Dynamic camouflage by Nassau groupers Epinephelus striatus on a Caribbean coral reef.

Journal of Fish Biology (2014) 85, 1634–1649 doi:10.1111/jfb.12519, available online at wileyonlinelibrary.com

Dynamic camouflage by Nassau groupers Epinephelus striatus on a Caribbean coral reef A. C. Watson*¶, L. A. Siemann†¶ and R. T. Hanlon†‡§ *University of Rhode Island, Graduate School of Oceanography, Narragansett, RI 02882, U.S.A., †Marine Biological Laboratory, Program in Sensory Physiology and Behavior, 7 MBL Street, Woods Hole, MA 02543, U.S.A. and ‡Brown University, Department of Ecology and Evolutionary Biology, Providence, RI 02912, U.S.A. (Received 26 March 2014, Accepted 30 July 2014) This field study describes the camouflage pattern repertoire, associated behaviours and speed of pattern change of Nassau groupers Epinephelus striatus at Little Cayman Island, British West Indies. Three basic camouflaged body patterns were observed under natural conditions and characterized quantitatively. The mean speed of pattern change across the entire body was 4⋅44 s (range = 0⋅97–9⋅87 s); the fastest pattern change as well as contrast change within a fixed pattern occurred within 1 s. Aside from apparent defensive camouflage, E. striatus used camouflage offensively to approach crustacean or fish prey, and three successful predation events were recorded. Although animal camouflage is a widespread tactic, dynamic camouflage is relatively uncommon and has been studied rarely in marine teleosts under natural conditions. The rapid changes observed in E. striatus suggest direct neural control of some skin colouration elements, and comparative studies of functional morphology and behaviour of colour change in other coral-reef teleosts are likely to reveal new mechanisms and adaptations of dynamic colouration. © 2014 The Fisheries Society of the British Isles

Key words: adaptive colouration; chromatophore; colour pattern; crypsis; defence; disruptive colouration.

INTRODUCTION Camouflage is used throughout the animal kingdom as a defence mechanism against visual predation or as offence to enhance prey capture, and various mechanisms and adaptations have evolved across phyla (Cott, 1940; Edmunds, 1974; Ruxton et al., 2004; Stevens & Merilaita, 2011). Most animals have a fixed or slowly changing camouflage pattern in which they must (1) move to the right habitat at the correct time and with ideal lighting conditions and (2) take up the appropriate posture, orientation and behaviour to implement effective camouflage. Rapid body pattern change is relatively uncommon yet provides the added benefit of increased behavioural versatility for camouflage and communication. Certain molluscs, crustaceans, insects, reptiles and fishes are capable of rapid colour and pattern change (Cott, 1940), which is thought to be controlled mainly by visual input and implemented physiologically via hormonal control §Author to whom correspondence should be addressed. Tel.: +1 508 274 3633; email: [email protected] ¶Shared first authorship.

