Coral Reefs (2014) 33:639–650 DOI 10.1007/s00338-014-1163-0

REPORT

Effects of predation on diel activity and habitat use of the coral- reef shrimp Cinetorhynchus hendersoni ()

Nicolas C. Ory • David Dudgeon • Nicolas Duprey • Martin Thiel

Received: 3 January 2014 / Accepted: 29 April 2014 / Published online: 17 May 2014 Ó Springer-Verlag Berlin Heidelberg 2014

Abstract Nonlethal effects of predators on prey behav- on the reef; complex substrata were preferred, while simple iour are still poorly understood, although they may have substrata were avoided. Shrimps were abundant on high- cascading effects through food webs. Underwater obser- complexity columnar–foliate Porites rus, but tended to vations and experiments were conducted on a shallow make little use of branching Acropora spp. Subsequent fringing coral reef in Malaysia to examine whether pre- tethering experiments, conducted during daytime in June dation risks affect diel activity, habitat use, and survival of 2013, compared the relative mortality of shrimps on simple the rhynchocinetid shrimp Cinetorhynchus hendersoni. The (sand–rubble, massive Porites spp.) and complex (P. rus, study site was within a protected area where predatory fish branching Acropora spp.) substrata under different preda- were abundant. Visual surveys and tethering experiments tion risk scenarios (i.e., different tether lengths and expo- were conducted in April–May 2010 to compare the abun- sure durations). The mortality of shrimps with short tethers dance of shrimps and predatory fishes and the relative (high risk) was high on all substrata while, under low and predation intensity on shrimps during day and night. intermediate predation risks (long tethers), shrimp mortal- Shrimps were not seen during the day but came out of ity was reduced on complex corals relative to that on sand– refuges at night, when the risk of being eaten was reduced. rubble or massive Porites spp. Overall, mortality was Shrimp preferences for substrata of different complexities lowest on P. rus. Our study indicates that predation risks and types were examined at night when they could be seen constrain shrimp activity and habitat choice, forcing them to hide deep inside complex substrata during the day. Such Communicated by Biology Editor Dr. Glenn Richard Almany behavioural responses to predation risks and their conse- quences for the trophic role of invertebrate mesoconsumers Electronic supplementary material The online version of this warrant further investigation, especially in areas where article (doi:10.1007/s00338-014-1163-0) contains supplementary predatory fishes have been overexploited. material, which is available to authorized users.

N. C. Ory (&) N. Duprey Keywords Rhynchocinetid shrimps Habitat The Swire Institute of Marine Science, The University of Hong complexity Substratum structure Predator–prey Kong, Pokfulam Rd, Hong Kong, People’s Republic of China interactions Risk effects Tethering e-mail: [email protected]

N. C. Ory D. Dudgeon N. Duprey School of Biological Sciences, The University of Hong Kong, Introduction Pokfulam Rd, Hong Kong, People’s Republic of China

M. Thiel Predators can affect prey abundance by increasing their Facultad Ciencias del Mar, Universidad Cato´lica del Norte, mortality, or by causing sublethal reductions in prey Larrondo 1281, Coquimbo, Chile activity due to behavioural adjustments in response to predators (i.e., risk effects; e.g., Lima 1998; Creel and M. Thiel Centro de Estudios Avanzados en Zonas A´ ridas (CEAZA), Christianson 2008). A growing body of evidence indicates Coquimbo, Chile that such risk effects can have important effects on 123 640 Coral Reefs (2014) 33:639–650 mesoconsumer activity that can cascade through food webs were more numerous and diverse on those corals with (Peacor and Werner 2001; Schmitz et al. 2004; Steffan and narrowest branch spacing where prey mortality was lowest. Snyder 2010). Nonetheless, the consequences of risk Similarly, Edwards and Emberton (1980) observed that the effects remain difficult to predict because the factors abundance of decapods associated with individual colonies influencing predator avoidance by mesoconsumers are of Stylophora pistillata (Pocilloporidae) decreased as the poorly known (Reebs 2002; Heithaus et al. 2009). spacing between coral branches widened. Given that a reduction in risk usually comes at the cost The need to avoid predators may confine prey activities of reduced foraging and mating opportunities (Werner et al. to periods when predators are less active (Duffy and Hay 1983; Sih 1997), antipredatory behaviours generate trade- 2001; Aumack et al. 2011). For example, nocturnal for- offs between benefits and costs to prey fitness. The use of aging by small fishes and invertebrates may be an adap- structurally complex habitats may reduce prey detectabil- tation to avoid visually oriented predatory fishes (Vance ity, impair predator attack success, or prevent predators 1992; Jacobsen and Berg 1998; Lammers et al. 2009)as from accessing prey hiding inside small refuges such as prey mortality is usually lower at night (Clark et al. 2003; holes or crevices (reviewed in Denno et al. 2005). Indeed, a Bassett et al. 2008). However, the general effects of pre- refuge size that matches the size of the prey is one of the dation risk on diel activity of coral-reef invertebrates best predictors of the protective value of a refuge (Eggle- remain unclear. ston et al. 1990; Wahle 1992; Wilson et al. 2013). Con- The present study examined the antipredatory responses versely, however, habitat complexity can improve the of coral-reef shrimps to predation risks from fishes, in foraging efficiency of predators (e.g., Flynn and Ritz 1999), terms of both temporal activity pattern and microhabitat or protect them from intraguild predation (reviewed by selection. The model species was Cinetorhynchus hender- Janssen et al. 2007), and cannibalism (Finke and Denno soni (Rhynchocenitidae), which is common in shallow 2006), indicating that the relationship between prey sur- (1–10 m) waters of the Indo-Pacific, from the east coast of vival and habitat complexity may not be straightforward. Africa to French Polynesia, and to Honshu (Japan) in the Accordingly, when predation risks are high, prey tend to north (Okuno 1997). Rhynchocinetid shrimps are important use only the most complex habitats that provide the most components of many coastal benthic communities (Caill- effective protection against predators (i.e., habitats that aux and Stotz 2003; Ory et al. 2013) where they can play a equal or exceed the ‘habitat complexity threshold’; Nelson significant role as prey for many fish species (Va´squez 1979; Gotceitas and Colgan 1989). 1993; Ory et al. 2012) and as epibenthic predators (Dumont Coral reefs are heterogeneous environments comprising et al. 2009, 2011). C. hendersoni has been reported as a mosaic of discrete habitats with different structural being nocturnal, hiding inside small holes and crevices on complexity (e.g., Gratwicke and Speight 2005; Wilson reefs during the day while emerging at night to forage et al. 2007; Holmes 2008). Thus, they provide an excellent (Okuno 1993). opportunity to determine whether habitat use by inverte- In order to examine whether predation risk influenced brate prey subject to predation by fishes is affected by diel activity and habitat preference of shrimps, we under- substratum complexity. Most studies of the relationship took underwater visual surveys and field experiments on a between habitat complexity and prey abundance or diver- protected Malaysian coral reef in Tioman Island where sity have focussed on fish as prey (e.g., Caley and St John fishes were diverse and abundant (Harborne et al. 2000). 1996; Holbrook et al. 2002a; Noonan et al. 2012). How- Observations were made during the day and at night to test ever, invertebrates, such as shrimps and other decapods, are whether diel variations of shrimp abundance on the reef abundant and diverse on coral reefs (Stella et al. 2010, were negatively related to fish abundance and relative risk 2011a) and, as they are usually less mobile than fishes, of predation. Surveys and tethering experiments were also their distribution is more likely to be strongly influenced by used to test the hypothesis that shrimps most often use variations in habitat complexity (Vytopil and Willis 2001; complex habitats and that their preferred substrata (i.e., Dulvy et al. 2002), as has been shown in various studies microhabitats) offer better protection against fishes. 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 Materials and methods (e.g., whether they are branching, columnar, foliate, or massive) may affect their effectiveness as a refuge for Study site shrimps and other invertebrates and may thereby influence diversity and abundance of these epibionts. For example, The study area (200 9 50 m) was located *20 m offshore Vytopil and Willis (2001) found that epibionts associated Kampung Tekek, Pulau Tioman Marine Park, Malaysia with four species of branching Acropora (Acroporidae) (Fig. 1) on a shallow (4–8 m deep), gently sloped, fringing 123 Coral Reefs (2014) 33:639–650 641

