondo 1281, Coquimbo, Chile
M. Thiel
Centro de Estudios Avanzados en Zonas Aridas (CEAZA),
Coquimbo, Chile
123
Coral Reefs (2014) 33:639–650
DOI 10.1007/s00338-014-1163-0
mesoconsumer activity that can cascade through food webs
(Peacor and Werner 2001; Schmitz et al. 2004; Steffan and
Snyder 2010). Nonetheless, the consequences of risk
effects remain difficult to predict because the factors
influencing predator avoidance by mesoconsumers are
poorly known (Reebs 2002; Heithaus et al. 2009).
Given that a reduction in risk usually comes at the cost
of reduced foraging and mating opportunities (Werner et al.
1983; Sih 1997), antipredatory behaviours generate trade-
offs between benefits and costs to prey fitness. The use of
structurally complex habitats may reduce prey detectabil-
ity, impair predator attack success, or prevent predators
from accessing prey hiding inside small refuges such as
holes or crevices (reviewed in Denno et al. 2005). Indeed, a
refuge size that matches the size of the prey is one of the
best predictors of the protective value of a refuge (Eggle-
ston et al. 1990; Wahle 1992; Wilson et al. 2013). Con-
versely, however, habitat complexity can improve the
foraging efficiency of predators (e.g., Flynn and Ritz 1999),
or protect them from intraguild predation (reviewed by
Janssen et al. 2007), and cannibalism (Finke and Denno
2006), indicating that the relationship between prey sur-
vival and habitat complexity may not be straightforward.
Accordingly, when predation risks are high, prey tend to
use only the most complex habitats that provide the most
effective protection against predators (i.e., habitats that
equal or exceed the ‘habitat complexity threshold’; Nelson
1979; Gotceitas and Colgan 1989).
Coral reefs are heterogeneous environments comprising
a mosaic of discrete habitats with different structural
complexity (e.g., Gratwicke and Speight 2005; Wilson
et al. 2007; Holmes 2008). Thus, they provide an excellent
opportunity to determine whether habitat use by inverte-
brate prey subject to predation by fishes is affected by
substratum complexity. Most studies of the relationship
between habitat complexity and prey abundance or diver-
sity have focussed on fish as prey (e.g., Caley and St John
1996; Holbrook et al. 2002a; Noonan et al. 2012). How-
ever, invertebrates, such as shrimps and other decapods, are
abundant and diverse on coral reefs (Stella et al. 2010,
2011a) and, as they are usually less mobile than fishes,
their distribution is more likely to be strongly influenced by
variations in habitat complexity (Vytopil and Willis 2001;
Dulvy et al. 2002), as has been shown in various studies
from mangrove and macrophyte habitats (Meager et al.
2005; Ochwada-Doyle et al. 2009; Tait and Hovel 2012).
Variations in the growth form of scleractinian corals
(e.g., whether they are branching, columnar, foliate, or
massive) may affect their effectiveness as a refuge for
shrimps and other invertebrates and may thereby influence
diversity and abundance of these epibionts. For example,
Vytopil and Willis (2001) found that epibionts associated
with four species of branching Acropora (Acroporidae)
were more numerous and diverse on those corals with
narrowest branch spacing where prey mortality was lowest.
Similarly, Edwards and Emberton (1980) observed that the
abundance of decapods associated with individual colonies
of Stylophora pistillata (Pocilloporidae) decreased as the
spacing between coral branches widened.
The need to avoid predators may confine prey activities
to periods when predators are less active (Duffy and Hay
2001; Aumack et al. 2011). For example, nocturnal for-
aging by small fishes and invertebrates may be an adap-
tation to avoid visually oriented predatory fishes (Vance
1992; Jacobsen and Berg 1998; Lammers et al. 2009) as
prey mortality is usually lower at night (Clark et al. 2003;
Bassett et al. 2008). However, the general effects of pre-
dation risk on diel activity of coral-reef invertebrates
remain unclear.
The present study examined the antipredatory responses
of coral-reef shrimps to predation risks from fishes, in
terms of both temporal activity pattern and microhabitat
selection. The model species was Cinetorhynchus hender-
soni (Rhynchocenitidae), which is common in shallow
(1–10 m) waters of the Indo-Pacific, from the east coast of
Africa to French Polynesia, and to Honshu (Japan) in the
north (Okuno 1997). Rhynchocinetid shrimps are important
components of many coastal benthic communities (Caill-
aux and Stotz 2003; Ory et al. 2013) where they can play a
significant role as prey for many fish species (Vasquez
1993; Ory et al. 2012) and as epibenthic predators (Dumont
et al. 2009, 2011). C. hendersoni has been reported as
being nocturnal, hiding inside small holes and crevices on
reefs during the day while emerging at night to forage
(Okuno 1993).
In order to examine whether predation risk influenced
diel activity and habitat preference of shrimps, we under-
took underwater visual surveys and field experiments on a
protected Malaysian coral reef in Tioman Island where
fishes were diverse and abundant (Harborne et al. 2000).
Observations were made during the day and at night to test
whether diel variations of shrimp abundance on the reef
were negatively related to fish abundance and relative risk
of predation. Surveys and tethering experiments were also
used to test the hypothesis that shrimps most often use
complex habitats and that their preferred substrata (i.e.,
microhabitats) offer better protection against fishes.
Materials and methods
Study site
The study area (200 9 50 m) was located *20 m offshore
Kampung Tekek, Pulau Tioman Marine Park, Malaysia
(Fig. 1) on a shallow (4–8 m deep), gently sloped, fringing
640 Coral Reefs (2014) 33:639–650
123
coral reef (Amri et al. 2008). All in situ observations and
experiments were conducted on seven coral reef patches
(250–500 m2 total area) separated from each other by at
least 10 m of sandy bottom. The community of hard
scleractinian corals, described by Amri et al. (2008), was
dominated by large colonies of columnar–foliose Porites
rus (Poritidae), massive Porites spp. (P. lobata and P. lutea
were both common), and tabulate and branching Acropo-
ridae including Acropora nobilis and A. formosa (Harborne
et al. 2000). An initial study was conducted in 2010 to
compare diel patterns of fish and shrimp abundance and
shrimp mortality using underwater visual surveys and
tethering experiments. Further tethering experiments were
carried out in 2013 to examine mortality of shrimps asso-
ciated with substrata (microhabitats) that varied in com-
plexity (see below). Water temperatures were similar
(range 29–31 �C) between the 2 yr, and all experiments
were conducted when underwater visibility exceeded 7 m.
