Communicated cooperated hunting in two coral reef predator species
Tamara Gademann, s3465535
Essay for the marine biology master at the University of Groningen
Supervised through Sancia van der Meij, Evolutionary Ecology of Marine Animals, RUG
2 Abstract
Groupers can communicate a cooperative hunt. Hunting partner is for example toe moray, eel or the napoleon wrasse. Other animals that are known to be able to communicate a joined hunt are for instance lions, chimpanzees or killer whales, all mammals. This essay wants to discover the differences and similarities between the mammal joined hunting and the groupers. Furthermore, it wants to discover how the communicated hunting between the grouper and its hunting partner looks alike and how the grouper can give the necessary signals.
Is the behaviour territorial or does it happen all over the world? Is just one grouper species able to communicate a cooperative hunting, or several? Which factors affect the tendency of a grouper to ask for joined hunting?
3 Table of contents
INTRODUCTION 4
SPECIES OF INTEREST 6
PRESENTATION OF RESEARCH FINDINGS 7
DISCUSSION OF RESEARCH FINDINGS 14
COMPARATIVE DISCUSSION 15
LITERATURE 17
4 Introduction
From human infants it is known that they use gestures to communicate, pointing, showing or giving to draw attention of a social partner to a specific subject of interest [36, 37]. Gestures and signals are also important while the act of hunting in a group.
Hunting is an act of a human or an animal, to pursuit and kill other living individuals to feed on them and to increase the own fitness. Every predatory animal is also a hunter, but not every hunter hunts with the same method. Some animals, as tigers hunt alone, some like lioness hunt in a group, but how does this “group-hunting” work? How do the animals communicate with each other and how do they share their prey without aggressive behaviour?
In the very past humans joined together to hunt in a group, because a group means a higher likelihood of security and a greater probability of hunt-success. But the act of hunting also caused in the evolution of social relationships due to required communication between the partners [1,2]. Important for a successful group hunting is foremost the coordination and communication, thus if groups specialize on prey that is risky or difficult to catch, an individual benefits from cooperation with others during the hunt and takes advantage from the sharing of the killed prey [3]. This can not only be shown in human societies, but also in many mammal predator species as chimpanzees, lions, hyenas, orcas and dolphins. Evolutionary, chimpanzees are very close to humans and they also show a group hunting behaviour, which is called: “intentional hunting” [4]. Nineteen of all known chimpanzee species are carnivorous and they tend to reach kill rates much higher than comparable with other mammal predator species such as hyenas [5].
Group hunting in wild chimpanzees was classified as an act in which more than one hunter acts at the same time against the same (group of) prey [5]. Different hunting methods that have been observed in the monitored chimpanzees were described: First there is the
“group hunt” in which only one hunter is hunting at a time with a couple of bystanders doing nothing, or rather starts hunting when the before-hunting individual has finished [5, 6]. The second method is the “cooperative hunting”, in which only one individual acts in total. The second individual waits and watches [5, 9]. Chimpanzees are using gestures to communicate, those they learn from their parents and the social community they belong to [10].
Some Lions, especially the species Panthera leo [12], are also known as group hunting animals. Their method is, that they usually hunt in a formation, whereby some group members circle the prey while others wait in the centre. Due to that they impel the prey3???? in the middle, where it is killed [12]. Every lioness has its position in the group, which is the same in every hunt, hence this behaviour increases the hunt success of the group [12]. Thus, lions also behave cooperated while hunting. Therefore, that lions have a very different habitat to those species that were mentioned above, their group hunting is mainly evolved due to reduce????
problems of location and subduing large prey [12 – 15]. In their case cooperative hunting supports social predators as lions in catching prey in open habitats [16]. Generally said, for all grouping predators applies what Hamilton has once defined: If there is cooperative behaviour, animals only do things that benefit itself, meaning its fitness (survival/ reproduction) [5, 11].
Another example are killer whales. Killer whales are intelligent, social mammals that live in a completely different habitat than all animals that were mentioned before: The water.
