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1 Department of Psychology, Dalhousie University, Halifax, Nova Scotia B3H 4J1
2 Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1
* To whom correspondence should be addressed. E-mail: sadamo{at}dal.ca
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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Chromatophore organs are controlled by innervated muscle fibers, giving S. officinalis the ability to rapidly change both the pattern and color of its skin (Messenger, 2001). These muscles are innervated directly from the chromatophore lobes of the brain (see Messenger, 2001), at least for chromatophore organs in the fin (Gaston and Tublitz, 2004). However, only by stimulating higher brain centers such as the optic lobe can the cuttlefish be induced to display a coherent body pattern (Boycott, 1961).
Although cuttlefish can produce many body patterns in theory, in practice they use only some combinations frequently (Table 1; Hanlon and Messenger, 1988). The main function of these patterns appears to be crypsis (Hanlon and Messenger, 1988). Body patterns are also used for communication signals in males (Adamo and Hanlon, 1996) and probably females (Boal et al., 2004; Palmer et al., 2006). Body patterns may also play a role in foraging behavior, because some body patterns, such as Passing Cloud (Table 1), are frequently observed during hunting (Hanlon and Messenger, 1988, 1996). Hanlon and Messenger (1996) suggest that these body patterns may distract or lure prey.
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To determine whether body patterns observed during hunting may be useful in ecologically relevant studies of cephalopod cognition, we examine whether their expression changes depending on prey type, prey context, or the presence of a sudden stimulus (i.e., potential predator).
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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To avoid cueing by the experimenters, opaque curtains were hung around all experimental tanks. Cuttlefish were observed via a camera attached to a monitor. Trials were recorded on Hi8 videotape. The introduction of any material into the experimental tank was done remotely by the observer from behind the blinds. The experimental tanks used to test the cuttlefish were located in a room adjacent to that containing the home tanks. Cuttlefish were moved from their home tanks to the experimental tanks by gently scooping them into clear plastic bags. The cuttlefish, and their surrounding seawater, were then transported to the experimental tank in the adjoining room. Cuttlefish spent less than 2 min in the plastic bags during the transfer.
Data analyses
Data were analyzed using nonparametric tests (Sokal and Rohlf, 1981; Meddis, 1984). The alpha criterion was adjusted when more than one statistical test was performed on the same data set. Because body patterns are somewhat subjective, random sequences (chosen by lot) were tested for inter-observer reliability. Inter-observer reliability scores were r > 0.85 (Pearson correlation). Values are given as medians and first and third quartiles.
Hunting behavior in cuttlefish
Cuttlefish hunting behavior can be divided into three phases: attention, positioning, and seizure (Messenger, 1968). During attention, the cuttlefish aligns itself with the prey item. During positioning, the cuttlefish moves until it is about 1 mantle length from its prey. Seizure, the final phase, can be accomplished by two different maneuvers. During a tentacle strike, two tentacles are ejected and grab the prey. During an "arm-grab," the cuttlefish jumps on its prey and wraps its arms around it. Table 1 describes some of the body patterns commonly observed during hunting.
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Experiment 1. Effect of Prey Type on Hunting Behavior and Body Patterns |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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The experimental tank (91 x 61 x 44 cm, water depth 37 cm) had an opaque plastic shelf (61 x 17 cm) above the outlet pipe, creating a shelter for the cuttlefish. At the start of a trial, cuttlefish were placed under this shelter in the experimental tank and left undisturbed for 30 min. At 30 min, a prey item from one of the three prey types was introduced into the tank at the opposite end from the shelter. Crabs were tied between their fourth and fifth walking legs and lowered into the tank. Goldfish were placed in a container that was tipped into the tank (via a pulley system). Shrimp were tethered to a weighted nylon filament and lowered into the tank. Trials lasted a maximum of 10 min or until the cuttlefish had consumed the prey. Cuttlefish were given no more than one trial per day.
All cuttlefish were presented with each prey type twice, in separate trials. The order that the prey types were presented was randomized to prevent order effects.
Results
Cuttlefish always seized fish using a tentacle strike (7/7 cuttlefish, all trials). Crabs were seized using an arm-grab (4/7 cuttlefish attacked a crab, 4/7 used an arm-grab). In all but one attack, the cuttlefish approached the crab from the posterior end, away from the claws. In one trial, a cuttlefish attacked the crab laterally. Shrimp were seized using a tentacle strike (5/7 cuttlefish attacked, 5/7 used tentacle strike, both trials).