Abundance of fishes and shrimps
Abundance of fishes and shrimps was visually assessed
from 1 May to 5 May 2010 during the day and at night by
scuba diving along a 20-m transect line laid on the surface
of the coral reefs (total n = 7 transects). At night, torches
with a wide angle light beam were used to cover the entire
transect width. As observed in other studies (Nagelkerken
et al. 2000; Ray and Corkum 2001), light did not appear to
scare fishes as they did not flee farther from the observer
than during the day. Preliminary field observations indi-
cated that artificial lights did not induce rapid escape
reactions by C. hendersoni although, when disturbed, they
retreated slowly into the closest refuge. Observations made
in the laboratory (Corredor 1978; Kenyon et al. 1995)
confirmed that artificial lights did not induce erratic escape
reactions from other shrimp species. All predatory fishes
[5 cm in total length within 2.5 m of each side of the
transect line were identified to the species level and
counted (following Lieske and Myers 2002). Shrimp
abundance was assessed by a second diver, following
5 min after the fish surveyor, who counted all C. hender-
soni (henceforth ‘shrimps’) observed within a 50 9 50 cm
quadrat placed on the reef surface at 1-m intervals on
alternate sides of the transect line. After counting the
shrimps, a photograph of the quadrat was taken with a
Canon G10 digital camera for later analysis of substratum
type and complexity. On a single day, one or at most two
transects were surveyed once in the afternoon, between
1400 hrs and 1600 hrs, and again after dusk on the same
night, between 2000 hrs and 2200 hrs.
Fig. 1 Map of part of Southeast
Asia, and insets showing
Tioman island and the location
of the studied site (circle) on a
fringing coral reef in front of
Tekek village (N 2�4805700; E
104�0903100)
Coral Reefs (2014) 33:639–650 641
123
The abundance of fishes and shrimps was compared
between night and day using a nonparametric Wilcoxon
paired-test (number of transect replicates = 7); homoge-
neity of variance of the data was verified with Levene’s test
(a = 0.001). These and all other statistical tests were
undertaken using SPSS� version 18.
Substratum type and complexity
Photoquadrats were analysed to examine shrimp prefer-
ences for substratum complexities and type, separately.
The complexity of the substratum was defined here by the
rugosity of the reef surface (i.e., the amount of ‘irregular-
ities’ of the reef surface; Dunn and Halpin 2009) and the
presence of small (\5 cm) refuges (i.e., holes and crevices
of the substratum, as for example in Friedlander and Par-
rish 1998; Almany 2004; Gratwicke and Speight 2005;
Wilson et al. 2007). Substratum complexity was estimated
from photoquadrats using five complexity scores adapted
from Ory et al. (2012). Complexity scores of 1, 2, 3, 4, and
5 were assigned to quadrats with, respectively, \5 %,
5–25 %, 26–50 %, 51–75 %, and over 75 % of their sur-
face covered by complex three-dimensional architecture
substrata (e.g., branching, columnar, or foliate dead or
living coral; Fig. 2). Bedrock, sand–rubble mixture, loose
or consolidated rubble, or massive coral (dead or living)
were categorized as low complexity substrata (Fig. 2),
because they provided no or few refuges to shrimps. Sur-
face cover of complex substrata was quantified for each
quadrat from the analysis of the photoquadrats using the
Coral Point Count with Excel extensions (CPCe) program
with 50 random points (Kohler and Gill 2006).
The percentage cover of substratum types within each
quadrat was quantified from photoquadrats as above to
examine shrimp preferences for each type of substratum.
Substratum types were recorded using eight main catego-
ries (see electronic supplementary materials, ESM, Table
S1): (1) bedrock and large boulders (referred as ‘rock’
thereafter), (2) loose (unconsolidated) rubble, (3) consoli-
dated rubble, (4) sand–rubble (sand mixed with small
Fig. 2 Examples of photoquadrats with substratum complexity scores of 1 (1a, 1b), 2 (2a, 2b), 3 (3a, 3b), 4 (4a, 4b), and 5 (5a, 5b) and of the
most commonly observed complex and simple substrata (see text for further details on substratum complexity scores)
642 Coral Reefs (2014) 33:639–650
123
pieces of loose rubble), (5) soft coral (Alcyonacea), (6)
bleached or recently dead hard coral (white Scleractinia not
yet overgrown), (7) hard dead coral (dead Scleractinia with
its original structure overgrown by fouling organisms), and
(8) hard living scleractinian coral (Fig. 2). Hard corals (in
substratum types 6, 7, and 8) were further subcategorized
by their genus or species and their growth forms, i.e.,
massive, encrusting, digitate, columnar, foliate, or
branching (Veron 2000; ESM Table S1).
Shrimp preferences for substrata were examined sepa-
rately, using two Pearson chi-squared goodness-of-fit tests
(vp2) to test the null hypotheses of random choice of sub-
strata complexity and type as a function of their availability
(Manly et al. 2002). Where the null hypothesis was rejec-
ted, substratum preference was determined using the Manly
resource selection index wi, which is the ratio between
proportions of resource (i.e., substratum types) of category
i used by shrimps (oi) and the availability of these substrata
ðpiÞ estimated from their percentage cover within each
quadrat in the survey area.
Calculation of the standard error of wi depends on the
basic sampling unit used to estimate resource (i.e., substra-
tum) availability (Manly et al. 2002). In this study, sub-
stratum complexity was an index estimated from a single
value for each quadrat, i.e., random points were used as the
basic sampling units; standard error of wi was therefore
seðwiÞ ¼ wi
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
1=li � 1=lþ þ 1=mi � 1=mþ
q
(Manly et al. 2002: Eq. 4.23), where mi is the number of
quadrats of complexity category i sampled, m? is the total
number of quadrats sampled, li is the proportion of
shrimps using quadrats of complexity category i, and u?
the total number of shrimps sampled.
The mean availability of each substratum type was
estimated as its proportion of all substrata within each
quadrat. The standard error of wi was therefore
seðwiÞ ¼ wi
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
ð1� oiÞ=ðoilþÞ þ seðpiÞ2=p2i
q
(Manly et al. 2002: Eq. 4.25).
Bonferroni-corrected 95 % confidence intervals (CI)
were calculated around each wi to test whether they dif-
fered from 1, i.e., the null hypothesis of no selection, with
values [1 indicating overuse (i.e., selection) of a substra-
tum category, and values \1 indicating underuse (i.e.,
avoidance). Substratum complexity categories 1 and 2 were
pooled into a single category (Manly et al. 2002) to ensure
that [25 % of expected shrimp counts were [5 and none
\1 (Yates et al. 1999). For the same reason, the three types
of substratum with the lowest complexity (sand–rubble,
rock, and massive Porites spp.) were pooled. Substrata
seldom recorded (occurring in \10 quadrats) were not
included in the analysis (ESM Table S1).
Shrimp capture and maintenance
Shrimps were collected by hand, using plastic calipers to
gently coax them into a plastic Ziploc bag, or by traps that were
deployed at night to increase the number of shrimps collected.
A plastic colander (30 9 15 9 15 cm) with 3-mm holes was
filled with coral rubble to provide shelter for shrimps and
placed on the reef surface near colonies of P. rus and
branching Acropora spp. where shrimps were often sighted.
The following night, a second inverted colander was placed
over the first one, thereby enclosing any shrimps among the
rubble. Prior to being used in tethering experiments, all
shrimps were held together for up to 3 d in an opaque plastic
bucket (60 cm diameter) containing 20 cm of aerated sea
water at 28–31 �C under a natural lighting regime. There was
no shrimp mortality during this pre-tethering period.