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(which is relatively slow) or via neural control (which is fast) (Cott, 1940; Parker, 1948; Hanlon & Messenger, 1988; Fujii, 1993). In cephalopods, which possess diverse changeable body patterns (Hanlon & Messenger, 1996), camouflage is categorized into three basic pattern templates: uniform, mottle and disruptive. There are variations in each pattern type (Hanlon et al., 2009), but it has been postulated that these three main categories occur across phyla and ecological habitat (Hanlon, 2007). Uniform body patterns are characterized by little or no contrast, and colour that is similar throughout the body pattern. Mottle body patterns are characterized by small to moderate-scale (relative to the size of the animal) light and dark patches of moderate contrast distributed across the body surface; patch size often correlates to that of background features (Chiao et al., 2010). Both uniform and mottle body patterns provide some degree of general resemblance (or background matching) to the surrounding substratum, implying that the cryptic animal matches certain elements of background colour, contrast, texture, intensity and brightness (Endler, 1984; Cuthill et al., 2005; Hanlon, 2007). Disruptive body patterns are characterized by large-scale light and dark components of multiple shapes, orientations, scales and high-contrast colours (Hanlon et al., 2009). Disruptive body patterns can be conspicuous when seen out of context, but provide both background matching and disruption on certain backgrounds (Cott, 1940; Hanlon & Messenger, 1988; Cuthill et al., 2005; Stevens & Cuthill, 2006; Fraser et al., 2007). Background matching (to impair detection by prey and predators) and disruptive colouration (to impair recognition as well as detection) have been discussed widely in recent scientific literature (Merilaita, 1998; Cuthill et al., 2005, 2006; Merilaita & Lind, 2005; Schaefer & Stobbe, 2006; Stevens & Cuthill, 2006; Stevens et al., 2006a, b; Fraser et al., 2007; Hanlon et al., 2009; Stevens & Merilaita, 2011). Body patterns of fishes presented through different body positions (e.g. fins out and tail fanned) across diverse taxa and ecological habitats have characteristics of disruptive colouration. Many species have dark ocular bands contrasted by adjacent light borders, such as freshwater sculpins (Cottidae) that develop saddles or vertical bars when moving from a pelagic to benthic phase (Armbruster & Page, 1996). Sculpins also have the ability to change the size and contrast of their dark saddles to enhance camouflage (Armbruster & Page, 1996). Three saltwater flatfishes, English sole Parophrys vetulus Girard 1854, northern rock sole Lepidopsetta polyxystra Orr & Matarese 2000 and Pacific halibut Hippoglossus stenolepis Schmidt 1904, were most active when placed on mismatched substrata, probably in search of better-matching sediment (Ryer et al., 2008). Each flatfish was capable of changing pattern within a day (Ryer et al., 2008), whereas the eyed flounder Bothus ocellatus (Agassiz 1831) is capable of pattern matching, using both uniform and mottle patterns, in 2–8 s by adjusting skin markings in relation to substratum grain size (Ramachandran et al., 1996). Similarly, juvenile plaice Pleuronectes platessa L. 1758 adjust the expression of their spots and blotches in response to background patterns, showing patterns of little contrast on plain backgrounds and patterns with strong spots and blotches on high-contrast gravel (Kelman et al., 2006). Surgeonfishes (Acanthuridae) undergo pattern changes in relation to the environment; for example, they show a pure pale and blue-grey in the water column and a dark black colour on benthic habitats (Longley, 1920). Kelp bass Paralabrax clathratus (Girard 1854) were also observed changing body patterns in relation to habitat and behavioural activity (Erisman & Allen, 2005).

© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1634–1649

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A . C . WAT S O N E T A L.

Pattern changes of serranids during social behaviours and spawning have been documented to varying degrees (Smith, 1961; Thresher, 1984; Gilmore & Jones, 1992; Erisman & Allen, 2005). A recent five-year study on Nassau groupers Epinephelus striatus (Bloch 1792) on annual spawning aggregations reported three colour phases used apparently for intraspecific signalling: bicolour, dark and white belly (Archer et al., 2012). A fourth pattern, the barred pattern, was observed on spawning grounds but is more commonly seen during non-spawning periods. For serranids, only a few observers have identified pattern change in relation to habitat (Townsend, 1909, 1929; Longley, 1917; Nemtzov et al., 1993; Erisman & Allen, 2005). Townsend (1909, 1929) first commented on the ability of E. striatus to change colour in ‘a few moments’ within the tanks of the New York Aquarium. He observed a correlation of body patterns and background where roughly six patterns were described and attributed as an ‘emotional response’. On light backgrounds, Townsend (1909) observed bold banding and black mottled patterns on light backgrounds, which easily changed if the individuals were feeding or frightened by aquarium staff or the addition of new fish. Longley (1917) also published observations in which E. striatus showed different body patterns in relation to habitat and during feeding. Other observations have confirmed that E. striatus is capable of extreme colour change from uniform to ‘banded’ or ‘barred’ patterns within seconds (rather than minutes), and it has been discussed that these pattern changes may depend on the fish’s ‘mood’, surroundings and activity (Bohlke & Chaplin, 1968; Jory & Iversen, 1989; Bullock & Smith, 1991; Heemstra & Randall, 1993; Humann & DeLoach, 1993; Nemtzov et al., 1993; Archer et al., 2012). Most groupers are solitary, benthic-orientated species found on hard-bottom substrata such as boulders or coral reefs in tropical and subtropical waters (Heemstra & Randall, 1993). They are characterized as unspecialized and opportunistic feeders, most active at dawn and dusk (Randall, 1965, 1967; Thompson & Munro, 1978; Heemstra & Randall, 1993). Groupers are also ambush hunters, rushing out from hiding places to engulf passing prey (Hobson, 1968, 1974; Heemstra & Randall, 1993). Individuals hide among corals or rocks until prey approach and then engulf them by either snapping their jaws or sucking both water and prey in like a vacuum (Heemstra & Randall, 1993). Gut content analysis has shown that E. striatus consumes a wide assortment of prey, ranging from molluscs to crustaceans to many fish species (Randall, 1965, 1967; Thompson & Munro, 1978; Jory & Iversen, 1989; Heemstra & Randall, 1993; Sadovy & Eklund, 1999). Epinephelus striatus are generally considered as top predators in coral-reef communities (Jory & Iversen, 1989; Sadovy & Eklund, 1999; NMFS, 2006). The few known predators of adult and juvenile E. striatus are sharks and other large fishes including groupers (Thompson & Munro, 1978). Body patterns may differ between juveniles and adults, but little has been documented on the juvenile body patterns of this species, and they appear to resemble adults (Sadovy & Eklund, 1999). In this study, body patterns of E. striatus were investigated in their natural habitat of coral reefs at Little Cayman Island, British West Indies. Observations suggest that, when not engaged in the annual spawning event, they commonly show three body patterns: barred [Fig. 1(a)], mottle [Fig. 1(b)] and white belly [Fig. 1(c)]. The three body patterns were characterized quantitatively and the rapidity of pattern change for adaptive colouration in E. striatus species was determined.