5 Furthermore, they are the largest apex predators in the ocean [17]. Genetically there are different species in the killer whales and in Pitman`s paper [17], the hunting behaviour of
“pack ice killer whales” was monitored. The first-time cooperative hunting in pack ice killer whales was described, was 1981 from Smith et al. [18], which is the same hunting method Pitman observed. Smith et al. was not the only one who wrote about this kind of hunting behaviour, also Visser et al. did [19]. Thus, it can be said that killer whales, even though they are living in the water, also hunt prey successfully outside the water [17], next to hunting in the water. But there are more hunting methods than just this one, for instance other killer whale species often hunt other mammals, such as minke whales. Here they often come from below, ramming the prey to kill it [20]. Another method is to jump out the water, landing on the prey, or to kill prey through swatting their tail against them, etc. [21, 22]. Pitman says in his report, that for communication between the killer whales their very large postocular eye patch might be used mainly [17]. By that, coordinating the wave-washing seems to be easiest when swimming in a tight synchronized formation. Hence, acoustic coordination might not be as effective as using a landmark for the hunt, when being in close quarters [17]. It can be said, that killer whale hunting behaviour resemble the hunting behaviour of lions: If prey is close, they often decide to hunt cooperated, with several animals flanking the prey to keep it from escaping, while one (or more) whale chases and kills it [23].
The last given example that explains cooperative hunting in mammals, is the hunting method of bottlenose dolphins, which has been described as “division of labour” [24]. This means, that there is a role specialization found, when the individuals of the group specialize in subtasks while fulfilling the team task. The only other known species that can implement a role specialisation, are the African lionesses (Panthera leo), which were already discussed above: Females in “centre role” wait for the prey while others force the prey towards them [12]. The hunting technique that evolved in bottlenose dolphins is similar: The prey, mainly fish swarms, are herded into a ball, which is then urged ahead a crescent dolphin formation [25 - 27]. Another method is, to drive the prey against a mud bank or dolphins beach themselves to feed on fish that have chased to these mud banks [28, 29]. To get to the
“division of labour”: In Cedar Key, Florida [24], there are two types of herding fish, in bottlenose dolphins: “drivers” and “non-drivers”. The drivers are those individuals, usually it is just one, if the group of dolphins is between three to six individuals, that impel the fish into balls, as well as force them against a barrier (mud banks/ dolphin formation). This barrier consists of the “non-driving” dolphins.
So, if all these species and examples would be combined, there are clear common grounds: All species are mammals, all species are able to behave in different roles, all species cooperate with other individuals of their own species for hunting (and often also for living) and all of them live inside a social society where they learn how to behave, how to hunt, etc.
from their parents. Therefore, the next questions are: Are animals, that are independent from their parents, like fish, able to learn how to communicate with other species to do a cooperative hunt? And why should they do so, what are the advantages or disadvantages of a cooperative hunt between these species?
Cooperative hunting was observed 2014 in lionfish predators by the authors of the article: “Lionfish predators use flared fin displays to initiate cooperative hunting” [30]. They found, that one lionfish species: Dendrochirus zebra can indicate communicative hunting to another lionfish species, which is Pterois antennata, but also to their own species. To initiate a cooperated hunt, zebra lionfish use their stereotyped flared fin to give a hunting signal that
6 supports members of their own species, as well as individuals of different lionfish species. If an individual agrees, it responds actively with the same signal of the fin. These cooperative hunts act in a group of two hunters. When hunting predators use their large extended pectoral fine to herd the prey into a corner, thus they cannot flee, then feed on the prey. The article says furthermore, that there was kind of a sharing behaviour monitored, they call it “tit-for- tat-like role alternation” [31], which is kind of a sharing-the-prey behaviour. If there is hunting success the successful hunter swallows the prey directly, lionfish can swallow four or five times sequentially, thus sharing does not have the same meaning as in mammals. Sharing means here, that the successful hunter returns the gesture, thus the hunting partner feeds on the next hunted prey.
Another paper shows the behaviour of sea brasses that follow star fish in shallow, flat bottoms, feeding on disturbed or exposed prey due to sea star activities [32]. Here is to say, that this behaviour is not a communicated hunting, but just a behaviour that gives an advantage to the sea brasses, though they have a lower hunting effort like when hunting alone. But it is interesting to see, that fish can find “partners” that benefits their own feeding success and are not from the same species or family, as in the lionfish.