Fig. 1 Map of part of Southeast Asia, and insets showing Tioman island and the location of the studied site (circle)ona fringing coral reef in front of Tekek village (N 2°4805700;E 104°0903100)

coral reef (Amri et al. 2008). All in situ observations and with a wide angle light beam were used to cover the entire experiments were conducted on seven coral reef patches transect width. As observed in other studies (Nagelkerken (250–500 m2 total area) separated from each other by at et al. 2000; Ray and Corkum 2001), light did not appear to least 10 m of sandy bottom. The community of hard scare fishes as they did not flee farther from the observer scleractinian corals, described by Amri et al. (2008), was than during the day. Preliminary field observations indi- dominated by large colonies of columnar–foliose Porites cated that artificial lights did not induce rapid escape rus (Poritidae), massive Porites spp. (P. lobata and P. lutea reactions by C. hendersoni although, when disturbed, they were both common), and tabulate and branching Acropo- retreated slowly into the closest refuge. Observations made ridae including Acropora nobilis and A. formosa (Harborne in the laboratory (Corredor 1978; Kenyon et al. 1995) et al. 2000). An initial study was conducted in 2010 to confirmed that artificial lights did not induce erratic escape compare diel patterns of fish and shrimp abundance and reactions from other shrimp species. All predatory fishes shrimp mortality using underwater visual surveys and [5 cm in total length within 2.5 m of each side of the tethering experiments. Further tethering experiments were transect line were identified to the species level and carried out in 2013 to examine mortality of shrimps asso- counted (following Lieske and Myers 2002). Shrimp ciated with substrata (microhabitats) that varied in com- abundance was assessed by a second diver, following plexity (see below). Water temperatures were similar 5 min after the fish surveyor, who counted all C. hender- (range 29–31 °C) between the 2 yr, and all experiments soni (henceforth ‘shrimps’) observed within a 50 9 50 cm were conducted when underwater visibility exceeded 7 m. quadrat placed on the reef surface at 1-m intervals on alternate sides of the transect line. After counting the Abundance of fishes and shrimps shrimps, a photograph of the quadrat was taken with a Canon G10 digital camera for later analysis of substratum Abundance of fishes and shrimps was visually assessed type and complexity. On a single day, one or at most two from 1 May to 5 May 2010 during the day and at night by transects were surveyed once in the afternoon, between scuba diving along a 20-m transect line laid on the surface 1400 hrs and 1600 hrs, and again after dusk on the same of the coral reefs (total n = 7 transects). At night, torches night, between 2000 hrs and 2200 hrs. 123 642 Coral Reefs (2014) 33:639–650

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)

The abundance of fishes and shrimps was compared 5 were assigned to quadrats with, respectively, \5%, between night and day using a nonparametric Wilcoxon 5–25 %, 26–50 %, 51–75 %, and over 75 % of their sur- paired-test (number of transect replicates = 7); homoge- face covered by complex three-dimensional architecture neity of variance of the data was verified with Levene’s test substrata (e.g., branching, columnar, or foliate dead or (a = 0.001). These and all other statistical tests were living coral; Fig. 2). Bedrock, sand–rubble mixture, loose undertaken using SPSSÒ version 18. or consolidated rubble, or massive coral (dead or living) were categorized as low complexity substrata (Fig. 2), Substratum type and complexity because they provided no or few refuges to shrimps. Sur- face cover of complex substrata was quantified for each Photoquadrats were analysed to examine shrimp prefer- quadrat from the analysis of the photoquadrats using the ences for substratum complexities and type, separately. Coral Point Count with Excel extensions (CPCe) program The complexity of the substratum was defined here by the with 50 random points (Kohler and Gill 2006). rugosity of the reef surface (i.e., the amount of ‘irregular- The percentage cover of substratum types within each ities’ of the reef surface; Dunn and Halpin 2009) and the quadrat was quantified from photoquadrats as above to presence of small (\5 cm) refuges (i.e., holes and crevices examine shrimp preferences for each type of substratum. of the substratum, as for example in Friedlander and Par- Substratum types were recorded using eight main catego- rish 1998; Almany 2004; Gratwicke and Speight 2005; ries (see electronic supplementary materials, ESM, Table Wilson et al. 2007). Substratum complexity was estimated S1): (1) bedrock and large boulders (referred as ‘rock’ from photoquadrats using five complexity scores adapted thereafter), (2) loose (unconsolidated) rubble, (3) consoli- from Ory et al. (2012). Complexity scores of 1, 2, 3, 4, and dated rubble, (4) sand–rubble (sand mixed with small

123 Coral Reefs (2014) 33:639–650 643 pieces of loose rubble), (5) soft coral (Alcyonacea), (6) Shrimp capture and maintenance bleached or recently dead hard coral (white Scleractinia not yet overgrown), (7) hard dead coral (dead Scleractinia with Shrimps were collected by hand, using plastic calipers to its original structure overgrown by fouling organisms), and gently coax them into a plastic Ziploc bag, or by traps that were (8) hard living scleractinian coral (Fig. 2). Hard corals (in deployed at night to increase the number of shrimps collected. substratum types 6, 7, and 8) were further subcategorized A plastic colander (30 9 15 9 15 cm) with 3-mm holes was by their or species and their growth forms, i.e., filled with coral rubble to provide shelter for shrimps and massive, encrusting, digitate, columnar, foliate, or placed on the reef surface near colonies of P. rus and branching (Veron 2000; ESM Table S1). branching Acropora spp. where shrimps were often sighted. Shrimp preferences for substrata were examined sepa- The following night, a second inverted colander was placed rately, using two Pearson chi-squared goodness-of-fit tests over the first one, thereby enclosing any shrimps among the 2 (vp) to test the null hypotheses of random choice of sub- rubble. Prior to being used in tethering experiments, all strata complexity and type as a function of their availability shrimps were held together for up to 3 d in an opaque plastic (Manly et al. 2002). Where the null hypothesis was rejec- bucket (60 cm diameter) containing 20 cm of aerated sea ted, substratum preference was determined using the Manly water at 28–31 °C under a natural lighting regime. There was resource selection index wˆ i, which is the ratio between no shrimp mortality during this pre-tethering period. proportions of resource (i.e., substratum types) of category i used by shrimps (oi) and the availability of these substrata Tethering experiments ðp^iÞ estimated from their percentage cover within each quadrat in the survey area. Shrimps were tethered during the day or at night to