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Fig. 1. Representative images of Epinephelus striatus patterns (cut-outs from underwater photographs). Background is the mean intensity of the fish. (a) Barred, (b) mottle and (c) white belly body patterns.

MATERIALS AND METHODS Epinephelus striatus were observed from 30 April to 5 May 2007, and from 15 to 23 April 2009, on Bloody Bay coral reef (depths of 3–20 m) at Little Cayman Island (19∘ 41′ N; 80∘ 03′ W). Fish were photographed using a Canon EOS-1DS Mark II (17 mp; www.usa.canon.com) and videotaped using a Panasonic HVX200 (HDTV format; www.panasonic.com) and a Sony VX1000 (mini-digital video format; www.sony.com). All images and video were acquired solely with natural light; i.e. no flash or video lights were used. In 2007, five individuals of E. striatus were observed during 13 dives (13 diver hours). In 2009, eight individuals of E. striatus were observed during 41 dives (61⋅5 diver hours). Overall, 820 photographs and 482 min of video were acquired. Total length (LT ) and standard length (LS ) of E. striatus were measured using dual laser pointers. Fish ranged in size from 37 to 85 cm LT and 25 to 66 cm LS , and based on size standards, all were adults (>30 cm LT ) and most were sexually mature (>40 cm LS ; Sadovy & Eklund, 1999). Individual fish were followed and filmed from a distance of 3–8 m (focal animal sampling; Martin & Bateson, 2007); the fish readily habituated to the divers’ presence. To gain an impression of how the patterns might look to predators in different parts of the water column, camouflage patterns were imaged from three angles: 90∘ or directly overhead for the view of a large pelagic predator [Fig. 2 (d-barred), (e-white belly)], 45∘ also for the view of a large pelagic predator and 0∘ or horizontal to the fish for the view of prey or benthic predators [Fig. 2 (a-barred), (b-mottle), (c-white belly)]. Close-up images of the skin were also taken (Fig. 3). Body patterns were characterized and differentiated quantitatively using a MATLAB programme developed for cephalopods (Barbosa et al., 2008). A variation of this programme has been used to characterize camouflaged bird eggs (Spottiswoode & Stevens, 2010; Stoddard & Stevens, 2010). The programme used in this study was modified to distinguish the patterns observed on E. striatus. The digital images were sized so that all the fish were of the same length, subjected to a fast Fourier transform and filtered into four two-octave-wide spatial frequency or granularity bands. This provides a granularity spectrum that summarizes the scale and contrast of light and dark components in the skin, and the shape of the resulting curve for each fish pattern corresponds to its body pattern classification (Fig. 4). Because red light attenuates


Fig. 2. (a) Barred, (b) mottle and (c) white belly patterns. Images taken horizontally to fish, representing the view from a benthic predator or prey’s perspective. (d) Dorsal view of a barred pattern and (e) dorsal view with mottling in the white bars. Images taken from a 90∘ top–down angle, directly over the fish, for the view of a pelagic predator such as a shark or larger grouper. (f) Epinephelus striatus when viewed from the front, in the perspective of benthic prey such as crabs. (g) Epinephelus striatus showing mottle pattern while settled next to a gorgonian (soft-coral sea fan). (h) Well-camouflaged E. striatus showing a barred pattern. (i) Well-camouflaged E. striatus showing a white belly pattern. All photographs were taken with available light in the natural habitat.