To give an answer to the research question: If communicated hunting is possible between two completely different species and how this works, the example of the grouper and the giant moray eel is the best example, that can be given here [4]. In the following the species that are part of this cooperative hunt are going to be introduced, as well as their method of hunting, plus advantages and disadvantages referred to the hunting. Further, references will be taken to groupers social structures/ lack of culture and their type of communication.
Species of interest
Groupers are teleosts that belong to the family Serranidae and the subfamily Epinephelinae.
But not all fish that belong to the Epinephelinae are called groupers, some are called sea brasses. Generally, the genera Epinephelus and Mycteroperca are called groupers, as well as the small genera Anyperidon, Cromileptes, Dermatolepis, Gracila, Saloptia, and Triso. There are 15 different species described in the genus Mycteroperca and 89 different species in the genus Epinephelus. Groupers can grow big: About a body size of a meter and a weight of 100 kg. They are not made for fast swimming or for swimming long distances. Moreover, groupers are diurnal predators, that are piscivores and hunt on other fish. Their hunting areal is the open water, where they usually wait until prey swims from the corals into the open ocean and then catch it [4]. Usefully hereby is, that their mouth and gills form a powerful sucking system that sucks their prey in, from a distance. Groupers are protogynous hermaphrodites, that means they can change their sex [39, 40]. Hence, they mature only as females and can change their sex after sexual maturing.
The moray eel belongs to the family Muraenidae and to the order Anguilliformes. For the cooperation hunt between the grouper and the moray eel, always the giant moray eel (Gymnothorax javanicus) is the hunting partner, in case of moray eels that one is the largest eel [41]. It can reach a size/ length of 3 meters and a weight of 30 kg [42]. The body colour is brownish, the shape is serpent-shaped. The giant moray eel lives in crevices in the coral reef and is a nocturnal hunter [43]. Usually they wait inside those until prey passes by or the moray eel swims through crevices searching for prey [4].
7 Next to the giant moray eel, there exists another species that serves as a hunting partner to the grouper: The octopus. The referred paper [33] gives the reef octopus (Octopus cyanea) as an observed hunting partner for the highfin grouper (Epinephelus maculatus). This octopus is also called big blue octopus or day octopus and occurs in the Pacific and Indian Ocean.
Individuals can grow up to a mantle length of 16 cm and an arm length of 80 cm [34]. This octopus lives on coral reefs and can change skin colour, as well as its skin texture.
Furthermore, it is a diurnal almost crepuscular hunter [35], that searches for fish, molluscs and crabs.
Further, some additional coral reef fish were described to hunt with the grouper, for example the: Chelinus undulates [36], which is the humphead or napoleon wrasse, as well as the emperator [36]. The napoleon wrasse is a mainly Indo-pacific coral reef predator. It is the tallest member of the family Labridae, ranges up to 2 meters from tip to tail and about 180 kg weight. It is easy to identify due to thick lips, the large size, the hump that appears on the adult’s heads and the blue-green plus purple colour [44, 45].
Presentation of research findings
There are two ways a grouper communicates the “wish” for a joint hunt to the potential hunting partners: The first method is the behaviour of the grouper to actively visit the moray eel at their resting places and give visual signs to communicate that they wish a cooperative hunt [4]. The sign is usually a head shaking movement in a high frequency (3 to 6 shakes per second), really close to the moray eels head. Another, toned version of this method is, when the grouper swims to the resting place of the moray eel, without shaking head, but just waiting to be recognized, above or really close to the moray eel. This behaviour was often observed, after an unsuccessful hunt on the groupers side [4]. When for example prey hides in the corals.
Thus, the grouper knows a place where prey is hiding and guide the moray eel to this place, thus it can drive the prey out the crevice into the groupers mouth, or rather eat it itself if fast enough.
The second method, that was monitored, is the head-stand: The grouper gives this signal, when he is on a hunt, noticing prey is hiding at a place, he is not able to reach. When, while hunting already a potential hunting partner, like a moray eel or a wrasse, passed by, he is giving the head-stand signal to show them, that prey is hiding. But also, if the grouper did not see anyone to hunt with, he gives the signal and maybe a close octopus or moray, etc.
sees the signal and joints the hunt [36]. This signal does not indicate that prey leaves the hiding place, but it indicates that potential hunting partners can see, that prey is close and probably easy to catch. Therefore they, an octopus or a moray eel, can swim into the crevice and either surprise the prey, hence have a successful hunt, or drive them out the crevice into the groupers hunting area, which means that he has a hunting success.
