In this study, we provide field-based observational evidence for a coordinated, cooperative vigilance system in four species of pairing rabbitfishes. Specifically, we demonstrate that during foraging, pair members strongly coordinate their positions: while one individual forages with its head down, its partner assumes an elevated, upright position in the water column, allowing for an unobstructed visual field to scan the surrounding environment. Paired fishes alternate frequently between foraging and the vigilance position. Compared to solitary individuals, individuals in pairs exhibit longer vigilance bouts than their solitary counterparts, but appear to benefit from the presence of the partner by exhibiting more consecutive bites per foray and deeper penetration into crevices in the substratum.

The posture assumed by one of the rabbitfishes while its partner is foraging closely matches reports in birds and mammals, where vigilant individuals are commonly identified by raised heads and/or elevated positions72,73,74,75, a behaviour that has only recently been reported for teleost fishes62. For rabbitfishes, the upright position is likely to favour vigilance as it potentially enables a greater ability to detect predators (and possibly also competitors) compared to foraging fishes, probably due to a less obstructed visual field76,77. The assumed angle may allow an unobstructed field of view while remaining close to the reef and the partner. While we are unable to demonstrate that the upright position serves primarily for the detection of predators, our observations and previous evidence suggest that scanning the surroundings for competitors, potential new partners, or food are of limited importance when compared to predator detection. While rabbitfishes do occasionally engage in aggressive behaviour with other pairs, these interactions are infrequent (<1% of the total behaviours observed in this study) and home-ranges of pairs are non-exclusive58, suggesting that scanning the surroundings for competitors may only play a minor role. In addition, pair bonds between rabbitfishes are relatively stable57,58, questioning the need to continuously look out for a new partner. Finally, the foraging strategy of rabbitfishes along with their dietary preferences for small and cryptic algae, sponges and cyanobacteria61,63, which require careful and close examination of concealed micro-habitats, make it unlikely that an elevated position will be beneficial for the detection of food. However, as we are unable to quantify the relative contributions of these various roles, we use the term ‘vigilance’ in its widest sense as being aware of the surrounding environment.

Whenever the pair was observed to rapidly abandon its positions (i.e. engaged in rapid directional swimming behaviour), the vigilant individual had an unobstructed view of the surrounding environment, while the visual field of the forager was often blocked by the reef substratum. Upon the vigilant individual abandoning its position (which was far more frequent than the forager abandoning its position first), the forager consistently trailed the vigilant individual, suggesting that foraging individuals reliably (94.1% of all cases) respond to actions or potential warning cues generated by the vigilant individual. While peripheral vision and social monitoring by the forager may facilitate the reaction to the vigilant partner’s behaviour78, the frequent occurrence of fin-flicks prior to abandoning the vigilance position may indicate intentional communication79,80,81. Although the significance of fin-flicks has not yet been investigated in rabbitfishes, fin-flicks are known to generate an acoustic signal in another family of reef fishes in which pairing is prevalent (f. Chaetodontidae66,67) and fin-flicks have been described as an important warning signal in other fish species65,68. Thus, although the role of fin-flicking remains to be determined in rabbitfishes, it seems likely that fin-flicks serve as a communication signal and that the forager is able to perceive these signals despite visual restrictions. Our findings that the vast majority of fin-flicks in rabbitfishes occurred in situations in which communication is beneficial (i.e. when one fish was foraging while the partner was vigilant or while displaying to other pairs) support a role of fin-flicks in in the maintenance of coordination between the forager and the vigilant fish.

Interestingly, the described scenario, in which foraging severely compromises vigilance while information is readily available from a vigilant conspecific, precisely matches the conditions under which coordinated vigilance should be favoured37,76. This is strongly supported by the angles rabbitfishes assume during foraging episodes where one fish’s angle and height above the substratum are the best predictors for complementary behaviour in the partner (Fig. 3). Clearly, pairs of rabbitfishes coordinate their positions during foraging and possibly do so through communication via fin-flicks.

Given this, the question then arises whether the coordinated behaviour in rabbitfish pairs represents a cooperative system based on by-product mutualism/pseudo-reciprocity29,34, or if rabbitfishes may satisfy the requirements of direct reciprocity. Several recent papers have emphasized the lack of evidence supporting the fundamental characteristics of direct reciprocity in animals23,29,30. These include: i) continuous cooperation between the same individuals, ii) behavioural adaptations to assist the partner, iii) adjustment of assistance provided according to received assistance, iv) cooperation not restricted to kin or potential mates, v) assistance entailing momentary net fitness costs to the assisting individual and vi) cooperative behaviour being found in wild populations (after23).

For rabbitfishes, there is evidence supporting all of these requirements. (i) As rabbitfish pairs are stable and remain together for extended periods of time57,58, cooperation is likely to occur continuously between the same individuals. (ii) Our results show that individuals prolong the length of vigilance bouts in the presence of a partner. This may represent a behavioural adaptation to assist the partner, as paired fishes exhibited an increased number of bites per foray (S. doliatus, S. puellus, S. corallinus) or deeper substratum penetration (S. corallinus, S. doliatus), therefore increasing the likelihood of a higher overall food intake (as reported for pied babblers Turdoides bicolor79). (iii) Pair members frequently alternate between foraging and vigilance and the ratio between assistance provided and assistance received appears to be well balanced. While feeding was unevenly distributed in a few of the observed pairs, this may be a consequence of the length of observations and a more balanced distributions may be observed if fish were monitored over an entire day. (iv) The observation that feeding within pairs is not generally skewed toward one individual suggests that cooperation is not solely based on male mate-guarding (as found in sleepy lizards, Tiliqua rugosa82) and the common occurrence of same-sex pairs in rabbitfishes58 suggests that cooperation is not limited to reproductive pairs83. Due to the reproductive strategies of reef fishes and their pelagic larval stage, cooperation limited to kin is also highly unlikely.