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Fig. 3. Close-up photographs of Epinephelus striatus skin showing light and dark vertical bars in different grades of expression. (a) Barred, (b) mottle and (c) white belly patterns. Note how white bars can be darkened and dark bars can be lightened by recruitment of pigmentation within each scale in the skin. Five grades of lightness were observed in photographs: white, grey, light brown, dark brown and black.

rapidly underwater, analysis was limited to the green and blue channels of the images. To give adequate numbers for statistical analysis, images taken from a distance with reduced pattern contrast and clarity were included. To compensate for this effect, the analysis focused only on the power spectrum of the granularity curves. This removes information about the overall contrast of the pattern and focuses on the relative contributions of each component scale to the overall pattern. This allowed comparison of patterns in images of varying photographic quality taken at different distances, and the granularity power spectrum is not as sensitive to image variables such as illumination and exposure of the original digital image. The lateral and dorsal surfaces of the fish were analysed. To confirm that the same side of the same fish was not used more than once to characterize a single pattern, the individually distinct bar patterns were examined carefully. For the lateral surface analysis, seven white belly, 11 mottle and seven barred pattern images were analysed (Fig. 4). This included both sides of four fish, with three fish used for analysis of more than one pattern type. The number of images available for the dorsal surface analysis was limited, and thus the dorsal surface for three barred, four mottle and three white belly pattern images were analysed. The dorsal surface images were classified by looking at side-view images taken immediately preceding or following the image in question. To evaluate rapidity of pattern change, fish were followed more closely and video was recorded close-up with a time resolution of 1/30th of a second. These video clips were analysed carefully frame-by-frame, and the start and end points of a change were selected as the last frame before a change started to occur and the first frame after the new pattern remained stable for at least 1 s. A total of 26 examples of pattern changes occurred with the lateral surface of a fish visible throughout the entire clip (Table I). Granularity analysis of images taken at five-frame intervals was used to confirm this visual assessment of pattern types for two sequences.

RESULTS B O DY PAT T E R N T Y P E S A N D E . S T R I A T U S B E H AV I O U R

Epinephelus striatus showed mottle and barred body patterns (or mottle and barred hybrid patterns) when settled on or cruising near the seafloor [Fig. 2(a), (b)] and white belly patterns when settled on light substrata or swimming in the water column [Fig. 2(c)]. Epinephelus striatus often deployed barred and mottle patterns on dark heterogeneous substrata near soft corals, especially the purple sea fan Gorgonia ventalina [Fig. 2(g), (h)], and moved slightly with wave surge at the same rhythm as


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0·7

(a)

0·6

Proportion of contrast at each spatial scale

0·5 0·4 0·3 0·2 0·1 0 0·9

(b)

0·8 0·7 0·6 0·5 0·4 0·3 0·2 0·1 0 1 2 3 4 Granularity bands corresponding to pattern components of different scales

Fig. 4. Quantification of Epinephelus striatus body patterns: the curve shape distinguishes the camouflage pattern. The granularity power spectrum shows the relative contributions of each spatial scale to the overall patterns. Bands 1–4 were designed to correspond with components of different scales in E. striatus body patterns. Examples of filtered images for the lateral surface are shown along the bottom of the figure, with band 1 corresponding to areas larger than the bars, band 2 corresponding to areas the size of the bars, band 3 corresponding to areas the size of the white splotches and spots in the mottle pattern and band 4 corresponding to areas smaller than the white spots. (a) Average granularity curves for each of the three pattern types viewed laterally [ , white belly (n = 7); , mottle pattern (n = 11); , barred pattern (n = 7)]. (b) Same as (a) viewed dorsally [ , white belly (n = 3); , mottle pattern (n = 4); , barred pattern (n = 3)]. Values are mean ± s.d.

the soft corals. In all cases, E. striatus showed mottle patterns when they settled in one place for >10 s and were camouflaged to the human eye. Head and tail fins of E. striatus also appeared well-camouflaged horizontally and from a 45∘ angle. Three predation events were observed at evening crepuscular periods where fish appeared camouflaged before ambushing crabs hidden amidst coral heads and rocks. In an unsuccessful attempt, an E. striatus used a lie and wait tactic and lunged upwards at a swimming bar jack Carangoides ruber (Bloch 1793). Fish usually moved about the reef, most likely looking for food, in a saltatory search pattern or stop-go continuum (O’Brien et al., 1990). This foraging behaviour presumably gives the fish time to pause



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Table I. Speed of Epinephelus striatus camouflage pattern changes observed in s, described as mean ± s.d. and range of pattern changes. Speed measured to two decimal places because video frame rate was 30 frames s−1 Pattern change

Mean speed of pattern change (s)

Range of pattern change speeds (s)

B to M (n = 2) B to W (n = 10) M to B (n = 1) M to W (n = 6) W to B (n = 4) W to M (n = 3)

3⋅62 ± 2⋅05 3⋅07 ± 1⋅47 3⋅80 6⋅72 ± 3⋅06 4⋅58 ± 0⋅36 4⋅97 ± 0⋅90

2⋅17–5⋅07 0⋅96–6⋅67 3⋅80 3⋅57–9⋅87 4⋅20–5⋅03 4⋅37–6⋅00

B, barred; M, mottled; W, white belly.