Usually the communicative hunting is indicated through the grouper, because he has had a couple of unsuccessful hunts. Thus, the chance to increase the own prey success is higher, even when hunting with two. Advantages and disadvantages of this cooperative hunt can be found in Table 2.
8 Tab. A1: Which grouper species are known to do the cooperative hunt? Which species are joining those hunts?
GROUPER SPECIES PARTNER SPECIES REFERENCE
EPINEPHELUS FASCIATUS
Octopus cyaneus, Octopus macropus, Lycodontis sp., Myrichthys sp., Sidera grisea
[38]
PLECTROPOMUS
LEOPARDUS Octopus cyanea [36]
PLECTROPOMUS
PESSULIFERUS Gymnothorax javanicus [4]
PLECTROPOMUS
PESSULIFERUS Chelinus undulates, Gymnothorax javanicus [36]
EPINEPHELUS MARGINATUS
Myrichthys ocellatus [33]
Tab. A1.2: Where do these groupers occur? [46]
GROUPER SPECIES OCCURRENCE
EPINEPHELUS FASCIATUS Indian Ocean, Japan, Korea, Red Sea, South Africa
PLECTROPOMUS LEOPARDUS Australia, China, Fidschi, Indian Ocean, Japan, Korea, Malaysia, North-Pacific, East- Pacific, Papua-Neuginea, West-Pacific, Central-Pacific, etc.
PLECTROPOMUS PESSULIFERUS Red Sea, Australia, Fidschi, Hongkong, Indian Ocean, Indo-Pacific, Israel, Maldives, Mauritius, Sri Lanka, etc.
EPINEPHELUS MARGINATUS Red Sea, Brazil, Argentina, West-Africa, European Waters, Gulf of Oman, Gulf of Guinea, Israel, Kamerun, Madagascar, Mediterranean Sea, Black Sea, West-Africa, West-Indian Ocean, etc.
9 Tab. A2: What are the advantages/ disadvantages of joint hunting for the grouper?
ADVANTAGES DISADVANTAGES
THE CHANCE TO CHATCH FOOD IS HIGHER THAN
WHEN HUNTING ALONE Not all food is caught by the grouper, thus he must share the food, or rather the probability to get all the food is low.
BECAUSE THE MORAY EEL IS RESTING, IT SEEMS TO BE NOT HUNGRY, THUS THE GROUPERS SUCCESS MIGHT INCREASE
There is a chance, that the grouper needs to motivate the moray eel to join the hunt WHEN RECRUITING WAS SUCCESSFUL, THE
GROUPER HAS NOT ANY WORK, HE JUST WAITS OUTSIDE THE CREVICE FOR THE PREY TO FLEE OUTSIDE
If prey is hiding, the grouper needs to do headstands, sometimes more than one and thus spends time and energy in waiting and recruiting
THE MORAY CAN REACH TO PLACES THE
GROUPER CAN NOT REACH The moray can surprise the prey and catch it before it is able to flee
Tab. A3: Where does this communicational hunt take place? Are there only certain areas?
PLACE HUNT TOOK PLACE REFERNCE
GULF OF ELIAT, AGABA [38]
GREAT BARRIER REEF, AUSTRALIA [36]
ARVOREDO BIOLOGICAL MARINE RESERVE (ABMR),
SOUTHERN BRAZIL [33]
RED SEA [4]
10 The paper: “Referential gestures in fish collaborative hunting” [36] monitored, that in 29 of 127 unsuccessful hunts a joint hunt follows the grouper pointing a place where prey is hiding by giving the headstand signal (Tab. 1). The joint hunting species, which were involved were in 17 of 29 hunts a moray eel and in 10 of 29 instances a wrasse (in 5 situations the grouper showed more than 1 headstand shortly after each other). Here is to say, that in 10 of 17 hunts the moray eel did not react or swam away in the wrong direction. In 8 of this 10 cases the grouper swam to the moray eel shaking his head to motivate him to join the hunt.