Tethering experiments
Shrimps were tethered during the day or at night to
examine diel variation of relative predation risks. We also
tested the relative mortality of shrimps tethered on different
substrata with complex or simple structure to compare
which offered better protection against predators. We ran
the experiments for short (10 min) and long (30 min)
durations and employed different lengths of tethers
allowing shrimps to hide in the periphery of the tested
substrata (short tethers) or deeper inside the complex
substrata (long tethers). Shrimp mortality was thus com-
pared among each substratum under increasing predation
risks: low (shrimps with long tether for 10 min), interme-
diate (shrimps with long tether for 30 min), and high
(shrimps with short tether for 30 min). Despite the recog-
nized short comings of tethering experiments and the need
to interpret the results with caution (e.g., Kneib and
Scheele 2000), these experiments can help to identify the
safest time periods for shrimps to be active and to provide a
first indication of the protective value of different substrata.
Diel comparison of relative predation on shrimps
After fish and shrimp surveys in May 2010, tethering
experiments were conducted in the field from 09 May to 13
May to compare the relative intensity of predation by fishes
on shrimps during the day and at night. The day prior to
experiments a 15-cm long monofilament was attached to
the dorsum of the third abdominal segment of each shrimp
using cyanoacrylate glue. All tethers remained attached to
the shrimps by the next morning, with the exception of two
shrimps that had moulted overnight. The size of shrimps
(5–7 mm carapace length, CL) used in tethering experi-
ments was chosen according to the mean CL (6.0 ± SD
0.9 mm) measured from 52 shrimps previously collected
Coral Reefs (2014) 33:639–650 643
123
from the field (these shrimps were not used in experi-
ments). Large males, which develop hypertrophied first
pereopods (Okuno 1997), were not used in the experiments
to avoid potentially confounding effects of shrimp mor-
phology that can affect their susceptibility to predators
(Ory et al. 2012). Tethered shrimps were placed inside
individual plastic tubes (length 9 diameter = 10 9 5 cm)
and transported to the field site within 20 min. Under
water, a single shrimp, was tethered to the centre of a grey
PVC plate (50 9 50 9 0.5 cm) anchored to the seafloor
with a 1-kg diving weight. Tethered shrimps were unable to
leave the plate, with nowhere to hide, and were thus
exposed to predators for 30 min, after which they were
scored as present (and live) or absent (presumed eaten).
Tethering experiments were conducted in the afternoon
(1400–1600 hrs) and the same night (2000–2200 hrs) for
two consecutive days (9 and 10 May). Fifteen and nine
unique shrimp individuals were used during the day and ten
and 11 at night, on the two respective dates. Two Pearson
chi-square tests (Quinn 2002) were performed separately to
test the null hypotheses that shrimp mortality (i.e., disap-
pearance) was similar during the day and at night, and
between the two consecutive days.
Comparison of shrimp mortality on different substrata
On 16 June 2013, tethering experiments were conducted to
compare mortality after 30 min of shrimps tethered with
15-cm nylon monofilament (high predation risk) among
four of the most common substrata observed in 2010: two
with complex structure (living P. rus and branching Ac-
ropora spp.) and two with simple structure (sand–rubble
and living massive Porites spp., see below). All trials were
conducted during the day (1400–1600 hrs) on a single coral
patch (70 9 50 m) studied in 2010 where all four substrata
were present and fish abundance was high. Shrimps were
tethered to a branch or a column of large ([50 cm diam-
eter) P. rus (number of shrimp tested = 5) or Acropora
spp. (n = 5), or to a fishing weight (200 g) placed on the
surface of massive Porites colonies (n = 5), or to a weight
placed on the sand–rubble bottom (n = 5). All shrimps
were observed being quickly eaten by fishes, so that no
further trials were conducted to not unnecessarily kill more
shrimps in the Marine Park.
On the 19 and 21 June 2013, tethering experiments were
conducted during the day on the same coral patch to test the
survival of shrimps tethered with longer nylon monofilament
(40 cm) and to verify whether mortality was reduced when
shrimps were able to retreat deeper into coral refuges. Shrimp
mortality was thus tested under intermediate (shrimps with
long tether for 30 min) and low (shrimps with long tether for
10 min) predation risks for all substrata. A total of 15 tethered
shrimps were tested on P. rus and 14 on Acropora spp. The
number of shrimps tested on living massive Porites spp. and
sand–rubble bottom was limited to 8 and 7, respectively,
because all shrimps were observed being eaten quickly by
fishes. Shrimp presence was monitored after 10 min and,
again, after 30 min. Any shrimp that had disappeared by
10 min was also scored absent after 30 min. Upon completion
of tethering experiments, surviving shrimps were released at
the site where they had been captured.
Shrimp mortality among different substrata under high
predation risk scenario was not analysed as all shrimps
were eaten on all substrata. Two Pearson chi-square tests
were run separately to test the null hypotheses that mor-
tality of tethered shrimps was similar on different substrata
and under low or intermediate predation risk scenarios.
When the null hypothesis was rejected, pairwise compari-
sons were performed to test differences in mortality among
all substratum categories. Sand–rubble and living massive
Porites spp. were pooled in a single ‘simple substrata’
category to ensure that[25 % of expected shrimp presence
counts were [5 and none \1.
Results
Diel variation of fish and shrimp abundance
A total of 181 individuals of 25 species of predatory fishes
were recorded during the day and 84 individuals of 11 spe-
cies at night (Table S2). Fish abundance varied from 11 to 25
individuals per 100 m-2 (mean ± SE = 20.3 ± 1.9;
n = 7; Fig. 3a) during the day, but was lower at night
(U = 3.0, P = 0.006, number of transects = 7), ranging
from four to 16 individuals 100 m-2 (9.9 ± 1.9; n = 7;
Fig. 3a). Predatory fish species richness was also higher
during the day (10.3 ± 1.01 species 100 m-2; n = 7) than
at night (4.1 ± 0.6 species 100 m-2; U = 0.50, P \ 0.001).
No shrimps were seen on the reef during the day, whereas
their abundance along all transects was 1.8 ± 0.3 individ-
uals 0.25 m-2 (number of quadrats = 140) at night
(Fig. 3a), ranging from 0.8 ± 0.4 SE to 3.3 ± 0.6 individ-
uals 0.25 m-2 per transect (number of quadrats per tran-
sect = 20). The maximum number of shrimps within a
quadrat was nine individuals, with 2.7 ± 0.2 ind 0.25 m-2
in quadrats where at least one shrimp was present (n = 79).
Shrimp habitat use
The mean number of shrimps ranged from 0.5 ± 0.1 to
2.8 ± 0.3 individuals 0.25 m-2 in quadrats of lowest (i.e.,
pooled category 1–3) and highest complexity, respectively.
The abundance of shrimps differed in relation to substra-
tum complexity (v2 = 59.9, df = 3, P \ 0.001; Fig. 4a).