and search for prey while constantly repositioning to scan new territory while camouflaged. Other observed behaviours included utilizing cleaning stations with barred or mottle body patterns and species signalling, noticeable by a quick extension of the dorsal-fin. S TAT I S T I C A L C H A R A C T E R I Z AT I O N O F T H E B O DY PAT T E R N S

The barred body pattern, recognized as the most common pattern in this species (Bohlke & Chaplin, 1968; Humann & DeLoach, 1993; Archer et al., 2012), was characterized qualitatively by large-scale, high-contrast vertical bars or patches across the entire body (dorsal and ventral surfaces). Mottle patterns were characterized by light brown vertical bars interspersed with small white splotches of moderate to high contrast; the vertical light bars were interspersed with small dark splotches or much lighter splotches. The gross morphology of the skin that allows the regulation of splotches can be seen in Fig. 3. White belly patterns were characterized by bars on the dorsal surface and little to no contrast of light and dark components on the ventral surface. The granularity band power spectrum was calculated for the fish’s lateral surface to differentiate all three patterns quantitatively. The average curves for the granularity power spectrum for the lateral aspect of the three main grouper patterns are shown in Fig. 4(a). The curves for barred patterns peaked at granularity band 2, which represents the wider light and dark vertical bars in the body pattern, then decreased steeply through granularity bands 3 and 4. The curves for mottle patterns peaked at granularity band 3, corresponding to the moderate-scale light and dark splotches in the body pattern. The curves for white belly patterns not only peaked in band 2 because of the still-present vertical bars, but also had a higher proportion of energy in band 1 corresponding to regions such as the extensive white belly that was larger than the vertical bars. An initial multivariate analysis of variance (MANOVA) showed a significant difference between the three patterns with the first three band energies as covariates (Pillai’s trace = 1⋅46, F 8,40 = 13⋅64, P < 0⋅001). Follow-up analysis using analysis of variance (ANOVA) found significant differences among the three patterns for granularity bands 1, 2 and 3, which express the largest-scale components of the body patterns (band 1: F 2,22 = 9⋅08, P < 0⋅01; band 2: F 2,22 = 27⋅10, P < 0⋅01; band 3: F 2,22 = 47⋅14, P < 0⋅01). The observed body patterns could not be separated exclusively into three main pattern types. A mottle and barred hybrid pattern was observed, as was a mottle or barred


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pattern with pale but not white belly. These hybrid patterns were frequently observed during pattern changes. Functionally, it could be considered that there are five rather than three cryptic body patterns that are shown in a live coral habitat such as Little Cayman. The patterns on the dorsal surface of E. striatus (i.e. those viewed by a predator directly above in the water column) were also examined using the same analysis. Thus, images taken from directly above the fish were analysed [Fig. 2(d), (e)]. As the dark vertical bars tend to visually dominate the dorsal aspect of all patterns (barred, mottle and white belly patterns as classified from a lateral view), all of the dorsal granularity curves peaked strongly in band 2. The average dorsal granularity curves for the three main lateral view grouper patterns are shown in Fig. 4(b) and are grouped tightly. Because of the limited sample size (n = 10), no statistical tests were performed. Thus, E. striatus could simultaneously appear mottled when viewed laterally, but appear barred when viewed from above. S P E E D O F PAT T E R N C H A N G E A N D C O N T R A S T C H A N G E

The mean ± s.d. speed of overall body pattern change for 26 documented changes was 4⋅44 ± 2⋅24 s and all possible combinations of pattern changes were observed at least once (Table I). There is a limit to body pattern change in E. striatus because the vertical bars on the dorsal surface were always present to some degree in the observations at this location. The ventro-lateral aspect of pattern change most often depended on the behaviour of the fish. For example, when fish changed from benthic immobility to swimming in the water column, the ventral surface or belly would always turn pale (i.e. white belly). When settling back onto benthic substrata, the fish’s ventral surface would darken, and the large-scale, high-contrast bars or moderate-scale mottle patches became visible. Detailed video analysis was conducted on two examples of pattern changes from barred to mottle with images analysed at one third of a second intervals (Fig. 5 shows one example). In this figure, the granularity power spectrum curves shift from peaking in band 2 to peaking in band 3 as the pattern changes from barred to mottle. Increased contrast at the scale highlighted by band 3 occurred when the background in the white bars was darkened while the white splotches became brighter with changes of dark pigmentation within each skin scale. From the close-up digital images, five grades of lightness and darkness of individual scales could be distinguished qualitatively: white, grey, light brown, dark brown and black (Fig. 3).