Compared to the moray eel, the wrasse always inspects the pointed place directly. In total the grouper did 34 headstands, 29 of them were answered by one of the above-mentioned species, thus 85,3 % of the groupers communication trials were noticed and successful.
11 In Table 2 it is to see how many potentially hunting partners were close to the grouper when began to signal.
The paper also gives the information, that the grouper already hunts with a moray or a wrasse immediately before he shows a headstand signal. When the grouper has had an unsuccessful hunt, he does not directly show the headstand, but he waits for some time if the prey will leave its hiding place before showing a potentially partner where prey is hiding (Tab. 4). This research also shows that groupers are passionate when hunting, though they do not move away until someone inspects the hiding place. Also, if no reaction followed the headstand signal, the grouper swam to the potentially partner, trying to motivate him. Or in case the hunting partner leaves the hiding place, the grouper follows to attempt it to go on with hunting.
12 Figure 1 shows the percentage of grouper head-standing and a wrasse reacting.
The second reference: “Interspecific Communicative and Coordinated Hunting between Groupers and Giant Moray Eels in the Red Sea” [4], observed the duration of the interaction between grouper and moray eel (Fig. 1). Here, the total amount of individual moray eels that have joint the hunt, is unknown. Also, this paper did research on the distance of moray eel and grouper during the hunt, which is shown in average in Figure 2.
13 In Table 1 it is furthermore shown, how often the grouper benefits from the joint hunting. In this study the grouper always swam to the moray eel trying to recruit it with headshaking movements (all 14 observed Groupers showed this behaviour). The chance that a moray eels reacts positive to this behaviour and follows the grouper to the hunt, was 58 %.
Here is to say, that the duration of the joint hunting was measured from the moment the moray left its place to follow the grouper until the moray eel left for another crevice and did not came back. Usually the grouper tries to re-recruit the moray than, again through the head- shaking movement. Six of 14 groupers were observed to guide the moray to the place where prey was hiding, waiting above the corals, repeating the head shaking to get the morays attention to this spot, the others did not show head-shaking. The paper shows also, that the signalling to moray eels depends on the alone-hunting-success of the grouper. If he already
14 had success, he won’t recruit a moray eel for another hunt. But if there have been a few unsuccessful hunts after each other, the hunger forces the grouper to ask for a joint hunt.
Furthermore, the authors of the paper did not expect the grouper being as successful during joint hunting, as he is (Tab. 1), but they found out, that groupers caught almost five times as many prey per unit time than when morays were absent (0.19 preys 1/h with moray to 0.04 preys 1/h without moray). The moray caught 5 times prey, when hunting with the grouper, thus both were almost equivalent while hunting together.
In addition, this paper also mentioned the napoleon wrasse. Through obvious reasons, the napoleon wrasse is not able to swim into crevices as the moray eel, but the advantage when hunting together is, that the wrasse is able to destroy the corals/ hiding places of the prey with its powerful jaws.
Discussion of the research findings
Four different Grouper species were found that can communicate a joint hunt. Furthermore, seven species are known to join these hunts (Tab. A1). In Table A1.2 it is to see, that the mentioned grouper species are spread all over the world, thus the idea that the communicative hunting could have evolved just in a special area, is not true. This was also proven through the used papers: 4 papers and different observation places: Australia, Gulf of Eliat, Brazil and the Red Sea. Maybe there are more species doing joint hunting, but it is possible that they have not been observed yet, or that just video records of potential communicative hunts between a grouper and another species exists. Researches in species that actually do this kind of hunting, are rare.
The first paper that was evaluated showed that a grouper communicated a joint hunt (headstand-signal) after unsuccessful hunts in 22,8 % of the cases [36]. In 58,6 % of the cases a moray eel joined and in 34,4 % it was a wrasse. In all cases a moray eel joint, it did not always stay, but left in 58,8 % of the cases it joined (Tab. 1 – 4 and Fig. 1). Possible solutions to this findings might be, that a moray eel is a nocturnal hunter. Maybe the moray eel is still full due to successful hunts in the night, or it is still in resting mood. Hence the moray eel is not hungry it might be possible, that he is the preferred hunting partner of the grouper: Because the moray is not hungry there might be more prey for the grouper. This can also be explained due to the observed behaviour of the grouper following to moray when it is leaving, trying to motivate it to go on with the hunt (In 80 % of the cases the moray eel left, the grouper follows).