Overall, 56.3 % of all shrimps observed (n = 215) were
644 Coral Reefs (2014) 33:639–650
123
found in quadrats with the highest complexity, which
constituted 30.7 ± 0.1 % of all the quadrats (n = 140).
Quadrats with the lowest substratum complexity (i.e., cat-
egories 1 and 2) accounted for 37.9 ± 0.1 % of all quad-
rats, but harboured only 10.7 % of all shrimps. Shrimps
selected the most complex substrata (wi = 1.8; Fig. 4b;
ESM Table S3a) and did not show any preference for
substrata of intermediate complexity (wi = 1.0), but avoi-
ded those with the lowest complexity (wi = 0.4).
The most abundant substratum types within the study area
were the foliate–columnar living scleractinian P. rus (22 % of
total cover), consolidated rubble (15 %), sand–rubble (16 %),
branching living scleractinian Acropora spp. (7 %), rock
(6 %), dead P. rus (5 %), and branching (4 %) and massive
living Porites spp. (4 %; Fig. 5a; ESM Table S1). Loose
rubble (3 %), soft coral (2 %), and bleached scleractinian
corals (\0.1 %) were present at low abundance and excluded
from subsequent analyses (ESM Table S1). Shrimps showed
preferences for particular substrata (v2 = 129.09, df = 5,
P \ 0.001; ESM Table S3b). Shrimps preferred living coral
P. rus (wi = 2.1; Fig. 5b; ESM Table S3b) and consolidated
rubble (wi = 1.7), but avoided sand–rubble, rock, and mas-
sive Porites spp. (wi = 0.0) with low complexity. Shrimps
also showed a tendency to avoid branching Acropora spp.
(wi = 0.5), despite their complex structure. Shrimps had no
significant preference between dead P. rus (wi = 1.6) or liv-
ing branching Porites spp. (wi = 1.2).
Tethering experiments
Tethering experiments in 2010 revealed that mortality of
shrimps tethered for 30 min on plates without refuges was
substantially higher during the day (64 % of the total,
n = 24) than at night (6 %; n = 21; v2 = 16.29, df = 1,
P \ 0.001; Fig. 3b), but did not vary between the two con-
secutive days of experiments (v2 = 0.15, df = 1, P = 0.70).
Under the high predation risk scenario, all shrimp with
15-cm tethers were eaten within 30 min on branching Ac-
ropora spp. or massive Porites spp., while those on sand–
rubble or massive Porites spp. were observed being eaten
within several seconds of exposure (Fig. 6; ESM Table
S4a). Under intermediate predation risks, shrimp mortality
varied according to substratum category (v2 = 6.27,
df = 2, P = 0.036). Although shrimp mortality did not
differ between branching Acropora spp. (89 %) and P.rus
(67 %; v2 = 1.44, df = 1, P = 0.39) or between Acropora
spp. and sand–rubble ? massive Porites spp. (100 %;
v2 = 2.30, df = 1, P = 0.22), it was nonetheless lower on
P. rus compared to sand–rubble ? massive Porites spp.
(v2 = 6.0, df = 1, P = 0.01; Fig. 6; ESM Table S4b).
Under the low predation risk scenario (i.e., 40-cm tether,
10-min duration), shrimp mortality also differed among all
substrata (v2 = 15.47, df = 2, P \ 0.001): it was lower on
branching Acropora spp. (71 %) than on sand–rub-
ble ? massive Porites spp. pooled (100 %; v2 = 4.97,
df = 1, P = 0.026), but higher than on P. rus (33 %;
v2 = 4.21, df = 1, P = 0.04; Fig. 6; ESM Table S4c).
Discussion
Diel activity patterns
Shrimps hid during the day and were visible on the reef only
at night, a behaviour typical of many small and medium-
sized prey organisms (e.g., Bauer 1985; Beck 1997;
Day Night
Num
ber
of f
ishe
s (i
nd 1
00 m
-2)
0
5
10
15
20
25
30Fishes
SE
Day Night
Shri
mp
mor
talit
y (%
)
0
10
20
30
40
50
60
70
Day Night
Num
ber
of s
hrim
ps(i
nd 0
.25
m-2
)
0
1
2
3
4
5Shrimps
0
a b
Fig. 3 a Median (solid line crossing the box) and average (dotted
line) shrimp and predatory fish abundances along reef surface
transects (n = 7) around Tioman. The lower and upper boundaries
of the box represent, respectively, the first and third quartile; the
whiskers are the minimum and maximum within 1.5 times the
interquartiles. b Mortality of shrimps tethered for 30 min on a plate
with no refuge during the day (n = 24) and at night (n = 21)
a b
Fig. 4 a Availability (proportion total quadrats) of substrata of
different complexity and their use by shrimps (proportion of total
shrimp number). b Selection index (±95 % CI) for each substratum
complexity category. Asterisks indicate selection ([1) or avoidance
(\1) at the level of error a = 5 % (after Bonferroni correction)
Coral Reefs (2014) 33:639–650 645
123
Kulbicki et al. 2005). While nocturnal activity may, in some
cases, have evolved in response to heat stress (Cannicci et al.
1999), hypoxia (Berglund and Bengtsson 1981), or changes
in food availability (Vance 1992), it is unlikely that these
factors are responsible for diel activity patterns of C.
hendersoni. Instead, C. hendersoni are inactive during the
day to avoid predators: our tethering experiments revealed
that shrimp mortality was substantially lower at night than
during the day, as also found from other experiments on
small fish and decapod prey in coral reefs (Acosta and Butler
1999), macrophyte habitats (Linehan et al. 2001; Peterson
et al. 2001), rocky reefs (Diaz et al. 2005; Bassett et al. 2008)
and estuaries (Clark et al. 2003).
Nocturnal activity appears to be more pronounced in
tropical waters (Castro 1978; Knowlton 1980) than in tem-
perate waters, where some crustaceans may also exhibit
daytime activity (De Grave and Turner 1997; Cannicci et al.
1999), perhaps because of lower predation risks at higher
latitudes (Heck and Wilson 1987; Freestone et al. 2011). In
contrast to C. hendersoni in Malaysia, Rhynchocinetes ty-
pus, a rhynchocinetid that inhabits temperate reefs in Chile,
was visible during the day (Ory et al. 2012). R. typus
occupied shelters that did not prevent access to predators,
but where they were able to form large aggregations. Fish
abundance and diversity, and thus predation on shrimps,
were lower on rocky reefs in Chile than in Malaysia, and
densities of R. typus were [10 times higher than C. hen-
dersoni in Malaysia. Latitudinal comparisons of day–night
activity and host use of small invertebrates could be used to
test the hypothesis that prey are strictly nocturnal in envi-
ronments where predation risks are the highest.
Mortality risks on shrimps
During the day, shrimp are only safe if they can hide in the
most complex habitats. P. rus colonies comprise a
a bFig. 5 a Availability
(proportion of cover per
quadrat) of the most common
type of substratum within the
survey area (sand and rubble,
rock, and massive Porites spp.
were pooled in a single category
for analysis, see text) and their
use by shrimps (proportion of
shrimp total number).
b Selection index (±95 % CI)
for each substratum type.