Calculation of the standard error of wˆ i depends on the examine diel variation of relative predation risks. We also basic sampling unit used to estimate resource (i.e., substra- tested the relative mortality of shrimps tethered on different tum) availability (Manly et al. 2002). In this study, sub- substrata with complex or simple structure to compare stratum complexity was an index estimated from a single which offered better protection against predators. We ran value for each quadrat, i.e., random points were used as the the experiments for short (10 min) and long (30 min) basic sampling units; standard error of wˆ i was therefore durations and employed different lengths of tethers qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi allowing shrimps to hide in the periphery of the tested seðw^iÞ¼w^i 1=li 1=lþ þ 1=mi 1=mþ substrata (short tethers) or deeper inside the complex substrata (long tethers). Shrimp mortality was thus com- (Manly et al. 2002: Eq. 4.23), where m is the number of i pared among each substratum under increasing predation quadrats of complexity category i sampled, m is the total ? risks: low (shrimps with long tether for 10 min), interme- number of quadrats sampled, l is the proportion of i diate (shrimps with long tether for 30 min), and high shrimps using quadrats of complexity category i, and u ? (shrimps with short tether for 30 min). Despite the recog- the total number of shrimps sampled. nized short comings of tethering experiments and the need The mean availability of each substratum type was to interpret the results with caution (e.g., Kneib and estimated as its proportion of all substrata within each Scheele 2000), these experiments can help to identify the quadrat. The standard error of wˆ i was therefore qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi safest time periods for shrimps to be active and to provide a 2 2 first indication of the protective value of different substrata. seðw^iÞ¼w^i ð1 oiÞ=ðoilþÞþseðp^iÞ =p^i (Manly et al. 2002: Eq. 4.25). Diel comparison of relative predation on shrimps Bonferroni-corrected 95 % confidence intervals (CI) were calculated around each wˆ i to test whether they dif- After fish and shrimp surveys in May 2010, tethering fered from 1, i.e., the null hypothesis of no selection, with experiments were conducted in the field from 09 May to 13 values [1 indicating overuse (i.e., selection) of a substra- May to compare the relative intensity of predation by fishes tum category, and values \1 indicating underuse (i.e., on shrimps during the day and at night. The day prior to avoidance). Substratum complexity categories 1 and 2 were experiments a 15-cm long monofilament was attached to pooled into a single category (Manly et al. 2002) to ensure the dorsum of the third abdominal segment of each shrimp that [25 % of expected shrimp counts were [5 and none using cyanoacrylate glue. All tethers remained attached to \1 (Yates et al. 1999). For the same reason, the three types the shrimps by the next morning, with the exception of two of substratum with the lowest complexity (sand–rubble, shrimps that had moulted overnight. The size of shrimps rock, and massive Porites spp.) were pooled. Substrata (5–7 mm carapace length, CL) used in tethering experi- seldom recorded (occurring in \10 quadrats) were not ments was chosen according to the mean CL (6.0 ± SD included in the analysis (ESM Table S1). 0.9 mm) measured from 52 shrimps previously collected 123 644 Coral Reefs (2014) 33:639–650 from the field (these shrimps were not used in experi- number of shrimps tested on living massive Porites spp. and ments). Large males, which develop hypertrophied first sand–rubble bottom was limited to 8 and 7, respectively, pereopods (Okuno 1997), were not used in the experiments because all shrimps were observed being eaten quickly by to avoid potentially confounding effects of shrimp mor- fishes. Shrimp presence was monitored after 10 min and, phology that can affect their susceptibility to predators again, after 30 min. Any shrimp that had disappeared by (Ory et al. 2012). Tethered shrimps were placed inside 10 min was also scored absent after 30 min. Upon completion individual plastic tubes (length 9 diameter = 10 9 5 cm) of tethering experiments, surviving shrimps were released at and transported to the field site within 20 min. Under the site where they had been captured. water, a single shrimp, was tethered to the centre of a grey Shrimp mortality among different substrata under high PVC plate (50 9 50 9 0.5 cm) anchored to the seafloor predation risk scenario was not analysed as all shrimps with a 1-kg diving weight. Tethered shrimps were unable to were eaten on all substrata. Two Pearson chi-square tests leave the plate, with nowhere to hide, and were thus were run separately to test the null hypotheses that mor- exposed to predators for 30 min, after which they were tality of tethered shrimps was similar on different substrata scored as present (and live) or absent (presumed eaten). and under low or intermediate predation risk scenarios. Tethering experiments were conducted in the afternoon When the null hypothesis was rejected, pairwise compari- (1400–1600 hrs) and the same night (2000–2200 hrs) for sons were performed to test differences in mortality among two consecutive days (9 and 10 May). Fifteen and nine all substratum categories. Sand–rubble and living massive unique shrimp individuals were used during the day and ten Porites spp. were pooled in a single ‘simple substrata’ and 11 at night, on the two respective dates. Two Pearson category to ensure that[25 % of expected shrimp presence chi-square tests (Quinn 2002) were performed separately to counts were [5 and none \1. 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. Results

Comparison of shrimp mortality on different substrata Diel variation of fish and shrimp abundance

