Groupers often repeated the head-shaking signal in these situations Figure 2 , arrows. In addition to signalling before any hunting events, groupers also recruited moray eels after unsuccessful hunts.
Typically, a hunt ended unsuccessfully because prey escaped into a crevice that was inaccessible to the grouper. In the majority of observations, the groupers either swam off immediately without further hunting attempts, or they remained nearby, usually above the hole but out of sight.
This latter behaviour usually lasted several minutes and sometimes led to a second hunt, presumably involving the same prey fish. The dorsal fin was used as in the standard head-shake signal to the moray, but the head movements differed, most obviously because of the pauses between single shakes Video S3. Headstand shakes invariably attracted other predators to the prey's location in the crevice.
On ten occasions, a moray eel joined the grouper and explored the crevices Video S4. Napoleon wrasses, Cheilinus undulatus, approached and inspected the hiding place on ten occasions, and a yellowlip emperor, Lethrinus xanthochilus, approached on one occasion.
Guiding moray eels to hidden prey and signalling above hidden prey to attract other predators resembles the behaviour of honey guides that catch the attention of badgers or humans and guide them to bee nests [ 11 ]. The badgers or humans raid the nest and the bird is then able to feed on what remains. Six individual groupers received a fish at the onset of an observation session, and we therefore knew that their hunger level was likely to be lower than during an average random observation.
The groupers did not signal to a moray eel during the min observations following the consumption of the prey. The analysis does not control for individual contribution to the dataset. Five different individuals were successful in presence of moray eels and eight individuals were successful in the absence of moray eels three individuals appear in both datasets.
In association, groupers caught almost five times as many prey items per unit time than when morays were absent 0. The ten occasions on which groupers hunted successfully without a moray included one observation of two groupers hunting the same prey simultaneously and two observations of a grouper hunting with a napoleon wrasse.
The wrasse seems to fulfil a similar function to the moray eel; Although it cannot enter crevices where preys are hiding, it can often destroy hides with its powerful jaws. Groupers Benefit from Joint Hunting.
On five occasions, we observed moray eels catch prey when hunting with a grouper. Thus, the hunting success of both predators was roughly equivalent. Moray eels were never observed to hunt successfully when solitary. This is not surprising, however, as moray eels observed alone simply remained in their crevice and did not appear to search for prey.
Therefore, statistical analysis seems inappropriate because solitary morays were merely resting. Nevertheless, the success rate of 0. During the This includes the 11 observations of successful hunts. The individual fish that caught the prey swallowed it quickly and whole without any aggression from the unsuccessful partner.
We have presented several lines of evidence for interspecific communicative, coordinated, and cooperative hunting between two species of reef fish predators. We found the following: 1 individual groupers and moray eels frequently spent more time in association than predicted by a null model of chance encounters, 2 groupers actively signalled to elicit joint hunting and to recruit moray eels, 3 satiated groupers did not signal, and 4 both partner species increased their hunting success in association.
Although the evidence for groupers is straightforward, the typical nightly activity pattern of moray eels precluded any detailed statistical comparison of hunting success data.
However, given that moray eels showed a higher success rate than groupers in association 0. We did not detect any behaviour of either partner that might have served to increase the hunting success of the other species at the expense of its own hunting success.
In other words, altruistic behaviour did not seem to occur during joint hunting events. Thus, the outcome of joint hunting between the groupers and the moray eels appears to be a by-product mutualism [ 12 ]. Intraspecific coordinated hunting with role differentiation between individuals is known for only a handful of species [ 5 — 8 ] and has not yet been observed in fish, although simultaneous group hunting exists [ 13 ].
The evolution of coordinated hunting may occur only rarely because several problems related to the coordination of behaviour must be overcome. For example, individuals must perform actions during coordinated hunts that are successful only if they are accompanied by complementary actions performed by other individuals at the same time. Consequently, cognitive constraints may limit species' ability to coordinate in this manner.
In addition, the adoption of different roles during coordinated hunts means that certain individuals will experience a reduced probability of catching prey themselves when hunting and so incur a net cost, whereas other roles are associated with increased rates of prey capture, and therefore yield a net benefit for the individuals' playing these roles. Hence, intraspecific coordinated hunting is linked to the well-known evolutionary problems of unequal payoffs and potential defection that are associated with altruistic behaviour.