Asterisks indicate selection ([1)
or avoidance (\1) at the level of
error a = 5 % (after Bonferroni
correction)
Shri
mp
mor
tali
ty (
%)
0
20
40
60
80
100
Porites rusBranching Acropora spp.Sand-rubble + massive Porites spp. pooled
High risks (short tether, long duration)
14 14105 5 15 1515 15
a
b
c
A,B
B
A
NA
Intermediate risks (long tether,
long duration)
Low risks (long tether,
short duration)
a b
Fig. 6 Proportion of shrimp mortality (i.e., absence) on different type
of substrata (branching Acropora spp.; columnar–foliate Porites rus;
massive Porites spp., and sand–rubble pooled) under (a) high
(shrimps attached with 15-cm tethers for 30 min) and (b) intermediate
(shrimp attached with 40-cm tethers for 30 min), and low (shrimps
attached with 40-cm tethers for 10 min) predation risks. Numbers
inside bars indicate the sample size. Similar letters indicate no
difference in shrimp mortality after 10 (lower case) and 30 (upper
case) min. NA not analysed
646 Coral Reefs (2014) 33:639–650
123
combination of tightly packed columns and complex foliate
structures containing many small holes and crevices that
provide refuges from most predators (Holbrook et al.
2002b; Lecchini et al. 2007). Although the branching
structure of Acropora spp. was complex, these corals did
not provide good protection for shrimps since they failed to
prevent access of small predatory fishes. Other studies have
reported that small fishes which attempt to seek refuge
among coral colonies with widely spaced branches suffer
high rates of predation from resident fishes that hide in the
coral in order to avoid their own predators (Holbrook and
Schmitt 2002; Kane et al. 2009). Indeed, on two occasions,
shrimps still attached to their tether were found inside the
mouths of small Cephalopholis boenak (Serranidae;
5–7 cm total length), which were hiding among the bran-
ches of Acropora spp.
The length of the tether did not enhance the survival of
C. hendersoni on sand and massive Porites spp., where no
refuges were available, but tended to reduce shrimp mor-
tality on both Acropora spp. and P. rus. Longer tethers
appeared to have allowed shrimps to access deeper spaces
inside coral colonies where they were less vulnerable to
predators, and Holbrook and Schmitt (2002) have noted
that damselfish (Dascyllus trimaculatus: Pomacentridae)
suffer lower predation risks in the centre of branching coral
colonies than at their periphery. Nonetheless, the mortality
of shrimps was high in the high predation risk scenarios on
both Acropora spp. and P. rus, perhaps because the tethers
were too short to allow shrimps to retreat into the deepest
and most effective refuges.
Predation intensity may be higher on tethered than free
prey, mainly because tethered prey cannot escape when
attacked by predators (e.g., Wahle and Steneck 1992;
Kneib and Scheele 2000; Haywood et al. 2003). Our
tethering experiments did not intend to assess the absolute
intensity of predation on shrimps but, instead, were used to
compare relative shrimp mortality attributable to predation
between different treatments (day-night and type of sub-
stratum). Such comparisons are valid if any potential
tethering artefacts are independent of the treatments and do
not confound their comparison (Peterson and Black 1994).
In our experiments, tethered shrimps may have suffered
increased mortality in complex habitats where they could
have become entangled, but any confounding effect would
only have made our results more conservative (i.e., it
would tend to reduce the difference in shrimp mortality
between complex and more simple substrata).
It is unlikely that predation on shrimps could have been
attributable to other invertebrates, such as urchins or crabs,
or from cannibalism, because shrimp mortality was very
low at night when invertebrates are active. Also, none of
these invertebrates were observed in the vicinity of shrimps
at the end of the experiments. In addition, video recordings
of four preliminary tethering experiments revealed that
shrimps were eaten by fishes: C. boenak, Halichoeres
melanurus (Labridae) and Cheilinus trilobatus (Labridae).
Habitat features and shrimp preferences
Shrimps were mostly observed on complex habitats and
were seldom encountered on sand–rubble or massive hard
corals, where tethering experiments during the day dem-
onstrated that they suffered the highest mortality. These
results indicate that high predation risks restricted shrimps
to those habitats that exceeded the ‘habitat complexity
threshold’ (Nelson 1979; Coull and Wells 1983; Bar-
tholomew et al. 2000). Unlike C. hendersoni, other shrimp
species appear to be protected at relatively low levels of
substratum complexity (Primavera 1997; Ory et al. 2012),
further supporting the notion that shrimps in Malaysia
experience high predation risk within the marine protected
area where we worked.
Cinetorhynchus hendersoni showed strong preferences
for the columnar–foliate P. rus, but tended to avoid
branching Acropora spp., although both coral genera have
complex structures. Many small crustaceans and fish prey
species hide among a wide range of coral species of different
structural complexities (Patton 1994; Stella et al. 2011a)
according to the level of protection they provide against
predators (Vytopil and Willis 2001; Noonan et al. 2012). Our
tethering results showed that shrimp mortality was lower on
P. rus than on Acropora spp., indicating that these corals
offered shrimps different levels of protection from preda-
tors. These observations confirm that shrimp habitat pref-
erences are driven, at least in part, by predation risks, as also
shown in other environments such as macrophyte beds
(Meager et al. 2005; Ochwada-Doyle et al. 2009).
Shrimps in Malaysia were abundant on dead P. rus
colonies, which contradicts the commonly held view that
coral-associated invertebrates and fishes are less abundant
when living coral cover is low (Munday 2004; Stella et al.
2011b). However, other studies have also found that
crustacean epibionts are most abundant on dead corals
(Preston and Doherty 1990, 1994; Stella et al. 2010), per-
haps because they feed on the sediments accumulating on
the coral (Preston and Doherty 1994) or on the over-
growing fouling communities (e.g., R. typus in rocky reefs
in Chile: Dumont et al. 2009, 2011). Although, in the long-
term, coral-associates such as shrimps may suffer higher
mortality when dead corals lose their structural complexity,
they can use these corals as shelter and feeding ground in
the interim (Wilson et al. 2006). Grazing by C. hendersoni
and other small mesoconsumers may even, as shown for
fishes and urchins (Bellwood et al. 2004), reduce fouling of
dead coral (Brawley and Adey 1981), thereby favouring
settlement of new colonies.
Coral Reefs (2014) 33:639–650 647
123
Implications of research findings
Predation was an important factor influencing diel activity
and habitat use of C. hendersoni, as also shown for many
other coral-reef invertebrates (e.g., Acosta and Butler 1999;
Clark et al. 2003; Aumack et al. 2011). Small decapod
crustaceans often dominate marine benthic communities
(e.g., Austin et al. 1980; Stella et al. 2010), where they are
prey for many fishes (Angel and Ojeda 2001; Medina et al.