On 16 June 2013, tethering experiments were conducted to A total of 181 individuals of 25 species of predatory fishes compare mortality after 30 min of shrimps tethered with were recorded during the day and 84 individuals of 11 spe- 15-cm nylon monofilament (high predation risk) among cies at night (Table S2). Fish abundance varied from 11 to 25 four of the most common substrata observed in 2010: two individuals per 100 m-2 (mean ± SE = 20.3 ± 1.9; with complex structure (living P. rus and branching Ac- n = 7; Fig. 3a) during the day, but was lower at night ropora spp.) and two with simple structure (sand–rubble (U = 3.0, P = 0.006, number of transects = 7), ranging and living massive Porites spp., see below). All trials were from four to 16 individuals 100 m-2 (9.9 ± 1.9; n = 7; conducted during the day (1400–1600 hrs) on a single coral Fig. 3a). Predatory fish species richness was also higher patch (70 9 50 m) studied in 2010 where all four substrata during the day (10.3 ± 1.01 species 100 m-2; n = 7) than were present and fish abundance was high. Shrimps were at night (4.1 ± 0.6 species 100 m-2; U = 0.50, P \ 0.001). tethered to a branch or a column of large ([50 cm diam- No shrimps were seen on the reef during the day, whereas eter) P. rus (number of shrimp tested = 5) or Acropora their abundance along all transects was 1.8 ± 0.3 individ- spp. (n = 5), or to a fishing weight (200 g) placed on the uals 0.25 m-2 (number of quadrats = 140) at night surface of massive Porites colonies (n = 5), or to a weight (Fig. 3a), ranging from 0.8 ± 0.4 SE to 3.3 ± 0.6 individ- placed on the sand–rubble bottom (n = 5). All shrimps uals 0.25 m-2 per transect (number of quadrats per tran- were observed being quickly eaten by fishes, so that no sect = 20). The maximum number of shrimps within a further trials were conducted to not unnecessarily kill more quadrat was nine individuals, with 2.7 ± 0.2 ind 0.25 m-2 shrimps in the Marine Park. in quadrats where at least one shrimp was present (n = 79). On the 19 and 21 June 2013, tethering experiments were conducted during the day on the same coral patch to test the Shrimp habitat use survival of shrimps tethered with longer nylon monofilament (40 cm) and to verify whether mortality was reduced when The mean number of shrimps ranged from 0.5 ± 0.1 to shrimps were able to retreat deeper into coral refuges. Shrimp 2.8 ± 0.3 individuals 0.25 m-2 in quadrats of lowest (i.e., mortality was thus tested under intermediate (shrimps with pooled category 1–3) and highest complexity, respectively. long tether for 30 min) and low (shrimps with long tether for The abundance of shrimps differed in relation to substra- 10 min) predation risks for all substrata. A total of 15 tethered tum complexity (v2 = 59.9, df = 3, P \ 0.001; Fig. 4a). shrimps were tested on P. rus and 14 on Acropora spp. The Overall, 56.3 % of all shrimps observed (n = 215) were 123 Coral Reefs (2014) 33:639–650 645

abFishes 70 ab 30 Shrimps 5 SE 60 ) ) 25 -2 -2 4 50 (%)

20 y 3 40

15 30 mortalit 2 p 10

20 Shrim

1 5 10 Number of fishes (ind 100 m Number of shrimps(ind 0.25 m 0 0 0 0 Day Night Day Night Day Night Fig. 4 a Availability (proportion total quadrats) of substrata of Fig. 3 a Median (solid line crossing the box) and average (dotted different complexity and their use by shrimps (proportion of total line) shrimp and predatory fish abundances along reef surface shrimp number). b Selection index (±95 % CI) for each substratum transects (n = 7) around Tioman. The lower and upper boundaries complexity category. Asterisks indicate selection ([1) or avoidance of the box represent, respectively, the first and third quartile; the (\1) at the level of error a = 5 % (after Bonferroni correction) 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) substantially higher during the day (64 % of the total, n = 24) than at night (6 %; n = 21; v2 = 16.29, df = 1, found in quadrats with the highest complexity, which P \ 0.001; Fig. 3b), but did not vary between the two con- constituted 30.7 ± 0.1 % of all the quadrats (n = 140). secutive days of experiments (v2 = 0.15, df = 1, P = 0.70). Quadrats with the lowest substratum complexity (i.e., cat- Under the high predation risk scenario, all shrimp with egories 1 and 2) accounted for 37.9 ± 0.1 % of all quad- 15-cm tethers were eaten within 30 min on branching Ac- rats, but harboured only 10.7 % of all shrimps. Shrimps ropora spp. or massive Porites spp., while those on sand– selected the most complex substrata (wˆ i = 1.8; Fig. 4b; rubble or massive Porites spp. were observed being eaten ESM Table S3a) and did not show any preference for within several seconds of exposure (Fig. 6; ESM Table substrata of intermediate complexity (wˆ i = 1.0), but avoi- S4a). Under intermediate predation risks, shrimp mortality 2 ded those with the lowest complexity (wˆ i = 0.4). varied according to substratum category (v = 6.27, The most abundant substratum types within the study area df = 2, P = 0.036). Although shrimp mortality did not were the foliate–columnar living scleractinian P. rus (22 % of differ between branching Acropora spp. (89 %) and P.rus total cover), consolidated rubble (15 %), sand–rubble (16 %), (67 %; v2 = 1.44, df = 1, P = 0.39) or between Acropora branching living scleractinian Acropora spp. (7 %), rock spp. and sand–rubble ? massive Porites spp. (100 %; (6 %), dead P. rus (5 %), and branching (4 %) and massive v2 = 2.30, df = 1, P = 0.22), it was nonetheless lower on living Porites spp. (4 %; Fig. 5a; ESM Table S1). Loose P. rus compared to sand–rubble ? massive Porites spp. rubble (3 %), soft coral (2 %), and bleached scleractinian (v2 = 6.0, df = 1, P = 0.01; Fig. 6; ESM Table S4b). corals (\0.1 %) were present at low abundance and excluded Under the low predation risk scenario (i.e., 40-cm tether, from subsequent analyses (ESM Table S1). Shrimps showed 10-min duration), shrimp mortality also differed among all preferences for particular substrata (v2 = 129.09, df = 5, substrata (v2 = 15.47, df = 2, P \ 0.001): it was lower on P \ 0.001; ESM Table S3b). Shrimps preferred living coral branching Acropora spp. (71 %) than on sand–rub- 2 P. rus (wˆ i = 2.1; Fig. 5b; ESM Table S3b) and consolidated ble ? massive Porites spp. pooled (100 %; v = 4.97, rubble (wˆ i = 1.7), but avoided sand–rubble, rock, and mas- df = 1, P = 0.026), but higher than on P. rus (33 %; 2 sive Porites spp. (wˆ i = 0.0) with low complexity. Shrimps v = 4.21, df = 1, P = 0.04; Fig. 6; ESM Table S4c). also showed a tendency to avoid branching Acropora spp.

(wˆ i = 0.5), despite their complex structure. Shrimps had no significant preference between dead P. rus (wˆ i = 1.6) or liv- Discussion ing branching Porites spp. (wˆ i = 1.2). Diel activity patterns Tethering experiments Shrimps hid during the day and were visible on the reef only Tethering experiments in 2010 revealed that mortality of at night, a behaviour typical of many small and medium- shrimps tethered for 30 min on plates without refuges was sized prey organisms (e.g., Bauer 1985;Beck1997; 123 646 Coral Reefs (2014) 33:639–650

Fig. 5 a Availability ab (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)