Tit-for-tat—like role alternation [ 14 ] or the sharing of prey [ 5 ] are potential solutions to this problem. Finally, phylogenetic constraints may limit the kind of roles that individuals are able to adopt, and so reduce the likelihood of successful coordinated hunting. For example, a lioness will never be able to run with the speed of a cheetah, even though this ability would help in a coordinated hunt.
Interspecific cooperation, as we have observed between groupers and morays, seems to overcome the difficulties of intraspecific coordinated hunting. Any potential cognitive constraints regarding the division of roles are absent, because associating partners behave in exactly the same manner as they do when hunting alone. Each player uses only its evolved hunting strategy, and there is no pressure to learn specific new behaviours that yield advantages when they form part of a coordinated effort.
In addition, both grouper and moray apparently try to maximise their individual capture rates, with mutual benefits accruing simply from the joint movements that serve to amplify their individual predation efforts. Interspecific coordinated hunting of this kind can emerge, therefore, from a simple associative learning process, whereby each species associates increased rewards with hunting in the vicinity of the other species.
The same mechanism may explain the many commensal associations in coral reef fish, where individuals of one species follow a so-called nuclear species [ 15 — 17 ]. However, these associations lack the signalling and mutually coordinated movements observed in grouper—moray interactions. At present, we can only speculate about the nature of the information that is conveyed by grouper head-shake signals.
We have never observed head shaking of this kind, or anything similar, in moray eels, so it seems unlikely that grouper signals represent the generalisation of the morays' natural intraspecific repertoire to an interspecific context.
The simplest explanation, therefore, is that these signals indicate only the motivation of the grouper to engage in hunting, which then becomes positively associated with hunting success for the moray eels. That is, head shakes may act as a form of conditioned stimulus for the morays.
This is particularly likely in situations where a grouper has already cornered a vulnerable prey fish, allowing morays easily to associate head shaking by the grouper with their own hunting success, or at least a close encounter with a prey. Active signalling between partners to initiate joint hunting rather than merely indicating the presence of a food source as in the honeyguide example [ 11 ] has been interpreted as a major cognitive achievement in chimpanzees [ 5 ].
Such differences have generated great interest in the anthropological literature because of the disputed importance of complex cooperative hunting for early human evolution [ 20 — 22 ]. Whether these differences between populations reflect true cognitive differences rather than mere differences in ecology remains to be tested.
Our results suggest the latter, unless future studies are able to demonstrate more convincingly that complex cognitive processes underlie chimpanzee communication during hunt initiation.
In our study system, signalling by groupers seems to be a necessary adjustment to the morays' activity pattern. Because moray eels are usually inactive during daytime, groupers cannot join a partner that is already looking for prey but must induce a moray to become active.
We hypothesise that swallowing prey whole, as we observed in the groupers and moray eels, is an important condition for the occurrence of interspecific cooperative hunting. In principle, interspecific hunting could also improve the hunting success of mammalian predators, but it is rarely found, and examples always involve humans as one of the partners [ 23 , 24 ]. Pursuit hunters, like hyenas, that coordinate their hunts with a speed predator, like a cheetah, or a sit-and-wait predator, like a leopard, could also increase their hunting success in the same way as groupers and moray eels.
However, after successful hunts, competition would arise immediately over which species feeds first and which parts of the carcass are eaten, and problems of cheating and defection would be rife. Consequently, we propose that the defensibility of a kill is the decisive obstacle preventing the evolution of interspecific cooperative hunting in mammals and other taxa.
If cheating after a successful hunt is not an option, however, interspecific cooperative hunting may readily evolve. Moreover, we suggest that the multiple predation effect of interspecific cooperation is the key to overcoming the inherent problem presented by the joint hunting of nonsharable prey; namely, overall prey capture rate needs to be at least twice that obtained by a solitary hunter in order to yield net benefits [ 4 ].
In accordance with our hypothesis, we have two observations, one video-documented unpublished data , of lunartail groupers, Variola louti, which signalled once to a grey moray eel and once to a giant moray eel in a very similar way to our study groupers [ 25 ]. The latter happened after we had first attracted the grouper with a dead fish and then hidden the fish in a crevice near the moray.
We expect to find other species combinations that hunt cooperatively, but only in situations where there is no competition over carcasses. Along the m coastline, 14 groupers, varying between 55 and cm in total length estimation were recognised by individual spot patterns on their body. What countries do moray eels live in? Do moray eels lay eels? Are moray eels endangered?
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