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1.
Oecologia ; 190(4): 783-797, 2019 Aug.
Article in English | MEDLINE | ID: mdl-31267237

ABSTRACT

Predation on parasites is an important ecological process, but few experimental studies have examined the long-term impacts on the prey. Cleaner fish prey upon large numbers and selectively feed on the larger individuals of the ectoparasitic stage of gnathiid isopods. Removal of cleaner fish Labroides dimidiatus for 1.5-12.5 years negatively affects coral reef fishes, but the mechanism is unclear. A reduction in local parasite populations or the size of individual parasites would benefit all susceptible fishes. We tested whether cleaner presence reduces local gnathiid populations using 18 patch-reefs distributed between two sites (both at Lizard Island, Great Barrier Reef) which were maintained cleaner-free or undisturbed for 12 years. Using emergence traps (1 m2), free-living gnathiid stages were sampled before and after cleaner fish were removed during the day and night, up to 11 times over the course of the experiment. There were effects of the removal in the predicted direction, driven largely by the response at one site over the other involving 200% more gnathiids, but manifested only in the daytime sampling after 4 months. There was also a main effect (36%) for the shared sample dates at both sites after 12 years. Gnathiid size occasionally differed with cleaner presence, but in no consistent way over time. Contrary to our predictions, changes in free-living gnathiid population numbers and their size structure rarely reflected the changes in fish populations and individuals observed on cleaner-free reefs. Therefore, evidence that this predator alone regulates gnathiids remains limited, suggesting other contributing processes are involved.


Subject(s)
Isopoda , Parasites , Perciformes , Animals , Coral Reefs , Fishes
2.
J Fish Biol ; 81(1): 210-9, 2012 Jul.
Article in English | MEDLINE | ID: mdl-22747814

ABSTRACT

Diet analyses and observations of cleaning behaviour of two cleaner fishes revealed that Labroides bicolor fed more on client mucus, but Labroides dimidiatus fed more on ectoparasites, and that L. bicolor interacted with fewer species (36 species) compared with L. dimidiatus (44 species). The client species which contributed most to the dissimilarity between cleaner species were the dusky farmerfish Stegastes nigricans and bicolor chromis Chromis margaritifer damselfishes, which L. dimidiatus interacted with more often than L. bicolor, and the striated Ctenochaetus striatus and brown Acanthurus nigrofuscus surgeonfishes, which L. bicolor interacted with more; L. bicolor interacted with all parrotfishes (Scaridae) more. These results confirm the importance of repeated interactions and partner choice in determining the nature of interactions in mutualisms.


Subject(s)
Diet , Feeding Behavior , Perciformes/physiology , Animals , Behavior, Animal , Gastrointestinal Contents
3.
Proc Biol Sci ; 279(1737): 2479-86, 2012 Jun 22.
Article in English | MEDLINE | ID: mdl-22357262

ABSTRACT

Joint group membership is of major importance for cooperation in humans, and close ties or familiarity with a partner are also thought to promote cooperation in other animals. Here, we present the opposite pattern: female cleaner fish, Labroides dimidiatus, behave more cooperatively (by feeding more against their preference) when paired with an unfamiliar male rather than with their social partner. We propose that cooperation based on asymmetric punishment causes this reversed pattern. Males are larger than and dominant to female partners and are more aggressive to unfamiliar than to familiar female partners. In response, females behave more cooperatively with unfamiliar male partners. Our data suggest that in asymmetric interactions, weaker players might behave more cooperatively with out-group members than with in-group members to avoid harsher punishment.


Subject(s)
Cooperative Behavior , Grooming/physiology , Models, Biological , Perciformes/physiology , Recognition, Psychology/physiology , Animals , Appetitive Behavior/physiology , Australia , Feeding Behavior/physiology , Female , Male , Pacific Ocean , Punishment
4.
J Evol Biol ; 24(8): 1628-39, 2011 Aug.
Article in English | MEDLINE | ID: mdl-21599777