Porites rus hendersoni. Instead, C. hendersoni are inactive during the Branching Acropora spp. Sand-rubble + massive Porites spp. pooled day to avoid predators: our tethering experiments revealed that shrimp mortality was substantially lower at night than ab NA B c during the day, as also found from other experiments on 100 small fish and decapod prey in coral reefs (Acosta and Butler A,B 1999), macrophyte habitats (Linehan et al. 2001; Peterson 80 b et al. 2001), rocky reefs (Diaz et al. 2005; Bassett et al. 2008) A and estuaries (Clark et al. 2003). 60 Nocturnal activity appears to be more pronounced in tropical waters (Castro 1978; Knowlton 1980) than in tem- 40 perate waters, where some may also exhibit a daytime activity (De Grave and Turner 1997; Cannicci et al. Shrimp mortality (%) 20 1999), perhaps because of lower predation risks at higher latitudes (Heck and Wilson 1987; Freestone et al. 2011). In 5 5 10 15 14 15 15 14 15 contrast to C. hendersoni in Malaysia, ty- 0 High risks Intermediate risks Low risks pus, a rhynchocinetid that inhabits temperate reefs in Chile, (short tether, (long tether, (long tether, was visible during the day (Ory et al. 2012). R. typus long duration) long duration) short duration) occupied shelters that did not prevent access to predators, Fig. 6 Proportion of shrimp mortality (i.e., absence) on different type but where they were able to form large aggregations. Fish of substrata (branching Acropora spp.; columnar–foliate Porites rus; abundance and diversity, and thus predation on shrimps, massive Porites spp., and sand–rubble pooled) under (a) high were lower on rocky reefs in Chile than in Malaysia, and (shrimps attached with 15-cm tethers for 30 min) and (b) intermediate (shrimp attached with 40-cm tethers for 30 min), and low (shrimps densities of R. typus were [10 times higher than C. hen- attached with 40-cm tethers for 10 min) predation risks. Numbers dersoni in Malaysia. Latitudinal comparisons of day–night inside bars indicate the sample size. Similar letters indicate no activity and host use of small invertebrates could be used to difference in shrimp mortality after 10 (lower case) and 30 (upper test the hypothesis that prey are strictly nocturnal in envi- case) min. NA not analysed ronments where predation risks are the highest. Kulbicki et al. 2005). While nocturnal activity may, in some cases, have evolved in response to heat stress (Cannicci et al. Mortality risks on shrimps 1999), hypoxia (Berglund and Bengtsson 1981), or changes in food availability (Vance 1992), it is unlikely that these During the day, shrimp are only safe if they can hide in the factors are responsible for diel activity patterns of C. most complex habitats. P. rus colonies comprise a 123 Coral Reefs (2014) 33:639–650 647 combination of tightly packed columns and complex foliate of four preliminary tethering experiments revealed that structures containing many small holes and crevices that shrimps were eaten by fishes: C. boenak, Halichoeres provide refuges from most predators (Holbrook et al. melanurus (Labridae) and Cheilinus trilobatus (Labridae). 2002b; Lecchini et al. 2007). Although the branching structure of Acropora spp. was complex, these corals did Habitat features and shrimp preferences not provide good protection for shrimps since they failed to prevent access of small predatory fishes. Other studies have Shrimps were mostly observed on complex habitats and reported that small fishes which attempt to seek refuge were seldom encountered on sand–rubble or massive hard among coral colonies with widely spaced branches suffer corals, where tethering experiments during the day dem- high rates of predation from resident fishes that hide in the onstrated that they suffered the highest mortality. These coral in order to avoid their own predators (Holbrook and results indicate that high predation risks restricted shrimps Schmitt 2002; Kane et al. 2009). Indeed, on two occasions, to those habitats that exceeded the ‘habitat complexity shrimps still attached to their tether were found inside the threshold’ (Nelson 1979; Coull and Wells 1983;Bar- mouths of small Cephalopholis boenak (Serranidae; tholomew et al. 2000). Unlike C. hendersoni, other shrimp 5–7 cm total length), which were hiding among the bran- species appear to be protected at relatively low levels of ches of Acropora spp. substratum complexity (Primavera 1997; Ory et al. 2012), The length of the tether did not enhance the survival of further supporting the notion that shrimps in Malaysia C. hendersoni on sand and massive Porites spp., where no experience high predation risk within the marine protected refuges were available, but tended to reduce shrimp mor- area where we worked. tality on both Acropora spp. and P. rus. Longer tethers Cinetorhynchus hendersoni showed strong preferences appeared to have allowed shrimps to access deeper spaces for the columnar–foliate P. rus, but tended to avoid inside coral colonies where they were less vulnerable to branching Acropora spp., although both coral genera have predators, and Holbrook and Schmitt (2002) have noted complex structures. Many small crustaceans and fish prey that damselfish (Dascyllus trimaculatus: Pomacentridae) species hide among a wide range of coral species of different suffer lower predation risks in the centre of branching coral structural complexities (Patton 1994; Stella et al. 2011a) colonies than at their periphery. Nonetheless, the mortality according to the level of protection they provide against of shrimps was high in the high predation risk scenarios on predators (Vytopil and Willis 2001; Noonan et al. 2012). Our both Acropora spp. and P. rus, perhaps because the tethers tethering results showed that shrimp mortality was lower on were too short to allow shrimps to retreat into the deepest P. rus than on Acropora spp., indicating that these corals and most effective refuges. offered shrimps different levels of protection from preda- Predation intensity may be higher on tethered than free tors. These observations confirm that shrimp habitat pref- prey, mainly because tethered prey cannot escape when erences are driven, at least in part, by predation risks, as also attacked by predators (e.g., Wahle and Steneck 1992; shown in other environments such as macrophyte beds Kneib and Scheele 2000; Haywood et al. 2003). Our (Meager et al. 2005; Ochwada-Doyle et al. 2009). tethering experiments did not intend to assess the absolute Shrimps in Malaysia were abundant on dead P. rus intensity of predation on shrimps but, instead, were used to colonies, which contradicts the commonly held view that compare relative shrimp mortality attributable to predation coral-associated invertebrates and fishes are less abundant between different treatments (day-night and type of sub- when living coral cover is low (Munday 2004; Stella et al. stratum). Such comparisons are valid if any potential 2011b). However, other studies have also found that tethering artefacts are independent of the treatments and do epibionts are most abundant on dead corals not confound their comparison (Peterson and Black 1994). (Preston and Doherty 1990, 1994; Stella et al. 2010), per- In our experiments, tethered shrimps may have suffered haps because they feed on the sediments accumulating on increased mortality in complex habitats where they could the coral (Preston and Doherty 1994) or on the over- have become entangled, but any confounding effect would growing fouling communities (e.g., R. typus in rocky reefs only have made our results more conservative (i.e., it in Chile: Dumont et al. 2009, 2011). Although, in the long- would tend to reduce the difference in shrimp mortality term, coral-associates such as shrimps may suffer higher between complex and more simple substrata). mortality when dead corals lose their structural complexity, It is unlikely that predation on shrimps could have been they can use these corals as shelter and feeding ground in attributable to other invertebrates, such as urchins or crabs, the interim (Wilson et al. 2006). Grazing by C. hendersoni or from cannibalism, because shrimp mortality was very and other small mesoconsumers may even, as shown for low at night when invertebrates are active. Also, none of fishes and urchins (Bellwood et al. 2004), reduce fouling of these invertebrates were observed in the vicinity of shrimps dead coral (Brawley and Adey 1981), thereby favouring at the end of the experiments. In addition, video recordings settlement of new colonies. 123 648 Coral Reefs (2014) 33:639–650