(v) Fitness costs may include predation risk and lost foraging opportunities during vigilance behaviour but such costs are inherently difficult to quantify38,84. As in other animals where mutual vigilance has been described as a potential cooperative system72,79,85,86, the vigilant individual in rabbitfish pairs is positioned above the underlying substratum with its head elevated, making vigilance beneficial for the overall awareness of the surroundings and therefore potentially self-serving rather than costly (provided predators selectively target foraging individuals). However, given the nutritive constraints of marine herbivory (or spongivory), which necessitate constant and intensive grazing, prolonged vigilance bouts are probably nutritionally costly rather than self-serving87. This is further supported by the low levels of simultaneous vigilance (both pair members hovering motionless above the substratum, 6.6% of behaviours across all pairs), which would indicate competition for vigilance in a scenario where predators preferentially target foragers37,84,88,89. Thus, while gaps in foraging activity associated with prolonged vigilance are likely to represent a significant cost, the deeper penetrations into crevices, as well as the higher number of bites per foray appear to be an intuitive reward for the partner. The lack of a clear difference between solitary and paired individuals in S. puellus and S. vulpinus in terms of penetration depth may point towards differences in the dietary preferences of these two species or their morphological adaptations. While S. corallinus and S. doliatus feed predominantly on filamentous and corticated red algae, food that is readily used by other herbivorous fish species63,90, only a few reef fishes feed on cyanobacteria, which are the main food source for S. vulpinus. Thus, the latter might be more readily available in more accessible microhabitats. In addition, S. vulpinus exhibits the morphological characteristics most suited for the exploitation of crevices among the four investigated species, suggesting that even solitary individuals might be able to penetrate into the substratum with no substantial obstructions to the visual field59. S. puellus, in turn, exhibits the most fusiform morphology among the examined species59, suggesting that quick escape from predators might play a bigger role in this species, possibly permitting solitary individuals to penetrate into the substratum despite the lack of a vigilant partner. However, given the relatively small sample size, the lack of significance in these comparisons should be interpreted with caution. These minor differences notwithstanding, there appear to be clear costs (vigilance bouts) and benefits (foraging efficiency) associated with cooperative vigilance in all four rabbitfish species examined. Finally, vi) all observations were conducted on the reef, indicating that the described vigilance system occurs in wild populations. Thus, the coordination of foraging and vigilance in rabbitfish pairs appears to satisfy all the basic requirements for reciprocal cooperation.

While we cannot hope to fully resolve the question of reciprocity with observational evidence alone, our findings are consistent with direct reciprocity. Thus, our study corroborates the tenor of several recent studies, which posit that reciprocity may be a lot more common under natural settings than when forced into the stringent rules of game-theoretical models31,32,33,36,38. Indeed, our results help us to understand why we may find reciprocity in animals, which lack the presumed cognitive requirements for reciprocity23. First, cooperative interactions among rabbitfishes are restricted to just one partner at a time. This alleviates frequently-cited cognitive issues arising from recognizing a range of individuals and remembering their previous actions in a large group of animals13,24,27 in order to repay for the behaviour of a previous partner, as has been posited for predator inspection and egg-trading in fishes23,46,47. Second, continuous foraging activity, immediate alternation and the similar and simultaneous needs (food and safety) for both pair members in rabbitfishes prevent long time-lags between rounds in an IPD, as often found in, for instance, primates33,91. This again relaxes the need for complex cognitive abilities, such as memory, to underpin reciprocal cooperation20. Third, rabbitfishes cooperate continuously with the same partner over an extended period of time. There is now considerable evidence that such interdependence between social partners can foster high levels of cooperation in an IPD, as individuals do not systematically surrender to the short-term temptation of cheating on the partner92,93, therefore making tit-for-tat (or, more specifically ‘generous tit-for-tat’) a strategy with high levels of cooperation. Finally, our study provides preliminary evidence for the continuous exchange of social information between partners by means of fin-flicks and suggests that individuals quickly react to the behaviour displayed by the partner, as indicated by high levels of coordination37. Such elimination of discrete rounds in the IPD and the continuous exchange of information have been proposed as a major factor in favouring cooperation (either by coaction or reciprocity), as it lowers the cost for cooperating individuals36. Given the low levels of simultaneous vigilance observed in the present study, reciprocity appears more likely to operate in rabbitfishes than coaction, which would incline individuals to simply copy the partner’s behaviour36.

In summary, our study identifies pairing rabbitfishes as an intriguing group of animals in the context of reciprocity, cooperation and cognition. Although limited to observational data, we provide strong evidence for a clear coordination of foraging and vigilance behaviour in pairs and demonstrate that pair members frequently alternate their foraging. We further show that rabbitfish pairs have the potential to satisfy all the basic requirements of reciprocity and discuss a range of conditions, which may favour reciprocal exchange in animals. Our evidence suggests that the complex cognitive and social skills, frequently assumed to be necessary for the evolution of direct reciprocity in animals, may be advantageous but, as in fishes, may not be essential.