ABSTRACT

Pairs of unrelated individuals face a prisoner's dilemma if cooperation is the best mutual outcome, but each player does best to defect regardless of his partner's behaviour. Although mutual defection is the only evolutionarily stable strategy in one-shot games, cooperative solutions based on reciprocity can emerge in iterated games. Among the most prominent theoretical solutions are the so-called bookkeeping strategies, such as tit-for-tat, where individuals copy their partner's behaviour in the previous round. However, the lack of empirical data conforming to predicted strategies has prompted the suggestion that the iterated prisoner's dilemma (IPD) is neither a useful nor realistic basis for investigating cooperation. Here, we discuss several recent studies where authors have used the IPD framework to interpret their data. We evaluate the validity of their approach and highlight the diversity of proposed solutions. Strategies based on precise accounting are relatively uncommon, perhaps because the full set of assumptions of the IPD model are rarely satisfied. Instead, animals use a diverse array of strategies that apparently promote cooperation, despite the temptation to cheat. These include both positive and negative reciprocity, as well as long-term mutual investments based on 'friendships'. Although there are various gaps in these studies that remain to be filled, we argue that in most cases, individuals could theoretically benefit from cheating and that cooperation cannot therefore be explained with the concept of positive pseudo-reciprocity. We suggest that by incorporating empirical data into the theoretical framework, we may gain fundamental new insights into the evolution of mutual reciprocal investment in nature.


Subject(s)
Behavior, Animal , Cooperative Behavior , Game Theory , Animals , Biological Evolution , Punishment , Reproducibility of Results
5.
J Evol Biol ; 21(3): 879-88, 2008 May.
Article in English | MEDLINE | ID: mdl-18312320

ABSTRACT

Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one-sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. The effectiveness of the threat of terminating an encounter, however, depends upon the ease with which both the potential victim and the potential exploiter can find replacement partners. Here, we extend a simple, game-theoretical model of this form of partner control to incorporate variation in the relative abundance of potential victims and exploiters, which leads to variation in the time required for individuals of each type to find a new partner. We show that such market effects have a dramatic influence on the stable level of exploitation (and consequent duration of interaction). As the relative abundance of victims decreases, they become less tolerant to exploitation, terminating encounters earlier (for a given level of exploitation), whereas exploiters behave in a more cooperative manner. As a result, the stable duration of interaction actually increases, despite the decreasing tolerance of the victims. Below a critical level of relative victim abundance, the model suggests that the cost of finding a replacement partner becomes so great that it does not pay to exploit at all.


Subject(s)
Feeding Behavior/physiology , Fishes/physiology , Symbiosis/physiology , Animals , Models, Biological
6.
J Evol Biol ; 21(2): 405-20, 2008 Mar.
Article in English | MEDLINE | ID: mdl-18179515

ABSTRACT

The evolution and stability of helping behaviour has attracted great research efforts across disciplines. However, the field is also characterized by a great confusion over terminology and a number of disagreements, often between disciplines but also along taxonomic boundaries. In an attempt to clarify several issues, we identify four distinct research fields concerning the evolution of helping: (1) basic social evolution theory that studies helping within the framework of Hamilton's inclusive fitness concept, i.e. direct and indirect benefits, (2) an ecological approach that identifies settings that promote life histories or interaction patterns that favour unconditional cooperative and altruistic behaviour, e.g. conditions that lead to interdependency or interactions among kin, (3) the game theoretic approach that identifies strategies that provide feedback and control mechanisms (protecting from cheaters) favouring cooperative behaviour (e.g. pseudo-reciprocity, reciprocity), and (4) the social scientists' approach that particularly emphasizes the special cognitive requirements necessary for human cooperative strategies. The four fields differ with respect to the 'mechanisms' and the 'conditions' favouring helping they investigate. Other major differences concern a focus on either the life-time fitness consequences or the immediate payoff consequences of behaviour, and whether the behaviour of an individual or a whole interaction is considered. We suggest that distinguishing between these four separate fields and their complementary approaches will reduce misunderstandings, facilitating further integration of concepts within and across disciplines.


Subject(s)
Biological Evolution , Cooperative Behavior , Animals , Ecosystem , Game Theory , Humans , Selection, Genetic , Social Sciences , Terminology as Topic
7.
Anim Cogn ; 5(3): 139-45, 2002 Sep.
Article in English | MEDLINE | ID: mdl-12357286