Implications of research findings 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 Predation was an important factor influencing diel activity Aumack CF, Amsler CD, McClintock JB, Baker BJ (2011) Changes and habitat use of C. hendersoni, as also shown for many in amphipod densities among macroalgal habitats in day versus other coral-reef invertebrates (e.g., Acosta and Butler 1999; night collections along the Western Antarctic Peninsula. Mar Clark et al. 2003; Aumack et al. 2011). Small decapod Biol 158:1879–1885 Austin A, Austin S, Sale P (1980) Community structure of the fauna crustaceans often dominate marine benthic communities associated with the coral Pocillopora damicornis (L.) on the (e.g., Austin et al. 1980; Stella et al. 2010), where they are Great Barrier Reef. Mar Freshw Res 31:163–174 prey for many fishes (Angel and Ojeda 2001; Medina et al. Bartholomew A, Diaz RJ, Cicchetti G (2000) New dimensionless 2004; Kulbicki et al. 2005) and predators of small sessile indices of structural habitat complexity: predicted and actual effects on a predator’s foraging success. Mar Ecol Prog Ser organisms (Dumont et al. 2009), thereby playing an 206:45–58 important role within marine food webs (Howard 1984; Bassett DK, Jeffs AG, Montgomery JC (2008) Identification of Worm and Myers 2003; Dumont et al. 2011). Depletion of predators using a novel photographic tethering device. Mar predators due to overfishing can release predation risks on Freshw Res 59:1079–1083 Bauer RT (1985) Diel and seasonal variation in species composition mesoconsumers such as shrimps (Albers and Anderson and abundance of caridean shrimps (Crustacea, ) from 1985; Worm and Myers 2003) and thereby affect lower seagrass meadows on the north coast of Puerto Rico. Bull Mar trophic levels (Schmitz et al. 1997; Dorn et al. 2006). On the Sci 36:150–162 other hand, destruction of coral reefs may increase predation Beck MW (1997) A test of the generality of the effects of shelter bottlenecks in four stone crab populations. Ecology risks on mesoconsumers which use complex coral habitats as 78:2487–2503 refuge. These interactions and the behavioural responses of Bellwood D, Hughes T, Folke C, Nystro¨m M (2004) Confronting the mesoconsumers in the face of varying predation risks war- coral reef crisis. Nature 429:827–833 rant further investigation, as they could enhance under- Berglund A, Bengtsson J (1981) Biotic and abiotic factors determin- ing the distribution of two prawn species: Palaemon adspersus standing of the potential cascading of effects of overfishing and P. squilla. Oecologia 49:300–304 and the degradation of coastal reefs (Heithaus et al. 2008). Brawley S, Adey W (1981) The effect of micrograzers on algal community structure in a coral reef microcosm. Mar Biol Acknowledgments This study was financed by the Swire Educa- 61:167–177 tional Trust, John Swire & Sons (Hong Kong) Ltd., and was part of a Caillaux LM, Stotz WB (2003) Distribution and abundance of Ph.D. project by NCO. We are grateful to Clement Dumont who Rhynchocinetes typus (Crustacea: Decapoda), in different ben- initiated the study of the biology of rhynchocinetid shrimps in thic community structures in northern Chile. J Mar Biol Assoc U Southeast Asia and encouraged this study. We thank Kee Alfian Adzis K 83:143–150 for logistical assistance, and the Malaysian Ministry of the Natural Caley MJ, St John J (1996) Refuge availability structures assemblages Resources and the Environment for allowing us to work in Tioman of tropical reef fishes. J Anim Ecol 65:414–428 Marine Park. We are also grateful to Katie Yewdall, Rosie Cotton and Cannicci S, Paula J, Vannini M (1999) Activity pattern and spatial members of Tioman Dive Centre and East Divers in Tekek for their strategy in Pachygrapsus marmoratus (Decapoda: Grapsidae) kindness and professionalism; Solomon Chak for his assistance dur- from Mediterranean and Atlantic shores. Mar Biol 133:429–435 ing 2010; Daniel Pedraza for his help during field experiments; and Castro P (1978) Movements between coral colonies in Trapezia Raymond Bauer for the identification of C. hendersoni.We ferruginea (Crustacea: Brachyura), an obligate symbiont of acknowledge the constant support of Evelyn Lostarnau and her design scleractinian corals. Mar Biol 46:237–245 and construction of tools for the 2013 fieldwork. 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 References Natantia, Palaemonidae). Crustaceana 35:35–40 Coull BC, Wells J (1983) Refuges from fish predation: experiments Acosta CA, Butler MJ (1999) Adaptive strategies that reduce with phytal meiofauna from the New Zealand rocky intertidal. predation on Caribbean spiny lobster postlarvae during onshore Ecology 64:1599–1609 transport. Limnol Oceanogr 44:494–501 Creel S, Christianson D (2008) Relationships between direct preda- Albers WD, Anderson PJ (1985) Diet of Pacific cod, Gadus tion and risk effects. Trends Ecol Evol 23:194–201 macrocephalus, and predation on the northern pink shrimp, De Grave S, Turner J (1997) Activity rhythms of the squat lobsters, Pandalus borealis, in Pavlof Bay, Alaska. Fish Bull 83:601–610 Galathea squamifera and G. strigosa (Crustacea: Decapoda: Almany GR (2004) Does increased habitat complexity reduce Anomura) in south-west Ireland. J Mar Biol Assoc U K 44:860 predation and competition in coral reef fish assemblages? Oikos Denno RF, Finke DL, Langellotto GA (2005) Direct and indirect 106:275–284 effects of vegetation structure and habitat complexity on Amri AY, Tajuddin BH, Lee YL, Adzis KA, Yusuf Y (2008) predator–prey and predator–predator interactions. In: Barbosa Scleractinian coral diversity of Kg Tekek, Pulau Tioman marine P, Castellanos I (eds) Ecology of predator–prey interactions. park. In: Phang SM (ed) IOES monograph series: NaturaI Oxford University Press, Oxford, pp 211–239 History of The Pulau Tioman Group of Islands. Institute of Diaz D, Zabala M, Linares C, Hereu B, Abello P (2005) Increased Ocean and Earth Sciences, University of Malaya, Kuala Lumpur, predation of juvenile European spiny lobster (Palinurus elephas) pp 53–68 in a marine protected area. N Z J Mar Freshw Res 39:447–453