DISCUSSION Camouflage is used throughout the animal kingdom as a defence mechanism against visual predation or as offence to enhance prey capture (Cott, 1940; Edmunds, 1974; Ruxton et al., 2004; Stevens & Merilaita, 2011). Rapid pattern change, most notably in cephalopods, has proven interesting due to its versatility across varying types of habitats. Serranids are known to change pattern and colour for communication, particularly during spawning events (Erisman & Allen, 2005; Archer et al., 2012). Comments about colour change by groupers for camouflage can be found scattered in the literature (Townsend, 1909, 1929; Longley, 1917; Smith, 1961; Colin, 1992; Heemstra


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Proportion of contrast at each spatial scale


0·6 0·5 0·4 0·3 0·2 0·1 0 1

2

3

4

Granularity bands corresponding to pattern components of different scales

Fig. 5. Granularity curves shifting during a subtle pattern change from barred to mottle in Epinephelus striatus. The entire pattern change took place over 2⋅3 s. Granularity curves were generated for images analysed at one third second intervals. The curve for the initial image ( ) peaks in band 2 (barred), and the curve for the final image ( ) peaks in band 3 (mottle). During the pattern change, the peak shifts from band 2 to 3 ( ), and one sample intermediate image is shown (middle fish image). The growing peak in band 3 corresponds to the appearance of mottles as the white bars darkened around their white splotches, and white splotches became brighter in all bars, thus increasing the contrast and visibility of smaller-scale splotches.

& Randall, 1993; Sadovy & Eklund, 1999), and in fish identification books such as Humann & DeLoach (1993). In this study, some of the principles of adaptive camouflage found in cephalopods were applied (Hanlon, 2007; Hanlon et al., 2009) to the serranid E. striatus. It was explored whether the observed camouflage patterns shown by E. striatus in their natural environments fall into three main categories, similar to those documented in cuttlefish and differentiated by the scale and contrast of the pattern elements (white belly, mottle and barred); secondarily, it was examined whether the rate of pattern change is as fast as what is seen in cephalopods or other fishes. B O DY PAT T E R N T Y P E S A N D E . S T R I A T U S B E H AV I O U R

The natural behaviour of E. striatus was studied during daylight and sunset, and outside of the spawning season, which is from January to March at Little Cayman (Archer et al., 2012). The basic body patterns observed were mottle, barred and white belly. As illustrated in Figs 1 and 2, these three patterns tend to show some hybridization between them, and functionally might be considered as five common camouflage patterns owing


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to the combination of mottle and barred as well as patterns that had mottle or barred with a pale but not white belly. It is noteworthy that uniform light or uniform dark patterns were not observed for crypsis by groupers, as they are for many fishes such as P. platessa or B. ocellatus (Ramachandran et al., 1996; Kelman et al., 2006). Studies on spawning behaviours of E. striatus have documented uniform dark patterns (Smith, 1961; Colin, 1992; Sadovy & Eklund, 1999; Archer et al., 2012), so the species has the physiological capability to show uniform patterns. The dark patch on the caudal peduncle was always present; the present observations suggest that this is a fixed-component of body patterns of unknown function. The variability between the three basic pattern types shown by E. striatus is more limited than that seen in previous studies on cephalopods (Hanlon & Messenger, 1988, 1996; Hanlon, 2007). The disruptive body patterns of a cuttlefish can include up to 11 contrasting components (six dark and five light components); these components are not visible when the mottle or uniform patterns are expressed fully, and cuttlefish patterns show a range of colours that allow them to match a wide array of natural backgrounds (Mäthger et al., 2008). The pattern changes observed in E. striatus at Little Cayman were far more limited and rather subtle compared with cuttlefish, i.e. vertical bars were always present on the dorsal surface, and variable colours were not a major feature of the patterns. The components of their barred patterns were basically of two types: light bars or dark brown bars. The bars on the lateral aspect of the body were mostly broad and vertically oriented, whereas those near the head and on the dorsal-most aspect of the body were of narrower dimensions and of differing orientations [Fig. 2(d)–(f)]. These components fulfil some of the requirements of disruptive colouration (Cott, 1940) by being bold in contrast (which is controlled by the fish) and having different size scales and orientations (which were not varied by the fish and appear fixed in size scale). Some other serranids show similar bars on the dorsal surface [e.g. goliath grouper Epinephelus itajara (Lichtenstein 1822) and tiger grouper Mycteroperca tigris (Valenciennes 1833)], whereas others have more variable dorsal surface patterning, e.g. red grouper Epinephelus morio (Valenciennes 1828), yellowfin grouper Mycteroperca venenosa (L. 1758), black grouper Mycteroperca bonaci (Poey 1860) and red hind Epinephelus guttatus (L. 1758) (Humann & DeLoach, 1993; see also www.fishbase.org). Barred body patterns in E. striatus marked by high-contrast, large-scale vertical bars (dorsal and ventral surface) may function as disruptive colouration by obscuring the fish’s longitudinal body orientation and hindering recognition by hiding edges and eyes (Fig. 2) (Neudecker, 1989) and providing false outlines (Cott, 1940; Hanlon & Messenger, 1988; Cuthill et al., 2005; Stevens & Cuthill, 2006), yet this remains speculative. The presumed disruptive colouration effect of bars on the dorsal surface might provide crypsis for E. striatus when viewed from above (Fig. 2), similar to the saddles or vertical bars of freshwater sculpins that enhance camouflage (Armbruster & Page, 1996). In the field, it was most difficult to find E. striatus from the above perspective, especially when fish were located amidst branching soft corals; this is not unusual, because disruptive colouration in other organisms not only impedes recognition, but also often provides some degree of background matching to retard detection (Hanlon & Messenger, 1988; Merilaita, 1998; Stevens & Merilaita, 2009). Granularity analysis of the dorsal surface showed that barred, mottle and white belly patterns are indistinguishable when viewed from directly above [Fig. 4(b)] because the dorsal-most part of the body appears to be the least changeable.