The napoleon wrasse and the Octopus cyaneus on the other hand are hunting during the day.
Thus, they show a higher motivation: Every time a wrasse joined the hunt, it directly inspected the area the grouper points on (Fig. 1) The authors found out, that groupers do not directly ask for a joined hunt but wait for the prey leaves the hiding place on its own (Tab. 4). Probably this is because the chance to actually catch the prey reduces, when two hunters try to feed on it. Therefore, it seems as if the grouper considers his chances to be successful before communicating joined hunting to anyone.
The second reference lists the results of research about the duration and the distance between the two hunting partners during a joined hunt [4]. They found out that communicated hunts can take from 1 to 93 minutes. There are many short hunts: About 65 observed hunts that just took one minute, and less hunts that took long: About 10 hunts that took 41 to 93 minutes (Fig. 1). When taking this as a base there are three possibilities that might have influence on the short duration of the joined hunt: 1) The moray leaves because
15 prey is not obviously visible, and it is not hungry enough to spend effort or time in the hunt.
2) The prey was caught fast, thus either the grouper or the moray, or both had a successful hunt. Or the third possible solution: The prey escaped while the grouper searched for a hunting partner. But, to be fair, there were also long hunts. Maybe the grouper recruited a moray that has not been successful while hunting in the last night, thus still hungry and very motivated to catch some prey. The mean distance between grouper and moray eel was 70 cm (Fig. 2), which is enough space to swim on their own but still be in eyesight.
Comparative discussion
It was the aim of this essay to study the role of communication in cooperative hunting between predatory reef fishes compared to other marine and non-marine species.
Mammals are hunting together with individuals of their own species and with members of a group they are in: Chimpanzees, dolphins, lions, orcas, etc. . Groupers are singles, living and hunting alone. They never hunt with other groupers and they first consider about the chance to be successful before asking for a cooperative hunt with another species as the moray eel.
Mammals are used to cooperative hunting and sharing or rather, they are used to the fact, that the most powerful individual of the group feeds first on the prey: It is a ranking. The grouper and its hunting partner are equal partners. Who catches it eats it. There has not been observed any aggression behaviour. Unlike on land: Lions often fight for the position of the most powerful individual or for the benefit to feed as the first.
Thus, to conclude, the groupers way of joined hunting is much calmer and more peaceful than hunting between chimpanzees or lions. It is a fantastic example about how different species, even different predatory species that live in the same niche can behave together without any potential of aggression and help each other right away. The grouper overcomes problems of food limitation or better the problem of being unsuccessful while hunting with a very interesting solution. He searches for a partner that can help with its own characteristic skills.
Therefore, obviously the grouper must know about other species skills and characteristics, because he is choosing the hunting partners wisely. If they would not be able to help, it would not make a lot of sense to do a cooperative hunt. Hence, even though a grouper is a fish it must be intelligent in a way humans do not understand yet. Groupers are able to ask for help, which is a rare skill in the fauna and, which is most important, they are able to ask another species for help. Wherefore it is interesting to find out more about the circumstances these events happen.
Thus, after reading all these findings there are still open questions: For instance, it is known that groupers can change their sex. Hence, it would be interesting to find out if there is a difference in females and males. Is just one sex giving signals for cooperative hunting? Or do they just give it shortly before changing sex? Or is there hardly any difference? Another question might be the most interesting one: How did it evolve that groupers show this cooperative behaviour? Honestly this question won’t be easy to answer, but maybe someday?
Really interesting is also, that the communicative hunting is not a territorial thing due to observed behaviour all over the world. Therefore, nobody can say, that there is just one area this happens and not only one species or rather group of species in this special area is different to all the others. In that case it would have been interesting to find out which abiotic and biotic factors would have led to these findings.
16 Furthermore, it would be very helpful to find out more about the benefits of the hunting partner. In every study the grouper has been observed, never the moray eel, wrasse or octopus.
17 Literature
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