123 Coral Reefs (2014) 33:639–650 649

Dorn NJ, Trexler JC, Gaiser EE (2006) Exploring the role of large Holbrook SJ, Brooks AJ, Schmitt RJ (2002b) Variation in structural predators in marsh food webs: evidence for a behaviorally- attributes of patch-forming corals and in patterns of abundance mediated trophic cascade. Hydrobiologia 569:375–386 of associated fishes. Mar Freshw Res 53:1045–1053 Duffy JE, Hay ME (2001) The ecology and evolution of marine Holmes G (2008) Estimating three-dimensional surface areas on coral consumer-prey interactions. In: Bertness MD, Hay ME, Gaines reefs. J Exp Mar Biol Ecol 365:67–73 SD (eds) Marine Community Ecology. Sinauer Associates, Howard RK (1984) The trophic ecology of caridean shrimps in an Sunderland, Massachusetts, USA, pp 131–157 eelgrass community. Aquat Bot 18:155–174 Dulvy NK, Mitchell RE, Watson D, Sweeting CJ, Polunin NV (2002) Jacobsen L, Berg S (1998) Diel variation in habitat use by Scale-dependant control of motile epifaunal community structure planktivores in field enclosure experiments: the effect of along a coral reef fishing gradient. J Exp Mar Biol Ecol 278:1–29 submerged macrophytes and predation. J Fish Biol Dumont CP, Gaymer CF, Thiel M (2011) Predation contributes to 53:1207–1219 invasion resistance of benthic communities against the non-indig- Janssen A, Sabelis MW, Magalha˜es S, Montserrat M, Van der enous tunicate Ciona intestinalis. Biol Invasions 13:2023–2034 Hammen T (2007) Habitat structure affects intraguild predation. Dumont CP, Urriago JD, Abarca A, Gaymer CF, Thiel M (2009) The Ecology 88:2713–2719 native rock shrimp Rhynchocinetes typus as a biological control Kane CN, Brooks AJ, Holbrook SJ, Schmitt RJ (2009) The role of of fouling in suspended scallop cultures. Aquaculture 292:74–79 microhabitat preference and social organization in determining Dunn DC, Halpin PN (2009) Rugosity-based regional modeling of the spatial distribution of a coral reef fish. Environ Biol Fishes hard-bottom habitat. Mar Ecol Prog Ser 377:1–11 84:1–10 Edwards A, Emberton H (1980) Crustacea associated with the Kenyon RA, Loneragan NR, Hughes JM (1995) Habitat type and light scleractinian coral, Stylophora pistillata (Esper), in the Sudanese affect sheltering behaviour of juvenile tiger prawns (Penaeus Red Sea. J Exp Mar Biol Ecol 42:225–240 esculentus Haswell) and success rates of their fish predators. Eggleston DB, Lipcius RN, Miller DL, Coba-Cetina L (1990) Shelter J Exp Mar Biol Ecol 192:87–105 scaling regulates survival of juvenile Caribbean spiny lobster Kneib RT, Scheele CEH (2000) Does tethering of mobile prey Panulirus argus. Mar Ecol Prog Ser 62:79–88 measure relative predation potential? An empirical test using Finke D, Denno R (2006) Spatial refuge from intraguild predation: mummichogs and grass shrimp. Mar Ecol Prog Ser 198:181–190 implications for prey suppression and trophic cascades. Oeco- Knowlton N (1980) Sexual selection and dimorphism in two demes of logia 149:265–275 a symbiotic, pair-bonding snapping shrimp. Evolution Flynn AJ, Ritz DA (1999) Effect of habitat complexity and predatory 34:161–173 style on the capture success of fish feeding on aggregated prey. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions J Mar Biol Ass UK 79:487–494 (CPCe): a Visual Basic program for the determination of coral Freestone AL, Osman RW, Ruiz GM, Torchin ME (2011) Stronger and substrate coverage using random point count methodology. predation in the tropics shapes species richness patterns in Comput Geosci 32:1259–1269 marine communities. Ecology 92:983–993 Kulbicki M, Bozec Y-M, Labrosse P, Letourneur Y, Mou-Tham G, Friedlander A, Parrish J (1998) Habitat characteristics affecting fish Wantiez L (2005) Diet composition of carnivorous fishes from assemblages on a Hawaiian coral reef. J Exp Mar Biol Ecol coral reef lagoons of New Caledonia. Aquat Living Resour 224:1–30 18:231–250 Gotceitas V, Colgan P (1989) Predator foraging success and habitat Lammers JH, Warburton K, Cribb BW (2009) Anti-predator strate- complexity: quantitative test of the threshold hypothesis. Oec- gies in relation to diurnal refuge usage and exploration in the ologia 80:158–166 Australian freshwater prawn, Macrobrachium australiense. Gratwicke B, Speight MR (2005) The relationship between fish Journal of Crustacean Biology 29:175–182 species richness, abundance and habitat complexity in a range of Lecchini D, Planes S, Galzin R (2007) The influence of habitat shallow tropical marine habitats. J Fish Biol 66:650–667 characteristics and conspecifics on attraction and survival of Harborne A, Fenner D, Barnes A, Beger M, Harding S, Roxburgh T coral reef fish juveniles. J Exp Mar Biol Ecol 341:85–90 (2000) Status report on the coral reefs of the east coast of Peninsula Lieske E, Myers R (2002) Coral reef fishes - Indo-Pacific and Malaysia. Coral Cay Conservation Ltd. in conjunction with Marine Caribbean. Princeton University Press, Princeton, New Jersey Parks Section Department of Fisheries Malaysia, London Lima SL (1998) Nonlethal effects in the ecology of predator-prey Haywood MDE, Manson FJ, Loneragan NR, Toscas PJ (2003) interactions. What are the ecological effects of anti-predator Investigation of artifacts from chronographic tethering experi- decision-making? BioScience 48:25–34 ments - interactions between tethers and predators. J Exp Mar Linehan JE, Gregory RS, Schneider DC (2001) Predation risk of age- Biol Ecol 290:271–292 0 cod (Gadus) relative to depth and substrate in coastal waters. Heck KL, Wilson KA (1987) Predation rates on Decapod crustaceans J Exp Mar Biol Ecol 263:25–44 in latitudinally separated seagrass communities - A study of Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP spatial and temporal variation using tethering techniques. J Exp (2002) Resource selection by : statistical design and Mar Biol Ecol 107:87–100 analysis for field studies. Kluwer Press, New York, USA Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting Meager JJ, Williamson I, Loneragan NR, Vance DJ (2005) Habitat ecological consequences of marine top predator declines. Trends selection of juvenile banana prawns, Penaeus merguiensis de Ecol Evol 23:202–210 Man: testing the roles of habitat structure, predators, light phase Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) and prawn size. J Exp Mar Biol Ecol 324:89–98 Towards a predictive framework for predator risk effects: the Medina M, Araya M, Vega C (2004) Alimentacio´n y relaciones interaction of landscape features and prey escape tactics. J Anim tro´ficas de peces costeros de la zona norte de Chile. Invest Mar Ecol 78:556–562 Valparaı´so 32:33–47 Holbrook SJ, Schmitt RJ (2002) Competition for shelter space causes Munday PL (2004) Habitat loss, resource specialization, and extinc- density-dependent predation mortality in damselfishes. Ecology tion on coral reefs. Global Change Biol 10:1642–1647 83:2855–2868 Nagelkerken I, Dorenbosch M, Verberk W, de la Moriniere EC, van Holbrook SJ, Brooks AJ, Schmitt RJ (2002a) Predictability of fish der Velde G (2000) Day-night shifts of fishes between shallow- assemblages on coral patch reefs. Mar Freshw Res 53:181–188 water biotopes of a Caribbean bay, with emphasis on the