During hunting, cuttlefish displayed a variety of body patterns prior to seizure (i.e., attention and positioning stages). Cuttlefish expressed the patterns Disruptive, Light Mottle, Stipple, Weak Zebra, and Uniform Light. They also exhibited the postural display of Raised arms. There were no consistent differences related to prey type (Test for trends for frequency data; Meddis, 1984; Z < 1.0, P > 0.1, all tests). No Passing Cloud displays were observed. During the seizure phase, cuttlefish frequently expressed the Dark Mottle, regardless of prey type (7/7 cuttlefish expressed Dark Mottle during at least one seizure event). Interestingly, frame-by-frame analysis revealed that this change in pattern occurred after the prey had been caught by the tentacles.
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Experiment 2. Effect of Prey Context on Hunting Tactics and Body Pattern Use |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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Treatment 1: Bare Tank.
Cuttlefish were presented with a shrimp in the center of a bare tank. The shrimp was tethered by tying a nylon filament just anterior to the telson. The shrimp was unable to camouflage itself against the blue-green color of the tank.
Treatment 2: Rock Pile.
A shrimp was tethered to the top of a pile of small rocks. The rocks were 5 to 20 cm in length along their longest axis, and each rock was no more than 2.5 cm in height. The total height of the rock pile was 12 cm. If untethered, the shrimp could have hidden between the rocks. The shrimp were clearly visible to a human observer, and presumably to the cuttlefish as well. Cuttlefish are visual predators with excellent acuity (Messenger, 1968).
Treatment 3: Sand.
The experimental tank was filled 0.5 to 1.5 cm depth with fine brown sand, into which the shrimp buried themselves. Shrimp were tethered under the sand.
To start a trial, cuttlefish were placed in the larger of the two sections of tank. We found that after 15 min, cuttlefish adopted a resting pattern and settled on to the bottom of the tank. After a 15-min acclimation period, the partition was raised and the cuttlefish entered the treatment area. Each trial lasted 10 min after the partition was raised or until the shrimp was eaten. Cuttlefish were given four trials with each treatment. The order of presentation of each treatment was randomized. Cuttlefish were given no more than one trial per day.
Results
No cuttlefish exhibited the Passing Cloud display during any of the three treatments, although in one of the sand trials one cuttlefish expressed a pulsating dark pattern on its arms that resembled a Passing Cloud display. All cuttlefish (11/11) expressed the Dark or Light Mottle body pattern during seizure of the shrimp in 3/3 treatments in at least 1/4 trials. Frame-by-frame analysis revealed that the change in body pattern occurred after the seizure of the shrimp.
Cuttlefish had never experienced sand-covered tank bottoms prior to this study. In their first Sand trial, none of the cuttlefish used their funnels to blow sand away from the shrimp to aid in its capture. For 5/11 cuttlefish, the shrimp was plainly visible during their first Sand trial, and all but 1 of the cuttlefish successfully captured the shrimp. For 3/11 cuttlefish, the shrimp was invisible (i.e., completely buried) during their first Sand trial. In these trials, none of the cuttlefish engaged in hunting behavior. For the remaining 3/11 cuttlefish, the shrimp was partly visible during their first Sand trial. In 3/3 of these trials, the cuttlefish attempted a tentacle strike in the sand but only 1 was successful in catching the shrimp. By the last two sets of Sand trials, of the six trials in which 5/11 cuttlefish were exposed to shrimp that were completely or partially covered with sand, in two of these trials no hunting sequences were initiated until the experimenter moved the shrimp remotely, removing it from the sand. In the other four trials, all initial tentacle strikes failed to capture the shrimp. In one trial, the cuttlefish blew the sand off the shrimp after its first tentacle strike was unsuccessful, and the shrimp remained partially covered in the sand. The cuttlefish then successfully seized the shrimp.
Cuttlefish (n = 11) required the least amount of hunting time (i.e., start of the attention stage to extrusion of the tentacles) in the Bare Tank treatment (median, 2 s; first quartile, 1 s; third quartile, 3 s), followed by the shrimp on the Rock Pile (median, 9 s; first quartile, 7 s; third quartile, 16 s), and finally shrimp in Sand (median, 14 s; first quartile, 13 s; third quartile, 20 s; Test for trends, repeated measures; Meddis, 1984; Z = 2.63, P < 0.001).
Over the four sets of trials, cuttlefish showed a decrease in the duration of hunting time in the Rock Pile trials (Test for trends, repeated measures; Meddis, 1984; Z = 1.92, P < 0.05, n = 11). Test for trends in the Sand treatment was not possible because of the variability in the degree to which shrimp buried themselves in the different trials.