ABSTRACT

Individual recognition has been attributed a crucial role in the evolution of complex social systems such as helping behaviour and cooperation. A classical example for interspecific cooperation is the mutualism between the cleaner fish Labroides dimidiatus and its client reef fish species. For stable cooperation to evolve, it is generally assumed that partners interact repeatedly and remember each other's past behaviour. Repeated interactions may be achieved by site fidelity or individual recognition. However, as some cleaner fish have more than 2,300 interactions per day with various individuals per species and various species of clients, basic assumptions of cooperation theory might be violated in this mutualism. We tested the cleaner L. dimidiatus and its herbivorous client, the surgeon fish Ctenochaetus striatus, for their ability to distinguish between a familiar and an unfamiliar partner in a choice experiment. Under natural conditions, cleaners and clients have to build up their relationship, which is probably costly for both. We therefore predicted that both clients and cleaners should prefer the familiar partner in our choice experiment. We found that cleaners spent significantly more time near the familiar than the unfamiliar clients in the first 2 minutes of the experiment. This indicates the ability for individual recognition in cleaners. In contrast, the client C. striatus showed no significant preference. This could be due to a sampling artefact, possibly due to a lack of sufficient motivation. Alternatively, clients may not need to recognise their cleaners but instead remember the defined territories of L. dimidiatus to achieve repeated interactions with the same individual.


Subject(s)
Biological Evolution , Fishes , Recognition, Psychology , Adaptation, Physiological , Animals , Motivation , Social Behavior , Visual Perception
8.
Proc Biol Sci ; 268(1475): 1495-501, 2001 Jul 22.
Article in English | MEDLINE | ID: mdl-11454294

ABSTRACT

The cleaner wrasse Labroides dimidiatus often touches 'client' reef fish dorsal fin areas with its pelvic and pectoral fins. The relative spatial positions of cleaner and client remain constant and the cleaner's head points away from the client's body. Therefore, this behaviour is not compatible with foraging and the removal of client ectoparasites. As clients seek such 'tactile stimulation', it can be classified as an interspecific socio-positive behaviour. Our field observations on 12 cleaners (observation time of 112h) suggest that cleaners use tactile stimulation in order to successfully (i) alter client decisions over how long to stay for an inspection, and (ii) stop clients from fleeing or aggressive chasing of the cleaner in response to a cleaner fish bite that made them jolt. Finally, predatory clients receive tactile stimulation more often than non-predatory clients, which might be interpreted as an extra service that cleaners give to specific partners as pre-conflict management, as these partners would be particularly dangerous if they started a conflict. We therefore propose that cleaner fish use interspecific social strategies, which have so far been reported only from mammals, particularly primates.


Subject(s)
Animal Communication , Fishes/physiology , Animals , Feeding Behavior/physiology , Fishes/parasitology , Host-Parasite Interactions , Predatory Behavior , Touch
9.
Proc Biol Sci ; 264(1379): 253-9, 1997 Feb 22.
Article in English | MEDLINE | ID: mdl-9061972

ABSTRACT

It is generally assumed that most primates live in monospecific or polyspecific groups because group living provides protection against predation, but hard evidence is scarce. We tested the antipredation hypothesis with observational and experimental data on mixed-species groups of red colobus (Procolobus badius) and diana monkeys (Cercopithecus diana) in the Taï National Park, Ivory Coast. Red colobus, but not diana monkeys, are frequently killed by cooperatively hunting chimpanzees. Association rates peaked during the chimpanzees' hunting season, as a result of changes in the behaviour of the red colobus. In addition, playbacks of recordings of chimpanzee sounds induced the formation of new associations and extended the duration of existing associations. No such effects were observed in reaction to control experiments and playbacks of leopard recordings.


Subject(s)
Colobus/physiology , Pan troglodytes/physiology , Predatory Behavior , Animals
10.
Anim Behav ; 54(6): 1461-1474, 1997 Dec.
Article in English | MEDLINE | ID: mdl-9794772

ABSTRACT

We tested the hypothesis that red colobus monkeys, Procolobus badius and Diana monkeys, Cercopithecus diana in Taï National Park, Ivory Coast, associate to increase safety from predation. We recorded stratum use, exposure and vigilance of each species in the presence and in the absence of the partner species. In the presence of Diana monkeys, red colobus used lower strata more often, were more exposed to the forest floor and looked down less often while foraging. This suggests that red colobus reduce predation pressure from ground predators by associating with Diana. There are several indications that both species are less vulnerable to birds of prey when associated: red colobus looked sideways less often and were more exposed to the front, Diana monkeys used greater heights and were more exposed to the front, to the rear and from above. We also asked whether specific sentinel qualities of Diana monkeys might explain why other sympatric monkey species additionally seek their presence. When groups of various species compositions were approached by an observer, or confronted with an eagle model, Diana monkeys raised the alarm in most cases. Since neither monkey species improves its foraging success when associated, this study shows that predation can both maintain and be the ultimate cause of interspecific associations.Copyright 1997 The Association for the Study of Animal Behaviour

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