Simulating more realistic predation threat using attack playbacks

Use of virtual proxies of live animals are rapidly gaining ground in studies of animal behaviour. Such proxies help to reduce the number of live experimental animals needed to stimulate the behaviour of experimental individuals and to increase standardisation. However, using too simplistic proxies may fail to induce a desired effect and/or lead to quick habituation. For instance, in a predation context, prey often employ multimodal cues to detect predators or use specific aspects of predator behaviour to assess threat. In a live interaction, predator and prey often show behaviours directed towards each other, which are absent in virtual proxies. Here we compared the effectiveness of chemical and visual predator cues in the cooperatively breeding cichlid Neolamprologus pulcher, a species in which predation pressure has been the evolutionary driver of its sociality. We created playbacks of predators simulating an attack and tested their effectiveness in comparison to a playback showing regular activity and to a live predator. We further compared the effectiveness of predator odour and conspecific skin extracts on behaviours directed towards a predator playback. Regular playbacks of calmly swimming predators were less effective than live predators in stimulating a focal individual’s aggression and attention. However, playbacks mimicking an attacking predator induced responses much like a live predator. Chemical cues did not affect predator directed behaviour.

Territorial fish distinguish familiar neighbours individually

True individual recognition (TIR), the ability to distinguish multiple familiar members individually, is more elaborate than class-level recognition, and evidence for the ability to perform TIR is reported from primates, some other social mammals, birds and lizard in vertebrates. These animals exhibit a highly social structure, wherein TIR is essential for their social interactions. Such high sociality has been documented in fish, but clear evidence of TIR has been limited. The cichlid, Neolamprologus pulcher, a cooperative breeder that guards a territory, exhibits the dear enemy relationship. Here, we show that this fish distinguishes two familiar neighbours individually, i.e., TIR ability, using one-way mirrors in experimental tanks. Focal fish established the dear enemy relationship with two neighbours, NA and NB, and displayed limited aggression towards these familiar neighbours. However, their aggressiveness towards neighbour NB increased when they were shifted from the original side of the tank after NA was removed, suggesting that they distinguished NB from NA or regarded NB as a stranger. Interestingly, this aggression level against the shifted neighbour NB largely decreased within 1 min. This decrease contrasted with the longer and more frequent aggressiveness towards unfamiliar strangers. These results suggest that focal fish recognised neighbour NB as a familiar stranger but probably punished NB that moved beyond its territory, that is, betrayed the dear enemy relationship. We prevented the effects of the behavioural reactions of exposed individuals using a one-way mirror. Thus, we conclude that this fish species displays TIR and discuss that TIR is prevalent in territorial animals in which the dear enemy effect is common.

Singing above the chorus: cooperative Princess cichlid fish (Neolamprologus pulcher) has high pitch

Teleost fishes not only communicate with well-known visual cues, but also olfactory and acoustic signals. Communicating with sound has advantages, as signals propagate fast, omnidirectionally, around obstacles, and over long distances. Heterogeneous environments might favour multimodal communication, especially in socially complex species, as combination of modalities’ strengths helps overcome their individual limitations. Cichlid fishes are known to be vocal, but a recent report suggests that this is not the case for the socially complex Princess cichlid Neolamprologus pulcher from Lake Tanganyika. Here we further investigated acoustic communication in this species. Wild and captive N. pulcher produced high frequency sounds (mean: 12 kHz), when stimulated by mirror images. In laboratory experiments, N. pulcher produced distinct two-pulsed calls mostly, but not exclusively, associated with agonistic displays. Our results suggest that male N. pulcher produce more sounds at greater durations than females. Thus, we confirm that the Princess cichlid does not produce low frequency sounds, but does produce high frequency sounds, both in combination with and independent from visual displays, suggesting that sounds are not a by-product of displays. Further studies on the hearing abilities of N. pulcher are needed to clarify if the high-frequency sounds are used in intra-or inter-specific communication.