Despite extensive variability in the body patterns expressed both within and between animals, the postural component Raised arms was used significantly more often when cuttlefish were hunting in the Sand and Rock Pile treatments than in the Bare Tank (Fig. 1; Repeated measures test for trends; Meddis, 1984; Z = 2.73, P < 0.01, n = 11).
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Experiment 3. Hunting in the Presence of a Sudden Stimulus |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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To determine whether the cuttlefish could potentially see the model, an experimenter entered the water-filled tank, positioned her head to be about 20 cm from the posterior edge (striking distance for the cuttlefish from the shrimp) and looked up. To the human observer, the model was clearly visible from underneath the water, both while it was sliding along its track and once it stopped at the end of its run. However, because cuttlefish eyes are differently placed than human eyes, this information does not demonstrate that the cuttlefish could see the model, only that the image of the model penetrated into the tank. However, in another study using a similar apparatus, cuttlefish produced robust behavioral and physiological responses to an overhead bird model (King and Adamo, 2006). Therefore, we know that cuttlefish are capable of responding to visual stimuli located in the air above them in an experimental set-up very similar to ours and completed in the same laboratory.
After 30 min of acclimation in the experimental tank, the shrimp was lowered into the tank. Cuttlefish were then given 10 min to initiate a hunting sequence. If the shrimp was not attacked within that time, the trial was terminated. During the first trial, cuttlefish were allowed to attack and consume the shrimp without the model bird being present (pre-bird trial). In the three bird trials, as soon as the cuttlefish had adopted the attention stage of hunting, the model was released and allowed to fly over the tank, producing a sudden novel stimulus. The model stopped above the end of the tank containing the shrimp and was left there for the remainder of the trial. After three bird trials, the cuttlefish were given one trial without the model bird being released (post-bird trial). There were always 2 to 4 days between any two trials.
Results
Body patterns observed during foraging.
Prior to orienting toward the prey, cuttlefish expressed a Stipple body pattern (10/10 cuttlefish, all trials). This cryptic pattern allowed the cuttlefish to blend in with the coarse sand substrate (Hanlon and Messenger, 1988). Most cuttlefish (8/10 in at least 2/5 trials) maintained a Stipple pattern as they raised themselves from the substrate and oriented toward the prey (i.e., the attention stage of hunting). The pattern often darkened as the cuttlefish approached the shrimp (positioning stage, 8/10 cuttlefish in at least 1/5 trials). Orienting cuttlefish extended their fourth arms forward (8/10 cuttlefish, at least 1/5 trials) or sometimes splayed them out to the side (6/10 cuttlefish, at least 1/5 trials). All cuttlefish (n = 10) seized the prey using a tentacle strike. During prey seizure, the cuttlefish usually adopted a darker body pattern, such as Light or Dark Mottle (Table 2); however, 1/10 cuttlefish showed Uniform Blanching during the attack instead of a darker body pattern (Table 2). Frame-by-frame analysis demonstrated that the body pattern darkened either at the same time as the tentacles contacted the prey or immediately after. Most cuttlefish (7/10) returned to Stipple within 15 s of seizure in at least 2/5 trials.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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However, further studies, such as showing that Passing Cloud displays increase predation in the field, must be completed before we can conclude that decreasing this display reduces predation on cuttlefish. Nevertheless, indirect evidence supports this hypothesis. Dark arms, another conspicuous display, is also reduced after exposure to the model bird (Table 2). Fish can alter their foraging behavior when predation risk is increased (Kelley and Magurran, 2003), as can non-cephalopod molluscs (Serra et al., 1997). Therefore, this ability in cuttlefish would not be surprising.
Unfortunately the function of the Passing Cloud display is unknown. In juveniles, Hanlon and Messenger (1988) noted that young cuttlefish expressed the Passing Cloud display during hunting, when approached by large fish, and when swimming. In the context of hunting, it is thought to distract or mesmerize prey (Hanlon and Messenger, 1996). Other cephalopods also exhibit Passing Cloud displays, typically during hunting (e.g., Mather and Mather, 2004). Interestingly, we did not see Passing Cloud displays in adult cuttlefish. Whatever function it may have during hunting, adults appear to use it less than juveniles.
The observation that all cuttlefish (10/10) responded to the overhead model demonstrates that they were capable of perceiving it. We assume that the cuttlefish used visual cues to perceive the model. The model’s track apparatus was not attached to the experimental tank and, therefore, it probably did not produce vibrational cues.