2004; Kulbicki et al. 2005) and predators of small sessile
organisms (Dumont et al. 2009), thereby playing an
important role within marine food webs (Howard 1984;
Worm and Myers 2003; Dumont et al. 2011). Depletion of
predators due to overfishing can release predation risks on
mesoconsumers such as shrimps (Albers and Anderson
1985; Worm and Myers 2003) and thereby affect lower
trophic levels (Schmitz et al. 1997; Dorn et al. 2006). On the
other hand, destruction of coral reefs may increase predation
risks on mesoconsumers which use complex coral habitats as
refuge. These interactions and the behavioural responses of
mesoconsumers in the face of varying predation risks war-
rant further investigation, as they could enhance under-
standing of the potential cascading of effects of overfishing
and the degradation of coastal reefs (Heithaus et al. 2008).
Acknowledgments This study was financed by the Swire Educa-
tional Trust, John Swire & Sons (Hong Kong) Ltd., and was part of a
Ph.D. project by NCO. We are grateful to Clement Dumont who
initiated the study of the biology of rhynchocinetid shrimps in
Southeast Asia and encouraged this study. We thank Kee Alfian Adzis
for logistical assistance, and the Malaysian Ministry of the Natural
Resources and the Environment for allowing us to work in Tioman
Marine Park. We are also grateful to Katie Yewdall, Rosie Cotton and
members of Tioman Dive Centre and East Divers in Tekek for their
kindness and professionalism; Solomon Chak for his assistance dur-
ing 2010; Daniel Pedraza for his help during field experiments; and
Raymond Bauer for the identification of C. hendersoni. We
acknowledge the constant support of Evelyn Lostarnau and her design
and construction of tools for the 2013 fieldwork.
References
Acosta CA, Butler MJ (1999) Adaptive strategies that reduce
predation on Caribbean spiny lobster postlarvae during onshore
transport. Limnol Oceanogr 44:494–501
Albers WD, Anderson PJ (1985) Diet of Pacific cod, Gadus
macrocephalus, and predation on the northern pink shrimp,
Pandalus borealis, in Pavlof Bay, Alaska. Fish Bull 83:601–610
Almany GR (2004) Does increased habitat complexity reduce
predation and competition in coral reef fish assemblages? Oikos
106:275–284
Amri AY, Tajuddin BH, Lee YL, Adzis KA, Yusuf Y (2008)
Scleractinian coral diversity of Kg Tekek, Pulau Tioman marine
park. In: Phang SM (ed) IOES monograph series: NaturaI
History of The Pulau Tioman Group of Islands. Institute of
Ocean and Earth Sciences, University of Malaya, Kuala Lumpur,
pp 53–68
Angel A, Ojeda FP (2001) Structure and trophic organization of
subtidal fish assemblages on the northern Chilean coast: the
effect of habitat complexity. Mar Ecol Prog Ser 217:81–91
Aumack CF, Amsler CD, McClintock JB, Baker BJ (2011) Changes
in amphipod densities among macroalgal habitats in day versus
night collections along the Western Antarctic Peninsula. Mar
Biol 158:1879–1885
Austin A, Austin S, Sale P (1980) Community structure of the fauna
associated with the coral Pocillopora damicornis (L.) on the
Great Barrier Reef. Mar Freshw Res 31:163–174
Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless
indices of structural habitat complexity: predicted and actual
effects on a predator’s foraging success. Mar Ecol Prog Ser
206:45–58
Bassett DK, Jeffs AG, Montgomery JC (2008) Identification of
predators using a novel photographic tethering device. Mar
Freshw Res 59:1079–1083
Bauer RT (1985) Diel and seasonal variation in species composition
and abundance of caridean shrimps (Crustacea, Decapoda) from
seagrass meadows on the north coast of Puerto Rico. Bull Mar
Sci 36:150–162
Beck MW (1997) A test of the generality of the effects of shelter
bottlenecks in four stone crab populations. Ecology
78:2487–2503
Bellwood D, Hughes T, Folke C, Nystrom M (2004) Confronting the
coral reef crisis. Nature 429:827–833
Berglund A, Bengtsson J (1981) Biotic and abiotic factors determin-
ing the distribution of two prawn species: Palaemon adspersus
and P. squilla. Oecologia 49:300–304
Brawley S, Adey W (1981) The effect of micrograzers on algal
community structure in a coral reef microcosm. Mar Biol
61:167–177
Caillaux LM, Stotz WB (2003) Distribution and abundance of
Rhynchocinetes typus (Crustacea: Decapoda), in different ben-
thic community structures in northern Chile. J Mar Biol Assoc U
K 83:143–150
Caley MJ, St John J (1996) Refuge availability structures assemblages
of tropical reef fishes. J Anim Ecol 65:414–428
Cannicci S, Paula J, Vannini M (1999) Activity pattern and spatial
strategy in Pachygrapsus marmoratus (Decapoda: Grapsidae)
from Mediterranean and Atlantic shores. Mar Biol 133:429–435
Castro P (1978) Movements between coral colonies in Trapezia
ferruginea (Crustacea: Brachyura), an obligate symbiont of
scleractinian corals. Mar Biol 46:237–245
Clark KL, Ruiz GM, Hines AH (2003) Diel variation in predator
abundance, predation risk and prey distribution in shallow-water
estuarine habitats. J Exp Mar Biol Ecol 287:37–55
Corredor L (1978) Notes on the behavior and ecology of the new fish
cleaner shrimp Brachycarpus biunguiculatus (Lucas) (Decapoda
Natantia, Palaemonidae). Crustaceana 35:35–40
Coull BC, Wells J (1983) Refuges from fish predation: experiments
with phytal meiofauna from the New Zealand rocky intertidal.
Ecology 64:1599–1609
Creel S, Christianson D (2008) Relationships between direct preda-
tion and risk effects. Trends Ecol Evol 23:194–201
De Grave S, Turner J (1997) Activity rhythms of the squat lobsters,
Galathea squamifera and G. strigosa (Crustacea: Decapoda:
Anomura) in south-west Ireland. J Mar Biol Assoc U K 44:860
Denno RF, Finke DL, Langellotto GA (2005) Direct and indirect
effects of vegetation structure and habitat complexity on
predator–prey and predator–predator interactions. In: Barbosa
P, Castellanos I (eds) Ecology of predator–prey interactions.