123 650 Coral Reefs (2014) 33:639–650

nocturnal feeding of Haemulidae and Lutjanidae. Mar Ecol Prog Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the Ser 194:55–64 primacy of trait-mediated indirect interactions. Ecol Lett Nelson WG (1979) Experimental studies of selective predation on 7:153–163 amphipods: consequences for amphipod distribution and abun- Sih A (1997) To hide or not to hide? Refuge use in a fluctuating dance. J Exp Mar Biol Ecol 38:225–245 environment. Trends Ecol Evol 12:375–376 Noonan SH, Jones GP, Pratchett MS (2012) Coral size, health and Steffan SA, Snyder WE (2010) Cascading diversity effects transmitted structural complexity: effects on the ecology of a coral reef exclusively by behavioral interactions. Ecology 91:2242–2252 damselfish. Mar Ecol Prog Ser 456:127–137 Stella JS, Jones GP, Pratchett M (2010) Variation in the structure of Ochwada-Doyle F, Loneragan NR, Gray CA, Suthers IM, Taylor MD epifaunal invertebrate assemblages among coral hosts. Coral (2009) Complexity affects habitat preference and predation Reefs 29:957–973 mortality in postlarval Penaeus plebejus: implications for stock Stella JS, Munday PL, Jones GP (2011b) Effects of coral bleaching on enhancement. Mar Ecol Prog Ser 380:161–171 the obligate coral-dwelling crab Trapezia cymodoce. Coral Reefs Okuno J (1993) New record of a hinge-beak shrimp, Rhynchocinetes 30:719–727 hendersoni from eastern coast of Izu Peninsula, Japan. IOP Stella JS, Pratchett MS, Hutchings PA, Jones GP (2011a) Coral- Diving News 4:4–5 associated invertebrates: diversity, ecological importance and Okuno J (1997) Crustacea Decapoda : Review on the genus vulnerability to disturbance. In: Gibson R, Atkinson R, Gordon J, Cinetorhynchus Holthuis, 1995 from the Indo-West Pacific Smith I, Hughes D (eds) Oceanogr Mar Biol Ann Rev pp 43–104 ( : Rhynchocinetidae). In: Richer de Forges B (ed) Les Tait KJ, Hovel KA (2012) Do predation risk and food availability fonds meubles des lagons de Nouvelle-Cale´donie (Se´dimentol- modify prey and mesopredator microhabitat selection in eelgrass ogie, Benthos). Orstom, E´ tudes & The`ses, Paris, pp 31–58 (Zostera marina) habitat? J Exp Mar Biol Ecol 426:60–67 Ory NC, Dudgeon D, Thiel M (2013) Host-use patterns and factors Vance D (1992) Activity patterns of juvenile penaeid prawns in influencing the choice between anemone and urchin hosts by a response to artificial tidal and day-night cycles: a comparison of caridean shrimp. J Exp Mar Biol Ecol 449:85–92 three species. Mar Ecol Prog Ser 87:215–226 Ory NC, Dudgeon D, Dumont CP, Miranda L, Thiel M (2012) Effects Va´squez J (1993) Abundance, distributional patterns and diets of of predation and habitat structure on the abundance and main herbivorous and carnivorous species associated to Lessonia population structure of the rock shrimp Rhynchocinetes typus trabeculata kelp beds in Northern Chile. Serie Ocasional (Caridea) on temperate rocky reefs. Mar Biol 159:2075–2089 Universidad Catolica del Norte 2:213–229 Patton WK (1994) Distribution and ecology of animals associated Veron J (2000) Corals of the world. AIMS, Townsville with branching corals (Acropora spp.) from the Great Barrier Vytopil E, Willis B (2001) Epifaunal community structure in Reef, Australia. Bull Mar Sci 55:193–211 Acropora spp. (Scleractinia) on the Great Barrier Reef: impli- Peacor SD, Werner EE (2001) The contribution of trait-mediated cations of coral morphology and habitat complexity. Coral Reefs indirect effects to the net effects of a predator. Proc Natl Acad 20:281–288 Sci USA 98:3904–3908 Wahle RA (1992) Substratum constraints on body size and the Peterson CH, Black R (1994) An experimentalist’s challenge - when behavioral scope of shelter use in the American lobster. J Exp artifacts of intervention interact with treatments. Mar Ecol Prog Mar Biol Ecol 159:59–75 Ser 111:289–297 Wahle RA, Steneck RS (1992) Habitat restrictions in early benthic Peterson BJ, Thompson KR, Cowan JH, Heck KL (2001) Comparison of life: experiments on habitat selection and in situ predation with predation pressure in temperate and subtropical seagrass habitats the American lobster. J Exp Mar Biol Ecol 157:91–114 based on chronographic tethering. Mar Ecol Prog Ser 224:77–85 Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An Preston NP, Doherty PJ (1990) Cross-shelf patterns in the community experimental test of the effects of predation risk on habitat use structure of coral-dwelling Crustacea in the central region of the in fish. Ecology 64:1540–1548 Great Barrier Reef. I. Agile shrimps. Mar Ecol Prog Ser 66:47–61 Wilson SK, Graham NAJ, Polunin NVC (2007) Appraisal of visual Preston NP, Doherty PJ (1994) Cross-shelf patterns in the community assessments of habitat complexity and benthic composition on structure of coral-dwelling Crustacea in the central region of the coral reefs. Mar Biol 151:1069–1076 Great Barrier Reef. II. Cryptofauna. Mar Ecol Prog Ser 104:27 Wilson SK, Fisher R, Pratchett MS (2013) Differential use of shelter Primavera JH (1997) Fish predation on mangrove-associated penae- holes by sympatric species of blennies (Blennidae). Mar Biol ids: the role of structures and substrate. J Exp Mar Biol Ecol 160:2405–2411 215:205–216 Wilson SK, Graham NAJ, Pratchett MS, Jones GP, Polunin NVC Quinn GP (2002) Experimental design and data analysis for (2006) Multiple disturbances and the global degradation of coral biologists. Cambridge University Press, Cambridge reefs: are reef fishes at risk or resilient? Global Change Biol Ray WJ, Corkum LD (2001) Habitat and site affinity of the round 12:2220–2234 goby. J Gt Lakes Res 27:329–334 Worm B, Myers RA (2003) Meta-analysis of cod-shrimp interactions Reebs SG (2002) Plasticity of diel and circadian activity rhythms in reveals top-down control in oceanic food webs. Ecology fishes. Rev Fish Biol Fish 12:349–371 84:162–173 Schmitz OJ, Beckerman AP, Obrien KM (1997) Behaviorally Yates D, Moore D, McCabe G (1999) The Practice of Statistics. mediated trophic cascades: effects of predation risk on food Freeman, W.H., New York web interactions. Ecology 78:1388–1399

123