The conspicuous change in body pattern that occurs at the time of seizure (typically Dark or Light Mottle) was observed in all experiments, regardless of prey type, context, or the presence of a potential predator. Messenger (1968) also noted that cuttlefish express color changes during seizure, although he described it as Uniform Dark. Crypsis is usually the cuttlefish’s major defense against predation (Hanlon and Messenger, 1988, 1996), and the sudden change in contrast and color that occurs during seizure probably puts them at risk. Given that this display is often performed after the prey has been seized, it is unlikely to be a signal designed to confuse or startle the prey. Mauris (1989) found that a related cephalopod, Sepiola affinis, also makes a number of striking body pattern changes at the time of prey seizure. Mauris (1989) suggests that these pattern changes serve to "startle" potential predators while the cephalopod is attending to its attack on the prey and not watching for predators. Hanlon and Messenger (1988) noted that the only predation events they witnessed on juvenile Sepia officinalis in the field occurred when the cuttlefish’s attention was directed at their video camera, leaving them oblivious to predators. Further field studies are required to test whether predators are startled by the display and whether expressing this display results in increased survival for cuttlefish. The sudden change in appearance that occurs during seizure does fit the description of a Deimatic Behavior (Hanlon and Messenger, 1996), which is a behavior designed to deter predation. However, this explanation seems incomplete because it does not explain why cuttlefish in a sizable minority of trials (about 10%–15%) did not exhibit a dramatic change in body pattern contrast at the time of seizure. Regardless of its functional significance, this result demonstrates that not all body patterns used during hunting are equally plastic.
We have little evidence that the body patterns used during hunting differ depending on context or the identity of the prey used in this study. Even though Raised arms did differ between prey contexts (Experiment 3), the tendency to exhibit Raised arms correlated with the length of the hunting bout. It is possible that Raised arms may be more likely to occur the longer the foraging event lasts, regardless of the context of the target.
This study corroborates earlier work (e.g., Messenger, 1968) that also found that cuttlefish tend to use tentacle strikes on fish and arm-grabs on crabs, depending on crab size and other factors (Messenger, 1968; Duval et al., 1984). Our naïve cuttlefish positioned themselves away from the claws of the crab on their first attack. Boal et al. (2000) found similar results, but only if crab odor was present. These authors suggest that the smell of crab can induce a state of food arousal, heighten the animal’s attention, and decrease the chance that it will attack the crab facing the claws. Our cuttlefish were probably exposed to crab odor from earlier trials in the same tank, even though there was constant water flow in the experimental tank. However, their lack of experience with crabs may explain why 3 of the 7 cuttlefish never attacked the crabs, even though they always attacked the fish.
Cuttlefish have been observed using their funnel to remove sand covering prey (shrimp, see Tinbergen, 1969 who cites a personal communication by Dutch zoologist Jan Verwey; crab, see Mather, 1995). After four repeated trials, we observed this behavior only once, after a failed tentacle strike. Possibly our cuttlefish required more experience hunting in sand to learn this technique. Having experience with sand may be important for cuttlefish to learn how to manipulate it (Poirier et al., 2004).
Strong individual differences existed for at least one body pattern used during hunting (Raised arms; Fig. 2), even though the animals were reared in the same laboratories, under the same conditions. S. officinalis appears to show other individual differences as well (Calvé, 2005), as do other cephalopods (e.g., Mather and Anderson, 1993). The function, if any, of Raised arms during hunting remains an area of active research (e.g., see Hanlon and Messenger, 1996). However, if it does serve some function, as suggested by preliminary studies (Hanlon and Messenger, 1996), then individual differences in its use may reflect differences in hunting strategies between individual cuttlefish. Such differences could arise because of a combination of early learning and genetic influences. These same factors are thought to produce individual differences in fish (Warburton, 2003), in other cephalopods (e.g., Sinn et al., 2001), and in non-cephalopod molluscs (e.g., West, 1986). Differences in body pattern use during hunting may be helpful for exploring how environmental influences can produce individual differences.
This study suggests that body pattern production may serve as a sensitive indicator of ecologically relevant learning (see also Mather, 1995). For example, it may be possible to use changes in body pattern expression to test whether cuttlefish can learn to associate cues with the presence of predators. Studying the effect of potential predators on the foraging behavior of fish has proven a useful paradigm for examining their cognitive ethology (e.g., Kelley and Magurran, 2003). Use of body pattern changes as a measure of learning also has the advantage that the brain areas controlling their expression are under active investigation (Messenger, 2001; Gaston and Tublitz, 2004).
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Acknowledgments |
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Footnotes |
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Literature Cited |
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TOPAbstractIntroductionMaterials and MethodsExperiment 1. Effect of...Experiment 2. Effect of...Experiment 3. Hunting in...DiscussionLiterature Cited |
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