Oxford University Press, Oxford, pp 211–239
Diaz D, Zabala M, Linares C, Hereu B, Abello P (2005) Increased
predation of juvenile European spiny lobster (Palinurus elephas)
in a marine protected area. N Z J Mar Freshw Res 39:447–453
648 Coral Reefs (2014) 33:639–650
123
Dorn NJ, Trexler JC, Gaiser EE (2006) Exploring the role of large
predators in marsh food webs: evidence for a behaviorally-
mediated trophic cascade. Hydrobiologia 569:375–386
Duffy JE, Hay ME (2001) The ecology and evolution of marine
consumer-prey interactions. In: Bertness MD, Hay ME, Gaines
SD (eds) Marine Community Ecology. Sinauer Associates,
Sunderland, Massachusetts, USA, pp 131–157
Dulvy NK, Mitchell RE, Watson D, Sweeting CJ, Polunin NV (2002)
Scale-dependant control of motile epifaunal community structure
along a coral reef fishing gradient. J Exp Mar Biol Ecol 278:1–29
Dumont CP, Gaymer CF, Thiel M (2011) Predation contributes to
invasion resistance of benthic communities against the non-indig-
enous tunicate Ciona intestinalis. Biol Invasions 13:2023–2034
Dumont CP, Urriago JD, Abarca A, Gaymer CF, Thiel M (2009) The
native rock shrimp Rhynchocinetes typus as a biological control
of fouling in suspended scallop cultures. Aquaculture 292:74–79
Dunn DC, Halpin PN (2009) Rugosity-based regional modeling of
hard-bottom habitat. Mar Ecol Prog Ser 377:1–11
Edwards A, Emberton H (1980) Crustacea associated with the
scleractinian coral, Stylophora pistillata (Esper), in the Sudanese
Red Sea. J Exp Mar Biol Ecol 42:225–240
Eggleston DB, Lipcius RN, Miller DL, Coba-Cetina L (1990) Shelter
scaling regulates survival of juvenile Caribbean spiny lobster
Panulirus argus. Mar Ecol Prog Ser 62:79–88
Finke D, Denno R (2006) Spatial refuge from intraguild predation:
implications for prey suppression and trophic cascades. Oeco-
logia 149:265–275
Flynn AJ, Ritz DA (1999) Effect of habitat complexity and predatory
style on the capture success of fish feeding on aggregated prey.
J Mar Biol Ass UK 79:487–494
Freestone AL, Osman RW, Ruiz GM, Torchin ME (2011) Stronger
predation in the tropics shapes species richness patterns in
marine communities. Ecology 92:983–993
Friedlander A, Parrish J (1998) Habitat characteristics affecting fish
assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol
224:1–30
Gotceitas V, Colgan P (1989) Predator foraging success and habitat
complexity: quantitative test of the threshold hypothesis. Oec-
ologia 80:158–166
Gratwicke B, Speight MR (2005) The relationship between fish
species richness, abundance and habitat complexity in a range of
shallow tropical marine habitats. J Fish Biol 66:650–667
Harborne A, Fenner D, Barnes A, Beger M, Harding S, Roxburgh T
(2000) Status report on the coral reefs of the east coast of Peninsula
Malaysia. Coral Cay Conservation Ltd. in conjunction with Marine
Parks Section Department of Fisheries Malaysia, London
Haywood MDE, Manson FJ, Loneragan NR, Toscas PJ (2003)
Investigation of artifacts from chronographic tethering experi-
ments - interactions between tethers and predators. J Exp Mar
Biol Ecol 290:271–292
Heck KL, Wilson KA (1987) Predation rates on Decapod crustaceans
in latitudinally separated seagrass communities - A study of
spatial and temporal variation using tethering techniques. J Exp
Mar Biol Ecol 107:87–100
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting
ecological consequences of marine top predator declines. Trends
Ecol Evol 23:202–210
Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009)
Towards a predictive framework for predator risk effects: the
interaction of landscape features and prey escape tactics. J Anim
Ecol 78:556–562
Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes
density-dependent predation mortality in damselfishes. Ecology
83:2855–2868
Holbrook SJ, Brooks AJ, Schmitt RJ (2002a) Predictability of fish
assemblages on coral patch reefs. Mar Freshw Res 53:181–188
Holbrook SJ, Brooks AJ, Schmitt RJ (2002b) Variation in structural
attributes of patch-forming corals and in patterns of abundance
of associated fishes. Mar Freshw Res 53:1045–1053
Holmes G (2008) Estimating three-dimensional surface areas on coral
reefs. J Exp Mar Biol Ecol 365:67–73
Howard RK (1984) The trophic ecology of caridean shrimps in an
eelgrass community. Aquat Bot 18:155–174
Jacobsen L, Berg S (1998) Diel variation in habitat use by
planktivores in field enclosure experiments: the effect of
submerged macrophytes and predation. J Fish Biol
53:1207–1219
Janssen A, Sabelis MW, Magalhaes S, Montserrat M, Van der
Hammen T (2007) Habitat structure affects intraguild predation.
Ecology 88:2713–2719
Kane CN, Brooks AJ, Holbrook SJ, Schmitt RJ (2009) The role of
microhabitat preference and social organization in determining
the spatial distribution of a coral reef fish. Environ Biol Fishes
84:1–10
Kenyon RA, Loneragan NR, Hughes JM (1995) Habitat type and light
affect sheltering behaviour of juvenile tiger prawns (Penaeus
esculentus Haswell) and success rates of their fish predators.
J Exp Mar Biol Ecol 192:87–105
Kneib RT, Scheele CEH (2000) Does tethering of mobile prey
measure relative predation potential? An empirical test using
mummichogs and grass shrimp. Mar Ecol Prog Ser 198:181–190
Knowlton N (1980) Sexual selection and dimorphism in two demes of
a symbiotic, pair-bonding snapping shrimp. Evolution
34:161–173
Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions
(CPCe): a Visual Basic program for the determination of coral
and substrate coverage using random point count methodology.
Comput Geosci 32:1259–1269
Kulbicki M, Bozec Y-M, Labrosse P, Letourneur Y, Mou-Tham G,
Wantiez L (2005) Diet composition of carnivorous fishes from
coral reef lagoons of New Caledonia. Aquat Living Resour
18:231–250
Lammers JH, Warburton K, Cribb BW (2009) Anti-predator strate-
gies in relation to diurnal refuge usage and exploration in the
Australian freshwater prawn, Macrobrachium australiense.
Journal of Crustacean Biology 29:175–182
Lecchini D, Planes S, Galzin R (2007) The influence of habitat
characteristics and conspecifics on attraction and survival of
coral reef fish juveniles. J Exp Mar Biol Ecol 341:85–90
Lieske E, Myers R (2002) Coral reef fishes - Indo-Pacific and
Caribbean. Princeton University Press, Princeton, New Jersey
Lima SL (1998) Nonlethal effects in the ecology of predator-prey
interactions. What are the ecological effects of anti-predator
decision-making? BioScience 48:25–34
Linehan JE, Gregory RS, Schneider DC (2001) Predation risk of age-
0 cod (Gadus) relative to depth and substrate in coastal waters.