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The lateral surface of E. striatus was more dynamic in appearance, allowing fish to show different body patterns and camouflage on varying substrata against prey viewing horizontally from the perspectives of 0 or 45∘ angles. Mottle patterns in E. striatus appeared different from those observed in cephalopods (Hanlon et al., 2009; Chiao et al., 2010) because the broad dark vertical bars were always expressed to some degree, yet the fish could express small-scale light splotches in the dark bars as well as small-scale dark and light splotches in the light bars [Figs 1(b), (c), 2(b), (e), (g) and 3(b), (c)]. Overall, these body patterns fulfil the quantitative characteristics of mottle patterns (Chiao et al., 2010) when viewed from the side because small to moderate-scale contrasting patches characterize the pattern (Figs 4 and 5). Because the mottle pattern was the one shown by fish that settled for >10 s at this Little Cayman coral-reef habitat, it may be particularly important for camouflage. The white belly pattern was observed when fish were swimming above the reef, over light substrata or in the water column (Fig. 2). White belly patterns had little to no contrast on the ventral surface, whereas the dorsal surface had vertical bars. White belly patterns have been observed in spawning aggregations (Archer et al., 2012) and attributed to females containing ova in their abdomens (Colin, 1992). The white belly pattern, however, was found to be a common pattern shown by all observed fish during daily activities, well outside the spawning season or spawning sites at Little Cayman. When in the water column, E. striatus always used this pattern, which probably aided countershading or self-shadow concealment when viewed from the side and background matching when viewed from below (Cott, 1940; Edmunds, 1974; Stevens & Merilaita, 2009). Self-shadow concealment occurs when shadows created by light hitting the dorsal surface of an animal are eliminated by lighter colouration on the ventral surface (Cott, 1940; Ruxton et al., 2004; Stevens & Merilaita, 2009). This contrast change of the ventral surface has also been noted in surgeonfishes, freshwater sculpins and P. clathratus (Longley, 1920; Armbruster & Page, 1996; Erisman & Allen, 2005). On lighter substrata such as sand, E. striatus showed a white belly pattern, enabling the ventral surface to generally resemble substrata [Fig. 2(i)]. Quantitative differentiation of three body patterns was best illustrated by analysing the lateral body surface [Fig. 4(a)]. Granularity power spectrum curves for the barred pattern peaked in band 2. This peak is consistent with the spatial scale of wider vertical dark and light bars of E. striatus. Mottle granularity curves for the lateral surface peaked in band 3, consistent with the moderately sized spatial scale of the white splotches and spots that characterize this pattern. Both of these pattern characteristics are similar to the disruptive and mottled camouflaged body patterns seen in cuttlefish (Hanlon & Messenger, 1988; Hanlon et al., 2009) and bird eggs (Stoddard & Stevens, 2010; Stoddard et al., 2011). White belly patterns were differentiated from all other patterns with proportionally higher energy in the large-scale band 1, corresponding to the spatial scale of the entire white belly itself (Fig. 4). As summarized by Kelman et al. (2006), P. platessa have two basic patterns: fine spots and coarser blotches that correspond to two variations of mottle in the present E. striatus study (i.e. a small-scale mottle and a larger-scale mottle); the detailed study of skin patterns by Healey (1999) supports this finding. Bothus ocellatus has three basic patterns but were not described explicitly (Ramachandran et al., 1996). The flounders Paralichthys lethostigma Jordan & Gilbert 1884 and Pseudopleuronectes americanus (Walbaum 1792) have (at least) one and two patterns, respectively (Saidel, 1988).