A dear enemy relationship in a territorial cichlid: evidence for the threat-level hypothesis

Despite competing for resources such as space, food and mates, many territorial animals are less aggressive towards neighbours who rarely go beyond their territorial boundaries. This so-called dear enemy phenomenon is advantageous in territorial defence, but it has not been well studied in fish. In this work, we tested the ‘correct–incorrect boundary paradigm’ of the dear enemy phenomenon using the territorial cichlid fishNeolamprologus pulcher, which exhibits dear enemy relationships. When the fish was placed in a small experimental tank, in which fish established its territory, it was initially very aggressive against a neighbouring fish in an adjacent tank, but the aggression level decreased rapidly (within 4 days). When the tank containing the neighbour was shifted to the opposite side, the focal fish was more aggressive than the day before, but it exhibited less aggression than it did against a stranger placed on the shifted side. This lower level of aggression suggested that the focal fish did not regard the shifted neighbour as a stranger. Our observations provide support for the threat-level hypothesis, according to which territory owners will modulate aggression intensity based on the threat level.

Dominance network structure across reproductive contexts in the cooperatively breeding cichlid fish Neolamprologus pulcher

While a large number of studies have described animal social networks, we have a poor understanding of how these networks vary with ecological and social conditions. For example, reproductive periods are an important life-history stage that may involve changes in dominance relationships among individuals, yet no study to date has compared social networks of dominance interactions (i.e. dominance networks) across reproductive contexts. We first analyzed a long-term dataset on captive social groups of the cooperatively breeding cichlid Neolamprologus pulcher, and found that eviction events were significantly more common around reproduction than expected by chance. Next, we compared the structure of dominance networks during early parental care and non-reproductive periods, using one of the first applications of exponential random graph models in behavioral biology. Contrary to our predictions, we found that dominance networks showed few changes between early parental care and non-reproductive periods. We found no evidence that dominance interactions became more skewed towards larger individuals, became more frequent between similar-sized individuals, or became more biased towards a particular sex during parental care. However, we did find that there were relatively more dominance interactions between opposite-sex dyads in the early parental care period, which may be a by-product of increased sexual interactions during this time. This is the first study in behavioral ecology to compare social networks using exponential random graph modeling, and demonstrates a powerful analytical framework for future studies in the field.

Isotocin and sociality in the cooperatively breeding cichlid fish, Neolamprologus pulcher

The ultimate functions of sociality, or the tendency to associate with conspecifics and to live within a social group, are increasingly well understood. However, the proximate mechanisms that mediate this behaviour have received less attention. The oxytocin family of nonapeptide hormones (including isotocin in teleost fish) is thought to play an important role in regulating social behaviour across a wide range of taxa and social contexts. In the current study, we investigated the influence of exogenous administration of isotocin and an oxytocin receptor antagonist on sociality in a cooperatively breeding fish, Neolamprologus pulcher. In our first experiment, we found that a high (and a low) dose of peripherally administered exogenous isotocin decreased the time spent associating with conspecifics in N. pulcher, while an intermediate dose had no effect relative to control. In our second experiment, we found that a peripheral administration of an oxytocin receptor antagonist increased grouping preference in male N. pulcher. The results of both experiments suggest that IT may inhibit grouping behaviour in this species. These results contribute to a growing body of literature suggesting that the broad generalization that the oxytocin family of nonapeptides facilitate grouping behaviour is overly simplistic, and that specific behavioural effects depend the study species and testing conditions.

Strategic reduction of help before dispersal in a cooperative breeder

In cooperative breeders, sexually mature subordinates can either queue for chances to inherit the breeding position in their natal group, or disperse to reproduce independently. The choice of one or the other option may be flexible, as when individuals respond to attractive dispersal options, or they may reflect fixed life-history trajectories. Here, we show in a permanently marked, natural population of the cooperatively breeding cichlid fish Neolamprologus pulcher that subordinate helpers reduce investment in territory defence shortly before dispersing. Such reduction of effort is not shown by subordinates who stay and inherit the breeding position. This difference suggests that subordinates ready to leave reduce their investment in the natal territory strategically in favour of future life-history perspectives. It seems to be part of a conditional choice of the dispersal tactic, as this reduction in effort appears only shortly before dispersal, whereas philopatric and dispersing helpers do not differ in defence effort earlier in life. Hence, cooperative territory defence is state-dependent and plastic rather than a consistent part of a fixed life-history trajectory.