J Exp Mar Biol Ecol 263:25–44
Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP
(2002) Resource selection by animals: statistical design and
analysis for field studies. Kluwer Press, New York, USA
Meager JJ, Williamson I, Loneragan NR, Vance DJ (2005) Habitat
selection of juvenile banana prawns, Penaeus merguiensis de
Man: testing the roles of habitat structure, predators, light phase
and prawn size. J Exp Mar Biol Ecol 324:89–98
Medina M, Araya M, Vega C (2004) Alimentacion y relaciones
troficas de peces costeros de la zona norte de Chile. Invest Mar
Valparaıso 32:33–47
Munday PL (2004) Habitat loss, resource specialization, and extinc-
tion on coral reefs. Global Change Biol 10:1642–1647
Nagelkerken I, Dorenbosch M, Verberk W, de la Moriniere EC, van
der Velde G (2000) Day-night shifts of fishes between shallow-
water biotopes of a Caribbean bay, with emphasis on the
Coral Reefs (2014) 33:639–650 649
123
nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog
Ser 194:55–64
Nelson WG (1979) Experimental studies of selective predation on
amphipods: consequences for amphipod distribution and abun-
dance. J Exp Mar Biol Ecol 38:225–245
Noonan SH, Jones GP, Pratchett MS (2012) Coral size, health and
structural complexity: effects on the ecology of a coral reef
damselfish. Mar Ecol Prog Ser 456:127–137
Ochwada-Doyle F, Loneragan NR, Gray CA, Suthers IM, Taylor MD
(2009) Complexity affects habitat preference and predation
mortality in postlarval Penaeus plebejus: implications for stock
enhancement. Mar Ecol Prog Ser 380:161–171
Okuno J (1993) New record of a hinge-beak shrimp, Rhynchocinetes
hendersoni from eastern coast of Izu Peninsula, Japan. IOP
Diving News 4:4–5
Okuno J (1997) Crustacea Decapoda : Review on the genus
Cinetorhynchus Holthuis, 1995 from the Indo-West Pacific
(Caridea : Rhynchocinetidae). In: Richer de Forges B (ed) Les
fonds meubles des lagons de Nouvelle-Caledonie (Sedimentol-
ogie, Benthos). Orstom, Etudes & Theses, Paris, pp 31–58
Ory NC, Dudgeon D, Thiel M (2013) Host-use patterns and factors
influencing the choice between anemone and urchin hosts by a
caridean shrimp. J Exp Mar Biol Ecol 449:85–92
Ory NC, Dudgeon D, Dumont CP, Miranda L, Thiel M (2012) Effects
of predation and habitat structure on the abundance and
population structure of the rock shrimp Rhynchocinetes typus
(Caridea) on temperate rocky reefs. Mar Biol 159:2075–2089
Patton WK (1994) Distribution and ecology of animals associated
with branching corals (Acropora spp.) from the Great Barrier
Reef, Australia. Bull Mar Sci 55:193–211
Peacor SD, Werner EE (2001) The contribution of trait-mediated
indirect effects to the net effects of a predator. Proc Natl Acad
Sci USA 98:3904–3908
Peterson CH, Black R (1994) An experimentalist’s challenge - when
artifacts of intervention interact with treatments. Mar Ecol Prog
Ser 111:289–297
Peterson BJ, Thompson KR, Cowan JH, Heck KL (2001) Comparison of
predation pressure in temperate and subtropical seagrass habitats
based on chronographic tethering. Mar Ecol Prog Ser 224:77–85
Preston NP, Doherty PJ (1990) Cross-shelf patterns in the community
structure of coral-dwelling Crustacea in the central region of the
Great Barrier Reef. I. Agile shrimps. Mar Ecol Prog Ser 66:47–61
Preston NP, Doherty PJ (1994) Cross-shelf patterns in the community
structure of coral-dwelling Crustacea in the central region of the
Great Barrier Reef. II. Cryptofauna. Mar Ecol Prog Ser 104:27
Primavera JH (1997) Fish predation on mangrove-associated penae-
ids: the role of structures and substrate. J Exp Mar Biol Ecol
215:205–216
Quinn GP (2002) Experimental design and data analysis for
biologists. Cambridge University Press, Cambridge
Ray WJ, Corkum LD (2001) Habitat and site affinity of the round
goby. J Gt Lakes Res 27:329–334
Reebs SG (2002) Plasticity of diel and circadian activity rhythms in
fishes. Rev Fish Biol Fish 12:349–371
Schmitz OJ, Beckerman AP, Obrien KM (1997) Behaviorally
mediated trophic cascades: effects of predation risk on food
web interactions. Ecology 78:1388–1399
Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the
primacy of trait-mediated indirect interactions. Ecol Lett
7:153–163
Sih A (1997) To hide or not to hide? Refuge use in a fluctuating
environment. Trends Ecol Evol 12:375–376
Steffan SA, Snyder WE (2010) Cascading diversity effects transmitted
exclusively by behavioral interactions. Ecology 91:2242–2252
Stella JS, Jones GP, Pratchett M (2010) Variation in the structure of
epifaunal invertebrate assemblages among coral hosts. Coral
Reefs 29:957–973
Stella JS, Munday PL, Jones GP (2011b) Effects of coral bleaching on
the obligate coral-dwelling crab Trapezia cymodoce. Coral Reefs
30:719–727
Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011a) Coral-
associated invertebrates: diversity, ecological importance and
vulnerability to disturbance. In: Gibson R, Atkinson R, Gordon J,
Smith I, Hughes D (eds) Oceanogr Mar Biol Ann Rev pp 43–104
Tait KJ, Hovel KA (2012) Do predation risk and food availability
modify prey and mesopredator microhabitat selection in eelgrass
(Zostera marina) habitat? J Exp Mar Biol Ecol 426:60–67
Vance D (1992) Activity patterns of juvenile penaeid prawns in
response to artificial tidal and day-night cycles: a comparison of
three species. Mar Ecol Prog Ser 87:215–226
Vasquez J (1993) Abundance, distributional patterns and diets of
main herbivorous and carnivorous species associated to Lessonia
trabeculata kelp beds in Northern Chile. Serie Ocasional
Universidad Catolica del Norte 2:213–229
Veron J (2000) Corals of the world. AIMS, Townsville
Vytopil E, Willis B (2001) Epifaunal community structure in
Acropora spp. (Scleractinia) on the Great Barrier Reef: impli-
cations of coral morphology and habitat complexity. Coral Reefs
20:281–288
Wahle RA (1992) Substratum constraints on body size and the
behavioral scope of shelter use in the American lobster. J ExpMar Biol Ecol 159:59–75
Wahle RA, Steneck RS (1992) Habitat restrictions in early benthic
life: experiments on habitat selection and in situ predation with
the American lobster. J Exp Mar Biol Ecol 157:91–114
Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An
experimental test of the effects of predation risk on habitat use
in fish. Ecology 64:1540–1548
Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual
assessments of habitat complexity and benthic composition on
coral reefs. Mar Biol 151:1069–1076
Wilson SK, Fisher R, Pratchett MS (2013) Differential use of shelter
holes by sympatric species of blennies (Blennidae). Mar Biol
160:2405–2411
Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC
(2006) Multiple disturbances and the global degradation of coral
reefs: are reef fishes at risk or resilient? Global Change Biol
12:2220–2234
Worm B, Myers RA (2003) Meta-analysis of cod-shrimp interactions
reveals top-down control in oceanic food webs. Ecology
84:162–173
Yates D, Moore D, McCabe G (1999) The Practice of Statistics.
Freeman, W.H., New York
650 Coral Reefs (2014) 33:639–650
123