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Epinephelus striatus in the coral habitat of Little Cayman were often observed next to soft corals and gorgonian fans [Fig. 2(g)–(i)]. As a benthic opportunistic feeder, it is not surprising that E. striatus is located most often amidst soft corals where their prey are located and that they would position themselves against some of the most common structures during their daily foraging activities. The mottle and barred patterns were expressed with these backgrounds and produced effective crypsis, at least to human observers. Three predation events occurred in which separate individual fish swayed with gorgonian fans in the surge, looking underneath a coral head or rock each time before striking crabs. A cryptic E. striatus next to a large gorgonian fan was also observed attempting to prey upon swimming bar jacks Caranx ruber (Bloch 1793): it struck upwards at the passing fish but failed, thereafter settling on the bottom next to a soft coral and then continuing on a benthic saltatory search pattern (O’Brien et al., 1990). S P E E D O F PAT T E R N C H A N G E A N D C O N T R A S T C H A N G E

Previous observations of various grouper species have suggested pattern change ranging from 1 to 3 s in some species, to minutes in others (Townsend, 1909; Longley, 1917; Smith, 1961; Sadovy & Eklund, 1999). Video analysis of E. striatus showed that the swiftest body pattern change occurred in 0⋅97 s (Table I). Moreover, in some video clips with an unchanging pattern, changes of contrast took less than half a second, although accurately quantifying these changes was complicated by changing light fields. These fastest speeds were surprising in that they are comparable with the speed of pattern change in cephalopods, which can change pattern as quickly as 270–700 ms or as long as 2 s (Hill & Solandt, 1935; Hanlon & Messenger, 1988; Hanlon, 2007; Hanlon et al., 2009). The swift change documented in our study implies that E. striatus has direct neural control of their chromatophores but, as far as is known, there is no information available on the structure or control of these dermal structures. The time for a complete pattern change of E. striatus, however, lasted longer than what is typically seen with cephalopods. Full pattern changes across the entire body took an average of 4⋅44 s and as long as 9⋅87 s (Table I). This difference may be the result of multiple mechanisms of overall body pattern control by the brain; i.e. there may be direct neural control of contrast change in body patterns but hormonal influence or control for overall body pattern change. For example, Healey (1999) found fast neural change (‘seconds to minutes’) in some skin elements of P. platessa and slow hormonal (hours or days) change in other skin elements. Alternatively, because most pattern changes occurred as E. striatus were swimming, body pattern changes might only occur when fish travelled into new visual surroundings. Future investigations of the morphology and physiology of E. striatus chromatophores, iridophores and leucophores would be informative and rewarding. Contrast changes that did occur on the fish’s lateral surface among vertical bars were usually associated with feeding and other daily behaviours, consistent with the report of Colin (1992). Epinephelus striatus is capable of additional body patterns, especially those associated with spawning activities (Archer et al., 2012). It would be most informative to document the speed of change and diversity of body patterns shown during the mass spawning aggregations of E. striatus in the Caribbean to complement the initial field study reported here. Studies on flatfish (Ramachandran et al., 1996; Healey, 1999; Kelman et al., 2006; Ryer et al., 2008) and cephalopods (Marshall & Messenger, 1996; Chiao et al., 2007; Hanlon, 2007; Kelman et al., 2007) have focused



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on how the visual features of the immediate background affect the choice of camouflage patterns, and similar studies should be conducted with E. striatus. Furthermore, dozens of other serranids and teleosts on coral and rock reefs worldwide change pattern for camouflage (Marshall & Johnsen, 2011) and these phenomena are among the most understudied in zoology despite the key role they play in natural selection. Sincere thanks to the Office of Naval Research Grant N00014-06-1-0202, Department of Marine Science at the University of Connecticut, Little Cayman Research Centre, Feng Travel Fund, George Burlew Scholarship and Explorer’s Fund of the Explorer’s Club for their support. J. Allen provided dive assistance. The collective advice of R. Whitlatch, E. Ward, C. C. Chiao, L. Mäthger and C. Chubb was most helpful and appreciated.

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Population structure and phylogeography in Nassau grouper (Epinephelus striatus), a mass-aggregating marine fish.

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