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: orynicolas@yahoo.fr

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.

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